Stretching actin filaments within cells enhances their affinity for the myosin ii motor domain

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Uyeda, Taro Q P ^a   Iwadate, Yoshiaki ^b,c   Umeki, Nobuhisa ^a   Nagasaki, Akira ^a   Yumura, Shigehiko ^b  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^b YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CORTEXILLIN; GREEN FLUORESCENT PROTEIN; MYOSIN I; MYOSIN II; MYOSIN II MOTOR DOMAIN PROTEIN; PHALLOIDIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; RHODAMINE; UNCLASSIFIED DRUG; DRUG DERIVATIVE; MUTANT PROTEIN; RHODAMINE PHALLOIDIN; RHODAMINE-PHALLOIDIN;

ACTIN FILAMENT; AMOEBOID CELL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CELL DIVISION; CELL POLARITY; CELL TYPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DICTYOSTELIUM; IN VIVO STUDY; MECHANICAL STIMULATION; MOLECULAR PROBE; NONHUMAN; PROTEIN BINDING; PROTEIN LOCALIZATION; BIOLOGICAL MODEL; CHEMISTRY; CYTOLOGY; GENE INACTIVATION; METABOLISM; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT;

DICTYOSTELIUM;

ACTIN CYTOSKELETON; DICTYOSTELIUM; GENE KNOCKOUT TECHNIQUES; GREEN FLUORESCENT PROTEINS; MODELS, BIOLOGICAL; MOLECULAR PROBES; MUTANT PROTEINS; MYOSIN TYPE II; PHALLOIDINE; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RHODAMINES;

EID: 80054084623     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026200     Document Type: Article

References (94)

1. Chhabra ES, Higgs HN, (2007) The many faces of actin: matching assembly factors with cellular structures. Nat Cell Biol 9: 1110-1121.
2. Pollard TD, Cooper JA, (2009) Actin, a central player in cell shape and movement. Science 326: 1208-1212.
3. McGough A, (1998) F-actin-binding proteins. Curr Opin Struct Biol 8: 166-176.
4. Hild G, Bugyi B, Nyitrai M, (2010) Conformational dynamics of actin: effectors and implications for biological function. Cytoskeleton (Hoboken) 67: 609-629.
5. Oda T, Maeda Y, (2010) Multiple Conformations of F-actin. Structure 18: 761-767.
6. Galkin VE, Orlova A, Salmazo A, Djinovic-Carugo K, Egelman EH, (2010) Opening of tandem calponin homology domains regulates their affinity for F-actin. Nat Struct Mol Biol 17: 614-616.
7. McGough A, Pope B, Chiu W, Weeds A, (1997) Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function. J Cell Biol 138: 771-781.
8. Galkin VE, Orlova A, Lukoyanova N, Wriggers W, Egelman EH, (2001) Actin depolymerizing factor stabilizes an existing state of F-actin and can change the tilt of F-actin subunits. J Cell Biol 153: 75-86.
9. Ressad F, Didry D, Xia GX, Hong Y, Chua NH, et al. (1998) Kinetic analysis of the interaction of actin-depolymerizing factor (ADF)/cofilin with G- and F-actins. Comparison of plant and human ADFs and effect of phosphorylation. J Biol Chem 273: 20894-20902.
10. Egelman EH, Francis N, DeRosier DJ, (1982) F-actin is a helix with a random variable twist. Nature 298: 131-135.
11. Galkin VE, Orlova A, Schroder GF, Egelman EH, (2010) Structural polymorphism in F-actin. Nat Struct Mol Biol 17: 1318-1323.
12. Fujii T, Iwane AH, Yanagida T, Namba K, (2010) Direct visualization of secondary structures of F-actin by electron cryomicroscopy. Nature 467: 724-728.
13. Oosawa F, Fujime S, Ishiwata S, Mihashi K, (1972) Dynamic properties of F-actin and thin filament. Cold Spring Harbor Symp Quant Biol 37: 277-285.
