UNLABELLED: Invasive cell growth and migration is usually considered a specifically metazoan phenomenon. However, common features and mechanisms of cytoskeletal rearrangements, membrane trafficking and signalling processes contribute to cellular invasiveness in organisms as diverse as metazoans and plants - two eukaryotic realms genealogically connected only through the last common eukaryotic ancestor (LECA). By comparing current understanding of cell invasiveness in model cell types of both metazoan and plant origin (invadopodia of transformed metazoan cells, neurites, pollen tubes and root hairs), we document that invasive cell behavior in both lineages depends on similar mechanisms. While some superficially analogous processes may have arisen independently by convergent evolution (e.g. secretion of substrate- or tissue-macerating enzymes by both animal and plant cells), at the heart of cell invasion is an evolutionarily conserved machinery of cellular polarization and oriented cell mobilization, involving the actin cytoskeleton and the secretory pathway. Its central components - small GTPases (in particular RHO, but also ARF and Rab), their specialized effectors, actin and associated proteins, the exocyst complex essential for polarized secretion, or components of the phospholipid- and redox- based signalling circuits (inositol-phospholipid kinases/PIP2, NADPH oxidases) are aparently homologous among plants and metazoans, indicating that they were present already in LECA. REVIEWER: This article was reviewed by Arcady Mushegian, Valerian Dolja and Purificacion Lopez-Garcia.

Department of Cell Biology Faculty of Science Charles University Prague Vinicna 7 128 43 Prague 2 Czech Republic

Zobrazit více v PubMed

Simpson AG, Roger AJ. The real ‘kingdoms’ of eukaryotes. Curr Biol. 2004;14:R693–R696. doi: 10.1016/j.cub.2004.08.038. PubMed DOI

Arkowitz RA, Bassilana M. Polarized growth in fungi: symmetry breaking and hyphal formation. Semin Cell Dev Biol. 2011;22:806–815. doi: 10.1016/j.semcdb.2011.08.010. PubMed DOI

Dickinson JR. Filament formation in Saccharomyces cerevisiae–a review. Folia Microbiol (Praha) 2008;53:3–14. doi: 10.1007/s12223-008-0001-6. PubMed DOI

Howell AS, Lew DJ. Morphogenesis and the cell cycle. Genetics. 2012;190:51–77. doi: 10.1534/genetics.111.128314. PubMed DOI PMC

Kebdani N, Pieuchot L, Deleury E, Panabieres F, Le Berre JY, Gourgues M. Cellular and molecular characterization of Phytophthora parasitica appressorium-mediated penetration. New Phytol. 2010;185:248–257. doi: 10.1111/j.1469-8137.2009.03048.x. PubMed DOI

Wang Y, Meng Y, Zhang M, Tong X, Wang Q, Sun Y, Quan J, Govers F, Shan W. Infection of Arabidopsis thaliana by Phytophthora parasitica and identification of variation in host specificity. Mol Plant Pathol. 2011;12:187–201. doi: 10.1111/j.1364-3703.2010.00659.x. PubMed DOI PMC

Buccione R, Caldieri G, Ayala I. Invadopodia: specialized tumor cell structures for the focal degradation of the extracellular matrix. Cancer Metastasis Rev. 2009;28:137–149. doi: 10.1007/s10555-008-9176-1. PubMed DOI

Caldieri G, Buccione R. Aiming for invadopodia: organizing polarized delivery at sites of invasion. Trends Cell Biol. 2010;20:64–70. doi: 10.1016/j.tcb.2009.10.006. PubMed DOI

Murphy DA, Courtneidge SA. The ‘ins’ and ‘outs’ of podosomes and invadopodia: characteristics, formation and function. Nat Rev Mol Cell Biol. 2011;12:413–426. doi: 10.1038/nrm3141. PubMed DOI PMC

Poincloux R, Lizarraga F, Chavrier P. Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia. J Cell Sci. 2009;122:3015–3024. doi: 10.1242/jcs.034561. PubMed DOI

Kelly T, Mueller SC, Yeh Y, Chen WT. Invadopodia promote proteolysis of a wide variety of extracellular matrix proteins. J Cell Physiol. 1994;158:299–308. doi: 10.1002/jcp.1041580212. PubMed DOI

Chen WT. Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells. J Exp Zool. 1989;251:167–185. doi: 10.1002/jez.1402510206. PubMed DOI

Mueller SC, Chen WT. Cellular invasion into matrix beads: localization of beta 1 integrins and fibronectin to the invadopodia. J Cell Sci. 1991;99(Pt 2):213–225. PubMed

Bowden ET, Barth M, Thomas D, Glazer RI, Mueller SC. An invasion-related complex of cortactin, paxillin and PKCmu associates with invadopodia at sites of extracellular matrix degradation. Oncogene. 1999;18:4440–4449. doi: 10.1038/sj.onc.1202827. PubMed DOI

Chen WT. Proteases associated with invadopodia, and their role in degradation of extracellular matrix. Enzyme Protein. 1996;49:59–71. PubMed

Monsky WL, Lin CY, Aoyama A, Kelly T, Akiyama SK, Mueller SC, Chen WT. A potential marker protease of invasiveness, seprase, is localized on invadopodia of human malignant melanoma cells. Cancer Res. 1994;54:5702–5710. PubMed

Mueller SC, Yeh Y, Chen WT. Tyrosine phosphorylation of membrane proteins mediates cellular invasion by transformed cells. J Cell Biol. 1992;119:1309–1325. doi: 10.1083/jcb.119.5.1309. PubMed DOI PMC

Nakahara H, Howard L, Thompson EW, Sato H, Seiki M, Yeh Y, Chen WT. Transmembrane/cytoplasmic domain-mediated membrane type 1-matrix metalloprotease docking to invadopodia is required for cell invasion. Proc Natl Acad Sci U S A. 1997;94:7959–7964. doi: 10.1073/pnas.94.15.7959. PubMed DOI PMC

Baldassarre M, Ayala I, Beznoussenko G, Giacchetti G, Machesky LM, Luini A, Buccione R. Actin dynamics at sites of extracellular matrix degradation. Eur J Cell Biol. 2006;85:1217–1231. doi: 10.1016/j.ejcb.2006.08.003. PubMed DOI

Bowden ET, Onikoyi E, Slack R, Myoui A, Yoneda T, Yamada KM, Mueller SC. Co-localization of cortactin and phosphotyrosine identifies active invadopodia in human breast cancer cells. Exp Cell Res. 2006;312:1240–1253. doi: 10.1016/j.yexcr.2005.12.012. PubMed DOI

Yamaguchi H, Lorenz M, Kempiak S, Sarmiento C, Coniglio S, Symons M, Segall J, Eddy R, Miki H, Takenawa T. Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J Cell Biol. 2005;168:441–452. doi: 10.1083/jcb.200407076. PubMed DOI PMC

Linder S. The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol. 2007;17:107–117. doi: 10.1016/j.tcb.2007.01.002. PubMed DOI

Linder S, Aepfelbacher M. Podosomes: adhesion hot-spots of invasive cells. Trends Cell Biol. 2003;13:376–385. doi: 10.1016/S0962-8924(03)00128-4. PubMed DOI

Janostiak R, Tolde O, Bruhova Z, Novotny M, Hanks SK, Rosel D, Brabek J. Tyrosine phosphorylation within the SH3 domain regulates CAS subcellular localization, cell migration, and invasiveness. Mol Biol Cell. 2011;22:4256–4267. doi: 10.1091/mbc.E11-03-0207. PubMed DOI PMC

Li A, Dawson JC, Forero-Vargas M, Spence HJ, Yu X, Konig I, Anderson K, Machesky LM. The actin-bundling protein fascin stabilizes actin in invadopodia and potentiates protrusive invasion. Curr Biol. 2010;20:339–345. doi: 10.1016/j.cub.2009.12.035. PubMed DOI PMC

Schoumacher M, Goldman RD, Louvard D, Vignjevic DM. Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J Cell Biol. 2010;189:541–556. doi: 10.1083/jcb.200909113. PubMed DOI PMC

Tolde O, Rosel D, Vesely P, Folk P, Brabek J. The structure of invadopodia in a complex 3D environment. Eur J Cell Biol. 2010;89:674–680. doi: 10.1016/j.ejcb.2010.04.003. PubMed DOI

Fishell G, Hanashima C. Pyramidal neurons grow up and change their mind. Neuron. 2008;57:333–338. doi: 10.1016/j.neuron.2008.01.018. PubMed DOI

Megias M, Emri Z, Freund TF, Gulyas AI. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience. 2001;102:527–540. doi: 10.1016/S0306-4522(00)00496-6. PubMed DOI

Noctor SC, Flint AC, Weissman TA, Wong WS, Clinton BK, Kriegstein AR. Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci. 2002;22:3161–3173. PubMed PMC

Valiente M, Marin O. Neuronal migration mechanisms in development and disease. Curr Opin Neurobiol. 2010;20:68–78. doi: 10.1016/j.conb.2009.12.003. PubMed DOI

Zheng W, Yuan X. Guidance of cortical radial migration by gradient of diffusible factors. Cell Adh Migr. 2008;2:48–50. doi: 10.4161/cam.2.1.6001. PubMed DOI PMC

Reiner O, Sapir T. Polarity regulation in migrating neurons in the cortex. Mol Neurobiol. 2009;40:1–14. doi: 10.1007/s12035-009-8065-0. PubMed DOI

Kawauchi T, Chihama K, Nabeshima Y, Hoshino M. Cdk5 phosphorylates and stabilizes p27kip1 contributing to actin organization and cortical neuronal migration. Nat Cell Biol. 2006;8:17–26. doi: 10.1038/ncb1338. PubMed DOI

Letinic K, Sebastian R, Toomre D, Rakic P. Exocyst is involved in polarized cell migration and cerebral cortical development. Proc Natl Acad Sci U S A. 2009;106:11342–11347. doi: 10.1073/pnas.0904244106. PubMed DOI PMC

Shu T, Ayala R, Nguyen MD, Xie Z, Gleeson JG, Tsai LH. Ndel1 operates in a common pathway with LIS1 and cytoplasmic dynein to regulate cortical neuronal positioning. Neuron. 2004;44:263–277. doi: 10.1016/j.neuron.2004.09.030. PubMed DOI

