Supervillin slows cell spreading by facilitating myosin II activation at the cell periphery

Journal of Cell Science

Volumn 120, Issue 21, 2007, Pages 3792-3803

  Takizawa, Norio ^a   Ikebe, Reiko ^a   Ikebe, Mitsuo ^a   Luna, Elizabeth J ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Cell spreading; Cytoskeleton; MLCK; Myosin II; Supervillin

Indexed keywords

1 (5 IODO 1 NAPHTHALENESULFONYL)HEXAHYDRO 1H 1,4 DIAZEPINE; 1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; ADENOSINE TRIPHOSPHATASE; BLEBBISTATIN; ENHANCED GREEN FLUORESCENT PROTEIN; F ACTIN; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN HEAVY CHAIN; MYOSIN II; MYOSIN IIA; MYOSIN IIB; MYOSIN LIGHT CHAIN KINASE; RHO KINASE; SCAFFOLD PROTEIN; SUPERVILLIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CELL SPREADING; CONTROLLED STUDY; MODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE;

ACTINS; ANIMALS; CELL ADHESION; CELL MOVEMENT; CERCOPITHECUS AETHIOPS; COS CELLS; HUMANS; ISOENZYMES; MEMBRANE PROTEINS; MICE; MICROFILAMENT PROTEINS; MYOSIN TYPE II; MYOSIN-LIGHT-CHAIN KINASE; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE;

EID: 36549055594     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.008219     Document Type: Article

References (85)

