Search tips
Search criteria 


Logo of jcellbiolHomeThe Rockefeller University PressEditorsContactInstructions for AuthorsThis issue
J Cell Biol. 1996 July 1; 134(1): 53–66.
PMCID: PMC2120914

Myosin filament structure in vertebrate smooth muscle


The in vivo structure of the myosin filaments in vertebrate smooth muscle is unknown. Evidence from purified smooth muscle myosin and from some studies of intact smooth muscle suggests that they may have a nonhelical, side-polar arrangement of crossbridges. However, the bipolar, helical structure characteristic of myosin filaments in striated muscle has not been disproved for smooth muscle. We have used EM to investigate this question in a functionally diverse group of smooth muscles (from the vascular, gastrointestinal, reproductive, and visual systems) from mammalian, amphibian, and avian species. Intact muscle under physiological conditions, rapidly frozen and then freeze substituted, shows many myosin filaments with a square backbone in transverse profile. Transverse sections of fixed, chemically skinned muscles also show square backbones and, in addition, reveal projections (crossbridges) on only two opposite sides of the square. Filaments gently isolated from skinned smooth muscles and observed by negative staining show crossbridges with a 14.5-nm repeat projecting in opposite directions on opposite sides of the filament. Such filaments subjected to low ionic strength conditions show bare filament ends and an antiparallel arrangement of myosin tails along the length of the filament. All of these observations are consistent with a side-polar structure and argue against a bipolar, helical crossbridge arrangement. We conclude that myosin filaments in all smooth muscles, regardless of function, are likely to be side-polar. Such a structure could be an important factor in the ability of smooth muscles to contract by large amounts.

