Membrane associated Ca2+ buffers in the heart

BMB Reports

Volumn 43, Issue 3, 2010, Pages 151-157

  Lee, Dukgyu ^a   Michalak, Marek ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Ca2+ homeostasis; Calreticulin; Calsequestrin; Endoplasmicreticulum; Heart; Sarcoplasmic reticulum

Indexed keywords

BUFFER; CALCIUM; CALRETICULIN; CALSEQUESTRIN;

CALCIUM SIGNALING; ENDOPLASMIC RETICULUM; HEART MUSCLE; METABOLISM; REVIEW; SARCOPLASMIC RETICULUM;

BUFFERS; CALCIUM; CALCIUM SIGNALING; CALRETICULIN; CALSEQUESTRIN; ENDOPLASMIC RETICULUM; MYOCARDIUM; SARCOPLASMIC RETICULUM;

EID: 77953532176     PISSN: 19766696     EISSN: 1976670X     Source Type: Journal    
DOI: 10.5483/BMBRep.2010.43.3.151     Document Type: Review

References (75)

1. Baumann, O. and Walz, B. (2001) Endoplasmic reticulum of animal cells and its organization into structural and functional domains. Int. Rev. Cytol. 205, 149-214.
2. Berridge, M. J., Lipp, P. and Bootman, M. D. (2000) The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell. Biol. 1, 11-21.
3. Corbett, E. F. and Michalak, M. (2000) Calcium, a signaling molecule in the endoplasmic reticulum? Trends. Biochem. Sci. 25, 307-311.
4. Nicchitta, C. V. (1998) Biochemical, cell biological and immunological issues surrounding the endoplasmic reticulum chaperone GRP94/gp96. Curr. Opin. Immunol. 10, 103-109.
5. + regulation of interactions between endoplasmic reticulum chaperones. J. Biol. Chem. 274, 6203-6211.
6. Molinari, M. and Helenius, A. (2000) Chaperone selection during glycoprotein translocation into the endoplasmic reticulum. Science 288, 331-333.
7. Rossi, D., Barone, V., Giacomello, E., Cusimano, V. and Sorrentino, V. (2008) The sarcoplasmic reticulum: an organized patchwork of specialized domains. Traffic 9, 1044-1049.
8. Rossi, A. E. and Dirksen, R. T. (2006) Sarcoplasmic reticulum: the dynamic calcium governor of muscle. Muscle Nerve 33, 715-731.
9. Vitadello, M., Colpo, P. and Gorza, L. (1998) Rabbit cardiac and skeletal myocytes differ in constitutive and inducible expression of the glucose-regulated protein GRP94. Biochem. J. 332, 351-359.
10. Fliegel, L., Newton, E., Burns, K. and Michalak, M. (1990) Molecular cloning of cDNA encoding a 55-kDa multifunctional thyroid hormone binding protein of skeletal muscle sarcoplasmic reticulum. J. Biol. Chem. 265, 15496-15502.
11. Volpe, P., Villa, A., Podini, P., Martini, A., Nori, A., Panzeri, M. C. and Meldolesi, J. (1992) The endoplasmic reticulum-sarcoplasmic reticulum connection: distribution of endoplasmic reticulum markers in the sarcoplasmic reticulum of skeletal muscle fibers. Proc. Natl. Acad. Sci. U.S.A. 89, 6142-6146.
12. Bootman, M. D., Collins, T. J., Peppiatt, C. M., Prothero, L. S., MacKenzie, L., De Smet, P., Travers, M., Tovey, S. C., Seo, J. T., Berridge, M. J., Ciccolini, F. and Lipp, P. (2001) Calcium signalling-an overview. Semin. Cell. Dev. Biol. 12, 3-10.
13. Berridge, M. J., Bootman, M. D. and Roderick, H. L.(2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell. Biol. 4, 517-529.
14. Webb, S. E. and Miller, A. L. (2003) Calcium signalling during embryonic development. Nat. Rev. Mol. Cell. Biol. 4, 539-551.
15. Baksh, S., Burns, K., Andrin, C. and Michalak, M. (1995) Interaction of calreticulin with protein disulfide isomerase. J. Biol. Chem. 270, 31338-31344.
16. Putney, J. W., Jr. and McKay, R. R. (1999) Capacitative calcium entry channels. Bioessays. 21, 38-46.
17. Kaufman, R. J. (1999) Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes. Dev. 13, 1211-1233.
