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Calcium binding proteins in the sarcoplasmic/endoplasmic reticulum of muscle and nonmuscle cells

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Abstract

In this paper we review some of the large quantities of information currently available concerning the identification, structure and function of Ca2+-binding proteins of endoplasmic and sarcoplasmic reticulum membranes. The review places particular emphasis on identification and discussion of Ca2+ ‘storage’ proteins in these membranes. We believe that the evidence reviewed here supports the contention that the Ca2+-binding capacity of both calsequestrin and calreticulin favor their contribution as the major Ca2+-binding proteins of muscle and nonmuscle cells, respectively. Other Ca2+-binding proteins discovered in both endoplasmic reticulum and sarcoplasmic reticulum membranes probably contribute to the overall Ca2+ storage capacity of these membrane organelles, and they also play other important functional role such as posttranslational modification of newly synthesized proteins, a cytoskeletal (structural) function, or movement of Ca2+ within the lumen of the sarcoplasmic/endoplasmic reticulum towards the storage sites.

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Abbreviations

SR:

Sarcoplasmic Reticulum

ER:

Endoplasmic Reticulum

InsP3 :

Inositol 1,4,5-trisphosphate

SDS-PAGE:

Sodium Dodecyl Sulfate-Polyacrylamide Gel Electrophoresis

PDI:

Protein Disulphide Isomerase

T3BP:

Thyroid Hormone Binding Protein

Grp:

Glucose regulated proteins

HCP:

Histidine-rich Ca2+ binding Protein

LDL:

Low Density Lipoprotein

References

  1. Carafoli E: Intracellular calcium homeostasis. Annu Rev Biochem 56: 395–433, 1987

    Google Scholar 

  2. Berridge MJ: Calcium oscillations. J Biol Chem 265: 9585–9586, 1990

    Google Scholar 

  3. Fleischer S, Inui M: Biochemistry and biophysics of excitation-contraction coupling. Annu Rev Biophys Chem 18: 333–343, 1989

    Google Scholar 

  4. Samlyo AP, Himpens B: Cell calcium and its regulation in smooth muscle. FASEB J 3: 226–2276, 1989

    Google Scholar 

  5. van Breeman C, Saido K: Cellular mechanisms regulation [Ca+]i smooth muscle. Annu Rev Physiol 51: 315–329, 1989

    Google Scholar 

  6. Walz B, Baumann O: Calcium-sequestering cell organelles: in situ localization, morphological and functional characterization. Topics Histochem Cytochem 20: 1–45, 1989

    Google Scholar 

  7. MacLennan DH, Campbell KP, Reithmeier RAF: Calsequestrin. In: Calcium and Cell Function 4: 151–173, 1983

    Google Scholar 

  8. Michalak M, Campbell KP, MacLennan DH: Localization of the high affinity calcium binding protein and an intrinsic glycoprotein in sarcoplasmic reticulum membranes. J Biol Chem 255: 1317–1326, 1980

    Google Scholar 

  9. Fliegel L, Ohnishi M, Carpenter MR, Khanna VK, Reithmeier RAF, MacLennan DH: Amino acid sequence of rabbit fast-twitch skeletal muscle calsequestrin deduced from cDNA and peptide sequencing. Proc Natl Acad Sci USA 84: 1167–1171, 1987

    Google Scholar 

  10. Cala SE, Scott BT, Jones LR: Intralumenal sarcoplasmic reticulum Ca2+-binding proteins. Sem Cell Biol 1: 265–275, 1990

    Google Scholar 

  11. Damiani E, Spamer C, Heilmann C, Salvatory S, Margreth A: Endoplasmic reticulum of rat liver contains two proteins closely related to skeletal sarcoplasmic reticulum Ca-ATPase and calsequestrin. J Biol Chem 263: 340–343, 1988

    Google Scholar 

  12. Hashimoto S, Bruno B, Lew DP, Pozzan T, Volpe P, Meldolesi J: Immunocytochemistry of calciosomes in liver and pancreas. J Cell Biol 107: 2523–2531, 1988

    Google Scholar 

  13. Krause K-H, Pittet D, Volpe P, Pozzan T, Meldolesi J, Lew DP: Calciosome, a sarcoplasmic reticulum-like organelle involved in intracellular Ca2+-handling by nonmuscle cells: studies in human neutrophils and HL-60 cells. Cell Calcium 10: 351–361, 1989

    Google Scholar 

  14. Milner RE, Baksh S, Shemanko C, Carpenter MR, Smillie L, Vance JE, Opas M, Michalak M: 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, 1991

    Google Scholar 

  15. Koch GLE, Smith MJ, Macer DRJ, Booth C, Wooding FBP: Structure and assembly of the endoplasmic reticulum. Biochem Soc Trans 17: 328–331, 1989

