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Skip residues modulate the structural properties of the myosin rod and guide thick filament assembly.

Taylor KC, Buvoli M, Korkmaz EN, Buvoli A, Zheng Y, Heinze NT, Cui Q, Leinwand LA, Rayment I
Proc Natl Acad Sci U S A 112 E3806-15 (2015)
Related entries: 4xa3, 4xa4, 4xa6

Cited: 36 times
EuropePMC logo PMID: 26150528

Abstract

The rod of sarcomeric myosins directs thick filament assembly and is characterized by the insertion of four skip residues that introduce discontinuities in the coiled-coil heptad repeats. We report here that the regions surrounding the first three skip residues share high structural similarity despite their low sequence homology. Near each of these skip residues, the coiled-coil transitions to a nonclose-packed structure inducing local relaxation of the superhelical pitch. Moreover, molecular dynamics suggest that these distorted regions can assume different conformationally stable states. In contrast, the last skip residue region constitutes a true molecular hinge, providing C-terminal rod flexibility. Assembly of myosin with mutated skip residues in cardiomyocytes shows that the functional importance of each skip residue is associated with rod position and reveals the unique role of the molecular hinge in promoting myosin antiparallel packing. By defining the biophysical properties of the rod, the structures and molecular dynamic calculations presented here provide insight into thick filament formation, and highlight the structural differences occurring between the coiled-coils of myosin and the stereotypical tropomyosin. In addition to extending our knowledge into the conformational and biological properties of coiled-coil discontinuities, the molecular characterization of the four myosin skip residues also provides a guide to modeling the effects of rod mutations causing cardiac and skeletal myopathies.

Articles - 4xa1 mentioned but not cited (3)

  1. Structure of myosin filaments from relaxed Lethocerus flight muscle by cryo-EM at 6 Å resolution. Hu Z, Taylor DW, Reedy MK, Edwards RJ, Taylor KA. Sci Adv 2 e1600058 (2016)
  2. Skip residues modulate the structural properties of the myosin rod and guide thick filament assembly. Taylor KC, Buvoli M, Korkmaz EN, Buvoli A, Zheng Y, Heinze NT, Cui Q, Leinwand LA, Rayment I. Proc Natl Acad Sci U S A 112 E3806-15 (2015)
  3. The myosin II coiled-coil domain atomic structure in its native environment. Rahmani H, Ma W, Hu Z, Daneshparvar N, Taylor DW, McCammon JA, Irving TC, Edwards RJ, Taylor KA. Proc Natl Acad Sci U S A 118 e2024151118 (2021)


Reviews citing this publication (2)

  1. Disease mutations in striated muscle myosins. Parker F, Peckham M. Biophys Rev 12 887-894 (2020)
  2. Filament evanescence of myosin II and smooth muscle function. Wang L, Chitano P, Seow CY. J Gen Physiol 153 e202012781 (2021)

