DOI QR코드

DOI QR Code

Membrane associated Ca2+ buffers in the heart

  • Lee, Duk-Gyu (Department of Biochemistry, School of Molecular and Systems Medicine, University of Alberta) ;
  • Michalak, Marek (Department of Biochemistry, School of Molecular and Systems Medicine, University of Alberta)
  • Published : 2010.03.31

Abstract

$Ca^{2+}$ is a universal signalling molecule that affects a variety of cellular processes including cardiac development. The majority of intracellular $Ca^{2+}$ is stored in the endoplasmic and sarcoplasmic reticulum of muscle and non-muscle cells. Calreticulin is a well studied $Ca^{2+}$-buffering protein in the endoplasmic reticulum, and calreticulin deficiency is embryonic lethal due to impaired cardiac development. Despite calsequestrin being the most abundant $Ca^{2+}$-buffering protein in the sarcoplasmic reticulum, viability is maintained in embryos without calsequestrin and normal $Ca^{2+}$ release and contractile function is observed. The $Ca^{2+}$ homeostasis regulated by the endoplasmic and sarcoplasmic reticulum is critical for the development and proper function of the heart.

Keywords

References

  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 https://doi.org/10.1016/S0074-7696(01)05004-5
  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 https://doi.org/10.1038/35036035
  3. Corbett, E. F. and Michalak, M. (2000) Calcium, a signaling molecule in the endoplasmic reticulum? Trends. Biochem. Sci. 25, 307-311 https://doi.org/10.1016/S0968-0004(00)01588-7
  4. Nicchitta, C. V. (1998) Biochemical, cell biological and immunological issues surrounding the endoplasmic reticulum chaperone GRP94/gp96. Curr. Opin. Immunol. 10, 103-109 https://doi.org/10.1016/S0952-7915(98)80039-3
  5. Corbett, E. F., Oikawa, K., Francois, P., Tessier, D. C., Kay, C., Bergeron, J. J., Thomas, D. Y., Krause, K. H. and Michalak, M. (1999) $Ca^{2+}$ regulation of interactions between endoplasmic reticulum chaperones. J. Biol. Chem. 274, 6203-6211 https://doi.org/10.1074/jbc.274.10.6203
  6. Molinari, M. and Helenius, A. (2000) Chaperone selection during glycoprotein translocation into the endoplasmic reticulum. Science 288, 331-333 https://doi.org/10.1126/science.288.5464.331
  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 https://doi.org/10.1111/j.1600-0854.2008.00717.x
  8. Rossi, A. E. and Dirksen, R. T. (2006) Sarcoplasmic reticulum: the dynamic calcium governor of muscle. Muscle Nerve 33, 715-731 https://doi.org/10.1002/mus.20512
  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 https://doi.org/10.1042/bj3320351
  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 https://doi.org/10.1073/pnas.89.13.6142
  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 https://doi.org/10.1006/scdb.2000.0211
  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 https://doi.org/10.1038/nrm1155
  14. Webb, S. E. and Miller, A. L. (2003) Calcium signalling during embryonic development. Nat. Rev. Mol. Cell. Biol. 4, 539-551 https://doi.org/10.1038/nrm1149
  15. Baksh, S., Burns, K., Andrin, C. and Michalak, M. (1995) Interaction of calreticulin with protein disulfide isomerase. J. Biol. Chem. 270, 31338-31344 https://doi.org/10.1074/jbc.270.52.31338
  16. Putney, J. W., Jr. and McKay, R. R. (1999) Capacitative calcium entry channels. Bioessays. 21, 38-46 https://doi.org/10.1002/(SICI)1521-1878(199901)21:1<38::AID-BIES5>3.0.CO;2-S
  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 https://doi.org/10.1101/gad.13.10.1211
  18. Meldolesi, J. and Pozzan, T. (1998) The endoplasmic reticulum $Ca^{2+}$ store: a view from the lumen. Trends. Biochem. Sci. 23, 10-14 https://doi.org/10.1016/S0968-0004(97)01143-2
  19. Ashby, M. C. and Tepikin, A. V. (2001) ER calcium and the functions of intracellular organelles. Semin. Cell. Dev. Biol. 12, 11-17 https://doi.org/10.1006/scdb.2000.0212
  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 https://doi.org/10.1083/jcb.128.1.5
  21. Stevens, F. J. and Argon, Y. (1999) Protein folding in the ER. Semin. Cell. Dev. Biol. 10, 443-454 https://doi.org/10.1006/scdb.1999.0315
  22. Liou, J., Kim, M. L., Heo, W. D., Jones, J. T., Myers, J. W., Ferrell, J. E., Jr. and Meyer, T. (2005) STIM is a $Ca^{2+}$ sensor essential for $Ca^{2+}$-store-depletion-triggered $Ca^{2+}$ influx. Curr. Biol. 15, 1235-1241 https://doi.org/10.1016/j.cub.2005.05.055
  23. Bastianutto, C., Clementi, E., Codazzi, F., Podini, P., De Giorgi, F., Rizzuto, R., Meldolesi, J. and Pozzan, T. (1995) Overexpression of calreticulin increases the $Ca^{2+}$ capacity of rapidly exchanging $Ca^{2+}$ stores and reveals aspects of their lumenal microenvironment and function. J. Cell. Biol. 130, 847-855 https://doi.org/10.1083/jcb.130.4.847
  24. Mery, L., Mesaeli, N., Michalak, M., Opas, M., Lew, D. P. and Krause, K. H. (1996) Overexpression of calreticulin increases intracellular $Ca^{2+}$ storage and decreases storeoperated $Ca^{2+}$ influx. J. Biol. Chem. 271, 9332-9339 https://doi.org/10.1074/jbc.271.16.9332
  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 https://doi.org/10.1074/jbc.M202395200
  26. Baksh, S. and Michalak, M. (1991) Expression of calreticulin in Escherichia coli and identification of its $Ca^{2+}$ 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 https://doi.org/10.1083/jcb.144.5.857
