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Formin homology 2 domains occur in multiple contexts in angiosperms

. 2004 Jul 15 ; 5 (1) : 44. [epub] 20040715

Language English Country Great Britain, England Media electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

BACKGROUND: Involvement of conservative molecular modules and cellular mechanisms in the widely diversified processes of eukaryotic cell morphogenesis leads to the intriguing question: how do similar proteins contribute to dissimilar morphogenetic outputs. Formins (FH2 proteins) play a central part in the control of actin organization and dynamics, providing a good example of evolutionarily versatile use of a conserved protein domain in the context of a variety of lineage-specific structural and signalling interactions. RESULTS: In order to identify possible plant-specific sequence features within the FH2 protein family, we performed a detailed analysis of angiosperm formin-related sequences available in public databases, with particular focus on the complete Arabidopsis genome and the nearly finished rice genome sequence. This has led to revision of the current annotation of half of the 22 Arabidopsis formin-related genes. Comparative analysis of the two plant genomes revealed a good conservation of the previously described two subfamilies of plant formins (Class I and Class II), as well as several subfamilies within them that appear to predate the separation of monocot and dicot plants. Moreover, a number of plant Class II formins share an additional conserved domain, related to the protein phosphatase/tensin/auxilin fold. However, considerable inter-species variability sets limits to generalization of any functional conclusions reached on a single species such as Arabidopsis. CONCLUSIONS: The plant-specific domain context of the conserved FH2 domain, as well as plant-specific features of the domain itself, may reflect distinct functional requirements in plant cells. The variability of formin structures found in plants far exceeds that known from both fungi and metazoans, suggesting a possible contribution of FH2 proteins in the evolution of the plant type of multicellularity.

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Wallar BJ, Alberts AS. The formins: active scaffolds that remodel the cytoskeleton. Trends Cell Biol. 2003;13:435–446. doi: 10.1016/S0962-8924(03)00153-3. PubMed DOI

Deeks MJ, Hussey P, 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

Zigmond SH. Formin-induced nucleation of actin filaments. Curr Opin Cell Biol. 2004;16:99–105. doi: 10.1016/j.ceb.2003.10.019. PubMed DOI

Castrillon DH, Wasserman SA. Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the limb deformity gene. Development. 1994;120:3367–3377. PubMed

Evangelista M, Blundell K, Longtine MS, Chow CJ, Adames N, Pringle JR, Peter M, Boone C. Bni1p, a yeast formin linking Cdc42p and the actin cytoskeleton during polarized morphogenesis. Science. 1997;276:118–122. doi: 10.1126/science.276.5309.118. PubMed DOI

Fujiwara T, Tanaka K, Mino A, Kikyo M, Takahashi K, Shimizu K, Takai Y. Rho1p-Bni1p-Spa2p interactions: implication in localization of bni1p at the bud site and regulation of the actin cytoskeleton in saccharomyces cerevisiae. Mol Biol Cell. 1998;9:1221–1233. PubMed PMC

Magie CR, Meyer MR, Gorsuch MS, Parkhurst SM. Mutations in the Rho1 small GTPase disrupt morphogenesis and segmentation during early Drosophila development. Development. 1999;126:5353–5364. PubMed

Ozaki-Kuroda K, Yamamoto Y, Nohara H, Kinoshita M, Fujiwara T, Irie K, Takai Y. Dynamic localization and function of Bni1p at the sites of directed growth in Saccharomyces cerevisiae. Mol Cell Biol. 2001;21:827–839. doi: 10.1128/MCB.21.3.827-839.2001. PubMed DOI PMC

Huckaba TM, Pon LA. Cytokinesis: Rho and Formins Are the Ringleaders. Curr Biol. 2002;12:R813–R814. doi: 10.1016/S0960-9822(02)01316-7. PubMed DOI

Trumpp A, Blundell PA, de la Pompa JL, Zeller R. The chicken limb deformity gene encodes nuclear proteins expressed in specific cell types during morphogenesis. Genes Dev. 1992;6:14–28. PubMed

de la Pompa JL, James D, Zeller R. The limb deformity proteins during avian neurulation and sense organ development. Dev Dyn. 1995;204:156–167. PubMed

