Impact of disease-causing mutations on inter-domain interactions in cMyBP-C: a steered molecular dynamics study

References

• Ababou, A., Gautel, M., & Pfuhl, M. (2007). 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, 282, 9204–9215.10.1074/jbc.M610899200
   PubMed Web of Science ®Google Scholar
• Ashrafian, H., Redwood, C., Blair, E., & Watkins, H. (2003). Hypertrophic cardiomyopathy: A paradigm for myocardial energy depletion. Trends in Genetics, 19, 263–268.10.1016/S0168-9525(03)00081-7
   PubMed Web of Science ®Google Scholar
• Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., & Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. The Journal of Chemical Physics, 81, 3684–3691.10.1063/1.448118
   Web of Science ®Google Scholar
• Colson, B. A., Bekyarova, T., Locher, M. R., Fitzsimons, D. P., Irving, T. C., & Moss, R. L. (2008). Protein kinase A-mediated phosphorylation of cMyBP-C increases proximity of myosin heads to actin in resting myocardium. Circulation Research, 103, 244–251.10.1161/CIRCRESAHA.108.178996
   PubMed Web of Science ®Google Scholar
• Comeau, S. R., Gatchell, D. W., Vajda, S., & Camacho, C. J. (2004). ClusPro: An automated docking and discrimination method for the prediction of protein complexes. Bioinformatics, 20, 45–50.10.1093/bioinformatics/btg371
   PubMed Web of Science ®Google Scholar
• Craig, R., Lee, K. H., Mun, J. Y., Torre, I., & Luther, P. K. (2014). Structure, sarcomeric organization and thin filament binding of cardiac myosin-binding protein-C. Pflügers Archiv – European Journal of Physiology, 466, 425–431.10.1007/s00424-013-1426-6
   PubMed Web of Science ®Google Scholar
• Finley, N. L., & Cuperman, T. I. (2014). Cardiac myosin binding protein-C: A structurally dynamic regulator of myocardial contractility. Pflügers Archiv – European Journal of Physiology, 466, 433–438.10.1007/s00424-014-1451-0
   PubMed Web of Science ®Google Scholar
• Flashman, E., Redwood, C., Moolman-Smook, J., & Watkins, H. (2004). Cardiac myosin binding protein C: Its role in physiology and disease. Circulation Research, 94, 1279–1289.10.1161/01.RES.0000127175.21818.C2
   PubMed Web of Science ®Google Scholar
• Frey, N., Luedde, M., & Katus, H. A. (2011). Mechanisms of disease: Hypertrophic cardiomyopathy. Nature Reviews Cardiology, 9, 91–100.10.1038/nrcardio.2011.159
   PubMed Web of Science ®Google Scholar
• Gajendrarao, P., Krishnamoorthy, N., Kassem, H. S., Moharem-Elgamal, S., Cecchi, F., Olivotto, I., & Yacoub, M. H. (2013). Molecular modeling of disease causing mutations in domain C1 of cMyBP-C. PLoS ONE, 8, e59206.10.1371/journal.pone.0059206
   PubMed Web of Science ®Google Scholar
• Gajendrarao, P., Krishnamoorthy, N., Selvaraj, S., Girolami, F., Cecchi, F., Olivotto, I., & Yacoub, M. H. (2015). An Investigation of the molecular mechanism of double cMyBP-C mutation in a patient with end-stage hypertrophic cardiomyopathy. Journal of Cardiovascular Translational Research, 8, 232–243.10.1007/s12265-015-9624-6
   PubMed Web of Science ®Google Scholar
• Gautel, M., Zuffardi, O., Freiburg, A., & Labeit, S. (1995). Phosphorylation switches specific for the cardiac isoform of myosin binding protein-C: A modulator of cardiac contraction? EMBO Journal, 14, 1952–1960.