Tanaka T, Serneo FF, Higgins C, Gambello MJ, Wynshaw-Boris A, Gleeson JG. Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J Cell Biol. 2004;165:709–721. doi: 10.1083/jcb.200309025. PubMed DOI PMC

Xie Z, Sanada K, Samuels BA, Shih H, Tsai LH. Serine 732 phosphorylation of FAK by Cdk5 is important for microtubule organization, nuclear movement, and neuronal migration. Cell. 2003;114:469–482. doi: 10.1016/S0092-8674(03)00605-6. PubMed DOI

Anton ES, Kreidberg JA, Rakic P. Distinct functions of alpha3 and alpha(v) integrin receptors in neuronal migration and laminar organization of the cerebral cortex. Neuron. 1999;22:277–289. doi: 10.1016/S0896-6273(00)81089-2. PubMed DOI

Elias LA, Wang DD, Kriegstein AR. Gap junction adhesion is necessary for radial migration in the neocortex. Nature. 2007;448:901–907. doi: 10.1038/nature06063. PubMed DOI

Forster E, Bock HH, Herz J, Chai X, Frotscher M, Zhao S. Emerging topics in reelin function. Eur J Neurosci. 2010;31:1511–1518. PubMed PMC

Gongidi V, Ring C, Moody M, Brekken R, Sage EH, Rakic P, Anton ES. SPARC-like 1 regulates the terminal phase of radial glia-guided migration in the cerebral cortex. Neuron. 2004;41:57–69. doi: 10.1016/S0896-6273(03)00818-3. PubMed DOI

Gupta A, Sanada K, Miyamoto DT, Rovelstad S, Nadarajah B, Pearlman AL, Brunstrom J, Tsai LH. Layering defect in p35 deficiency is linked to improper neuronal-glial interaction in radial migration. Nat Neurosci. 2003;6:1284–1291. doi: 10.1038/nn1151. PubMed DOI

Rakic S, Yanagawa Y, Obata K, Faux C, Parnavelas JG, Nikolic M. Cortical interneurons require p35/Cdk5 for their migration and laminar organization. Cereb Cortex. 2009;19:1857–1869. doi: 10.1093/cercor/bhn213. PubMed DOI PMC

Causeret F, Terao M, Jacobs T, Nishimura YV, Yanagawa Y, Obata K, Hoshino M, Nikolic M. The p21-activated kinase is required for neuronal migration in the cerebral cortex. Cereb Cortex. 2009;19:861–875. PubMed PMC

Banker GA, Cowan WM. Rat hippocampal neurons in dispersed cell culture. Brain Res. 1977;126:397–42. doi: 10.1016/0006-8993(77)90594-7. PubMed DOI

Craig AM, Banker G. Neuronal polarity. Annu Rev Neurosci. 1994;17:267–310. doi: 10.1146/annurev.ne.17.030194.001411. PubMed DOI

Dotti CG, Sullivan CA, Banker GA. The establishment of polarity by hippocampal neurons in culture. J Neurosci. 1988;8:1454–1468. PubMed PMC

Arimura N, Kaibuchi K. Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat Rev Neurosci. 2007;8:194–205. doi: 10.1038/nrn2056. PubMed DOI

Bradke F, Dotti CG. Establishment of neuronal polarity: lessons from cultured hippocampal neurons. Curr Opin Neurobiol. 2000;10:574–581. doi: 10.1016/S0959-4388(00)00124-0. PubMed DOI

Barnes AP, Solecki D, Polleux F. New insights into the molecular mechanisms specifying neuronal polarity in vivo. Curr Opin Neurobiol. 2008;18:44–52. doi: 10.1016/j.conb.2008.05.003. PubMed DOI PMC

de Anda FC, Pollarolo G, Da Silva JS, Camoletto PG, Feiguin F, Dotti CG. Centrosome localization determines neuronal polarity. Nature. 2005;436:704–708. doi: 10.1038/nature03811. PubMed DOI

Asada N, Sanada K, Fukada Y. LKB1 regulates neuronal migration and neuronal differentiation in the developing neocortex through centrosomal positioning. J Neurosci. 2007;27:11769–11775. doi: 10.1523/JNEUROSCI.1938-07.2007. PubMed DOI PMC

Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci. 2004;7:136–144. doi: 10.1038/nn1172. PubMed DOI

Sapir T, Shmueli A, Levy T, Timm T, Elbaum M, Mandelkow EM, Reiner O. Antagonistic effects of doublecortin and MARK2/Par-1 in the developing cerebral cortex. J Neurosci. 2008;28:13008–13013. doi: 10.1523/JNEUROSCI.2363-08.2008. PubMed DOI PMC

de Anda FC, Meletis K, Ge X, Rei D, Tsai LH. Centrosome motility is essential for initial axon formation in the neocortex. J Neurosci. 2010;30:10391–10406. doi: 10.1523/JNEUROSCI.0381-10.2010. PubMed DOI PMC

Chae K, Lord EM. Pollen tube growth and guidance: roles of small, secreted proteins. Ann Bot. 2011;108:627–636. doi: 10.1093/aob/mcr015. PubMed DOI PMC

Lord EM. Adhesion and guidance in compatible pollination. J Exp Bot. 2003;54:47–54. doi: 10.1093/jxb/erg015. PubMed DOI

Tabuchi A, Li LC, Cosgrove DJ. Matrix solubilization and cell wall weakening by beta-expansin (group-1 allergen) from maize pollen. Plant J. 2011;68:546–559. doi: 10.1111/j.1365-313X.2011.04705.x. PubMed DOI

Szymanski DB, Cosgrove DJ. Dynamic coordination of cytoskeletal and cell wall systems during plant cell morphogenesis. Curr Biol. 2009;19:R800–R811. doi: 10.1016/j.cub.2009.07.056. PubMed DOI

Winship LJ, Obermeyer G, Geitmann A, Hepler PK. Pollen tubes and the physical world. Trends Plant Sci. 2011;16:353–355. doi: 10.1016/j.tplants.2011.03.010. PubMed DOI

Carol RJ, Dolan L. Building a hair: tip growth in Arabidopsis thaliana root hairs. Philos Trans R Soc Lond B Biol Sci. 2002;357:815–821. doi: 10.1098/rstb.2002.1092. PubMed DOI PMC

Schiefelbein J, Kwak SH, Wieckowski Y, Barron C, Bruex A. The gene regulatory network for root epidermal cell-type pattern formation in Arabidopsis. J Exp Bot. 2009;60:1515–1521. doi: 10.1093/jxb/ern339. PubMed DOI PMC

Fischer U, Ikeda Y, Grebe M. Planar polarity of root hair positioning in Arabidopsis. Biochem Soc Trans. 2007;35:149–151. doi: 10.1042/BST0350149. PubMed DOI

Baluska F, Salaj J, Mathur J, Braun M, Jasper F, Samaj J, Chua NH, Barlow PW, Volkmann D. Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. Dev Biol. 2000;227:618–632. doi: 10.1006/dbio.2000.9908. PubMed DOI

Vissenberg K, Fry SC, Verbelen JP. Root hair initiation is coupled to a highly localized increase of xyloglucan endotransglycosylase action in Arabidopsis roots. Plant Physiol. 2001;127:1125–1135. doi: 10.1104/pp.010295. PubMed DOI PMC

Singh SK, Fischer U, Singh M, Grebe M, Marchant A. Insight into the early steps of root hair formation revealed by the procuste1 cellulose synthase mutant of Arabidopsis thaliana. BMC Plant Biol. 2008;8:57. doi: 10.1186/1471-2229-8-57. PubMed DOI PMC

Zarsky V, Fowler JE. ROP (Rho-related protein from plants) GTPases for spatial control of root hair morphogenesis. New York: Springer; 2009. pp. 191–210. (Root hairs).

Monshausen GB, Bibikova TN, Messerli MA, Shi C, Gilroy S. Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc Natl Acad Sci U S A. 2007;104:20996–21001. doi: 10.1073/pnas.0708586104. PubMed DOI PMC

Monshausen GB, Messerli MA, Gilroy S. Imaging of the Yellow Cameleon 3.6 indicator reveals that elevations in cytosolic Ca2+ follow oscillating increases in growth in root hairs of Arabidopsis. Plant Physiol. 2008;147:1690–1698. doi: 10.1104/pp.108.123638. PubMed DOI PMC

Iwano M, Entani T, Shiba H, Kakita M, Nagai T, Mizuno H, Miyawaki A, Shoji T, Kubo K, Isogai A. Fine-tuning of the cytoplasmic Ca2+ concentration is essential for pollen tube growth. Plant Physiol. 2009;150:1322–1334. doi: 10.1104/pp.109.139329. PubMed DOI PMC

Xu T, Wen M, Nagawa S, Fu Y, Chen JG, Wu MJ, Perrot-Rechenmann C, Friml J, Jones AM, Yang Z. Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell. 2010;143:99–110. doi: 10.1016/j.cell.2010.09.003. PubMed DOI PMC

Robert S, Kleine-Vehn J, Barbez E, Sauer M, Paciorek T, Baster P, Vanneste S, Zhang J, Simon S, Covanova M. ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell. 2010;143:111–121. doi: 10.1016/j.cell.2010.09.027. PubMed DOI PMC

Bourne HR, Sanders DA, McCormick F. The GTPase superfamily: a conserved switch for diverse cell functions. Nature. 1990;348:125–132. doi: 10.1038/348125a0. PubMed DOI

Bourne HR, Sanders DA, McCormick F. The GTPase superfamily: conserved structure and molecular mechanism. Nature. 1991;349:117–127. doi: 10.1038/349117a0. PubMed DOI

Hall A. Small GTP-binding proteins and the regulation of the actin cytoskeleton. Annu Rev Cell Biol. 1994;10:31–54. doi: 10.1146/annurev.cb.10.110194.000335. PubMed DOI

Hall A. Rho GTPases and the control of cell behaviour. Biochem Soc Trans. 2005;33:891–895. PubMed

Harris SD. Cdc42/Rho GTPases in fungi: variations on a common theme. Mol Microbiol. 2011;79:1123–1127. doi: 10.1111/j.1365-2958.2010.07525.x. PubMed DOI