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  2. Coiled-Coil Formation Conveys a STIM1 Signal from ER Lumen to Cytoplasm. Hirve N, Rajanikanth V, Hogan PG, Gudlur A. Cell Rep 22 72-83 (2018)
  3. Cryo-EM structure of the inhibited (10S) form of myosin II. Yang S, Tiwari P, Lee KH, Sato O, Ikebe M, Padrón R, Craig R. Nature 588 521-525 (2020)
  4. Kinesin-2 KIF3AC and KIF3AB Can Drive Long-Range Transport along Microtubules. Guzik-Lendrum S, Rank KC, Bensel BM, Taylor KC, Rayment I, Gilbert SP. Biophys J 109 1472-1482 (2015)
  5. Structure and Misfolding of the Flexible Tripartite Coiled-Coil Domain of Glaucoma-Associated Myocilin. Hill SE, Nguyen E, Donegan RK, Patterson-Orazem AC, Hazel A, Gumbart JC, Lieberman RL. Structure 25 1697-1707.e5 (2017)
  6. Insights into myosin regulatory and essential light chains: a focus on their roles in cardiac and skeletal muscle function, development and disease. Sitbon YH, Yadav S, Kazmierczak K, Szczesna-Cordary D. J Muscle Res Cell Motil 41 313-327 (2020)
  7. The SARS-CoV-2 SSHHPS Recognized by the Papain-like Protease. Reynolds ND, Aceves NM, Liu JL, Compton JR, Leary DH, Freitas BT, Pegan SD, Doctor KZ, Wu FY, Hu X, Legler PM. ACS Infect Dis 7 1483-1502 (2021)
  8. The SH3 domain of UNC-89 (obscurin) interacts with paramyosin, a coiled-coil protein, in Caenorhabditis elegans muscle. Qadota H, Mayans O, Matsunaga Y, McMurry JL, Wilson KJ, Kwon GE, Stanford R, Deehan K, Tinley TL, Ngwa VM, Benian GM. Mol Biol Cell 27 1606-1620 (2016)
  9. A composite approach towards a complete model of the myosin rod. Korkmaz EN, Taylor KC, Andreas MP, Ajay G, Heinze NT, Cui Q, Rayment I. Proteins 84 172-189 (2016)
  10. CryoEM structure of Drosophila flight muscle thick filaments at 7 Å resolution. Daneshparvar N, Taylor DW, O'Leary TS, Rahmani H, Abbasiyeganeh F, Previs MJ, Taylor KA. Life Sci Alliance 3 e202000823 (2020)
  11. Addressing the Molecular Mechanism of Longitudinal Lamin Assembly Using Chimeric Fusions. Stalmans G, Lilina AV, Vermeire PJ, Fiala J, Novák P, Strelkov SV. Cells 9 E1633 (2020)
  12. Endogenous protein tagging in medaka using a simplified CRISPR/Cas9 knock-in approach. Seleit A, Aulehla A, Paix A. Elife 10 e75050 (2021)
  13. Family-specific Kinesin Structures Reveal Neck-linker Length Based on Initiation of the Coiled-coil. Phillips RK, Peter LG, Gilbert SP, Rayment I. J Biol Chem 291 20372-20386 (2016)
  14. The small molecule chemical compound cinobufotalin attenuates resistance to DDP by inducing ENKUR expression to suppress MYH9-mediated c-Myc deubiquitination in lung adenocarcinoma. Liu JH, Yang HL, Deng ST, Hu Z, Chen WF, Yan WW, Hou RT, Li YH, Xian RT, Xie YY, Su Y, Wu LY, Xu P, Zhu ZB, Liu X, Deng YL, Wang YB, Liu Z, Fang WY. Acta Pharmacol Sin 43 2687-2695 (2022)
  15. Distal myopathy with coexisting heterozygous TIA1 and MYH7 Variants. Brand P, Dyck PJ, Liu J, Berini S, Selcen D, Milone M. Neuromuscul Disord 26 511-515 (2016)
  16. Structure and function of Spc42 coiled-coils in yeast centrosome assembly and duplication. Drennan AC, Krishna S, Seeger MA, Andreas MP, Gardner JM, Sether EKR, Jaspersen SL, Rayment I. Mol Biol Cell 30 1505-1522 (2019)
  17. Clinical diversity of MYH7-related cardiomyopathies: Insights into genotype-phenotype correlations. Hershkovitz T, Kurolap A, Ruhrman-Shahar N, Monakier D, DeChene ET, Peretz-Amit G, Funke B, Zucker N, Hirsch R, Tan WH, Baris Feldman H. Am J Med Genet A 179 365-372 (2019)
  18. A1603P and K1617del, Mutations in β-Cardiac Myosin Heavy Chain that Cause Laing Early-Onset Distal Myopathy, Affect Secondary Structure and Filament Formation In Vitro and In Vivo. Parker F, Batchelor M, Wolny M, Hughes R, Knight PJ, Peckham M. J Mol Biol 430 1459-1478 (2018)
  19. Evidence for S2 flexibility by direct visualization of quantum dot-labeled myosin heads and rods within smooth muscle myosin filaments moving on actin in vitro. Brizendine RK, Anuganti M, Cremo CR. J Gen Physiol 153 e202012751 (2021)
  20. Design considerations in coiled-coil fusion constructs for the structural determination of a problematic region of the human cardiac myosin rod. Andreas MP, Ajay G, Gellings JA, Rayment I. J Struct Biol 200 219-228 (2017)
  21. Electrostatic and bending energies predict staggering and splaying in nonmuscle myosin II minifilaments. Kaufmann TL, Schwarz US. PLoS Comput Biol 16 e1007801 (2020)
  22. Post-translational modification patterns on β-myosin heavy chain are altered in ischemic and nonischemic human hearts. Landim-Vieira M, Childers MC, Wacker AL, Garcia MR, He H, Singh R, Brundage EA, Johnston JR, Whitson BA, Chase PB, Janssen PML, Regnier M, Biesiadecki BJ, Pinto JR, Parvatiyar MS. Elife 11 e74919 (2022)
  23. Secondary Structure of the Novel Myosin Binding Domain WYR and Implications within Myosin Structure. Menard LM, Wood NB, Vigoreaux JO. Biology (Basel) 10 603 (2021)
  24. Stability profile of vimentin rod domain. Lilina AV, Leekens S, Hashim HM, Vermeire PJ, Harvey JN, Strelkov SV. Protein Sci 31 e4505 (2022)
  25. Microtubule pivoting enables mitotic spindle assembly in S. cerevisiae. Fong KK, Davis TN, Asbury CL. J Cell Biol 220 e202007193 (2021)
  26. Contiguity and Structural Impacts of a Non-Myosin Protein within the Thick Filament Myosin Layers. Menard LM, Wood NB, Vigoreaux JO. Biology (Basel) 10 613 (2021)
  27. Mapping genotype-phenotype associations of nsSNPs in coiled-coil oligomerization domains of the human proteome. Mohanasundaram KA, Grover MP, Crowley TM, Goscinski A, Wouters MA. Hum Mutat 38 1378-1393 (2017)
  28. Structure of the Flight Muscle Thick Filament from the Bumble Bee, Bombus ignitus, at 6 Å Resolution. Li J, Rahmani H, Abbasi Yeganeh F, Rastegarpouyani H, Taylor DW, Wood NB, Previs MJ, Iwamoto H, Taylor KA. Int J Mol Sci 24 377 (2022)
  29. Cryo-EM structure of the human cardiac myosin filament. Dutta D, Nguyen V, Campbell KS, Padrón R, Craig R. Nature (2023)
  30. Effects of specific disease mutations in non-muscle myosin 2A on its structure and function. Casas-Mao D, Carrington G, Pujol MG, Peckham M. J Biol Chem 300 105514 (2023)
  31. Human skeletal myopathy myosin mutations disrupt myosin head sequestration. Carrington G, Hau A, Kosta S, Dugdale HF, Muntoni F, D'Amico A, Van den Bergh P, Romero NB, Malfatti E, Vilchez JJ, Oldfors A, Pajusalu S, Õunap K, Giralt-Pujol M, Zanoteli E, Campbell KS, Iwamoto H, Peckham M, Ochala J. JCI Insight 8 e172322 (2023)


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