Malignant familial hypertrophic cardiomyopathy D166V mutation in the ventricular myosin regulatory light chain causes profound effects in skinned and intact papillary muscle fibers from transgenic mice

FASEB Journal

Volumn 23, Issue 3, 2009, Pages 855-865

  Glenn L Kerrick, W ^a   Kazmierczak, Katarzyna ^b   Xu, Yuanyuan ^a   Wang, Yingcai ^b   Szczesna Cordary, Danuta ^b  

^a Department of Physiology and Biophysics ^*  (United States)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

ATPase pCa dependence; Calcium and force transients; Cross bridge dissociation rate; Energy cost; Phosphorylation

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ASPARTIC ACID; CALCIUM; VALINE; VENTRICULAR MYOSIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; DISSOCIATION; ENERGY; FAMILIAL HYPERTROPHIC CARDIOMYOPATHY; GENE MUTATION; HEART MUSCLE; HEART PAPILLARY MUSCLE; HISTOPATHOLOGY; KINETICS; LIGHT CHAIN; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN PHOSPHORYLATION; TRANSGENIC MOUSE;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CALCIUM; CARDIOMYOPATHY, HYPERTROPHIC, FAMILIAL; ENERGY METABOLISM; GENE EXPRESSION REGULATION; HUMANS; MICE; MICE, TRANSGENIC; MODELS, MOLECULAR; MUTATION; MYOCARDIAL CONTRACTION; MYOCARDIUM; MYOSIN LIGHT CHAINS; MYOSINS; PAPILLARY MUSCLES; PHOSPHORYLATION; PROTEIN CONFORMATION;

MUS; MUS MUSCULUS;

EID: 61449250645     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-118182     Document Type: Article

References (49)

