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Journal of Biomedicine and Biotechnology
Volume 2011, Article ID 636403, 9 pages
http://dx.doi.org/10.1155/2011/636403
Review Article

Myosin Binding Protein-C: A Regulator of Actomyosin Interaction in Striated Muscle

Department of Biochemistry and Molecular Biology, School of Medicine, University of Maryland, Baltimore, MD 21201, USA

Received 19 June 2011; Accepted 25 July 2011

Academic Editor: Robert J. Bloch

Copyright © 2011 Maegen A. Ackermann and Aikaterini Kontrogianni-Konstantopoulos. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. A. Clark, A. S. McElhinny, M. C. Beckerle, and C. C. Gregorio, “Striated muscle cytoarchitecture: an intricate web of form and function,” Annual Review of Cell and Developmental Biology, vol. 18, pp. 637–706, 2002. View at Publisher · View at Google Scholar · View at Scopus
  2. G. Offer, C. Moos, and R. Starr, “A new protein of the thick filaments of vertebrate skeletal myofibrils. Extraction, purification and characterization,” Journal of Molecular Biology, vol. 74, no. 4, pp. 653–676, 1973. View at Google Scholar · View at Scopus
  3. E. Flashman, C. Redwood, J. Moolman-Smook, and H. Watkins, “Cardiac myosin binding protein C: its role in physiology and disease,” Circulation Research, vol. 94, no. 10, pp. 1279–1289, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. C. E. Oakley, J. Chamoun, L. J. Brown, and B. D. Hambly, “Myosin binding protein-C: enigmatic regulator of cardiac contraction,” International Journal of Biochemistry and Cell Biology, vol. 39, no. 12, pp. 2161–2166, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. P. Bennett, R. Craig, R. Starr, and G. Offer, “The ultrastructural location of C-protein, X-protein and H-protein in rabbit muscle,” Journal of Muscle Research and Cell Motility, vol. 7, no. 6, pp. 550–567, 1986. View at Google Scholar · View at Scopus
  6. F. A. Pepe, F. T. Ashton, C. Street, and J. Weisel, “The myosin filament. X. Observation of nine subfilaments in transverse sections,” Tissue and Cell, vol. 18, no. 4, pp. 499–508, 1986. View at Google Scholar · View at Scopus
  7. F. A. Pepe and B. Drucker, “The myosin filament. III. C protein,” Journal of Molecular Biology, vol. 99, no. 4, pp. 609–617, 1975. View at Google Scholar · View at Scopus
  8. M. Gautel, O. Zuffardi, P. Freiburg, and S. Labeit, “Phosphorylation switches specific for the cardiac isoform of myosin binding protein-C: a modulator of cardiac contraction?” EMBO Journal, vol. 14, no. 9, pp. 1952–1960, 1995. View at Google Scholar · View at Scopus
  9. F. E. Weber, K. T. Vaughan, F. C. Reinach, and D. A. Fischman, “Complete sequence of human fast-type and slow-type muscle myosin-binding-protein C (MyBP-C). Differential expression, conserved domain structure and chromosome assignment,” European Journal of Biochemistry, vol. 216, no. 2, pp. 661–669, 1993. View at Google Scholar · View at Scopus
  10. S. Einheber and D. A. Fischman, “Isolation and characterization of a cDNA clone encoding avian skeletal muscle C-protein: an intracellular member of the immunoglobulin superfamily,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 6, pp. 2157–2161, 1990. View at Google Scholar · View at Scopus
  11. M. Yasuda, S. Koshida, N. Sato, and T. Obinata, “Complete primary structure of chicken cardiac C-protein (MyBP-C) and its expression in developing striated muscles,” Journal of Molecular and Cellular Cardiology, vol. 27, no. 10, pp. 2275–2286, 1995. View at Google Scholar · View at Scopus
  12. M. A. Ackermann and A. Kontrogianni-Konstantopoulos, “Myosin binding protein-C slow: an intricate subfamily of proteins,” Journal of Biomedicine and Biotechnology, vol. 2010, Article ID 652065, 10 pages, 2010. View at Publisher · View at Google Scholar
  13. M. A. Ackermann, L. Y. R. Hu, A. L. Bowman, R. J. Bloch, and A. Kontrogianni-Konstantopoulos, “Obscurin interacts with a novel isoform of MyBP-C slow at the periphery of the sarcomeric M-band and regulates thick filament assembly,” Molecular Biology of the Cell, vol. 20, no. 12, pp. 2963–2978, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. B. Udd, “Third filament diseases,” Advances in Experimental Medicine and Biology, vol. 642, pp. 99–115, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. B. Udd, H. Haravuori, H. Kalimo et al., “Tibial muscular dystrophy - from clinical description to linkage on chromosome 2q31,” Neuromuscular Disorders, vol. 8, no. 5, pp. 327–332, 1998. View at Publisher · View at Google Scholar · View at Scopus
