Abstract
Directed movements on actin filaments within the cell are powered by molecular motors of the myosin superfamily. On actin filaments, myosin motors convert the energy from ATP into force and movement. Myosin motors power such diverse cellular functions as cytokinesis, membrane trafficking, organelle movements, and cellular migration. Myosin generates force and movement via a number of structural changes associated with hydrolysis of ATP, binding to actin, and release of the ATP hydrolysis products while bound to actin. Herein we provide an overview of those structural changes and how they relate to the actin-myosin ATPase cycle. These structural changes are the basis of chemo-mechanical transduction by myosin motors.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Coates JH, Criddle AH, Geeves MA (1985) Pressure-relaxation studies of pyrene-labelled actin and myosin subfragment-1 from rabbit skeletal muscle. Biochem 232:351–356
Coureux P-D, Wells AL, Ménétrey J, Yengo CM, Morris CA, Sweeney HL, Houdusse A (2003) The structure of myosin V motor without bound nucleotide. Nature 425:419–423
Dantzig JA, Goldman YE, Millar NC, Lacktis J, Homsher E (1992) Reversal of the cross-bridge force-generating transition by photogeneration of phosphate in rabbit psoas muscle fibres. J Physiol 451:247–278
De La Cruz EM, Ostap EM (2004) Relating biochemistry and function in the myosin superfamily. Curr Opin Cell Biol 16:61–67
Dominguez R, Freyzon Y, Trybus KM, Cohen C (1998) 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 94:559–571
Fisher AJ, Smith CA, Thoden JB, Smith R, Sutoh K, Holden HM, Rayment I (1995) X-ray structures of the myosin motor domain of Dictyostelium discoideum complexed with MgADP.BeFx and MgADP.AlF4-. Biochemistry 34:8960–8972
Foth BJ, Goedecke MC, Soldati D (2006) New insights into myosin evolution and classification. Proc Natl Acad Sci U S A 103:3681–3686
Holmes KC, Geeves MA (1999) Structural mechanism of muscle contraction. Annu Rev Biochem 68:687–728
Houdusse A, Sweeney HL (2016) How myosin generates force on actin filaments. Trends Biochem Sci 41:989–997
Houdusse A, Kalabokis VN, Himmel D, Szent-Gyorgyi AG, Cohen C (1999) Atomic structure of scallop myosin subfragment S1 complexed with MgADP: a novel conformation of the myosin head. Cell 97:459–470
Houdusse A, Szent-Györgyi AG, Cohen C (2000) Three conformational states of scallop myosin S1. Proc Natl Acad Sci U S A 97:11238–11243
Huxley H, Reconditi M, Stewart A, Irving T (2006) X-ray interference studies of crossbridge action in muscle contraction: evidence from quick releases. J Mol Biol 363:743–761
Kodera N, Ando T (2014) The path to visualization of walking myosin V by high-speed atomic force microscopy. Biophys Rev 6(3–4):237–260
Laakso JM, Lewis JH, Shuman H, Ostap EM (2008) Myosin I can act as a molecular force sensor. Science 321:133–136
Llinas P, Isabet T, Song L, Ropars V, Zong B, Benisty H, Sirigu S, Morris C, Kikuti C, Safer D, Sweeney HL, Houdusse A (2015) How actin initiates the motor activity of myosin. Dev Cell 33(4):401–412
Lymn RW, Taylor EW (1971) Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10:4617–4624
Mehta AD, Rock RS, Rief M, Spudich JA, Mooseker MS, Cheney RE (1999) Myosin V is a processive actin-based motor. Nature 400:590–593
Ménétrey J, Bahloul A, Wells AL, Yengo CM, Morris CA, Sweeney HL, Houdusse A (2005) The structure of the myosin VI motor reveals the mechanism of directionality reversal. Nature 435:779–785
Ménétrey J, Llinas P, Mukherjea M, Sweeney HL, Houdusse A (2007) The structural basis for the large powerstroke of myosin VI. Cell 131:300–308
Ménétrey J, Isabet T, Ropars V, Mukherjea M, Pylypenko O, Liu X, Perez J, Vachette P, Sweeney HL, Houdusse AM (2012) Processive steps in the reverse direction require uncoupling of the Lead head lever arm of myosin VI. Mol Cell 48:75–86