Petersen J, Nielsen O, Egel R, Hagan IM. FH3, a domain found in formins, targets the fission yeast formin FUS1 to the projection tip during conjugation. J Cell Biol. 1998;141:1217–1228. doi: 10.1083/jcb.141.5.1217. PubMed DOI PMC

Zeller R, Haramis AG, Zuniga A, McGuigan C, Dono R, Davidson G, Chabanis S, Gibson T. Formin defines a large family of morphoregulatory genes and functions in establishment of the polarising region. Cell Tissue Res. 1999;296:85–93. doi: 10.1007/s004410051269. PubMed DOI

Xu Y, Moseley JB, Sagot I, Poy F, Pellman D, Goode BL, Eck MJ. Crystal structures of a formin homology-2 domain reveal a tethered dimer architecture. Cell. 2004;116:711–723. doi: 10.1016/S0092-8674(04)00210-7. PubMed DOI

Shimada A, Nyitrai M, Vetter IR, Kuhlmann D, Bugyi B, Narumiya S, Geeves MA, Wittinghofer A. The core FH2 domain of diaphanous-related formins is an elongated actin binding protein that inhibits polymerization. Mol Cell. 2004;13:511–522. doi: 10.1016/S1097-2765(04)00059-0. PubMed DOI

Evangelista M, Pruyne D, Amberg DC, Boone C, Bretscher A. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat Cell Biol. 2002;4:32–41. doi: 10.1038/ncb718. PubMed DOI

Pruyne D, Evangelista M, Yang C, Bi E, Zigmond SH, Bretscher A, Boone C. Role of formins in actin assembly: nucleation and barbed-end association. Science. 2002;297:612–615. doi: 10.1126/science.1072309. PubMed DOI

Severson AF, Baillie DL, Bowerman B. A Formin Homology Protein and a Profilin Are Required for Cytokinesis and Arp2/3-Independent Assembly of Cortical Microfilaments in C. elegans. Curr Biol. 2002;12:2066–2075. doi: 10.1016/S0960-9822(02)01355-6. PubMed DOI

Li F, Higgs HN. The mouse formin mDia1 is a potent actin nucleation factor regulated by autoinhibition. Curr Biol. 2003;13:1335–1340. doi: 10.1016/S0960-9822(03)00540-2. PubMed DOI

Pring M, Evangelista M, Boone C, Yang C, Zigmond SH. Mechanism of formin-induced nucleation of actin filaments. Biochemistry. 2003;42:486–496. doi: 10.1021/bi026520j. PubMed DOI

Kovar DR, Kuhn JR, Tichy AL, Pollard TD. The fission yeast cytokinesis formin Cdc12p is a barbed end actin filament capping protein gated by profilin. J Cell Biol. 2003;161:875–887. doi: 10.1083/jcb.200211078. PubMed DOI PMC

Cvrčková F, Bavlnka B, Rivero F. Evolutionarily conserved modules in actin nucleation: lessons from Dictyostelium and plants. Protoplasma. 2004. PubMed

Alberts AS. Diaphanous-related Formin homology proteins. Curr Biol. 2002;12:R796–R796. doi: 10.1016/S0960-9822(02)01309-X. PubMed DOI

Olson MF. GTPase Signalling: New Functions for Diaphanous-Related Formins. Curr Biol. 2003;13:R360–R362. doi: 10.1016/S0960-9822(03)00277-X. PubMed DOI

Fujiwara T, Mammoto A, Kim Y, Takai Y. Rho small G-protein-dependent binding of mDia to an Src homology 3 domain-containing IRSp53/BAIAP2. Biochem Biophys Res Commun. 2000;271:626–629. doi: 10.1006/bbrc.2000.2671. PubMed DOI