Kwon MJ, Arentshorst M, Roos ED, van den Hondel CA, Meyer V, Ram AF. Functional characterization of Rho GTPases in Aspergillus niger uncovers conserved and diverged roles of Rho proteins within filamentous fungi. Mol Microbiol. 2011;79:1151–1167. doi: 10.1111/j.1365-2958.2010.07524.x. PubMed DOI

Etienne-Manneville S. Cdc42–the centre of polarity. J Cell Sci. 2004;117:1291–1300. doi: 10.1242/jcs.01115. PubMed DOI

Heasman SJ, Ridley AJ. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol. 2008;9:690–701. doi: 10.1038/nrm2476. PubMed DOI

Nobes CD, Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell. 1995;81:53–62. doi: 10.1016/0092-8674(95)90370-4. PubMed DOI

Nakahara H, Otani T, Sasaki T, Miura Y, Takai Y, Kogo M. Involvement of Cdc42 and Rac small G proteins in invadopodia formation of RPMI7951 cells. Genes Cells. 2003;8:1019–1027. doi: 10.1111/j.1365-2443.2003.00695.x. PubMed DOI

Sakurai-Yageta M, Recchi C, Le Dez G, Sibarita JB, Daviet L, Camonis J, D’Souza-Schorey C, Chavrier P. The interaction of IQGAP1 with the exocyst complex is required for tumor cell invasion downstream of Cdc42 and RhoA. J Cell Biol. 2008;181:985–998. doi: 10.1083/jcb.200709076. PubMed DOI PMC

Luo L, Liao YJ, Jan LY, Jan YN. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 1994;8:1787–1802. doi: 10.1101/gad.8.15.1787. PubMed DOI

Allen MJ, Shan X, Murphey RK. A role for Drosophila Drac1 in neurite outgrowth and synaptogenesis in the giant fiber system. Mol Cell Neurosci. 2000;16:754–765. doi: 10.1006/mcne.2000.0903. PubMed DOI

Ng J, Nardine T, Harms M, Tzu J, Goldstein A, Sun Y, Dietzl G, Dickson BJ, Luo L. Rac GTPases control axon growth, guidance and branching. Nature. 2002;416:442–447. doi: 10.1038/416442a. PubMed DOI

Hakeda-Suzuki S, Ng J, Tzu J, Dietzl G, Sun Y, Harms M, Nardine T, Luo L, Dickson BJ. Rac function and regulation during Drosophila development. Nature. 2002;416:438–442. doi: 10.1038/416438a. PubMed DOI

Malartre M, Ayaz D, Amador FF, Martin-Bermudo MD. The guanine exchange factor vav controls axon growth and guidance during Drosophila development. J Neurosci. 2010;30:2257–2267. doi: 10.1523/JNEUROSCI.1820-09.2010. PubMed DOI PMC

Miyamoto Y, Yamauchi J. Cellular signaling of Dock family proteins in neural function. Cell Signal. 2010;22:175–182. doi: 10.1016/j.cellsig.2009.09.036. PubMed DOI

Song JK, Giniger E. Noncanonical Notch function in motor axon guidance is mediated by Rac GTPase and the GEF1 domain of Trio. Dev Dyn. 2011;240:324–332. doi: 10.1002/dvdy.22525. PubMed DOI PMC

Chen L, Liao G, Waclaw RR, Burns KA, Linquist D, Campbell K, Zheng Y, Kuan CY. Rac1 controls the formation of midline commissures and the competency of tangential migration in ventral telencephalic neurons. J Neurosci. 2007;27:3884–3893. doi: 10.1523/JNEUROSCI.3509-06.2007. PubMed DOI PMC

Kassai H, Terashima T, Fukaya M, Nakao K, Sakahara M, Watanabe M, Aiba A. Rac1 in cortical projection neurons is selectively required for midline crossing of commissural axonal formation. Eur J Neurosci. 2008;28:257–267. doi: 10.1111/j.1460-9568.2008.06343.x. PubMed DOI

Corbetta S, Gualdoni S, Ciceri G, Monari M, Zuccaro E, Tybulewicz VL, de Curtis I. Essential role of Rac1 and Rac3 GTPases in neuronal development. FASEB J. 2009;23:1347–1357. doi: 10.1096/fj.08-121574. PubMed DOI PMC

Tahirovic S, Hellal F, Neukirchen D, Hindges R, Garvalov BK, Flynn KC, Stradal TE, Chrostek-Grashoff A, Brakebusch C, Bradke F. Rac1 regulates neuronal polarization through the WAVE complex. J Neurosci. 2010;30:6930–6943. doi: 10.1523/JNEUROSCI.5395-09.2010. PubMed DOI PMC

Chen L, Liao G, Yang L, Campbell K, Nakafuku M, Kuan CY, Zheng Y. Cdc42 deficiency causes Sonic hedgehog-independent holoprosencephaly. Proc Natl Acad Sci U S A. 2006;103:16520–16525. doi: 10.1073/pnas.0603533103. PubMed DOI PMC

Cappello S, Attardo A, Wu X, Iwasato T, Itohara S, Wilsch-Brauninger M, Eilken HM, Rieger MA, Schroeder TT, Huttner WB. The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat Neurosci. 2006;9:1099–1107. doi: 10.1038/nn1744. PubMed DOI

Yalovsky S, Bloch D, Sorek N, Kost B. Regulation of membrane trafficking, cytoskeleton dynamics, and cell polarity by ROP/RAC GTPases. Plant Physiol. 2008;147:1527–1543. doi: 10.1104/pp.108.122150. PubMed DOI PMC

Hazak O, Bloch D, Poraty L, Sternberg H, Zhang J, Friml J, Yalovsky S. A rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution. PLoS Biol. 2010;8:e1000282. doi: 10.1371/journal.pbio.1000282. PubMed DOI PMC

Nagawa S, Xu T, Yang Z. RHO GTPase in plants: Conservation and invention of regulators and effectors. Small GTPases. 2010;1:78–88. doi: 10.4161/sgtp.1.2.14544. PubMed DOI PMC

Li H, Lin Y, Heath RM, Zhu MX, Yang Z. Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell. 1999;11:1731–1742. PubMed PMC

Molendijk AJ, Bischoff F, Rajendrakumar CS, Friml J, Braun M, Gilroy S, Palme K. Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth. EMBO J. 2001;20:2779–2788. doi: 10.1093/emboj/20.11.2779. PubMed DOI PMC

Carol RJ, Takeda S, Linstead P, Durrant MC, Kakesova H, Derbyshire P, Drea S, Zarsky V, Dolan L. A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature. 2005;438:1013–1016. doi: 10.1038/nature04198. PubMed DOI

Fischer U, Ikeda Y, Ljung K, Serralbo O, Singh M, Heidstra R, Palme K, Scheres B, Grebe M. Vectorial information for Arabidopsis planar polarity is mediated by combined AUX1, EIN2, and GNOM activity. Curr Biol. 2006;16:2143–2149. doi: 10.1016/j.cub.2006.08.091. PubMed DOI

Berken A, Thomas C, Wittinghofer A. A new family of RhoGEFs activates the Rop molecular switch in plants. Nature. 2005;436:1176–1180. doi: 10.1038/nature03883. PubMed DOI

Locke S, Fricke I, Mucha E, Humpert ML, Berken A. Interactions in the pollen-specific receptor-like kinases-containing signaling network. Eur J Cell Biol. 2010;89:917–923. doi: 10.1016/j.ejcb.2010.08.002. PubMed DOI

Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell. 2004;16:1220–1234. doi: 10.1105/tpc.020834. PubMed DOI PMC

Duan Q, Kita D, Li C, Cheung AY, Wu HM. FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc Natl Acad Sci U S A. 2010;107:17821–17826. doi: 10.1073/pnas.1005366107. PubMed DOI PMC

Zhou K, Wang Y, Gorski JL, Nomura N, Collard J, Bokoch GM. Guanine nucleotide exchange factors regulate specificity of downstream signaling from Rac and Cdc42. J Biol Chem. 1998;273:16782–16786. doi: 10.1074/jbc.273.27.16782. PubMed DOI

Olson MF. Guanine nucleotide exchange factors for the Rho GTPases: a role in human disease? J Mol Med (Berl) 1996;74:563–571. doi: 10.1007/s001090050060. PubMed DOI

Pasteris NG, Cadle A, Logie LJ, Porteous ME, Schwartz CE, Stevenson RE, Glover TW, Wilroy RS, Gorski JL. Isolation and characterization of the faciogenital dysplasia (Aarskog-Scott syndrome) gene: a putative Rho/Rac guanine nucleotide exchange factor. Cell. 1994;79:669–678. doi: 10.1016/0092-8674(94)90552-5. PubMed DOI

Ayala I, Giacchetti G, Caldieri G, Attanasio F, Mariggio S, Tete S, Polishchuk R, Castronovo V, Buccione R. Faciogenital dysplasia protein Fgd1 regulates invadopodia biogenesis and extracellular matrix degradation and is up-regulated in prostate and breast cancer. Cancer Res. 2009;69:747–752. doi: 10.1158/0008-5472.CAN-08-1980. PubMed DOI

Kost B. Spatial control of Rho (Rac-Rop) signaling in tip-growing plant cells. Trends Cell Biol. 2008;18:119–127. doi: 10.1016/j.tcb.2008.01.003. PubMed DOI

Donaldson JG, Jackson CL. ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat Rev Mol Cell Biol. 2011;12:362–375. doi: 10.1038/nrm3117. PubMed DOI PMC

Nielsen ME, Feechan A, Bohlenius H, Ueda T, Thordal-Christensen H. Arabidopsis ARF-GTP exchange factor, GNOM, mediates transport required for innate immunity and focal accumulation of syntaxin PEN1. Proc Natl Acad Sci U S A. 2012;109:11443–11448. doi: 10.1073/pnas.1117596109. PubMed DOI PMC

Palacios F, Price L, Schweitzer J, Collard JG, D’Souza-Schorey C. An essential role for ARF6-regulated membrane traffic in adherens junction turnover and epithelial cell migration. EMBO J. 2001;20:4973–4986. doi: 10.1093/emboj/20.17.4973. PubMed DOI PMC

Hashimoto S, Onodera Y, Hashimoto A, Tanaka M, Hamaguchi M, Yamada A, Sabe H. Requirement for Arf6 in breast cancer invasive activities. Proc Natl Acad Sci U S A. 2004;101:6647–6652. doi: 10.1073/pnas.0401753101. PubMed DOI PMC