    Google Scholar 

  16. Meldolesi J, Madeddu L, Pozzan T: Intracellular Ca2+ storage organelles in nonmuscle cells: heterogeneity and functional assignment. Biochim Biophys Acta 1055: 130–140, 1990

    Google Scholar 

  17. Koch GLE: The endoplasmic reticulum and calcium storage. BioEssays 12: 527–531, 1990

    Google Scholar 

  18. Tsien RW, Tsien RY: Calcium channels, stores, and oscillations. Annu Rev Cell Biol 6: 715–760, 1990

    Google Scholar 

  19. Pietrobon D, Di Virgilio F, Pozzan T: Structural and functional aspects of calcium homeostasis in eukaryotic cells. Eur J Biochem 193: 599–622, 1990

    Google Scholar 

  20. MacLennan DH: Molecular tools to elucidate problems in excitation-contraction coupling. Biophys J 58: 1355–1365, 1990

    Google Scholar 

  21. Sulakhe PV, St. Louis PJ: Passive and active calcium fluxes across plasma membranes. Prog Biophys Mol Biol 35: 135–195, 1980

    Google Scholar 

  22. Aaron BMB, Oikawa K, Reithmeier RAF, Sykes BD: Characterization of the skeletal muscle calsequestrin by 1H NMR spectroscopy. J Biol Chem 259: 11876–11881, 1984

    Google Scholar 

  23. Cozens B, Reithmeier RAF: Size and shape of rabbit skeletal muscle calsequestrin. J Biol Chem 259: 6248–6252, 1984

    Google Scholar 

  24. Slupsky JR, Ohnishi M, Carpenter MR, Reithmeier RAF: Characterization of cardiac calsequestrin. Biochemistry 26: 6539–6544, 1987

    Google Scholar 

  25. Ohnishi M, Reithmeier RAF: Fragmentation of rabbit skeletal muscle calsequestrin: spectral and ion binding properties of the carboxyl-terminal region. Biochemistry 26: 7458–7465, 1987

    Google Scholar 

  26. Mitchell RD, Simmerman HKB, Jones LR: Ca2+ binding effects protein of canine cardiac calsequestrin. J Biol Chem 263: 1376–1381, 1988

    Google Scholar 

  27. Maurer A, Tanaka M, Ozawa T, Fleischer S: Purification and crystallization of the calcium binding protein of sarcoplasmic reticulum from skeletal muscle. Proc Natl Acad Sci USA 82: 4036–4040, 1985

    Google Scholar 

  28. Williams RW, Beeler TJ: Secondary structure of calsequestrin in solutions and in crystals as determined by Raman spectroscopy. J Biol Chem 261: 12408–12413, 1986

    Google Scholar 

  29. Cala SE, Jones LR: Rapid purification of calsequestrin from cardiac and skeletal muscle sarcoplasmic reticulum vesicles by Ca2+-dependent elution from phenyl-Sepharose. J Biol Chem 258: 11932–11936, 1983

    Google Scholar 

  30. Jones LR, Besch Jr HR, Fleming JW, McConnaughey MM, Watanabe M: Separation of vesicles of cardiac sarcolemma from vesicles of cardiac sarcoplasmic reticulum. Comparative bio chemical analysis of component activities. J Biol Chem 254: 530–539, 1979

    Google Scholar 

  31. Campbell KP, MacLennan DH, Jorgensen AO: Staining of the Ca2+-binding proteins, calsequestrin, calmodulin, troponin C, and S-100, with the cationic carbocyanine dye ‘Stains-All’. J Biol Chem 258: 11267–11273, 1983

    Google Scholar 

  32. Franzini-Armstrong C, Kenney LJ, Varriano-Marston E: The structure of calsequestrin in triads of vertebrate skeletal muscle: a deep-etch study. J Cell Biol 105: 49–56, 1987

    Google Scholar 

  33. Collins JH, Tarcsafalvi A, Ikemoto N: Identification of a region of calsequestrin that binds to the junctional face membrane of sarcoplasmic reticulum. Biochem Biophys Res Commun 167: 189–193, 1990

    Google Scholar 

  34. Ikemoto N, Ronjat M, Meszaros LG, Koshita M: Postulated role of calsequestrin in the regulation of calcium release from sarcoplasmic reticulum. Biochemistry 28: 6764–6771, 1989

    Google Scholar 

  35. Damiani E, Margreth A: Specific protein-protein interactions of calsequestrin with junctional sarcoplasmic reticulum of skeletal muscle. Biochem Biophys Res Commun 172: 1253–1259, 1990

    Google Scholar 

  36. Campbell KP, Knudson CM, Imagawa T, Leung AT, Sutko JL: Identification and characterization of the high affinity [3H] ryanodine receptor of the junctional sarcoplasmic reticulum. J Biol Chem 262: 6460–6463, 1987

