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. 2002 Aug;83(2):1050–1073. doi: 10.1016/S0006-3495(02)75230-2

Polarized fluorescence depletion reports orientation distribution and rotational dynamics of muscle cross-bridges.

Marcus G Bell 1, Robert E Dale 1, Uulke A van der Heide 1, Yale E Goldman 1
PMCID: PMC1302208  PMID: 12124286

Abstract

The method of polarized fluorescence depletion (PFD) has been applied to enhance the resolution of orientational distributions and dynamics obtained from fluorescence polarization (FP) experiments on ordered systems, particularly in muscle fibers. Previous FP data from single fluorescent probes were limited to the 2(nd)- and 4(th)-rank order parameters, <P(2)(cos beta)> and <P(4)(cos beta)>, of the probe angular distribution (beta) relative to the fiber axis and <P(2d)>, a coefficient describing the extent of rapid probe motions. We applied intense 12-micros polarized photoselection pulses to transiently populate the triplet state of rhodamine probes and measured the polarization of the ground-state depletion using a weak interrogation beam. PFD provides dynamic information describing the extent of motions on the time scale between the fluorescence lifetime (e.g., 4 ns) and the duration of the photoselection pulse and it potentially supplies information about the probe angular distribution corresponding to order parameters above rank 4. Gizzard myosin regulatory light chain (RLC) was labeled with the 6-isomer of iodoacetamidotetramethylrhodamine and exchanged into rabbit psoas muscle fibers. In active contraction, dynamic motions of the RLC on the PFD time scale were intermediate between those observed in relaxation and rigor. The results indicate that previously observed disorder of the light chain region in contraction can be ascribed principally to dynamic motions on the microsecond time scale.

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Selected References

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

  1. Adhikari B., Hideg K., Fajer P. G. Independent mobility of catalytic and regulatory domains of myosin heads. Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9643–9647. doi: 10.1073/pnas.94.18.9643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Allen T. S., Ling N., Irving M., Goldman Y. E. Orientation changes in myosin regulatory light chains following photorelease of ATP in skinned muscle fibers. Biophys J. 1996 Apr;70(4):1847–1862. doi: 10.1016/S0006-3495(96)79750-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Axelrod D., Koppel D. E., Schlessinger J., Elson E., Webb W. W. Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys J. 1976 Sep;16(9):1055–1069. doi: 10.1016/S0006-3495(76)85755-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baker J. E., Brust-Mascher I., Ramachandran S., LaConte L. E., Thomas D. D. A large and distinct rotation of the myosin light chain domain occurs upon muscle contraction. Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):2944–2949. doi: 10.1073/pnas.95.6.2944. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barnett V. A., Thomas D. D. Microsecond rotational motion of spin-labeled myosin heads during isometric muscle contraction. Saturation transfer electron paramagnetic resonance. Biophys J. 1989 Sep;56(3):517–523. doi: 10.1016/S0006-3495(89)82698-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Barnett V. A., Thomas D. D. Saturation transfer electron paramagnetic resonance of spin-labeled muscle fibers. Dependence of myosin head rotational motion on sarcomere length. J Mol Biol. 1984 Oct 15;179(1):83–102. doi: 10.1016/0022-2836(84)90307-3. [DOI] [PubMed] [Google Scholar]
