Increased susceptibility to isoproterenol-induced cardiac hypertrophy and impaired weight gain in mice lacking the histidine-rich calcium-binding protein

Molecular and Cellular Biology

Volumn 26, Issue 24, 2006, Pages 9315-9326

  Jaehnig, Eric J ^a   Heidt, Analeah B ^a   Greene, Stephanie B ^a   Cornelissen, Ivo ^a   Black, Brian L ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM BINDING PROTEIN; HISTIDINE RICH CALCIUM BINDING PROTEIN; ISOPRENALINE; PROTEIN; REGULATOR PROTEIN; RYANODINE RECEPTOR; TRIADIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CALCIUM BINDING; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CONTROLLED STUDY; DISEASE PREDISPOSITION; ENVIRONMENTAL FACTOR; FUNCTIONAL PROTEOMICS; GENE; GENE MUTATION; HEART FAILURE; HEART VENTRICLE HYPERTROPHY; HEREDITY; HRC GENE; IN VIVO STUDY; KNOCKOUT MOUSE; MOUSE; MUSCLE TISSUE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SARCOPLASMIC RETICULUM; SKELETAL MUSCLE; WEIGHT GAIN; WILD TYPE;

ANIMALS; CALCIUM; CALCIUM-BINDING PROTEINS; CARDIOMEGALY; GENETIC PREDISPOSITION TO DISEASE; ISOPROTERENOL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE PROTEINS; MUSCLE, SKELETAL; WEIGHT GAIN;

EID: 33845405157     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00482-06     Document Type: Article

References (68)

1. Allen, D. L., B. C. Harrison, A. Maass, M. L. Bell, W. C. Byrnes, and L. A. Leinwand. 2001. Cardiac and skeletal muscle adaptations to voluntary wheel running in the mouse. J Appl. Physiol. 90:1900-1908.
2. Anderson, J. P., E. Dodou, A. B. Heidt, S. J. De Val, E. J. Jaehnig, S. B. Greene, E. N. Olson, and B. L. Black. 2004. HRC is a direct transcriptional target of MEF2 during cardiac, skeletal, and arterial smooth muscle development in vivo. Mol. Cell. Biol. 24:3757-3768.
3. Arai, M., H. Matsui, and M. Periasamy. 1994. Sarcoplasmic reticulum gene expression in cardiac hypertrophy and heart failure. Circ. Res. 74:555-564.
4. Ashrafian, H., C. Redwood, E. Blair, and H. Watkins. 2003. Hypertrophic cardiomyopathy: a paradigm for myocardial energy depletion. Trends Genet. 19:263-268.
5. Balke, C. W., and S. R. Shorofsky. 1998. Alterations in calcium handling in cardiac hypertrophy and heart failure. Cardiovasc. Res. 37:290-299.
6. Beard, N. A., D. R. Laver, and A. F. Dulhunty. 2004. Calsequestrin and the calcium release channel of skeletal and cardiac muscle. Prog. Biophys. Mol. Biol. 85:33-69.
7. Bers, D. M. 2002. Cardiac excitation-contraction coupling. Nature 415:198-205.
8. Bers, D. M. 2004. Macromolecular complexes regulating cardiac ryanodine receptor function. J. Mol. Cell Cardiol. 37:417-429.
9. Bueno, O. F., B. J. Wilkins, K. M. Tymitz, B. J. Glascock, T. F. Kimball, J. N. Lorenz, and J. D. Molkentin. 2002. Impaired cardiac hypertrophic response in calcineurin Abeta-deficient mice. Proc. Natl. Acad. Sci. USA 99:4586-4591.
10. Campbell, K. P., and A. E. Shamoo. 1980. Chloride-induced release of actively loaded calcium from light and heavy sarcoplasmic reticulum vesicles. J. Membr. Biol. 54:73-80.
11. Carvajal, K., and R. Moreno-Sanchez. 2003. Heart metabolic disturbances in cardiovascular diseases. Arch. Med. Res. 34:89-99.
