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. 1996 Nov;71(5):2289–2306. doi: 10.1016/S0006-3495(96)79464-X

Structure and periodicities of cross-bridges in relaxation, in rigor, and during contractions initiated by photolysis of caged Ca2+.

T D Lenart 1, J M Murray 1, C Franzini-Armstrong 1, Y E Goldman 1
PMCID: PMC1233720  PMID: 8913571

Abstract

Ultra-rapid freezing and electron microscopy were used to directly observe structural details of frog muscle fibers in rigor, in relaxation, and during force development initiated by laser photolysis of DM-nitrophen (a caged Ca2+). Longitudinal sections from relaxed fibers show helical tracks of the myosin heads on the surface of the thick filaments. Fibers frozen at approximately 13, approximately 34, and approximately 220 ms after activation from the relaxed state by photorelease of Ca2+ all show surprisingly similar cross-bridge dispositions. In sections along the 1,1 lattice plane of activated fibers, individual cross-bridge densities have a wide range of shapes and angles, perpendicular to the fiber axis or pointing toward or away from the Z line. This highly variable distribution is established very early during development of contraction. Cross-bridge density across the interfilament space is more uniform than in rigor, wherein the cross-bridges are more dense near the thin filaments. Optical diffraction (OD) patterns and computed power density spectra of the electron micrographs were used to analyze periodicities of structures within the overlap regions of the sarcomeres. Most aspects of these patterns are consistent with time resolved x-ray diffraction data from the corresponding states of intact muscle, but some features are different, presumably reflecting different origins of contrast between the two methods and possible alterations in the structure of the electron microscopy samples during processing. In relaxed fibers, OD patterns show strong meridional spots and layer lines up to the sixth order of the 43-nm myosin repeat, indicating preservation and resolution of periodic structures smaller than 10 nm. In rigor, layer lines at 18, 24, and 36 nm indicate cross-bridge attachment along the thin filament helix. After activation by photorelease of Ca2+, the 14.3-nm meridional spot is present, but the second-order meridional spot (22 nm) disappears. The myosin 43-nm layer line becomes less intense, and higher orders of 43-nm layer lines disappear. A 36-nm layer line is apparent by 13 ms and becomes progressively stronger while moving laterally away from the meridian of the pattern at later times, indicating cross-bridges labeling the actin helix at decreasing radius.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Amemiya Y., Wakabayashi K., Tanaka H., Ueno Y., Miyahara J. Laser-stimulated luminescence used to measure x-ray diffraction of a contracting striated muscle. Science. 1987 Jul 10;237(4811):164–168. doi: 10.1126/science.3496662. [DOI] [PubMed] [Google Scholar]
  2. Bard F., Franzini-Armstrong C., Ip W. Rigor crossbridges are double-headed in fast muscle from crayfish. J Cell Biol. 1987 Nov;105(5):2225–2234. doi: 10.1083/jcb.105.5.2225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bennett P., Craig R., Starr R., Offer G. The ultrastructural location of C-protein, X-protein and H-protein in rabbit muscle. J Muscle Res Cell Motil. 1986 Dec;7(6):550–567. doi: 10.1007/BF01753571. [DOI] [PubMed] [Google Scholar]