    Google Scholar 

  37. Inui M, Saito A, Fleischer S: Purification of the ryanodine receptor and identity with feet structures of junctional terminal cisternae of sarcoplasmic reticulum from fast skeletal muscle. J Biol Chem 262: 1740–1747, 1987

    Google Scholar 

  38. Lai FA, Erickson HP, Rousseau E, Liu Q-Y, Meissner G: Purification and reconstitution of the calcium release channel from skeletal muscle. Nature 331: 315–319, 1988

    Google Scholar 

  39. Rardon DP, Cefali DC, Mitchell RD, Seiler SM, Jones LR: High molecular weight proteins purified from cardiac junctional sarcoplasmic reticulum vesicles are ryanodine-sensitive calcium channels. Circ Res 64: 779–789, 1989

    Google Scholar 

  40. Smith JS, Imagawa T, Ma J, Fill M, Campbell KP, Coronado R: Purified ryanodine receptor from rabbit skeletal muscle is the Ca2+-release channel of sarcoplasmic reticulum. J Gen Physiol 92: 1–26, 1988

    Google Scholar 

  41. Penner R, Neher E, Takesima H, Nishimura S, Numa S: Functional expression of the calcium release channel from skeletal muscle ryanodine receptor cDNA. FEBS Lett. 259: 391–398, 1991

    Google Scholar 

  42. Zorzato F, Fujii J, Otsu K, Phillips M, Green NM, Lai FA, Meissner G, MacLennan DH: Molecular cloning of cDNA encoding human and rabbit forms of the Ca2+ release channel (ryanodine receptor) of skeletal muscle sarcoplasmic reticulum. J Biol Chem 265: 2244–2256, 1990

    Google Scholar 

  43. Otsu K, Willard HF, Khanna VJ, Zorzato F, Green NM, MacLennan DH: Molecular cloning of cDNA encoding the Ca2+ release channel (ryanodine receptor) of rabbit cardiac muscle sarcoplasmic reticulum. J Biol Chem 265: 13472–13483, 1990

    Google Scholar 

  44. Takeshima H, Nishimura S, Matsumoto T, Ishiada H, Kangawa K, Minamino N, Matsuo H, Ueda M, Hanaoka M, Hirose T, Numa S: Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature 339: 439–445, 1987

    Google Scholar 

  45. Cala SE, Jones LR: Phosphorylation of cardiac and skeletal muscle calsequestrin isoforms by casein kinase II. J Biol Chem 266: 391–398, 1991

    Google Scholar 

  46. Thomas K, Navarro J, Benson RJJ, Campbell KP, Rotundo RL, Fine RE: Newly synthesized calsequestrin, destined for the sarcoplasmic reticulum, is contained in early/intermediate Golgi derived clathrin-coated vesicles. J Biol Chem 264: 3140–3145, 1989

    Google Scholar 

  47. Fliegel L, Ohnishi M, Carpenter MR, Khanna VK, Reithmeier RAF, MacLennan DH: Amino acid sequence of rabbit fast-twitch skeletal muscle calsequestrin deduced from cDNA and peptide sequencing. Proc Natl Acad Sci USA 84: 1167–1171, 1987

    Google Scholar 

  48. Scott BT, Simmerman HKB, Collins JH, Nadal-Ginard B, Jones LR: Complete amino acid sequence of canine cardiac calsequestrin deduced by cDNA cloning. J Biol Chem 263: 8958–8964, 1988

    Google Scholar 

  49. Leberer E, Timms BG, Campbell KP, MacLennan DH: Purification, calcium binding properties, and ultrastructural localization of the 53,000- and 160,000 (sarcalumenin)-dalton gly coproteins of the sarcoplasmic reticulum. J Biol Chem 265: 10118–10124, 1990

    Google Scholar 

  50. Ostwald TJ, MacLennan DH: Isolation of a high affinity calcium-binding protein from sarcoplasmic reticulum. J Biol Chem 249: 974–979, 1974

    Google Scholar 

  51. Hofmann SL, Goldstein JL, Orth K, Moomaw CR, Slaughter CA, Brown MS: Molecular cloning of a histidine-rich Ca2+-binding protein of sarcoplasmic reticulum that contains highly conserved repeated elements. J Biol Chem 264: 18083–18090, 1989

    Google Scholar 

  52. Hofmann SL, Brown MS, Lee E, Pathak RK, Anderson RGW, Goldstein JL: Purification of a sarcoplasmic reticulum protein that binds Ca2+ and plasma lipoproteins. J Biol Chem 264: 8260–8270, 1989

    Google Scholar 

  53. Hofmann SL, Topham M, Hsieh CL, Francke U: cDNA and genomic cloning of HPC, a human sarcoplasmic reticulum protein, and localization of the gene to human chromosome 19 and mouse chromosome 7. Genomics 9: 656–669, 1991