Full Text

The Full Text of this article is available as a PDF (5.8M).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Ashton FT, Somlyo AV, Somlyo AP. The contractile apparatus of vascular smooth muscle: intermediate high voltage stereo electron microscopy. J Mol Biol. 1975 Oct 15;98(1):17–29. [PubMed]
  • Bülbring E, Golenhofen K. Oxygen consumption by the isolated smooth muscle of guinea-pig taenia coli. J Physiol. 1967 Nov;193(1):213–224. [PubMed]
  • Cooke PH, Kargacin G, Craig R, Fogarty K, Fay FS. Molecular structure and organization of filaments in single, skinned smooth muscle cells. Prog Clin Biol Res. 1987;245:1–25. [PubMed]
  • Cooke PH, Fay FS, Craig R. Myosin filaments isolated from skinned amphibian smooth muscle cells are side-polar. J Muscle Res Cell Motil. 1989 Jun;10(3):206–220. [PubMed]
  • Craig R, Megerman J. Assembly of smooth muscle myosin into side-polar filaments. J Cell Biol. 1977 Dec;75(3):990–996. [PMC free article] [PubMed]
  • Craig R, Alamo L, Padrón R. Structure of the myosin filaments of relaxed and rigor vertebrate striated muscle studied by rapid freezing electron microscopy. J Mol Biol. 1992 Nov 20;228(2):474–487. [PubMed]
  • Cross RA, Engel A. Scanning transmission electron microscopic mass determination of in vitro self-assembled smooth muscle myosin filaments. J Mol Biol. 1991 Dec 5;222(3):455–458. [PubMed]
  • Cross RA, Geeves MA, Kendrick-Jones J. A nucleation--elongation mechanism for the self-assembly of side polar sheets of smooth muscle myosin. EMBO J. 1991 Apr;10(4):747–756. [PubMed]
  • Fay FS, Hoffmann R, Leclair S, Merriam P. Preparation of individual smooth muscle cells from the stomach of Bufo marinus. Methods Enzymol. 1982;85(Pt B):284–292. [PubMed]
  • Gabella G. Structural apparatus for force transmission in smooth muscles. Physiol Rev. 1984 Apr;64(2):455–477. [PubMed]
  • Gordon AM, Huxley AF, Julian FJ. The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol. 1966 May;184(1):170–192. [PubMed]
  • Heuser JE, Reese TS, Dennis MJ, Jan Y, Jan L, Evans L. Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J Cell Biol. 1979 May;81(2):275–300. [PMC free article] [PubMed]
  • Hinssen H, D'Haese J, Small JV, Sobieszek A. Mode of filament assembly of myosins from muscle and nonmuscle cells. J Ultrastruct Res. 1978 Sep;64(3):282–302. [PubMed]
  • Hodgkinson JL, Newman TM, Marston SB, Severs NJ. The structure of the contractile apparatus in ultrarapidly frozen smooth muscle: freeze-fracture, deep-etch, and freeze-substitution studies. J Struct Biol. 1995 Mar-Apr;114(2):93–104. [PubMed]
  • Huxley HE. Structural difference between resting and rigor muscle; evidence from intensity changes in the lowangle equatorial x-ray diagram. J Mol Biol. 1968 Nov 14;37(3):507–520. [PubMed]
  • Huxley HE, Brown W. The low-angle x-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor. J Mol Biol. 1967 Dec 14;30(2):383–434. [PubMed]
  • Kargacin GJ, Fay FS. Physiological and structural properties of saponin-skinned single smooth muscle cells. J Gen Physiol. 1987 Jul;90(1):49–73. [PMC free article] [PubMed]
  • Kensler RW, Levine RJ. An electron microscopic and optical diffraction analysis of the structure of Limulus telson muscle thick filaments. J Cell Biol. 1982 Feb;92(2):443–451. [PMC free article] [PubMed]
  • Knight P, Trinick J. Structure of the myosin projections on native thick filaments from vertebrate skeletal muscle. J Mol Biol. 1984 Aug 15;177(3):461–482. [PubMed]
  • Maw MC, Rowe AJ. Fraying of A-filaments into three subfilaments. Nature. 1980 Jul 24;286(5771):412–414. [PubMed]
  • Padrón R, Alamo L, Craig R, Caputo C. A method for quick-freezing live muscles at known instants during contraction with simultaneous recording of mechanical tension. J Microsc. 1988 Aug;151(Pt 2):81–102. [PubMed]
  • Padrón R, Guerrero JR, Alamo L, Granados M, Gherbesi N, Craig R. Direct visualization of myosin filament symmetry in tarantula striated muscle by electron microscopy. J Struct Biol. 1993 Jul-Aug;111(1):17–21. [PubMed]
  • Shoenberg CF, Haselgrove JC. Filaments and ribbons in vertebrate smooth muscle. Nature. 1974 May 10;249(453):152–154. [PubMed]
  • Shoenberg CF, Needham DM. A study of the mechanism of contraction in vertebrate smooth muscle. Biol Rev Camb Philos Soc. 1976 Feb;51(1):53–104. [PubMed]
  • Small JV. Studies on isolated smooth muscle cells: The contractile apparatus. J Cell Sci. 1977 Apr;24:327–349. [PubMed]
  • Small JV, Squire JM. Structural basis of contraction in vertebrate smooth muscle. J Mol Biol. 1972 Jun 14;67(1):117–149. [PubMed]
  • Small JV, Herzog M, Barth M, Draeger A. Supercontracted state of vertebrate smooth muscle cell fragments reveals myofilament lengths. J Cell Biol. 1990 Dec;111(6 Pt 1):2451–2461. [PMC free article] [PubMed]
  • Smith RC, Cande WZ, Craig R, Tooth PJ, Scholey JM, Kendrick-Jones J. Regulation of myosin filament assembly by light-chain phosphorylation. Philos Trans R Soc Lond B Biol Sci. 1983 Jul 5;302(1108):73–82. [PubMed]
  • Sobieszek A. Cross-bridges on self-assembled smooth muscle myosin filaments. J Mol Biol. 1972 Oct 14;70(3):741–744. [PubMed]
  • Somlyo AP, Somlyo AV, Devine CE, Rice RV. Aggregation of thick filaments into ribbons in mammalian smooth muscle. Nat New Biol. 1971 Jun 23;231(25):243–246. [PubMed]
  • Somlyo AV, Butler TM, Bond M, Somlyo AP. Myosin filaments have non-phosphorylated light chains in relaxed smooth muscle. Nature. 1981 Dec 10;294(5841):567–569. [PubMed]
  • Squire JM. Muscle filament structure and muscle contraction. Annu Rev Biophys Bioeng. 1975;4(00):137–163. [PubMed]
  • Stewart M, Kensler RW. Arrangement of myosin heads in relaxed thick filaments from frog skeletal muscle. J Mol Biol. 1986 Dec 20;192(4):831–851. [PubMed]
  • Stewart PR, Spudich JA. Structural states of dictyostelium myosin. J Supramol Struct. 1979;12(1):1–14. [PubMed]
  • Suzuki H, Onishi H, Takahashi K, Watanabe S. Structure and function of chicken gizzard myosin. J Biochem. 1978 Dec;84(6):1529–1542. [PubMed]
  • Trinick JA. End-filaments: a new structural element of vertebrate skeletal muscle thick filaments. J Mol Biol. 1981 Sep 15;151(2):309–314. [PubMed]
  • Trybus KM, Lowey S. Assembly of smooth muscle myosin minifilaments: effects of phosphorylation and nucleotide binding. J Cell Biol. 1987 Dec;105(6 Pt 2):3007–3019. [PMC free article] [PubMed]
  • Tsukita S, Tsukita S, Usukura J, Ishikawa H. Myosin filaments in smooth muscle cells of the guinea pig taenia coli: a freeze-substitution study. Eur J Cell Biol. 1982 Oct;28(2):195–201. [PubMed]
  • Watanabe M, Takemori S, Yagi N. X-ray diffraction study on mammalian visceral smooth muscles in resting and activated states. J Muscle Res Cell Motil. 1993 Oct;14(5):469–475. [PubMed]
  • Wray JS, Vibert PJ, Cohen C. Diversity of cross-bridge configurations in invertebrate muscles. Nature. 1975 Oct 16;257(5527):561–564. [PubMed]
  • Yanagida T, Ishijima A. Forces and steps generated by single myosin molecules. Biophys J. 1995 Apr;68(4 Suppl):312S–320S. [PubMed]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press