The emerging role of microtubules in invasion plasticity
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články, přehledy
PubMed
36860323
PubMed Central
PMC9969133
DOI
10.3389/fonc.2023.1118171
Knihovny.cz E-zdroje
- Klíčová slova
- 3D migration, amoeboid, cancer, invasion plasticity, mesenchymal, microtubules,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
The ability of cells to switch between different invasive modes during metastasis, also known as invasion plasticity, is an important characteristic of tumor cells that makes them able to resist treatment targeted to a particular invasion mode. Due to the rapid changes in cell morphology during the transition between mesenchymal and amoeboid invasion, it is evident that this process requires remodeling of the cytoskeleton. Although the role of the actin cytoskeleton in cell invasion and plasticity is already quite well described, the contribution of microtubules is not yet fully clarified. It is not easy to infer whether destabilization of microtubules leads to higher invasiveness or the opposite since the complex microtubular network acts differently in diverse invasive modes. While mesenchymal migration typically requires microtubules at the leading edge of migrating cells to stabilize protrusions and form adhesive structures, amoeboid invasion is possible even in the absence of long, stable microtubules, albeit there are also cases of amoeboid cells where microtubules contribute to effective migration. Moreover, complex crosstalk of microtubules with other cytoskeletal networks participates in invasion regulation. Altogether, microtubules play an important role in tumor cell plasticity and can be therefore targeted to affect not only cell proliferation but also invasive properties of migrating cells.
Zobrazit více v PubMed
Alexandrova AY, Chikina AS, Svitkina TM. Actin cytoskeleton in mesenchymal-to-amoeboid transition of cancer cells. In: International review of cell and molecular biology. Elsevier; (2020). p. 197–256. Available at: https://linkinghub.elsevier.com/retrieve/pii/S1937644820300782. PubMed PMC
Fife CM, McCarroll JA, Kavallaris M. Movers and shakers: cell cytoskeleton in cancer metastasis: Cytoskeleton and cancer metastasis. Br J Pharmacol (2014) 171(24):5507–23. doi: 10.1111/bph.12704 PubMed DOI PMC
Gandalovičová A, Vomastek T, Rosel D, Brábek J. Cell polarity signaling in the plasticity of cancer cell invasiveness. Oncotarget (2016) 7(18):25022–49. doi: 10.18632/oncotarget.7214 PubMed DOI PMC
Strouhalova K, Přechová M, Gandalovičová A, Brábek J, Gregor M, Rosel D. Vimentin intermediate filaments as potential target for cancer treatment. Cancers (2020) 12(1):184. doi: 10.3390/cancers12010184 PubMed DOI PMC
Paňková K, Rösel D, Novotný M, Brábek J. The molecular mechanisms of transition between mesenchymal and amoeboid invasiveness in tumor cells. Cell Mol Life Sci (2010) 67(1):63–71. doi: 10.1007/s00018-009-0132-1 PubMed DOI PMC
te Boekhorst V, Friedl P. Plasticity of cancer cell invasion–mechanisms and implications for therapy. In: Advances in cancer research. Elsevier; (2016). p. 209–64. Available at: https://linkinghub.elsevier.com/retrieve/pii/S0065230X16300562. PubMed
Tolde O, Gandalovičová A, Křížová A, Veselý P, Chmelík R, Rosel D, et al. . Quantitative phase imaging unravels new insight into dynamics of mesenchymal and amoeboid cancer cell invasion. Sci Rep (2018) 8(1):12020. doi: 10.1038/s41598-018-30408-7 PubMed DOI PMC
Norman LL, Brugés J, Sengupta K, Sens P, Aranda-Espinoza H. Cell blebbing and membrane area homeostasis in spreading and retracting cells. Biophys J (2010) 99(6):1726–33. doi: 10.1016/j.bpj.2010.07.031 PubMed DOI PMC
Schick J, Raz E. Blebs–formation, regulation, positioning, and role in amoeboid cell migration. Front Cell Dev Biol (2022) 10:926394. doi: 10.3389/fcell.2022.926394 PubMed DOI PMC
Raftopoulou M, Hall A. Cell migration: Rho GTPases lead the way. Dev Biol (2004) 265(1):23–32. doi: 10.1016/j.ydbio.2003.06.003 PubMed DOI
Eden S, Rohatgi R, Podtelejnikov AV, Mann M, Kirschner MW. Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and nck. Nature (2002) 418(6899):790–3. doi: 10.1038/nature00859 PubMed DOI
Rohatgi R, Ho H yi H, Kirschner MW. Mechanism of n-wasp activation by Cdc42 and phosphatidylinositol 4,5-bisphosphate. J Cell Biol (2000) 150(6):1299–310. doi: 10.1083/jcb.150.6.1299 PubMed DOI PMC
Weaver AM, Young ME, Lee WL, Cooper JA. Integration of signals to the Arp2/3 complex. Curr Opin Cell Biol (2003) 15(1):23–30. doi: 10.1016/S0955-0674(02)00015-7 PubMed DOI
Kraynov VS, Chamberlain C, Bokoch GM, Schwartz MA, Slabaugh S, Hahn KM. Localized rac activation dynamics visualized in living cells. Science (2000) 290(5490):333–7. doi: 10.1126/science.290.5490.333 PubMed DOI
Alblas J, Ulfman L, Hordijk P, Koenderman L. Activation of RhoA and ROCK are essential for detachment of migrating Leukocytes Mol Biol Cell (2001) 12:9. doi: 10.1091/mbc.12.7.2137 PubMed DOI PMC
