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Conserved microtubule–actin interactions in cell movement and morphogenesis

Abstract

Interactions between microtubules and actin are a basic phenomenon that underlies many fundamental processes in which dynamic cellular asymmetries need to be established and maintained. These are processes as diverse as cell motility, neuronal pathfinding, cellular wound healing, cell division and cortical flow. Microtubules and actin exhibit two mechanistic classes of interactions — regulatory and structural. These interactions comprise at least three conserved 'mechanochemical activity modules' that perform similar roles in these diverse cell functions.

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Figure 1: Regulatory and structural interactions between microtubules and actin.
Figure 2: Models for microtubule–actin interactions.
Figure 3: Comparison of microtubule–actin interactions in various systems.
Figure 4: Conserved microtubule–actin interaction 'activity modules'.

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References

  1. Vasiliev, J.M. et al. Effect of colcemid on the locomotory behaviour of fibroblasts. J. Embryol. Exp. Morphol. 24, 625–640 (1970).

    CAS  PubMed  Google Scholar 

  2. Ingber, D.E. Tensegrity II. How structural networks influence cellular information processing networks. J. Cell Sci. 116, 1397–1408 (2003).

    Article  CAS  PubMed  Google Scholar 

  3. Ingber, D.E. Tensegrity I. Cell structure and hierarchical systems biology. J. Cell Sci. 116, 1157–1173 (2003).

    Article  CAS  PubMed  Google Scholar 

  4. Wittmann, T. & Waterman-Storer, C.M. Cell motility: can Rho GTPases and microtubules point the way? J. Cell Sci. 114, 3795–3803 (2001).

    CAS  PubMed  Google Scholar 

  5. Etienne-Manneville, S. & Hall, A. Rho GTPases in cell biology. Nature 420, 629–635 (2002).

    Article  CAS  PubMed  Google Scholar 

  6. Cook, T.A., Nagasaki, T. & Gundersen, G.G. Rho guanosine triphosphatase mediates the selective stabilization of microtubules induced by lysophosphatidic acid. J. Cell Biol. 141, 175–185 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Ridley, A.J. Rho GTPases and cell migration. J. Cell Sci. 114, 2713–2722 (2001).

    CAS  PubMed  Google Scholar 

  8. Pruyne, D. et al. Role of formins in actin assembly: nucleation and barbed-end association. Science 297, 612–615 (2002).

    Article  CAS  PubMed  Google Scholar 

  9. Sagot, I., Rodal, A.A., Moseley, J., Goode, B.L. & Pellman, D. An actin nucleation mechanism mediated by Bni1 and profilin. Nature Cell Biol. 4, 626–631 (2002).

    Article  CAS  PubMed  Google Scholar 

  10. Palazzo, A.F., Cook, T.A., Alberts, A.S. & Gundersen, G.G. mDia mediates Rho-regulated formation and orientation of stable microtubules. Nature Cell Biol. 3, 723–729 (2001).

    Article  CAS  PubMed  Google Scholar 

  11. Small, J.V., Stradal, T., Vignal, E. & Rottner, K. The lamellipodium: where motility begins. Trends Cell Biol. 12, 112–120 (2002).

    Article  CAS  PubMed  Google Scholar 

  12. Wittmann, T., Bokoch, G.M. & Waterman-Storer, C. Regulation of leading edge microtubule and actin dynamics downstream of Rac1. J. Cell Biol. 161, 845–851 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. 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. 276, 1677–1680 (2001).

    Article  CAS  PubMed  Google Scholar 

  14. Ren, X.D., Kiosses, W.B. & Schwartz, M.A. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 18, 578–585 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Waterman-Storer, C.M., Worthylake, R.A., Liu, B.P., Burridge, K. & Salmon, E.D. Microtubule growth activates Rac1 to promote lamellipodial protrusion in fibroblasts. Nature Cell Biol. 1, 45–50 (1999).

    Article  CAS  PubMed  Google Scholar 

  16. Krendel, M., Zenke, F.T. & Bokoch, G.M. Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nature Cell Biol. 4, 294–301 (2002).

    Article  CAS  PubMed  Google Scholar 

  17. Waterman-Storer, C. et al. Microtubules remodel actomyosin networks in Xenopus egg extracts via two mechanisms of F-actin transport. J. Cell Biol. 150, 361–376 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Leung, C.L., Green, K.J. & Liem, R.K. Plakins: a family of versatile cytolinker proteins. Trends Cell Biol. 12, 37–45 (2002).