  4. Bordas J., Diakun G. P., Diaz F. G., Harries J. E., Lewis R. A., Lowy J., Mant G. R., Martin-Fernandez M. L., Towns-Andrews E. Two-dimensional time-resolved X-ray diffraction studies of live isometrically contracting frog sartorius muscle. J Muscle Res Cell Motil. 1993 Jun;14(3):311–324. doi: 10.1007/BF00123096. [DOI] [PubMed] [Google Scholar]
  5. Bordas J., Diakun G. P., Harries J. E., Lewis R. A., Mant G. R., Martin-Fernandez M. L., Towns-Andrews E. Two-dimensional time resolved X-ray diffraction of muscle: recent results. Adv Biophys. 1991;27:15–33. doi: 10.1016/0065-227x(91)90005-x. [DOI] [PubMed] [Google Scholar]
  6. Cantino M., Squire J. Resting myosin cross-bridge configuration in frog muscle thick filaments. J Cell Biol. 1986 Feb;102(2):610–618. doi: 10.1083/jcb.102.2.610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cooke R., Crowder M. S., Thomas D. D. Orientation of spin labels attached to cross-bridges in contracting muscle fibres. Nature. 1982 Dec 23;300(5894):776–778. doi: 10.1038/300776a0. [DOI] [PubMed] [Google Scholar]
  8. 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. doi: 10.1016/0022-2836(92)90836-9. [DOI] [PubMed] [Google Scholar]
  9. Craig R., Offer G. The location of C-protein in rabbit skeletal muscle. Proc R Soc Lond B Biol Sci. 1976 Mar 16;192(1109):451–461. doi: 10.1098/rspb.1976.0023. [DOI] [PubMed] [Google Scholar]
  10. Crowther R. A., Padrón R., Craig R. Arrangement of the heads of myosin in relaxed thick filaments from tarantula muscle. J Mol Biol. 1985 Aug 5;184(3):429–439. doi: 10.1016/0022-2836(85)90292-x. [DOI] [PubMed] [Google Scholar]
  11. Duong A. M., Reisler E. Binding of myosin to actin in myofibrils during ATP hydrolysis. Biochemistry. 1989 Feb 7;28(3):1307–1313. doi: 10.1021/bi00429a054. [DOI] [PubMed] [Google Scholar]
  12. Goldman Y. E., Hibberd M. G., Trentham D. R. Relaxation of rabbit psoas muscle fibres from rigor by photochemical generation of adenosine-5'-triphosphate. J Physiol. 1984 Sep;354:577–604. doi: 10.1113/jphysiol.1984.sp015394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Goldman Y. E., Simmons R. M. Active and rigor muscle stiffness [proceedings]. J Physiol. 1977 Jul;269(1):55P–57P. [PubMed] [Google Scholar]
  14. Goldman Y. E., Simmons R. M. Control of sarcomere length in skinned muscle fibres of Rana temporaria during mechanical transients. J Physiol. 1984 May;350:497–518. doi: 10.1113/jphysiol.1984.sp015215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. HUXLEY A. F. Muscle structure and theories of contraction. Prog Biophys Biophys Chem. 1957;7:255–318. [PubMed] [Google Scholar]
  16. Harford J. J., Chew M. W., Squire J. M., Towns-Andrews E. Crossbridge states in isometrically contracting fish muscle: evidence for swinging of myosin heads on actin. Adv Biophys. 1991;27:45–61. doi: 10.1016/0065-227x(91)90007-z. [DOI] [PubMed] [Google Scholar]
  17. Harford J. J., Squire J. M. Evidence for structurally different attached states of myosin cross-bridges on actin during contraction of fish muscle. Biophys J. 1992 Aug;63(2):387–396. doi: 10.1016/S0006-3495(92)81613-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Haselgrove J. C. A model of myosin crossbridge structure consistent with the low-angle x-ray diffraction pattern of vertebrate muscle. J Muscle Res Cell Motil. 1980 Jun;1(2):177–191. doi: 10.1007/BF00711798. [DOI] [PubMed] [Google Scholar]