Amano M, Ito M, Kimura K, Fukata Y, Chihara K, Nakano T, et al. . Phosphorylation and activation of myosin by rho-associated kinase (Rho-kinase). J Biol Chem (1996) 271(34):20246–9. doi: 10.1074/jbc.271.34.20246 PubMed DOI
Kimura K, Ito M, Amano M, Chihara K, Fukata Y, Nakafuku M, et al. . Regulation of myosin phosphatase by rho and rho-associated kinase (Rho-kinase). Science. (1996) 273(5272):245–8. doi: 10.1126/science.273.5272.245 PubMed DOI
Maekawa M, Ishizaki T, Boku S, Watanabe N, Fujita A, Iwamatsu A, et al. . Signaling from rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science (1999) 285(5429):895–8. doi: 10.1126/science.285.5429.895 PubMed DOI
Kosla J, Paňková D, Plachý J, Tolde O, Bicanová K, Dvořák M, et al. . Metastasis of aggressive amoeboid sarcoma cells is dependent on Rho/ROCK/MLC signaling. Cell Commun Signal (2013) 11(1):51. doi: 10.1186/1478-811X-11-51 PubMed DOI PMC
Orgaz JL, Herraiz C, Sanz-Moreno V. Rho GTPases modulate malignant transformation of tumor cells. Small GTPases (2014) 5(4):e983867. doi: 10.4161/sgtp.29019 PubMed DOI PMC
Čermák V, Gandalovičová A, Merta L, Harant K, Rösel D, Brábek J. High-throughput transcriptomic and proteomic profiling of mesenchymal-amoeboid transition in 3D collagen. Sci Data (2020) 7(1):160. doi: 10.1038/s41597-020-0499-2 PubMed DOI PMC
Sahai E, Marshall CJ. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat Cell Biol (2003) 5(8):711–9. doi: 10.1038/ncb1019 PubMed DOI
MacKay JL, Kumar S. Simultaneous and independent tuning of RhoA and Rac1 activity with orthogonally inducible promoters. Integr Biol (2014) 6(9):885–94. doi: 10.1039/c4ib00099d PubMed DOI PMC
Sanz-Moreno V, Gadea G, Ahn J, Paterson H, Marra P, Pinner S, et al. . Rac activation and inactivation control plasticity of tumor cell movement. Cell (2008) 135(3):510–23. doi: 10.1016/j.cell.2008.09.043 PubMed DOI
Waterman-Storer CM, Worthylake RA, Liu BP, Burridge K, Salmon ED. Microtubule growth activates Rac1 to promote lamellipodial protrusion in fibroblasts. Nat Cell Biol (1999) 1(1):45–50. doi: 10.1038/9018 PubMed DOI
Waterman-Storer CM, Salmon E. Positive feedback interactions between microtubule and actin dynamics during cell motility. Curr Opin Cell Biol (1999) 11(1):61–7. doi: 10.1016/S0955-0674(99)80008-8 PubMed DOI
Daub H, Gevaert K, Vandekerckhove J, Sobel A, Hall A. Rac/Cdc42 and p65PAK regulate the microtubule-destabilizing protein stathmin through phosphorylation at serine 16. J Biol Chem (2001) 276(3):1677–80. doi: 10.1074/jbc.C000635200 PubMed DOI
Zeitz M, Kierfeld J. Feedback mechanism for microtubule length regulation by stathmin gradients. Biophys J (2014) 107(12):2860–71. doi: 10.1016/j.bpj.2014.10.056 PubMed DOI PMC
Ishizaki T, Morishima Y, Okamoto M, Furuyashiki T, Kato T, Narumiya S. Coordination of microtubules and the actin cytoskeleton by the rho effector mDia1. Nat Cell Biol (2001) 3(1):8–14. doi: 10.1038/35050598 PubMed DOI
Palazzo AF, Cook TA, Alberts AS, Gundersen GG. mDia mediates rho-regulated formation and orientation of stable microtubules. Nat Cell Biol (2001) 3(8):723–9. doi: 10.1038/35087035 PubMed DOI
Sakamoto Y, Boëda B, Etienne-Manneville S. APC binds intermediate filaments and is required for their reorganization during cell migration. J Cell Biol (2013) 200(3):249–58. doi: 10.1083/jcb.201206010 PubMed DOI PMC
Schaedel L, Lorenz C, Schepers AV, Klumpp S, Köster S. Vimentin intermediate filaments stabilize dynamic microtubules by direct interactions. Nat Commun (2021) 12(1):3799. doi: 10.1038/s41467-021-23523-z PubMed DOI PMC
Bouchet BP, Akhmanova A. Microtubules in 3D cell motility. J Cell Sci (2017) 130(1):39–50. doi: 10.1242/jcs.189431 PubMed DOI
Etienne-Manneville S. Microtubules in cell migration. Annu Rev Cell Dev Biol (2013) 29(1):471–99. doi: 10.1146/annurev-cellbio-101011-155711 PubMed DOI
Garcin C, Straube A. Microtubules in cell migration. Essays Biochem (2019) 63(5):509–20. doi: 10.1042/EBC20190016 PubMed DOI PMC
Vaughan KT. TIP maker and TIP marker; EB1 as a master controller of microtubule plus ends. J Cell Biol (2005) 171(2):197–200. doi: 10.1083/jcb.200509150 PubMed DOI PMC
van Haren J, Charafeddine RA, Ettinger A, Wang H, Hahn KM, Wittmann T. Local control of intracellular microtubule dynamics by EB1 photodissociation. Nat Cell Biol (2018) 20(3):252–61. doi: 10.1038/s41556-017-0028-5 PubMed DOI PMC
Jayatilaka H, Giri A, Karl M, Aifuwa I, Trenton NJ, Phillip JM, et al. . EB1 and cytoplasmic dynein mediate protrusion dynamics for efficient 3-dimensional cell migration. FASEB J (2018) 32(3):1207–21. doi: 10.1096/fj.201700444RR PubMed DOI PMC
Bouchet BP, Noordstra I, van Amersfoort M, Katrukha EA, Ammon YC, ter Hoeve ND, et al. . Mesenchymal cell invasion requires cooperative regulation of persistent microtubule growth by SLAIN2 and CLASP1. Dev Cell (2016) 39(6):708–23. doi: 10.1016/j.devcel.2016.11.009 PubMed DOI PMC
White CD, Erdemir HH, Sacks DB. IQGAP1 and its binding proteins control diverse biological functions. Cell Signal (2012) 24(4):826–34. doi: 10.1016/j.cellsig.2011.12.005 PubMed DOI PMC