  7. Berger C. L., Craik J. S., Trentham D. R., Corrie J. E., Goldman Y. E. Fluorescence polarization of skeletal muscle fibers labeled with rhodamine isomers on the myosin heavy chain. Biophys J. 1996 Dec;71(6):3330–3343. doi: 10.1016/S0006-3495(96)79526-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Berger C. L., Thomas D. D. Rotational dynamics of actin-bound myosin heads in active myofibrils. Biochemistry. 1993 Apr 13;32(14):3812–3821. doi: 10.1021/bi00065a038. [DOI] [PubMed] [Google Scholar]
  9. Borejdo J., Assulin O., Ando T., Putnam S. Cross-bridge orientation in skeletal muscle measured by linear dichroism of an extrinsic chromophore. J Mol Biol. 1982 Jul 5;158(3):391–414. doi: 10.1016/0022-2836(82)90205-4. [DOI] [PubMed] [Google Scholar]
  10. Burghardt T. P., Garamszegi S. P., Ajtai K. Probes bound to myosin Cys-707 rotate during length transients in contraction. Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9631–9636. doi: 10.1073/pnas.94.18.9631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. CHEN R. F., BOWMAN R. L. FLUORESCENCE POLARIZATION: MEASUREMENT WITH ULTRAVIOLET-POLARIZING FILTERS IN A SPECTROPHOTOFLUOROMETER. Science. 1965 Feb 12;147(3659):729–732. doi: 10.1126/science.147.3659.729. [DOI] [PubMed] [Google Scholar]
  12. Calhoun D. B., Vanderkooi J. M., Woodrow G. V., 3rd, Englander S. W. Penetration of dioxygen into proteins studied by quenching of phosphorescence and fluorescence. Biochemistry. 1983 Mar 29;22(7):1526–1532. doi: 10.1021/bi00276a002. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Cooke R. Stress does not alter the conformation of a domain of the myosin cross-bridge in rigor muscle fibres. Nature. 1981 Dec 10;294(5841):570–571. doi: 10.1038/294570a0. [DOI] [PubMed] [Google Scholar]
  15. Cooke R. The mechanism of muscle contraction. CRC Crit Rev Biochem. 1986;21(1):53–118. doi: 10.3109/10409238609113609. [DOI] [PubMed] [Google Scholar]
  16. Corin A. F., Blatt E., Jovin T. M. Triplet-state detection of labeled proteins using fluorescence recovery spectroscopy. Biochemistry. 1987 Apr 21;26(8):2207–2217. doi: 10.1021/bi00382a021. [DOI] [PubMed] [Google Scholar]
  17. Corrie J. E., Brandmeier B. D., Ferguson R. E., Trentham D. R., Kendrick-Jones J., Hopkins S. C., van der Heide U. A., Goldman Y. E., Sabido-David C., Dale R. E. Dynamic measurement of myosin light-chain-domain tilt and twist in muscle contraction. Nature. 1999 Jul 29;400(6743):425–430. doi: 10.1038/22704. [DOI] [PubMed] [Google Scholar]
  18. Dale R. E., Hopkins S. C., an der Heide U. A., Marszałek T., Irving M., Goldman Y. E. Model-independent analysis of the orientation of fluorescent probes with restricted mobility in muscle fibers. Biophys J. 1999 Mar;76(3):1606–1618. doi: 10.1016/S0006-3495(99)77320-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Dobbie I., Linari M., Piazzesi G., Reconditi M., Koubassova N., Ferenczi M. A., Lombardi V., Irving M. Elastic bending and active tilting of myosin heads during muscle contraction. Nature. 1998 Nov 26;396(6709):383–387. doi: 10.1038/24647. [DOI] [PubMed] [Google Scholar]
  20. Dobrowolski Z., Xu G. Q., Hitchcock-DeGregori S. E. Modified calcium-dependent regulatory function of troponin C central helix mutants. J Biol Chem. 1991 Mar 25;266(9):5703–5710. [PubMed] [Google Scholar]
  21. Dominguez R., Freyzon Y., Trybus K. M., Cohen C. 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. Cell. 1998 Sep 4;94(5):559–571. doi: 10.1016/s0092-8674(00)81598-6. [DOI] [PubMed] [Google Scholar]