Tague SE, Muralidharan V, D’Souza-Schorey C. ADP-ribosylation factor 6 regulates tumor cell invasion through the activation of the MEK/ERK signaling pathway. Proc Natl Acad Sci U S A. 2004;101:9671–9676. doi: 10.1073/pnas.0403531101. PubMed DOI PMC

Muralidharan-Chari V, Hoover H, Clancy J, Schweitzer J, Suckow MA, Schroeder V, Castellino FJ, Schorey JS, D’Souza-Schorey C. ADP-ribosylation factor 6 regulates tumorigenic and invasive properties in vivo. Cancer Res. 2009;69:2201–2209. doi: 10.1158/0008-5472.CAN-08-1301. PubMed DOI PMC

Hernandez-Deviez DJ, Casanova JE, Wilson JM. Regulation of dendritic development by the ARF exchange factor ARNO. Nat Neurosci. 2002;5:623–624. PubMed

Albertinazzi C, Za L, Paris S, de Curtis I. ADP-ribosylation factor 6 and a functional PIX/p95-APP1 complex are required for Rac1B-mediated neurite outgrowth. Mol Biol Cell. 2003;14:1295–1307. doi: 10.1091/mbc.E02-07-0406. PubMed DOI PMC

Hernandez-Deviez DJ, Roth MG, Casanova JE, Wilson JM. ARNO and ARF6 regulate axonal elongation and branching through downstream activation of phosphatidylinositol 4-phosphate 5-kinase alpha. Mol Biol Cell. 2004;15:111–120. PubMed PMC

Moore CD, Thacker EE, Larimore J, Gaston D, Underwood A, Kearns B, Patterson SI, Jackson T, Chapleau C, Pozzo-Miller L. The neuronal Arf GAP centaurin alpha1 modulates dendritic differentiation. J Cell Sci. 2007;120:2683–2693. doi: 10.1242/jcs.006346. PubMed DOI PMC

Song XF, Yang CY, Liu J, Yang WC. RPA, a class II ARFGAP protein, activates ARF1 and U5 and plays a role in root hair development in Arabidopsis. Plant Physiol. 2006;141:966–976. doi: 10.1104/pp.106.077818. PubMed DOI PMC

Yoo CM, Wen J, Motes CM, Sparks JA, Blancaflor EB. A class I ADP-ribosylation factor GTPase-activating protein is critical for maintaining directional root hair growth in Arabidopsis. Plant Physiol. 2008;147:1659–1674. doi: 10.1104/pp.108.119529. PubMed DOI PMC

Yoo CM, Quan L, Cannon AE, Wen J, Blancaflor EB. AGD1, a class 1 ARF-GAP, acts in common signaling pathways with phosphoinositide metabolism and the actin cytoskeleton in controlling Arabidopsis root hair polarity. Plant J. 2012;69:1064–1076. doi: 10.1111/j.1365-313X.2011.04856.x. PubMed DOI

Hutagalung AH, Novick PJ. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev. 2011;91:119–149. doi: 10.1152/physrev.00059.2009. PubMed DOI PMC

Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol. 2009;10:513–525. PubMed

Woollard AA, Moore I. The functions of Rab GTPases in plant membrane traffic. Curr Opin Plant Biol. 2008;11:610–619. doi: 10.1016/j.pbi.2008.09.010. PubMed DOI

Bravo-Cordero JJ, Marrero-Diaz R, Megias D, Genis L, Garcia-Grande A, Garcia MA, Arroyo AG, Montoya MC. MT1-MMP proinvasive activity is regulated by a novel Rab8-dependent exocytic pathway. EMBO J. 2007;26:1499–1510. doi: 10.1038/sj.emboj.7601606. PubMed DOI PMC

Caswell PT, Spence HJ, Parsons M, White DP, Clark K, Cheng KW, Mills GB, Humphries MJ, Messent AJ, Anderson KI. Rab25 associates with alpha5beta1 integrin to promote invasive migration in 3D microenvironments. Dev Cell. 2007;13:496–510. doi: 10.1016/j.devcel.2007.08.012. PubMed DOI

Hendrix A, Maynard D, Pauwels P, Braems G, Denys H, Van den BR, Lambert J, Van Belle S, Cocquyt V, Gespach C. Effect of the secretory small GTPase Rab27B on breast cancer growth, invasion, and metastasis. J Natl Cancer Inst. 2010;102:866–880. doi: 10.1093/jnci/djq153. PubMed DOI PMC

Peranen J. Rab8 GTPase as a regulator of cell shape. Cytoskeleton (Hoboken) 2011;68:527–539. doi: 10.1002/cm.20529. PubMed DOI

Wang L, Liang Z, Li G. Rab22 controls NGF signaling and neurite outgrowth in PC12 cells. Mol Biol Cell. 2011;22:3853–3860. doi: 10.1091/mbc.E11-03-0277. PubMed DOI PMC

Mori Y, Matsui T, Furutani Y, Yoshihara Y, Fukuda M. Small GTPase Rab17 regulates dendritic morphogenesis and postsynaptic development of hippocampal neurons. J Biol Chem. 2012;287:8963–8973. doi: 10.1074/jbc.M111.314385. PubMed DOI PMC

Viotti C, Bubeck J, Stierhof YD, Krebs M, Langhans M. van den BW, van Dongen W, Richter S, Geldner N, Takano J et al.: Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell. 2010;22:1344–1357. doi: 10.1105/tpc.109.072637. PubMed DOI PMC

Preuss ML, Serna J, Falbel TG, Bednarek SY, Nielsen E. The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell. 2004;16:1589–1603. doi: 10.1105/tpc.021634. PubMed DOI PMC

de Graaf BH, Cheung AY, Andreyeva T, Levasseur K, Kieliszewski M, Wu HM. Rab11 GTPase-regulated membrane trafficking is crucial for tip-focused pollen tube growth in tobacco. Plant Cell. 2005;17:2564–2579. doi: 10.1105/tpc.105.033183. PubMed DOI PMC

Szumlanski AL, Nielsen E. The Rab GTPase RabA4d regulates pollen tube tip growth in Arabidopsis thaliana. Plant Cell. 2009;21:526–544. doi: 10.1105/tpc.108.060277. PubMed DOI PMC

Vignjevic D, Montagnac G. Reorganisation of the dendritic actin network during cancer cell migration and invasion. Semin Cancer Biol. 2008;18:12–22. doi: 10.1016/j.semcancer.2007.08.001. PubMed DOI

Jacobs T, Causeret F, Nishimura YV, Terao M, Norman A, Hoshino M, Nikolic M. Localized activation of p21-activated kinase controls neuronal polarity and morphology. J Neurosci. 2007;27:8604–8615. doi: 10.1523/JNEUROSCI.0765-07.2007. PubMed DOI PMC

Geitmann A. How to shape a cylinder: pollen tube as a model system for the generation of complex cellular geometry. Sex Plant Reprod. 2010;23:63–71. doi: 10.1007/s00497-009-0121-4. PubMed DOI

Gossot O, Geitmann A. Pollen tube growth: coping with mechanical obstacles involves the cytoskeleton. Planta. 2007;226:405–416. doi: 10.1007/s00425-007-0491-5. PubMed DOI

Cheung AY, Niroomand S, Zou Y, Wu HM. A transmembrane formin nucleates subapical actin assembly and controls tip-focused growth in pollen tubes. Proc Natl Acad Sci U S A. 2010;107:16390–16395. doi: 10.1073/pnas.1008527107. PubMed DOI PMC

Daher FB, Geitmann A. Actin depolymerizing factors ADF7 and ADF10 play distinct roles during pollen development and pollen tube growth. Plant Signal Behav. 2012;7:879–881. PubMed PMC

Lovy-Wheeler A, Wilsen KL, Baskin TI, Hepler PK. Enhanced fixation reveals the apical cortical fringe of actin filaments as a consistent feature of the pollen tube. Planta. 2005;221:95–104. doi: 10.1007/s00425-004-1423-2. PubMed DOI

Gibbon BC, Kovar DR, Staiger CJ. Latrunculin B has different effects on pollen germination and tube growth. Plant Cell. 1999;11:2349–2363. PubMed PMC

Ketelaar T, de Ruijter NC, Emons AM. Unstable F-actin specifies the area and microtubule direction of cell expansion in Arabidopsis root hairs. Plant Cell. 2003;15:285–292. doi: 10.1105/tpc.007039. PubMed DOI PMC

Chen T, Teng N, Wu X, Wang Y, Tang W, Samaj J, Baluska F, Lin J. Disruption of actin filaments by latrunculin B affects cell wall construction in Picea meyeri pollen tube by disturbing vesicle trafficking. Plant Cell Physiol. 2007;48:19–30. PubMed

Muallem S, Kwiatkowska K, Xu X, Yin HL. Actin filament disassembly is a sufficient final trigger for exocytosis in nonexcitable cells. J Cell Biol. 1995;128:589–598. doi: 10.1083/jcb.128.4.589. PubMed DOI PMC

Bradke F, Dotti CG. The role of local actin instability in axon formation. Science. 1999;283:1931–1934. doi: 10.1126/science.283.5409.1931. PubMed DOI

Jog NR, Rane MJ, Lominadze G, Luerman GC, Ward RA, McLeish KR. The actin cytoskeleton regulates exocytosis of all neutrophil granule subsets. Am J Physiol Cell Physiol. 2007;292:C1690–C1700. PubMed

Valentijn KM, Gumkowski FD, Jamieson JD. The subapical actin cytoskeleton regulates secretion and membrane retrieval in pancreatic acinar cells. J Cell Sci. 1999;112(Pt 1):81–96. PubMed

Goley ED, Welch MD. The ARP2/3 complex: an actin nucleator comes of age. Nat Rev Mol Cell Biol. 2006;7:713–726. doi: 10.1038/nrm2026. PubMed DOI

Stradal TE, Scita G. Protein complexes regulating Arp2/3-mediated actin assembly. Curr Opin Cell Biol. 2006;18:4–10. doi: 10.1016/j.ceb.2005.12.003. PubMed DOI

Lorenz M, Yamaguchi H, Wang Y, Singer RH, Condeelis J. Imaging sites of N-wasp activity in lamellipodia and invadopodia of carcinoma cells. Curr Biol. 2004;14:697–703. doi: 10.1016/j.cub.2004.04.008. PubMed DOI

