Conserved microtubule–actin interactions in cell movement and morphogenesis

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.

[1]  L. Marsh,et al.  Growth of neurites without filopodial or lamellipodial activity in the presence of cytochalasin B , 1984, The Journal of cell biology.

[2]  W. Kiosses,et al.  Regulation of the small GTP‐binding protein Rho by cell adhesion and the cytoskeleton , 1999, The EMBO journal.

[3]  G. Gundersen Evolutionary conservation of microtubule-capture mechanisms , 2002, Nature Reviews Molecular Cell Biology.

[4]  Gary M. Bokoch,et al.  Regulation of leading edge microtubule and actin dynamics downstream of Rac1 , 2003, The Journal of cell biology.

[5]  A. Hyman,et al.  Determination of cell division axes in the early embryogenesis of Caenorhabditis elegans , 1987, The Journal of cell biology.

[6]  D. Ingber Tensegrity II. How structural networks influence cellular information processing networks , 2003, Journal of Cell Science.

[7]  J. Yates,et al.  Coronin Promotes the Rapid Assembly and Cross-linking of Actin Filaments and May Link the Actin and Microtubule Cytoskeletons in Yeast , 1999, The Journal of cell biology.

[8]  James Q. Zheng,et al.  Growth Cone Turning Induced by Direct Local Modification of Microtubule Dynamics , 2002, The Journal of Neuroscience.

[9]  Shoichiro Tsukita,et al.  Adenomatous Polyposis Coli (APC) Protein Moves along Microtubules and Concentrates at Their Growing Ends in Epithelial Cells , 2000, The Journal of cell biology.

[10]  John B. Shoven,et al.  I , Edinburgh Medical and Surgical Journal.

[11]  Keith E. Mostov,et al.  Building epithelial architecture: insights from three-dimensional culture models , 2002, Nature Reviews Molecular Cell Biology.

[12]  D. Burgess,et al.  Transitions Regulating the Timing of Cytokinesis in Embryonic Cells , 2002, Current Biology.

[13]  N. Copeland,et al.  Direct interaction of microtubule- and actin-based transport motors , 1999, Nature.

[14]  R. Merriam,et al.  A contractile ring-like mechanism in wound healing and soluble factors affecting structural stability in the cortex of Xenopus eggs and oocytes. , 1983, Journal of embryology and experimental morphology.

[15]  S. Kuroda,et al.  Rac1 and Cdc42 Capture Microtubules through IQGAP1 and CLIP-170 , 2002, Cell.

[16]  P. Janmey,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 , 1997, The Journal of cell biology.

[17]  R. Vallee,et al.  Dynein at the cortex. , 2002, Current opinion in cell biology.

[18]  J. Canman,et al.  Microtubules suppress actomyosin-based cortical flow in Xenopus oocytes. , 1997, Journal of cell science.

[19]  Carol L. Williams,et al.  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* , 2002, The Journal of Biological Chemistry.

[20]  I. Gelfand,et al.  Effect of colcemid on the locomotory behaviour of fibroblasts. , 1970, Journal of embryology and experimental morphology.

[21]  S. J. Smith,et al.  Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone , 1988, The Journal of cell biology.

[22]  G. Bokoch,et al.  Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton , 2002, Nature Cell Biology.

[23]  Irina Kaverina,et al.  Microtubule Targeting of Substrate Contacts Promotes Their Relaxation and Dissociation , 1999, The Journal of cell biology.

[24]  M. Matsuda,et al.  Activation of Rac and Cdc42 Video Imaged by Fluorescent Resonance Energy Transfer-Based Single-Molecule Probes in the Membrane of Living Cells , 2002, Molecular and Cellular Biology.

[25]  G. Wiche,et al.  Role of plectin in cytoskeleton organization and dynamics. , 1998, Journal of cell science.

[26]  A. Mikhailov,et al.  Centripetal transport of microtubules in motile cells. , 1995, Cell motility and the cytoskeleton.

[27]  T. J. Keating,et al.  Xenopus egg extracts as a model system for analysis of microtubule, actin filament, and intermediate filament interactions. , 2001, Methods in molecular biology.

[28]  S. Karki,et al.  Dynein binds to β-catenin and may tether microtubules at adherens junctions , 2001, Nature Cell Biology.

[29]  A. Yvon,et al.  Region-Specific Microtubule Transport in Motile Cells , 2000, The Journal of cell biology.

[30]  R. J. Finst,et al.  Direct observation of microtubule-f-actin interaction in cell free lysates. , 1999, Journal of cell science.