1. Amano, M., Ito, M., Kimura, K., Fukata, Y., Chihara, K., Nakano, T., Matsuura, Y. and Kaibuchi, K. (1996). Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271, 20246-20249.
2. Bain, J., McLauchlan, H., Elliott, M. and Cohen, P. (2003). The specificities of protein kinase inhibitors: an update. Biochem. J. 371. 199-204.
3. Bao, J., Jana, S. S. and Adelstein. R. S. (2005). Vertebrate nonmuscle myosin II isoforms rescue small interfering RNA-induced defects, in COS-7 cell cytokinesis. J. Biol. Chem. 280, 19594-19599.
4. Beningo, K. A., Hamao, K., Dembo, M., Wang, Y. L. and Hosoya, H. (2006). 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.
5. Betapudi, V., Licate, L. S. and Egelhoff, T. T. (2006). Distinct roles of nonmuscle myosin II isoforms in the regulation of MDA-MB-231 breast cancer cell spreading and migration. Cancer Res. 66, 4725-4733.
6. Blue, E. K., Goeckeler, Z. M., Jin, Y., Hou, L., Dixon, S. A.. Herring, B. P., Wysolmerski, R. B. and Gallagher, P. J. (2002). 220- and 130-kDa MLCKs have distinct tissue distributions and intracellular localization paterns. Am. J. Physiol. Cell Physiol. 282, C451-C460.
7. Bretscher, M. S. (1996). Getting membrane flow and the cytoskeleton to cooperate in moving cells. Cell 87, 601-606.
8. Bridgman, P. C., Dave. S., Asnes, C. F., Tullio, A. N. and Adelstein, R. S. (2001). Myosin IIB is required for growth cone motility. J. Neurosci. 21, 6159-6169.
9. Brown, M. E. and Bridgman, P. C. (2003). Retrograde flow rate is increased in growth cones from myosin IIB knockout mice. J. Cell Sci. 116, 1087-1094.
10. Cai, Y., Biais, N., Giannone, G., Tanase, M., Jiang, G., Hofman, J. M., Wiggins, C. H., Silberzan, P., Buguin, A., Ladoux, B. et al. (2006). Nonmuscle Myosin IIA-dependent force inhibits cell spreading and drives, F-actin flow. Biophys. J. 91, 3907- 3920.
11. Chen, Y., Takizawa, N., Crowley, J. L., Oh, S. W., Gatto, C. L., Kambara, T.. Sato, O., Li, X., Ikebe, M. and Luna, E. J. (2003). F-actin and myosin II binding domains in supervillin. J. Biol. Chem. 278, 46094-46106.
12. Chew, T. L., Wolf, W. A., Gallagher, P. J., Matsumura, F. and Chisholm, R. L. (2002). A fluorescent resonant energy transfer-based biosensor reveals transient and regional myosin light chain kinase activation in lamella and cleavage furrows. J. Cell Biol. 156, 543-553.
13. Choi, O. H., Adelstein, R. S. and Beaven, M. A. (1994). Secretion from rat basophilic RBL-2H3 cells is associated with diphosphorylation of myosin light chains by myosin light chain kinase as well as phosphorylation by protein kinase C. J. Biol. Chem. 269, 536-541.
14. Connell, L. E. and Helfman, D. M. (2006). Myosin light chain kinase plays a role in the regulation of epithelial cell survival. J. Cell Sci. 119, 2269-2281.
15. Cramer, L. P. and Mitchison, T. J. (1995). Myosin is involved in postmitotic cell spreading. J. Cell Biol. 131, 179-199.
16. DeBiasio, R. L., Wang, L.-L., Fisher, G. W. and Taylor, D. L. (1988). The dynamic distribution of fluorescent analogues of actin and myosin in protrusions at the leading edge of migrating Swiss 3T3 fibroblasts. J. Cell Biol. 107, 2631-2645.
17. Dubin-Thaler, B. J., Giannone, G., Döbereiner, H.-G. and Sheetz, M. P. (2004). Nanometer analysis of cell spreading on matrix-coated surfaces reveals two distinct cell states and STEPs. Biophys. J. 86, 1794-1806.
18. Dulyaninova, N. G., Patskovsky, Y. V. and Bresnick, A. R. (2004). The N-terminus of the long MLCK induces a disruption in normal spindle morphology and metaphase arrest. J. Cell Sci. 117, 1481-1493.
19. Duxbury, M. S., Ashley, S. W. and Whang, E. E. (2004). Inhibition of pancreatic adenocarcinoma cellular invasiveness by blebbistatin: a novel myosin II inhibitor. Biochem. Biophys. Res. Commun. 313, 992-997.
20. El-Mezgueldi, M. and Marston, S. B. (1996). The effects of smooth muscle calponin on the strong and weak myosin binding sites of F-actin. J. Biol. Chem. 271, 28161-28167.
21. Fazal, F., Gu, L., Ihnatovych, I., Han, Y., Hu, W., Antic, N., Carreira, F., Blomquist, J. F., Hope, T. J., Ucker, D. S. et al. (2005). Inhibiting myosin light chain kinase induces apoptosis in vitro and in vivo. Mol. Cell. Biol. 25, 6259-6266.