  16. M. A. Ackermann and A. Kontrogianni-Konstantopoulos, “Myosin Binding Protein-C Slow is a Novel Substrate for Protein Kinase A (PKA) and C (PKC) in Skeletal Muscle.,” Journal of proteome research, vol. 10, no. 10, Article ID 652065, pp. 4547–4555, 2011. View at Google Scholar
  17. R. Starr and G. Offer, “Polypeptide chains of intermediate molecular weight in myosin preparations,” FEBS Letters, vol. 15, no. 1, pp. 40–44, 1971. View at Google Scholar · View at Scopus
  18. G. Bonne, L. Carrier, J. Bercovici et al., “Cardiac myosin binding protein-C gene splice acceptor site mutation is associated with familial hypertrophic cardiomyopathy,” Nature Genetics, vol. 11, no. 4, pp. 438–440, 1995. View at Google Scholar · View at Scopus
  19. H. Watkins, D. Conner, L. Thierfelder et al., “Mutations in the cardiac myosin binding protein-C gene on chromosome 11 cause familial hypertrophic cardiomyopathy,” Nature Genetics, vol. 11, no. 4, pp. 434–437, 1995. View at Google Scholar · View at Scopus
  20. T. Chakrabarty, M. Xiao, R. Cooke, and P. R. Selvin, “Holding two heads together: stability of the myosin II rod measured by resonance energy transfer between the heads,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 9, pp. 6011–6016, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. I. Rayment, W. R. Rypniewski, K. Schmidt-Base et al., “Three-dimensional structure of myosin subfragment-1: a molecular motor,” Science, vol. 261, no. 5117, pp. 50–58, 1993. View at Google Scholar · View at Scopus
  22. J. L. Woodhead, F. Q. Zhao, R. Craig, E. H. Egelman, L. Alamo, and R. Padrón, “Atomic model of a myosin filament in the relaxed state,” Nature, vol. 436, no. 7054, pp. 1195–1199, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. I. Rayment, H. M. Holden, M. Whittaker et al., “Structure of the actin-myosin complex and its implications for muscle contraction,” Science, vol. 261, no. 5117, pp. 58–65, 1993. View at Google Scholar · View at Scopus
  24. B. A. Colson, M. R. Locher, T. Bekyarova et al., “Differential roles of regulatory light chain and myosin binding protein-C phosphorylations in the modulation of cardiac force development,” Journal of Physiology, vol. 588, no. 6, pp. 981–993, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. I. Morano, “Tuning the human heart molecular motors by myosin light chairs,” Journal of Molecular Medicine, vol. 77, no. 7, pp. 544–555, 1999. View at Publisher · View at Google Scholar · View at Scopus
  26. R. Starr and G. Offer, “The interaction of C-protein with heavy meromyosin and subfragment-2,” Biochemical Journal, vol. 171, no. 3, pp. 813–816, 1978. View at Google Scholar · View at Scopus
  27. T. Okagaki, F. E. Weber, D. A. Fischman, K. T. Vaughan, T. Mikawa, and F. C. Reinach, “The major myosin-binding domain of skeletal muscle MyBP-C (C protein) resides in the COOH-terminal, immunoglobulin C2 motif,” Journal of Cell Biology, vol. 123, no. 3, pp. 619–626, 1993. View at Publisher · View at Google Scholar · View at Scopus
  28. E. Flashman, H. Watkins, and C. Redwood, “Localization of the binding site of the C-terminal domain of cardiac myosin-binding protein-C on the myosin rod,” Biochemical Journal, vol. 401, no. 1, pp. 97–102, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. C. A. Miyamoto, D. A. Fischman, and F. C. Reinach, “The interface between MyBP-C and myosin: site-directed mutagenesis of the CX myosin-binding domain of MyBP-C,” Journal of Muscle Research and Cell Motility, vol. 20, no. 7, pp. 703–715, 1999. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Kontrogianni-Konstantopoulos, M. A. Ackermann, A. L. Bowman, S. V. Yap, and R. J. Bloch, “Muscle giants: molecular scaffolds in sarcomerogenesis,” Physiological Reviews, vol. 89, no. 4, pp. 1217–1267, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Freiburg and M. Gautel, “A molecular map of the interactions between titin and myosin-binding protein C Implications for sarcomeric assembly in familial hypertrophic cardiomyopathy,” European Journal of Biochemistry, vol. 235, no. 1-2, pp. 317–323, 1996. View at Google Scholar · View at Scopus