[31]  A. Shearn,et al.  The ubiquitin ligase Hyperplastic discs negatively regulates hedgehog and decapentaplegic expression by independent mechanisms , 2002, Development.

[32]  J. Small,et al.  Modulation of substrate adhesion dynamics via microtubule targeting requires kinesin-1 , 2002, The Journal of cell biology.

[33]  C. Waterman-Storer,et al.  Cell motility: can Rho GTPases and microtubules point the way? , 2001, Journal of cell science.

[34]  R. Vallee,et al.  Cdc42, dynein, and dynactin regulate MTOC reorientation independent of Rho-regulated microtubule stabilization , 2001, Current Biology.

[35]  G. Bloom,et al.  IQGAP1, a Rac- and Cdc42-binding Protein, Directly Binds and Cross-links Microfilaments , 1997, The Journal of cell biology.

[36]  G. Gundersen,et al.  mDia mediates Rho-regulated formation and orientation of stable microtubules , 2001, Nature Cell Biology.

[37]  R. Maccioni,et al.  The interaction of Mip-90 with microtubules and actin filaments in human fibroblasts. , 1998, Experimental cell research.

[38]  W. Bement,et al.  Actomyosin Transports Microtubules and Microtubules Control Actomyosin Recruitment during Xenopus Oocyte Wound Healing , 2003, Current Biology.

[39]  K. Kalil,et al.  Axon Branching Requires Interactions between Dynamic Microtubules and Actin Filaments , 2001, The Journal of Neuroscience.

[40]  Charles Boone,et al.  Role of Formins in Actin Assembly: Nucleation and Barbed-End Association , 2002, Science.

[41]  T D Pollard,et al.  The interaction of actin filaments with microtubules and microtubule-associated proteins. , 1982, The Journal of biological chemistry.

[42]  D. Ingber Tensegrity I. Cell structure and hierarchical systems biology , 2003, Journal of Cell Science.

[43]  A. Forer,et al.  Evidence that actin and myosin are involved in the poleward flux of tubulin in metaphase kinetochore microtubules of crane-fly spermatocytes. , 2000, Journal of cell science.

[44]  C. Waterman-Storer,et al.  Dual-wavelength fluorescent speckle microscopy reveals coupling of microtubule and actin movements in migrating cells , 2002, The Journal of cell biology.

[45]  John G. White,et al.  The dynactin complex is required for cleavage plane specification in early Caenorhabditis elegans embryos , 1998, Current Biology.

[46]  W. Nelson,et al.  Dissecting interactions between EB1, microtubules and APC in cortical clusters at the plasma membrane. , 2002, Journal of cell science.

[47]  W. Nelson,et al.  What can humans learn from flies about adenomatous polyposis coli? , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[48]  E. Salmon,et al.  The role of pre- and post-anaphase microtubules in the cytokinesis phase of the cell cycle , 2000, Current Biology.

[49]  E. Salmon,et al.  Microtubule growth activates Rac1 to promote lamellipodial protrusion in fibroblasts , 1999, Nature Cell Biology.

[50]  D. Pellman,et al.  The social life of actin and microtubules: interaction versus cooperation. , 2001, Current opinion in microbiology.

[51]  P. Forscher,et al.  An emerging link between cytoskeletal dynamics and cell adhesion molecules in growth cone guidance , 1998, Current Opinion in Neurobiology.

[52]  A. Ridley Rho GTPases and cell migration. , 2001, Journal of cell science.

[53]  J. White,et al.  The spd-2 gene is required for polarization of the anteroposterior axis and formation of the sperm asters in the Caenorhabditis elegans zygote. , 2000, Developmental biology.

[54]  L. Cramer Organization and polarity of actin filament networks in cells: implications for the mechanism of myosin-based cell motility. , 1999, Biochemical Society symposium.

[55]  C. Waterman-Storer,et al.  Converging Populations of F-Actin Promote Breakage of Associated Microtubules to Spatially Regulate Microtubule Turnover in Migrating Cells , 2002, Current Biology.

[56]  Cramer Lp Organization and polarity of actin filament networks in cells: implications for the mechanism of myosin-based cell motility. , 1999 .

[57]  E. Salmon,et al.  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 , 1997, The Journal of cell biology.

[58]  Klemens Rottner,et al.  Targeting, Capture, and Stabilization of Microtubules at Early Focal Adhesions , 1998, The Journal of cell biology.