    Article  CAS  PubMed  Google Scholar 

  19. Wiche, G. Role of plectin in cytoskeleton organization and dynamics. J. Cell Sci. 111, 2477–2486 (1998).

    CAS  PubMed  Google Scholar 

  20. Salmon, W.C., Adams, M.C., & Waterman-Storer, C.M. Dual-wavelength fluorescent speckle microscopy reveals coupling of microtubule and actin movements in migrating cells. J. Cell Biol. 158, 31–37 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Schaefer, A.W., Kabir, N., & Forscher, P. Filopodia and actin arcs guide the assembly and transport of two populations of microtubules with unique dynamic parameters in neuronal growth cones. J. Cell Biol. 158, 139–152 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Mandato, C.A., Weber, K.L., Zandy, A.J., Keating, T.J., & Bement, W.M. Xenopus egg extracts as a model system for analysis of microtubule, actin filament, and intermediate filament interactions. Methods Mol. Biol. 161, 229–239 (2001).

    CAS  PubMed  Google Scholar 

  23. Mandato, C.A. & Bement, W.M. Actomyosin transports microtubules while microtubules control actomyosin recruitment during Xenopus oocyte wound healing. Curr. Biol. (in the press).

  24. Cramer, L.P. Organization and polarity of actin filament networks in cells: implications for the mechanism of myosin-based cell motility. Biochem. Soc. Symp. 65, 173–205 (1999).

    CAS  PubMed  Google Scholar 

  25. Cramer, L.P., Siebert, M. & Mitchison, T.J. Identification of novel graded polarity actin filament bundles in locomoting heart fibroblasts: implications for the generation of motile force. J. Cell Biol. 136, 1287–1305 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Gupton, S.L., Salmon, W.C. & Waterman-Storer, C. Converging populations of f-actin promote breakage of associated microtubules to spatially regulate microtubule turnover in migrating cells. Curr. Biol. 12, 1891–1899 (2002).

    Article  CAS  PubMed  Google Scholar 

  27. Webb, D.J., Parsons, J.T. & Horwitz, A.F. Adhesion assembly, disassembly and turnover in migrating cells — over and over and over again. Nature Cell Biol. 4, E97–E100 (2002).

    Article  CAS  PubMed  Google Scholar 

  28. Waterman-Storer, C.M. & Salmon, E.D. 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. 139, 417–434 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Yvon, A.M. & Wadsworth, P. Region-specific microtubule transport in motile cells. J. Cell Biol. 151, 1003–1012 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Mikhailov, A.V. & Gundersen, G.G. Centripetal transport of microtubules in motile cells. Cell Motil. Cytoskeleton 32, 173–186 (1995).

    Article  CAS  PubMed  Google Scholar 

  31. Wadsworth, P. Regional regulation of microtubule dynamics in polarized, motile cells. Cell Motil. Cytoskeleton 42, 48–59 (1999).

    Article  CAS  PubMed  Google Scholar 

  32. Kraynov, V.S. et al. Localized Rac activation dynamics visualized in living cells. Science 290, 333–337 (2000).

    Article  CAS  PubMed  Google Scholar 

  33. Itoh, R.E. et al. Activation of rac and cdc42 video imaged by fluorescent resonance energy transfer-based single-molecule probes in the membrane of living cells. Mol. Cell Biol. 22, 6582–6591 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Barth, A.I. & Nelson, W.J. What can humans learn from flies about adenomatous polyposis coli? Bioessays 24, 771–774 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Nathke, M. et al. The adenomatous polyposis coli tumor suppressor protein localizes to plasma membrane sites involved in active cell migration. J. Cell Biol. 134, 165–179 (1996).

    Article  CAS  PubMed  Google Scholar 

  36. Kawasaki, Y. et al. Asef, a link between the tumor suppressor APC and G-protein signaling. Science 289, 1194–1197 (2000).

    Article  CAS  PubMed  Google Scholar 

  37. Kawasaki, Y., Sato, R. & Akiyama, T. Mutated APC and Asef are involved in the migration of colorectal tumour cells. Nature Cell Biol. 5, 211–215 (2003).