Bashour AM, Fullerton AT, Hart MJ, Bloom GS. IQGAP1, a rac- and Cdc42-binding protein, directly binds and cross-links microfilaments. J Cell Biol (1997) 137(7):1555–66. doi: 10.1083/jcb.137.7.1555 PubMed DOI PMC
Hoeprich GJ, Sinclair AN, Shekhar S, Goode BL. Single-molecule imaging of IQGAP1 regulating actin filament dynamics. Mol Biol Cell (2022) 33(1):ar2. doi: 10.1091/mbc.E21-04-0211 PubMed DOI PMC
Kuroda S, Fukata M, Kobayashi K, Nakafuku M, Nomura N, Iwamatsu A, et al. . Identification of IQGAP as a putative target for the small GTPases, Cdc42 and Rac1. J Biol Chem (1996) 271(38):23363–7. doi: 10.1074/jbc.271.38.23363 PubMed DOI
Fukata M, Kuroda S, Fujii K, Nakamura T, Shoji I, Matsuura Y, et al. . Regulation of cross-linking of actin filament by IQGAP1, a target for Cdc42. J Biol Chem (1997) 272(47):29579–83. doi: 10.1074/jbc.272.47.29579 PubMed DOI
Benseñor LB, Kan HM, Wang N, Wallrabe H, Davidson LA, Cai Y, et al. . IQGAP1 regulates cell motility by linking growth factor signaling to actin assembly. J Cell Sci (2007) 120(4):658–69. doi: 10.1242/jcs.03376 PubMed DOI
Le Clainche C, Schlaepfer D, Ferrari A, Klingauf M, Grohmanova K, Veligodskiy A, et al. . IQGAP1 stimulates actin assembly through the n-Wasp-Arp2/3 pathway. J Biol Chem (2007) 282(1):426–35. doi: 10.1074/jbc.M607711200 PubMed DOI
Mataraza JM, Briggs MW, Li Z, Entwistle A, Ridley AJ, Sacks DB. IQGAP1 promotes cell motility and invasion. J Biol Chem (2003) 278(42):41237–45. doi: 10.1074/jbc.M304838200 PubMed DOI
Hart MJ, Callow MG, Souza B, Polakis P. IQGAP1, a calmodulin-binding protein with a rasGAP-related domain, is a potential effector for cdc42Hs. EMBO J (1996) 15(12):2997–3005. doi: 10.1002/j.1460-2075.1996.tb00663.x PubMed DOI PMC
Etienne-Manneville S, Hall A. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCζ. Cell (2001) 106(4):489–98. doi: 10.1016/S0092-8674(01)00471-8 PubMed DOI
Fukata M, Watanabe T, Noritake J, Nakagawa M, Yamaga M, Kuroda S, et al. . Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell (2002) 109(7):873–85. doi: 10.1016/S0092-8674(02)00800-0 PubMed DOI
Watanabe T, Wang S, Noritake J, Sato K, Fukata M, Takefuji M, et al. . Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev Cell (2004) 7(6):871–83. doi: 10.1016/j.devcel.2004.10.017 PubMed DOI
Cao D, Su Z, Wang W, Wu H, Liu X, Akram S, et al. . Signaling scaffold protein IQGAP1 interacts with microtubule plus-end tracking protein SKAP and links dynamic microtubule plus-end to steer cell migration. J Biol Chem (2015) 290(39):23766–80. doi: 10.1074/jbc.M115.673517 PubMed DOI PMC
Yamaoka-Tojo M, Ushio-Fukai M, Hilenski L, Dikalov SI, Chen YE, Tojo T, et al. . IQGAP1, a novel vascular endothelial growth factor receptor binding protein, is involved in reactive oxygen species–dependent endothelial migration and proliferation. Circ Res (2004) 95(3):276–83. doi: 10.1161/01.RES.0000136522.58649.60 PubMed DOI
Li S, Guan JL, Chien S. Biochemistry and biomechanics of cell motility. Annu Rev BioMed Eng (2005) 7(1):105–50. doi: 10.1146/annurev.bioeng.7.060804.100340 PubMed DOI
Sánchez-Huertas C, Bonhomme M, Falco A, Fagotto-Kaufmann C, van Haren J, Jeanneteau F, et al. . The +TIP navigator-1 is an actin–microtubule crosslinker that regulates axonal growth cone motility. J Cell Biol (2020) 219(9):e201905199. doi: 10.1083/jcb.201905199 PubMed DOI PMC
van Haren J, Draegestein K, Keijzer N, Abrahams JP, Grosveld F, Peeters PJ, et al. . Mammalian navigators are microtubule plus-end tracking proteins that can reorganize the cytoskeleton to induce neurite-like extensions. Cell Motil Cytoskeleton (2009) 66(10):824–38. doi: 10.1002/cm.20370 PubMed DOI
van Haren J, Boudeau J, Schmidt S, Basu S, Liu Z, Lammers D, et al. . Dynamic microtubules catalyze formation of navigator-TRIO complexes to regulate neurite extension. Curr Biol (2014) 24(15):1778–85. doi: 10.1016/j.cub.2014.06.037 PubMed DOI
Bellanger JM, Lazaro JB, Diriong S, Fernandez A, Lamb N, Debant A. The two guanine nucleotide exchange factor domains of trio link the Rac1 and the RhoA pathways in vivo. Oncogene (1998) 16(2):147–52. doi: 10.1038/sj.onc.1201532 PubMed DOI
Briançon-Marjollet A, Ghogha A, Nawabi H, Triki I, Auziol C, Fromont S, et al. . Trio mediates netrin-1-Induced Rac1 activation in axon outgrowth and guidance. Mol Cell Biol (2008) 28(7):2314–23. doi: 10.1128/MCB.00998-07 PubMed DOI PMC
Cohen-Dvashi H, Ben-Chetrit N, Russell R, Carvalho S, Lauriola M, Nisani S, et al. . Navigator-3, a modulator of cell migration, may act as a suppressor of breast cancer progression. EMBO Mol Med (2015) 7(3):299–314. doi: 10.15252/emmm.201404134 PubMed DOI PMC
Belmont LD, Mitchison TJ. Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules. Cell (1996) 84(4):623–31. doi: 10.1016/S0092-8674(00)81037-5 PubMed DOI
Curmi PA, Andersen SSL, Lachkar S, Gavet O, Karsenti E, Knossow M, et al. . The Stathmin/Tubulin interaction in vitro. J Biol Chem (1997) 272(40):25029–36. doi: 10.1074/jbc.272.40.25029 PubMed DOI