  19. Haselgrove J. C., Huxley H. E. X-ray evidence for radial cross-bridge movement and for the sliding filament model in actively contracting skeletal muscle. J Mol Biol. 1973 Jul 15;77(4):549–568. doi: 10.1016/0022-2836(73)90222-2. [DOI] [PubMed] [Google Scholar]
  20. Hawkins C. J., Bennett P. M. Evaluation of freeze substitution in rabbit skeletal muscle. Comparison of electron microscopy to X-ray diffraction. J Muscle Res Cell Motil. 1995 Jun;16(3):303–318. doi: 10.1007/BF00121139. [DOI] [PubMed] [Google Scholar]
  21. Heuser J. E., Cooke R. Actin-myosin interactions visualized by the quick-freeze, deep-etch replica technique. J Mol Biol. 1983 Sep 5;169(1):97–122. doi: 10.1016/s0022-2836(83)80177-6. [DOI] [PubMed] [Google Scholar]
  22. Heuser J. E., Reese T. S., Dennis M. J., 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. doi: 10.1083/jcb.81.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hirose K., Franzini-Armstrong C., Goldman Y. E., Murray J. M. Structural changes in muscle crossbridges accompanying force generation. J Cell Biol. 1994 Nov;127(3):763–778. doi: 10.1083/jcb.127.3.763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hirose K., Lenart T. D., Murray J. M., Franzini-Armstrong C., Goldman Y. E. Flash and smash: rapid freezing of muscle fibers activated by photolysis of caged ATP. Biophys J. 1993 Jul;65(1):397–408. doi: 10.1016/S0006-3495(93)81061-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hirose K., Wakabayashi T. Conformations of crossbridges in contracting skeletal muscle. Adv Biophys. 1991;27:197–203. doi: 10.1016/0065-227x(91)90018-9. [DOI] [PubMed] [Google Scholar]
  26. Holmes K. C., Popp D., Gebhard W., Kabsch W. Atomic model of the actin filament. Nature. 1990 Sep 6;347(6288):44–49. doi: 10.1038/347044a0. [DOI] [PubMed] [Google Scholar]
  27. Huxley H. E., 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. doi: 10.1016/s0022-2836(67)80046-9. [DOI] [PubMed] [Google Scholar]
  28. Huxley H. E., Faruqi A. R., Bordas J., Koch M. H., Milch J. R. The use of synchrotron radiation in time-resolved X-ray diffraction studies of myosin layer-line reflections during muscle contraction. Nature. 1980 Mar 13;284(5752):140–143. doi: 10.1038/284140a0. [DOI] [PubMed] [Google Scholar]
  29. Huxley H. E., Faruqi A. R., Kress M., Bordas J., Koch M. H. Time-resolved X-ray diffraction studies of the myosin layer-line reflections during muscle contraction. J Mol Biol. 1982 Jul 15;158(4):637–684. doi: 10.1016/0022-2836(82)90253-4. [DOI] [PubMed] [Google Scholar]
  30. Huxley H. E., Kress M. Crossbridge behaviour during muscle contraction. J Muscle Res Cell Motil. 1985 Apr;6(2):153–161. doi: 10.1007/BF00713057. [DOI] [PubMed] [Google Scholar]
  31. Huxley H. E., Simmons R. M., Faruqi A. R., Kress M., Bordas J., Koch M. H. Millisecond time-resolved changes in x-ray reflections from contracting muscle during rapid mechanical transients, recorded using synchrotron radiation. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2297–2301. doi: 10.1073/pnas.78.4.2297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Huxley H. E. The mechanism of muscular contraction. Science. 1969 Jun 20;164(3886):1356–1365. doi: 10.1126/science.164.3886.1356. [DOI] [PubMed] [Google Scholar]
  33. Ip W., Heuser J. Direct visualization of the myosin crossbridge helices on relaxed rabbit psoas thick filaments. J Mol Biol. 1983 Nov 25;171(1):105–109. doi: 10.1016/s0022-2836(83)80317-9. [DOI] [PubMed] [Google Scholar]
