Thick filament length and isoform composition determine self-organized contractile units in actomyosin bundles

Biophysical Journal

Volumn 104, Issue 3, 2013, Pages 655-665

  Thoresen, Todd ^a   Lenz, Martin ^b,c,d   Gardel, Margaret L ^a,b,c  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d UNIVERSITÉ PARIS SUD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ISOPROTEIN; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN II;

ANIMAL; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CHICKEN; CYTOSKELETON; FLUORESCENCE MICROSCOPY; HUMAN; PROTEIN MULTIMERIZATION; SKELETAL MUSCLE; SMOOTH MUSCLE; THROMBOCYTE; TURKEY (BIRD); ULTRASTRUCTURE;

ACTINS; ACTOMYOSIN; ANIMALS; BLOOD PLATELETS; CHICKENS; CYTOSKELETON; HUMANS; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; MUSCLE, SKELETAL; MUSCLE, SMOOTH; MYOSIN TYPE II; PROTEIN ISOFORMS; PROTEIN MULTIMERIZATION; TURKEYS;

EID: 84873362091     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.12.042     Document Type: Article

References (43)

1. M. Vicente-Manzanares, and X. Ma A.R. Horwitz Non-muscle myosin II takes centre stage in cell adhesion and migration Nat. Rev. Mol. Cell Biol. 10 2009 778 790
2. M.L. Gardel, and I.C. Schneider C.M. Waterman Mechanical integration of actin and adhesion dynamics in cell migration Annu. Rev. Cell Dev. Biol. 26 2010 3.1-3.19
3. F. Matsumura Regulation of myosin II during cytokinesis in higher eukaryotes Trends Cell Biol. 15 2005 371 377
4. A. Carvalho, A. Desai, and K. Oegema Structural memory in the contractile ring makes the duration of cytokinesis independent of cell size Cell 137 2009 926 937
5. A.M. Gordon, E. Homsher, and M. Regnier Regulation of contraction in striated muscle Physiol. Rev. 80 2000 853 924
6. M. Löfgren, U. Malmqvist, and A. Arner Substrate and product dependence of force and shortening in fast and slow smooth muscle J. Gen. Physiol. 117 2001 407 418
7. T. Lecuit, P.F. Lenne, and E. Munro Force generation, transmission, and integration during cell and tissue morphogenesis Annu. Rev. Cell Dev. Biol. 27 2011 157 184
8. A.F. Huxley Muscle structure and theories of contraction Prog. Biophys. Biophys. Chem. 7 1957 255 318
9. H.L. Sweeney, and A. Houdusse Structural and functional insights into the Myosin motor mechanism Annu. Rev. Biophys. 39 2010 539 557
10. K.A. Edman The velocity of unloaded shortening and its relation to sarcomere length and isometric force in vertebrate muscle fibres J. Physiol. 291 1979 143 159
11. A.M. Herrera, and B.E. McParland C.Y. Seow 'Sarcomeres' of smooth muscle: functional characteristics and ultrastructural evidence J. Cell Sci. 118 2005 2381 2392
12. C.M. Hai, and R.A. Murphy Regulation of shortening velocity by cross-bridge phosphorylation in smooth muscle Am. J. Physiol. 255 1988 C86 C94
13. U. Malmqvist, and A. Arner Correlation between isoform composition of the 17 kDa myosin light chain and maximal shortening velocity in smooth muscle Pflugers Arch. 418 1991 523 530
14. K. Tanner, and A. Boudreau S. Kumar Dissecting regional variations in stress fiber mechanics in living cells with laser nanosurgery Biophys. J. 99 2010 2775 2783
15. K. Katoh, and Y. Kano K. Fujiwara Isolation and contraction of the stress fiber Mol. Biol. Cell 9 1998 1919 1938
16. M. Bárány ATPase activity of myosin correlated with speed of muscle shortening J. Gen. Physiol. 50 Suppl. 6 1967 197 218
17. G. Ijpma, and A.M. Al-Jumaily G.C. Sieck Myosin filament polymerization and depolymerization in a model of partial length adaptation in airway smooth muscle J. Appl. Physiol. 111 2011 735 742
18. C.Y. Seow Myosin filament assembly in an ever-changing myofilament lattice of smooth muscle Am. J. Physiol. Cell Physiol. 289 2005 C1363 C1368