Howell B, Larsson N, Gullberg M, Cassimeris L. Dissociation of the tubulin-sequestering and microtubule catastrophe-promoting activities of oncoprotein 18/Stathmin. Mol Biol Cell (1999) 10(1):105–18. doi: 10.1091/mbc.10.1.105 PubMed DOI PMC
Melander Gradin H, Marklund U, Larsson N, Chatila TA, Gullberg M. Regulation of microtubule dynamics by Ca2+/calmodulin-dependent kinase IV/Gr-dependent phosphorylation of oncoprotein 18. Mol Cell Biol (1997) 17(6):3459–67. doi: 10.1128/MCB.17.6.3459 PubMed DOI PMC
Gavet O, Ozon S, Manceau V, Lawler S, Curmi P, Sobel A. The stathmin phosphoprotein family: intracellular localization and effects on the microtubule network. J Cell Sci (1998) 111(22):3333–46. doi: 10.1242/jcs.111.22.3333 PubMed DOI
Ng DCH, Lin BH, Lim CP, Huang G, Zhang T, Poli V, et al. . Stat3 regulates microtubules by antagonizing the depolymerization activity of stathmin. J Cell Biol (2006) 172(2):245–57. doi: 10.1083/jcb.200503021 PubMed DOI PMC
Baldassarre G, Belletti B, Nicoloso MS, Schiappacassi M, Vecchione A, Spessotto P, et al. . p27Kip1-stathmin interaction influences sarcoma cell migration and invasion. Cancer Cell (2005) 7(1):51–63. doi: 10.1016/j.ccr.2004.11.025 PubMed DOI
Schiappacassi M, Lovat F, Canzonieri V, Belletti B, Berton S, Di Stefano D, et al. . p27 Kip1 expression inhibits glioblastoma growth, invasion, and tumor-induced neoangiogenesis. Mol Cancer Ther (2008) 7(5):1164–75. doi: 10.1158/1535-7163.MCT-07-2154 PubMed DOI
Klausen P, Pedersen L, Jurlander J, Baumann H. Oncostatin m and interleukin 6 inhibit cell cycle progression by prevention of p27kip1 degradation in HepG2 cells. Oncogene (2000) 19(32):3675–83. doi: 10.1038/sj.onc.1203707 PubMed DOI
Niethammer P, Bastiaens P, Karsenti E. Stathmin-tubulin interaction gradients in motile and mitotic cells. Science (2004) 303(5665):1862–6. doi: 10.1126/science.1094108 PubMed DOI
Belletti B, Nicoloso MS, Schiappacassi M, Berton S, Lovat F, Wolf K, et al. . Stathmin activity influences sarcoma cell shape, motility, and metastatic potential. Mol Biol Cell (2008) 19(5):2003–13. doi: 10.1091/mbc.e07-09-0894 PubMed DOI PMC
Baldassarre G, Belletti B, Bruni P, Boccia A, Trapasso F, Pentimalli F, et al. . Overexpressed cyclin D3 contributes to retaining the growth inhibitor p27 in the cytoplasm of thyroid tumor cells. J Clin Invest (1999) 104(7):865–74. doi: 10.1172/JCI6443 PubMed DOI PMC
Besson A, Gurian-West M, Schmidt A, Hall A, Roberts JM. p27 Kip1 modulates cell migration through the regulation of RhoA activation. Genes Dev (2004) 18(8):862–76. doi: 10.1101/gad.1185504 PubMed DOI PMC
Morelli G, Even A, Gladwyn-Ng I, Le Bail R, Shilian M, Godin JD, et al. . p27Kip1 modulates axonal transport by regulating α-tubulin acetyltransferase 1 stability. Cell Rep (2018) 23(8):2429–42. doi: 10.1016/j.celrep.2018.04.083 PubMed DOI
McAllister SS, Becker-Hapak M, Pintucci G, Pagano M, Dowdy SF. Novel p27 kip1 c-terminal scatter domain mediates rac-dependent cell migration independent of cell cycle arrest functions. Mol Cell Biol (2003) 23(1):216–28. doi: 10.1128/MCB.23.1.216-228.2003 PubMed DOI PMC
Berton S, Belletti B, Wolf K, Canzonieri V, Lovat F, Vecchione A, et al. . The tumor suppressor functions of p27 kip1 include control of the Mesenchymal/Amoeboid transition. Mol Cell Biol (2009) 29(18):5031–45. doi: 10.1128/MCB.00144-09 PubMed DOI PMC
Gui P, Labrousse A, Van Goethem E, Besson A, Maridonneau-Parini I, Le Cabec V. Rho/ROCK pathway inhibition by CDK inhibitor p27kip1 participates in the onset of macrophage 3D-mesenchymal migration. J Cell Sci (2014) 127(18):4009–23. doi: 10.1242/jcs.150987 PubMed DOI
Chalkia D, Nikolaidis N, Makalowski W, Klein J, Nei M. Origins and evolution of the formin multigene family that is involved in the formation of actin filaments. Mol Biol Evol (2008) 25(12):2717–33. doi: 10.1093/molbev/msn215 PubMed DOI PMC
Hager MH, Morley S, Bielenberg DR, Gao S, Morello M, Holcomb IN, et al. . DIAPH3 governs the cellular transition to the amoeboid tumour phenotype. EMBO Mol Med (2012) 4(8):743–60. doi: 10.1002/emmm.201200242 PubMed DOI PMC
Wyse MM, Goicoechea S, Garcia-Mata R, Nestor-Kalinoski AL, Eisenmann KM. mDia2 and CXCL12/CXCR4 chemokine signaling intersect to drive tumor cell amoeboid morphological transitions. Biochem Biophys Res Commun (2017) 484(2):255–61. doi: 10.1016/j.bbrc.2017.01.087 PubMed DOI PMC
Pettee KM, Dvorak KM, Nestor-Kalinoski AL, Eisenmann KM. An mDia2/ROCK signaling axis regulates invasive egress from epithelial ovarian cancer spheroids. Aspenstrom P editor PloS One (2014) 9(2):e90371. doi: 10.1371/journal.pone.0090371 PubMed DOI PMC
Morley S, You S, Pollan S, Choi J, Zhou B, Hager MH, et al. . Regulation of microtubule dynamics by DIAPH3 influences amoeboid tumor cell mechanics and sensitivity to taxanes. Sci Rep (2015) 5(1):12136. doi: 10.1038/srep12136 PubMed DOI PMC