18. 2+ store: a view from the lumen. Trends. Biochem. Sci. 23, 10-14.
19. Ashby, M. C. and Tepikin, A. V. (2001) ER calcium and the functions of intracellular organelles. Semin. Cell. Dev. Biol. 12, 11-17.
20. Greber, U. F. and Gerace, L. (1995) Depletion of calcium from the lumen of endoplasmic reticulum reversibly inhibits passive diffusion and signal-mediated transport into the nucleus. J. Cell. Bio.l 128, 5-14.
21. Stevens, F. J. and Argon, Y. (1999) Protein folding in the ER. Semin. Cell. Dev. Biol. 10, 443-454.
22. 2+ influx. Curr. Biol. 15, 1235-1241.
23. 2+ stores and reveals aspects of their lumenal microenvironment and function. J. Cell. Biol. 130, 847-855.
24. 2+ influx. J. Biol. Chem. 271, 9332-9339.
25. Arnaudeau, S., Frieden, M., Nakamura, K., Castelbou, C., Michalak, M. and Demaurex, N. (2002) Calreticulin differentially modulates calcium uptake and release in the endoplasmic reticulum and mitochondria. J. Biol. Chem. 277, 46696-46705.
26. 2+ binding domains. J. Biol. Chem. 266, 21458-21465.
27. Mesaeli, N., Nakamura, K., Zvaritch, E., Dickie, P., Dziak, E., Krause, K. H., Opas, M., MacLennan, D. H. and Michalak, M. (1999) Calreticulin is essential for cardiac development. J. Cell. Biol. 144, 857-868.
28. Guo, L., Lynch, J., Nakamura, K., Fliegel, L., Kasahara, H., Izumo, S., Komuro, I., Agellon, L. B. and Michalak, M. (2001) COUP-TF1 antagonizes Nkx2.5-mediated activation of the calreticulin gene during cardiac development. J. Biol. Chem. 276, 2797-2801.
29. Koch, G., Smith, M., Macer, D., Webster, P. and Mortara, R. (1986) Endoplasmic reticulum contains a common, abundant calcium-binding glycoprotein, endoplasmin. J. Cell. Sci. 86, 217-232.
30. Haas, I. G. and Wabl, M. (1983) Immunoglobulin heavy chain binding protein. Nature 306, 387-389.
31. 2+. J. Biol. Chem. 272, 30873-30879.
32. Lebeche, D., Lucero, H. A. and Kaminer, B. (1994) Calcium binding properties of rabbit liver protein disulfide isomerase. Biochem. Biophys. Res. Commun. 202, 556-561.
33. Hirano, N., Shibasaki, F., Sakai, R., Tanaka, T., Nishida, J., Yazaki, Y., Takenawa, T. and Hirai, H. (1995) Molecular cloning of the human glucose-regulated protein ERp57/GRP58, a thiol-dependent reductase. Identification of its secretory form and inducible expression by the oncogenic transformation. Eur. J. Biochem. 234, 336-342.
34. Wada, I., Rindress, D., Cameron, P. H., Ou, W. J., Doherty, J. J., 2nd, Louvard, D., Bell, A. W., Dignard, D., Thomas, D. Y. and Bergeron, J. J. (1991) SSR alpha and associated calnexin are major calcium binding proteins of the endoplasmic reticulum membrane. J. Biol. Chem. 266, 19599-19610.
35. Milner, R. E., Baksh, S., Shemanko, C., Carpenter, M. R., Smillie, L., Vance, J. E., Opas, M. and Michalak, M. (1991) Calreticulin, and not calsequestrin, is the major calcium binding protein of smooth muscle sarcoplasmic reticulum and liver endoplasmic reticulum. J. Biol. Chem. 266, 7155-7165.
36. MacLennan, D. H. and Reithmeier, R. A. (1998) Ion tamers. Nat. Struct. Biol. 5, 409-411.
37. 2+ signalling and muscle disease. Eur. J. Biochem. 267, 5291-5297.
38. Fan, G. C., Yuan, Q. and Kranias, E. G. (2008) Regulatory roles of junctin in sarcoplasmic reticulum calcium cycling and myocardial function. Trends. Cardiovasc. Med. 18, 1-5.
39. Kapoor, M., Ellgaard, L., Gopalakrishnapai, J., Schirra, C., Gemma, E., Oscarson, S., Helenius, A. and Surolia, A. (2004) Mutational analysis provides molecular insight into the carbohydrate-binding region of calreticulin: pivotal roles of tyrosine-109 and aspartate-135 in carbohydrate recognition. Biochemistry 43, 97-106.
