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Regulation of cell migration by dynamic microtubules
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Kaverina, Irina and Straube, Anne. (2011) Regulation of cell migration by dynamic microtubules. Seminars in Cell & Developmental Biology, Volume 22 (Number 9). pp. 968-974. ISSN 1084-9521
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Official URL: http://dx.doi.org/10.1016/j.semcdb.2011.09.017
Abstract
Microtubules define the architecture and internal organization of cells by positioning organelles and activities, as well as by supporting cell shape and mechanics. One of the major functions of microtubules is the control of polarized cell motility. In order to support the asymmetry of polarized cells, microtubules have to be organized asymmetrically themselves. Asymmetry in microtubule distribution and stability is regulated by multiple molecular factors, most of which are microtubule-associated proteins that locally control microtubule nucleation and dynamics. At the same time, the dynamic state of microtubules is key to the regulatory mechanisms by which microtubules regulate cell polarity, modulate cell adhesion and control force-production by the actin cytoskeleton. Here, we propose that even small alterations in microtubule dynamics can influence cell migration via several different microtubule-dependent pathways. We discuss regulatory factors, potential feedback mechanisms due to functional microtubule-actin crosstalk and implications for cancer cell motility.
| Item Type: | Journal Article |
|---|---|
| Subjects: | Q Science > QH Natural history > QH301 Biology Q Science > QR Microbiology |
| Divisions: | Faculty of Medicine > Warwick Medical School > Biomedical Cell Biology Faculty of Medicine > Warwick Medical School |
| Library of Congress Subject Headings (LCSH): | Microtubules, Cell organelles, Cell migration, Cytology, Cells -- Motility, Microbiology -- Research , Cancer cells -- Motility |
| Journal or Publication Title: | Seminars in Cell & Developmental Biology |
| Publisher: | Elsevier Ltd |
| ISSN: | 1084-9521 |
| Date: | December 2011 |
| Volume: | Volume 22 |
| Number: | Number 9 |
| Page Range: | pp. 968-974 |
| Identification Number: | 10.1016/j.semcdb.2011.09.017 |
| Status: | Peer Reviewed |
| Publication Status: | Published |
| Access rights to Published version: | Restricted or Subscription Access |
| Funder: | National Institutes of Health (U.S.) (NIH), National Institute of General Medical Sciences (U.S.) (NIGMS), American Heart Association (AHA), Marie Curie Cancer Care, University of Warwick |
| Grant number: | R01 GM078373 (NIH NIGMS) ; 10GRNT4230026 |
| References: | [1] Brangwynne CP, MacKintosh FC, Weitz DA. Force fluctuations and polymerization dynamics of intracellular microtubules. Proceedings of the National Academy of Sciences of the United States of America 2007;104:16128-33. [2] Kirschner MW, Mitchison T. Microtubule dynamics. Nature 1986;324:621. [3] Mandelkow EM, Mandelkow E, Milligan RA. Microtubule dynamics and microtubule caps: a time-resolved cryo-electron microscopy study. J Cell Biol 1991;114:977-91. [4] Howard J, Hyman AA. Growth, fluctuation and switching at microtubule plus ends. Nat Rev Mol Cell Biol 2009;10:569-74. [5] Dammermann A, Desai A, Oegema K. The minus end in sight. Curr Biol 2003;13:R614-24. [6] Komarova YA, Vorobjev IA, Borisy GG. Life cycle of MTs: persistent growth in the cell interior, asymmetric transition frequencies and effects of the cell boundary. J Cell Sci 2002;115:3527-39. [7] Drummond DR, Cross RA. Dynamics of interphase microtubules in Schizosaccharomyces pombe. Curr Biol 2000;10:766-75. [8] Straube A. How to measure microtubule dynamics? Methods Mol Biol 2011:in press. [9] van der Vaart B, Akhmanova A, Straube