Non-muscle myosin II takes centre stage in cell adhesion and migration (original) (raw)

• Holmes, K. C. in Myosins (ed. Coluccio, L. M.) 35–54 (Springer, The Netherlands, 2007). Provides an in depth survey of selective myosin class members, including NM IIs. See also references 2, 3, 6, 7 and 9.
  Google Scholar
• Mooseker, M. S. & Foth, B. J. in Myosins (ed. Coluccio, L. M.) 1–34 (Springer, The Netherlands, 2007).
  Google Scholar
• El-Mezgueldi, M. & Bagshaw, C. R. in Myosins (ed. Coluccio, L. M.) 55–93 (Springer, The Netherlands, 2007).
  Google Scholar
• Richards, T. A. & Cavalier-Smith, T. Myosin domain evolution and the primary divergence of eukaryotes. Nature 436, 1113–1118 (2005).
  CAS PubMed Google Scholar
• Odronitz, F. & Kollmar, M. Drawing the tree of eukaryotic life based on the analysis of 2,269 manually annotated myosins from 328 species. Genome Biol. 8, R196 (2007).
  PubMed PubMed Central Google Scholar
• Cremo, C. R. & Hartshorne, D. J. in Myosins (ed. Coluccio, L. M.) 171–222 (Springer, The Netherlands, 2007).
  Google Scholar
• Reggiani, C. & Bottinelli, R. in Myosins (ed. Coluccio, L. M.) 125–169 (Springer, The Netherlands, 2007).
  Google Scholar
• Clark, K., Langeslag, M., Figdor, C. G. & van Leeuwen, F. N. Myosin II and mechanotransduction: a balancing act. Trends Cell Biol. 17, 178–186 (2007).
  CAS PubMed Google Scholar
• Conti, M. A., Kawamoto, S. & Adelstein, R. S. in Myosins (ed. Coluccio, L. M.) 223–264 (Springer, The Netherlands, 2007).
  Google Scholar
• Conti, M. A. & Adelstein, R. S. Nonmuscle myosin II moves in new directions. J. Cell Sci. 121, 11–18 (2008).
  CAS PubMed Google Scholar
• Krendel, M. & Mooseker, M. S. Myosins: tails (and heads) of functional diversity. Physiology 20, 239–251 (2005).
  CAS PubMed Google Scholar
• Swailes, N. T., Colegrave, M., Knight, P. J. & Peckham, M. Non-muscle myosins 2A and 2B drive changes in cell morphology that occur as myoblasts align and fuse. J. Cell Sci. 119, 3561–3570 (2006).
  CAS PubMed Google Scholar
• Yuen, S. L., Ogut, O. & Brozovich, F. V. Nonmuscle myosin is regulated during smooth muscle contraction. Am. J. Physiol. Heart Circ. Physiol. 297, H191–H199 (2009).
  CAS PubMed PubMed Central Google Scholar
• Morano, I. et al. Smooth-muscle contraction without smooth-muscle myosin. Nature Cell Biol. 2, 371–375 (2000). The first demonstration that NM II can play a part in smooth muscle contraction. The authors make use of smooth muscle myosin knockout mice to study smooth muscle contraction and show that the sustained phase of contraction is due to NM II. See reference 13 for recent work in this area which suggests that NM IIB might contribute to the smooth muscle 'latch' state.
  CAS PubMed Google Scholar
• Niederman, R. & Pollard, T. D. Human platelet myosin. II. In vitro assembly and structure of myosin filaments. J. Cell Biol. 67, 72–92 (1975).
  CAS PubMed Google Scholar
• Svitkina, T. M., Verkhovsky, A. B. & Borisy, G. G. Improved procedures for electron microscopic visualization of the cytoskeleton of cultured cells. J. Struct. Biol. 115, 290–303 (1995).
  CAS PubMed Google Scholar
• Mansfield, S. G., al-Shirawi, D. Y., Ketchum, A. S., Newbern, E. C. & Kiehart, D. P. Molecular organization and alternative splicing in Zipper, the gene that encodes the Drosophila non-muscle myosin II heavy chain. J. Mol. Biol. 255, 98–109 (1996).
  CAS PubMed Google Scholar
• Jana, S. S. et al. An alternatively spliced isoform of nonmuscle myosin II-C is not regulated by myosin light chain phosphorylation. J. Biol. Chem. 284, 11563–11571 (2009).
  CAS PubMed PubMed Central Google Scholar
• Li, Y., Lalwani, A. K. & Mhatre, A. N. Alternative splice variants of MYH9. DNA Cell Biol. 27, 117–125 (2008).
  CAS PubMed Google Scholar
• Maupin, P., Phillips, C. L., Adelstein, R. S. & Pollard, T. D. Differential localization of myosin-II isozymes in human cultured cells and blood cells. J. Cell Sci. 107, 3077–3090 (1994).