  32. J. Ratti, “Structure and interactions of myosin-binding protein c domain c0: cardiac-specific regulation of myosin at its neck?” Journal of Biological Chemistry, vol. 286, no. 14, pp. 12650–12658, 2011. View at Google Scholar
  33. A. Ababou, E. Rostkova, S. Mistry, C. L. Masurier, M. Gautel, and M. Pfuhl, “Myosin binding protein C positioned to play a key role in regulation of muscle contraction: structure and interactions of domain C1,” Journal of Molecular Biology, vol. 384, no. 3, pp. 615–630, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Gruen and M. Gautel, “Mutations in β-myosin S2 that cause familial hypertrophic cardiomyopathy (FHC) abolish the interaction with the regulatory domain of myosin-binding protein-C,” Journal of Molecular Biology, vol. 286, no. 3, pp. 933–949, 1999. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Ababou, M. Gautel, and M. Pfuhl, “Dissecting the N-terminal myosin binding site of human cardiac myosin-binding protein C: structure and myosin binding of domain C2,” Journal of Biological Chemistry, vol. 282, no. 12, pp. 9204–9215, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Moos, C. M. Mason, and J. M. Besterman, “The binding of skeletal muscle C-protein to F-actin, and its relation to the interaction of actin with myosin subfragment-1,” Journal of Molecular Biology, vol. 124, no. 5, pp. 571–586, 1978. View at Google Scholar · View at Scopus
  37. I. Kulikovskaya, G. McClellan, J. Flavigny, L. Carrier, and S. Winegrad, “Effect of MyBP-C binding to actin on contractility in heart muscle,” Journal of General Physiology, vol. 122, no. 6, pp. 761–774, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. A. E. Whitten, C. M. Jeffries, S. P. Harris, and J. Trewhella, “Cardiac myosin-binding protein C decorates F-actin: implications for cardiac function,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 47, pp. 18360–18365, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. R. W. Kensler, J. F. Shaffer, and S. P. Harris, “Binding of the N-terminal fragment C0-C2 of cardiac MyBP-C to cardiac F-actin,” Journal of Structural Biology, vol. 174, no. 1, pp. 44–51, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. M. V. Razumova, J. F. Shaffer, A. Y. Tu, G. V. Flint, M. Regnier, and S. P. Harris, “Effects of the N-terminal domains of myosin binding protein-C in an in vitro motility assay: evidence for long-lived cross-bridges,” Journal of Biological Chemistry, vol. 281, no. 47, pp. 35846–35854, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. J. F. Shaffer, R. W. Kensler, and S. P. Harris, “The myosin-binding protein C motif binds to F-actin in a phosphorylation-sensitive manner,” Journal of Biological Chemistry, vol. 284, no. 18, pp. 12318–12327, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. I. N. Rybakova, M. L. Greaser, and R. L. Moss, “Myosin binding protein C interaction with actin: characterization and mapping of the binding site,” The Journal of Biological Chemistry, vol. 286, no. 3, pp. 2008–2016, 2011. View at Google Scholar
  43. J. Moolman-Smook, E. Flashman, W. De Lange et al., “Identification of novel interactions between domains of myosin binding protein-C that are modulated by hypertrophic cardiomyopathy missense mutations,” Circulation Research, vol. 91, no. 8, pp. 704–711, 2002. View at Publisher · View at Google Scholar · View at Scopus
  44. R. Gilbert, J. A. Cohen, S. Pardo, A. Basu, and D. A. Fischman, “Identification of the A-band localization domain of myosin binding proteins C and H (MyBP-C, MyBP-H) in skeletal muscle,” Journal of Cell Science, vol. 112, no. 1, pp. 69–79, 1999. View at Google Scholar · View at Scopus
  45. R. Gilbert, M. G. Kelly, T. Mikawa, and D. A. Fischman, “The carboxyl terminus of myosin binding protein C (MyBP-C, C-protein) specifies incorporation into the A-band of striated muscle,” Journal of Cell Science, vol. 109, no. 1, pp. 101–111, 1996. View at Google Scholar · View at Scopus