A. Regulation of microtubule dynamic instability. Biochem Soc Trans 2009;37:1007-13. [10] Brouhard GJ, Stear JH, Noetzel TL, Al-Bassam J, Kinoshita K, Harrison SC, et al. XMAP215 is a processive microtubule polymerase. Cell 2008;132:79-88. [11] Hunter AW, Caplow M, Coy DL, Hancock WO, Diez S, Wordeman L, et al. The kinesinrelated protein MCAK is a microtubule depolymerase that forms an ATP-hydrolyzing complex at microtubule ends. Mol Cell 2003;11:445-57. [12] Ogawa T, Nitta R, Okada Y, Hirokawa N. A common mechanism for microtubule destabilizers-M type kinesins stabilize curling of the protofilament using the class-specific neck and loops. Cell 2004;116:591-602. [13] Mimori-Kiyosue Y, Grigoriev I, Lansbergen G, Sasaki H, Matsui C, Severin F, et al. CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex. J Cell Biol 2005;168:141-53. [14] Straube A, Merdes A. EB3 regulates microtubule dynamics at the cell cortex and is required for myoblast elongation and fusion. Curr Biol 2007;17:1318-25. [15] 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;109:873-85. [16] 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;7:871-83. [17] Manneville JB, Jehanno M, Etienne-Manneville S. Dlg1 binds GKAP to control dynein association with microtubules, centrosome positioning, and cell polarity. J Cell Biol 2010;191:585-98. [18] Wittmann T, Bokoch GM, Waterman-Storer CM. Regulation of leading edge microtubule and actin dynamics downstream of Rac1. J Cell Biol 2003;161:845-51. [19] Niethammer P, Bastiaens P, Karsenti E. Stathmin-tubulin interaction gradients in motile and mitotic cells. Science 2004;303:1862-6. [20] Efimov A, Kharitonov A, Efimova N, Loncarek J, Miller PM, Andreyeva N, et al. Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Dev Cell 2007;12:917-30. [21] Liu M, Nadar VC, Kozielski F, Kozlowska M, Yu W, Baas PW. Kinesin-12, a mitotic microtubule-associated motor protein, impacts axonal growth, navigation, and branching. J Neurosci 2010;30:14896-906. [22] Nadar VC, Ketschek A, Myers KA, Gallo G, Baas PW. Kinesin-5 is essential for growthcone turning. Curr Biol 2008;18:1972-7. [23] Myers KA, Baas PW. Kinesin-5 regulates the growth of the axon by acting as a brake on its microtubule array. J Cell Biol 2007;178:1081-91. [24] Jolly AL, Kim H, Srinivasan D, Lakonishok M, Larson AG, Gelfand VI. Kinesin-1 heavy chain mediates microtubule sliding to drive changes in cell shape. Proceedings of the National Academy of Sciences of the United States of America 2010;107:12151-6. [25] Gundersen GG, Bulinski JC. Selective stabilization of microtubules oriented toward the direction of cell migration. Proc Natl Acad Sci U S A 1988;85:5946-50. [26] Bulinski JC, Gundersen GG. Stabilization of post-translational modification of microtubules during cellular morphogenesis. Bioessays 1991;13:285-93. [27] Matov A, Applegate K, Kumar P, Thoma C, Krek W, Danuser G, et al. Analysis of microtubule dynamic instability using a plus-end growth marker. Nat Methods 2010;7:761-8. [28] Tran AD, Marmo TP, Salam AA, Che S, Finkelstein E, Kabarriti R, et al. HDAC6 deacetylation of tubulin modulates dynamics of cellular adhesions. J Cell Sci 2007;120:1469-79. [29] Hammond JW, Huang CF, Kaech S, Jacobson C, Banker G, Verhey KJ. Posttranslational modifications of tubulin and the polarized transport of kinesin-1 in neurons. Mol Biol Cell 2010;21:572-83. [30] Reed NA, Cai D, Blasius TL, Jih GT, Meyhofer E, Gaertig J, et al. Microtubule acetylation promotes kinesin-1 binding and transport. Curr Biol 2006;16:2166-72. [31] Salaycik KJ, Fagerstrom CJ, Murthy K, Tulu US, Wadsworth P. Quantification of microtubule nucleation, growth and dynamics in wound-edge cells. J Cell Sci 2005;118:4113-22. [32] Efimov A, Schiefermeier N, Grigoriev I, Ohi R, Brown MC, Turner CE, et al. Paxillindependent stimulation of microtubule catastrophes at focal adhesion sites. J Cell Sci 2008;121:196-204. [33] Kaverina I, Rottner K, Small JV. Targeting, capture, and stabilization of microtubules at early focal adhesions. J Cell Biol 1998;142:181-90. [34] Lansbergen G, Grigoriev I, Mimori-Kiyosue Y, Ohtsuka T, Higa S, Kitajima I, et al. CLASPs attach microtubule plus ends to the cell cortex through a complex with LL5beta. Dev Cell 2006;11:21-32. [35] Kaverina I, Krylyshkina O, Small JV. Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J Cell Biol 1999;146:1033-44. [36] Waterman-Storer CM, Salmon ED. Actomyosin-based retrograde flow of microtubules in the lamella of migrating epithelial cells influences microtubule dynamic instability and turnover and is associated with microtubule breakage and treadmilling. J Cell Biol 1997;139:417-34. [37] Vasiliev JM, Gelfand IM, Domnina LV, Ivanova OY, Komm SG, Olshevskaja LV. Effect of colcemid on the locomotory behaviour of fibroblasts. J Embryol Exp Morphol 1970;24:625-40. [38] Liao G, Nagasaki T, Gundersen GG. Low concentrations of nocodazole interfere with fibroblast locomotion without significantly affecting microtubule level: implications for the role of dynamic microtubules in cell locomotion. J Cell Sci 1995;108 ( Pt 11):3473-83. [39] 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;1:45-50. [40] Montenegro-Venegas C, Tortosa E, Rosso S, Peretti D, Bollati F, Bisbal M, et al. MAP1B regulates axonal development by modulating Rho-GTPase Rac1 activity. Mol Biol Cell 2010;21:3518-28. [41] Rooney C, White G, Nazgiewicz A, Woodcock SA, Anderson KI, Ballestrem C, et al. The Rac activator STEF (Tiam2) regulates cell migration by microtubule-mediated focal adhesion disassembly. EMBO Rep 2010;11:292-8. [42] Watanabe T, Noritake J, Kakeno M, Matsui T, Harada T, Wang S, et al. Phosphorylation of CLASP2 by GSK-3beta regulates its interaction with IQGAP1, EB1 and microtubules. J Cell Sci 2009;122:2969-79. [43] Brandt DT, Grosse R. Get to grips: steering local actin dynamics with IQGAPs. EMBO Rep 2007;8:1019-23. [44] 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. Mol Biol Cell 2009;20:4070-82. [45] Chang YC, Nalbant P, Birkenfeld J, Chang ZF, Bokoch GM. GEF-H1 couples nocodazoleinduced microtubule disassembly to cell contractility via RhoA. Mol Biol Cell 2008;19:2147-53. [46] Krendel M, Zenke FT, Bokoch GM. Nucleotide exchange factor GEF-H1 mediates crosstalk between microtubules and the actin cytoskeleton. Nat Cell Biol 2002;4:294-301. [47] Kaverina I, Krylyshkina O, Small JV. Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J Cell Biol 1999;146:1033-44. [48] Wu X, Kodama A, Fuchs E. ACF7 regulates cytoskeletal-focal adhesion dynamics and migration and has ATPase activity. Cell 2008;135:137-48. [49] Wu X, Shen QT, Oristian DS, Lu CP, Zheng Q, Wang HW, et al. Skin Stem Cells Orchestrate Directional Migration by Regulating Microtubule-ACF7 Connections through GSK3beta. Cell 2011;144:341-52. [50] Ezratty EJ, Bertaux C, Marcantonio EE, Gundersen GG. Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells. J Cell Biol 2009;187:733-47. [51] Ezratty EJ, Partridge MA, Gundersen GG. Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat Cell Biol 2005;7:581-90. [52] Yadav S, Puri S, Linstedt AD. A primary role for Golgi positioning in directed secretion, cell polarity, and wound healing. Mol Biol Cell 2009;20:1728-36. [53] Miller PM, Folkmann AW, Maia AR, Efimova N, Efimov A, Kaverina I. Golgi-derived CLASPdependent microtubules control Golgi organization and polarized trafficking in motile cells. Nat Cell Biol 2009;11:1069-80. [54] Palamidessi A, Frittoli E, Garre M, Faretta M, Mione M, Testa I, et al. Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration. Cell 2008;134:135-47. [55] Mingle LA, Okuhama NN, Shi J, Singer RH, Condeelis J, Liu G. Localization of all seven messenger RNAs for the actin-polymerization nucleator Arp2/3 complex in the protrusions of fibroblasts. J Cell Sci 2005;118:2425-33. [56] Krylyshkina O, Kaverina I, Kranewitter W, Steffen W, Alonso MC, Cross RA, et al. Modulation of substrate adhesion dynamics via microtubule targeting requires kinesin-1. J Cell Biol 2002;156:349-59. [57] Pellinen T, Ivaska J. Integrin traffic. J Cell Sci 2006;119:3723-31. [58] Schmidt MR, Maritzen T, Kukhtina V, Higman VA, Doglio L, Barak NN, et al. Regulation of endosomal membrane traffic by a Gadkin/AP-1/kinesin KIF5 complex. Proceedings of the National Academy of Sciences of the United States of America 2009;106:15344-9. [59] Kopp P, Lammers R, Aepfelbacher M, Woehlke G, Rudel T, Machuy N, et al. The kinesin KIF1C and microtubule plus ends regulate podosome dynamics in macrophages. Mol Biol Cell 2006;17:2811-23. [60] Cornfine S, Himmel M, Kopp P, El Azzouzi K, Wiesner C, Kruger M, et al. The kinesin KIF9 and reggie/flotillin proteins regulate matrix degradation by macrophage podosomes. Mol Biol Cell 2011;22:202-15. [61] Sung HH, Telley IA, Papadaki P, Ephrussi A, Surrey T, Rorth P. Drosophila ensconsin promotes productive recruitment of Kinesin-1 to microtubules. Dev Cell 2008;15:866-76. [62] Seitz A, Kojima H, Oiwa K, Mandelkow EM, Song YH, Mandelkow E. Single-molecule investigation of the interference between kinesin, tau and MAP2c. Embo J 2002;21:4896-905. [63] Gouveia SM, Akhmanova A. Cell and molecular biology of microtubule plus end tracking proteins: end binding proteins and their partners. Int Rev Cell Mol Biol 2010;285:1-74. [64] Jimbo T, Kawasaki Y, Koyama R, Sato R, Takada S, Haraguchi K, et al. Identification of a link between the tumour suppressor APC and the kinesin superfamily. Nat Cell Biol 2002;4:323- 7. [65] Honnappa S, Gouveia SM, Weisbrich A, Damberger FF, Bhavesh NS, Jawhari H, et al. An EB1-binding motif acts as a microtubule tip localization signal. Cell 2009;138:366-76. [66] Miller AL, Wang Y, Mooseker MS, Koleske AJ. The Abl-related gene (Arg) requires its Factin- microtubule cross-linking activity to regulate lamellipodial dynamics during fibroblast adhesion. J Cell Biol 2004;165:407-19. [67] Schober JM, Cain JM, Komarova YA, Borisy GG. Migration and actin protrusion in melanoma cells are regulated by EB1 protein. Cancer Lett 2009;284:30-6. [68] Kroboth K, Newton IP, Kita K, Dikovskaya D, Zumbrunn J, Waterman-Storer CM, et al. Lack of adenomatous polyposis coli protein correlates with a decrease in cell migration and overall changes in microtubule stability. Mol Biol Cell 2007;18:910-8. [69] Nakamura M, Zhou XZ, Lu KP. Critical role for the EB1 and APC interaction in the regulation of microtubule polymerization. Curr Biol 2001;11:1062-7. [70] Drabek K, van Ham M, Stepanova T, Draegestein K, van Horssen R, Sayas CL, et al. Role of CLASP2 in microtubule stabilization and the regulation of persistent motility. Curr Biol 2006;16:2259-64. [71] Akhmanova A, Hoogenraad CC, Drabek K, Stepanova T, Dortland B, Verkerk T, et al. Clasps are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 2001;104:923-35. [72] Dallol A, Agathanggelou A, Tommasi S, Pfeifer GP, Maher ER, Latif F. Involvement of the RASSF1A tumor suppressor gene in controlling cell migration. Cancer Res 2005;65:7653-9. [73] Nakano A, Kato H, Watanabe T, Min KD, Yamazaki S, Asano Y, et al. AMPK controls the speed of microtubule polymerization and directional cell migration through CLIP-170 phosphorylation. Nat Cell Biol 2010;12:583-90. [74] Wen Y, Eng CH, Schmoranzer J, Cabrera-Poch N, Morris EJ, Chen M, et al. EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat Cell Biol 2004;6:820-30. [75] Komarova Y, De Groot CO, Grigoriev I, Gouveia SM, Munteanu EL, Schober JM, et