Probing myosin structural conformation in vivo by second-harmonic generation microscopy

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 17, 2010, Pages 7763-7768

  Nucciotti, V ^a   Stringari, C ^b,c   Sacconi, L ^b   Vanzi, F ^b   Fusi, L ^a   Linari, M ^a   Piazzesi, G ^a   Lombardi, V ^a,b   Pavone, F S ^a,b  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

^c UNIVERSITY OF TRENTO   (Italy)

Author keywords

Hyper Rayleigh scattering; Nonlinear microscopy; Protein organization

Indexed keywords

MYOSIN;

ACTIN FILAMENT; ANISOTROPY; ARTICLE; IN VIVO STUDY; MICROSCOPY; MUSCLE CELL; MUSCLE FIBRIL; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; SECOND HARMONIC GENERATION MICROSCOPY;

ANIMALS; ANISOTROPY; CELL POLARITY; MODELS, BIOLOGICAL; MOLECULAR IMAGING; MUSCLE CELLS; MUSCLE CONTRACTION; MYOSINS; PROTEIN CONFORMATION; PSOAS MUSCLES; RABBITS;

EID: 77952411548     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0914782107     Document Type: Article

References (51)

1. Rayment I, et al. (1993) Three-dimensional structure of myosin subfragment-1: A molecular motor. Science 261:50-58. (Pubitemid 23265379)
2. Kabsch W, Mannherz HG, Suck D, Pai EF, Holmes KC (1990) Atomic structure of the actin:DNase I complex. Nature 347:37-44.
3. Reedy MC (2000) Visualizing myosin's power stroke in muscle contraction. J Cell Sci 113(Pt 20):3551-3562.
4. Thomas DD, Kast D, Korman VL (2009) Site-directed spectroscopic probes of actomyosin structural dynamics. Ann Rev Biophys 38:347-369.
5. Huxley HE (2004) Fifty years of muscle and the sliding filament hypothesis. Eur J Biochem 271:1403-1415.
6. Corrie JE, et al. (1999) Dynamic measurement of myosin light-chain-domain tilt and twist in muscle contraction. Nature 400:425-430.
7. Rayment I, et al. (1993) Structure of the actin-myosin complex and its implications for muscle contraction. Science 261:58-65. (Pubitemid 23265380)
8. Holmes KC (1997) The swinging lever-arm hypothesis of muscle contraction. Curr Biol 7:R112-118.
9. Moreaux L, Sandre O, Charpak S, Blanchard-Desce M, Mertz J (2001) Coherent scattering in multi-harmonic light microscopy. Biophys J 80:1568-1574. (Pubitemid 32182180)
10. Zipfel WR, Williams RM, Webb WW (2003) Nonlinear magic: Multiphoton microscopy in the biosciences. Nat Biotechnol 21:1369-1377.
11. Campagnola PJ, Loew LM (2003) Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms. Nat Biotechnol 21:1356-1360.
12. Both M, et al. (2004) Second harmonic imaging of intrinsic signals in muscle fibers in situ. J Biomed Opt 9:882-892. (Pubitemid 41268670)
13. Plotnikov SV, Millard AC, Campagnola PJ, Mohler WA (2006) Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres. Biophys J 90:693-703.
14. Plotnikov SV, et al. (2008) Measurement of muscle disease by quantitative second-harmonic generation imaging. J Biomed Opt 13:044018 doi: 10.1117/1.2967536.
15. Kriech MA, Conboy JC (2003) Label-free chiral detection of melittin binding to a membrane. J Am Chem Soc 125:1148-1149.
16. Mitchell SA, McAloney RA, Moffatt D, Mora-Diez N, Zgierski MZ (2005) Second-harmonic generation optical activity of a polypeptide alpha-helix at the air/water interface. J Chem Phys 122:114707 doi: 10.1063/1.1862613. (Pubitemid 40661778)
17. Lovell SJ, Knight PJ, Harrington WF (1981) Fraction of myosin heads bound to thin filaments in rigor fibrils from insect flight and vertebrate muscles. Nature 293:664-666.
18. Pate E, Cooke R (1988) Energetics of the actomyosin bond in the filament array of muscle fibers. Biophys J 53:561-573. (Pubitemid 18095304)
19. Berisio R, Vitagliano L, Mazzarella L, Zagari A (2002) Crystal structure of the collagen triple helix model [(Pro-Pro-Gly)(10)](3). Protein Sci 11:262-270.
20. Roth S, Freund I (1981) Optical second-harmonic scattering in rat-tail tendon. Biopolymers 20:1271-1290.
21. Freund I, Deutsch M, Sprecher A (1986) Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon. Biophys J 50:693-712.
22. Tiaho F, Recher G, Rouede D (2007) Estimation of helical angles of myosin and collagen by second harmonic generation imaging microscopy. Opt Express 15:12286-12295. (Pubitemid 47460092)
23. Chen LF, Winkler H, Reedy MK, Reedy MC, Taylor KA (2002) Molecular modeling of averaged rigor crossbridges from tomograms of insect flight muscle. J Struct Biol 138:92-104. (Pubitemid 35300751)
24. Irving M, et al. (2000) Conformation of the myosin motor during force generation in skeletal muscle. Nat Struct Biol 7:482-485. (Pubitemid 30414470)