    Article  CAS  PubMed  Google Scholar 

  38. Fukata, M. et al. Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell 109, 873–885 (2002).

    Article  CAS  PubMed  Google Scholar 

  39. Gundersen, G.G. Evolutionary conservation of microtubule-capture mechanisms. Nature Rev. Mol. Cell Biol. 3, 296–304 (2002).

    Article  CAS  Google Scholar 

  40. Palazzo, A.F. et al. Cdc42, dynein, and dynactin regulate MTOC reorientation independent of Rho-regulated microtubule stabilization. Curr. Biol. 11, 1536–1541 (2001).

    Article  CAS  PubMed  Google Scholar 

  41. Etienne-Manneville, S. & Hall, A. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106, 489–498 (2001).

    Article  CAS  PubMed  Google Scholar 

  42. Hwang, E., Kusch, J., Barral, Y. & Huffaker, T.C. Spindle orientation in Saccharomyces cerevisiae depends on the transport of microtubule ends along polarized actin cables. J. Cell Biol. 161, 483–488 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Yarm, F., Sagot, I. & Pellman, D. The social life of actin and microtubules: interaction versus cooperation. Curr. Opin. Microbiol. 4, 696–702 (2001).

    Article  CAS  PubMed  Google Scholar 

  44. Barth, A.I., Siemers, K.A. & Nelson, W.J. Dissecting interactions between EB1, microtubules and APC in cortical clusters at the plasma membrane. J. Cell Sci. 115, 1583–1590 (2002).

    CAS  PubMed  Google Scholar 

  45. Mimori-Kiyosue, Y., Shiina, N. & Tsukita, S. Adenomatous polyposis coli (APC) protein moves along microtubules and concentrates at their growing ends in epithelial cells. J. Cell Biol. 148, 505–518 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Ligon, L.A., Karki, S., Tokito, M. & Holzbaur, E.L. Dynein binds to beta-catenin and may tether microtubules at adherens junctions. Nature Cell Biol. 3, 913–917 (2001).

    Article  CAS  PubMed  Google Scholar 

  47. Kaverina, I., Rottner, K. & Small, J.V. Targeting, capture, and stabilization of microtubules at early focal adhesions. J. Cell Biol. 142, 181–190 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Kaverina, I., Krylyshkina, O. & Small, J.V. Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J. Cell Biol. 146, 1033–1044 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Krylyshkina, O. et al. Nanometer targeting of microtubules to focal adhesions. J. Cell Biol. 161, 853–859 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Krylyshkina, O. et al. Modulation of substrate adhesion dynamics via microtubule targeting requires kinesin-1. J. Cell Biol. 156, 349–359 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Bentley, D. & Toroian-Raymond, A. Disoriented pathfinding by pioneer neuron growth cones deprived of filopodia by cytochalasin treatment. Nature 323, 712–715 (1986).

    Article  CAS  PubMed  Google Scholar 

  52. Marsh, L. & Letourneau, P.C. Growth of neurites without filopodial or lamellipodial activity in the presence of cytochalasin B. J. Cell Biol. 99, 2041–2047 (1984).

    Article  CAS  PubMed  Google Scholar 

  53. Tanaka, E., Ho, T. & Kirschner, M.W. The role of microtubule dynamics in growth cone motility and axonal growth. J. Cell Biol. 128, 139–155 (1995).

    Article  CAS  PubMed  Google Scholar 

  54. Suter, D.M. & Forscher, P. An emerging link between cytoskeletal dynamics and cell adhesion molecules in growth cone guidance. Curr. Opin. Neurobiol. 8, 106–116 (1998).

    Article  CAS  PubMed  Google Scholar 

  55. Forscher, P. & Smith, S.J. Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J. Cell Biol. 107, 1505–1516 (1988).

    Article  CAS  PubMed  Google Scholar 

  56. Kabir, N., Schaefer, A.W., Nakhost, A., Sossin, W.S. & Forscher, P. Protein kinase C activation promotes microtubule advance in neuronal growth cones by increasing average microtubule growth lifetimes. J. Cell Biol. 152, 1033–1044 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Zhou, F.Q., Waterman-Storer, C.M. & Cohan, C.S. Focal loss of actin bundles causes microtubule redistribution and growth cone turning. J. Cell Biol. 157, 839–849 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Buck, K.B. & Zheng, J.Q. Growth cone turning induced by direct local modification of microtubule dynamics. J. Neurosci. 22, 9358–9367 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Dent, E.W. & Kalil, K. Axon branching requires interactions between dynamic microtubules and actin filaments. J. Neurosci. 21, 9757–9769 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Griffith, L.M. & Pollard, T.D. The interaction of actin filaments with microtubules and microtubule- associated proteins. J. Biol.Chem. 257, 9143–9151 (1982).