Cudmore S, Cossart P, Griffiths G, Way M. Actin-based motility of vaccinia virus. Nature. 1995;378:636–638. doi: 10.1038/378636a0. PubMed DOI

Gouin E, Welch MD, Cossart P. Actin-based motility of intracellular pathogens. Curr Opin Microbiol. 2005;8:35–45. doi: 10.1016/j.mib.2004.12.013. PubMed DOI

Strasser GA, Rahim NA, VanderWaal KE, Gertler FB, Lanier LM. Arp2/3 is a negative regulator of growth cone translocation. Neuron. 2004;43:81–94. doi: 10.1016/j.neuron.2004.05.015. PubMed DOI

Mongiu AK, Weitzke EL, Chaga OY, Borisy GG. Kinetic-structural analysis of neuronal growth cone veil motility. J Cell Sci. 2007;120:1113–1125. doi: 10.1242/jcs.03384. PubMed DOI

Korobova F, Svitkina T. Molecular architecture of synaptic actin cytoskeleton in hippocampal neurons reveals a mechanism of dendritic spine morphogenesis. Mol Biol Cell. 2010;21:165–176. doi: 10.1091/mbc.E09-07-0596. PubMed DOI PMC

Pommereit D, Wouters FS. An NGF-induced Exo70-TC10 complex locally antagonises Cdc42-mediated activation of N-WASP to modulate neurite outgrowth. J Cell Sci. 2007;120:2694–2705. doi: 10.1242/jcs.03475. PubMed DOI

Szymanski DB. Breaking the WAVE complex: the point of Arabidopsis trichomes. Curr Opin Plant Biol. 2005;8:103–112. doi: 10.1016/j.pbi.2004.11.004. PubMed DOI

Basu D, Le J, Zakharova T, Mallery EL, Szymanski DB. A SPIKE1 signaling complex controls actin-dependent cell morphogenesis through the heteromeric WAVE and ARP2/3 complexes. Proc Natl Acad Sci U S A. 2008;105:4044–4049. doi: 10.1073/pnas.0710294105. PubMed DOI PMC

Deeks MJ, Hussey PJ, Davies B. Formins: intermediates in signal-transduction cascades that affect cytoskeletal reorganization. Trends Plant Sci. 2002;7:492–498. doi: 10.1016/S1360-1385(02)02341-5. PubMed DOI

Cvrckova F, Novotny M, Pickova D, Zarsky V. Formin homology 2 domains occur in multiple contexts in angiosperms. BMC Genomics. 2004;5:44. doi: 10.1186/1471-2164-5-44. PubMed DOI PMC

Grunt M, Zarsky V, Cvrckova F. Roots of angiosperm formins: the evolutionary history of plant FH2 domain-containing proteins. BMC Evol Biol. 2008;8:115. doi: 10.1186/1471-2148-8-115. PubMed DOI PMC

Lizarraga F, Poincloux R, Romao M, Montagnac G, Le Dez G, Bonne I, Rigaill G, Raposo G, Chavrier P. Diaphanous-related formins are required for invadopodia formation and invasion of breast tumor cells. Cancer Res. 2009;69:2792–2800. doi: 10.1158/0008-5472.CAN-08-3709. PubMed DOI

Ridley AJ. Life at the leading edge. Cell. 2011;145:1012–1022. doi: 10.1016/j.cell.2011.06.010. PubMed DOI

Matusek T, Gombos R, Szecsenyi A, Sanchez-Soriano N, Czibula A, Pataki C, Gedai A, Prokop A, Rasko I, Mihaly J. Formin proteins of the DAAM subfamily play a role during axon growth. J Neurosci. 2008;28:13310–13319. doi: 10.1523/JNEUROSCI.2727-08.2008. PubMed DOI PMC

Cheung AY, Wu HM. Overexpression of an Arabidopsis formin stimulates supernumerary actin cable formation from pollen tube cell membrane. Plant Cell. 2004;16:257–269. doi: 10.1105/tpc.016550. PubMed DOI PMC

Ye J, Zheng Y, Yan A, Chen N, Wang Z, Huang S, Yang Z. Arabidopsis formin3 directs the formation of actin cables and polarized growth in pollen tubes. Plant Cell. 2009;21:3868–3884. doi: 10.1105/tpc.109.068700. PubMed DOI PMC

Yi K, Guo C, Chen D, Zhao B, Yang B, Ren H. Cloning and functional characterization of a formin-like protein (AtFH8) from Arabidopsis. Plant Physiol. 2005;138:1071–1082. doi: 10.1104/pp.104.055665. PubMed DOI PMC

Deeks MJ, Cvrckova F, Machesky LM, Mikitova V, Ketelaar T, Zarsky V, Davies B, Hussey PJ. Arabidopsis group Ie formins localize to specific cell membrane domains, interact with actin-binding proteins and cause defects in cell expansion upon aberrant expression. New Phytol. 2005;168:529–540. doi: 10.1111/j.1469-8137.2005.01582.x. PubMed DOI

Goode BL, Eck MJ. Mechanism and function of formins in the control of actin assembly. Annu Rev Biochem. 2007;76:593–627. doi: 10.1146/annurev.biochem.75.103004.142647. PubMed DOI

Vidali L, van Gisbergen PA, Guerin C, Franco P, Li M, Burkart GM, Augustine RC, Blanchoin L, Bezanilla M. Rapid formin-mediated actin-filament elongation is essential for polarized plant cell growth. Proc Natl Acad Sci U S A. 2009;106:13341–13346. PubMed PMC

Firat-Karalar EN, Welch MD. New mechanisms and functions of actin nucleation. Curr Opin Cell Biol. 2011;23:4–13. doi: 10.1016/j.ceb.2010.10.007. PubMed DOI PMC

Ahuja R, Pinyol R, Reichenbach N, Custer L, Klingensmith J, Kessels MM, Qualmann B. Cordon-bleu is an actin nucleation factor and controls neuronal morphology. Cell. 2007;131:337–350. doi: 10.1016/j.cell.2007.08.030. PubMed DOI PMC

Vidali L, Burkart GM, Augustine RC, Kerdavid E, Tuzel E, Bezanilla M. Myosin XI is essential for tip growth in Physcomitrella patens. Plant Cell. 2010;22:1868–1882. doi: 10.1105/tpc.109.073288. PubMed DOI PMC

Peremyslov VV, Prokhnevsky AI, Dolja VV. Class XI myosins are required for development, cell expansion, and F-Actin organization in Arabidopsis. Plant Cell. 2010;22:1883–1897. doi: 10.1105/tpc.110.076315. PubMed DOI PMC

Prokhnevsky AI, Peremyslov VV, Dolja VV. Overlapping functions of the four class XI myosins in Arabidopsis growth, root hair elongation, and organelle motility. Proc Natl Acad Sci U S A. 2008;105:19744–19749. doi: 10.1073/pnas.0810730105. PubMed DOI PMC

Peremyslov VV, Prokhnevsky AI, Avisar D, Dolja VV. Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol. 2008;146:1109–1116. doi: 10.1104/pp.107.113654. PubMed DOI PMC

Ojangu EL, Jarve K, Paves H, Truve E. Arabidopsis thaliana myosin XIK is involved in root hair as well as trichome morphogenesis on stems and leaves. Protoplasma. 2007;230:193–202. doi: 10.1007/s00709-006-0233-8. PubMed DOI

Peremyslov VV, Mockler TC, Filichkin SA, Fox SE, Jaiswal P, Makarova KS, Koonin EV, Dolja VV. Expression, splicing, and evolution of the myosin gene family in plants. Plant Physiol. 2011;155:1191–1204. doi: 10.1104/pp.110.170720. PubMed DOI PMC

Wagner W, Brenowitz SD, Hammer JA III. Myosin-Va transports the endoplasmic reticulum into the dendritic spines of Purkinje neurons. Nat Cell Biol. 2011;13:40–48. doi: 10.1038/ncb2132. PubMed DOI PMC

McMichael BK, Cheney RE, Lee BS. Myosin X regulates sealing zone patterning in osteoclasts through linkage of podosomes and microtubules. J Biol Chem. 2010;285:9506–9515. doi: 10.1074/jbc.M109.017269. PubMed DOI PMC

Peremyslov VV, Klocko AL, Fowler JE, Dolja VV. Arabidopsis Myosin XI-K Localizes to the Motile Endomembrane Vesicles Associated with F-actin. Front Plant Sci. 2012;3:184. PubMed PMC

Schott DH, Collins RN, Bretscher A. Secretory vesicle transport velocity in living cells depends on the myosin-V lever arm length. J Cell Biol. 2002;156:35–39. doi: 10.1083/jcb.200110086. PubMed DOI PMC

Oser M, Yamaguchi H, Mader CC, Bravo-Cordero JJ, Arias M, Chen X, Desmarais V, van Rheenen J, Koleske AJ, Condeelis J. Cortactin regulates cofilin and N-WASp activities to control the stages of invadopodium assembly and maturation. J Cell Biol. 2009;186:571–587. doi: 10.1083/jcb.200812176. PubMed DOI PMC

Kronenberg G, Gertz K, Baldinger T, Kirste I, Eckart S, Yildirim F, Ji S, Heuser I, Schrock H, Hortnagl H. Impact of actin filament stabilization on adult hippocampal and olfactory bulb neurogenesis. J Neurosci. 2010;30:3419–3431. doi: 10.1523/JNEUROSCI.4231-09.2010. PubMed DOI PMC

Ren H, Xiang Y. The function of actin-binding proteins in pollen tube growth. Protoplasma. 2007;230:171–182. doi: 10.1007/s00709-006-0231-x. PubMed DOI

Strohmaier AR, Porwol T, Acker H, Spiess E. Three-dimensional organization of microtubules in tumor cells studied by confocal laser scanning microscopy and computer-assisted deconvolution and image reconstruction. Cells Tissues Organs. 2000;167:1–8. doi: 10.1159/000016760. PubMed DOI

Kikuchi K, Takahashi K. W. Cancer Sci. 2008;99:2252–2259. doi: 10.1111/j.1349-7006.2008.00927.x. PubMed DOI PMC

