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The on-off switch in regulated myosins: different triggers but related mechanisms.

Himmel DM, Mui S, O'Neall-Hennessey E, Szent-Györgyi AG, Cohen C
J Mol Biol 394 496-505 (2009)
Cited: 26 times
EuropePMC logo PMID: 19769984

Abstract

In regulated myosin, motor and enzymatic activities are toggled between the on-state and off-state by a switch located on its lever arm domain, here called the regulatory domain (RD). This region consists of a long alpha-helical "heavy chain" stabilized by a "regulatory" light chain (RLC) and an "essential" light chain (ELC). The on-state is activated by phosphorylation of the RLC of vertebrate smooth muscle RD or by direct binding of Ca(2+) to the ELC of molluscan RD. Crystal structures are available only for the molluscan RD. To understand in more detail the pathway between the on-state and the off-state, we have now also determined the crystal structure of a molluscan (scallop) RD in the absence of Ca(2+). Our results indicate that loss of Ca(2+) abolishes most of the interactions between the light chains and may increase the flexibility of the RD heavy chain. We propose that disruption of critical links with the C-lobe of the RLC is the key event initiating the off-state in both smooth muscle myosins and molluscan myosins.

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  2. Two structural motifs within canonical EF-hand calcium-binding domains identify five different classes of calcium buffers and sensors. Denessiouk K, Permyakov S, Denesyuk A, Permyakov E, Johnson MS. PLoS One 9 e109287 (2014)
  3. Visualizing key hinges and a potential major source of compliance in the lever arm of myosin. Brown JH, Kumar VS, O'Neall-Hennessey E, Reshetnikova L, Robinson H, Nguyen-McCarty M, Szent-Györgyi AG, Cohen C. Proc Natl Acad Sci U S A 108 114-119 (2011)


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  2. The apicomplexan glideosome and adhesins - Structures and function. Boucher LE, Bosch J. J Struct Biol 190 93-114 (2015)
  3. Vascular smooth muscle myosin light chain diphosphorylation: mechanism, function, and pathological implications. Walsh MP. IUBMB Life 63 987-1000 (2011)

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  2. A molecular model of phosphorylation-based activation and potentiation of tarantula muscle thick filaments. Brito R, Alamo L, Lundberg U, Guerrero JR, Pinto A, Sulbarán G, Gawinowicz MA, Craig R, Padrón R. J Mol Biol 414 44-61 (2011)
  3. The molecular basis for sarcomere organization in vertebrate skeletal muscle. Wang Z, Grange M, Wagner T, Kho AL, Gautel M, Raunser S. Cell 184 2135-2150.e13 (2021)
  4. Structural basis of the relaxed state of a Ca2+-regulated myosin filament and its evolutionary implications. Woodhead JL, Zhao FQ, Craig R. Proc Natl Acad Sci U S A 110 8561-8566 (2013)
  5. Two Essential Light Chains Regulate the MyoA Lever Arm To Promote Toxoplasma Gliding Motility. Williams MJ, Alonso H, Enciso M, Egarter S, Sheiner L, Meissner M, Striepen B, Smith BJ, Tonkin CJ. mBio 6 e00845-15 (2015)
  6. Phosphorylated smooth muscle heavy meromyosin shows an open conformation linked to activation. Baumann BA, Taylor DW, Huang Z, Tama F, Fagnant PM, Trybus KM, Taylor KA. J Mol Biol 415 274-287 (2012)
  7. Role of the essential light chain in the activation of smooth muscle myosin by regulatory light chain phosphorylation. Taylor KA, Feig M, Brooks CL, Fagnant PM, Lowey S, Trybus KM. J Struct Biol 185 375-382 (2014)
  8. Broad disorder and the allosteric mechanism of myosin II regulation by phosphorylation. Vileno B, Chamoun J, Liang H, Brewer P, Haldeman BD, Facemyer KC, Salzameda B, Song L, Li HC, Cremo CR, Fajer PG. Proc Natl Acad Sci U S A 108 8218-8223 (2011)
  9. Flexibility within the heads of muscle myosin-2 molecules. Billington N, Revill DJ, Burgess SA, Chantler PD, Knight PJ. J Mol Biol 426 894-907 (2014)
  10. Essential "ankle" in the myosin lever arm. Pylypenko O, Houdusse AM. Proc Natl Acad Sci U S A 108 5-6 (2011)
  11. Modification of interface between regulatory and essential light chains hampers phosphorylation-dependent activation of smooth muscle myosin. Ni S, Hong F, Haldeman BD, Baker JE, Facemyer KC, Cremo CR. J Biol Chem 287 22068-22079 (2012)
  12. Sequential myosin phosphorylation activates tarantula thick filament via a disorder-order transition. Espinoza-Fonseca LM, Alamo L, Pinto A, Thomas DD, Padrón R. Mol Biosyst 11 2167-2179 (2015)
  13. Allosteric communication in Dictyostelium myosin II. Guhathakurta P, Prochniewicz E, Muretta JM, Titus MA, Thomas DD. J Muscle Res Cell Motil 33 305-312 (2012)
  14. Twitchin can regulate the ATPase cycle of actomyosin in a phosphorylation-dependent manner in skinned mammalian skeletal muscle fibres. Avrova SV, Rysev NA, Matusovsky OS, Shelud'ko NS, Borovikov YS. Arch Biochem Biophys 521 1-9 (2012)
  15. Crystal structure of a phosphorylated light chain domain of scallop smooth-muscle myosin. Kumar VS, O'Neall-Hennessey E, Reshetnikova L, Brown JH, Robinson H, Szent-Györgyi AG, Cohen C. Biophys J 101 2185-2189 (2011)
  16. EF-hand proteins and the regulation of actin-myosin interaction in the eutardigrade Hypsibius klebelsbergi (tardigrada). Prasath T, Greven H, D'Haese J. J Exp Zool A Ecol Genet Physiol 317 311-320 (2012)
  17. Calcium-mediated regulation of recombinant hybrids of full-length Physarum myosin heavy chain with Physarum/scallop myosin light chains. Zhang Y, Kawamichi H, Kohama K, Nakamura A. Acta Biochim Biophys Sin (Shanghai) 48 536-543 (2016)
  18. Hypertrophic cardiomyopathy mutations in the pliant and light chain-binding regions of the lever arm of human β-cardiac myosin have divergent effects on myosin function. Morck MM, Bhowmik D, Pathak D, Dawood A, Spudich J, Ruppel KM. Elife 11 e76805 (2022)
  19. Molluscan twitchin can control actin-myosin interaction during ATPase cycle. Borovikov YS, Shelud'ko NS, Avrova SV. Arch Biochem Biophys 495 122-128 (2010)
  20. Regulatory light chains modulate in vitro actin motility driven by skeletal heavy meromyosin. Vikhoreva NN, Månsson A. Biochem Biophys Res Commun 403 1-6 (2010)


Related citations provided by authors (2)

  1. Structure of the Regulatory Domain of Scallop Myosin at 2 A Resolution: Implications for Regulation.. Houdusse A, Cohen C Structure 4 21-32 (1996)
  2. Structure of the Regulatory Domain of Scallop Myosin at 2.8 A Resolution.. Xie X, Harrison DH, Schlichting I, Sweet RM, Kalabokis VN, Szent-Gyorgyi A, Cohen C Nature 368 306-312 (1994)

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