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Molecular modeling of averaged rigor crossbridges from tomograms of insect flight muscle.

Chen LF, Winkler H, Reedy MK, Reedy MC, Taylor KA
J Struct Biol 138 92-104
Related entries: 1m8q, 1mvw, 1o18, 1o1a, 1o1b, 1o1c, 1o1d, 1o1e, 1o1f, 1o1g

Cited: 49 times
EuropePMC logo PMID: 12160705

Abstract

Electron tomography, correspondence analysis, molecular model building, and real-space refinement provide detailed 3-D structures for in situ myosin crossbridges in the nucleotide-free state (rigor), thought to represent the end of the power stroke. Unaveraged tomograms from a 25-nm longitudinal section of insect flight muscle preserved native structural variation. Recurring crossbridge motifs that repeat every 38.7 nm along the actin filament were extracted from the tomogram and classified by correspondence analysis into 25 class averages, which improved the signal to noise ratio. Models based on the atomic structures of actin and of myosin subfragment 1 were rebuilt to fit 11 class averages. A real-space refinement procedure was applied to quantitatively fit the reconstructions and to minimize steric clashes between domains introduced during the fitting. These combined procedures show that no single myosin head structure can fit all the in situ crossbridges. The validity of the approach is supported by agreement of these atomic models with fluorescent probe data from vertebrate muscle as well as with data from regulatory light chain crosslinking between heads of smooth muscle heavy meromyosin when bound to actin.

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  1. Electron microscopy holdings of the Protein Data Bank: the impact of the resolution revolution, new validation tools, and implications for the future. Burley SK, Berman HM, Chiu W, Dai W, Flatt JW, Hudson BP, Kaelber JT, Khare SD, Kulczyk AW, Lawson CL, Pintilie GD, Sali A, Vallat B, Westbrook JD, Young JY, Zardecki C. Biophys Rev 14 1281-1301 (2022)

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  1. Myosin lever arm orientation in muscle determined with high angular resolution using bifunctional spin labels. Savich Y, Binder BP, Thompson AR, Thomas DD. J Gen Physiol 151 1007-1016 (2019)


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  1. Structural studies by electron tomography: from cells to molecules. Lucić V, Förster F, Baumeister W. Annu Rev Biochem 74 833-865 (2005)
  2. Electron tomography of membrane-bound cellular organelles. Frey TG, Perkins GA, Ellisman MH. Annu Rev Biophys Biomol Struct 35 199-224 (2006)
  3. Regulation of cytoskeletal dynamics by phospholipase D and phosphatidic acid. Pleskot R, Li J, Zárský V, Potocký M, Staiger CJ. Trends Plant Sci 18 496-504 (2013)
  4. Invertebrate muscles: thin and thick filament structure; molecular basis of contraction and its regulation, catch and asynchronous muscle. Hooper SL, Hobbs KH, Thuma JB. Prog Neurobiol 86 72-127 (2008)
  5. Large macromolecular complexes in the Protein Data Bank: a status report. Dutta S, Berman HM. Structure 13 381-388 (2005)
  6. Mechanical design of translocating motor proteins. Hwang W, Lang MJ. Cell Biochem Biophys 54 11-22 (2009)
  7. Multiscale modeling and mechanics of filamentous actin cytoskeleton. Yamaoka H, Matsushita S, Shimada Y, Adachi T. Biomech Model Mechanobiol 11 291-302 (2012)
  8. Protein conformation and molecular order probed by second-harmonic-generation microscopy. Vanzi F, Sacconi L, Cicchi R, Pavone FS. J Biomed Opt 17 060901 (2012)
  9. Evolution of standardization and dissemination of cryo-EM structures and data jointly by the community, PDB, and EMDB. Chiu W, Schmid MF, Pintilie GD, Lawson CL. J Biol Chem 296 100560 (2021)
  10. Insights into Actin-Myosin Interactions within Muscle from 3D Electron Microscopy. Taylor KA, Rahmani H, Edwards RJ, Reedy MK. Int J Mol Sci 20 E1703 (2019)