Govek EE, Hatten ME, Van Aelst L. The role of Rho GTPase proteins in CNS neuronal migration. Dev Neurobiol. 2011;71:528–553. doi: 10.1002/dneu.20850. PubMed DOI PMC

Pak CW, Flynn KC, Bamburg JR. Actin-binding proteins take the reins in growth cones. Nat Rev Neurosci. 2008;9:136–147. doi: 10.1038/nrn2236. PubMed DOI

Stiess M, Bradke F. Neuronal polarization: the cytoskeleton leads the way. Dev Neurobiol. 2011;71:430–444. doi: 10.1002/dneu.20849. PubMed DOI

Gallo G. The cytoskeletal and signaling mechanisms of axon collateral branching. Dev Neurobiol. 2011;71:201–220. doi: 10.1002/dneu.20852. PubMed DOI

Goryunov D, He CZ, Lin CS, Leung CL, Liem RK. Nervous-tissue-specific elimination of microtubule-actin crosslinking factor 1a results in multiple developmental defects in the mouse brain. Mol Cell Neurosci. 2010;44:1–14. doi: 10.1016/j.mcn.2010.01.010. PubMed DOI PMC

Leung CL, Sun D, Zheng M, Knowles DR, Liem RK. Microtubule actin cross-linking factor (MACF): a hybrid of dystonin and dystrophin that can interact with the actin and microtubule cytoskeletons. J Cell Biol. 1999;147:1275–1286. doi: 10.1083/jcb.147.6.1275. PubMed DOI PMC

Wu X, Kodama A, Fuchs E. ACF7 regulates cytoskeletal-focal adhesion dynamics and migration and has ATPase activity. Cell. 2008;135:137–148. doi: 10.1016/j.cell.2008.07.045. PubMed DOI PMC

Kodama A, Karakesisoglou I, Wong E, Vaezi A, Fuchs E. ACF7: an essential integrator of microtubule dynamics. Cell. 2003;115:343–354. doi: 10.1016/S0092-8674(03)00813-4. PubMed DOI

Tischfield MA, Baris HN, Wu C, Rudolph G, Van Maldergem L, He W, Chan WM, Andrews C, Demer JL, Robertson RL. Human TUBB3 mutations perturb microtubule dynamics, kinesin interactions, and axon guidance. Cell. 2010;140:74–87. doi: 10.1016/j.cell.2009.12.011. PubMed DOI PMC

Sieberer BJ, Ketelaar T, Esseling JJ, Emons AM. Microtubules guide root hair tip growth. New Phytol. 2005;167:711–719. doi: 10.1111/j.1469-8137.2005.01506.x. PubMed DOI

Bao Y, Kost B, Chua NH. Reduced expression of alpha-tubulin genes in Arabidopsis thaliana specifically affects root growth and morphology, root hair development and root gravitropism. Plant J. 2001;28:145–157. doi: 10.1046/j.1365-313X.2001.01142.x. PubMed DOI

Potocky M, Elias M, Profotova B, Novotna Z, Valentova O, Zarsky V. Phosphatidic acid produced by phospholipase D is required for tobacco pollen tube growth. Planta. 2003;217:122–130. PubMed

Bibikova TN, Blancaflor EB, Gilroy S. Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J. 1999;17:657–665. doi: 10.1046/j.1365-313X.1999.00415.x. PubMed DOI

Cai G, Faleri C, Del Casino C, Emons AM, Cresti M. Distribution of callose synthase, cellulose synthase, and sucrose synthase in tobacco pollen tube is controlled in dissimilar ways by actin filaments and microtubules. Plant Physiol. 2011;155:1169–1190. doi: 10.1104/pp.110.171371. PubMed DOI PMC

Wu G, Gu Y, Li S, Yang Z. A genome-wide analysis of Arabidopsis Rop-interactive CRIB motif-containing proteins that act as Rop GTPase targets. Plant Cell. 2001;13:2841–2856. PubMed PMC

Fu Y, Gu Y, Zheng Z, Wasteneys G, Yang Z. Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell. 2005;120:687–700. doi: 10.1016/j.cell.2004.12.026. PubMed DOI

Novick P, Medkova M, Dong G, Hutagalung A, Reinisch K, Grosshans B. Interactions between Rabs, tethers, SNAREs and their regulators in exocytosis. Biochem Soc Trans. 2006;34:683–686. doi: 10.1042/BST0340683. PubMed DOI

Wu H, Rossi G, Brennwald P. The ghost in the machine: small GTPases as spatial regulators of exocytosis. Trends Cell Biol. 2008;18:397–404. doi: 10.1016/j.tcb.2008.06.007. PubMed DOI PMC

Koumandou VL, Dacks JB, Coulson RM, Field MC. Control systems for membrane fusion in the ancestral eukaryote; evolution of tethering complexes and SM proteins. BMC Evol Biol. 2007;7:29. doi: 10.1186/1471-2148-7-29. PubMed DOI PMC

Synek L, Schlager N, Elias M, Quentin M, Hauser MT, Zarsky V. AtEXO70A1, a member of a family of putative exocyst subunits specifically expanded in land plants, is important for polar growth and plant development. Plant J. 2006;48:54–72. doi: 10.1111/j.1365-313X.2006.02854.x. PubMed DOI PMC

Zarsky V, Cvrckova F, Potocky M, Hala M. Exocytosis and cell polarity in plants - exocyst and recycling domains. New Phytol. 2009;183:255–272. doi: 10.1111/j.1469-8137.2009.02880.x. PubMed DOI

Cvrckova F, Grunt M, Bezvoda R, Hala M, Kulich I, Rawat A, Zarsky V. Evolution of the land plant exocyst complexes. Front Plant Sci. 2012;3:159. PubMed PMC

Liu J, Yue P, Artym VV, Mueller SC, Guo W. The role of the exocyst in matrix metalloproteinase secretion and actin dynamics during tumor cell invadopodia formation. Mol Biol Cell. 2009;20:3763–3771. doi: 10.1091/mbc.E08-09-0967. PubMed DOI PMC

Lalli G. RalA and the exocyst complex influence neuronal polarity through PAR-3 and aPKC. J Cell Sci. 2009;122:1499–1506. doi: 10.1242/jcs.044339. PubMed DOI

Lalli G, Hall A. Ral GTPases regulate neurite branching through GAP-43 and the exocyst complex. J Cell Biol. 2005;171:857–869. doi: 10.1083/jcb.200507061. PubMed DOI PMC

Cole RA, Synek L, Zarsky V, Fowler JE. SEC8, a subunit of the putative Arabidopsis exocyst complex, facilitates pollen germination and competitive pollen tube growth. Plant Physiol. 2005;138:2005–2018. doi: 10.1104/pp.105.062273. PubMed DOI PMC

Hala M, Cole R, Synek L, Drdova E, Pecenkova T, Nordheim A, Lamkemeyer T, Madlung J, Hochholdinger F, Fowler JE. An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell. 2008;20:1330–1345. doi: 10.1105/tpc.108.059105. PubMed DOI PMC

Geitmann A, Dumais J. Not-so-tip-growth. Plant Signal Behav. 2009;4:136–138. doi: 10.4161/psb.4.2.7633. PubMed DOI PMC

Zuo X, Zhang J, Zhang Y, Hsu SC, Zhou D, Guo W. Exo70 interacts with the Arp2/3 complex and regulates cell migration. Nat Cell Biol. 2006;8:1383–1388. doi: 10.1038/ncb1505. PubMed DOI

Wang S, Liu Y, Adamson CL, Valdez G, Guo W, Hsu SC. The mammalian exocyst, a complex required for exocytosis, inhibits tubulin polymerization. J Biol Chem. 2004;279:35958–35966. doi: 10.1074/jbc.M313778200. PubMed DOI

Noritake J, Watanabe T, Sato K, Wang S, Kaibuchi K. IQGAP1: a key regulator of adhesion and migration. J Cell Sci. 2005;118:2085–2092. doi: 10.1242/jcs.02379. PubMed DOI

Jadeski L, Mataraza JM, Jeong HW, Li Z, Sacks DB. IQGAP1 stimulates proliferation and enhances tumorigenesis of human breast epithelial cells. J Biol Chem. 2008;283:1008–1017. doi: 10.1074/jbc.M708466200. PubMed DOI

Dupraz S, Grassi D, Bernis ME, Sosa L, Bisbal M, Gastaldi L, Jausoro I, Caceres A, Pfenninger KH, Quiroga S. The TC10-Exo70 complex is essential for membrane expansion and axonal specification in developing neurons. J Neurosci. 2009;29:13292–13301. doi: 10.1523/JNEUROSCI.3907-09.2009. PubMed DOI PMC

Sosa L, Dupraz S, Laurino L, Bollati F, Bisbal M, Caceres A, Pfenninger KH, Quiroga S. IGF-1 receptor is essential for the establishment of hippocampal neuronal polarity. Nat Neurosci. 2006;9:993–995. doi: 10.1038/nn1742. PubMed DOI

Lavy M, Bloch D, Hazak O, Gutman I, Poraty L, Sorek N, Sternberg H, Yalovsky S. A Novel ROP/RAC effector links cell polarity, root-meristem maintenance, and vesicle trafficking. Curr Biol. 2007;17:947–952. doi: 10.1016/j.cub.2007.04.038. PubMed DOI

Li S, Gu Y, Yan A, Lord E, Yang ZB. RIP1 (ROP Interactive Partner 1)/ICR1 marks pollen germination sites and may act in the ROP1 pathway in the control of polarized pollen growth. Mol Plant. 2008;1:1021–1035. doi: 10.1093/mp/ssn051. PubMed DOI PMC

Das A, Guo W. Rabs and the exocyst in ciliogenesis, tubulogenesis and beyond. Trends Cell Biol. 2011;21:383–386. doi: 10.1016/j.tcb.2011.03.006. PubMed DOI PMC

Caldieri G, Giacchetti G, Beznoussenko G, Attanasio F, Ayala I, Buccione R. Invadopodia biogenesis is regulated by caveolin-mediated modulation of membrane cholesterol levels. J Cell Mol Med. 2009;13:1728–1740. doi: 10.1111/j.1582-4934.2008.00568.x. PubMed DOI PMC