1. Poetter, K., Jiang, H., Hassanzadeh, S., Master, S. R., Chang, A., Dalakas, M. C., Rayment, I., Sellers, J. R., Fananapazir, L., and Epstein, N. D. (1996) Mutations in either the essential or regulatory light chains of myosin are associated with a rare myopathy in human heart and skeletal muscle. Nat. Genet. 13, 63-69
2. Andersen, P. S., Havndrup, O., Bundgaard, H., Moolman-Smook, J. C., Larsen, L. A., Mogensen, J., Brink, P. A., Borglum, A. D., Corfield, V. A., Kjeldsen, K., Vuust, J., and Christiansen, M. (2001) Myosin light chain mutations in familial hypertrophic cardiomyopathy: phenotypic presentation and frequency in Danish and South African populations. J. Med. Genet. 38, E43
3. Kabaeva, Z. T. (2002) Genetic analysis in hypertrophic cardiomyopathy: missense mutations in the ventricular myosin regulatory light chain gene. Ph.D. thesis, The Humboldt University of Berlin
4. Kabaeva, Z. T., Perrot, A., Wolter, B., Dietz, R., Cardim, N., Correia, J. M., Schulte, H. D., Aldashev, A. A., Mirrakhimov, M. M., and Osterziel, K. J. (2002) Systematic analysis of the regulatory and essential myosin light chain genes: genetic variants and mutations in hypertrophic cardiomyopathy. Eur. J. Hum. Genet. 10, 741-748
5. Richard, P., Charron, P., Carrier, L., Ledeuil, C., Cheav, T., Pichereau, C., Benaiche, A., Isnard, R., Dubourg, O., Burban, M., Gueffet, J.-P., Millaire, A., Desnos, M., Schwartz, K., Hainque, B., Komajda, M., for the EUROGENE Heart Failure Project (2003) Hypertrophic cardiomyopathy: distribution of disease genes, spectrum of mutations, and implications for a molecular diagnosis strategy. Circulation 107, 2227-2232
6. Morner, S., Richard, P., Kazzam, E., Hellman, U., Hainque, B., Schwartz, K., and Waldenstrom, A. (2003) Identification of the genotypes causing hypertrophic cardiomyopathy in northern Sweden. J. Mol. Cell. Cardiol. 35, 841-849
7. Hougs, L., Havndrup, O., Bundgaard, H., Kober, L., Vuust, J., Larsen, L. A., Christiansen, M., and Andersen, P. S. (2005) One third of Danish hypertrophic cardiomyopathy patients have mutations in MYH7 rod region. Eur. J. Hum. Genet. 13, 161-165
8. Seidman, C. E., and Seidman, J. G. (1998) Molecular genetic studies of familial hypertrophic cardiomyopathy. Basic Res. Cardiol. 93, 13-16
9. Seidman, J. G., and Seidman, C. (2001) The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms. Cell 104, 557-567
10. Maron, B. J., Olivotto, I., Spirito, P., Casey, S. A., Bellone, P., Gohman, T. E., Graham, K. J., Burton, D. A., and Cecchi, F. (2000) Epidemiology of hypertrophic cardiomyopathy-related death: revisited in a large non-referral-based patient population. Circulation 102, 858 -864
11. Maron, B. J. (2002) Hypertrophic cardiomyopathy: a systematic review. JAMA 287, 1308 -1320
12. Szczesna, D. (2003) Regulatory light chains of striated muscle myosin: structure, function and malfunction. Curr. Drug Targets Cardiovasc. Haematol. Disord. 3, 187-197
13. Alcalai, R., Seidman, J. G., and Seidman, C. E. (2008) Genetic basis of hypertrophic cardiomyopathy: from bench to the clinics. J. Cardiovasc. Electrophysiol. 19, 104-110
14. 2+ binding, and phosphorylation. J. Biol. Chem. 276, 7086 -7092
15. 2+ binding of human cardiac myosin regulatory light chain affect cardiac muscle contraction. J. Biol. Chem. 279, 3535-3542
16. Richard, P., Charron, P., Carrier, L., Ledeuil, C., Cheav, T., Pichereau, C., Benaiche, A., Isnard, R., Dubourg, O., Burban, M., Gueffet, J.-P., Millaire, A., Desnos, M., Schwartz, K., Hainque, B., and Komajda, M. (2004) Correction (Hypertro- phic cardiomyopathy: distribution of disease genes, spectrum of mutations, and implications for a molecular diagnosis strategy). Circulation 109, 3258
17. 2+ and force transients in myosin RLC transgenic mouse fibers expressing malignant and benign FHC mutations. J. Mol. Biol. 361, 286-299
18. Szczesna-Cordary, D., Guzman, G., Zhao, J., Hernandez, O., Wei, J., and Diaz-Perez, Z. (2005) The E22K mutation of myosin RLC that causes familial hypertrophic cardiomyopathy increases calcium sensitivity offorce and ATPase in transgenic mice. J. Cell Sci. 118, 3675-3683
19. Szczesna-Cordary, D., Jones, M., Moore, J. R., Watt, J., Kerrick, W. G. L., Xu, Y., Wang, Y., Wagg, C., and Lopaschuk, G. D. (2007) Myosin regulatory light chain E22K mutation results in decreased cardiac intracellular calcium and force transients. FASEB J. 21, 3974-3985
20. Davis, J. S., Hassanzadeh, S., Winitsky, S., Lin, H., Satorius, C., Vemuri, R., Aletras, A. H., Wen, H., and Epstein, N. D. (2001) The overall pattern of cardiac contraction depends on a spatial gradient of myosin regulatory light chain phosphorylation. Cell 107, 631-641
21. 2+ -sensitivity, phosphoryla- tion kinetics and proteolytic susceptibility of troponin. J. Mol. Cell. Cardiol. 39, 754-765
22. Guth, K., and Wojciechowski, R. (1986) Perfusion cuvette for the simultaneous measurement of mechanical, optical and energetic parameters of skinned muscle fibres. Pflügers Arch. 407, 552-557
23. 2+ activation of force and fiber ATPase. J. Appl. Physiol. 88, 180-185