Kamei T, Tanaka K, Hihara T, Umikawa M, Imamura H, Kikyo M, Ozaki K, Takai Y. Interaction of Bnr1p with a novel Src homology 3 domain-containing Hof1p. Implication in cytokinesis in Saccharomyces cerevisiae. J Biol Chem. 1998;273:28341–28345. doi: 10.1074/jbc.273.43.28341. PubMed DOI

Tominaga T, Sahai E, Chardin P, McCormick F, Courtneidge SA, Alberts A. Diaphanous-related formins bridge Rho GTPase and Src tyrosine kinase signaling. Mol Cell. 2000;5:13–25. doi: 10.1016/S1097-2765(00)80399-8. PubMed DOI

Yayoshi-Yamamoto S, Taniuchi I, Watanabe T. FRL, a novel formin-related protein, binds to Rac and regulates cell motility and survival of macrophages. Mol Cell Biol. 2000;20:6872–6881. doi: 10.1128/MCB.20.18.6872-6881.2000. PubMed DOI PMC

Chang F. Movement of a cytokinesis factor cdc12p to the site of cell division. Curr Biol. 1999;9:849–852. doi: 10.1016/S0960-9822(99)80372-8. PubMed DOI

Ishizaki T, Morishima Y, Okamoto M, Furuyashiki T, Kato T, Narumiya S. Coordination of microtubules and the actin cytoskeleton by the effector mDia1. Nat Cell Biol. 2001;3:8–14. doi: 10.1038/35050598. PubMed DOI

Kato T, Watanabe T, Morishima Y, Fujita A, Ishizaki T, Narumiya S. Localization of a mammalian homolog of Diaphanous, mDia1, to the mitotic spindle in HeLa cells. J Cell Sci. 2001;114:775–784. PubMed

Banno H, Chua NH. Characterization of the arabidopsis formin-like protein AFH1 and its interacting protein. Plant Cell Physiol. 2000;41:617–626. PubMed

Cvrčková F. Are plant formins integral membrane proteins? Genome Biology. 2000;1:research001. PubMed PMC

Cheung AY, Wu H.-m. 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

Craigon DJ, James N, Okyere J, Higgins J, Jotham J, May S. NASCArrays: a repository for microarray data generated by NASC's transcriptomics service. Nucleic Acids Res. 2004;32 Database issue:D575–D577. doi: 10.1093/nar/gkh133. Database issue. PubMed DOI PMC

Haas BJ, Volfovsky N, Town CD, Troukhan M, Alexandrov N, Feldmann KA, Flavell RB, White O, Salzberg SL. Full-length messenger RNA sequences greatly improve genome annotation. Genome Biol. 2002;3:research0029. doi: 10.1186/gb-2002-3-6-research0029. PubMed DOI PMC

Haas BJ, Delcher AL, Mount SM, Wortman JR, Smith R.K.Jr., Hannick LI, Maiti R, Ronning CM, Rusch DB, Town CD, Salzberg SL, White O. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res. 2003;31:5654–5666. doi: 10.1093/nar/gkg770. PubMed DOI PMC

Eliáš M, Potocký M, Cvrčková F, Zárský V. Molecular diversity of phospholipase D in angiosperms. BMC Genomics. 2002;3:2. doi: 10.1186/1471-2164-3-2. PubMed DOI PMC

Deutsch M, Long M. Intron-exon structures of eukaryotic model organisms. Nucleic Acids Res. 1999;27:3219–3228. doi: 10.1093/nar/27.15.3219. PubMed DOI PMC

Wang CC, Chan DC, Leder P. The mouse formin (Fmn) gene: genomic structure, novel exons, and genetic mapping. Genomics. 1997;39:303–311. doi: 10.1006/geno.1996.4519. PubMed DOI

Honys D, Twell D. Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol. 2003;132:640–652. doi: 10.1104/pp.103.020925. PubMed DOI PMC

Kikuchi S, Satoh K, Nagata T, Kawagashira N, Doi K, Kishimoto N, Yazaki J, Ishikawa M, Yamada H, Ooka H, Hotta I, Kojima K, Namiki T, Ohneda E, Yahagi W, Suzuki K, Ohtsuki K, Shishiki T, Otomo Y, Murakami K. Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science. 2003;301:376–379. doi: 10.1126/science.1081288. PubMed DOI

Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetictrees. Mol Biol Evol. 1987;4:406–425. PubMed

Schultz J, Milpetz F, Bork P, Ponting C. SMART, a simple modular architecture research tool: Identification of signalling domains. Proc Natl Acad Sci U S A. 1998;95:5857–5864. doi: 10.1073/pnas.95.11.5857. PubMed DOI PMC

Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database searchprograms. Nucleic Acids Res. 1997;25:3389–3402. doi: 10.1093/nar/25.17.3389. PubMed DOI PMC

Kelley LA, MacCallum RM, Sternberg MJE. Enhanced Genome Annotation using Structural Profiles in the Program 3D-PSSM. J Mol Biol. 2000;299:499–520. doi: 10.1006/jmbi.2000.3741. PubMed DOI

Shi J, Blundell T, Mizuguchi K. FUGUE: Sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J Mol Biol. 2001;310:243–257. doi: 10.1006/jmbi.2001.4762. PubMed DOI

Karplus K, Hu B. Evaluation of protein multiple alignments by SAM-T99 using the BAliBASE multiple alignment test set. Bioinformatics. 2001;17:713–720. doi: 10.1093/bioinformatics/17.8.713. PubMed DOI

Jones DT. Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol. 1999;292:195–202. doi: 10.1006/jmbi.1999.3091. PubMed DOI

Li J, Yen C, Liaw D, Podsypanina K, Bose S, Wang SI, Puc J, Miliaresis C, Rodgers L, McCombie R, Bigner SH, Giovanella BC, Ittmann M, Tycko B, Hibshoosh H, Wigler MH, Parsons R. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science. 1997;275:1943–1946. doi: 10.1126/science.275.5308.1943. PubMed DOI

Steck PA, Pershouse MA, Jasser SA, Yung WKA, Lin H, Ligon AH, Langford LA, Baumgard ML, Hattier T, Davis T, Frye C, Hu R, Swedlund B, Teng DHF, Tavtigian SV. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nature Genetics. 1997;15:356–362. PubMed

Li L, Ernsting BR, Wishart MJ, Lohse DL, Dixon JE. A family of putative tumor suppressors is structurally and functionally conserved in humans and yeast. J Biol Chem. 1997;272:29403–29406. doi: 10.1074/jbc.272.47.29403. PubMed DOI

Yamada KM, Araki M. Tumor suppressor PTEN: modulator of cell signaling, growth, migration and apoptosis. J Cell Sci. 2001;114:2375–2382. PubMed

Lo SH. Molecules in focus: tensin. Int J Biochem Cell Biol. 2004;36:31–34. doi: 10.1016/S1357-2725(03)00171-7. PubMed DOI

Lemmon SK. Clathrin uncoating: auxilin comes to life. Curr Biol. 2001;11:R49–R52. doi: 10.1016/S0960-9822(01)00010-0. PubMed DOI

Lo SH, Janmey PA, Hartwig JH, Chen LB. Interactions of tensin with actin and identification of its three distinct actin-binding domains. J Cell Biol. 1994;125:1067–1075. doi: 10.1083/jcb.125.5.1067. PubMed DOI PMC

Tamura M, Gu J, Matsumoto K, Aota S, Parsons R, Yamada KM. Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN. Science. 1998;280:1614–1617. doi: 10.1126/science.280.5369.1614. PubMed DOI

Barford D, Flint AJ, Tonks NK. Crystal structure of human protein tyrosine phosphatase 1B. Science. 1994;263:1397–1404. PubMed

Stuckey JA, Schubert HL, Fauman EB, Zhang ZY, Dixon JE, Saper MA. Crystal structure of Yersinia protein tyrosine phosphatase at 2.5 A and the complex with tungstate. Nature. 1994;370:571–575. doi: 10.1038/370571a0. PubMed DOI