Yamaguchi H, Takeo Y, Yoshida S, Kouchi Z, Nakamura Y, Fukami K. Lipid rafts and caveolin-1 are required for invadopodia formation and extracellular matrix degradation by human breast cancer cells. Cancer Res. 2009;69:8594–8602. doi: 10.1158/0008-5472.CAN-09-2305. PubMed DOI

Harel R, Futerman AH. Inhibition of sphingolipid synthesis affects axonal outgrowth in cultured hippocampal neurons. J Biol Chem. 1993;268:14476–14481. PubMed

Schwarz A, Rapaport E, Hirschberg K, Futerman AH. A regulatory role for sphingolipids in neuronal growth. Inhibition of sphingolipid synthesis and degradation have opposite effects on axonal branching. J Biol Chem. 1995;270:10990–10998. doi: 10.1074/jbc.270.18.10990. PubMed DOI

Pfrieger FW. Outsourcing in the brain: do neurons depend on cholesterol delivery by astrocytes? Bioessays. 2003;25:72–78. doi: 10.1002/bies.10195. PubMed DOI

Spor TC, Dezonne RS, Rehen SK, Gomes FC. Astrocytes treated by lysophosphatidic acid induce axonal outgrowth of cortical progenitors through extracellular matrix protein and epidermal growth factor signaling pathway. J Neurochem. 2011;119:113–123. doi: 10.1111/j.1471-4159.2011.07421.x. PubMed DOI

Ovecka M, Berson T, Beck M, Derksen J, Samaj J, Baluska F, Lichtscheidl IK. Structural sterols are involved in both the initiation and tip growth of root hairs in Arabidopsis thaliana. Plant Cell. 2010;22:2999–3019. doi: 10.1105/tpc.109.069880. PubMed DOI PMC

Liu P, Li RL, Zhang L, Wang QL, Niehaus K, Baluska F, Samaj J, Lin JX. Lipid microdomain polarization is required for NADPH oxidase-dependent ROS signaling in Picea meyeri pollen tube tip growth. Plant J. 2009;60:303–313. doi: 10.1111/j.1365-313X.2009.03955.x. PubMed DOI

Boutte Y, Grebe M. Cellular processes relying on sterol function in plants. Curr Opin Plant Biol. 2009;12:705–713. doi: 10.1016/j.pbi.2009.09.013. PubMed DOI

Balasubramanian N, Scott DW, Castle JD, Casanova JE, Schwartz MA. Arf6 and microtubules in adhesion-dependent trafficking of lipid rafts. Nat Cell Biol. 2007;9:1381–1391. doi: 10.1038/ncb1657. PubMed DOI PMC

Hanzal-Bayer MF, Hancock JF. Lipid rafts and membrane traffic. FEBS Lett. 2007;581:2098–2104. doi: 10.1016/j.febslet.2007.03.019. PubMed DOI

Leitinger B, Hogg N. The involvement of lipid rafts in the regulation of integrin function. J Cell Sci. 2002;115:963–972. PubMed

Mazzone M, Baldassarre M, Beznoussenko G, Giacchetti G, Cao J, Zucker S, Luini A, Buccione R. Intracellular processing and activation of membrane type 1 matrix metalloprotease depends on its partitioning into lipid domains. J Cell Sci. 2004;117:6275–6287. doi: 10.1242/jcs.01563. PubMed DOI

Otsuki M, Itoh T, Takenawa T. Neural Wiskott-Aldrich syndrome protein is recruited to rafts and associates with endophilin A in response to epidermal growth factor. J Biol Chem. 2003;278:6461–6469. doi: 10.1074/jbc.M207433200. PubMed DOI

Lingwood D, Simons K. Lipid rafts as a membrane-organizing principle. Science. 2010;327:46–50. doi: 10.1126/science.1174621. PubMed DOI

Ko M, Zou K, Minagawa H, Yu W, Gong JS, Yanagisawa K, Michikawa M. Cholesterol-mediated neurite outgrowth is differently regulated between cortical and hippocampal neurons. J Biol Chem. 2005;280:42759–42765. doi: 10.1074/jbc.M509164200. PubMed DOI

Meriane M, Tcherkezian J, Webber CA, Danek EI, Triki I, McFarlane S, Bloch-Gallego E, Lamarche-Vane N. Phosphorylation of DCC by Fyn mediates Netrin-1 signaling in growth cone guidance. J Cell Biol. 2004;167:687–698. doi: 10.1083/jcb.200405053. PubMed DOI PMC

Pooler AM, Xi SC, Wurtman RJ. The 3-hydroxy-3-methylglutaryl co-enzyme A reductase inhibitor pravastatin enhances neurite outgrowth in hippocampal neurons. J Neurochem. 2006;97:716–723. doi: 10.1111/j.1471-4159.2006.03763.x. PubMed DOI

Niethammer P, Delling M, Sytnyk V, Dityatev A, Fukami K, Schachner M. Cosignaling of NCAM via lipid rafts and the FGF receptor is required for neuritogenesis. J Cell Biol. 2002;157:521–532. doi: 10.1083/jcb.200109059. PubMed DOI PMC

Shapiro L, Love J, Colman DR. Adhesion molecules in the nervous system: structural insights into function and diversity. Annu Rev Neurosci. 2007;30:451–474. doi: 10.1146/annurev.neuro.29.051605.113034. PubMed DOI

Gupta N, Wollscheid B, Watts JD, Scheer B, Aebersold R, DeFranco AL. Quantitative proteomic analysis of B cell lipid rafts reveals that ezrin regulates antigen receptor-mediated lipid raft dynamics. Nat Immunol. 2006;7:625–633. PubMed

Xu X, Warrington AE, Wright BR, Bieber AJ, Van KV, Pease LR, Rodriguez M. A human IgM signals axon outgrowth: coupling lipid raft to microtubules. J Neurochem. 2011;119:100–112. doi: 10.1111/j.1471-4159.2011.07416.x. PubMed DOI PMC

Morel J, Claverol S, Mongrand S, Furt F, Fromentin J, Bessoule JJ, Blein JP, Simon-Plas F. Proteomics of plant detergent-resistant membranes. Mol Cell Proteomics. 2006;5:1396–1411. doi: 10.1074/mcp.M600044-MCP200. PubMed DOI

Simon-Plas F, Perraki A, Bayer E, Gerbeau-Pissot P, Mongrand S. An update on plant membrane rafts. Curr Opin Plant Biol. 2011;14:642–649. doi: 10.1016/j.pbi.2011.08.003. PubMed DOI

Sorek N, Segev O, Gutman O, Bar E, Richter S, Poraty L, Hirsch JA, Henis YI, Lewinsohn E, Jurgens G. An S-acylation switch of conserved G domain cysteines is required for polarity signaling by ROP GTPases. Curr Biol. 2010;20:914–920. doi: 10.1016/j.cub.2010.03.057. PubMed DOI

del Pozo MA, Alderson NB, Kiosses WB, Chiang HH, Anderson RG, Schwartz MA. Integrins regulate Rac targeting by internalization of membrane domains. Science. 2004;303:839–842. doi: 10.1126/science.1092571. PubMed DOI

Golub T, Caroni P. PI(4,5)P2-dependent microdomain assemblies capture microtubules to promote and control leading edge motility. J Cell Biol. 2005;169:151–165. doi: 10.1083/jcb.200407058. PubMed DOI PMC

Yakir-Tamang L, Gerst JE. Phosphoinositides, exocytosis and polarity in yeast: all about actin? Trends Cell Biol. 2009;19:677–684. doi: 10.1016/j.tcb.2009.09.004. PubMed DOI

Pike LJ, Miller JM. Cholesterol depletion delocalizes phosphatidylinositol bisphosphate and inhibits hormone-stimulated phosphatidylinositol turnover. J Biol Chem. 1998;273:22298–22304. doi: 10.1074/jbc.273.35.22298. PubMed DOI

Caroni P. New EMBO members’ review: actin cytoskeleton regulation through modulation of PI(4,5)P(2) rafts. EMBO J. 2001;20:4332–4336. doi: 10.1093/emboj/20.16.4332. PubMed DOI PMC

Yamaguchi H, Yoshida S, Muroi E, Kawamura M, Kouchi Z, Nakamura Y, Sakai R, Fukami K. Phosphatidylinositol 4,5-bisphosphate and PIP5-kinase Ialpha are required for invadopodia formation in human breast cancer cells. Cancer Sci. 2010;101:1632–1638. doi: 10.1111/j.1349-7006.2010.01574.x. PubMed DOI PMC

Yamaguchi H, Yoshida S, Muroi E, Yoshida N, Kawamura M, Kouchi Z, Nakamura Y, Sakai R, Fukami K. Phosphoinositide 3-kinase signaling pathway mediated by p110alpha regulates invadopodia formation. J Cell Biol. 2011;193:1275–1288. doi: 10.1083/jcb.201009126. PubMed DOI PMC

Thapa N, Sun Y, Schramp M, Choi S, Ling K, Anderson RA. Phosphoinositide signaling regulates the exocyst complex and polarized integrin trafficking in directionally migrating cells. Dev Cell. 2012;22:116–130. doi: 10.1016/j.devcel.2011.10.030. PubMed DOI PMC

Koh CG. Rho GTPases and their regulators in neuronal functions and development. Neurosignals. 2006;15:228–237. doi: 10.1159/000101527. PubMed DOI

Kouchi Z, Igarashi T, Shibayama N, Inanobe S, Sakurai K, Yamaguchi H, Fukuda T, Yanagi S, Nakamura Y, Fukami K. Phospholipase Cdelta3 regulates RhoA/Rho kinase signaling and neurite outgrowth. J Biol Chem. 2011;286:8459–8471. doi: 10.1074/jbc.M110.171223. PubMed DOI PMC

Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua NH. Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol. 1999;145:317–330. doi: 10.1083/jcb.145.2.317. PubMed DOI PMC

Ischebeck T, Vu LH, Jin X, Stenzel I, Lofke C, Heilmann I. Functional cooperativity of enzymes of phosphoinositide conversion according to synergistic effects on pectin secretion in tobacco pollen tubes. Mol Plant. 2010;3:870–881. doi: 10.1093/mp/ssq031. PubMed DOI

Ischebeck T, Stenzel I, Hempel F, Jin X, Mosblech A, Heilmann I. Phosphatidylinositol-4,5-bisphosphate influences Nt-Rac5-mediated cell expansion in pollen tubes of Nicotiana tabacum. Plant J. 2011;65:453–468. doi: 10.1111/j.1365-313X.2010.04435.x. PubMed DOI