  22. Fajer P. G., Fajer E. A., Thomas D. D. Myosin heads have a broad orientational distribution during isometric muscle contraction: time-resolved EPR studies using caged ATP. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5538–5542. doi: 10.1073/pnas.87.14.5538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Fisher A. J., Smith C. A., Thoden J. B., Smith R., Sutoh K., Holden H. M., Rayment I. X-ray structures of the myosin motor domain of Dictyostelium discoideum complexed with MgADP.BeFx and MgADP.AlF4-. Biochemistry. 1995 Jul 18;34(28):8960–8972. doi: 10.1021/bi00028a004. [DOI] [PubMed] [Google Scholar]
  24. Geeves M. A., Holmes K. C. Structural mechanism of muscle contraction. Annu Rev Biochem. 1999;68:687–728. doi: 10.1146/annurev.biochem.68.1.687. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. 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]
  27. Goldman Y. E. Wag the tail: structural dynamics of actomyosin. Cell. 1998 Apr 3;93(1):1–4. doi: 10.1016/s0092-8674(00)81137-x. [DOI] [PubMed] [Google Scholar]
  28. Hambly B., Franks K., Cooke R. Paramagnetic probes attached to a light chain on the myosin head are highly disordered in active muscle fibers. Biophys J. 1992 Nov;63(5):1306–1313. doi: 10.1016/S0006-3495(92)81717-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hellen E. H., Burghardt T. P. Saturation effects in polarized fluorescence photobleaching recovery and steady state fluorescence polarization. Biophys J. 1994 Mar;66(3 Pt 1):891–897. doi: 10.1016/s0006-3495(94)80865-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Highsmith S., Eden D. Myosin subfragment 1 has tertiary structural domains. Biochemistry. 1986 Apr 22;25(8):2237–2242. doi: 10.1021/bi00356a058. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Hopkins S. C., Sabido-David C., Corrie J. E., Irving M., Goldman Y. E. Fluorescence polarization transients from rhodamine isomers on the myosin regulatory light chain in skeletal muscle fibers. Biophys J. 1998 Jun;74(6):3093–3110. doi: 10.1016/S0006-3495(98)78016-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Houdusse A., Kalabokis V. N., Himmel D., Szent-Györgyi A. G., Cohen C. Atomic structure of scallop myosin subfragment S1 complexed with MgADP: a novel conformation of the myosin head. Cell. 1999 May 14;97(4):459–470. doi: 10.1016/s0092-8674(00)80756-4. [DOI] [PubMed] [Google Scholar]
  34. Huxley A. F., Simmons R. M. Proposed mechanism of force generation in striated muscle. Nature. 1971 Oct 22;233(5321):533–538. doi: 10.1038/233533a0. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. 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]
  37. Huxley H. E., Simmons R. M., Faruqi A. R., Kress M., Bordas J., Koch M. H. Changes in the X-ray reflections from contracting muscle during rapid mechanical transients and their structural implications. J Mol Biol. 1983 Sep 15;169(2):469–506. doi: 10.1016/s0022-2836(83)80062-x. [DOI] [PubMed] [Google Scholar]
  38. Irving M., St Claire Allen T., Sabido-David C., Craik J. S., Brandmeier B., Kendrick-Jones J., Corrie J. E., Trentham D. R., Goldman Y. E. Tilting of the light-chain region of myosin during step length changes and active force generation in skeletal muscle. Nature. 1995 Jun 22;375(6533):688–691. doi: 10.1038/375688a0. [DOI] [PubMed] [Google Scholar]
  39. Ishii Y., Ishijima A., Yanagida T. Single molecule nanomanipulation of biomolecules. Trends Biotechnol. 2001 Jun;19(6):211–216. doi: 10.1016/s0167-7799(01)01635-3. [DOI] [PubMed] [Google Scholar]