14. Thomas DD, Seidel JC, Gergely J, (1979) Rotational dynamics of spin-labeled F-actin in the sub-millisecond time range. J Mol Biol 132: 257-273.
15. Tawada K, (1969) Physicochemical studies of F-actin-heavy meromyosin solutions. Biochim Biophys Acta 172: 311-318.
16. Miki M, Wahl P, Auchet JC, (1982) Fluorescence anisotropy of labeled F-actin: influence of divalent cations on the interaction between F-actin and myosin heads. Biochemistry 21: 3661-3665.
17. Loscalzo J, Reed GH, Weber A, (1975) Conformational change and cooperativity in actin filaments free of tropomyosin. Proc Natl Acad Sci USA 72: 3412-3415.
18. Fujime S, Ishiwata S, (1971) Dynamic study of F-actin by quasielastic scattering of laser light. J Mol Biol 62: 251-265.
19. Orlova A, Egelman EH, (1997) Cooperative rigor binding of myosin to actin is a function of F-actin structure. J Mol Biol 265: 469-474.
20. Tokuraku K, Kurogi R, Toya R, Uyeda TQP, (2008) Novel Mode of Cooperative Binding between Myosin and Mg2+-actin Filaments in the Presence of Low Concentrations of ATP. J Mol Biol 386: 149-162.
21. Sabry JH, Moores SL, Ryan S, Zang JH, Spudich JA, (1997) Myosin heavy chain phosphorylation sites regulate myosin localization during cytokinesis in live cells. Mol Biol Cell 8: 2605-2615.
22. Egelhoff TT, Lee RJ, Spudich JA, (1993) Dictyostelium myosin heavy chain phosphorylation sites regulate myosin filament assembly and localization in vivo. Cell 75: 363-371.
23. Uehara R, Goshima G, Mabuchi I, Vale RD, Spudich JA, et al. (2010) Determinants of myosin II cortical localization during cytokinesis. Curr Biol 20: 1080-1085.
24. Sussman M, (1987) Cultivation and synchronous morphogenesis of Dictyostelium under controlled experimental conditions. In: Spudich JA, editors. Dictyostelium discoideum: Molecular approaches to Cell Biology Orlando Academic Press pp. 9-29.
25. Ruppel KM, Uyeda TQP, Spudich JA, (1994) Role of highly conserved lysine 130 of myosin motor domain. J Biol Chem 269: 18773-18780.
26. Liu X, Ito K, Lee RJ, Uyeda TQP, (2000) Involvement of tail domains in regulation of Dictyostelium myosin II. Biochem Biophys Res Commun 271: 75-81.
27. Yumura S, Mori S, Fukui Y, (1984) Localization of actin and myosin for the study of amoeboid movement in Dictyostelium using improved immunofluorescence. J Cell Biol 99: 894-899.
28. Pramanik MK, Iijima M, Iwadate Y, Yumura S, (2009) PTEN is a mechanosensing signal transducer for myosin II localization in Dictyostelium cells. Genes Cells 14: 821-834.
29. Doyle T, Botstein D, (1996) Movement of yeast cortical actin cytoskeleton visualized in vivo. Proc Natl Acad Sci USA 93: 3886-3891.
30. Westphal M, Jungbluth A, Heidecker M, Muhlbauer B, Heizer C, et al. (1997) Microfilament dynamics during cell movement and chemotaxis monitored using a GFP-actin fusion protein. Curr Biol 7: 176-183.
31. Asano Y, Mizuno T, Kon T, Nagasaki A, Sutoh K, et al. (2004) Keratocyte-like locomotion in amiB-null Dictyostelium cells. Cell Motil Cytoskeleton 59: 17-27.
32. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, et al. (2008) Lifeact: a versatile marker to visualize F-actin. Nat Methods 5: 605-607.