  CAS PubMed Google Scholar
• Kolega, J. Cytoplasmic dynamics of myosin IIA and IIB: spatial 'sorting' of isoforms in locomoting cells. J. Cell Sci. 111, 2085–2095 (1998).
  CAS PubMed Google Scholar
• Vicente-Manzanares, M., Zareno, J., Whitmore, L., Choi, C. K. & Horwitz, A. F. Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells. J. Cell Biol. 176, 573–580 (2007).
  CAS PubMed PubMed Central Google Scholar
• Bao, J., Jana, S. S. & Adelstein, R. S. Vertebrate nonmuscle myosin II isoforms rescue small interfering RNA-induced defects in COS-7 cell cytokinesis. J. Biol. Chem. 280, 19594–19599 (2005).
  CAS PubMed Google Scholar
• Golomb, E. et al. Identification and characterization of nonmuscle myosin II-C, a new member of the myosin II family. J. Biol. Chem. 279, 2800–2808 (2004).
  CAS PubMed Google Scholar
• Kim, K. Y., Kovacs, M., Kawamoto, S., Sellers, J. R. & Adelstein, R. S. Disease-associated mutations and alternative splicing alter the enzymatic and motile activity of nonmuscle myosins II-B and II-C. J. Biol. Chem. 280, 22769–22775 (2005).
  CAS PubMed Google Scholar
• Kovacs, M., Wang, F., Hu, A., Zhang, Y. & Sellers, J. R. Functional divergence of human cytoplasmic myosin II: kinetic characterization of the non-muscle IIA isoform. J. Biol. Chem. 278, 38132–38140 (2003).
  CAS PubMed Google Scholar
• Wang, F. et al. Kinetic mechanism of non-muscle myosin IIB: functional adaptations for tension generation and maintenance. J. Biol. Chem. 278, 27439–27448 (2003). Together with reference 26, this paper details the differences in the kinetic properties of NM IIA and NM IIB. These studies provide a mechanistic framework for understanding the putative in vivo function of two of the three NM II isoforms.
  CAS PubMed Google Scholar
• Kovacs, M., Thirumurugan, K., Knight, P. J. & Sellers, J. R. Load-dependent mechanism of nonmuscle myosin 2. Proc. Natl Acad. Sci. USA 104, 9994–9999 (2007).
  CAS PubMed PubMed Central Google Scholar
• Bao, J., Ma, X., Liu, C. & Adelstein, R. S. Replacement of nonmuscle myosin II-B with II-A rescues brain but not cardiac defects in mice. J. Biol. Chem. 282, 22102–22111 (2007).
  CAS PubMed Google Scholar
• Nakasawa, T. et al. Critical regions for assembly of vertebrate nonmuscle myosin II. Biochemistry 44, 174–183 (2005).
  CAS PubMed Google Scholar
• Sato, M. K., Takahashi, M. & Yazawa, M. Two regions of the tail are necessary for the isoform-specific functions of nonmuscle myosin IIB. Mol. Biol. Cell 18, 1009–1017 (2007).
  CAS PubMed PubMed Central Google Scholar
• Sandquist, J. C. & Means, A. R. The C-terminal tail region of nonmuscle myosin II directs isoform-specific distribution in migrating cells. Mol. Biol. Cell 19, 5156–5167 (2008).
  CAS PubMed PubMed Central Google Scholar
• Vicente-Manzanares, M., Koach, M. A., Whitmore, L., Lamers, M. L. & Horwitz, A. F. Segregation and activation of myosin IIB creates a rear in migrating cells. J. Cell Biol. 183, 543–554 (2008).
  CAS PubMed PubMed Central Google Scholar
• Somlyo, A. P. & Somlyo, A. V. Ca2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol. Rev. 83, 1325–1358 (2003).
  CAS PubMed Google Scholar
• Wendt, T., Taylor, D., Trybus, K. M. & Taylor, K. Three-dimensional image reconstruction of dephosphorylated smooth muscle heavy meromyosin reveals asymmetry in the interaction between myosin heads and placement of subfragment 2. Proc. Natl Acad. Sci. USA 98, 4361–4366 (2001).
  CAS PubMed PubMed Central Google Scholar
• Sellers, J. R., Eisenberg, E. & Adelstein, R. S. The binding of smooth muscle heavy meromyosin to actin in the presence of ATP. Effect of phosphorylation. J. Biol. Chem. 257, 13880–13883 (1982).
  CAS PubMed Google Scholar
• Hirata, N., Takahashi, M. & Yazawa, M. Diphosphorylation of regulatory light chain of myosin IIA is responsible for proper cell spreading. Biochem. Biophys. Res. Commun. 381, 682–687 (2009).