Nalbant P, Chang YC, Birkenfeld J, Chang ZF, Bokoch GM. Guanine nucleotide exchange factor-H1 regulates cell migration via localized activation of RhoA at the leading edge. Forscher P editor Mol Biol Cell (2009) 20(18):4070–82. doi: 10.1091/mbc.e09-01-0041 PubMed DOI PMC
Azoitei ML, Noh J, Marston DJ, Roudot P, Marshall CB, Daugird TA, et al. . Spatiotemporal dynamics of GEF-H1 activation controlled by microtubule- and src-mediated pathways. J Cell Biol (2019) 218(9):3077–97. doi: 10.1083/jcb.201812073 PubMed DOI PMC
Pan YR, Chen CC, Chan YT, Wang HJ, Chien FT, Chen YL, et al. . STAT3-coordinated migration facilitates the dissemination of diffuse large b-cell lymphomas. Nat Commun (2018) 9(1):3696. doi: 10.1038/s41467-018-06134-z PubMed DOI PMC
Soltani MH, Pichardo R, Song Z, Sangha N, Camacho F, Satyamoorthy K, et al. . Microtubule-associated protein 2, a marker of neuronal differentiation, induces mitotic defects, inhibits growth of melanoma cells, and predicts metastatic potential of cutaneous melanoma. Am J Pathol (2005) 166(6):1841–50. doi: 10.1016/S0002-9440(10)62493-5 PubMed DOI PMC
Ou Y, Zheng X, Gao Y, Shu M, Leng T, Li Y, et al. . Activation of cyclic AMP/PKA pathway inhibits bladder cancer cell invasion by targeting MAP4-dependent microtubule dynamics. Urol Oncol Semin Orig Investig (2014) 32(1):47.e21–8. doi: 10.1016/j.urolonc.2013.06.017 PubMed DOI
Jiang YY, Shang L, Shi ZZ, Zhang TT, Ma S, Lu CC, et al. . Microtubule-associated protein 4 is an important regulator of cell invasion/migration and a potential therapeutic target in esophageal squamous cell carcinoma. Oncogene (2016) 35(37):4846–56. doi: 10.1038/onc.2016.17 PubMed DOI
Tortosa E, Montenegro-Venegas C, Benoist M, Härtel S, González-Billault C, Esteban JA, et al. . Microtubule-associated protein 1B (MAP1B) is required for dendritic spine development and synaptic maturation. J Biol Chem (2011) 286(47):40638–48. doi: 10.1074/jbc.M111.271320 PubMed DOI PMC
Chang W, Gruber D, Chari S, Kitazawa H, Hamazumi Y, Hisanaga S, et al. . Phosphorylation of MAP4 affects microtubule properties and cell cycle progression. J Cell Sci (2001) 114(15):2879–87. doi: 10.1242/jcs.114.15.2879 PubMed DOI
Krendel M, Zenke FT, Bokoch GM. Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat Cell Biol (2002) 4(4):294–301. doi: 10.1038/ncb773 PubMed DOI
Luxton GG, Gundersen GG. Orientation and function of the nuclear–centrosomal axis during cell migration. Curr Opin Cell Biol (2011) 23(5):579–88. doi: 10.1016/j.ceb.2011.08.001 PubMed DOI PMC
Burute M, Prioux M, Blin G, Truchet S, Letort G, Tseng Q, et al. . Polarity reversal by centrosome repositioning primes cell scattering during epithelial-to-Mesenchymal transition. Dev Cell (2017) 40(2):168–84. doi: 10.1016/j.devcel.2016.12.004 PubMed DOI PMC
Doyle AD, Wang FW, Matsumoto K, Yamada KM. One-dimensional topography underlies three-dimensional fibrillar cell migration. J Cell Biol (2009) 184(4):481–90. doi: 10.1083/jcb.200810041 PubMed DOI PMC
Zhang J, Wang Y. Centrosome defines the rear of cells during mesenchymal migration. Mol Biol Cell (2017) 28(23):3240–51. doi: 10.1091/mbc.e17-06-0366 PubMed DOI PMC
Pouthas F, Girard P, Lecaudey V, Ly TBN, Gilmour D, Boulin C, et al. . In migrating cells, the golgi complex and the position of the centrosome depend on geometrical constraints of the substratum. J Cell Sci (2008) 121(14):2406–14. doi: 10.1242/jcs.026849 PubMed DOI
Renkawitz J, Kopf A, Stopp J, de Vries I, Driscoll MK, Merrin J, et al. . Nuclear positioning facilitates amoeboid migration along the path of least resistance. Nature. (2019) 568(7753):546–50. doi: 10.1038/s41586-019-1087-5 PubMed DOI PMC
Sánchez-Madrid F, Serrador JM. Bringing up the rear: defining the roles of the uropod. Nat Rev Mol Cell Biol (2009) 10(5):353–9. doi: 10.1038/nrm2680 PubMed DOI
Friedl P, Wolf K. Plasticity of cell migration: A multiscale tuning model. J Cell Biol (2010) 188(1):11–9. doi: 10.1083/jcb.200909003 PubMed DOI PMC
Liu YJ, Le Berre M, Lautenschlaeger F, Maiuri P, Callan-Jones A, Heuzé M, et al. . Confinement and low adhesion induce fast amoeboid migration of slow mesenchymal cells. Cell (2015) 160(4):659–72. doi: 10.1016/j.cell.2015.01.007 PubMed DOI
Wolf K, Mazo I, Leung H, Engelke K, von Andrian UH, Deryugina EI, et al. . Compensation mechanism in tumor cell migration. J Cell Biol (2003) 160(2):267–77. doi: 10.1083/jcb.200209006 PubMed DOI PMC
Doyle AD, Carvajal N, Jin A, Matsumoto K, Yamada KM. Local 3D matrix microenvironment regulates cell migration through spatiotemporal dynamics of contractility-dependent adhesions. Nat Commun (2015) 6(1):8720. doi: 10.1038/ncomms9720 PubMed DOI PMC
Seetharaman S, Etienne-Manneville S. Integrin diversity brings specificity in mechanotransduction: Integrin diversity brings specificity in mechanotransduction. Biol Cell (2018) 110(3):49–64. doi: 10.1111/boc.201700060 PubMed DOI
Wozniak MA, Modzelewska K, Kwong L, Keely PJ. Focal adhesion regulation of cell behavior. Biochim Biophys Acta BBA - Mol Cell Res (2004) 1692(2–3):103–19. doi: 10.1016/j.bbamcr.2004.04.007 PubMed DOI