Jia Z, Barford D, Flint AJ, Tonks NK. Structural basis for phosphotyrosine peptide recognition by protein tyrosine phosphatase 1B. Science. 1995;268:1754–1758. PubMed

Murray D, Honig B. Electrostatic control of the membrane targeting of C2 domains. Mol Cell. 2002;9:145–154. doi: 10.1016/S1097-2765(01)00426-9. PubMed DOI

Lee JO, Yang H, Georgescu MM, Di Cristofano A, Maehama T, Shi Y, Dixon JE, Pandolfi P, Pavletich NP. Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association. Cell. 1999;99:323–334. doi: 10.1016/S0092-8674(00)81663-3. PubMed DOI

Raftopoulou M, Etienne-Manneville S, Self A, Nicholls S, Hall A. Regulation of cell migration by the C2 domain of the tumor suppressor PTEN. Science. 2004;303:1179–1181. doi: 10.1126/science.1092089. PubMed DOI

Gish W, States DJ. Identification of protein coding regions by database similarity search. Nature Genetics. 1993;3:266–272. PubMed

Schuler GD, Altschul SF, Lipman DJ. A workbench for multiple alignment construction analysis. Proteins. 1991;9:180–190. PubMed

Burge C, Karlin S. Prediction of complete gene structures in human genomic DNA. J Mol Biol. 1997;268:78–94. doi: 10.1006/jmbi.1997.0951. PubMed DOI

Burge C. Modeling dependencies in pre-mRNA splicing signals. In: SalzbergS, SearlsD and KasifS, editor. Computational Methods in Molecular Biology. Amsterdam, Elsevier Science; 1998. pp. 127–163.

Milanesi L, D'Angelo D, Rogozin IB. GeneBuilder: interactive in silico prediction of genes structure. Bioinformatics. 1999;15:612–621. doi: 10.1093/bioinformatics/15.7.612. PubMed DOI

Zhang MQ. Identification of protein coding regions in the human genome by quadratic discriminant analysis. Proc Natl Acad Sci U S A. 1997;94:565–568. doi: 10.1073/pnas.94.2.565. PubMed DOI PMC

Stothard P. The Sequence Manipulation Suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques. 2000;28:1102–1104. PubMed

The Sequence Manipulation Suite 2. 2004.

Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673–4680. PubMed PMC

Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser. 1999;41:95–98.

Van de Peer Y, De Wachter R. TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci. 1994;10:569–570. PubMed

Letunic I, Goodstadt L, Dickens NJ, Doerks T, Schultz J, Mott R, Ciccarelli F, Copley RR, Ponting C, Bork P. Recent improvements to the SMART domain-based sequence annotation resource. Nucleic Acids Res. 2002;30:242–244. doi: 10.1093/nar/30.1.242. PubMed DOI PMC

Nielsen H, Krogh A. Proceedings of the Sixth International Conference on Intelligent Systems for Molecular Biology (ISMB 6) Menlo Park, California, AAAI Press; 1998. Prediction of signal peptides and signal anchors by a hidden Markov model; pp. 122–130. PubMed

Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305:567–580. doi: 10.1006/jmbi.2000.4315. PubMed DOI

FUGUE:Sequence-structure homology recognition and alignment engine. 2004.

UCSC HMM Applications. 2004.

McGuffin LJ, Jones DT, Bryson K. The PSIPRED protein structure prediction server. Bioinformatics. 2000;16:404–405. doi: 10.1093/bioinformatics/16.4.404. PubMed DOI

Vriend G. WHAT IF: a molecular modeling and drug design program. J Mol Graph. 1990;8:52–56. doi: 10.1016/0263-7855(90)80070-V. PubMed DOI

Chinea G, Padron G, Hooft RW, Sander C, Vriend G. The use of position-specific rotamers in model building by homology. Proteins. 1995;23:415–421. PubMed

Guex N, Peitsch MC. SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling. Electrophoresis. 1997;18:2714–2723. PubMed

Deep View Swiss-PdbViewer. 2004.

POV-Ray - the Persistence of Vision Raytracer. 2004.

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