Xu N, Gao XQ, Zhao XY, Zhu DZ, Zhou LZ, Zhang XS. Arabidopsis AtVPS15 is essential for pollen development and germination through modulating phosphatidylinositol 3-phosphate formation. Plant Mol Biol. 2011;77:251–260. doi: 10.1007/s11103-011-9806-9. PubMed DOI PMC

Preuss ML, Schmitz AJ, Thole JM, Bonner HK, Otegui MS, Nielsen E. A role for the RabA4b effector protein PI-4Kbeta1 in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol. 2006;172:991–998. doi: 10.1083/jcb.200508116. PubMed DOI PMC

Camacho L, Smertenko AP, Perez-Gomez J, Hussey PJ, Moore I. Arabidopsis Rab-E GTPases exhibit a novel interaction with a plasma-membrane phosphatidylinositol-4-phosphate 5-kinase. J Cell Sci. 2009;122:4383–4392. doi: 10.1242/jcs.053488. PubMed DOI

Pleskot R, Pejchar P, Bezvoda R, Lichtscheidl IK, Wolters-Arts M, Marc J, Zarsky V, Potocky M. Turnover of Phosphatidic Acid through Distinct Signaling Pathways Affects Multiple Aspects of Pollen Tube Growth in Tobacco. Front Plant Sci. 2012;3:54. PubMed PMC

Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev. 2007;87:245–313. doi: 10.1152/physrev.00044.2005. PubMed DOI

Diaz B, Shani G, Pass I, Anderson D, Quintavalle M, Courtneidge SA. Tks5-dependent, nox-mediated generation of reactive oxygen species is necessary for invadopodia formation. Sci Signal. 2009;2:ra53. doi: 10.1126/scisignal.2000368. PubMed DOI PMC

Gianni D, Diaz B, Taulet N, Fowler B, Courtneidge SA, Bokoch GM. Novel p47(phox)-related organizers regulate localized NADPH oxidase 1 (Nox1) activity. Sci Signal. 2009;2:ra54. doi: 10.1126/scisignal.2000370. PubMed DOI PMC

Tsatmali M, Walcott EC, Crossin KL. Newborn neurons acquire high levels of reactive oxygen species and increased mitochondrial proteins upon differentiation from progenitors. Brain Res. 2005;1040:137–150. doi: 10.1016/j.brainres.2005.01.087. PubMed DOI

Tsatmali M, Walcott EC, Makarenkova H, Crossin KL. Reactive oxygen species modulate the differentiation of neurons in clonal cortical cultures. Mol Cell Neurosci. 2006;33:345–357. doi: 10.1016/j.mcn.2006.08.005. PubMed DOI PMC

Kennedy KA, Ostrakhovitch EA, Sandiford SD, Dayarathna T, Xie X, Waese EY, Chang WY, Feng Q, Skerjanc IS, Stanford WL. Mammalian numb-interacting protein 1/dual oxidase maturation factor 1 directs neuronal fate in stem cells. J Biol Chem. 2010;285:17974–17985. doi: 10.1074/jbc.M109.084616. PubMed DOI PMC

Katoh S, Mitsui Y, Kitani K, Suzuki T. Hyperoxia induces the differentiated neuronal phenotype of PC12 cells by producing reactive oxygen species. Biochem Biophys Res Commun. 1997;241:347–351. doi: 10.1006/bbrc.1997.7514. PubMed DOI

Katoh S, Mitsui Y, Kitani K, Suzuki T. Hyperoxia induces the neuronal differentiated phenotype of PC12 cells via a sustained activity of mitogen-activated protein kinase induced by Bcl-2. Biochem J. 1999;338(Pt 2):465–470. PubMed PMC

Suzukawa K, Miura K, Mitsushita J, Resau J, Hirose K, Crystal R, Kamata T. Nerve growth factor-induced neuronal differentiation requires generation of Rac1-regulated reactive oxygen species. J Biol Chem. 2000;275:13175–13178. doi: 10.1074/jbc.275.18.13175. PubMed DOI

Kamata H, Oka S, Shibukawa Y, Kakuta J, Hirata H. Redox regulation of nerve growth factor-induced neuronal differentiation of PC12 cells through modulation of the nerve growth factor receptor, TrkA. Arch Biochem Biophys. 2005;434:16–25. doi: 10.1016/j.abb.2004.07.036. PubMed DOI

Camacho L, Malho R. Endo/exocytosis in the pollen tube apex is differentially regulated by Ca2+ and GTPases. J Exp Bot. 2003;54:83–92. doi: 10.1093/jxb/erg043. PubMed DOI

Coelho PC, Malho R. Correlative Analysis of [Ca](C) and Apical Secretion during Pollen Tube Growth and Reorientation. Plant Signal Behav. 2006;1:152–157. doi: 10.4161/psb.1.3.2999. PubMed DOI PMC

Michard E, Lima PT, Borges F, Silva AC, Portes MT, Carvalho JE, Gilliham M, Liu LH, Obermeyer G, Feijo JA. Glutamate receptor-like genes form Ca2+ channels in pollen tubes and are regulated by pistil D-serine. Science. 2011;332:434–437. doi: 10.1126/science.1201101. PubMed DOI

Bibikova TN, Zhigilei A, Gilroy S. Root hair growth in Arabidopsis thaliana is directed by calcium and an endogenous polarity. Planta. 1997;203:495–505. doi: 10.1007/s004250050219. PubMed DOI

Wymer CL, Bibikova TN, Gilroy S. Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J. 1997;12:427–439. doi: 10.1046/j.1365-313X.1997.12020427.x. PubMed DOI

Mucha E, Hoefle C, Huckelhoven R, Berken A. RIP3 and AtKinesin- Eur J Cell Biol. 2010;89:906–916. doi: 10.1016/j.ejcb.2010.08.003. PubMed DOI

Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature. 2003;422:442–446. doi: 10.1038/nature01485. PubMed DOI

Potocky M, Jones MA, Bezvoda R, Smirnoff N, Zarsky V. Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol. 2007;174:742–751. doi: 10.1111/j.1469-8137.2007.02042.x. PubMed DOI

Weaver AM. Regulation of cancer invasion by reactive oxygen species and Tks family scaffold proteins. Sci Signal. 2009;2:e56. PubMed PMC

Giannoni E, Taddei ML, Chiarugi P. Src redox regulation: again in the front line. Free Radic Biol Med. 2010;49:516–527. doi: 10.1016/j.freeradbiomed.2010.04.025. PubMed DOI

Gianni D, Bohl B, Courtneidge SA, Bokoch GM. The involvement of the tyrosine kinase c-Src in the regulation of reactive oxygen species generation mediated by NADPH oxidase-1. Mol Biol Cell. 2008;19:2984–2994. doi: 10.1091/mbc.E08-02-0138. PubMed DOI PMC

Abo A, Pick E, Hall A, Totty N, Teahan CG, Segal AW. Activation of the NADPH oxidase involves the small GTP-binding protein p21rac1. Nature. 1991;353:668–670. doi: 10.1038/353668a0. PubMed DOI

Woo CH, Lee ZW, Kim BC, Ha KS, Kim JH. Involvement of cytosolic phospholipase A2, and the subsequent release of arachidonic acid, in signalling by rac for the generation of intracellular reactive oxygen species in rat-2 fibroblasts. Biochem J. 2000;348(Pt 3):525–530. PubMed PMC

Zhou L, Too HP. Mitochondrial localized STAT3 is involved in NGF induced neurite outgrowth. PLoS One. 2011;6:e21680. doi: 10.1371/journal.pone.0021680. PubMed DOI PMC

Sagi M, Fluhr R. Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol. 2006;141:336–340. doi: 10.1104/pp.106.078089. PubMed DOI PMC

Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L. Local positive feedback regulation determines cell shape in root hair cells. Science. 2008;319:1241–1244. doi: 10.1126/science.1152505. PubMed DOI

Munnamalai V, Suter DM. Reactive oxygen species regulate F-actin dynamics in neuronal growth cones and neurite outgrowth. J Neurochem. 2009;108:644–661. doi: 10.1111/j.1471-4159.2008.05787.x. PubMed DOI PMC

Swanson S, Gilroy S. ROS in plant development. Physiol Plant. 2010;138:384–392. doi: 10.1111/j.1399-3054.2009.01313.x. PubMed DOI

Elias M, Klimes V. Rho GTPases: deciphering the evolutionary history of a complex protein family. Methods Mol Biol. 2012;827:13–34. doi: 10.1007/978-1-61779-442-1_2. PubMed DOI

Cvrckova F, Rivero F, Bavlnka B. Evolutionarily conserved modules in actin nucleation: lessons from Dictyostelium discoideum and plants. Review article. Protoplasma. 2004;224:15–31. PubMed

Rivero F, Cvrckova F. Origins and evolution of the actin cytoskeleton. Adv Exp Med Biol. 2007;607:97–110. doi: 10.1007/978-0-387-74021-8_8. PubMed DOI

Zhang Y, Franco M, Ducret A, Mignot T. A bacterial Ras-like small GTP-binding protein and its cognate GAP establish a dynamic spatial polarity axis to control directed motility. PLoS Biol. 2010;8:e1000430. doi: 10.1371/journal.pbio.1000430. PubMed DOI PMC

High-throughput transcriptomic and proteomic profiling of mesenchymal-amoeboid transition in 3D collagen

Division of Labor Between Two Actin Nucleators-the Formin FH1 and the ARP2/3 Complex-in Arabidopsis Epidermal Cell Morphogenesis

Regulation of Exocyst Function in Pollen Tube Growth by Phosphorylation of Exocyst Subunit EXO70C2

Arabidopsis Class II Formins AtFH13 and AtFH14 Can Form Heterodimers but Exhibit Distinct Patterns of Cellular Localization

Analysis of Exocyst Subunit EXO70 Family Reveals Distinct Membrane Polar Domains in Tobacco Pollen Tubes

The exocyst at the interface between cytoskeleton and membranes in eukaryotic cells

Formins and membranes: anchoring cortical actin to the cell wall and beyond

Old AIMs of the exocyst: evidence for an ancestral association of exocyst subunits with autophagy-associated Atg8 proteins