    CAS  PubMed  Google Scholar 

  61. Ozer, R.S. & Halpain, S. Phosphorylation-dependent localization of microtubule-associated protein MAP2c to the actin cytoskeleton. Mol. Biol. Cell 11, 3573–3587 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Lee, S. & Kolodziej, P.A. Short Stop provides an essential link between F-actin and microtubules during axon extension. Development 129, 1195–1204 (2002).

    Article  CAS  PubMed  Google Scholar 

  63. McNeil, P.L. & Terasaki, M. Coping with the inevitable: how cells repair a torn surface membrane. Nature Cell Biol. 3, E124–E129 (2001).

    Article  CAS  PubMed  Google Scholar 

  64. Merriam, R.W. & Christensen, K. A contractile ring-like mechanism in wound healing and soluble factors affecting structural stability in the cortex of Xenopus eggs and oocytes. J. Embryol. Exp. Morphol. 75, 11–20 (1983).

    CAS  PubMed  Google Scholar 

  65. Bement, W.M., Mandato, C.A. & Kirsch, M.N. Wound-induced assembly and closure of an actomyosin purse string in Xenopus oocytes. Curr. Biol. 9, 579–587 (1999).

    Article  CAS  PubMed  Google Scholar 

  66. Mandato, C.A. & Bement, W.M. Contraction and polymerization cooperate to assemble and close actomyosin rings around Xenopus oocyte wounds. J. Cell Biol. 154, 785–797 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Mandato, C.A. & Bement, W.M. Transport and polymerization interactions between microtubules and F-actin during Xenopus oocyte wound healing. Mol. Biol. Cell 13, 333a (2002).

    Google Scholar 

  68. Benink, H.A. & Bement, W.M. Concentric rings of rho, rac and Cdc42 activity encircle oocyte wounds. Mol. Biol. Cell 13, 36a (2002).

    Google Scholar 

  69. Silverman-Gavrila, R.V. & Forer, A. Evidence that actin and myosin are involved in the poleward flux of tubulin in metaphase kinetochore microtubules of crane-fly spermatocytes. J. Cell Sci. 113, 597–609 (2000).

    CAS  PubMed  Google Scholar 

  70. Lutz, D.A., Hamaguchi, Y. & Inoue, S. Micromanipulation studies of the asymmetric positioning of the maturation spindle in Chaetopterus sp. oocytes: I. Anchorage of the spindle to the cortex and migration of a displaced spindle. Cell Motil. Cytoskeleton 11, 83–96 (1988).

    Article  CAS  PubMed  Google Scholar 

  71. Skop, A.R. & White, J.G. The dynactin complex is required for cleavage plane specification in early Caenorhabditis elegans embryos. Curr. Biol. 8, 1110–1116 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Gonczy, P., Pichler, S., Kirkham, M. & Hyman, A.A. Cytoplasmic dynein is required for distinct aspects of MTOC positioning, including centrosome separation, in the one cell stage Caenorhabditis elegans embryo. J. Cell Biol. 147, 135–150 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Hyman, A.A. & White, J.G. Determination of cell division axes in the early embryogenesis of Caenorhabditis elegans. J. Cell Biol. 105, 2123–2135 (1987).

    Article  CAS  PubMed  Google Scholar 

  74. McCartney, B.M. et al. Drosophila APC2 and Armadillo participate in tethering mitotic spindles to cortical actin. Nature Cell Biol. 3, 933–938 (2001).

    Article  CAS  PubMed  Google Scholar 

  75. Hiramoto, Y. Cell division without mitotic apparatus in sea urchin eggs. Exp. Cell Res. 11, 630–636 (1956).

    Article  CAS  PubMed  Google Scholar 

  76. Canman, J.C., Hoffman, D.B. & Salmon, E.D. The role of pre- and post-anaphase microtubules in the cytokinesis phase of the cell cycle. Curr. Biol. 10, 611–614 (2000).

    Article  CAS  PubMed  Google Scholar 

  77. Shuster, C.B. & Burgess, D.R. Transitions regulating the timing of cytokinesis in embryonic cells. Curr. Biol. 12, 854–858 (2002).