  CAS PubMed Google Scholar
• Ikebe, M., Hartshorne, D. J. & Elzinga, M. Identification, phosphorylation, and dephosphorylation of a second site for myosin light chain kinase on the 20,000-dalton light chain of smooth muscle myosin. J. Biol. Chem. 261, 36–39 (1986).
  CAS PubMed Google Scholar
• Umemoto, S., Bengur, A. R. & Sellers, J. R. Effect of multiple phosphorylations of smooth muscle and cytoplasmic myosins on movement in an in vitro motility assay. J. Biol. Chem. 264, 1431–1436 (1989).
  CAS PubMed Google Scholar
• Scholey, J. M., Taylor, K. A. & Kendrick-Jones, J. Regulation of non-muscle myosin assembly by calmodulin-dependent light chain kinase. Nature 287, 233–235 (1980).
  CAS PubMed Google Scholar
• Woodhead, J. L. et al. Atomic model of a myosin filament in the relaxed state. Nature 436, 1195–1199 (2005).
  CAS PubMed Google Scholar
• Jung, H. S., Komatsu, S., Ikebe, M. & Craig, R. Head–head and head–tail interaction: a general mechanism for switching off myosin II activity in cells. Mol. Biol. Cell 19, 3234–3242 (2008).
  CAS PubMed PubMed Central Google Scholar
• Craig, R. & Woodhead, J. L. Structure and function of myosin filaments. Curr. Opin. Struct. Biol. 16, 204–212 (2006).
  CAS PubMed Google Scholar
• Burgess, S. A. et al. Structures of smooth muscle myosin and heavy meromyosin in the folded, shutdown state. J. Mol. Biol. 372, 1165–1178 (2007). Together with references 35 and 41–43, this is an outstanding structural study that shows the transformation of the folded, blocked (10S) state to the unfolded, activated (6S) state of single NM II molecules following RLC phosphorylation. These studies also show the interaction of the two myosin heads in the inactive state.
  CAS PubMed Google Scholar
• Matsumura, F. Regulation of myosin II during cytokinesis in higher eukaryotes. Trends Cell Biol. 15, 371–377 (2005).
  CAS PubMed Google Scholar
• Tan, I., Yong, J., Dong, J. M., Lim, L. & Leung, T. A tripartite complex containing MRCK modulates lamellar actomyosin retrograde flow. Cell 135, 123–136 (2008).
  CAS PubMed Google Scholar
• Matsumura, F. & Hartshorne, D. J. Myosin phosphatase target subunit: Many roles in cell function. Biochem. Biophys. Res. Commun. 369, 149–156 (2008).
  CAS PubMed Google Scholar
• Totsukawa, G. et al. Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J. Cell Biol. 150, 797–806 (2000).
  CAS PubMed PubMed Central Google Scholar
• Totsukawa, G. et al. Distinct roles of MLCK and ROCK in the regulation of membrane protrusions and focal adhesion dynamics during cell migration of fibroblasts. J. Cell Biol. 164, 427–439 (2004).
  CAS PubMed PubMed Central Google Scholar
• Nishikawa, M., Sellers, J. R., Adelstein, R. S. & Hidaka, H. Protein kinase C modulates in vitro phosphorylation of the smooth muscle heavy meromyosin by myosin light chain kinase. J. Biol. Chem. 259, 8808–8814 (1984).
  CAS PubMed Google Scholar
• Komatsu, S. & Ikebe, M. The phosphorylation of myosin II at the Ser1 and Ser2 is critical for normal platelet-derived growth factor induced reorganization of myosin filaments. Mol. Biol. Cell 18, 5081–5090 (2007).
  CAS PubMed PubMed Central Google Scholar
• Bosgraaf, L. & van Haastert, P. J. The regulation of myosin II in Dictyostelium. Eur. J. Cell Biol. 85, 969–979 (2006).
  CAS PubMed Google Scholar
• Even-Faitelson, L. & Ravid, S. PAK1 and aPKCζ regulate myosin II-B phosphorylation: a novel signaling pathway regulating filament assembly. Mol. Biol. Cell 17, 2869–2881 (2006).
  CAS PubMed PubMed Central Google Scholar
• Dulyaninova, N. G., Malashkevich, V. N., Almo, S. C. & Bresnick, A. R. Regulation of myosin-IIA assembly and Mts1 binding by heavy chain phosphorylation. Biochemistry 44, 6867–6876 (2005).
  CAS PubMed Google Scholar
• Clark, K. et al. TRPM7 regulates myosin IIA filament stability and protein localization by heavy chain phosphorylation. J. Mol. Biol. 378, 790–803 (2008).