   PubMed Web of Science ®Google Scholar
• Govada, L., Carpenter, L., da Fonseca, P. C., Helliwell, J. R., Rizkallah, P., Flashman, E., … Squire, J. M. (2008). Crystal structure of the C1 domain of cardiac myosin binding protein-C: Implications for hypertrophic cardiomyopathy. Journal of Molecular Biology, 378, 387–397.10.1016/j.jmb.2008.02.044
   PubMed Web of Science ®Google Scholar
• Gruen, M., & Gautel, M. (1999). 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, 286, 933–949.10.1006/jmbi.1998.2522
   PubMed Web of Science ®Google Scholar
• Harris, S. P., Lyons, R. G., & Bezold, K. L. (2011). In the thick of it: HCM-causing mutations in myosin binding proteins of the thick filament. Circulation Research, 108, 751–764.10.1161/CIRCRESAHA.110.231670
   PubMed Web of Science ®Google Scholar
• Harris, S. P., Rostkova, E., Gautel, M., & Moss, R. L. (2004). Binding of myosin binding protein-C to myosin subfragment S2 affects contractility independent of a tether mechanism. Circulation Research, 95, 930–936.10.1161/01.RES.0000147312.02673.56
   PubMed Web of Science ®Google Scholar
• Hess, B., Bekker, H., Berendsen, H. J. C., & Fraaije, J. G. E. M. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18, 1463–1472.10.1002/(ISSN)1096-987X
   Web of Science ®Google Scholar
• Hess, B., Kutzner, C., van der Spoel, D., & Lindahl, E. (2008). GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. Journal of Chemical Theory and Computation, 4, 435–447.10.1021/ct700301q
   PubMed Web of Science ®Google Scholar
• Howarth, J. W., Ramisetti, S., Nolan, K., Sadayappan, S., & Rosevear, P. R. (2012). Structural insight into unique cardiac myosin-binding protein-C motif: A partially folded domain. Journal of Biological Chemistry, 287, 8254–8262.10.1074/jbc.M111.309591
   PubMed Web of Science ®Google Scholar
• Isralewitz, B., Gao, M., & Schulten, K. (2001). Steered molecular dynamics and mechanical functions of proteins. Current Opinion in Structural Biology, 11, 224–230.10.1016/S0959-440X(00)00194-9
   PubMed Web of Science ®Google Scholar
• Krishnamoorthy, N., Yacoub, M. H., & Yaliraki, S. N. (2011). A computational modeling approach for enhancing self-assembly and biofunctionalisation of collagen biomimetic peptides. Biomaterials, 32, 7275–7285.10.1016/j.biomaterials.2011.06.074
   PubMed Web of Science ®Google Scholar
• Li, M. S., & Mai, B. K. (2012). Steered molecular dynamics – A promising tool for drug design. Current Bioinformatics, 7, 342–351.
   Web of Science ®Google Scholar
• Luther, P. K., Winkler, H., Taylor, K., Zoghbi, M. E., Craig, R., Padron, R., Squire, J. M., & Liu, J. (2011). Direct visualization of myosin-binding protein C bridging myosin and actin filaments in intact muscle. Proceedings of the National Academy of Sciences, 108, 11423–11428.10.1073/pnas.1103216108
   PubMed Web of Science ®Google Scholar
• Maron, B. J., Ommen, S. R., Semsarian, C., Spirito, P., Olivotto, I., & Maron, M. S. (2014). Hypertrophic Cardiomyopathy. Journal of the American College of Cardiology, 64, 83–99.10.1016/j.jacc.2014.05.003
   PubMed Web of Science ®Google Scholar
• Maron, B. J., Shirani, J., Poliac, L. C., Mathenge, R., Roberts, W. C., & Mueller, F. O. (1996). Sudden death in young competitive athletes. JAMA, 276, 199–204.10.1001/jama.1996.03540030033028
   PubMed Web of Science ®Google Scholar
• Miyamoto, S., & Kollman, P. A. (1992). Settle: An analytical version of the SHAKE and RATTLE algorithm for rigid water models. Journal of Computational Chemistry, 13, 952–962.10.1002/(ISSN)1096-987X
   Web of Science ®Google Scholar