[59]  J. Chant,et al.  Regulation of the polarization of T cells toward antigen-presenting cells by Ras-related GTPase CDC42. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[60]  M. Glotzer,et al.  Centrosome separation and central spindle assembly act in redundant pathways that regulate microtubule density and trigger cleavage furrow formation. , 2003, Developmental cell.

[61]  Donna J. Webb,et al.  Adhesion assembly, disassembly and turnover in migrating cells – over and over and over again , 2002, Nature Cell Biology.

[62]  M. Kirschner,et al.  The role of microtubule dynamics in growth cone motility and axonal growth , 1995, The Journal of cell biology.

[63]  K. Kinzler,et al.  Asef , a Link Between the Tumor Suppressor APC and G-Protein Signaling , 2022 .

[64]  D. Bentley,et al.  Disoriented pathfinding by pioneer neurone growth cones deprived of filopodia by cytochalasin treatment , 1986, Nature.

[65]  A. Hall,et al.  Rac/Cdc42 and p65PAK Regulate the Microtubule-destabilizing Protein Stathmin through Phosphorylation at Serine 16* , 2001, The Journal of Biological Chemistry.

[66]  R. Liem,et al.  Protein products of human Gas2-related genes on chromosomes 17 and 22 (hGAR17 and hGAR22) associate with both microfilaments and microtubules , 2003, Journal of Cell Science.

[67]  M. Bownes,et al.  Class VI unconventional myosin is required for spermatogenesis in Drosophila. , 1999, Molecular biology of the cell.

[68]  Dietmar J. Manstein,et al.  Nanometer targeting of microtubules to focal adhesions , 2003, The Journal of cell biology.

[69]  W. Trimble,et al.  The mammalian septin MSF localizes with microtubules and is required for completion of cytokinesis. , 2002, Molecular biology of the cell.

[70]  A. W. Schaefer,et al.  Filopodia and actin arcs guide the assembly and transport of two populations of microtubules with unique dynamic parameters in neuronal growth cones , 2002, The Journal of cell biology.

[71]  Seungbok Lee,et al.  Short Stop provides an essential link between F-actin and microtubules during axon extension. , 2002, Development.

[72]  P. Gönczy,et al.  Cytoplasmic Dynein Is Required for Distinct Aspects of Mtoc Positioning, Including Centrosome Separation, in the One Cell Stage Caenorhabditis elegans Embryo , 1999, The Journal of cell biology.

[73]  Y. Barral,et al.  Spindle orientation in Saccharomyces cerevisiae depends on the transport of microtubule ends along polarized actin cables , 2003, The Journal of cell biology.

[74]  E. Salmon,et al.  Microtubules Remodel Actomyosin Networks in Xenopus Egg Extracts via Two Mechanisms of F-Actin Transport , 2000, The Journal of cell biology.

[75]  Yu-Li Wang,et al.  Both midzone and astral microtubules are involved in the delivery of cytokinesis signals , 2002, The Journal of cell biology.

[76]  James Moseley,et al.  An actin nucleation mechanism mediated by Bni1 and Profilin , 2002, Nature Cell Biology.

[77]  W. Bement,et al.  Wound-induced assembly and closure of an actomyosin purse string in Xenopus oocytes , 1999, Current Biology.

[78]  K. Miller,et al.  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 , 1998, The Journal of cell biology.

[79]  S. Halpain,et al.  Phosphorylation-dependent localization of microtubule-associated protein MAP2c to the actin cytoskeleton. , 2000, Molecular biology of the cell.

[80]  A. Hall,et al.  Rho GTPases in cell biology , 2002, Nature.

[81]  M. Glotzer,et al.  Animal cell cytokinesis. , 2001, Annual review of cell and developmental biology.

[82]  M. Peifer,et al.  Drosophila APC2 and Armadillo participate in tethering mitotic spindles to cortical actin , 2001, Nature Cell Biology.

[83]  Timothy J. Mitchison,et al.  Identification of Novel Graded Polarity Actin Filament Bundles in Locomoting Heart Fibroblasts: Implications for the Generation of Motile Force , 1997, The Journal of cell biology.

[84]  H. Benink,et al.  Microtubule-actomyosin interactions in cortical flow and cytokinesis. , 2000, Cell motility and the cytoskeleton.

[85]  C. L. Adams,et al.  The adenomatous polyposis coli tumor suppressor protein localizes to plasma membrane sites involved in active cell migration , 1996, The Journal of cell biology.