40. 2+ binding region in calreticulin. FEBS Lett. 376, 53-57.
41. Andrin, C., Corbett, E. F., Johnson, S., Dabrowska, M., Campbell, I. D., Eggleton, P., Opas, M. and Michalak, M. (2000) Expression and purification of mammalian calreticulin in Pichia pastoris. Protein. Expr. Purif. 20, 207-215.
42. Oliver, J. D., Roderick, H. L., Llewellyn, D. H. and High, S. (1999) ERp57 functions as a subunit of specific complexes formed with the ER lectins calreticulin and calnexin. Mol. Biol. Cell. 10, 2573-2582.
43. Ellgaard, L., Bettendorff, P., Braun, D., Herrmann, T., Fiorito, F., Jelesarov, I., Guntert, P., Helenius, A. and Wuthrich, K. (2002) NMR structures of 36 and 73-residue fragments of the calreticulin P-domain. J. Mol. Biol. 322, 773-784.
44. Frickel, E. M., Riek, R., Jelesarov, I., Helenius, A., Wuthrich, K. and Ellgaard, L. (2002) TROSY-NMR reveals interaction between ERp57 and the tip of the calreticulin P-domain. Proc. Natl. Acad. Sci. U.S.A. 99, 1954-1959.
45. Martin, V., Groenendyk, J., Steiner, S. S., Guo, L., Dabrowska, M., Parker, J. M., Muller-Esterl, W., Opas, M. and Michalak, M. (2006) Identification by mutational analysis of amino acid residues essential in the chaperone function of calreticulin. J. Biol. Chem. 281, 2338-2346.
46. Nakamura, K., Zuppini, A., Arnaudeau, S., Lynch, J., Ahsan, I., Krause, R., Papp, S., De Smedt, H., Parys, J. B., Muller-Esterl, W., Lew, D. P., Krause, K. H., Demaurex, N., Opas, M. and Michalak, M. (2001) Functional specialization of calreticulin domains. J. Cell. Biol. 154, 961-972.
47. Fasolato, C., Pizzo, P. and Pozzan, T. (1998) Delayed activation of the store-operated calcium current induced by calreticulin overexpression in RBL-1 cells. Mol. Biol. Cell. 9, 1513-1522.
48. 2+ waves. Cell 82, 765-771.
49. John, L. M., Lechleiter, J. D. and Camacho, P. (1998) Differential modulation of SERCA2 isoforms by calreticulin. J. Cell. Biol. 142, 963-973.
50. Coppolino, M. G., Woodside, M. J., Demaurex, N., Grinstein, S., St-Arnaud, R. and Dedhar, S. (1997) Calreticulin is essential for integrin-mediated calcium signalling and cell adhesion. Nature 386, 843-847.
51. Hebert, D. N. and Molinari, M. (2007) In and out of the ER: protein folding, quality control, degradation, and related human diseases. Physiol. Rev. 87, 1377-1408.
52. Molinari, M., Eriksson, K. K., Calanca, V., Galli, C., Cresswell, P., Michalak, M. and Helenius, A. (2004) Contrasting functions of calreticulin and calnexin in glycoprotein folding and ER quality control. Mol. Cell 13, 125-135.
53. Michalak, M., Groenendyk, J., Szabo, E., Gold, L. I. and Opas, M. (2009) Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochem. J. 417, 651-666.
54. Treves, S., Vilsen, B., Chiozzi, P., Andersen, J. P. and Zorzato, F. (1992) Molecular cloning, functional expression and tissue distribution of the cDNA encoding frog skeletal muscle calsequestrin. Biochem. J. 283, 767-772.
55. Slupsky, J. R., Ohnishi, M., Carpenter, M. R. and Reithmeier, R. A. (1987) Characterization of cardiac calsequestrin. Biochemistry 26, 6539-6544.
56. Yang, A., Sonin, D., Jones, L., Barry, W. H. and Liang, B. T. (2004) A beneficial role of cardiac P2X4 receptors in heart failure: rescue of the calsequestrin overexpression model of cardiomyopathy. Am. J. Physiol. Heart. Circ. Physiol. 287, H1096-1103.
57. Scott, B. T., Simmerman, H. K., Collins, J. H., Nadal-Ginard, B. and Jones, L. R. (1988) Complete amino acid sequence of canine cardiac calsequestrin deduced by cDNA cloning. J. Biol. Chem. 263, 8958-8964.