  PubMed PubMed Central Google Scholar
• Conti, M. A., Sellers, J. R., Adelstein, R. S. & Elzinga, M. Identification of the serine residue phosphorylated by protein kinase C in vertebrate nonmuscle myosin heavy chains. Biochemistry 30, 966–970 (1991).
  CAS PubMed Google Scholar
• Ludowyke, R. I. et al. Phosphorylation of nonmuscle myosin heavy chain IIA on Ser1917 is mediated by protein kinase C βII and coincides with the onset of stimulated degranulation of RBL-2H3 mast cells. J. Immunol. 177, 1492–1499 (2006).
  CAS PubMed Google Scholar
• Li, Z. H. & Bresnick, A. R. The S100A4 metastasis factor regulates cellular motility via a direct interaction with myosin-IIA. Cancer Res. 66, 5173–5180 (2006).
  CAS PubMed Google Scholar
• Clark, K. et al. The α-kinases TRPM6 and TRPM7, but not eEF-2 kinase, phosphorylate the assembly domain of myosin IIA, IIB and IIC. FEBS Lett. 582, 2993–2997 (2008).
  CAS PubMed Google Scholar
• Ronen, D. & Ravid, S. Myosin II tailpiece determines its paracrystal structure, filament assembly properties, and cellular localization. J. Biol. Chem. 284, 24948–24957 (2009).
  CAS PubMed PubMed Central Google Scholar
• Heath, J. P. & Holifield, B. F. Cell locomotion: new research tests old ideas on membrane and cytoskeletal flow. Cell. Motil. Cytoskeleton 18, 245–257 (1991).
  CAS PubMed Google Scholar
• Pollard, T. D. & Borisy, G. G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453–465 (2003).
  CAS PubMed Google Scholar
• Koestler, S. A., Auinger, S., Vinzenz, M., Rottner, K. & Small, J. V. Differentially oriented populations of actin filaments generated in lamellipodia collaborate in pushing and pausing at the cell front. Nature Cell Biol. 10, 306–313 (2008).
  CAS PubMed Google Scholar
• Ponti, A., Machacek, M., Gupton, S. L., Waterman-Storer, C. M. & Danuser, G. Two distinct actin networks drive the protrusion of migrating cells. Science 305, 1782–1786 (2004). Describes the kinetic and compositional distinction between the lamellipodium and the lamellum — the two actin networks in protrusions.
  CAS PubMed Google Scholar
• Delorme, V. et al. Cofilin activity downstream of Pak1 regulates cell protrusion efficiency by organizing lamellipodium and lamella actin networks. Dev. Cell 13, 646–662 (2007).
  CAS PubMed PubMed Central Google Scholar
• Cai, Y. et al. Nonmuscle myosin IIA-dependent force inhibits cell spreading and drives F-actin flow. Biophys. J. 91, 3907–3920 (2006).
  CAS PubMed PubMed Central Google Scholar
• Giannone, G. et al. Periodic lamellipodial contractions correlate with rearward actin waves. Cell 116, 431–443 (2004).
  CAS PubMed Google Scholar
• Giannone, G. et al. Lamellipodial actin mechanically links myosin activity with adhesion-site formation. Cell 128, 561–575 (2007).
  CAS PubMed PubMed Central Google Scholar
• Anderson, T. W., Vaughan, A. N. & Cramer, L. P. Retrograde flow and myosin II activity within the leading cell edge deliver F-actin to the lamella to seed the formation of graded polarity actomyosin II filament bundles in migrating fibroblasts. Mol. Biol. Cell 19, 5006–5018 (2008).
  CAS PubMed PubMed Central Google Scholar
• Nemethova, M., Auinger, S. & Small, J. V. Building the actin cytoskeleton: filopodia contribute to the construction of contractile bundles in the lamella. J. Cell Biol. 180, 1233–1244 (2008).
  CAS PubMed PubMed Central Google Scholar
• Even-Ram, S. et al. Myosin IIA regulates cell motility and actomyosin-microtubule crosstalk. Nature Cell Biol. 9, 299–309 (2007). Establishes the role of NM IIA in the co-regulation of actin and microtubule functions in motile cells.
  CAS PubMed Google Scholar
• Mitchison, T. & Kirschner, M. Cytoskeletal dynamics and nerve growth. Neuron 1, 761–772 (1988).
  CAS PubMed Google Scholar
• Lin, C. H. & Forscher, P. Growth cone advance is inversely proportional to retrograde F-actin flow. Neuron 14, 763–771 (1995).
  CAS PubMed Google Scholar
• Jay, P. Y., Pham, P. A., Wong, S. A. & Elson, E. L. A mechanical function of myosin II in cell motility. J. Cell Sci. 108, 387–393 (1995).