[86]  G. Gundersen,et al.  Rho Guanosine Triphosphatase Mediates the Selective Stabilization of Microtubules Induced by Lysophosphatidic Acid , 1998, The Journal of cell biology.

[87]  M. Terasaki,et al.  Coping with the inevitable: how cells repair a torn surface membrane , 2001, Nature Cell Biology.

[88]  K. Hahn,et al.  Localized Rac activation dynamics visualized in living cells. , 2000, Science.

[89]  R. Saint,et al.  A RhoGEF and Rho family GTPase-activating protein complex links the contractile ring to cortical microtubules at the onset of cytokinesis. , 2003, Developmental cell.

[90]  H. Benink,et al.  Analysis of cortical flow models in vivo. , 2000, Molecular biology of the cell.

[91]  E. Cundari,et al.  Molecular dissection of cytokinesis by RNA interference in Drosophila cultured cells. , 2002, Molecular biology of the cell.

[92]  K. Oegema,et al.  Functional Analysis of a Human Homologue of the Drosophila Actin Binding Protein Anillin Suggests a Role in Cytokinesis , 2000, The Journal of cell biology.

[93]  Y. Terada,et al.  CHO1, a mammalian kinesin-like protein, interacts with F-actin and is involved in the terminal phase of cytokinesis , 2002, The Journal of cell biology.

[94]  Steven N. Hird,et al.  Cortical and cytoplasmic flow polarity in early embryonic cells of Caenorhabditis elegans , 1993, The Journal of cell biology.

[95]  Y. Hiramoto Cell division without mitotic apparatus in sea urchin eggs. , 1956, Experimental cell research.

[96]  S. Inoué,et al.  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. , 1988, Cell motility and the cytoskeleton.

[97]  R. Liem,et al.  Plakins: a family of versatile cytolinker proteins. , 2002, Trends in cell biology.

[98]  W. Sullivan,et al.  Lava Lamp, a Novel Peripheral Golgi Protein, Is Required for Drosophila melanogaster Cellularization , 2000, The Journal of cell biology.

[99]  G. Odell,et al.  Microtubules and mitotic cycle phase modulate spatiotemporal distributions of F-actin and myosin II in Drosophila syncytial blastoderm embryos. , 2000, Development.

[100]  P Wadsworth,et al.  Regional regulation of microtubule dynamics in polarized, motile cells. , 1999, Cell motility and the cytoskeleton.

[101]  D. Cimini,et al.  Simultaneous inhibition of contractile ring and central spindle formation in mammalian cells treated with cytochalasin B , 1998, Chromosoma.

[102]  G. Bloom,et al.  The Mechanism for Regulation of the F-actin Binding Activity of IQGAP1 by Calcium/Calmodulin* 210 , 2002, The Journal of Biological Chemistry.

[103]  S. Karki,et al.  Dynein binds to beta-catenin and may tether microtubules at adherens junctions. , 2001, Nature cell biology.

[104]  S. Bonaccorsi,et al.  Cooperative interactions between the central spindle and the contractile ring during Drosophila cytokinesis. , 1998, Genes & development.

[105]  Tetsu Akiyama,et al.  Mutated APC and Asef are involved in the migration of colorectal tumour cells , 2003, Nature Cell Biology.

[106]  Klemens Rottner,et al.  The lamellipodium: where motility begins. , 2002, Trends in cell biology.

[107]  H. Bellen,et al.  pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for cytokinesis. , 1998, Genes & development.

[108]  W. Bement,et al.  Contraction and polymerization cooperate to assemble and close actomyosin rings around Xenopus oocyte wounds , 2001, The Journal of cell biology.

[109]  A. Hall,et al.  Integrin-Mediated Activation of Cdc42 Controls Cell Polarity in Migrating Astrocytes through PKCζ , 2001, Cell.

[110]  P. Janmey,et al.  Microtubule-associated Protein 2 c Reorganizes Both Microtubules and Microfilaments into Distinct Cytological Structures in an Actin-binding Protein-280 – deficient Melanoma Cell Line , 1997 .

[111]  G. Seydoux,et al.  Polarization of the anterior–posterior axis of C. elegans is a microtubule-directed process , 2000, Nature.

[112]  W. Sossin,et al.  Protein Kinase C Activation Promotes Microtubule Advance in Neuronal Growth Cones by Increasing Average Microtubule Growth Lifetimes , 2001, The Journal of cell biology.

[113]  C. Cohan,et al.  Focal loss of actin bundles causes microtubule redistribution and growth cone turning , 2002, The Journal of cell biology.