Mukherjea M, Llinas P, Kim HJ, Travaglia M, Safer D, Ménétrey J, Franzini-Armstrong C, Selvin PR, Houdusse A, Sweeney HL (2009) Myosin VI dimerization triggers an unfolding of a three-helix bundle in order to extend its reach. Mol Cell 35:305–315
Oke OA, Burgess SA, Forgacs E, Knight PJ, Sakamoto T, Sellers JR, White H, Trinick J (2010) Influence of lever structure on myosin 5a walking. Proc National Acad Sci 107:2509–2514
Park H, Li A, Chen LQ, Houdusse A, Selvin PR, Sweeney HL (2007) The unique insert at the end of the myosin VI motor is the sole determinant of directionality. Proc Natl Acad Sci U S A 104:778–783
Rayment I, Rypniewski WR, Schmidt-Bäde K, Smith R, Tomchick DR, Benning MM, Winkelmann DA, Wesenberg G, Holden HM (1993) Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261:50–58
Rohde JA, Thomas DD, Muretta JM (2017) Heart failure drug changes the mechanoenzymology of the cardiac myosin powerstroke. Proc Natl Acad Sci U S A 114:E1796–E1804
Sleep JA, Hutton RL (1980) Exchange between inorganic phosphate and adenosine 5′-triphosphate in the medium by actomyosin subfragment 1. Biochemistry 19:1276–1283
Stehle R (2017) Force responses and sarcomere dynamics of cardiac myofibrils induced by rapid changes in [pi]. Biophys J 112:356–367
Suzuki Y, Yasunaga T, Ohkura R, Wakabayashi T, Sutoh K (1998) Swing of the lever arm of a myosin motor at the isomerization and phosphate-release steps. Nature 396:380–383
Sweeney HL, Houdusse A (2010a) Myosin VI rewrites the rules for myosin motors. Cell 141:573–582
Sweeney HL, Houdusse A (2010b) Structural and functional insights into the myosin motor mechanism. Annu Rev Biophys 39:539–557
Sweeney HL, Park H, Zong AB, Yang Z, Selvin PR, Rosenfeld SS (2007) How myosin VI coordinates its heads during processive movement. EMBO J 26:2682–2692
Tyska MJ, Warshaw DM (2002) The myosin power stroke. Cell Motil Cytoskeleton 51:1–15
Uchihashi T, Kodera N, Ando T (2012) Guide to video recording of structure dynamics and dynamic processes of proteins by high-speed atomic force microscopy. Nat Protoc 7(6):1193–1206
Volkman N, Hanein D, Ouyang G, Trybus KM, DeRosier DJ, Lowey S (2000) Evidence for cleft closure in actomyosin upon ADP release. Nat Struct Biol 7:1147–1155
Walker ML, Burgess SA, Sellers JR, Wang F, Trinick J, Knight PJ (2000) Two-headed binding of a Processive myosin to F-actin. Nature 405:804–807
Wells AL, Lin AW, Chen L-Q, Safer D, Cain SM, Hasson T, Carragher BO, Milligan RA, Sweeney HL (1999) Myosin VI is an actin-based motor that moves backwards. Nature 401:505–508
Woody MS, Greenberg MJ, Barua B, Winkelmann DA, Goldman YE, Ostap EM (2018) Positive cardiac inotrope omecamtiv mecarbil activates muscle despite suppressing the myosin working stroke. Nat Commun 9:3838
Wulf SF, Ropars V, Fujita-Becker S, Oster M, Hofhaus G, Trabuco LG, Pylypenko O, Sweeney HL, Houdusse AM, Schröder RR (2016) Force-producing ADP state of myosin bound to actin. Proc Natl Acad Sci U S A 113:E1844–E1852
Yengo CM, Chrin L, Rovner AS, Berger CL (1999) Intrinsic tryptophan fluorescence identifies specific conformational changes at the actomyosin interface upon actin binding and ADP release. Biochemistry 38:14515–14523
Yount RG, Lawson D, Rayment I (1995) Is myosin a "back door" enzyme? Biophys J 68:44S–47S
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2020 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Sweeney, H.L., Houdusse, A., Robert-Paganin, J. (2020). Myosin Structures. In: Coluccio, L. (eds) Myosins. Advances in Experimental Medicine and Biology, vol 1239. Springer, Cham. https://doi.org/10.1007/978-3-030-38062-5_2
Download citation
DOI: https://doi.org/10.1007/978-3-030-38062-5_2
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-38061-8
Online ISBN: 978-3-030-38062-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)