Huveneers S, Danen EHJ. Adhesion signaling – crosstalk between integrins, src and rho. J Cell Sci (2009) 122(8):1059–69. doi: 10.1242/jcs.039446 PubMed DOI
Lawson CD, Burridge K. The on-off relationship of rho and rac during integrin-mediated adhesion and cell migration. Small GTPases (2014) 5(1):e27958. doi: 10.4161/sgtp.27958 PubMed DOI PMC
Stehbens S, Wittmann T. Targeting and transport: How microtubules control focal adhesion dynamics. J Cell Biol (2012) 198(4):481–9. doi: 10.1083/jcb.201206050 PubMed DOI PMC
Kaverina I, Rottner K, Small JV. Targeting, capture, and stabilization of microtubules at early focal adhesions. J Cell Biol (1998) 142(1):181–90. doi: 10.1083/jcb.142.1.181 PubMed DOI PMC
Krylyshkina O, Anderson KI, Kaverina I, Upmann I, Manstein DJ, Small JV, et al. . Nanometer targeting of microtubules to focal adhesions. J Cell Biol (2003) 161(5):853–9. doi: 10.1083/jcb.200301102 PubMed DOI PMC
Seetharaman S, Etienne-Manneville S. Microtubules at focal adhesions – a double-edged sword. J Cell Sci (2019) 132(19):jcs232843. doi: 10.1242/jcs.232843 PubMed DOI
Byron A, Askari JA, Humphries JD, Jacquemet G, Koper EJ, Warwood S, et al. . A proteomic approach reveals integrin activation state-dependent control of microtubule cortical targeting. Nat Commun (2015) 6(1):6135. doi: 10.1038/ncomms7135 PubMed DOI PMC
Kaverina I, Krylyshkina O, Small JV. Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J Cell Biol (1999) 146(5):1033–44. doi: 10.1083/jcb.146.5.1033 PubMed DOI PMC
Bershadsky A, Chausovsky A, Becker E, Lyubimova A, Geiger B. Involvement of microtubules in the control of adhesion-dependent signal transduction. Curr Biol (1996) 6(10):1279–89. doi: 10.1016/S0960-9822(02)70714-8 PubMed DOI
Ezratty EJ, Partridge MA, Gundersen GG. Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat Cell Biol (2005) 7(6):581–90. doi: 10.1038/ncb1262 PubMed DOI
Tolde O, Rösel D, Janostiak R, Vesely P, Brábek J. Dynamics and morphology of focal adhesions in complex 3D environment. Folia Biol (Praha) (2012) 58:177–84. PubMed
Linder S. The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol (2007) 17(3):107–17. doi: 10.1016/j.tcb.2007.01.002 PubMed DOI
Linder S, Hufner K, Wintergerst U, Aepfelbacher M. Microtubule-dependent formation of podosomal adhesion structures in primary human macrophages. J Cell Sci (2000) 113(23):4165–76. doi: 10.1242/jcs.113.23.4165 PubMed DOI
Ory S, Destaing O, Jurdic P. Microtubule dynamics differentially regulates rho and rac activity and triggers rho-independent stress fiber formation in macrophage polykaryons. Eur J Cell Biol (2002) 81(6):351–62. doi: 10.1078/0171-9335-00255 PubMed DOI
Biosse Duplan M, Zalli D, Stephens S, Zenger S, Neff L, Oelkers JM, et al. . Microtubule dynamic instability controls podosome patterning in osteoclasts through EB1, cortactin, and src. Mol Cell Biol (2014) 34(1):16–29. doi: 10.1128/MCB.00578-13 PubMed DOI PMC
Efimova N, Grimaldi A, Bachmann A, Frye K, Zhu X, Feoktistov A, et al. . Podosome-regulating kinesin KIF1C translocates to the cell periphery in a CLASP-dependent manner. J Cell Sci (2014) 127(24):5179–88. doi: 10.1242/jcs.149633 PubMed DOI PMC
Kopp P, Lammers R, Aepfelbacher M, Rudel T, Machuy N, Steffen W, et al. . The kinesin KIF1C and microtubule plus ends regulate podosome dynamics in Macrophages□D □V. Mol Biol Cell (2006) 17:13. doi: 10.1091/mbc.e05-11-1010 PubMed DOI PMC
Destaing O, Saltel F, Gilquin B, Chabadel A, Khochbin S, Ory S, et al. . A novel rho-mDia2-HDAC6 pathway controls podosome patterning through microtubule acetylation in osteoclasts. J Cell Sci (2005) 118(13):2901–11. doi: 10.1242/jcs.02425 PubMed DOI
Bhuwania R, Cornfine S, Fang Z, Krüger M, Luna EJ, Linder S. Supervillin couples myosin-dependent contractility to podosomes and enables their turnover. J Cell Sci (2012) 125(9):2300–14. doi: 10.1242/jcs.100032 PubMed DOI PMC
van den Dries K, Meddens MBM, de Keijzer S, Shekhar S, Subramaniam V, Figdor CG, et al. . Interplay between myosin IIA-mediated contractility and actin network integrity orchestrates podosome composition and oscillations. Nat Commun (2013) 4(1):1412. doi: 10.1038/ncomms2402 PubMed DOI PMC
van Helden SFG, Oud MM, Joosten B, Peterse N, Figdor CG, van Leeuwen FN. PGE2-mediated podosome loss in dendritic cells is dependent on actomyosin contraction downstream of the RhoA–rho-kinase axis. J Cell Sci (2008) 121(7):1096–106. doi: 10.1242/jcs.020289 PubMed DOI
Ory S, Brazier H, Pawlak G, Blangy A. Rho GTPases in osteoclasts: Orchestrators of podosome arrangement. Eur J Cell Biol (2008) 87(8–9):469–77. doi: 10.1016/j.ejcb.2008.03.002 PubMed DOI
Gimona M, Buccione R, Courtneidge SA, Linder S. Assembly and biological role of podosomes and invadopodia. Curr Opin Cell Biol (2008) 20(2):235–41. doi: 10.1016/j.ceb.2008.01.005 PubMed DOI
Schoumacher M, Goldman RD, Louvard D, Vignjevic DM. Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J Cell Biol (2010) 189(3):541–56. doi: 10.1083/jcb.200909113 PubMed DOI PMC