  34. Irving M., Lombardi V., Piazzesi G., Ferenczi M. A. Myosin head movements are synchronous with the elementary force-generating process in muscle. Nature. 1992 May 14;357(6374):156–158. doi: 10.1038/357156a0. [DOI] [PubMed] [Google Scholar]
  35. Kaplan J. H., Ellis-Davies G. C. Photolabile chelators for the rapid photorelease of divalent cations. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6571–6575. doi: 10.1073/pnas.85.17.6571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kensler R. W., Levine R. J. 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. doi: 10.1083/jcb.92.2.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kensler R. W., Stewart M. AN ultrastructural study of cross-bridge arrangement in the frog thigh muscle thick filament. Biophys J. 1986 Jan;49(1):343–351. doi: 10.1016/S0006-3495(86)83647-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Kensler R. W., Stewart M. An ultrastructural study of crossbridge arrangement in the fish skeletal muscle thick filament. J Cell Sci. 1989 Nov;94(Pt 3):391–401. doi: 10.1242/jcs.94.3.391. [DOI] [PubMed] [Google Scholar]
  39. Kensler R. W., Stewart M. Frog skeletal muscle thick filaments are three-stranded. J Cell Biol. 1983 Jun;96(6):1797–1802. doi: 10.1083/jcb.96.6.1797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Kress M., Huxley H. E., Faruqi A. R., Hendrix J. Structural changes during activation of frog muscle studied by time-resolved X-ray diffraction. J Mol Biol. 1986 Apr 5;188(3):325–342. doi: 10.1016/0022-2836(86)90158-0. [DOI] [PubMed] [Google Scholar]
  41. Lenart T. D., Allen T. S., Barsotti R. J., Ellis-Davies G. C., Kaplan J. H., Franzini-Armstrong C., Goldman Y. E. Mechanics and structure of cross-bridges during contractions initiated by photolysis of caged Ca2+. Adv Exp Med Biol. 1993;332:475–487. doi: 10.1007/978-1-4615-2872-2_43. [DOI] [PubMed] [Google Scholar]
  42. Levine R. J., Kensler R. W., Yang Z., Sweeney H. L. Myosin regulatory light chain phosphorylation and the production of functionally significant changes in myosin head arrangement on striated muscle thick filaments. Biophys J. 1995 Apr;68(4 Suppl):224S–224S. [PMC free article] [PubMed] [Google Scholar]
  43. Lowy J., Popp D., Stewart A. A. X-ray studies of order-disorder transitions in the myosin heads of skinned rabbit psoas muscles. Biophys J. 1991 Oct;60(4):812–824. doi: 10.1016/S0006-3495(91)82116-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Magid A., Reedy M. K. X-ray diffraction observations of chemically skinned frog skeletal muscle processed by an improved method. Biophys J. 1980 Apr;30(1):27–40. doi: 10.1016/S0006-3495(80)85074-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Matsubara I., Yagi N., Hashizume H. Use of an X-ray television for diffraction of the frog striated muscle. Nature. 1975 Jun 26;255(5511):728–729. doi: 10.1038/255728a0. [DOI] [PubMed] [Google Scholar]
  46. Matsubara I., Yagi N., Miura H., Ozeki M., Izumi T. Intensification of the 5.9-nm actin layer line in contracting muscle. 1984 Nov 29-Dec 5Nature. 312(5993):471–473. doi: 10.1038/312471a0. [DOI] [PubMed] [Google Scholar]
  47. Milligan R. A., Whittaker M., Safer D. Molecular structure of F-actin and location of surface binding sites. Nature. 1990 Nov 15;348(6298):217–221. doi: 10.1038/348217a0. [DOI] [PubMed] [Google Scholar]