33. Yumura S, Uyeda TQP, (2003) Myosins and cell dynamics in cellular slime molds. Int Rev Cytol 224: 173-225.
34. Hibberd MG, Trentham DR, (1986) Relationships between chemical and mechanical events during muscular contraction. Annu Rev Biophys Biophys Chem 15: 119-161.
35. Lymn RW, (1979) Kinetic analysis of myosin and actomyosin ATPase. Annu Rev Biophys Bioeng 8: 145-163.
36. Batra R, Geeves MA, Manstein DJ, (1999) Kinetic analysis of Dictyostelium discoideum myosin motor domains with glycine-to-alanine mutations in the reactive thiol region. Biochemistry 38: 6126-6134.
37. Patterson B, Ruppel KM, Wu Y, Spudich JA, (1997) Cold-sensitive mutants G680V and G691C of Dictyostelium myosin II confer dramatically different biochemical defects. J Biol Chem 272: 27612-27617.
38. Kinose F, Wang SX, Kidambi US, Moncman CL, Winkelmann DA, (1996) Glycine 699 is pivotal for the motor activity of skeletal muscle myosin. J Cell Biol 134: 895-909.
39. Uyeda TQP, Patterson B, Mendoza L, Hiratsuka Y, (2002) Amino acids 519-524 of Dictyostelium myosin II form a surface loop that aids actin binding by facilitating a conformational change. J Muscle Res Cell Motil 23: 685-695.
40. Moores SL, Sabry JH, Spudich JA, (1996) Myosin dynamics in live Dictyostelium cells. Proc Natl Acad Sci USA 93: 443-446.
41. De Lozanne A, Spudich JA, (1987) Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science 236: 1086-1091.
42. Knecht DA, Loomis WF, (1987) Antisense RNA inactivation of myosin heavy chain gene expression in Dictyostelium discoideum. Science 236: 1081-1086.
43. Uyeda TQP, Kitayama C, Yumura S, (2000) Myosin II-independent cytokinesis in Dictyostelium: its mechanism and implications. Cell Struct Funct 25: 1-10.
44. Fukui Y, Lynch TJ, Brzeska H, Korn ED, (1989) Myosin I is located at the leading edges of locomoting Dictyostelium amoebae. Nature 341: 328-331.
45. Bement WM, Mooseker MS, (1995) TEDS rule: a molecular rationale for differential regulation of myosins by phosphorylation of the heavy chain head. Cell Motil Cytoskeleton 31: 87-92.
46. Effler JC, Iglesias PA, Robinson DN, (2007) A mechanosensory system controls cell shape changes during mitosis. Cell Cycle 6: 30-35.
47. Merkel R, Simson R, Simson DA, Hohenadl M, Boulbitch A, et al. (2000) A micromechanic study of cell polarity and plasma membrane cell body coupling in Dictyostelium. Biophys J 79: 707-719.
48. Ren Y, Effler JC, Norstrom M, Luo T, Firtel RA, et al. (2009) Mechanosensing through Cooperative Interactions between Myosin II and the Actin Crosslinker Cortexillin I. Curr Biol 19: 1421-1428.
49. Janetopoulos C, Borleis J, Vazquez F, Iijima M, Devreotes P, (2005) Temporal and spatial regulation of phosphoinositide signaling mediates cytokinesis. Dev Cell 8: 467-477.
50. Faix J, Steinmetz M, Boves H, Kammerer RA, Lottspeich F, et al. (1996) Cortexillins, major determinants of cell shape and size, are actin-bundling proteins with a parallel coiled-coil tail. Cell 86: 631-642.
51. Hammer JA 3rd, (1994) Regulation of Dictyostelium myosin II by phosphorylation: what is essential and what is important? J Cell Biol 127: 1779-1782.
52. Yumura S, Yoshida M, Betapudi V, Licate LS, Iwadate Y, et al. (2005) Multiple myosin II heavy chain kinases: roles in filament assembly control and proper cytokinesis in Dictyostelium. Mol Biol Cell 16: 4256-4266.