24. Wang, Y., Xu, Y., Guth, K., and Kerrick, W. G. (1999) Troponin C regulates the rate constant for the dissociation of force- generating myosin cross-bridges in cardiac muscle. J. Muscle Res. Cell Motil. 20, 645-653
25. 2+] signals from calcium-indicator dyes. News Physiol. Sci. 15, 19-26
26. Sanbe, A., Nelson, D., Gulick, J., Setser, E., Osinska, H., Wang, X., Hewett, T. E., Klevitsky, R., Hayes, E., Warshaw, D. M., and Robbins, J. (2000) In vivo analysis of an essential myosin light chain mutation linked to familial hypertrophic cardiomyopathy. Circ. Res. 87, 296 -302
27. Huxley, A. F. (1957) A hypothesis for the mechanism of contraction of muscle. Prog. Biophys. Biophys. Chem. 7, 255-318
28. Brenner, B. (1988) Effect of Ca2+ on cross-bridge turnover kinetics in skinned single rabbit psoas fibers: implications for regulation of muscle contraction. Proc. Natl. Acad. Sci. U. S. A. 85, 3265-3269
29. Huxley, A. F. (2000) Cross-bridge action: present views, prospects, and unknowns. J. Biomech. 33, 1189 -1195
30. Prakash, Y. S., Cody, M. J., Housmans, P. R., Hannon, J. D., and Sieck, G. C. (1999) Comparison of cross-bridge cycling kinetics in neonatal vs. adult rat ventricular muscle. J. Muscle Res. Cell Motil. 20, 717-723
31. Kerrick, W. G., and Xu, Y. (2004) Inorganic phosphate affects the pCa-force relationship more than the pCa-ATPase by increasing the rate of dissociation of force generating cross- bridges in skinned fibers from both EDL and soleus muscles of the rat. J. Muscle Res. Cell Motil. 25, 107-117
32. Wen, Y., Pinto, J. R., Gomes, A. V., Xu, Y., Wang, Y., Wang, Y., Potter, J. D., and Kerrick, W. G. (2008) Functional consequences of the human cardiac troponin I hypertrophic cardio- myopathy mutation R145G in transgenic mice. J. Biol. Chem. 283, 20484-20494
33. Ferenczi, M. A., Homsher, E., and Trentham, D. R. (1984) The kinetics of magnesium adenosine triphosphate cleavage in skinned muscle fibres of the rabbit. J. Physiol. 352, 575-599
34. Rayment, I., Rypniewski, W. R., Schmidt-Base, K., Smith, R., Tomchick, D. R., Benning, M. M., Winkelmann, D. A., Wesen- berg, G., and Holden, H. M. (1993) Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261, 50-58
35. Geeves, M. A., and Holmes, K. C. (2005) The molecular mechanism of muscle contraction. Adv. Protein Chem. 71, 161-193
36. Omote, H., Figler, R. A., Polar, M. K., and Al-Shawi, M. K. (2004) Improved energy coupling of human P-glycoprotein by the glycine 185 to valine mutation. Biochemistry 43, 3917-3928
37. Doolittle, R. F., and Pandi, L. (2007) Probing the β-chain hole of fibrinogen with synthetic peptides that differ at their amino termini. Biochemistry 46, 10033-10038
38. Davis, J. S., Hassanzadeh, S., Winitsky, S., Wen, H., Aletras, A., and Epstein, N. D. (2002) A gradient of myosin regulatory light-chain phosphorylation across the ventricular wall supports cardiac torsion. Cold Spring Harb. Symp. Quant. Biol. 67, 345-352
39. Stelzer, J. E., Patel, J. R., and Moss, R. L. (2006) Acceleration of stretch activation in murine myocardium due to phosphoryla- tion of myosin regulatory light chain. J. Gen. Physiol. 128, 261-272
40. Sweeney, H. L., Bowman, B. F., and Stull, J. T. (1993) Myosin light chain phosphorylation in vertebrate striated muscle: regulation and function. Am. J. Physiol. 264, C1085-C1095
41. 2+ sensitivity of skeletal muscle contraction. J. Appl. Physiol. 92, 1661-1670
42. Metzger, J. M., Greaser, M. L., and Moss, R. L. (1989) Variations in cross-bridge attachment rate and tension with phosphorylation of myosin in mammalian skinned skeletal muscle fibers: implications for twitch potentiation in intact muscle. J. Gen. Physiol. 93, 855-883
43. Sweeney, H. L., and Stull, J. T. (1990) Alteration of cross-bridge kinetics by myosin light chain phosphorylation in rabbit skeletal muscle: implications for regulation of actin-myosin interaction. Proc. Natl. Acad. Sci. U. S. A. 87, 414-418
44. 2+ sensitivities of isometric tension, stiffness, and velocity of shortening in skinned skeletal muscle fibers. J. Gen. Physiol. 95, 477-498
45. Dias, F. A. L., Walker, L. A., Arteaga, G. M., Walker, J. S., Vijayan, K., Pena, J. R., Ke, Y., Fogaca, R. T. H., Sanbe, A., Robbins, J., and Wolska, B. M. (2006) The effect of myosin regulatory light chain phosphorylation on the frequency-dependent regulation of cardiac function. J. Mol. Cell. Cardiol. 41, 330-339
46. Geeves, M. A., and Lehrer, S. S. (2002) Cooperativity in the Ca2+ regulation of muscle contraction. Results Probl. Cell Differ. 36, 111-132
47. McKillop, D. F., and Geeves, M. A. (1993) Regulation of the interaction between actin and myosin subfragment 1: evidence for three states of the thin filament. Biophys. J. 65, 693-701
48. Robinson, J. M., Wang, Y., Kerrick, W. G., Kawai, R., and Cheung, H. C. (2002) Activation of striated muscle: nearest- neighbor regulatory-unit and cross-bridge influence on myofilament kinetics. J. Mol. Biol. 322, 1065-1088
49. 2+-specific regulatory sites in skinned rabbit psoas fibers. J. Biol. Chem. 262, 13627-13635