Kikuchi K, Takahashi K. WAVE2- and microtubule-dependent formation of long protrusions and invasion of cancer cells cultured on three-dimensional extracellular matrices. Cancer Sci (2008) 99(11):2252–9. doi: 10.1111/j.1349-7006.2008.00927.x PubMed DOI PMC
Revach OY, Weiner A, Rechav K, Sabanay I, Livne A, Geiger B. Mechanical interplay between invadopodia and the nucleus in cultured cancer cells. Sci Rep (2015) 5(1):9466. doi: 10.1038/srep09466 PubMed DOI PMC
Caldieri G, Buccione R. Aiming for invadopodia: organizing polarized delivery at sites of invasion. Trends Cell Biol (2010) 20(2):64–70. doi: 10.1016/j.tcb.2009.10.006 PubMed DOI
Schnaeker EM, Ossig R, Ludwig T, Dreier R, Oberleithner H, Wilhelmi M, et al. . Microtubule-dependent matrix metalloproteinase-2/Matrix metalloproteinase-9 exocytosis. Cancer Res (2004) 64(24):8924–31. doi: 10.1158/0008-5472.CAN-04-0324 PubMed DOI
Sakurai-Yageta M, Recchi C, Le Dez G, Sibarita JB, Daviet L, Camonis J, et al. . The interaction of IQGAP1 with the exocyst complex is required for tumor cell invasion downstream of Cdc42 and RhoA. J Cell Biol (2008) 181(6):985–98. doi: 10.1083/jcb.200709076 PubMed DOI PMC
Brábek J, Mierke CT, Rösel D, Veselý P, Fabry B. The role of the tissue microenvironment in the regulation of cancer cell motility and invasion. Cell Commun Signal (2010) 8(1):22. doi: 10.1186/1478-811X-8-22 PubMed DOI PMC
Wolf K, te Lindert M, Krause M, Alexander S, te Riet J, Willis AL, et al. . Physical limits of cell migration: Control by ECM space and nuclear deformation and tuning by proteolysis and traction force. J Cell Biol (2013) 201(7):1069–84. doi: 10.1083/jcb.201210152 PubMed DOI PMC
Ruprecht V, Wieser S, Callan-Jones A, Smutny M, Morita H, Sako K, et al. . Cortical contractility triggers a stochastic switch to fast amoeboid cell motility. Cell (2015) 160(4):673–85. doi: 10.1016/j.cell.2015.01.008 PubMed DOI PMC
Plotnikov SV, Waterman CM. Guiding cell migration by tugging. Curr Opin Cell Biol (2013) 25(5):619–26. doi: 10.1016/j.ceb.2013.06.003 PubMed DOI PMC
Montagnac G, Meas-Yedid V, Irondelle M, Castro-Castro A, Franco M, Shida T, et al. . αTAT1 catalyses microtubule acetylation at clathrin-coated pits. Nature (2013) 502(7472):567–70. doi: 10.1038/nature12571 PubMed DOI PMC
Pham TQ, Robinson K, Xu L, Pavlova MN, Skapek SX, Chen EY. HDAC6 promotes growth, migration/invasion, and self-renewal of rhabdomyosarcoma. Oncogene (2021) 40(3):578–91. doi: 10.1038/s41388-020-01550-2 PubMed DOI PMC
Clark ES, Whigham AS, Yarbrough WG, Weaver AM. Cortactin is an essential regulator of matrix metalloproteinase secretion and extracellular matrix degradation in invadopodia. Cancer Res (2007) 67(9):4227–35. doi: 10.1158/0008-5472.CAN-06-3928 PubMed DOI
Castro-Castro A, Janke C, Montagnac G, Paul-Gilloteaux P, Chavrier P. ATAT1/MEC-17 acetyltransferase and HDAC6 deacetylase control a balance of acetylation of alpha-tubulin and cortactin and regulate MT1-MMP trafficking and breast tumor cell invasion. Eur J Cell Biol (2012) 91(11–12):950–60. doi: 10.1016/j.ejcb.2012.07.001 PubMed DOI
Torrino S, Grasset EM, Audebert S, Belhadj I, Lacoux C, Haynes M, et al. . Mechano-induced cell metabolism promotes microtubule glutamylation to force metastasis. Cell Metab (2021) 33(7):1342–57. doi: 10.1016/j.cmet.2021.05.009 PubMed DOI
Heck JN, Ponik SM, Garcia-Mendoza MG, Pehlke CA, Inman DR, Eliceiri KW, et al. . Microtubules regulate GEF-H1 in response to extracellular matrix stiffness. Mol Biol Cell (2012) 23(13):2583–92. doi: 10.1091/mbc.e11-10-0876 PubMed DOI PMC
Hu JY, Chu ZG, Han J, Dang Y, Yan H, Zhang Q, et al. . The p38/MAPK pathway regulates microtubule polymerization through phosphorylation of MAP4 and Op18 in hypoxic cells. Cell Mol Life Sci (2010) 67(2):321–33. doi: 10.1007/s00018-009-0187-z PubMed DOI PMC
Zhang J, Li L, Zhang Q, Yang X, Zhang C, Zhang X, et al. . Phosphorylation of microtubule- associated protein 4 promotes hypoxic endothelial cell migration and proliferation. Front Pharmacol (2019) 10:368. doi: 10.3389/fphar.2019.00368 PubMed DOI PMC
Lehmann S, te Boekhorst V, Odenthal J, Bianchi R, van Helvert S, Ikenberg K, et al. . Hypoxia induces a HIF-1-Dependent transition from collective-to-Amoeboid dissemination in epithelial cancer cells. Curr Biol (2017) 27(3):392–400. doi: 10.1016/j.cub.2016.11.057 PubMed DOI
Čermák V, Dostál V, Jelínek M, Libusová L, Kovář J, Rösel D, et al. . Microtubule-targeting agents and their impact on cancer treatment. Eur J Cell Biol (2020) 99(4):151075. doi: 10.1016/j.ejcb.2020.151075 PubMed DOI
Bates D, Eastman A. Microtubule destabilising agents: far more than just antimitotic anticancer drugs: MDA mechanisms of action. Br J Clin Pharmacol (2017) 83(2):255–68. doi: 10.1111/bcp.13126 PubMed DOI PMC
Eitaki M, Yamamori T, Meike S, Yasui H, Inanami O. Vincristine enhances amoeboid-like motility via GEF-H1/RhoA/ROCK/Myosin light chain signaling in MKN45 cells. BMC Cancer (2012) 12(1):469. doi: 10.1186/1471-2407-12-469 PubMed DOI PMC