53. DeBiasio RL, LaRocca GM, Post PL, Taylor DL, (1996) Myosin II transport, organization, and phosphorylation: evidence for cortical flow/solation-contraction coupling during cytokinesis and cell locomotion. Mol Biol Cell 7: 1259-1282.
54. Yumura S, (2001) Myosin II dynamics and cortical flow during contractile ring formation in Dictyostelium cells. J Cell Biol 154: 137-146.
55. Yumura S, Ueda M, Sako Y, Kitanishi-Yumura T, Yanagida T, (2008) Multiple mechanisms for accumulation of myosin II filaments at the equator during cytokinesis. Traffic 9: 2089-2099.
56. Zang JH, Spudich JA, (1998) Myosin II localization during cytokinesis occurs by a mechanism that does not require its motor domain. Proc Natl Acad Sci USA 95: 13652-13657.
57. Naqvi NI, Eng K, Gould KL, Balasubramanian MK, (1999) Evidence for F-actin-dependent and-independent mechanisms involved in assembly and stability of the medial actomyosin ring in fission yeast. EMBO J 18: 854-862.
58. Lord M, Laves E, Pollard TD, (2005) Cytokinesis depends on the motor domains of myosin-II in fission yeast but not in budding yeast. Mol Biol Cell 16: 5346-5355.
59. Schroeder TE, Otto JJ, (1988) Immunofluorescent analysis of actin and myosin in isolated contractile rings of sea urchin eggs. Zool Sci 5: 713-725.
60. Tang N, Ostap EM, (2001) Motor domain-dependent localization of myo1b (myr-1). Curr Biol 11: 1131-1135.
61. Fanning AS, Wolenski JS, Mooseker MS, Izant JG, (1994) Differential regulation of skeletal muscle myosin-II and brush border myosin-I enzymology and mechanochemistry by bacterially produced tropomyosin isoforms. Cell Motil Cytoskeleton 29: 29-45.
62. Ostap EM, (2008) Tropomyosins as discriminators of myosin function. Adv Exp Med Biol 644: 273-282.
63. Kuhn TB, Bamburg JR, (2008) Tropomyosin and ADF/cofilin as collaborators and competitors. Adv Exp Med Biol 644: 232-249.
64. Bretscher A, (1991) Microfilament structure and function in the cortical cytoskeleton. Annu Rev Cell Biol 7: 337-374.
65. Ando T, Scales D, (1985) Skeletal muscle myosin subfragment-1 induces bundle formation by actin filaments. J Biol Chem 260: 2321-2327.
66. Hanein D, Matsudaira P, DeRosier DJ, (1997) Evidence for a conformational change in actin induced by fimbrin (N375) binding. J Cell Biol 139: 387-396.
67. Hodgkinson JL, el-Mezgueldi M, Craig R, Vibert P, Marston SB, et al. (1997) 3-D image reconstruction of reconstituted smooth muscle thin filaments containing calponin: visualization of interactions between F-actin and calponin. J Mol Biol 273: 150-159.
68. Schmid MF, Sherman MB, Matsudaira P, Chiu W, (2004) Structure of the acrosomal bundle. Nature 431: 104-107.
69. Galkin VE, Orlova A, Koleske AJ, Egelman EH, (2005) The Arg non-receptor tyrosine kinase modifies F-actin structure. J Mol Biol 346: 565-575.
70. Sharma S, Grintsevich EE, Phillips ML, Reisler E, Gimzewski JK, (2011) Atomic force microscopy reveals drebrin induced remodeling of F-actin with subnanometer resolution. Nano Lett 11: 825-827.
71. Tsaturyan AK, Koubassova N, Ferenczi MA, Narayanan T, Roessle M, et al. (2005) Strong binding of myosin heads stretches and twists the actin helix. Biophys J 88: 1902-1910.
72. Kozuka J, Yokota H, Arai Y, Ishii Y, Yanagida T, (2006) Dynamic polymorphism of single actin molecules in the actin filament. Nat Chem Biol 2: 83-86.