  CAS PubMed Google Scholar
• Choi, C. K. et al. Actin and α-actinin orchestrate the assembly and maturation of nascent adhesions in a myosin II motor-independent manner. Nature Cell Biol. 10, 1039–1050 (2008).
  CAS PubMed Google Scholar
• Alexandrova, A. Y. et al. Comparative dynamics of retrograde actin flow and focal adhesions: formation of nascent adhesions triggers transition from fast to slow flow. PLoS ONE 3, e3234 (2008).
  PubMed PubMed Central Google Scholar
• Humphries, J. D. et al. Vinculin controls focal adhesion formation by direct interactions with talin and actin. J. Cell Biol. 179, 1043–1057 (2007).
  CAS PubMed PubMed Central Google Scholar
• Sawada, Y. et al. Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 127, 1015–26 (2006).
  CAS PubMed PubMed Central Google Scholar
• del Rio, A. et al. Stretching single talin rod molecules activates vinculin binding. Science 323, 638–641 (2009).
  CAS PubMed Google Scholar
• Friedland, J. C., Lee, M. H. & Boettiger, D. Mechanically activated integrin switch controls α5β1 function. Science 323, 642–644 (2009).
  CAS PubMed Google Scholar
• Jiang, G., Giannone, G., Critchley, D. R., Fukumoto, E. & Sheetz, M. P. Two-piconewton slip bond between fibronectin and the cytoskeleton depends on talin. Nature 424, 334–337 (2003).
  CAS PubMed Google Scholar
• Zhong, C. et al. Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly. J. Cell Biol. 141, 539–551 (1998).
  CAS PubMed PubMed Central Google Scholar
• Schwaiger, I., Sattler, C., Hostetter, D. R. & Rief, M. The myosin coiled-coil is a truly elastic protein structure. Nature Mater. 1, 232–235 (2002).
  CAS Google Scholar
• Schneider, I. C., Hays, C. K. & Waterman, C. M. Epidermal growth factor-induced contraction regulates paxillin phosphorylation to temporally separate traction generation from de-adhesion. Mol. Biol. Cell 20, 3155-3167 (2009).
• Yoshigi, M., Hoffman, L. M., Jensen, C. C., Yost, H. J. & Beckerle, M. C. Mechanical force mobilizes zyxin from focal adhesions to actin filaments and regulates cytoskeletal reinforcement. J. Cell Biol. 171, 209–215 (2005).
  CAS PubMed PubMed Central Google Scholar
• Wang, H. B., Dembo, M., Hanks, S. K. & Wang, Y. Focal adhesion kinase is involved in mechanosensing during fibroblast migration. Proc. Natl Acad. Sci. USA 98, 11295–11300 (2001).
  CAS PubMed PubMed Central Google Scholar
• Galbraith, C. G., Yamada, K. M. & Sheetz, M. P. The relationship between force and focal complex development. J. Cell Biol. 159, 695–705 (2002).
  CAS PubMed PubMed Central Google Scholar
• Chen, C. S. Mechanotransduction — a field pulling together? J. Cell Sci. 121, 3285–3292 (2008).
  CAS PubMed Google Scholar
• Beningo, K. A., Dembo, M., Kaverina, I., Small, J. V. & Wang, Y. L. Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J. Cell Biol. 153, 881–888 (2001).
  CAS PubMed PubMed Central Google Scholar
• Beningo, K. A., Hamao, K., Dembo, M., Wang, Y. L. & Hosoya, H. Traction forces of fibroblasts are regulated by the Rho-dependent kinase but not by the myosin light chain kinase. Arch. Biochem. Biophys. 456, 224–231 (2006).
  CAS PubMed PubMed Central Google Scholar
• Parsons, J. T. Focal adhesion kinase: the first ten years. J. Cell Sci. 116, 1409–1416 (2003).
  CAS PubMed Google Scholar
• Deakin, N. O. & Turner, C. E. Paxillin comes of age. J. Cell Sci. 121, 2435–2444 (2008).
  CAS PubMed Google Scholar
• Mitra, S. K. & Schlaepfer, D. D. Integrin-regulated FAK–Src signaling in normal and cancer cells. Curr. Opin. Cell Biol. 18, 516–523 (2006).
  CAS PubMed Google Scholar
• Geiger, B., Spatz, J. P. & Bershadsky, A. D. Environmental sensing through focal adhesions. Nature Rev. Mol. Cell Biol. 10, 21–33 (2009).
  CAS Google Scholar
• Vicente-Manzanares, M., Choi, C. K. & Horwitz, A. R. Integrins in cell migration — the actin connection. J. Cell Sci. 122, 199–206 (2009).
  CAS PubMed Google Scholar
• Ballestrem, C. et al. Molecular mapping of tyrosine-phosphorylated proteins in focal adhesions using fluorescence resonance energy transfer. J. Cell Sci. 119, 866–875 (2006).