  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 https://doi.org/10.1074/jbc.C000822200
  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 https://doi.org/10.1038/306387a0
  31. Lievremont, J. P., Rizzuto, R., Hendershot, L. and Meldolesi, J. (1997) BiP, a major chaperone protein of the endoplasmic reticulum lumen, plays a direct and important role in the storage of the rapidly exchanging pool of $Ca^{2+}$,J. Biol. Chem. 272, 30873-30879 https://doi.org/10.1074/jbc.272.49.30873
  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 https://doi.org/10.1006/bbrc.1994.1964
  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 https://doi.org/10.1111/j.1432-1033.1995.336_c.x
  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 https://doi.org/10.1038/nsb0698-409
  37. MacLennan, D. H. (2000) $Ca^{2+}$ signalling and muscle disease. Eur. J. Biochem. 267, 5291-5297 https://doi.org/10.1046/j.1432-1327.2000.01566.x
  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 https://doi.org/10.1016/j.tcm.2007.10.002
  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 https://doi.org/10.1021/bi0355286
  40. Baksh, S., Spamer, C., Heilmann, C. and Michalak, M. (1995) Identification of the $Zn^{2+}$ binding region in calreticulin. FEBS Lett. 376, 53-57 https://doi.org/10.1016/0014-5793(95)01246-4
  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 https://doi.org/10.1006/prep.2000.1291
  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 https://doi.org/10.1091/mbc.10.8.2573
  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 https://doi.org/10.1016/S0022-2836(02)00812-4
  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 https://doi.org/10.1073/pnas.042699099
  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 https://doi.org/10.1074/jbc.M508302200
  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 https://doi.org/10.1083/jcb.200102073
  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 https://doi.org/10.1091/mbc.9.6.1513
  48. Camacho, P. and Lechleiter, J. D. (1995) Calreticulin inhibits repetitive intracellular $Ca^{2+}$ waves. Cell 82, 765-771 https://doi.org/10.1016/0092-8674(95)90473-5
  49. John, L. M., Lechleiter, J. D. and Camacho, P. (1998) Differential modulation of SERCA2 isoforms by calreticulin. J. Cell. Biol. 142, 963-973 https://doi.org/10.1083/jcb.142.4.963
  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 https://doi.org/10.1038/386843a0
  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 https://doi.org/10.1152/physrev.00050.2006
  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 https://doi.org/10.1016/S1097-2765(03)00494-5
  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 https://doi.org/10.1042/BJ20081847
  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 https://doi.org/10.1042/bj2830767
  55. Slupsky, J. R., Ohnishi, M., Carpenter, M. R. and Reithmeier, R. A. (1987) Characterization of cardiac calsequestrin. Biochemistry 26, 6539-6544 https://doi.org/10.1021/bi00394a038
  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 https://doi.org/10.1152/ajpheart.00079.2004
  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. Szegedi, C., Sarkozi, S., Herzog, A., Jona, I. and Varsanyi, M. (1999) Calsequestrin: more than 'only' a luminal Ca2+ buffer inside the sarcoplasmic reticulum. Biochem. J. 337, 19-22 https://doi.org/10.1042/0264-6021:3370019
  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 https://doi.org/10.1016/S0006-3495(04)74271-X
  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 https://doi.org/10.1091/mbc.E07-03-0275
  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 https://doi.org/10.1186/1471-213X-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 https://doi.org/10.1006/dbio.1998.9025
  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 https://doi.org/10.1074/jbc.M101676200
  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 https://doi.org/10.1074/jbc.274.21.15085
  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 https://doi.org/10.1172/JCI12412
  67. Knollmann, B. C., Chopra, N., Hlaing, T., Akin, B., Yang, T., Ettensohn, K., Knollmann, B. E., Horton, K. D., Weissman, N. J., Holinstat, I., Zhang, W., Roden, D. M., Jones, L. R., Franzini-Armstrong, C. and Pfeifer, K. (2006) Casq2 deletion causes sarcoplasmic reticulum volume increase, premature $Ca^{2+}$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 https://doi.org/10.1161/01.RES.0000038886.18992.6B
  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 https://doi.org/10.1074/jbc.273.43.28470
  70. Jones, L. R., Suzuki, Y. J., Wang, W., Kobayashi, Y. M., Ramesh, V., Franzini-Armstrong, C., Cleemann, L., and Morad, M. (1998) Regulation of $Ca^{2+}$signaling in transgenic mouse cardiac myocytes overexpressing calsequestrin. J. Clin. Invest. 101, 1385-1393 https://doi.org/10.1172/JCI1362
  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 https://doi.org/10.1016/j.cardiores.2005.04.023
  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 https://doi.org/10.1006/jmcc.2000.1268
  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 https://doi.org/10.1016/j.yexcr.2007.10.009
  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 https://doi.org/10.1016/S0014-4827(03)00231-3