Chang YC, Nalbant P, Birkenfeld J, Chang ZF, Bokoch GM. GEF-H1 couples nocodazole-induced microtubule disassembly to cell contractility via RhoA. Mol Biol Cell (2008) 19(5):2147–53. doi: 10.1091/mbc.e07-12-1269 PubMed DOI PMC
Belletti B, Pellizzari I, Berton S, Fabris L, Wolf K, Lovat F, et al. . p27 kip1 controls cell morphology and motility by regulating microtubule-dependent lipid raft recycling. Mol Cell Biol (2010) 30(9):2229–40. doi: 10.1128/MCB.00723-09 PubMed DOI PMC
Carey SP, Rahman A, Kraning-Rush CM, Romero B, Somasegar S, Torre OM, et al. . Comparative mechanisms of cancer cell migration through 3D matrix and physiological microtracks. Am J Physiol-Cell Physiol (2015) 308(6):C436–47. doi: 10.1152/ajpcell.00225.2014 PubMed DOI PMC
Tran TA, Gillet L, Roger S, Besson P, White E, Le Guennec JY. Non-anti-mitotic concentrations of taxol reduce breast cancer cell invasiveness. Biochem Biophys Res Commun (2009) 379(2):304–8. doi: 10.1016/j.bbrc.2008.12.073 PubMed DOI
Yvon AMC, Wadsworth P, Jordan MA. Taxol suppresses dynamics of individual microtubules in living human tumor cells. Mol Biol Cell (1999) 10(4):947–59. doi: 10.1091/mbc.10.4.947 PubMed DOI PMC
Takesono A, Heasman SJ, Wojciak-Stothard B, Garg R, Ridley AJ. Microtubules regulate migratory polarity through Rho/ROCK signaling in T cells. PloS One (2010) 5(1):e8774. doi: 10.1371/journal.pone.0008774 PubMed DOI PMC
Tabdanov ED, Rodríguez-Merced NJ, Cartagena-Rivera AX, Puram VV, Callaway MK, Ensminger EA, et al. . Engineering T cells to enhance 3D migration through structurally and mechanically complex tumor microenvironments. Nat Commun (2021) 12(1):2815. doi: 10.1038/s41467-021-22985-5 PubMed DOI PMC
Dumontet C, Jordan MA. Microtubule-binding agents: A dynamic field of cancer therapeutics. Nat Rev Drug Discov (2010) 9(10):790–803. doi: 10.1038/nrd3253 PubMed DOI PMC
Škubník J, Jurášek M, Ruml T, Rimpelová S. Mitotic poisons in research and medicine. Molecules (2020) 25(20):4632. doi: 10.3390/molecules25204632 PubMed DOI PMC
Fernandes M, Rosel D, Brábek J. Translation in solid cancer: are size-based response criteria an anachronism? Clin Transl Oncol (2015) 17(1):1–10. doi: 10.1007/s12094-014-1207-5 PubMed DOI
Gandalovičová A, Rosel D, Fernandes M, Veselý P, Heneberg P, Čermák V, et al. . Migrastatics–anti-metastatic and anti-invasion drugs: Promises and challenges. Trends Cancer (2017) 3(6):391–406. doi: 10.1016/j.trecan.2017.04.008 PubMed DOI PMC
Rosel D, Fernandes M, Sanz-Moreno V, Brábek J. Migrastatics: Redirecting R&D in solid cancer towards metastasis? Trends Cancer (2019) 5(12):755–6. doi: 10.1016/j.trecan.2019.10.011 PubMed DOI
Solomon J, Raškova M, Rösel D, Brábek J, Gil-Henn H. Are we ready for migrastatics? Cells (2021) 10(8):1845. doi: 10.3390/cells10081845 PubMed DOI PMC
Li Q, Ma Z, Liu Y, Kan X, Wang C, Su B, et al. . Low doses of paclitaxel enhance liver metastasis of breast cancer cells in the mouse model. FEBS J (2016) 283(15):2836–52. doi: 10.1111/febs.13767 PubMed DOI
Zenitani M, Nojiri T, Hosoda H, Kimura T, Uehara S, Miyazato M, et al. . Chemotherapy can promote liver metastasis by enhancing metastatic niche formation in mice. J Surg Res (2018) 224:50–7. doi: 10.1016/j.jss.2017.11.050 PubMed DOI
Thompson KN, Ju JA, Ory EC, Pratt SJP, Lee RM, Mathias TJ, et al. . Microtubule disruption reduces metastasis more effectively than primary tumor growth. Breast Cancer Res (2022) 24(1):13. doi: 10.1186/s13058-022-01506-2 PubMed DOI PMC
Watanabe K, Yui Y, Sasagawa S, Suzuki K, Kanamori M, Yasuda T, et al. . Low-dose eribulin reduces lung metastasis of osteosarcoma in vitro and in vivo. Oncotarget (2019) 10(2):161–74. doi: 10.18632/oncotarget.26536 PubMed DOI PMC
Yoshida T, Ozawa Y, Kimura T, Sato Y, Kuznetsov G, Xu S, et al. . Eribulin mesilate suppresses experimental metastasis of breast cancer cells by reversing phenotype from epithelial–mesenchymal transition (EMT) to mesenchymal–epithelial transition (MET) states. Br J Cancer (2014) 110(6):1497–505. doi: 10.1038/bjc.2014.80 PubMed DOI PMC
O’Shaughnessy J, Kaklamani V, Kalinsky K. Perspectives on the mechanism of action and clinical application of eribulin for metastatic breast cancer. Future Oncol (2019) 15(14):1641–53. doi: 10.2217/fon-2018-0936 PubMed DOI
Kopf A, Renkawitz J, Hauschild R, Girkontaite I, Tedford K, Merrin J, et al. . Microtubules control cellular shape and coherence in amoeboid migrating cells. J Cell Biol (2020) 219(6):e201907154. doi: 10.1083/jcb.201907154 PubMed DOI PMC
Welch MD. Cell migration, freshly squeezed. Cell (2015) 160(4):581–2. doi: 10.1016/j.cell.2015.01.053 PubMed DOI
Lämmermann T, Sixt M. Mechanical modes of a’moeboid’ cell migration. Curr Opin Cell Biol (2009) 21(5):636–44. doi: 10.1016/j.ceb.2009.05.003 PubMed DOI
Tekle YI, Williams JR. Cytoskeletal architecture and its evolutionary significance in amoeboid eukaryotes and their mode of locomotion. R Soc Open Sci (2016) 3(9):160283. doi: 10.1098/rsos.160283 PubMed DOI PMC