22. Fincham, V. J., James, M., Frame, M. C. and Winder, S. J. (2000). Active ERK/MAP kinase is targeted to newly forming cell-matrix adhesions by integrin engagement and v-Src. EMBO J. 19, 2911-2923.
23. Gangopadhyay, S. S., Takizawa, N., Gallant, C., Barber, A. L., Je, H. D., Smith, T. C., Luna, E. J. and Morgan, K. G. (2004). Smooth muscle archvillin: a novel regulator of signaling and contractility in vascular smooth muscle. J. Cell Sci. 117, 5043-5057.
24. Giannone, G., Dubin-Thaler, B. J., Dobereiner, H. G., Kieffer, N., Bresnick, A. R. and Sheetz, M. P. (2004). Periodic lamellipodial contractions correlate with rearward actin waves. Cell 116, 431-443.
25. Gupton, S. L. and Waterman-Storer, C. M. (2006). Spatiotemporal feedback between actomyosin and local-achesion systems optimi/es rapid cell migration. Cell 125, 1361-1374.
26. Herring, B. P., Dixon, S. and Gallagher, P. J. (2000). Smooth muscle myosin light chain kinase expression in cardiac and skeletal muscle. Am. J. Physiol. Cell Physiol. 279, C1656-C1664.
27. Huang, C., Jacobson, K. and Schaller, M. D. (2004). MAP kinases and cell migration. J. Cell Sci. 117, 4619-4628.
28. Huckaba, T. M., Lipkin, T. and Pon, L. A. (2006). Roles of type II myosin and a tropomyosin isoform in retrograde actin flow in budding yeast. J. Cell Biol. 175, 957-969.
29. Ikebe, M. (1989). Phosphorylation of a second site for myosin light chain kinase on platelet myosin. Biochemistry 28, 8750-8755.
30. Ikebe, M., Koretz, J. and Hartshorne, D. J. (1988). Effects of phosphorylation of light chain residues threonine 18 and serine 19 on the properties and conformation of smooth muscle myosin. J. Biol. Chem. 263, 6432-6437.
31. Ito, M., Nakano, T., Erdodi, F. and Hartshorne, D. J. (2004). Myosin phosphatase: Structure, regulation and function. Mol. Cell. Biochem. 259, 197-209.
32. Itoh, K., Hara, T. and Shibata, N. (1992). Diphosphorylation of platelet myosin by myosin light chain kinase. Biochim. Biophys. Acta 1133, 286-292.
33. Johnson, D., Cohen, P., Chen, M. X., Chen, Y. H. and Cohen, P. T. (1997). Identification of the regions on the M110 subunit of protein phosphatase 1M that interact with the M21 subunit and with myosin. Eur. J. Biochem. 244, 931-939.
34. Jurado, C., Haserick, J. R. and Lee, J. (2005). Slipping or gripping? Fluorescent speckle microscopy in fish keratocytes reveals two different mechanisms for generating a retrograde flow of actin. Mol. Biol. Cell 16, 507-518.
35. Kim, M., Jiang, L. H., Wilson, H. L., North, R. A. and Surprenant, A. (2001). Proteomic and functional evidence for a P2X7 receptor signalling complex. EMBO J. 20, 6347-6358.
36. Kimura, K., Ito, M., Amano, M., Chihara, K., Fukata, Y., Nakafuku, M., Yamamori, B., Feng, J., Nakano, T., Okawa, K. et al. (1996). Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248.
37. Klemke, R. L., Cai, S., Giannini, A. L., Gallagher, P. J., de Lanerolle, P. and Cheresh, D. A. (1997). Regulation of cell motility by mitogen-activated protein kinase. J. Cell Biol. 137, 481-492.
38. Kolega, J. (1998). Fluorescent analogues of myosin II for tracking the behavior of different myosin isoforms in living cells. J. Cell. Biochem. 68, 389-401.
39. Kolega, J. and Taylor, D. L. (1993). Gradients in the concentration and assembly of myosin II in living fibroblasts during locomotion and fiber transport. Mol. Biol. Cell 4, 819-836.
40. Komatsu, S. and Ikebe, M. (2004). ZIP kinase is responsible for the phosphorylation of myosin II and necessary for cell motility in mammalian fibroblasts. J. Cell Biol. 165, 243-254.
41. Kovacs, M., Toth, J., Hetenyi, C., Malnasi-Csizmadia, A. and Sellers, J. R. (2004). Mechanism of blebbistatin inhibition of myosin II. J. Biol. Chem. 279, 35557-35563.
42. Kowalczyk, A. P., Bornslaeger, E. A., Borgwardt, J. E., Palka, H. L., Dhaliwal, A. S., Corcoran, C. M., Denning, M. F. and Green, K. J. (1997). The amino-terminal domain of desmoplakin binds to plakoglobin and clusters desmosomal cadherin-plakoglobin complexes. J. Cell Biol. 139, 773-784.