Cited by

  1. Calcium-dependent protein folding in amyotrophic lateral sclerosis vol.54, pp.2, 2013, https://doi.org/10.1016/j.ceca.2013.05.007
  2. Calcium signalling in developing cardiomyocytes: implications for model systems and disease vol.593, pp.5, 2015, https://doi.org/10.1113/jphysiol.2014.274712
  3. The cardiac calsequestrin gene transcription is modulated at the promoter by NFAT and MEF-2 transcription factors vol.12, pp.9, 2017, https://doi.org/10.1371/journal.pone.0184724
  4. Intracellular organelles in the saga of Ca2+ homeostasis: different molecules for different purposes? vol.69, pp.7, 2012, https://doi.org/10.1007/s00018-011-0845-9
  5. The endoplasmic reticulum in cardiovascular health and disease vol.90, pp.9, 2012, https://doi.org/10.1139/y2012-058
  6. Plasma Membrane Calcium Pump (PMCA4)-Neuronal Nitric-oxide Synthase Complex Regulates Cardiac Contractility through Modulation of a Compartmentalized Cyclic Nucleotide Microdomain vol.286, pp.48, 2011, https://doi.org/10.1074/jbc.M111.290411
  7. Proteomic Identification of a Novel Hsp90-Containing Protein–Mineral Complex Which Can Be Induced in Cells in Response to Massive Calcium Influx vol.11, pp.6, 2012, https://doi.org/10.1021/pr201201y
  8. Roles for the Sarco-/Endoplasmic Reticulum in Cardiac Myocyte Contraction, Protein Synthesis, and Protein Quality Control vol.27, pp.6, 2012, https://doi.org/10.1152/physiol.00034.2012