58. 2+ buffer inside the sarcoplasmic reticulum. Biochem. J. 337, 19-22.
59. Gyorke, I., Hester, N., Jones, L. R. and Gyorke, S. (2004) The role of calsequestrin, triadin, and junctin in conferring cardiac ryanodine receptor responsiveness to luminal calcium. Biophys. J. 86, 2121-2128.
60. Wanderling, S., Simen, B. B., Ostrovsky, O., Ahmed, N. T., Vogen, S. M., Gidalevitz, T. and Argon, Y. (2007) GRP94 is essential for mesoderm induction and muscle development because it regulates insulin-like growth factor secretion. Mol. Biol. Cell. 18, 3764-3775.
61. Lozyk, M. D., Papp, S., Zhang, X., Nakamura, K., Michalak, M. and Opas, M. (2006) Ultrastructural analysis of development of myocardium in calreticulin-deficient mice. BMC. Dev. Biol. 6, 54.
62. Goncharova, E. J., Kam, Z., and Geiger, B. (1992) The involvement of adherens junction components in myofibrillogenesis in cultured cardiac myocytes. Development 114, 173-183.
63. Linask, K. K., Ludwig, C., Han, M. D., Liu, X., Radice, G. L. and Knudsen, K. A. (1998) N-cadherin/catenin-mediated morphoregulation of somite formation. Dev. Biol. 202, 85-102.
64. Fadel, M. P., Szewczenko-Pawlikowski, M., Leclerc, P., Dziak, E., Symonds, J. M., Blaschuk, O., Michalak, M. and Opas, M. (2001) Calreticulin affects beta-catenin-associated pathways. J. Biol. Chem. 276, 27083-27089.
65. Fadel, M. P., Dziak, E., Lo, C. M., Ferrier, J., Mesaeli, N., Michalak, M. and Opas, M. (1999) Calreticulin affects focal contact-dependent but not close contact-dependent cell-substratum adhesion. J. Biol. Chem. 274, 15085-15094.
66. Nakamura, K., Robertson, M., Liu, G., Dickie, P., Guo, J. Q., Duff, H. J., Opas, M., Kavanagh, K. and Michalak, M. (2001) Complete heart block and sudden death in mice overexpressing calreticulin. J. Clin. Invest. 107, 1245-1253.
67. 2+ release, and catecholaminergic polymorphic ventricular tachycardia. J. Clin. Invest. 116, 2510-2520.
68. Postma, A. V., Denjoy, I., Hoorntje, T. M., Lupoglazoff, J. M., Da Costa, A., Sebillon, P., Mannens, M. M., Wilde, A. A. and Guicheney, P. (2002) Absence of calsequestrin 2 causes severe forms of catecholaminergic polymorphic ventricular tachycardia. Circ Res. 91, e21-26.
69. Sato, Y., Ferguson, D. G., Sako, H., Dorn, G. W., 2nd, Kadambi, V. J., Yatani, A., Hoit, B. D., Walsh, R. A. and Kranias, E. G. (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.
70. + signaling in transgenic mouse cardiac myocytes overexpressing calsequestrin. J. Clin. Invest. 101, 1385-1393.
71. Miller, S. L., Currie, S., Loughrey, C. M., Kettlewell, S.,Seidler, T., Reynolds, D. F., Hasenfuss, G. and Smith, G. L. (2005) Effects of calsequestrin over-expression on excitation-contraction coupling in isolated rabbit cardiomyocytes. Cardiovasc Res. 67, 667-677.
72. Tsutsui, H., Ishibashi, Y., Imanaka-Yoshida, K., Yamamoto, S., Yoshida, T., Sugimachi, M., Urabe, Y. and Takeshita, A. (1997) Alterations in sarcoplasmic reticulum calcium-storing proteins in pressure-overload cardiac hypertrophy. Am. J. Physiol. 272, H168-175.
73. Allen, B. G. and Katz, S. (2000) Calreticulin and calsequestrin are differentially distributed in canine heart. J. Mol. Cell. Cardiol. 32, 2379-2384.
74. Kaakinen, M., Papponen, H. and Metsikko, K. (2008) Microdomains of endoplasmic reticulum within the sarcoplasmic reticulum of skeletal myofibers. Exp. Cell. Res. 314, 237-245.
75. Kaisto, T. and Metsikko, K. (2003) Distribution of the endoplasmic reticulum and its relationship with the sarcoplasmic reticulum in skeletal myofibers. Exp. Cell. Res. 289, 47-57.