• Offer, G., Moos, C., & Starr, R. (1973). A new protein of the thick filaments of vertebrate skeletal myofibrils. Journal of Molecular Biology, 74, 653–676.10.1016/0022-2836(73)90055-7
   PubMed Web of Science ®Google Scholar
• Olivotto, I., Cecchi, F., Poggesi, C., & Yacoub, M. H. (2012). Patterns of disease progression in hypertrophic cardiomyopathy: An individualized approach to clinical staging. Circulation: Heart Failure, 5, 535–546.10.1161/CIRCHEARTFAILURE.112.967026
   PubMed Web of Science ®Google Scholar
• Razumova, M. V., Shaffer, J. F., Tu, A. Y., Flint, G. V., Regnier, M., & Harris, S. P. (2006). 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, 281, 35846–35854.10.1074/jbc.M606949200
   PubMed Web of Science ®Google Scholar
• Sadayappan, S., & de Tombe, P. P. (2012). Cardiac myosin binding protein-C: Redefining its structure and function. Biophysical Reviews, 4, 93–106.10.1007/s12551-012-0067-x
   PubMedGoogle Scholar
• Sadayappan, S., Gulick, J., Osinska, H., Martin, L. A., Hahn, H. S., Dorn, G. W., … Robbins, J. (2005). Cardiac myosin-binding protein-C phosphorylation and cardiac function. Circulation Research, 97, 1156–1163.10.1161/01.RES.0000190605.79013.4d
   PubMed Web of Science ®Google Scholar
• Sadayappan, S., Osinska, H., Klevitsky, R., Lorenz, J. N., Sargent, M., Molkentin, J. D., … Robbins, J. (2006). Cardiac myosin binding protein c phosphorylation is cardioprotective. Proceedings of the National Academy of Sciences, 103, 16918–16923.10.1073/pnas.0607069103
   PubMed Web of Science ®Google Scholar
• Shen, M., Guan, J., Xu, L., Yu, Y., He, J., Jones, G. W., & Song, Y. (2012). Steered molecular dynamics simulations on the binding of the appendant structure and helix-β2 in domain-swapped human cystatin C dimer. Journal of Biomolecular Structure and Dynamics, 30, 652–661.10.1080/07391102.2012.689698
   PubMed Web of Science ®Google Scholar
• Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26, 1701–1718.10.1002/(ISSN)1096-987X
   PubMed Web of Science ®Google Scholar
• Weisberg, A., & Winegrad, S. (1996). Alteration of myosin cross bridges by phosphorylation of myosin-binding protein C in cardiac muscle. Proceedings of the National Academy of Sciences, 93, 8999–9003.10.1073/pnas.93.17.8999
   PubMed Web of Science ®Google Scholar
• Winegrad, S. (1999). Cardiac myosin binding protein C. Circulation Research, 84, 1117–1126.10.1161/01.RES.84.10.1117
   PubMed Web of Science ®Google Scholar
• Winegrad, S. (2000). Myosin binding protein C, a potential regulator of cardiac contractility. Circulation Research, 86, 6–7.10.1161/01.RES.86.1.6
   PubMed Web of Science ®Google Scholar
• Winegrad, S. (2001). Gene mutation in cardiac myosin binding protein C. Journal of Molecular and Cellular Cardiology, 33, 1555–1559.10.1006/jmcc.2001.1438
   PubMed Web of Science ®Google Scholar
• Winegrad, S. (2003). Myosin-binding protein C (MyBP-C) in cardiac muscle and contractility. Advances in Experimental Medicine and Biology, 538, 31–41.10.1007/978-1-4419-9029-7
   PubMed Web of Science ®Google Scholar
• Xu, L., Hasin, N., Shen, M., He, J., Xue, Y., Zhou, X., … Jones, G. W. (2013). Using steered molecular dynamics to predict and assess Hsp70 substrate-binding domain mutants that alter prion propagation. PLoS Computational Biology, 9, e1002896.10.1371/journal.pcbi.1002896
   PubMed Web of Science ®Google Scholar
• Yacoub, M. H., Olivotto, I., & Cecchi, F. (2007). ‘End–stage’ hypertrophic cardiomyopathy: From mystery to model. Nature Clinical Practice Cardiovascular Medicine, 4, 232–233.10.1038/ncpcardio0859
   PubMedGoogle Scholar