  46. M. Gruen, H. Prinz, and M. Gautel, “cAPK-phosphorylation controls the interaction of the regulatory domain of cardiac myosin binding protein C with myosin-S2 in an on-off fashion,” FEBS Letters, vol. 453, no. 3, pp. 254–259, 1999. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Sadayappan, J. Gulick, R. Klevitsky et al., “Cardiac myosin binding protein-C phosphorylation in a β-myosin heavy chain background,” Circulation, vol. 119, no. 9, pp. 1253–1262, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Sadayappan, J. Gulick, H. Osinska et al., “Cardiac myosin-binding protein-C phosphorylation and cardiac function,” Circulation Research, vol. 97, no. 11, pp. 1156–1163, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Sadayappan, H. Osinska, R. Klevitsky et al., “Cardiac myosin binding protein c phosphorylation is cardioprotective,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 45, pp. 16918–16923, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. K. Yamamoto, “The binding of skeletal muscle C-protein to regulated actin,” FEBS Letters, vol. 208, no. 1, pp. 123–127, 1986. View at Google Scholar · View at Scopus
  51. J. Y. Mun et al., “Electron microscopy and 3D reconstruction of F-actin decorated with cardiac myosin-binding protein C (cMyBP-C),” Journal of Molecular Biology, vol. 410, no. 2, pp. 214–225, 2011. View at Google Scholar
  52. M. E. Zoghbi, J. L. Woodhead, R. L. Moss, and R. Craig, “Three-dimensional structure of vertebrate cardiac muscle myosin filaments,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 7, pp. 2386–2390, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. C. A. Gurnett, D. M. Desruisseau, K. McCall et al., “Myosin binding protein C1: a novel gene for autosomal dominant distal arthrogryposis type 1,” Human Molecular Genetics, vol. 19, no. 7, pp. 1165–1173, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. D. O. Fürst, U. Vinkemeier, and K. Weber, “Mammalian skeletal muscle C-protein: purification from bovine muscle, binding to titin and the characterization of a full-length human cDNA,” Journal of Cell Science, vol. 102, no. 4, pp. 769–778, 1992. View at Google Scholar · View at Scopus
  55. M. J. McGrath, D. L. Cottle, M. A. Nguyen et al., “Four and a half LIM protein 1 binds myosin-binding protein C and regulates myosin filament formation and sarcomere assembly,” Journal of Biological Chemistry, vol. 281, no. 11, pp. 7666–7683, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. S. P. Harris, R. G. Lyons, and K. L. Bezold, “In the thick of it: HCM-causing mutations in myosin binding proteins of the thick filament,” Circulation Research, vol. 108, no. 6, pp. 751–764, 2011. View at Google Scholar
  57. T. Konno, S. Chang, J. G. Seidman, and C. E. Seidman, “Genetics of hypertrophic cardiomyopathy,” Current Opinion in Cardiology, vol. 25, no. 3, pp. 205–209, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. Q. Xu, S. Dewey, S. Nguyen, and A. V. Gomes, “Malignant and benign mutations in familial cardiomyopathies: insights into mutations linked to complex cardiovascular phenotypes,” Journal of Molecular and Cellular Cardiology, vol. 48, no. 5, pp. 899–909, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. C. E. Oakley, B. D. Hambly, P. M. Curmi, and L. J. Brown, “Myosin binding protein C: structural abnormalities in familial hypertrophic cardiomyopathy,” Cell Research, vol. 14, no. 2, pp. 95–110, 2004. View at Google Scholar · View at Scopus
  60. W. Rottbauer, M. Gautel, J. Zehelein et al., “Novel splice donor site mutation in the cardiac myosin-binding protein- C gene in familial hypertrophic cardiomyopathy. Characterization of cardiac transcript and protein,” Journal of Clinical Investigation, vol. 100, no. 2, pp. 475–482, 1997. View at Google Scholar · View at Scopus
  61. J. S. Davis, “Interaction of C-protein with pH 8.0 synthetic thick filaments prepared from the myosin of vertebrate skeletal muscle,” Journal of Muscle Research and Cell Motility, vol. 9, no. 2, pp. 174–183, 1988. View at Publisher · View at Google Scholar · View at Scopus
  62. J. F. Koretz, “Effects of C-protein on synthetic myosin filament structure,” Biophysical Journal, vol. 27, no. 3, pp. 433–446, 1979. View at Google Scholar · View at Scopus