    Article  CAS  PubMed  Google Scholar 

  78. Glotzer, M. Animal cell cytokinesis. Annu. Rev. Cell Dev. Biol. 17, 351–386 (2001).

    Article  CAS  PubMed  Google Scholar 

  79. Sider, J.R. et al. Direct observation of microtubule–F-actin interaction in cell free lysates. J. Cell Sci. 112, 1947–1956 (1999).

    CAS  PubMed  Google Scholar 

  80. Foe, V.E., Field, C.M. & Odell, G.M. Microtubules and mitotic cycle phase modulate spatiotemporal distributions of F-actin and myosin II in Drosophila syncytial blastoderm embryos. Development 127, 1767–1787 (2000).

    CAS  PubMed  Google Scholar 

  81. Mandato, C.A., Benink, H.A. & Bement, W.M. Microtubule-actomyosin interactions in cortical flow and cytokinesis. Cell Motil. Cytoskeleton 45, 87–92 (2000).

    Article  CAS  PubMed  Google Scholar 

  82. Sisson, J.C., Field, C., Ventura, R., Royou, A. & Sullivan, W. Lava lamp, a novel peripheral Golgi protein, is required for Drosophila melanogaster cellularization. J. Cell Biol. 151, 905–918 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Oegema, K., Savoian, M.S., Mitchison, T.J. & Field, C.M. Functional analysis of a human homologue of the Drosophila actin binding protein anillin suggests a role in cytokinesis. J. Cell Biol. 150, 539–552 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Surka, M.C., Tsang, C.W. & Trimble, W.S. The mammalian septin MSF localizes with microtubules and is required for completion of cytokinesis. Mol. Biol. Cell 13, 3532–3545 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Giansanti, M.G. et al. Cooperative interactions between the central spindle and the contractile ring during Drosophila cytokinesis. Genes Dev. 12, 396–410 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Cimini, D., Fioravanti, D., Tanzarella, C. & Degrassi, F. Simultaneous inhibition of contractile ring and central spindle formation in mammalian cells treated with cytochalasin B. Chromosoma 107, 479–485 (1998).

    Article  CAS  PubMed  Google Scholar 

  87. Somma, M.P., Fasulo, B., Cenci, G., Cundari, E. & Gatti, M. Molecular dissection of cytokinesis by RNA interference in Drosophila cultured cells. Mol. Biol. Cell 13, 2448–2460 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Dechant, R. & Glotzer, M. Centrosome separation and central spindle assembly act in redundant pathways that regulate microtubule density and trigger cleavage furrow formation. Dev. Cell 4, 333–344 (2003).

    Article  CAS  PubMed  Google Scholar 

  89. Somers, W.G. & Saint, R. A RhoGEF and Rho Family GTPase-Activating Protein Complex Links the Contractile Ring to Cortical Microtubules at the Onset of Cytokinesis. Dev. Cell 4, 29–39 (2003).

    Article  CAS  PubMed  Google Scholar 

  90. Adams, R.R., Tavares, A.A., Salzberg, A., Bellen, H.J. & Glover, D.M. pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for cytokinesis. Genes Dev. 12, 1483–1494 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Murata-Hori, M. & Wang, Y.L. Both midzone and astral microtubules are involved in the delivery of cytokinesis signals: insights from the mobility of aurora B. J. Cell Biol. 159, 45–53 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Kuriyama, R., Gustus, C., Terada, Y., Uetake, Y. & Matuliene, J. CHO1, a mammalian kinesin-like protein, interacts with F-actin and is involved in the terminal phase of cytokinesis. J. Cell Biol. 156, 783–790 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Hird, S.N. & White, J.G. Cortical and cytoplasmic flow polarity in early embryonic cells of Caenorhabditis elegans. J. Cell Biol. 121, 1343–1355 (1993).

    Article  CAS  PubMed  Google Scholar 

  94. O'Connell, K.F., Maxwell, K.N. & White, J.G. The spd-2 gene is required for polarization of the anteroposterior axis and formation of the sperm asters in the Caenorhabditis elegans zygote. Dev. Biol. 222, 55–70 (2000).

    Article  CAS  PubMed  Google Scholar 

  95. Wallenfang, M.R. & Seydoux, G. Polarization of the anterior-posterior axis of C. elegans is a microtubule-directed process. Nature 408, 89–92 (2000).