  CAS PubMed Google Scholar
• Smith, A. et al. A talin-dependent LFA-1 focal zone is formed by rapidly migrating T lymphocytes. J. Cell Biol. 170, 141–151 (2005).
  CAS PubMed PubMed Central Google Scholar
• Verkhovsky, A. B., Svitkina, T. M. & Borisy, G. G. Self-polarization and directional motility of cytoplasm. Curr. Biol. 9, 11–20 (1999).
  CAS PubMed Google Scholar
• Yam, P. T. et al. Actin-myosin network reorganization breaks symmetry at the cell rear to spontaneously initiate polarized cell motility. J. Cell Biol. 178, 1207–1221 (2007).
  CAS PubMed PubMed Central Google Scholar
• Mseka, T., Bamburg, J. R. & Cramer, L. P. ADF/cofilin family proteins control formation of oriented actin-filament bundles in the cell body to trigger fibroblast polarization. J. Cell Sci. 120, 4332–4344 (2007).
  CAS PubMed Google Scholar
• Xu, J. et al. Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell 114, 201–214 (2003).
  CAS PubMed Google Scholar
• Ridley, A. J. et al. Cell migration: integrating signals from front to back. Science 302, 1704–1709 (2003).
  CAS PubMed Google Scholar
• Eddy, R. J., Pierini, L. M., Matsumura, F. & Maxfield, F. R. Ca2+-dependent myosin II activation is required for uropod retraction during neutrophil migration. J. Cell Sci. 113, 1287–1298 (2000).
  CAS PubMed Google Scholar
• Kolega, J. Asymmetry in the distribution of free versus cytoskeletal myosin II in locomoting microcapillary endothelial cells. Exp. Cell Res. 231, 66–82 (1997).
  CAS PubMed Google Scholar
• Chrzanowska-Wodnicka, M. & Burridge, K. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133, 1403–1415 (1996). Implicates NM II in trailing edge retraction.
  CAS PubMed Google Scholar
• Worthylake, R. A., Lemoine, S., Watson, J. M. & Burridge, K. RhoA is required for monocyte tail retraction during transendothelial migration. J. Cell Biol. 154, 147–160 (2001).
  CAS PubMed PubMed Central Google Scholar
• Etienne-Manneville, S. & Hall, A. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCζ. Cell 106, 489–498 (2001).
  CAS PubMed Google Scholar
• Gomes, E. R., Jani, S. & Gundersen, G. G. Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 121, 451–463 (2005). Demonstrates the role of NM II in nuclear repositioning during cell migration.
  CAS PubMed Google Scholar
• Lo, C. M. et al. Nonmuscle myosin IIb is involved in the guidance of fibroblast migration. Mol. Biol. Cell 15, 982–989 (2004).
  CAS PubMed PubMed Central Google Scholar
• Warren, D. T., Zhang, Q., Weissberg, P. L. & Shanahan, C. M. Nesprins: intracellular scaffolds that maintain cell architecture and coordinate cell function? Expert Rev. Mol. Med. 7, 1–15 (2005).
  PubMed Google Scholar
• Nery, F. C. et al. TorsinA binds the KASH domain of nesprins and participates in linkage between nuclear envelope and cytoskeleton. J. Cell Sci. 121, 3476–3486 (2008).
  CAS PubMed Google Scholar
• Shewan, A. M. et al. Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. Mol. Biol. Cell 16, 4531–4542 (2005).
  CAS PubMed PubMed Central Google Scholar
• Ivanov, A. I. et al. A unique role for nonmuscle myosin heavy chain IIA in regulation of epithelial apical junctions. PLoS ONE 2, e658 (2007).
  PubMed PubMed Central Google Scholar
• Yamada, S. & Nelson, W. J. Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. J. Cell Biol. 178, 517–527 (2007).
  CAS PubMed PubMed Central Google Scholar
• Carmona-Fontaine, C. et al. Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature 456, 957–961 (2008).
  CAS PubMed PubMed Central Google Scholar
• Ilani, T., Vasiliver-Shamis, G., Vardhana, S., Bretscher, A. & Dustin, M. L. T cell antigen receptor signaling and immunological synapse stability require myosin IIA. Nature Immunol. 10, 531–539 (2009).
  CAS Google Scholar
• Young, P. E., Richman, A. M., Ketchum, A. S. & Kiehart, D. P. Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev. 7, 29–41 (1993).
  CAS PubMed Google Scholar
• Karess, R. E. et al. The regulatory light chain of nonmuscle myosin is encoded by spaghetti-squash, a gene required for cytokinesis in Drosophila. Cell 65, 1177–1189 (1991).
