About this Journal Submit a Manuscript Table of Contents
Biochemistry Research International
Volume 2012 (2012), Article ID 824068, 11 pages
http://dx.doi.org/10.1155/2012/824068
Research Article

Cardiomyopathy-Related Mutations in Cardiac Troponin C, L29Q and G159D, Have Divergent Effects on Rat Cardiac Myofiber Contractile Dynamics

Department of Veterinary and Comparative Anatomy, Pharmacology, and Physiology (VCAPP), Washington State University, Pullman, WA 99164-6520, USA

Received 14 May 2012; Revised 6 July 2012; Accepted 8 August 2012

Academic Editor: Danuta Szczesna-Cordary

Copyright © 2012 Sampath K. Gollapudi and Murali Chandra. 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. B. Hoffmann, H. Schmidt-Traub, A. Perrot, K. J. Osterziel, and R. Gessner, “First mutation in cardiac troponin C, L29Q, in a patient with hypertrophic cardiomyopathy,” Human Mutation, vol. 17, no. 6, p. 524, 2001. View at Scopus
  2. A. P. Landstrom, M. S. Parvatiyar, J. R. Pinto et al., “Molecular and functional characterization of novel hypertrophic cardiomyopathy susceptibility mutations in TNNC1-encoded troponin C,” Journal of Molecular and Cellular Cardiology, vol. 45, no. 2, pp. 281–288, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. W. K. Chung, C. Kitner, and B. J. Maron, “Novel frameshift mutation in Troponin C (TNNC1) associated with hypertrophic cardiomyopathy and sudden death,” Cardiology in the Young, vol. 21, no. 3, pp. 345–348, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. C. C. Lim, H. Yang, M. Yang et al., “A novel mutant cardiac troponin C disrupts molecular motions critical for calcium binding affinity and cardiomyocyte contractility,” Biophysical Journal, vol. 94, no. 9, pp. 3577–3589, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Mogensen, R. T. Murphy, T. Shaw et al., “Severe disease expression of cardiac troponin C and T mutations in patients with idiopathic dilated cardiomyopathy,” Journal of the American College of Cardiology, vol. 44, no. 10, pp. 2033–2040, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. R. E. Hershberger, N. Norton, A. Morales, D. Li, J. D. Siegfried, and J. Gonzalez-Quintana, “Coding sequence rare variants identified in MYBPC3, MYH6, TPM1, TNNC1, and TNNI3 from 312 patients with familial or idiopathic dilated cardiomyopathy,” Circulation, vol. 3, no. 2, pp. 155–161, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. K. B. Campbell, M. V. Razumova, R. D. Kirkpatrick, and B. K. Slinker, “Nonlinear myofilament regulatory processes affect frequency-dependent muscle fiber stiffness,” Biophysical Journal, vol. 81, no. 4, pp. 2278–2296, 2001. View at Scopus
  8. K. B. Campbell, M. V. Razumova, R. D. Kirkpatrick, and B. K. Slinker, “Myofilament kinetics in isometric twitch dynamics,” Annals of Biomedical Engineering, vol. 29, no. 5, pp. 384–405, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. T. E. Gillis, C. R. Marshall, and G. F. Tibbits, “Functional and evolutionary relationships of troponin C,” Physiological Genomics, vol. 32, no. 1, pp. 16–27, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. B. Liang, F. Chung, Y. Qu et al., “Familial hypertrophic cardiomyopathy-related cardiac troponin C mutation L29Q affects Ca2+ binding and myofilament contractility,” Physiological Genomics, vol. 33, no. 2, pp. 257–266, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Schmidtmann, C. Lindow, S. Villard et al., “Cardiac troponin C-L29Q, related to hypertrophic cardiomyopathy, hinders the transduction of the protein kinase A dependent phosphorylation signal from cardiac troponin I to C,” FEBS Journal, vol. 272, no. 23, pp. 6087–6097, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. J. D. Potter, Z. Sheng, B. S. Pan, and J. Zhao, “A direct regulatory role for troponin T and a dual role for troponin C in the Ca2+ regulation of muscle contraction,” Journal of Biological Chemistry, vol. 270, no. 6, pp. 2557–2562, 1995. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Takeda, A. Yamashita, K. Maeda, and Y. Maéda, “Structure of the core domain of human cardiac troponin in the Ca2+-saturated form,” Nature, vol. 424, no. 6944, pp. 35–41, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. D. Dweck, N. Hus, and J. D. Potter, “Challenging current paradigms related to cardiomyopathies: are changes in the Ca2+ sensitivity of myofilaments containing cardiac troponin C mutations (G159D and L29Q) good predictors of the phenotypic outcomes?” Journal of Biological Chemistry, vol. 283, no. 48, pp. 33119–33128, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Neulen, R. Stehle, and G. Pfitzer, “The cardiac troponin C mutation Leu29Gln found in a patient with hypertrophic cardiomyopathy does not alter contractile parameters in skinned murine myocardium,” Basic Research in Cardiology, vol. 104, no. 6, pp. 751–760, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. E. C. Dyer, A. M. Jacques, A. C. Hoskins et al., “Functional analysis of a unique troponin c mutation, gly159asp, that causes Familial dilated cardiomyopathy, studied in explanted heart muscle,” Circulation, vol. 2, no. 5, pp. 456–464, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Mirza, S. Marston, R. Willott et al., “Dilated cardiomyopathy mutations in three thin filament regulatory proteins result in a common functional phenotype,” Journal