  40. Johnson P., Garland P. B. Depolarization of fluorescence depletion. A microscopic method for measuring rotational diffusion of membrane proteins on the surface of a single cell. FEBS Lett. 1981 Sep 28;132(2):252–256. doi: 10.1016/0014-5793(81)81172-6. [DOI] [PubMed] [Google Scholar]
  41. Johnson P., Garland P. B. Fluorescent triplet probes for measuring the rotational diffusion of membrane proteins. Biochem J. 1982 Apr 1;203(1):313–321. doi: 10.1042/bj2030313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Kao H. P., Verkman A. S. Construction and performance of a photobleaching recovery apparatus with microsecond time resolution. Biophys Chem. 1996 Mar 7;59(1-2):203–210. doi: 10.1016/0301-4622(95)00139-5. [DOI] [PubMed] [Google Scholar]
  43. Kinosita K., Jr, Kawato S., Ikegami A. A theory of fluorescence polarization decay in membranes. Biophys J. 1977 Dec;20(3):289–305. doi: 10.1016/S0006-3495(77)85550-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Lenart T. D., Murray J. M., Franzini-Armstrong C., Goldman Y. E. Structure and periodicities of cross-bridges in relaxation, in rigor, and during contractions initiated by photolysis of caged Ca2+. Biophys J. 1996 Nov;71(5):2289–2306. doi: 10.1016/S0006-3495(96)79464-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Linari M., Piazzesi G., Dobbie I., Koubassova N., Reconditi M., Narayanan T., Diat O., Irving M., Lombardi V. Interference fine structure and sarcomere length dependence of the axial x-ray pattern from active single muscle fibers. Proc Natl Acad Sci U S A. 2000 Jun 20;97(13):7226–7231. doi: 10.1073/pnas.97.13.7226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Ling N., Shrimpton C., Sleep J., Kendrick-Jones J., Irving M. Fluorescent probes of the orientation of myosin regulatory light chains in relaxed, rigor, and contracting muscle. Biophys J. 1996 Apr;70(4):1836–1846. doi: 10.1016/S0006-3495(96)79749-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Lombardi V., Piazzesi G., Ferenczi M. A., Thirlwell H., Dobbie I., Irving M. Elastic distortion of myosin heads and repriming of the working stroke in muscle. Nature. 1995 Apr 6;374(6522):553–555. doi: 10.1038/374553a0. [DOI] [PubMed] [Google Scholar]
  48. Lombardi V., Piazzesi G., Linari M. Rapid regeneration of the actin-myosin power stroke in contracting muscle. Nature. 1992 Feb 13;355(6361):638–641. doi: 10.1038/355638a0. [DOI] [PubMed] [Google Scholar]
  49. Londo T. R., Rahman N. A., Roess D. A., Barisas B. G. Fluorescence depletion measurements in various experimental geometries provide true emission and absorption anisotropies for the study of protein rotation. Biophys Chem. 1993 Dec;48(2):241–257. doi: 10.1016/0301-4622(93)85013-8. [DOI] [PubMed] [Google Scholar]
  50. Ludescher R. D., Thomas D. D. Microsecond rotational dynamics of phosphorescent-labeled muscle cross-bridges. Biochemistry. 1988 May 3;27(9):3343–3351. doi: 10.1021/bi00409a034. [DOI] [PubMed] [Google Scholar]
  51. Martyn D. A., Chase P. B. Faster force transient kinetics at submaximal Ca2+ activation of skinned psoas fibers from rabbit. Biophys J. 1995 Jan;68(1):235–242. doi: 10.1016/S0006-3495(95)80179-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Mendelson R. A., Schneider D. K., Stone D. B. Conformations of myosin subfragment 1 ATPase intermediates from neutron and X-ray scattering. J Mol Biol. 1996 Feb 16;256(1):1–7. doi: 10.1006/jmbi.1996.0063. [DOI] [PubMed] [Google Scholar]