  63. W. Saber, K. J. Begin, D. M. Warshaw, and P. VanBuren, “Cardiac myosin binding protein-C modulates actomyosin binding and kinetics in the in vitro motility assay,” Journal of Molecular and Cellular Cardiology, vol. 44, no. 6, pp. 1053–1061, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. J. F. Shaffer, M. V. Razumova, A. Y. Tu, M. Regnier, and S. P. Harris, “Myosin S2 is not required for effects of myosin binding protein-C on motility,” FEBS Letters, vol. 581, no. 7, pp. 1501–1504, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. D. V. Shchepkin, G. V. Kopylova, L. V. Nikitina, L. B. Katsnelson, and S. Y. Bershitsky, “Effects of cardiac myosin binding protein-C on the regulation of interaction of cardiac myosin with thin filament in an in vitro motility assay,” Biochemical and Biophysical Research Communications, vol. 401, no. 1, pp. 159–163, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. K. Yamamoto and C. Moos, “The C-proteins of rabbit red, white, and cardiac muscles,” Journal of Biological Chemistry, vol. 258, no. 13, pp. 8395–8401, 1983. View at Google Scholar · View at Scopus
  67. S. S. Margossian, “Reversible dissociation of dog cardiac myosin regulatory light chain 2 and its influence on ATP hydrolysis,” Journal of Biological Chemistry, vol. 260, no. 25, pp. 13747–13754, 1985. View at Google Scholar · View at Scopus
  68. T. N. Alyonycheva, T. Mikawa, F. C. Reinach, and D. A. Fischman, “Isoform-specific interaction of the myosin-binding proteins (MyBPs) with skeletal and cardiac myosin is a property of the C-terminal immunoglobulin domain,” Journal of Biological Chemistry, vol. 272, no. 33, pp. 20866–20872, 1997. View at Publisher · View at Google Scholar · View at Scopus
  69. S. C. Calaghan, J. Trinick, P. J. Knight, and E. White, “A role for C-protein in the regulation of contraction and intracellular Ca2+ in intact rat ventricular myocytes,” Journal of Physiology, vol. 528, no. 1, pp. 151–156, 2000. View at Google Scholar · View at Scopus
  70. L. Carrier, “Cardiac myosin-binding protein C in the heart,” Archives des Maladies du Coeur et des Vaisseaux, vol. 100, no. 3, pp. 238–243, 2007. View at Google Scholar · View at Scopus
  71. J. M. Squire, P. K. Luther, and C. Knupp, “Structural evidence for the interaction of C-protein (MyBP-C) with actin and sequence identification of a possible actin-binding domain,” Journal of Molecular Biology, vol. 331, no. 3, pp. 713–724, 2003. View at Publisher · View at Google Scholar · View at Scopus
  72. E. Flashman, L. Korkie, H. Watkins, C. Redwood, and J. C. Moolman-Smook, “Support for a trimeric collar of myosin binding protein C in cardiac and fast skeletal muscle, but not in slow skeletal muscle,” FEBS Letters, vol. 582, no. 3, pp. 434–438, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. E. Rome, G. Offer, and F. A. Pepe, “X ray diffraction of muscle labelled with antibody to C protein,” Nature New Biology, vol. 244, no. 135, pp. 152–154, 1973. View at Google Scholar · View at Scopus
  74. F. J. Julian, R. L. Moss, and G. S. Waller, “Mechanical properties and myosin light chain composition of skinned muscle fibres from adult and new-born rabbits,” Journal of Physiology, vol. 311, pp. 201–218, 1981. View at Google Scholar · View at Scopus
  75. H. C. Hartzell and W. S. Sale, “Structure of C protein purified from cardiac muscle,” Journal of Cell Biology, vol. 100, no. 1, pp. 208–215, 1985. View at Google Scholar · View at Scopus
  76. D. J. Timson, “Fine tuning the myosin motor: the role of the essential light chain in striated muscle myosin,” Biochimie, vol. 85, no. 7, pp. 639–645, 2003. View at Publisher · View at Google Scholar · View at Scopus
  77. G. P. Farman, M. S. Miller, M. C. Reedy et al., “Phosphorylation and the N-terminal extension of the regulatory light chain help orient and align the myosin heads in Drosophila flight muscle,” Journal of Structural Biology, vol. 168, no. 2, pp. 240–249, 2009. View at Publisher · View at Google Scholar · View at Scopus
  78. T. M. Butler, S. U. Mooers, S. R. Narayan, and M. J. Siegman, “The N-terminal region of twitchin binds thick and thin contractile filaments: redundant mechanisms of catch force maintenance,” Journal of Biological Chemistry, vol. 285, no. 52, pp. 40654–40665, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. D. Funabara, C. Hamamoto, K. Yamamoto et al., “Unphosphorylated twitchin forms a complex with actin and myosin that may contribute to tension maintenance in catch,” Journal of Experimental Biology, vol. 210, no. 24, pp. 4399–4410, 2007. View at Publisher · View at Google Scholar · View at Scopus