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  1. Load-dependent mechanism of nonmuscle myosin 2. Kovács M, Thirumurugan K, Knight PJ, Sellers JR. Proc Natl Acad Sci U S A 104 9994-9999 (2007)
  2. 3D reconstruction and processing of volumetric data in cryo-electron tomography. Winkler H. J Struct Biol 157 126-137 (2007)
  3. Refined model of the 10S conformation of smooth muscle myosin by cryo-electron microscopy 3D image reconstruction. Liu J, Wendt T, Taylor D, Taylor K. J Mol Biol 329 963-972 (2003)
  4. Applications of a bilateral denoising filter in biological electron microscopy. Jiang W, Baker ML, Wu Q, Bajaj C, Chiu W. J Struct Biol 144 114-122 (2003)
  5. Probing myosin structural conformation in vivo by second-harmonic generation microscopy. Nucciotti V, Stringari C, Sacconi L, Vanzi F, Fusi L, Linari M, Piazzesi G, Lombardi V, Pavone FS. Proc Natl Acad Sci U S A 107 7763-7768 (2010)
  6. Myosin head configuration in relaxed insect flight muscle: x-ray modeled resting cross-bridges in a pre-powerstroke state are poised for actin binding. AL-Khayat HA, Hudson L, Reedy MK, Irving TC, Squire JM, Squire JM. Biophys J 85 1063-1079 (2003)
  7. Mechanism of action of myosin X, a membrane-associated molecular motor. Kovács M, Wang F, Sellers JR. J Biol Chem 280 15071-15083 (2005)
  8. Cross-bridge number, position, and angle in target zones of cryofixed isometrically active insect flight muscle. Tregear RT, Reedy MC, Goldman YE, Taylor KA, Winkler H, Franzini-Armstrong C, Sasaki H, Lucaveche C, Reedy MK. Biophys J 86 3009-3019 (2004)
  9. Electron tomography of fast frozen, stretched rigor fibers reveals elastic distortions in the myosin crossbridges. Liu J, Reedy MC, Goldman YE, Franzini-Armstrong C, Sasaki H, Tregear RT, Lucaveche C, Winkler H, Baumann BA, Squire JM, Squire JM, Irving TC, Reedy MK, Taylor KA. J Struct Biol 147 268-282 (2004)
  10. Use of frozen-hydrated axonemes to assess imaging parameters and resolution limits in cryoelectron tomography. McEwen BF, Marko M, Hsieh CE, Mannella C. J Struct Biol 138 47-57 (2002)
  11. Effect of tensile force on the mechanical behavior of actin filaments. Matsushita S, Inoue Y, Hojo M, Sokabe M, Adachi T. J Biomech 44 1776-1781 (2011)
  12. Electron tomography of swollen rigor fibers of insect flight muscle reveals a short and variably angled S2 domain. Liu J, Wu S, Reedy MC, Winkler H, Lucaveche C, Cheng Y, Reedy MK, Taylor KA. J Mol Biol 362 844-860 (2006)
  13. Graphene Oxide Nanosheets Retard Cellular Migration via Disruption of Actin Cytoskeleton. Tian X, Yang Z, Duan G, Wu A, Gu Z, Zhang L, Chen C, Chai Z, Ge C, Zhou R. Small 13 (2017)
  14. Quantitative self-organizing maps for clustering electron tomograms. Pascual-Montano A, Taylor KA, Winkler H, Pascual-Marqui RD, Carazo JM. J Struct Biol 138 114-122 (2002)
  15. The conformation of myosin head domains in rigor muscle determined by X-ray interference. Reconditi M, Koubassova N, Linari M, Dobbie I, Narayanan T, Diat O, Piazzesi G, Lombardi V, Irving M. Biophys J 85 1098-1110 (2003)
  16. Identification of a novel mutation in the myosin VIIA motor domain in a family with autosomal dominant hearing loss (DFNA11). Di Leva F, D'Adamo P, Cubellis MV, D'Eustacchio A, Errichiello M, Saulino C, Auletta G, Giannini P, Donaudy F, Ciccodicola A, Gasparini P, Franzè A, Marciano E. Audiol Neurootol 11 157-164 (2006)
  17. Methods for identifying and averaging variable molecular conformations in tomograms of actively contracting insect flight muscle. Wu S, Liu J, Reedy MC, Winkler H, Reedy MK, Taylor KA. J Struct Biol 168 485-502 (2009)
  18. Myosin regulatory domain orientation in skeletal muscle fibers: application of novel electron paramagnetic resonance spectral decomposition and molecular modeling methods. Baumann BA, Liang H, Sale K, Hambly BD, Fajer PG. Biophys J 86 3030-3041 (2004)