  48. Nassar R., Wallace N. R., Taylor I., Sommer J. R. The quick-freezing of single intact skeletal muscle fibers at known time intervals following electrical stimulation. Scan Electron Microsc. 1986;(Pt 1):309–328. [PubMed] [Google Scholar]
  49. 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. doi: 10.1111/j.1365-2818.1988.tb04616.x. [DOI] [PubMed] [Google Scholar]
  50. Padrón R., Craig R. Disorder induced in nonoverlap myosin cross-bridges by loss of adenosine triphosphate. Biophys J. 1989 Nov;56(5):927–933. doi: 10.1016/S0006-3495(89)82738-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Padrón R., Huxley H. E. The effect of the ATP analogue AMPPNP on the structure of crossbridges in vertebrate skeletal muscles: X-ray diffraction and mechanical studies. J Muscle Res Cell Motil. 1984 Dec;5(6):613–655. doi: 10.1007/BF00713923. [DOI] [PubMed] [Google Scholar]
  52. Pepe F. A., Drucker B. The myosin filament. III. C-protein. J Mol Biol. 1975 Dec 25;99(4):609–617. doi: 10.1016/s0022-2836(75)80175-6. [DOI] [PubMed] [Google Scholar]
  53. Persechini A., Rowe A. J. Modulation of myosin filament conformation by physiological levels of divalent cation. J Mol Biol. 1984 Jan 5;172(1):23–39. doi: 10.1016/0022-2836(84)90412-1. [DOI] [PubMed] [Google Scholar]
  54. Poole K. J., Maeda Y., Rapp G., Goody R. S. Dynamic X-ray diffraction measurements following photolytic relaxation and activation of skinned rabbit psoas fibres. Adv Biophys. 1991;27:63–75. doi: 10.1016/0065-227x(91)90008-2. [DOI] [PubMed] [Google Scholar]
  55. Popp D., Maeda Y., Stewart A. A., Holmes K. C. X-ray diffraction studies on muscle regulation. Adv Biophys. 1991;27:89–103. doi: 10.1016/0065-227x(91)90010-b. [DOI] [PubMed] [Google Scholar]
  56. Rayment I., Rypniewski W. R., Schmidt-Bäse K., Smith R., Tomchick D. R., Benning M. M., Winkelmann D. A., Wesenberg G., Holden H. M. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science. 1993 Jul 2;261(5117):50–58. doi: 10.1126/science.8316857. [DOI] [PubMed] [Google Scholar]
  57. Reedy M. K., Holmes K. C., Tregear R. T. Induced changes in orientation of the cross-bridges of glycerinated insect flight muscle. Nature. 1965 Sep 18;207(5003):1276–1280. doi: 10.1038/2071276a0. [DOI] [PubMed] [Google Scholar]
  58. Reisler E., Liu J., Cheung P. Role of magnesium binding to myosin in controlling the state of cross-bridges in skeletal rabbit muscle. Biochemistry. 1983 Oct 11;22(21):4954–4960. doi: 10.1021/bi00290a012. [DOI] [PubMed] [Google Scholar]
  59. Rome E. M., Hirabayashi T., Perry S. V. X-ray diffraction of muscle labelled with antibody to troponin-C. Nat New Biol. 1973 Aug 1;244(135):154–155. doi: 10.1038/newbio244154a0. [DOI] [PubMed] [Google Scholar]
  60. Rome E., Offer G., Pepe F. A. X-ray diffraction of muscle labelled with antibody to C-protein. Nat New Biol. 1973 Aug 1;244(135):152–154. doi: 10.1038/newbio244152a0. [DOI] [PubMed] [Google Scholar]
  61. Sosa H., Popp D., Ouyang G., Huxley H. E. Ultrastructure of skeletal muscle fibers studied by a plunge quick freezing method: myofilament lengths. Biophys J. 1994 Jul;67(1):283–292. doi: 10.1016/S0006-3495(94)80479-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Stewart M., Kensler R. W. Arrangement of myosin heads in relaxed thick filaments from frog skeletal muscle. J Mol Biol. 1986 Dec 20;192(4):831–851. doi: 10.1016/0022-2836(86)90032-x. [DOI] [PubMed] [Google Scholar]