of Biological Chemistry, vol. 280, no. 31, pp. 28498–28506, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. P. Robinson, P. J. Griffiths, H. Watkins, and C. S. Redwood, “Dilated and hypertrophic cardiomyopathy mutations in troponin and α-tropomyosin have opposing effects on the calcium affinity of cardiac thin filaments,” Circulation Research, vol. 101, no. 12, pp. 1266–1273, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. B. J. Biesiadecki, T. Kobayashi, J. S. Walker, R. J. Solaro, and P. P. de Tombe, “The troponin C G159D mutation blunts myofilament desensitization induced by troponin I Ser23/24 phosphorylation,” Circulation Research, vol. 100, no. 10, pp. 1486–1493, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. L. C. Preston, C. C. Ashley, and C. S. Redwood, “DCM troponin C mutant Gly159Asp blunts the response to troponin phosphorylation,” Biochemical and Biophysical Research Communications, vol. 360, no. 1, pp. 27–32, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Chandra, M. L. Tschirgi, S. J. Ford, B. K. Slinker, and K. B. Campbell, “Interaction between myosin heavy chain and troponin isoforms modulate cardiac myofiber contractile dynamics,” American Journal of Physiology, vol. 293, no. 4, pp. R1595–R1607, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Chandra, M. L. Tschirgi, I. Rajapakse, and K. B. Campbell, “Troponin T modulates sarcomere length-dependent recruitment of cross-bridges in cardiac muscle,” Biophysical Journal, vol. 90, no. 8, pp. 2867–2876, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Chandra, V. L. M. Rundell, J. C. Tardiff, L. A. Leinwand, P. P. De Tombe, and R. J. Solaro, “Ca2+ activation of myofilaments from transgenic mouse hearts expressing R92Q mutant cardiac troponin T,” American Journal of Physiology, vol. 280, no. 2, pp. H705–H713, 2001. View at Scopus
  24. X. Guo, J. Wattanapermpool, K. A. Palmiter, A. M. Murphy, and R. J. Solaro, “Mutagenesis of cardiac troponin I. Role of the unique NH2-terminal peptide in myofilament activation,” Journal of Biological Chemistry, vol. 269, no. 21, pp. 15210–15216, 1994. View at Scopus
  25. B. S. Pan and R. G. Johnson, “Interaction of cardiotonic thiadiazinone derivatives with cardiac troponin C,” Journal of Biological Chemistry, vol. 271, no. 2, pp. 817–823, 1996. View at Publisher · View at Google Scholar · View at Scopus
  26. D. E. Montgomery, J. C. Tardiff, and M. Chandra, “Cardiac troponin T mutations: correlation between the type of mutation and the nature of myofilament dysfunction in transgenic mice,” Journal of Physiology, vol. 536, no. 2, pp. 583–592, 2001. View at Publisher · View at Google Scholar · View at Scopus
  27. J. C. Tardiff, S. M. Factor, B. D. Tompkins et al., “A truncated cardiac troponin T molecule in transgenic mice suggests multiple cellular mechanisms for familial hypertrophic cardiomyopathy,” Journal of Clinical Investigation, vol. 101, no. 12, pp. 2800–2811, 1998. View at Scopus
  28. M. Chandra, M. L. Tschirgi, and J. C. Tardiff, “Increase in tension-dependent ATP consumption induced by cardiac troponin T mutation,” American Journal of Physiology, vol. 289, no. 5, pp. H2112–H2119, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Chandra, D. E. Montgomery, J. J. Kim, and R. J. Solaro, “The N-terminal region of troponin T is essential for the maximal activation of rat cardiac myofilaments,” Journal of Molecular and Cellular Cardiology, vol. 31, no. 4, pp. 867–880, 1999. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Chandra, J. J. Kim, and R. J. Solaro, “An improved method for exchanging troponin subunits in detergent skinned rat cardiac fiber bundles,” Biochemical and Biophysical Research Communications, vol. 263, no. 1, pp. 219–223, 1999. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Fabiato and F. Fabiato, “Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells,” Journal de Physiologie, vol. 75, no. 5, pp. 463–505, 1979. View at Scopus
  32. R. L. Lieber, Y. Yeh, and R. J. Baskin, “Sarcomere length determination using laser diffraction. Effect of beam and fiber diameter,” Biophysical Journal, vol. 45, no. 5, pp. 1007–1016, 1984. View at Scopus
  33. P. P. de Tombe and G. J. M. Stienen, “Protein kinase A does not alter economy of force maintenance in skinned rat cardiac trabeculae,” Circulation Research, vol. 76, no. 5, pp. 734–741, 1995. View at Scopus
  34. G. J. M. Stienen, G. Zaremba, and G. Elzinga, “ATP utilization for calcium uptake and force production in skinned muscle fibres of Xenopus laevis,” Journal of Physiology, vol. 482, no. 1, pp. 109–122, 1995. View at Scopus
  35. K. B. Campbell, M. Chandra, R. D. Kirkpatrick, B. K. Slinker, and W. C. Hunter, “Interpreting cardiac muscle force-length dynamics using a novel functional model,” American Journal of Physiology, vol. 286, no. 4, pp. H1535–H1545, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. K. Campbell, “Rate constant of muscle force redevelopment reflects cooperative activation as well as cross-bridge kinetics,” Biophysical Journal, vol. 72, no. 1, pp. 254–262, 1997. View at Scopus
  37. M. V. Vinogradova, D. B. Stone, G. G. Malanina et al., “Ca2+-regulated structural changes in troponin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 14, pp. 5038–5043, 2005. View at Publisher · View at Google Scholar · View at Scopus