Nonmuscle myosin II folds into a 10S form via two portions of tail for dynamic subcellular localization

Nonmuscle myosin II forms a folded conformation (10S form) in the inactivated state; however, the physiological importance of the 10S form is still unclear. To investigate the role of 10S form, we generated a chimeric mutant of nonmuscle myosin IIB (IIB‐SK1·2), in which S1462‐R1490 and L1551‐E1577 were replaced with the corresponding portions of skeletal muscle myosin heavy chain. The IIB‐SK1·2 mutant did not fold into a 10S form under physiological condition in vitro. IIB‐SK1·2 was less dynamic by stabilizing the filamentous form and accumulated in the posterior region of migrating cells. IIB‐SK1·2 functioned properly in cytokinesis but altered migratory properties; the rate and directional persistence were increased by IIB‐SK1·2 expression. Surprisingly, endogenous nonmuscle myosin IIA was excluded from the posterior region of migrating cells expressing IIB‐SK1·2, which may underlie the change of the cellular migratory properties. These results suggest that the 10S form is necessary for maintaining nonmuscle myosin II in an unassembled state and for recruitment of nonmuscle myosin II to a specific region of the cell.

[1]  J. Baker,et al.  Modification of Interface between Regulatory and Essential Light Chains Hampers Phosphorylation-dependent Activation of Smooth Muscle Myosin* , 2012, The Journal of Biological Chemistry.

[2]  K. Thirumurugan,et al.  Role of the tail in the regulated state of myosin 2. , 2011, Journal of molecular biology.

[3]  Amy N. Schneck,et al.  Direct evidence for functional smooth muscle myosin II in the 10S self-inhibited monomeric conformation in airway smooth muscle cells , 2011, Proceedings of the National Academy of Sciences.

[4]  S. Kawamoto,et al.  Nonmuscle myosin II isoform and domain specificity during early mouse development , 2010, Proceedings of the National Academy of Sciences.

[5]  K. Trybus,et al.  Common Structural Motifs for the Regulation of Divergent Class II Myosins* , 2010, The Journal of Biological Chemistry.

[6]  Miguel Vicente-Manzanares,et al.  Non-muscle myosin II takes centre stage in cell adhesion and migration , 2009, Nature Reviews Molecular Cell Biology.

[7]  Masayuki Takahashi,et al.  Diphosphorylation of regulatory light chain of myosin IIA is responsible for proper cell spreading. , 2009, Biochemical and biophysical research communications.

[8]  Atsushi Miyawaki,et al.  mKikGR, a Monomeric Photoswitchable Fluorescent Protein , 2008, PloS one.

[9]  A. Means,et al.  The C-terminal tail region of nonmuscle myosin II directs isoform-specific distribution in migrating cells. , 2008, Molecular biology of the cell.

[10]  Miguel Vicente-Manzanares,et al.  Segregation and activation of myosin IIB creates a rear in migrating cells , 2008, The Journal of cell biology.

[11]  H. Jung,et al.  Head-head and head-tail interaction: a general mechanism for switching off myosin II activity in cells. , 2008, Molecular biology of the cell.

[12]  M. Ikebe Regulation of the function of mammalian myosin and its conformational change. , 2008, Biochemical and biophysical research communications.

[13]  R. Straussman,et al.  MHC-IIB Filament Assembly and Cellular Localization Are Governed by the Rod Net Charge , 2008, PloS one.

[14]  R. Adelstein,et al.  Nonmuscle myosin II moves in new directions , 2008, Journal of Cell Science.

[15]  Matt L. Walker,et al.  Structures of smooth muscle myosin and heavy meromyosin in the folded, shutdown state. , 2007, Journal of molecular biology.

[16]  Masaaki Sato,et al.  Two regions of the tail are necessary for the isoform-specific functions of nonmuscle myosin IIB. , 2007, Molecular biology of the cell.

[17]  Kenneth M. Yamada,et al.  Myosin IIA regulates cell motility and actomyosin–microtubule crosstalk , 2007, Nature Cell Biology.

[18]  B. Beck,et al.  The N-terminal Lobes of Both Regulatory Light Chains Interact with the Tail Domain in the 10 S-inhibited Conformation of Smooth Muscle Myosin* , 2006, Journal of Biological Chemistry.

[19]  A. Abdukarimov,et al.  Transfection of insect cell lines using polyethylenimine , 2006, Cytotechnology.

[20]  Hiroshi Kimura,et al.  Cytosolic chaperonin prevents polyglutamine toxicity with altering the aggregation state , 2006, Nature Cell Biology.

[21]  F. Matsumura Regulation of myosin II during cytokinesis in higher eukaryotes. , 2005, Trends in cell biology.

[22]  S. Jana,et al.  Vertebrate Nonmuscle Myosin II Isoforms Rescue Small Interfering RNA-induced Defects in COS-7 Cell Cytokinesis* , 2005, Journal of Biological Chemistry.

[23]  A. Yamagishi,et al.  Critical regions for assembly of vertebrate nonmuscle myosin II. , 2005, Biochemistry.

[24]  Kenneth M. Yamada,et al.  Defects in Cell Adhesion and the Visceral Endoderm following Ablation of Nonmuscle Myosin Heavy Chain II-A in Mice* , 2004, Journal of Biological Chemistry.

[25]  Ehud Goldin,et al.  Identification and Characterization of Nonmuscle Myosin II-C, a New Member of the Myosin II Family* , 2004, Journal of Biological Chemistry.

[26]  Chun-Min Lo,et al.  Nonmuscle myosin IIb is involved in the guidance of fibroblast migration. , 2003, Molecular biology of the cell.