12. Chang, S., T. A. McKinsey, C. L. Zhang, J. A. Richardson, J. A. Hill, and E. N. Olson. 2004. Histone deacetylases 5 and 9 govern responsiveness of the heart to a subset of stress signals and play redundant roles in heart development. Mol. Cell. Biol. 24:8467-8476.
13. Cheah, S. S., and R. R. Behringer. 2000. Gene-targeting strategies. Methods Mol. Biol. 136:455-463.
14. Coronado, R., J. Morrissette, M. Sukhareva, and D. M. Vaughan. 1994. Structure and function of ryanodine receptors. Am. J. Physiol. 266:C1485-C1504.
15. Damiani, E., and A. Margreth. 1991. Subcellular fractionation to junctional sarcoplasmic reticulum and biochemical characterization of 170 kDa Ca(2+)- and low-density-lipoprotein-binding protein in rabbit skeletal muscle. Biochem. J. 277:825-832.
16. Damiani, E., E. Picello, L. Saggin, and A. Margreth. 1995. Identification of triadin and of histidine-rich Ca(2+)-binding protein as substrates of 60 kDa calmodulin-dependent protein kinase in junctional terminal cisternae of sarcoplasmic reticulum of rabbit fast muscle. Biochem. Biophys. Res. Commun. 209:457-465.
17. Damiani, E., G. Tobaldin, E. Bortoloso, and A. Margreth. 1997. Functional behaviour of the ryanodine receptor/Ca(2+)-release channel in vesiculated derivatives of the junctional membrane of terminal cisternae of rabbit fast muscle sarcoplasmic reticulum. Cell Calcium 22:129-150.
18. Fan, G. C., K. N. Gregory, W. Zhao, W. J. Park, and E. G. Kranias. 2004. Regulation of myocardial function by histidine-rich, calcium-binding protein. Am. J. Physiol. Heart Circ. Physiol. 287:H1705-H1711.
19. Forbes, M. S., L. A. Hawkey, S. K. Jirge, and N. Sperelakis. 1985. The sarcoplasmic reticulum of mouse heart: its divisions, configurations, and distribution. J. Ultrastruct. Res. 93:1-16.
20. Frey, N., T. Barrientos, J. M. Shelton, D. Frank, H. Rutten, D. Gehring, C. Kuhn, M. Lutz, B. Rothermel, R. Bassel-Duby, J. A. Richardson, H. A. Katus, J. A. Hill, and E. N. Olson. 2004. Mice lacking calsarcin-1 are sensitized to calcineurin signaling and show accelerated cardiomyopathy in response to pathological biomechanical stress. Nat. Med. 10:1336-1343.
21. Frey, N., and E. N. Olson. 2003. Cardiac hypertrophy: the good, the bad, and the ugly. Annu. Rev. Physiol. 65:45-79.
22. Friddle, C. J., T. Koga, E. M. Rubin, and J. Bristow. 2000. Expression profiling reveals distinct sets of genes altered during induction and regression of cardiac hypertrophy. Proc. Natl. Acad. Sci. USA 97:6745-6750.
23. Gregory, K. N., K. S. Ginsburg, I. Bodi, H. Hahn, Y. M. Marreez, Q. Song, P. A. Padmanabhan, B. A. Mitton, J. R. Waggoner, F. Del Monte, W. J. Park, G. W. Ii, D. M. Bers, and E. G. Kranias. 2006. Histidine-rich Ca binding protein: a regulator of sarcoplasmic reticulum calcium sequestration and cardiac function. J. Mol. Cell Cardiol. 40:653-665.
24. Guo, W., and K. P. Campbell. 1995. Association of triadin with the ryanodine receptor and calsequestrin in the lumen of the sarcoplasmic reticulum. J. Biol. Chem. 270:9027-9030.
25. Gyorke, I., N. Hester, L. R. Jones, and S. Gyorke. 2004. The role of calsequestrin, triadin, and junctin in conferring cardiac ryanodine receptor responsiveness to luminal calcium. Biophys. J. 86:2121-2128.