19. T. Thoresen, M. Lenz, and M.L. Gardel Reconstitution of contractile actomyosin bundles Biophys. J. 100 2011 2698 2705
20. M. Lenz, and T. Thoresen A.R. Dinner Contractile units in disordered actomyosin bundles arise from F-actin buckling Phys. Rev. Lett. 108 2012 238107
21. R.S. Adelstein, and C.B. Klee Purification and characterization of smooth muscle myosin light chain kinase J. Biol. Chem. 256 1981 7501 7509
22. D.R. Kovar, and J.R. Kuhn T.D. Pollard The fission yeast cytokinesis formin Cdc12p is a barbed end actin filament capping protein gated by profilin J. Cell Biol. 161 2003 875 887
23. L. Skubiszak, and L. Kowalczyk Myosin molecule packing within the vertebrate skeletal muscle thick filaments. A complete bipolar model Acta Biochim. Pol. 49 2002 829 840
24. Y. Aratyn-Schaus, and P.W. Oakes M.L. Gardel Preparation of complaint matrices for quantifying cellular contraction J. Vis. Exp. 14 2010 46
25. T. Yeung, and P.C. Georges P.A. Janmey Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion Cell Motil. Cytoskeleton 60 2005 24 34
26. R. Craig, and J. Megerman Assembly of smooth muscle myosin into side-polar filaments J. Cell Biol. 75 1977 990 996
27. R. Niederman, and T.D. Pollard Human platelet myosin. II. In vitro assembly and structure of myosin filaments J. Cell Biol. 67 1975 72 92
28. A.S. Rovner, and P.M. Fagnant K.M. Trybus The carboxyl-terminal isoforms of smooth muscle myosin heavy chain determine thick filament assembly properties J. Cell Biol. 156 2002 113 123
29. H.E. Huxley Electron microscope studies on the structure of natural and synthetic protein filaments from striated muscle J. Mol. Biol. 7 1963 281 308
30. B. Achim, and S.S. Ulrich Coupling biochemistry and mechanics in cell adhesion: a model for inhomogeneous stress fiber contraction New J. Phys. 9 2007 425
31. A. Draeger, and W.B. Amos J.V. Small The cytoskeletal and contractile apparatus of smooth muscle: contraction bands and segmentation of the contractile elements J. Cell Biol. 111 1990 2463 2473
32. W.T. Gerthoffer Regulation of the contractile element of airway smooth muscle Am. J. Physiol. 261 1991 L15 L28
33. R.J. Russell, and S.L. Xia T.P. Lele Sarcomere mechanics in capillary endothelial cells Biophys. J. 97 2009 1578 1585
34. A. Kishino, and T. Yanagida Force measurements by micromanipulation of a single actin filament by glass needles Nature 334 1988 74 76
35. F.T. Ashton, A.V. Somlyo, and A.P. Somlyo The contractile apparatus of vascular smooth muscle: intermediate high voltage stereo electron microscopy J. Mol. Biol. 98 1975 17 29
36. C.Y. Seow, V.R. Pratusevich, and L.E. Ford Series-to-parallel transition in the filament lattice of airway smooth muscle J. Appl. Physiol. 89 2000 869 876
37. G. Cuda, and E. Pate J.R. Sellers In vitro actin filament sliding velocities produced by mixtures of different types of myosin Biophys. J. 72 1997 1767 1779
38. S. Umemoto, and J.R. Sellers Characterization of in vitro motility assays using smooth muscle and cytoplasmic myosins J. Biol. Chem. 265 1990 14864 14869
39. D.E. Harris, and D.M. Warshaw Smooth and skeletal muscle myosin both exhibit low duty cycles at zero load in vitro J. Biol. Chem. 268 1993 14764 14768
40. M.J. Tyska, and D.E. Dupuis S. Lowey Two heads of myosin are better than one for generating force and motion Proc. Natl. Acad. Sci. USA 96 1999 4402 4407
41. J.E. Molloy, and J.E. Burns D.C. White Movement and force produced by a single myosin head Nature 378 1995 209 212
42. A. Sobieszek Cross-bridges on self-assembled smooth muscle myosin filaments J. Mol. Biol. 70 1972 741 744
43. P. Tonino, M. Simon, and R. Craig Mass determination of native smooth muscle myosin filaments by scanning transmission electron microscopy J. Mol. Biol. 318 2002 999 1007