43. Kudryashov, D. S., Stepanova, O. V., Vilitkevich, E. L., Nikonenko, T. A., Nadezhdina, E. S., Shanina, N. A., Lukas, T. J., Van Eldik, L. J., Watterson, D. M. and Shirinsky, V. P. (2004) Myosin light chain kinase (210 kDa) is a potential cytoskeleton integrator through its unique N-terminal domain. Exp. Cell Res. 298, 407-417.
44. Lauffenburger, D. A. and Horwitz, A. F. (1996). Cell migration: a physically integrated molecular process. Cell 84, 359-369.
45. Leinweber, B. D., Leavis, P. C., Grabarek, Z., Wang, C. L. and Morgan, K. G. (1999). Extracellular regulated kinase (ERK) interaction with actin and the calponin homology (CH) domain of actin-binding proteins. Biochem. J. 344, 117-123.
46. Limouze, J., Straight, A. F., Mitchison, T. and Sellers, J. R. (2004). Specificity of blebbistatin, an inhibitor of myosin II. J. Muscle Res. Cell Motil. 25, 337-341.
47. Lin, C.-H. and Forscher, P. (1995). Growth cone advance is inversely proportional to retrograde F-actin flow. Neuron 14, 763-771.
48. Lin, Y., Ye, L. H., Ishikawa, R., Fujita, K. and Kohama, K. (1993). Stimulatory effect of calponin on myosin ATPase activity. J. Biochem. 113, 643-645.
49. Lo, C. M., Buxton, D. B., Chua, G. C., Dembo, M., Adelstein, R. S. and Wang, Y. L. (2004). Nonmuscle myosin IIb is involved in the guidance of fibroblast migration. Mol. Biol. Cell 15, 982-989.
50. LoRusso, S. M., Rhee, D., Sanger, J. M. and Sanger, J. W. (1997). Premyofibrils in spreading adult cardiomyocytes in tissue culture: evidence for reexpression of the embryonic program for myofibrillogenesis in adult cells. Cell Motil. Cytoskeleton 37, 183-198.
51. Masato, T., Numata, T., Katoh, T., Morita, F. and Yazawa, M. (1997). Crosslinking of telokin to chicken gizzard smooth muscle myosin. J. Biochem. 121, 225-230.
52. 2+-dependent actin-binding domain in villin. Nature 315, 248-250.
53. Matsumura, E. (2005). Regulation of myosin II during cytokinesis in higher eukaryotes. Trends Cell Biol. 15, 371-377.
54. McKenna, N. M., Wang, Y.-L. and Konkel, M. E. (1989). Formation and movement of myosin-containing structures in living fibroblasts. J. Cell Biol. 109, 1163-1172.
55. Medeiros, N. A., Burnette, D. T. and Forscher, P. (2006). Myosin II function in actin-bundle turnover in neuronal growth cones. Nat. Cell Biol. 8, 215-226.
56. Mitsui, T., Inagaki, M. and Ikebe, M. (1992). Purification and characterization of smooth muscle myosin-associated phosphatase from chicken gizzards. J. Biol. Chem. 267, 16727-16735.
57. Morgan, K. G. and Gangopadhyay, S. S. (2001). Cross-bridge regulation by thin filament-associated proteins. J. Appl. Physiol. 91, 953-962.
58. Murthy, K. S. (2006). Signaling for contraction and relaxation in smooth muscle of the gut. Annu. Rev. Physiol. 68, 345-374.
59. Nebl, T., Pestonjamasp, K. N., Leszyk, J. D., Crowley, J. L., Oh, S. W. and Luna, E. J. (2002). Proteomic analysis of a detergent-resistant membrane skeleton from neutrophil plasma membranes. J. Biol. Chem. 277, 43399-43409.
60. Nguyen, D. H., Catling, A. D., Webb, D. J., Sankovic, M.. Walker, L. A., Somlyo, A. V., Weber, M. J. and Gonias, S. L. (1999). Myosin light chain kinase functions downstream of Ras/ERK to promote migration of urokinase-type plasminogen activator-stimulated cells in an integrin-selective manner. J. Cell Biol. 146, 149-164.
61. Oh, S. W., Pope, R. K., Smith, K. P., Crowley, J. L., Nebl, T., Lawrence, J. B. and Luna, E. J. (2003). Archvillin, a muscle-specific isoform of supervillin, is an early expressed component of the costameric membrane skeleton. J. Cell Sci. 116, 2261-2275.
62. Pestonjamasp, K. N., Pope, R. K., Wulfkuhle, J. D. and Luna, E. J. (1997). Supervillin (p205): a novel membrane-associated, F-actin-binding protein in the villin/gelsolin superfamily. J. Cell Biol. 139, 1255-1269.
63. Poperechnaya, A., Varlamova, O., Lin, P. J., Stull, J. T. and Bresnick, A. R. (2000). Localization and activity of myosin light chain kinase isoforms during the cell cycle. J. Cell Biol. 151, 697-708.
64. Rhee, D., Sanger, J. M. and Sanger, J. W. (1994). The premyofibril: evidence for its role in myofibrillogenesis. Cell Motil. Cytoskeleton 28, 1-24.
65. Sandquist, J. C., Swenson, K. I., Demali, K. A., Burridge, K. and Means, A. R. (2006). Rho kinase differentially regulates phosphorylation of nonmuscle myosin II isoforms A and B during cell rounding and migration. J. Biol. Chem. 281, 35873-35883.