  CAS PubMed Google Scholar
• Winter, C. G. et al. Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105, 81–91 (2001).
  CAS PubMed Google Scholar
• Skoglund, P., Rolo, A., Chen, X., Gumbiner, B. M. & Keller, R. Convergence and extension at gastrulation require a myosin IIB-dependent cortical actin network. Development 135, 2435–2444 (2008).
  CAS PubMed Google Scholar
• Brodu, V. & Casanova, J. The RhoGAP crossveinless-c links trachealess and EGFR signaling to cell shape remodeling in Drosophila tracheal invagination. Genes Dev. 20, 1817–1828 (2006).
  CAS PubMed PubMed Central Google Scholar
• Myat, M. M. Making tubes in the Drosophila embryo. Dev. Dyn. 232, 617–632 (2005).
  CAS PubMed Google Scholar
• Barrett, K., Leptin, M. & Settleman, J. The Rho GTPase and a putative RhoGEF mediate a signaling pathway for the cell shape changes in Drosophila gastrulation. Cell 91, 905–915 (1997).
  CAS PubMed Google Scholar
• Pilot, F. & Lecuit, T. Compartmentalized morphogenesis in epithelia: from cell to tissue shape. Dev. Dyn. 232, 685–694 (2005).
  CAS PubMed Google Scholar
• Rolo, A., Skoglund, P. & Keller, R. Morphogenetic movements driving neural tube closure in Xenopus require myosin IIB. Dev. Biol. 327, 327–338 (2009).
  CAS PubMed Google Scholar
• Hildebrand, J. D. & Soriano, P. Shroom, a PDZ domain-containing actin-binding protein, is required for neural tube morphogenesis in mice. Cell 99, 485–497 (1999).
  CAS PubMed Google Scholar
• Bertet, C., Sulak, L. & Lecuit, T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429, 667–671 (2004).
  CAS PubMed Google Scholar
• Yamamoto, N., Okano, T., Ma, X., Adelstein, R. S. & Kelley, M. W. Myosin II regulates extension, growth and patterning in the mammalian cochlear duct. Development 136, 1977–1986 (2009).
  CAS PubMed PubMed Central Google Scholar
• Corrigall, D., Walther, R. F., Rodriguez, L., Fichelson, P. & Pichaud, F. Hedgehog signaling is a principal inducer of Myosin-II-driven cell ingression in Drosophila epithelia. Dev. Cell 13, 730–742 (2007).
  CAS PubMed Google Scholar
• Meshel, A. S., Wei, Q., Adelstein, R. S. & Sheetz, M. P. Basic mechanism of three-dimensional collagen fibre transport by fibroblasts. Nature Cell Biol. 7, 157–164 (2005).
  CAS PubMed Google Scholar
• Zhang, Q., Magnusson, M. K. & Mosher, D. F. Lysophosphatidic acid and microtubule-destabilizing agents stimulate fibronectin matrix assembly through Rho-dependent actin stress fiber formation and cell contraction. Mol. Biol. Cell 8, 1415–1425 (1997).
  CAS PubMed PubMed Central Google Scholar
• Dzamba, B. J., Jakab, K. R., Marsden, M., Schwartz, M. A. & DeSimone, D. W. Cadherin adhesion, tissue tension, and noncanonical Wnt signaling regulate fibronectin matrix organization. Dev. Cell 16, 421–432 (2009).
  CAS PubMed PubMed Central Google Scholar
• Conti, M. A., Even-Ram, S., Liu, C., Yamada, K. M. & Adelstein, R. S. Defects in cell adhesion and the visceral endoderm following ablation of nonmuscle myosin heavy chain II-A in mice. J. Biol. Chem. 279, 41263–41266 (2004).
  CAS PubMed Google Scholar
• Tullio, A. N. et al. Nonmuscle myosin II-B is required for normal development of the mouse heart. Proc. Natl Acad. Sci. USA 94, 12407–12412 (1997).
  CAS PubMed PubMed Central Google Scholar
• Tullio, A. N. et al. Structural abnormalities develop in the brain after ablation of the gene encoding nonmuscle myosin II-B heavy chain. J. Comp. Neurol. 433, 62–74 (2001).
  CAS PubMed Google Scholar
• Burt, R. A., Joseph, J. E., Milliken, S., Collinge, J. E. & Kile, B. T. Description of a novel mutation leading to _MYH9_-related disease. Thromb. Res. 122, 861–863 (2008).
  CAS PubMed Google Scholar
• Canobbio, I. et al. Altered cytoskeleton organization in platelets from patients with _MYH9_-related disease. J. Thromb. Haemost. 3, 1026–1035 (2005).
  CAS PubMed Google Scholar
• Johnson, G. J., Leis, L. A., Krumwiede, M. D. & White, J. G. The critical role of myosin IIA in platelet internal contraction. J. Thromb. Haemost. 5, 1516–1529 (2007).