  53. Milligan R. A., Flicker P. F. Structural relationships of actin, myosin, and tropomyosin revealed by cryo-electron microscopy. J Cell Biol. 1987 Jul;105(1):29–39. doi: 10.1083/jcb.105.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Pollard T. D., Bhandari D., Maupin P., Wachsstock D., Weeds A. G., Zot H. G. Direct visualization by electron microscopy of the weakly bound intermediates in the actomyosin adenosine triphosphatase cycle. Biophys J. 1993 Feb;64(2):454–471. doi: 10.1016/S0006-3495(93)81387-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Rahman N. A., Pecht I., Roess D. A., Barisas B. G. Rotational dynamics of type I Fc epsilon receptors on individually-selected rat mast cells studied by polarized fluorescence depletion. Biophys J. 1992 Feb;61(2):334–346. doi: 10.1016/S0006-3495(92)81840-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Ramachandran S., Thomas D. D. Rotational dynamics of the regulatory light chain in scallop muscle detected by time-resolved phosphorescence anisotropy. Biochemistry. 1999 Jul 13;38(28):9097–9104. doi: 10.1021/bi9902945. [DOI] [PubMed] [Google Scholar]
  57. Rayment I., Holden H. M., Whittaker M., Yohn C. B., Lorenz M., Holmes K. C., Milligan R. A. Structure of the actin-myosin complex and its implications for muscle contraction. Science. 1993 Jul 2;261(5117):58–65. doi: 10.1126/science.8316858. [DOI] [PubMed] [Google Scholar]
  58. 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]
  59. 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]
  60. Roopnarine O., Szent-Györgyi A. G., Thomas D. D. Microsecond rotational dynamics of spin-labeled myosin regulatory light chain induced by relaxation and contraction of scallop muscle. Biochemistry. 1998 Oct 13;37(41):14428–14436. doi: 10.1021/bi9808363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sabido-David C., Brandmeier B., Craik J. S., Corrie J. E., Trentham D. R., Irving M. Steady-state fluorescence polarization studies of the orientation of myosin regulatory light chains in single skeletal muscle fibers using pure isomers of iodoacetamidotetramethylrhodamine. Biophys J. 1998 Jun;74(6):3083–3092. doi: 10.1016/S0006-3495(98)78015-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Sabido-David C., Hopkins S. C., Saraswat L. D., Lowey S., Goldman Y. E., Irving M. Orientation changes of fluorescent probes at five sites on the myosin regulatory light chain during contraction of single skeletal muscle fibres. J Mol Biol. 1998 Jun 5;279(2):387–402. doi: 10.1006/jmbi.1998.1771. [DOI] [PubMed] [Google Scholar]
  63. Shih W. M., Gryczynski Z., Lakowicz J. R., Spudich J. A. A FRET-based sensor reveals large ATP hydrolysis-induced conformational changes and three distinct states of the molecular motor myosin. Cell. 2000 Sep 1;102(5):683–694. doi: 10.1016/s0092-8674(00)00090-8. [DOI] [PubMed] [Google Scholar]
  64. Smith C. A., Rayment I. X-ray structure of the magnesium(II).ADP.vanadate complex of the Dictyostelium discoideum myosin motor domain to 1.9 A resolution. Biochemistry. 1996 Apr 30;35(17):5404–5417. doi: 10.1021/bi952633+. [DOI] [PubMed] [Google Scholar]
  65. Stein R. A., Ludescher R. D., Dahlberg P. S., Fajer P. G., Bennett R. L., Thomas D. D. Time-resolved rotational dynamics of phosphorescent-labeled myosin heads in contracting muscle fibers. Biochemistry. 1990 Oct 30;29(43):10023–10031. doi: 10.1021/bi00495a003. [DOI] [PubMed] [Google Scholar]
  66. Suzuki Y., Yasunaga T., Ohkura R., Wakabayashi T., Sutoh K. Swing of the lever arm of a myosin motor at the isomerization and phosphate-release steps. Nature. 1998 Nov 26;396(6709):380–383. doi: 10.1038/24640. [DOI] [PubMed] [Google Scholar]