al. Mammalian end binding proteins control persistent microtubule growth. J Cell Biol 2009;184:691-706. [76] Kita K, Wittmann T, Nathke IS, Waterman-Storer CM. Adenomatous polyposis coli on microtubule plus ends in cell extensions can promote microtubule net growth with or without EB1. Mol Biol Cell 2006;17:2331-45. [77] Takemura R, Okabe S, Umeyama T, Kanai Y, Cowan NJ, Hirokawa N. Increased microtubule stability and alpha tubulin acetylation in cells transfected with microtubuleassociated proteins MAP1B, MAP2 or tau. J Cell Sci 1992;103 ( Pt 4):953-64. [78] Riederer BM. Microtubule-associated protein 1B, a growth-associated and phosphorylated scaffold protein. Brain Res Bull 2007;71:541-58. [79] Dallol A, Hesson LB, Matallanas D, Cooper WN, O'Neill E, Maher ER, et al. RAN GTPase is a RASSF1A effector involved in controlling microtubule organization. Curr Biol 2009;19:1227- 32. [80] Al-Bassam J, Kim H, Brouhard G, van Oijen A, Harrison SC, Chang F. CLASP promotes microtubule rescue by recruiting tubulin dimers to the microtubule. Dev Cell 2010;19:245-58. [81] Komarova YA, Akhmanova AS, Kojima S, Galjart N, Borisy GG. Cytoplasmic linker proteins promote microtubule rescue in vivo. J Cell Biol 2002;159:589-99. [82] Arnal I, Heichette C, Diamantopoulos GS, Chretien D. CLIP-170/tubulin-curved oligomers coassemble at microtubule ends and promote rescues. Curr Biol 2004;14:2086-95. [83] Euteneuer U, Schliwa M. Persistent, directional motility of cells and cytoplasmic fragments in the absence of microtubules. Nature 1984;310:58-61. [84] Niggli V. Microtubule-disruption-induced and chemotactic-peptide-induced migration of human neutrophils: implications for differential sets of signalling pathways. J Cell Sci 2003;116:813-22. [85] Xu J, Wang F, Van Keymeulen A, Rentel M, Bourne HR. Neutrophil microtubules suppress polarity and enhance directional migration. Proc Natl Acad Sci U S A 2005;102:6884-9. [86] 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:e8774. [87] Keren K, Pincus Z, Allen GM, Barnhart EL, Marriott G, Mogilner A, et al. Mechanism of shape determination in motile cells. Nature 2008;453:475-80. [88] Verkhovsky AB, Svitkina TM, Borisy GG. Self-polarization and directional motility of cytoplasm. Curr Biol 1999;9:11-20. [89] Barnhart EL, Allen GM, Julicher F, Theriot JA. Bipedal locomotion in crawling cells. Biophys J;98:933-42. [90] Evans R, Patzak I, Svensson L, De Filippo K, Jones K, McDowall A, et al. Integrins in immunity. J Cell Sci 2009;122:215-25. [91] Chen D, Bromberg JS. T regulatory cells and migration. Am J Transplant 2006;6:1518-23. [92] Hogg N, Laschinger M, Giles K, McDowall A. T-cell integrins: more than just sticking points. J Cell Sci 2003;116:4695-705. [93] Anderson KI, Cross R. Contact dynamics during keratocyte motility. Curr Biol 2000;10:253- 60. [94] Okada K, Bartolini F, Deaconescu AM, Moseley JB, Dogic Z, Grigorieff N, et al. Adenomatous polyposis coli protein nucleates actin assembly and synergizes with the formin mDia1. J Cell Biol 2010;189:1087-96. [95] Bartolini F, Moseley JB, Schmoranzer J, Cassimeris L, Goode BL, Gundersen GG. The formin mDia2 stabilizes microtubules independently of its actin nucleation activity. J Cell Biol 2008;181:523-36. [96] Donninger H, Vos MD, Clark GJ. The RASSF1A tumor suppressor. J Cell Sci 2007;120:3163-72. [97] van Es JH, Giles RH, Clevers HC. The many faces of the tumor suppressor gene APC. Exp Cell Res 2001;264:126-34. [98] Humbert PO, Grzeschik NA, Brumby AM, Galea R, Elsum I, Richardson HE. Control of tumourigenesis by the Scribble/Dlg/Lgl polarity module. Oncogene 2008;27:6888-907. [99] Pienta KJ, Coffey DS. Cell motility as a chemotherapeutic target. Cancer Surv 1991;11:255-63. |
| URI: | http://wrap.warwick.ac.uk/id/eprint/46397 |
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