26. Haghighi, K., F. Kolokathis, A. O. Gramolini, J. R. Waggoner, L. Pater, R. A. Lynch, G. C. Fan, D. Tsiapras, R. R. Parekh, G. W. Dorn II, D. H. Maclennan, D. T. Kremastinos, and E. G. Kranias. 2006. A mutation in the human phospholamban gene, deleting arginine 14, results in lethal, hereditary cardiomyopathy. Proc. Natl. Acad. Sci. USA 103:1388-1393.
27. Haghighi, K., F. Kolokathis, L. Pater, R. A. Lynch, M. Asahi, A. O. Gramolini, G. C. Fan, D. Tsiapras, H. S. Hahn, S. Adamopoulos, S. B. Liggett, G. W. Dorn II, D. H. MacLennan, D. T. Kremastinos, and E. G. Kranias. 2003. Human phospholamban null results in lethal dilated cardiomyopathy revealing a critical difference between mouse and human. J. Clin. Investig. 111:869-876.
28. Hasenfuss, G. 1998. Alterations of calcium-regulatory proteins in heart failure. Cardiovasc. Res. 37:279-289.
29. Hofmann, S. L., M. S. Brown, E. Lee, R. K. Pathak, R. G. Anderson, and J. L. Goldstein. 1989. Purification of a sarcoplasmic reticulum protein that binds Ca2+ and plasma lipoproteins. J. Biol. Chem. 264:8260-8270.
30. Hofmann, S. L., J. L. Goldstein, K. Orth, C. R. Moomaw, C. A. Slaughter, and M. S. Brown. 1989. Molecular cloning of a histidine-rich Ca2+-binding protein of sarcoplasmic reticulum that contains highly conserved repeated elements. J. Biol. Chem. 264:18083-18090.
31. Hogan, B., R. Beddington, F. Costantini, and E. Lacy. 1994. Manipulating the mouse embryo, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
32. Jones, L. R., and S. E. Cala. 1981. Biochemical evidence for functional heterogeneity of cardiac sarcoplasmic reticulum vesicles. J. Biol. Chem. 256:11809-11818.
33. Jones, L. R., Y. J. Suzuki, W. Wang, Y. M. Kobayashi, V. Ramesh, C. Franzini-Armstrong, L. Cleemann, and M. Morad. 1998. Regulation of Ca2+ signaling in transgenic mouse cardiac myocytes overexpressing calsequestrin. J. Clin. Investig. 101:1385-1393.
34. Kim, E., D. W. Shin, C. S. Hong, D. Jeong, D. H. Kim, and W. J. Park. 2003. Increased Ca2+ storage capacity in the sarcoplasmic reticulum by overexpression of HRC (histidine-rich Ca2+ binding protein). Biochem. Biophys. Res. Commun. 300:192-196.
35. Kirchhefer, U., H. A. Baba, G. Hanske, L. R. Jones, P. Kirchhof, W. Schmitz, and J. Neumann. 2004. Age-dependent biochemical and contractile properties in atrium of transgenic mice overexpressing junctin. Am. J. Physiol. Heart Circ. Physiol. 287:H2216-H2225.
36. Kirchhefer, U., H. A. Baba, Y. M. Kobayashi, L. R. Jones, W. Schmitz, and J. Neumann. 2002. Altered function in atrium of transgenic mice overexpressing triadin 1. Am. J. Physiol. Heart Circ. Physiol. 283:H1334-H1343.
37. Kirchhefer, U., L. R. Jones, F. Begrow, P. Boknik, L. Hein, M. J. Lohse, B. Riemann, W. Schmitz, J. Stypmann, and J. Neumann. 2004. Transgenic triadin 1 overexpression alters SR Ca2+ handling and leads to a blunted contractile response to beta-adrenergic agonists. Cardiovasc. Res. 62:122-134.
38. Kirchhefer, U., J. Neumann, H. A. Baba, F. Begrow, Y. M. Kobayashi, U. Reinke, W. Schmitz, and L. R. Jones. 2001. Cardiac hypertrophy and impaired relaxation in transgenic mice overexpressing triadin 1. J. Biol. Chem. 276:4142-4149.
39. Kirchhefer, U., J. Neumann, D. M. Bers, I. B. Buchwalow, L. Fabritz, G. Hanske, I. Juslus, B. Riemann, W. Schmitz, and L. R. Jones. 2003. Impaired relaxation in transgenic mice overexpressing junctin. Cardiovasc. Res. 59:369-379.