25. Beck K, Brodsky B (1998) Supercoiled protein motifs: The collagen triple-helix and the alpha-helical coiled coil. J Struct Biol 122:17-29. (Pubitemid 28411182)
26. Blankenfeldt W, Thoma NH, Wray JS, Gautel M, Schlichting I (2006) Crystal structures of human cardiac beta-myosin II S2-Delta provide insight into the functional role of the S2 subfragment. Proc Natl Acad Sci USA 103:17713-17717. (Pubitemid 44852225)
27. Woodhead JL, et al. (2005) Atomic model of a myosin filament in the relaxed state. Nature 436:1195-1199.
28. Haselgrove JC, Huxley HE (1973) X-ray evidence for radial cross-bridge movement and for the sliding filament model in actively contracting skeletal muscle. J Mol Biol 77:549-568.
29. Matsubara I, Yagi N, Hashizume H (1975) Use of an x-ray television for diffraction of the frog striated muscle. Nature 255:728-729.
30. Cooke R, Crowder MS, Thomas DD (1982) Orientation of spin labels attached to cross-bridges in contracting muscle fibres. Nature 300:776-778. (Pubitemid 13224364)
31. LinariM, et al. (1998) The stiffness of skeletal muscle in isometric contraction and rigor: The fraction of myosin heads bound to actin. Biophys J 74:2459-2473.
32. Piazzesi G, et al. (2002) Mechanism of force generation by myosin heads in skeletal muscle. Nature 415:659-662. (Pubitemid 34136395)
33. Piazzesi G, et al. (2007) Skeletal muscle performance determined by modulation of number of myosin motors rather than motor force or stroke size. Cell 131:784-795. (Pubitemid 350103598)
34. Irving M, Lombardi V, Piazzesi G, Ferenczi MA (1992) Myosin head movements are synchronous with the elementary force-generating process in muscle. Nature 357:156-158.
35. Irving M(1993) Birefringence changes associated with isometric contraction and rapid shortening steps in frog skeletal muscle fibres. J Physiol 472:127-156.
36. Peckham M, Ferenczi MA, Irving M (1994) A birefringence study of changes in myosin orientation during relaxation of skinned muscle fibers induced by photolytic ATP release. Biophys J 67:1141-1148. (Pubitemid 24272965)
37. Thomas DD, Cooke R (1980) Orientation of spin-labeled myosin heads in glycerinated muscle fibers. Biophys J 32:891-906.
38. Allen TS, Ling N, Irving M, Goldman YE (1996) Orientation changes in myosin regulatory light chains following photorelease of ATP in skinned muscle fibers. Biophys J 70:1847-1862. (Pubitemid 26103958)
39. Huxley HE, et al. (1981) Millisecond time-resolved changes in x-ray reflections from contracting muscle during rapid mechanical transients, recorded using synchrotron radiation. Proc Natl Acad Sci USA 78:2297-2301.
40. Tregear RT, et al. (1998) X-ray diffraction indicates that active cross-bridges bind to actin target zones in insect flight muscle. Biophys J 74:1439-1451.
41. Reconditi M, et al. (2004) The myosin motor in muscle generates a smaller and slower working stroke at higher load. Nature 428:578-581. (Pubitemid 38480543)
42. Taylor KA, et al. (1999) Tomographic 3D reconstruction of quick-frozen, Ca2+-activated contracting insect flight muscle. Cell 99:421-431.
43. Sabido-David C, et al. (1998) 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 74:3083-3092. (Pubitemid 28268132)
44. Eberstein A, Rosenfalck A (1963) Birefringence of isolated muscle fibres in twitch and tetanus. Acta Physiol Scand 57:144-166.
45. Llewellyn ME, Barretto RP, Delp SL, Schnitzer MJ (2008) Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans. Nature 454:784-788.
46. Sacconi L, et al. (2005) Second-harmonic generation sensitivity to transmembrane potential in normal and tumor cells. J Biomed Opt 10:024014 doi: 10.1117/1.1895205. (Pubitemid 41046592)
47. Linari M, Caremani M, Piperio C, Brandt P, Lombardi V (2007) Stiffness and fraction of Myosin motors responsible for active force in permeabilized muscle fibers from rabbit psoas. Biophys J 92:2476-2490. (Pubitemid 46536429)
48. Lombardi V, Piazzesi G (1990) The contractile response during steady lengthening of stimulated frog muscle fibres. J Physiol 431:141-171.
49. Kleinmann DA (1962) Nonlinear dielectric polarization in optical media. Phys Rev 126:1977-1979.
50. Moreaux L, Sandre O, Mertz J (2000) Membrane imaging by second-harmonic generation microscopy. J Opt Soc Am B 17:1685-1694.
51. Holmes KC, Popp D, GebhardW, KabschW(1990) Atomic model of the actin filament. Nature 347:44-49.