  67. Tanner J. W., Thomas D. D., Goldman Y. E. Transients in orientation of a fluorescent cross-bridge probe following photolysis of caged nucleotides in skeletal muscle fibres. J Mol Biol. 1992 Jan 5;223(1):185–203. doi: 10.1016/0022-2836(92)90725-y. [DOI] [PubMed] [Google Scholar]
  68. Taylor K. A., Schmitz H., Reedy M. C., Goldman Y. E., Franzini-Armstrong C., Sasaki H., Tregear R. T., Poole K., Lucaveche C., Edwards R. J. Tomographic 3D reconstruction of quick-frozen, Ca2+-activated contracting insect flight muscle. Cell. 1999 Nov 12;99(4):421–431. doi: 10.1016/s0092-8674(00)81528-7. [DOI] [PubMed] [Google Scholar]
  69. Thomas D. D., Cooke R. Orientation of spin-labeled myosin heads in glycerinated muscle fibers. Biophys J. 1980 Dec;32(3):891–906. doi: 10.1016/S0006-3495(80)85024-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Thomas D. D., Ishiwata S., Seidel J. C., Gergely J. Submillisecond rotational dynamics of spin-labeled myosin heads in myofibrils. Biophys J. 1980 Dec;32(3):873–889. doi: 10.1016/S0006-3495(80)85023-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Thomas D. D., Ramachandran S., Roopnarine O., Hayden D. W., Ostap E. M. The mechanism of force generation in myosin: a disorder-to-order transition, coupled to internal structural changes. Biophys J. 1995 Apr;68(4 Suppl):135S–141S. [PMC free article] [PubMed] [Google Scholar]
  72. Tsaturyan A. K., Bershitsky S. Y., Burns R., Ferenczi M. A. Structural changes in the actin-myosin cross-bridges associated with force generation induced by temperature jump in permeabilized frog muscle fibers. Biophys J. 1999 Jul;77(1):354–372. doi: 10.1016/S0006-3495(99)76895-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Vibert P., Cohen C. Domains, motions and regulation in the myosin head. J Muscle Res Cell Motil. 1988 Aug;9(4):296–305. doi: 10.1007/BF01773873. [DOI] [PubMed] [Google Scholar]
  74. Vogel H., Jähnig F. Fast and slow orientational fluctuations in membranes. Proc Natl Acad Sci U S A. 1985 Apr;82(7):2029–2033. doi: 10.1073/pnas.82.7.2029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Wakabayashi K., Tokunaga M., Kohno I., Sugimoto Y., Hamanaka T., Takezawa Y., Wakabayashi T., Amemiya Y. Small-angle synchrotron x-ray scattering reveals distinct shape changes of the myosin head during hydrolysis of ATP. Science. 1992 Oct 16;258(5081):443–447. doi: 10.1126/science.1411537. [DOI] [PubMed] [Google Scholar]
  76. Yoshida T. M., Barisas B. G. Protein rotational motion in solution measured by polarized fluorescence depletion. Biophys J. 1986 Jul;50(1):41–53. doi: 10.1016/S0006-3495(86)83437-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Yoshida T. M., Zarrin F., Barisas B. G. Measurement of protein rotational motion using frequency domain polarized fluorescence depletion. Biophys J. 1988 Aug;54(2):277–288. doi: 10.1016/S0006-3495(88)82957-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Zhao L., Pate E., Baker A. J., Cooke R. The myosin catalytic domain does not rotate during the working power stroke. Biophys J. 1995 Sep;69(3):994–999. doi: 10.1016/S0006-3495(95)79974-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. van der Heide U. A., Hopkins S. C., Goldman Y. E. A maximum entropy analysis of protein orientations using fluorescence polarization data from multiple probes. Biophys J. 2000 Apr;78(4):2138–2150. doi: 10.1016/S0006-3495(00)76760-9. [DOI] [PMC free article] [PubMed] [Google Scholar]

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