40. Kong, Y., J. M. Shelton, B. Rothermel, X. Li, J. A. Richardson, R. Bassel-Duby, and R. S. Williams. 2001. Cardiac-specific LIM protein FHL2 modifies the hypertrophic response to beta-adrenergic stimulation. Circulation 103:2731-2738.
41. Krenz, M., and J. Robbins. 2004. Impact of beta-myosin heavy chain expression on cardiac function during stress. J. Am. Coll. Cardiol. 44:2390-2397.
42. Lahat, H., E. Pras, and M. Eldar. 2003. RYR2 and CASQ2 mutations in patients suffering from catecholaminergic polymorphic ventricular tachycardia. Circulation 107:e29. [Online.]
43. Lamb, G. D. 2000. Excitation-contraction coupling in skeletal muscle: comparisons with cardiac muscle. Clin. Exp. Pharmacol. Physiol. 27:216-224.
44. Lee, H. G., H. Kang, D. H. Kim, and W. J. Park. 2001. Interaction of HRC (histidine-rich Ca(2+)-binding protein) and triadin in the lumen of sarcoplasmic reticulum. J. Biol. Chem. 276:39533-39538.
45. Lokuta, A. J., T. B. Rogers, W. J. Lederer, and H. H. Valdivia. 1995. Modulation of cardiac ryanodine receptors of swine and rabbit by a phosphorylation-dephosphorylation mechanism. J. Physiol. 487:609-622.
46. Market, P., P. Shu, C. Ebeling, G. A. Carlson, D. L. Nagle, J. S. Smutko, and K. J. Moore. 1997. Theoretical and empirical issues for marker-assisted breeding of congenic mouse strains. Nat. Genet. 17:280-284.
47. Milner, R. E., K. S. Famulski, and M. Michalak. 1992. Calcium binding proteins in the sarcoplasmic/endoplasmic reticulum of muscle and non-muscle cells. Mol. Cell. Biochem. 112:1-13.
48. Molkentin, J. D. 2000. Calcineurin and beyond: cardiac hypertrophic signaling. Circ. Res. 87:731-738.
49. Morkin, E. 2000. Control of cardiac myosin heavy chain gene expression. Microsc. Res. Tech. 50:522-531.
50. Ohkura, M., K. Furukawa, H. Fujimori, A. Kuruma, S. Kawano, M. Hiraoka, A. Kuniyasu, H. Nakayama, and Y. Ohizumi. 1998. Dual regulation of the skeletal muscle ryanodine receptor by triadin and calsequestrin. Biochemistry 37:12987-12993.
51. Pathak, R. K., R. G. Anderson, and S. L. Hofmann. 1992. Histidine-rich calcium binding protein, a sarcoplasmic reticulum protein of striated muscle, is also abundant in arteriolar smooth muscle cells. J. Muscle Res. Cell Motil. 13:366-376.
52. Picello, E., E. Damiani, and A. Margreth. 1992. Low-affinity Ca(2+)-binding sites versus Zn(2+)-binding sites in histidine-rich Ca(2+)-binding protein of skeletal muscle sarcoplasmic reticulum. Biochem. Biophys. Res. Commun. 186:659-667.
53. Priori, S. G., C. Napolitano, N. Tiso, M. Memmi, G. Vignati, R. Bloise, V. Sorrentino, and G. A. Danieli. 2001. Mutations in the cardiac ryanodine receptor gene (hRyR2) underlie catecholaminergic polymorphic ventricular tachycardia. Circulation 103:196-200.
54. Rezgui, S. S., S. Vassilopoulos, J. Brocard, J. C. Platel, A. Bouron, C. Arnoult, S. Oddoux, L. Garcia, M. De Waard, and I. Marty. 2005. Triadin (Trisk 95) overexpression blocks excitation-contraction coupling in rat skeletal myotubes. J. Biol. Chem. 280:39302-39308.