  19. Androgens Exert a Cysticidal Effect upon Taenia crassiceps by Disrupting Flame Cell Morphology and Function. Ambrosio JR, Valverde-Islas L, Nava-Castro KE, Palacios-Arreola MI, Ostoa-Saloma P, Reynoso-Ducoing O, Escobedo G, Ruíz-Rosado A, Dominguez-Ramírez L, Morales-Montor J. PLoS One 10 e0127928 (2015)
  20. Kinematics of the lever arm swing in myosin VI. Mugnai ML, Thirumalai D. Proc Natl Acad Sci U S A 114 E4389-E4398 (2017)
  21. A possible mechanism for determining the directionality of myosin molecular motors. Masuda T. Biosystems 93 172-180 (2008)
  22. Different Myosin Head Conformations in Bony Fish Muscles Put into Rigor at Different Sarcomere Lengths. Eakins F, Harford JJ, Knupp C, Roessle M, Squire JM. Int J Mol Sci 19 E2091 (2018)
  23. Entropic potential field formed for a linear-motor protein near a filament: Statistical-mechanical analyses using simple models. Amano K, Yoshidome T, Iwaki M, Suzuki M, Suzuki M, Kinoshita M. J Chem Phys 133 045103 (2010)
  24. Quantitative analysis of extension-torsion coupling of actin filaments. Matsushita S, Inoue Y, Adachi T. Biochem Biophys Res Commun 420 710-713 (2012)
  25. Quasiperiodic distribution of rigor cross-bridges along a reconstituted thin filament in a skeletal myofibril. Suzuki M, Ishiwata S. Biophys J 101 2740-2748 (2011)
  26. Molecular dynamics simulation of a myosin subfragment-1 docking with an actin filament. Masuda T. Biosystems 113 144-148 (2013)
  27. Myosin S2 origins track evolution of strong binding on actin by azimuthal rolling of motor domain. Arakelian C, Warrington A, Winkler H, Perz-Edwards RJ, Reedy MK, Taylor KA. Biophys J 108 1495-1502 (2015)
  28. Tropomyosin movement is described by a quantitative high-resolution model of X-ray diffraction of contracting muscle. Koubassova NA, Bershitsky SY, Ferenczi MA, Narayanan T, Tsaturyan AK. Eur Biophys J 46 335-342 (2017)
  29. A deterministic mechanism producing the loose coupling phenomenon observed in an actomyosin system. Masuda T. Biosystems 95 104-113 (2009)
  30. Asymmetric myosin binding to the thin filament as revealed by a fluorescent nanocircuit. Coffee Castro-Zena PG, Root DD. Arch Biochem Biophys 535 14-21 (2013)
  31. Cardiac and skeletal actin substrates uniquely tune cardiac myosin strain-dependent mechanics. Wang Y, Ajtai K, Burghardt TP. Open Biol 8 180143 (2018)
  32. A model of protein association based on their hydrophobic and electric interactions. Mozo-Villarías A, Cedano J, Querol E. PLoS One 9 e110352 (2014)
  33. A protein self-assembly model guided by electrostatic and hydrophobic dipole moments. Mozo-Villarías A, Querol E. PLoS One 14 e0216253 (2019)
  34. Actomyosin interaction: mechanical and energetic properties in different nucleotide binding states. Aprodu I, Redaelli A, Soncini M. Int J Mol Sci 9 1927-1943 (2008)
  35. Coarse-grained simulation of myosin-V movement. Katsimitsoulia Z, Taylor WR. Comput Math Methods Med 2012 781456 (2012)
  36. Double-headed binding of myosin II to F-actin shows the effect of strain on head structure. Hojjatian A, Taylor DW, Daneshparvar N, Fagnant PM, Trybus KM, Taylor KA. J Struct Biol 215 107995 (2023)
  37. Molecular dynamics simulation for the reversed power stroke motion of a myosin subfragment-1. Masuda T. Biosystems 132-133 1-5 (2015)


Related citations provided by authors (3)

  1. Real Space Refinement of Acto-Myosin Structures from Sectioned Muscle.. Chen LF, Blanc E, Chapman MS, Taylor KA J. Struct. Biol. 133 221- (2001)
  2. Multivariate Statistical Analysis of Three-Dimensional Cross-Bridge Motifs in Insect Flight Muscle. Winkler H, Taylor KA Ultramicroscopy 77 141- (1999)
  3. The Use of Electron Tomography for Structural Analysis of Disordered Protein Arrays.. Taylor KA, Tang J, Cheng Y, Winkler H J. Struct. Biol. 120 372- (1997)

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