66. Simerly, C., Nowak, G., de Lanerolle, P. and Schatten, G. (1998). Differential expression and functions of cortical myosin IIA and IIB isotypes during meiotic maturation, fertilization, and mitosis in mouse oocytes and embryos. Mol. Biol. Cell 9, 2509-2525.
67. Small, J. V., Rottner, K. and Kaverina, I. (1999). Functional design in the actin cytoskeleton. Curr. Opin. Cell Biol. 11, 54-60.
68. Smith, L., Parizi-Robinson, M., Zhu, M. S., Zhi, G., Fukui, R., Kamm, K. E. and Stull, J. T. (2002). Properties of long myosin light chain kinase binding to F-actin in vitro and in vivo. J. Biol. Chem. 277, 35597-35604.
69. Straight, A. F., Cheung, A., Limouze, J., Chen, I., Westwood, N. J., Sellers, J. R. and Mitchison, T. J. (2003). Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science 299, 1743-1747.
70. Stull, J. T., Lin, P. J., Krueger, J. K., Trewhella, J. and Zhi, G. (1998). Myosin light chain kinase: functional domains and structural motifs. Acta Physiol. Scand. 164, 471-482.
71. Sumoza-Toledo, A., Gillespie, P. G., Romero-Ramirez, H., Ferreira-Ishikawa, H. C., Larson, R. E. and Santos-Argumedo, L. (2006). Differential localization of unconventional myosin I and nonmuscle myosin II during B cell spreading. Exp. Cell Res. 312, 3312-3322.
72. Szymanski, P. T. (2004). Calponin (CaP) as a latch-bridge protein-a new concept in regulation of contractility in smooth muscles. J. Muscle Res. Cell Motil. 25, 7-19.
73. Takizawa, N., Smith, T. C., Nebl, T., Crowley, J. L., Palmieri, S. J., Lifshitz, L. M., Ehrhardt, A. G., Hoffman, L. M., Beckerle, M. C. and Luna, E. J. (2006). Supervillin modulation of focal adhesions involving TRIP6/ZRP-1. J. Cell Biol. 174, 447-458.
74. Togo, T. and Steinhardt, R. A. (2004). Nonmuscle Myosin IIA and IIB have distinct functions in the exocytosis-dependent process of cell membrane repair. Mol. Biol. Cell 15, 688-695.
75. Totsukawa, G., Wu, Y., Sasaki, Y., Hartshorne, D. J., Yamakita, Y., Yamashiro, S. and Matsumura, E. (2004). 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.
76. Ueda, K., Murata-Hori, M., Tatsuka, M. and Hosoya, H. (2002). Rho-kinase contributes to diphosphorylation of myosin II regulatory light chain in nonmuscle cells. Oncogene 21, 5852-5860.
77. Uehata, M., Ishizaki, T., Satoh, H., Ono, T., Kawahara, T., Morishita, T., Tamakawa, H., Yamagami, K., Inui, J., Maekawa, M. et al. (1997). Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990-994.
78. Vicente-Manzanarés, M., Zareno, J., Whitmore, L., Choi, C. K. and Horwitz, A. F. (2007). Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells. J. Cell Biol. 176, 573-580.
79. Wadgaonkar, R., Nurmukhambetova, S., Zaiman, A. L. and Garcia, J. G. (2003). Mutation analysis of the non-muscle myosin light chain kinase (MLCK) deletion constructs on CV1 fibroblast contractile activity and proliferation. J. Cell, Biochem. 88, 623-634.
80. Wakatsuki, T., Wysolmerski, R. B. and Elson, E. L. (2003). Mechanics of cell spreading: role of myosin II. J. Cell Sci. 116, 1617-1625.
81. Watanabe, T., Hosoya, H. and Yonemura, S. (2007). Regulation of Myosin II dynamics by phosphorylation and dephosphorylation of its light chain in epithelial cells. Mol. Biol. Cell 18, 605-616.
82. Webb, D. J., Donais, K., Whitmore, L. A., Thomas, S. M., Turner, C. E., Parsons, J. T. and Horwitz, A. E. (2004). FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat. Cell Biol. 6, 154-161.
83. Wulfkuhle, J. D., Donina, I. E., Stark, N. H., Pope, R. K., Pestonjamasp, K. N., Niswonger, M. L. and Luna, E. J. (1999). Domain analysis of supervillin, an F-actin bundling plasma membrane protein with functional nuclear localization signals. J. Cell Sci. 112, 2125-2136.
84. Wylie, S. R. and Chantler, P. D. (2003). Myosin IIA drives neurite retraction. Mol. Biol. Cell 14, 4654-4666.
85. Yang, C. X., Chen, H. Q., Chen, C., Yu, W. P., Zhang, W. C., Peng, Y. J., He, W. Q., Wei, D. M., Gao, X. and Zhu, M. S. (2006). Microfilament-binding properties of N-terminal extension of the isoform of smooth muscle long myosin light chain kinase. Cell Res. 16, 367-376.