Common Structural Motifs for the Regulation of Divergent Class II Myosins*

This minireview focuses on structural studies that have provided insights into our current understanding of thick filament regulation in muscle. We describe how different domains in the myosin molecule interact to produce an inactive “off” state; included are head-head and head-rod interactions, the role of the regulatory light chain, and the significance of the α-helical coiled-coil rod in regulation. Several of these interactions have now been visualized in a wide variety of native myosin filaments, testifying to the generality of these structural motifs across the phylogenetic tree.

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

[2]  S. Burgess,et al.  Conservation of the regulated structure of folded myosin 2 in species separated by at least 600 million years of independent evolution , 2008, Proceedings of the National Academy of Sciences.

[3]  A. Houdusse,et al.  Structure of the regulatory domain of scallop myosin at 2 A resolution: implications for regulation. , 1996, Structure.

[4]  K. Taylor,et al.  Visualization of Head–Head Interactions in the Inhibited State of Smooth Muscle Myosin , 1999, The Journal of cell biology.

[5]  K. Trybus,et al.  Coiled-coil unwinding at the smooth muscle myosin head-rod junction is required for optimal mechanical performance. , 2001, Biophysical journal.

[6]  J. Squire,et al.  The 7-stranded structure of relaxed scallop muscle myosin filaments: support for a common head configuration in myosin-regulated muscles. , 2009, Journal of structural biology.

[7]  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.

[8]  R. Crowther,et al.  Arrangement of the heads of myosin in relaxed thick filaments from tarantula muscle. , 1985, Journal of Molecular Biology.

[9]  R. Moss,et al.  Three-dimensional structure of vertebrate cardiac muscle myosin filaments , 2008, Proceedings of the National Academy of Sciences.

[10]  Edward P. Morris,et al.  Myosin filament 3D structure in mammalian cardiac muscle , 2008, Journal of structural biology.

[11]  Clive R. Bagshaw,et al.  Active site trapping of nucleotide by smooth and non-muscle myosins. , 1988, Journal of molecular biology.

[12]  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.

[13]  J. Stull,et al.  Myosin light chain phosphorylation in vertebrate striated muscle: regulation and function. , 1993, The American journal of physiology.

[14]  R A Milligan,et al.  Structure of the actin-myosin complex and its implications for muscle contraction. , 1993, Science.

[15]  László Nyitray,et al.  Visualization of an unstable coiled coil from the scallop myosin rod , 2003, Nature.

[16]  J. Lawson,et al.  Structural Model of the Regulatory Domain of Smooth Muscle Heavy Meromyosin* , 2003, The Journal of Biological Chemistry.

[17]  Florence Tama,et al.  The requirement for mechanical coupling between head and S2 domains in smooth muscle myosin ATPase regulation and its implications for dimeric motor function. , 2005, Journal of molecular biology.

[18]  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.

[19]  Roberto Dominguez,et al.  Crystal Structure of a Vertebrate Smooth Muscle Myosin Motor Domain and Its Complex with the Essential Light Chain Visualization of the Pre–Power Stroke State , 1998, Cell.

[20]  Chun Y Seow,et al.  Myosin filament assembly in an ever-changing myofilament lattice of smooth muscle. , 2005, American journal of physiology. Cell physiology.

[21]  K. Trybus.  Regulation of expressed truncated smooth muscle myosins. Role of the essential light chain and tail length. , 1994, The Journal of biological chemistry.

[22]  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.

[23]  R. Adelstein,et al.  Phosphorylation of platelet myosin increases actin-activated myosin ATPase activity , 1975, Nature.

[24]  E. Eisenberg,et al.  Regulation and kinetics of the actin-myosin-ATP interaction. , 1980, Annual review of biochemistry.

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

[26]  J. Sellers,et al.  Two Heads Are Required for Phosphorylation-dependent Regulation of Smooth Muscle Myosin (*) , 1995, The Journal of Biological Chemistry.

[27]  E. Egelman.  A robust algorithm for the reconstruction of helical filaments using single-particle methods. , 2000, Ultramicroscopy.

[28]  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.

[29]  K. Taylor,et al.  Refined model of the 10S conformation of smooth muscle myosin by cryo-electron microscopy 3D image reconstruction. , 2003, Journal of molecular biology.

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

[31]  K. Trybus,et al.  Three-dimensional image reconstruction of dephosphorylated smooth muscle heavy meromyosin reveals asymmetry in the interaction between myosin heads and placement of subfragment 2 , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[32]  I. Schlichting,et al.  Crystal structures of human cardiac β-myosin II S2-Δ provide insight into the functional role of the S2 subfragment , 2006, Proceedings of the National Academy of Sciences.

[33]  E. Egelman,et al.  Atomic model of a myosin filament in the relaxed state , 2005, Nature.

[34]  David D. Thomas,et al.  Molecular dynamics simulations reveal a disorder-to-order transition on phosphorylation of smooth muscle myosin. , 2007, Biophysical journal.

[35]  R. Craig,et al.  Head-head interaction characterizes the relaxed state of Limulus muscle myosin filaments. , 2009, Journal of molecular biology.

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

[37]  David D. Thomas,et al.  Site-directed spin labeling reveals a conformational switch in the phosphorylation domain of smooth muscle myosin. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[38]  I. Schlichting,et al.  Structure of the regulatory domain of scallop myosin at 2.8 Ä resolution , 1994, Nature.

[39]  S. Lowey,et al.  Myosin subunit interactions. Properties of the 19,000-dalton light chain-deficient myosin. , 1986, The Journal of biological chemistry.

[40]  J. Stull,et al.  Myosin light chain phosphorylation affects the structure of rabbit skeletal muscle thick filaments. , 1996, Biophysical journal.

[41]  D A Winkelmann,et al.  Three-dimensional structure of myosin subfragment-1: a molecular motor. , 1993, Science.

[42]  H. Sweeney,et al.  Spare the rod, spoil the regulation: necessity for a myosin rod. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[43]  W. Rottbauer,et al.  Cardiac Myosin Light Chain-2: A Novel Essential Component of Thick-Myofilament Assembly and Contractility of the Heart , 2006, Circulation research.