[27]  J. Kolega Asymmetric distribution of myosin IIB in migrating endothelial cells is regulated by a rho-dependent kinase and contributes to tail retraction. , 2003, Molecular biology of the cell.

[28]  J. Sellers,et al.  Functional Divergence of Human Cytoplasmic Myosin II , 2003, Journal of Biological Chemistry.

[29]  J. Sellers,et al.  Kinetic Mechanism of Non-muscle Myosin IIB , 2003, Journal of Biological Chemistry.

[30]  Y. Maéda,et al.  Enhancement of protein expression in insect cells by a lobster tropomyosin cDNA leader sequence , 2002, FEBS letters.

[31]  M. Yazawa,et al.  Essential light chain modulates phosphorylation-dependent regulation of smooth muscle myosin. , 2002, Journal of biochemistry.

[32]  H. Haga,et al.  Differential localization of non‐muscle myosin II isoforms and phosphorylated regulatory light chains in human MRC‐5 fibroblasts , 2001, FEBS letters.

[33]  S. Yumura Myosin II dynamics and cortical flow during contractile ring formation in Dictyostelium cells , 2001, The Journal of cell biology.

[34]  J. Berg,et al.  A millennial myosin census. , 2001, Molecular biology of the cell.

[35]  R. Adelstein,et al.  Conditional expression of a truncated fragment of nonmuscle myosin II-A alters cell shape but not cytokinesis in HeLa cells. , 2000, Molecular biology of the cell.

[36]  J. Kolega,et al.  Cytoplasmic dynamics of myosin IIA and IIB: spatial 'sorting' of isoforms in locomoting cells. , 1998, Journal of cell science.

[37]  V. Ferrans,et al.  Nonmuscle myosin II-B is required for normal development of the mouse heart. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[38]  J. Kolega,et al.  Asymmetry in the distribution of free versus cytoskeletal myosin II in locomoting microcapillary endothelial cells. , 1997, Experimental cell research.

[39]  J. Sellers,et al.  Structure and Function of the 10 S Conformation of Smooth Muscle Myosin* , 1996, The Journal of Biological Chemistry.

[40]  V. Chauhan,et al.  Phospholipid binding, phosphorylation by protein kinase C, and filament assembly of the COOH terminal heavy chain fragments of nonmuscle myosin II isoforms MIIA and MIIB. , 1995, Biochemistry.

[41]  M. Yazawa,et al.  Evidence for involvement of a 12-residue peptide segment of the heavy chain in the neck region of smooth muscle myosin in formation of the 10S conformation. , 1995, Journal of biochemistry.

[42]  C. Sanders,et al.  Function of the NH2-terminal domain of the regulatory light chain on the regulation of smooth muscle myosin. , 1994, The Journal of biological chemistry.

[43]  T. Pollard,et al.  Differential localization of myosin-II isozymes in human cultured cells and blood cells. , 1994, Journal of cell science.

[44]  K. Trybus,et al.  Antibodies probe for folded monomeric myosin in relaxed and contracted smooth muscle , 1994, The Journal of cell biology.

[45]  J. Spudich,et al.  Dictyostelium myosin heavy chain phosphorylation sites regulate myosin filament assembly and localization in vivo , 1993, Cell.

[46]  R. Rigler,et al.  Fluorescence correlation spectroscopy with high count rate and low background: analysis of translational diffusion , 1993, European Biophysics Journal.

[47]  K. Trybus,et al.  The regulatory light chain is required for folding of smooth muscle myosin. , 1988, The Journal of biological chemistry.

[48]  J. Kendrick‐Jones,et al.  Polymerization of vertebrate non-muscle and smooth muscle myosins. , 1987, Journal of molecular biology.

[49]  K. E. Cross,et al.  ATP‐linked monomer‐polymer equilibrium of smooth muscle myosin: the free folded monomer traps ADP.Pi. , 1986, The EMBO journal.

[50]  K. Trybus,et al.  Conformational states of smooth muscle myosin. Effects of light chain phosphorylation and ionic strength. , 1984, The Journal of biological chemistry.

[51]  D. Hartshorne,et al.  Correlation of enzymatic properties and conformation of smooth muscle myosin. , 1983, Biochemistry.

[52]  K. Trybus,et al.  A bent monomeric conformation of myosin from smooth muscle. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[53]  T. Butler,et al.  Myosin filaments have non-phosphorylated light chains in relaxed smooth muscle , 1981, Nature.

[54]  T. Pollard,et al.  Human platelet myosin. II. In vitro assembly and structure of myosin filaments , 1975, The Journal of cell biology.

[55]  N. Dulyaninova,et al.  Multiple regulatory steps control mammalian nonmuscle myosin II assembly in live cells. , 2009, Molecular biology of the cell.

[56]  J. Sellers,et al.  Folding and regulation in myosins II and V , 2008, Journal of Muscle Research and Cell Motility.

[57]  C. Sanders,et al.  Function of the NH 2-terminal Domain of the Regulatory Light Chain on the Regulation of Smooth Muscle Myosin * , 2001 .

[58]  T. Uyeda,et al.  Myosin II can be localized to the cleavage furrow and to the posterior region of Dictyostelium amoebae without control by phosphorylation of myosin heavy and light chains. , 1997, Cell motility and the cytoskeleton.

[59]  J. Kendrick‐Jones,et al.  Light-chain phosphorylation controls the conformation of vertebrate non-muscle and smooth muscle myosin molecules , 1983, Nature.

[60]  T. Wakabayashi,et al.  Electron microscopic studies of myosin molecules from chicken gizzard muscle I: the formation of the intramolecular loop in the myosin tail. , 1982, Journal of biochemistry.