73. Hawkins M, Pope B, Maciver SK, Weeds AG, (1993) Human actin depolymerizing factor mediates a pH-sensitive destruction of actin filaments. Biochemistry 32: 9985-9993.
74. Hayden SM, Miller PS, Brauweiler A, Bamburg JR, (1993) Analysis of the interactions of actin depolymerizing factor with G- and F-actin. Biochemistry 32: 9994-10004.
75. Kovar DR, Sirotkin V, Lord M, (2010) Three's company: the fission yeast actin cytoskeleton. Trends Cell Biol 21: 177-187.
76. Matsushita S, Inoue Y, Hojo M, Sokabe M, Adachi T, (2011) Effect of tensile force on the mechanical behavior of actin filaments. J Biomech 44: 1776-1781.
77. Shimozawa T, Ishiwata S, (2009) Mechanical distortion of single actin filaments induced by external force: detection by fluorescence imaging. Biophys J 96: 1036-1044.
78. Hayakawa K, Tatsumi H, Sokabe M, (2011) Actin filaments function as a tension sensor by tension dependent binding of cofilin to the filament. J Cell Biol in press.
79. Washington RW, Knecht DA, (2008) Actin binding domains direct actin-binding proteins to different cytoskeletal locations. BMC Cell Biol 9: 10.
80. Marshall TW, Aloor HL, Bear JE, (2009) Coronin 2A regulates a subset of focal-adhesion-turnover events through the cofilin pathway. J Cell Sci 122: 3061-3069.
81. Martin C, Gunning P, (2008) Isoform sorting of tropomyosins. Adv Exp Med Biol 644: 187-200.
82. Tsujioka M, Yoshida K, Inouye K, (2004) Talin B is required for force transmission in morphogenesis of Dictyostelium. EMBO J 23: 2216-2225.
83. Aizawa H, Fukui Y, Yahara I, (1997) Live dynamics of Dictyostelium cofilin suggests a role in remodeling actin latticework into bundles. J Cell Sci 110: 2333-2344.
84. Svitkina TM, Borisy GG, (1999) Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J Cell Biol 145: 1009-1026.
85. Verkhovsky AB, Svitkina TM, Borisy GG, (1999) Self-polarization and directional motility of cytoplasm. Curr Biol 9: 11-20.
86. Orlova A, Prochniewicz E, Egelman EH, (1995) Structural dynamics of F-actin: II. Cooperativity in structural transitions. J Mol Biol 245: 598-607.
87. Skau CT, Kovar DR, (2010) Fimbrin and tropomyosin competition regulates endocytosis and cytokinesis kinetics in fission yeast. Curr Biol 20: 1415-1422.
88. Wakabayashi K, Sugimoto Y, Tanaka H, Ueno Y, Takezawa Y, et al. (1994) X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys J 67: 2422-2435.
89. Sawada Y, Tamada M, Dubin-Thaler BJ, Cherniavskaya O, Sakai R, et al. (2006) Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 127: 1015-1026.
90. Sawada Y, Sheetz MP, (2002) Force transduction by Triton cytoskeletons. J Cell Biol 156: 609-615.
91. Yonemura S, Wada Y, Watanabe T, Nagafuchi A, Shibata M, (2010) α-Catenin as a tension transducer that induces adherens junction development. Nat Cell Biol 12: 533-542.
92. Puchner EM, Alexandrovich A, Kho AL, Hensen U, Schafer LV, et al. (2008) Mechanoenzymatics of titin kinase. Proc Natl Acad Sci USA 105: 13385-13390.
93. Laakso JM, Lewis JH, Shuman H, Ostap EM, (2008) Myosin I Can Act As a Molecular Force Sensor. Science 321: 133-136.
94. Kee YS, Robinson DN, (2008) Motor proteins: myosin mechanosensors. Curr Biol 18: R860-862.