    Article  CAS  PubMed  Google Scholar 

  96. Canman, J.C. & Bement, W.M. Microtubules suppress actomyosin-based cortical flow in Xenopus oocytes. J. Cell Sci. 110, 1907–1917 (1997).

    CAS  PubMed  Google Scholar 

  97. Benink, H.A., Mandato, C.A. & Bement, W.M. Analysis of cortical flow models in vivo. Mol. Biol. Cell 11, 2553–2563 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Dujardin, D.L. & Vallee, R.B. Dynein at the cortex. Curr. Opin. Cell Biol. 14, 44–49 (2002).

    Article  CAS  PubMed  Google Scholar 

  99. Stowers, L., Yelon, D., Berg, L.J. & Chant, J. Regulation of the polarization of T cells toward antigen-presenting cells by Ras-related GTPase CDC42. Proc. Natl Acad. Sci. USA 92, 5027–5031 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. O'Brien, L.E., Zegers, M.M. & Mostov, K.E. Opinion: Building epithelial architecture: insights from three- dimensional culture models. Nature Rev. Mol. Cell Biol. 3, 531–537 (2002).

    Article  CAS  Google Scholar 

  101. Goode, B.L. et al. Coronin promotes the rapid assembly and cross-linking of actin filaments and may link the actin and microtubule cytoskeletons in yeast. J. Cell Biol. 144, 83–98 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Bashour, A.M., Fullerton, A.T., Hart, M.J. & Bloom, G.S. IQGAP1, a Rac- and Cdc42-binding protein, directly binds and cross- links microfilaments. J. Cell Biol. 137, 1555–1566 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Mateer, S.C. et al. The mechanism for regulation of the F-actin binding activity of IQGAP1 by calcium/calmodulin. J. Biol. Chem. 277, 12324–12333 (2002).

    Article  CAS  PubMed  Google Scholar 

  104. Ruiz-Velasco, R., Lanning, C.C. & Williams, C.L. The activation of Rac1 by M3 muscarinic acetylcholine receptors involves the translocation of Rac1 and IQGAP1 to cell junctions and changes in the composition of protein complexes containing Rac1, IQGAP1, and actin. J. Biol. Chem. 277, 33081–33091 (2002).

    Article  CAS  PubMed  Google Scholar 

  105. Cunningham, C.C. et al. Microtubule-associated protein 2c reorganizes both microtubules and microfilaments into distinct cytological structures in an actin-binding protein-280-deficient melanoma cell line. J. Cell Biol. 136, 845–857 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Gonzalez, M., Cambiazo, V. & Maccioni, R.B. The interaction of Mip-90 with microtubules and actin filaments in human fibroblasts. Exp. Cell Res. 239, 243–253 (1998).

    Article  CAS  PubMed  Google Scholar 

  107. Huang, J.D. et al. Direct interaction of microtubule- and actin-based transport motors. Nature 397, 267–270 (1999).

    Article  CAS  PubMed  Google Scholar 

  108. Lantz, V.A. & Miller, K.G. A class VI unconventional myosin is associated with a homologue of a microtubule-binding protein, cytoplasmic linker protein-170, in neurons and at the posterior pole of Drosophila embryos. J. Cell Biol. 140, 897–910 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Hicks, J.L., Deng, W.M., Rogat, A.D., Miller, K.G. & Bownes, M. Class VI unconventional myosin is required for spermatogenesis in Drosophila. Mol. Biol. Cell 10, 4341–4353 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Goriounov, D., Leung, C.L. & Liem, R.K. Protein products of human Gas2-related genes on chromosomes 17 and 22 (hGAR17 and hGAR22) associate with both microfilaments and microtubules. J. Cell Sci. 116, 1045–1058 (2003).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank J. Canman, G. von Dassow and members of the Waterman-Storer lab for helpful suggestions. C.W.S. is supported by National Institutes of Health (NIH) grant GM61804-03, W.M.B by NIH grant GM52932-04A1 and National Science Foundation (NSF) grant MCB#9630860, P.F. by NIH grant RO1-NS28695, A.W.S. by NIH and O.C.R. by NSF postdoctoral fellowships, respectively.

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Rodriguez, O., Schaefer, A., Mandato, C. et al. Conserved microtubule–actin interactions in cell movement and morphogenesis. Nat Cell Biol 5, 599–609 (2003). https://doi.org/10.1038/ncb0703-599

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