55. Ridgeway, A. G., H. Petropoulos, A. Siu, J. K. Ball, and I. S. Skerjanc. 1999. Cloning, tissue distribution, subcellular localization and overexpression of murine histidine-rich Ca2+ binding protein. FEBS Lett. 456:399-402.
56. Sacchetto, R., E. Damiani, F. Turcato, A. Nori, and A. Margreth. 2001. Ca(2+)-dependent interaction of triadin with histidine-rich Ca(2+)-binding protein carboxyl-terminal region. Biochem. Biophys. Res. Commun. 289:1125-1134.
57. Sacchetto, R., F. Turcato, E. Damiani, and A. Margreth. 1999. Interaction of triadin with histidine-rich Ca(2+)-binding protein at the triadic junction in skeletal muscle fibers. J. Muscle Res. Cell Motil. 20:403-415.
58. Sambandam, N., G. D. Lopaschuk, R. W. Brownsey, and M. F. Allard. 2002. Energy metabolism in the hypertrophied heart. Heart Fail. Rev. 7:161-173.
59. Sato, Y., D. G. Ferguson, H. Sako, G. W. Dorn II, V. J. Kadambi, A. Yatani, B. D. Hoit, R. A. Walsh, and E. G. Kranias. 1998. Cardiac-specific overexpression of mouse cardiac calsequestrin is associated with depressed cardiovascular function and hypertrophy in transgenic mice. J. Biol. Chem. 273:28470-28477.
60. Spindler, M., K. W. Saupe, M. E. Christe, H. L. Sweeney, C. E. Seidman, J. G. Seidman, and J. S. Ingwall. 1998. Diastolic dysfunction and altered energetics in the alphaMHC403/+ mouse model of familial hypertrophic cardiomyopathy. J. Clin. Investig. 101:1775-1783.
61. Terentyev, D., S. E. Cala, T. D. Houle, S. Viatchenko-Xarpinski, I. Gyorke, R. Terentyeva, S. C. Williams, and S. Gyorke. 2005. Triadin overexpression stimulates excitation-contraction coupling and increases predisposition to cellular arrhythmia in cardiac myocytes. Circ. Res. 96:651-658.
62. Terentyev, D., S. Viatchenko-Karpinski, I. Gyorke, P. Volpe, S. C. Williams, and S. Gyorke. 2003. Calsequestrin determines the functional size and stability of cardiac intracellular calcium stores: mechanism for hereditary arrhythmia. Proc. Natl. Acad. Sci. USA 100:11759-11764.
63. Tian, R., N. Musi, J. D'Agostino, M. F. Hirshman, and L. J. Goodyear. 2001. Increased adenosine monophosphate-activated protein kinase activity in rat hearts with pressure-overload hypertrophy. Circulation 104:1664-1669.
64. Viatchenko-Karpinski, S., D. Terentyev, I. Gyorke, R. Terentyeva, P. Volpe, S. G. Priori, C. Napolitano, A. Nori, S. C. Williams, and S. Gyorke. 2004. Abnormal calcium signaling and sudden cardiac death associated with mutation of calsequestrin. Circ. Res. 94:471-477.
65. Yano, K., and A. Zarain-Herzberg. 1994. Sarcoplasmic reticulum calsequestrins: structural and functional properties. Mol. Cell. Biochem. 135:61-70.
66. Zhang, C. L., T. A. McKinsey, S. Chang, C. L. Antos, J. A. Hill, and E. N. Olson. 2002. Class II histone deacetylases act as signal-responsive repressors of cardiac hypertrophy. Cell 110:479-488.
67. Zhang, L., J. Kelley, G. Schmeisser, Y. M. Kobayashi, and L. R. Jones. 1997. Complex formation between junctin, triadin, calsequestrin, and the ryanodine receptor. Proteins of the cardiac junctional sarcoplasmic reticulum membrane. J. Biol. Chem. 272:23389-23397.
68. Zucchi, R., R. J. Cerniway, S. Ronca-Testoni, R. R. Morrison, G. Ronca, and G. P. Matherne. 2002. Effect of cardiac A(1) adenosine receptor overexpression on sarcoplasmic reticulum function. Cardiovasc. Res. 53:326-333.