  CAS PubMed Google Scholar
• Calaminus, S. D. et al. MyosinIIa contractility is required for maintenance of platelet structure during spreading on collagen and contributes to thrombus stability. J. Thromb. Haemost. 5, 2136–2145 (2007).
  CAS PubMed Google Scholar
• Hu, A., Wang, F. & Sellers, J. R. Mutations in human nonmuscle myosin IIA found in patients with May-Hegglin anomaly and Fechtner syndrome result in impaired enzymatic function. J. Biol. Chem. 277, 46512–46517 (2002).
  CAS PubMed Google Scholar
• Kunishima, S., Hamaguchi, M. & Saito, H. Differential expression of wild-type and mutant NMMHC-IIA polypeptides in blood cells suggests cell-specific regulation mechanisms in MYH9 disorders. Blood 111, 3015–3023 (2008).
  CAS PubMed Google Scholar
• Pecci, A. et al. Pathogenetic mechanisms of hematological abnormalities of patients with MYH9 mutations. Hum. Mol. Genet. 14, 3169–3178 (2005). This study analyses 11 patients from 6 families, with 6 different NM IIA mutations, and provides evidence that defects in the megakaryocytic lineage arise from haploinsufficiency of NM IIA, whereas the inclusion bodies in granulocytes are due to the mutant form of NM IIA interfering with the wild-type form.
  CAS PubMed Google Scholar
• Leon, C. et al. Megakaryocyte-restricted MYH9 inactivation dramatically affects hemostasis while preserving platelet aggregation and secretion. Blood 110, 3183–3191 (2007).
  CAS PubMed Google Scholar
• Eckly, A. et al. Abnormal megakaryocyte morphology and proplatelet formation in mice with megakaryocyte-restricted MYH9 inactivation. Blood 113, 3182–3189 (2008).
  PubMed Google Scholar
• Ma, X., Kawamoto, S., Hara, Y. & Adelstein, R. S. A point mutation in the motor domain of nonmuscle myosin II-B impairs migration of distinct groups of neurons. Mol. Biol. Cell 15, 2568–2579 (2004).
  CAS PubMed PubMed Central Google Scholar
• Cantrell, J. R., Haller, J. A. & Ravitch, M. M. A syndrome of congenital defects involving the abdominal wall, sternum, diaphragm, pericardium, and heart. Surg. Gynecol. Obstet. 107, 602–614 (1958).
  CAS PubMed Google Scholar
• Ma, X., Bao, J. & Adelstein, R. S. Loss of cell adhesion causes hydrocephalus in nonmuscle myosin II-B-ablated and mutated mice. Mol. Biol. Cell 18, 2305–2312 (2007).
  CAS PubMed PubMed Central Google Scholar
• Donaudy, F. et al. Nonmuscle myosin heavy-chain gene MYH14 is expressed in cochlea and mutated in patients affected by autosomal dominant hearing impairment (DFNA4). Am. J. Hum. Genet. 74, 770–776 (2004).
  CAS PubMed PubMed Central Google Scholar
• Yang, T. et al. Genetic heterogeneity of deafness phenotypes linked to DFNA4. Am. J. Med. Genet. A 139, 9–12 (2005).
  PubMed Google Scholar
• Butcher, D. T., Alliston, T. & Weaver, V. M. A tense situation: forcing tumour progression. Nature Rev. Cancer 9, 108–122 (2009).
  CAS PubMed Google Scholar
• Medeiros, N. A., Burnette, D. T. & Forscher, P. Myosin II functions in actin-bundle turnover in neuronal growth cones. Nature Cell Biol. 8, 215–226 (2006).
  CAS PubMed Google Scholar
• Miyajima, Y. & Kunishima, S. Identification of the first in cis mutations in MYH9 disorder. Eur. J. Haematol. 82, 288–291 (2009).
  CAS PubMed Google Scholar
• Miyazaki, K., Kunishima, S., Fujii, W. & Higashihara, M. Identification of three in-frame deletion mutations in MYH9 disorders suggesting an important hot spot for small rearrangements in MYH9 exon 24. Eur. J. Haematol. 83, 230–234 (2009).
  CAS PubMed Google Scholar
• De Rocco, D. et al. Identification of the first duplication in _MYH9_-related disease: A hot spot for hot unequal crossing-over within exon 24 of the MYH9 gene. Eur. J. Med. Genet. 52, 191–194 (2009).
  PubMed Google Scholar
• Capria, M. et al. Double nucleotidic mutation of the MYH9 gene in a young patient with end-stage renal disease. Nephrol Dial Transplant 19, 249–251 (2004).
  CAS PubMed Google Scholar