  63. Suzuki S., Oshimi Y., Sugi H. Freeze-fracture studies on the cross-bridge angle distribution at various states and the thin filament stiffness in single skinned frog muscle fibers. J Electron Microsc (Tokyo) 1993 Apr;42(2):107–116. [PubMed] [Google Scholar]
  64. Sweeney H. L., Yang Z., Zhi G., Stull J. T., Trybus K. M. Charge replacement near the phosphorylatable serine of the myosin regulatory light chain mimics aspects of phosphorylation. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1490–1494. doi: 10.1073/pnas.91.4.1490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Taylor K. A., Reedy M. C., Córdova L., Reedy M. K. Three-dimensional reconstruction of rigor insect flight muscle from tilted thin sections. 1984 Jul 26-Aug 1Nature. 310(5975):285–291. doi: 10.1038/310285a0. [DOI] [PubMed] [Google Scholar]
  66. Tsukita S., Yano M. Actomyosin structure in contracting muscle detected by rapid freezing. Nature. 1985 Sep 12;317(6033):182–184. doi: 10.1038/317182a0. [DOI] [PubMed] [Google Scholar]
  67. Ueno H., Harrington W. F. Cross-bridge movement and the conformational state of the myosin hinge in skeletal muscle. J Mol Biol. 1981 Jul 15;149(4):619–640. doi: 10.1016/0022-2836(81)90350-8. [DOI] [PubMed] [Google Scholar]
  68. Varriano-Marston E., Franzini-Armstrong C., Haselgrove J. C. The structure and disposition of crossbridges in deep-etched fish muscle. J Muscle Res Cell Motil. 1984 Aug;5(4):363–386. doi: 10.1007/BF00818256. [DOI] [PubMed] [Google Scholar]
  69. Wakabayashi K., Tanaka H., Saito H., Moriwaki N., Ueno Y., Amemiya Y. Dynamic X-ray diffraction of skeletal muscle contraction: structural change of actin filaments. Adv Biophys. 1991;27:3–13. doi: 10.1016/0065-227x(91)90004-w. [DOI] [PubMed] [Google Scholar]
  70. Wakabayashi T., Akiba T., Hirose K., Tomioka A., Tokunaga M., Suzuki M., Toyoshima C., Sutoh K., Yamamoto K., Matsumoto T. Temperature-induced change of thick filament and location of the functional sites of myosin. Adv Exp Med Biol. 1988;226:39–48. [PubMed] [Google Scholar]
  71. Xie X., Harrison D. H., Schlichting I., Sweet R. M., Kalabokis V. N., Szent-Györgyi A. G., Cohen C. Structure of the regulatory domain of scallop myosin at 2.8 A resolution. Nature. 1994 Mar 24;368(6469):306–312. doi: 10.1038/368306a0. [DOI] [PubMed] [Google Scholar]
  72. Yagi N. Intensification of the first actin layer-line during contraction of frog skeletal muscle. Adv Biophys. 1991;27:35–43. doi: 10.1016/0065-227x(91)90006-y. [DOI] [PubMed] [Google Scholar]
  73. Yagi N., Ito M. H., Nakajima H., Izumi T., Matsubara I. Return of myosin heads to thick filaments after muscle contraction. Science. 1977 Aug 12;197(4304):685–687. doi: 10.1126/science.301660. [DOI] [PubMed] [Google Scholar]
  74. Yagi N., Matsubara I. Myosin heads do not move on activation in highly stretched vertebrate striated muscle. Science. 1980 Jan 18;207(4428):307–308. doi: 10.1126/science.6444254. [DOI] [PubMed] [Google Scholar]
  75. Yagi N., Matsubara I. Structural changes in the thin filament during activation studied by X-ray diffraction of highly stretched skeletal muscle. J Mol Biol. 1989 Jul 20;208(2):359–363. doi: 10.1016/0022-2836(89)90396-3. [DOI] [PubMed] [Google Scholar]
  76. Yagi N., O'Brien E. J., Matsubara I. Changes of thick filament structure during contraction of frog striated muscle. Biophys J. 1981 Jan;33(1):121–137. doi: 10.1016/S0006-3495(81)84876-X. [DOI] [PMC free article] [PubMed] [Google Scholar]

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