    Google Scholar 

  54. Cala SE, Jones LR: Purification and identification of endoplasmin (Grp94) from canine cardiac sarcoplasmic reticulum (SR). Biophys J 59: 249a, 1991

  55. Fliegel L, Newton E, Burns K, Michalak M: Molecular cloning of cDNA encoding a 55-kDa multifunctional thyroid hormone binding protein of skeletal muscle sarcoplasmic reticulum. J Biol Chem 265: 15496–15502, 1990

    Google Scholar 

  56. Fliegel L, Burns K, Opas M, Michalak M: The high affinity calcium binding protein of skeletal muscle sarcoplasmic reticulum. Biochem Biophys Acta 982: 1–8, 1989

    Google Scholar 

  57. Mahoney L, Jones LR: Developmental changes in cardiac sarcoplasmic reticulum in sheep. J Biol Chem 261: 15257–15265, 1986

    Google Scholar 

  58. Leberer E, Charuk JHM, Green NM, MacLennan DH: Molecular cloning and expression of cDNA encoding a lumenal calcium binding glycoprotein from sarcoplasmic reticulum. Proc Natl Acad Sci USA 86: 6047–6051, 1989

    Google Scholar 

  59. Leberer E, Charuk JHM, Clarke DM, Green NM, Zubrzycka-Gaarn E, MacLennan DH: Molecular cloning and expression of cDNA encoding the 53,000-Dalton glycoprotein of rabbits skeletal muscle sarcoplasmic reticulum. J Biol Chem 264: 3484–3493, 1989

    Google Scholar 

  60. Fliegel L, Burns K, MacLennan DH, Reithmeier RAF, Michalak M: Molecular cloning of the high affinity calcium binding protein (calreticulin) of skeletal muscle sarcoplasmic reticulum. J Biol Chem 264: 21522–21528, 1989

    Google Scholar 

  61. Fliegel L, Burns K, Wlasichuk K, Michalak M: Peripheral membrane proteins of sarcoplasmic and endoplasmic reticulum. Comparison of carboxyl-terminal amino acid sequences. Biochem Cell Biol 67: 696–702, 1989

    Google Scholar 

  62. Smith MJ, Koch GLE: Multiple zones in the sequence of calreticulin (CRP55, calregulin, HACBP), a major calcium binding ER/SR protein. EMBO J 8: 3581–3586, 1989

    Google Scholar 

  63. McCauliffe DP, Zappi E, Lieu TS, Michalak M, Sontheimer RD, Capra JD: A human Ro/SS-A autoantigen is the homologue of calreticulin and is highly homologous with Onchocercal RAL-1 antigen and an Aplysia ‘memory molecule’. J Clin Invest 86:332–335, 1990

    Google Scholar 

  64. Waisman DM, Salimath BP, Anderson MJ: Isolation and characterization of CAB-63, a novel calcium-binding protein. J Biol Chem 260: 1652–1660, 1985

    Google Scholar 

  65. Sorger PK, Pelham HRB: The glucose regulated protein Grp94 is related to the heat shock protein hsp90. J Mol Biol 194: 341–344, 1988

    Google Scholar 

  66. Koch GLE, Smith M, Macer D, Webster P, Mortara R: Endoplasmic reticulum contains a common, abundant calcium-binding glycoprotein, endoplasmin. J Cell Sci 86: 217–232, 1986

    Google Scholar 

  67. Edman JC, Ellies L, Blacker RW, Roth RA, Rutter WJ: Sequence of protein disulphide isomerase and implications of its relationship to thioredoxin. Nature 317: 267–270, 1985

    Google Scholar 

  68. Pihlajaniemi T, Helaakoski T, Tasanen K, Myllyla R, Huhtala ML, Koivu J, Kivirikko KI: tMolecular cloning of the β-subunit of human prolyl 4-hydroxylase. This subunit and protein disulphide isomerase are products of the same gene. EMBO J 6: 643–649

  69. Geetha-Habbib M, Noiva R, Kaplan HA, Lennarz WJ: Glycosylation site binding protein, a component of oligosaccharyl transferase, is highly similar to three other 57 kd lumenal proteins of the ER. Cell 54: 1053–1060, 1988

    Google Scholar 

  70. Pelham HRB: Control of protein exit from the endoplasmic reticulum. Annu Rev Cell Biol 5: 1–23, 1989

    Google Scholar 

  71. Vaux D, Tooze J, Fuller S: Identification by anti-idiotype antibodies of an intracellular membrane protein that recognizes a mammalian endoplasmic reticulum retention signal. Nature 345: 495–502, 1990

    Google Scholar 

  72. Volpe P, Krause K-H, Hashimoto S, Zorzato F, Pozzan T, Meldolesi J, Lew DP: ‘Calciosome’, a cytoplasmic organelle: the inositol 1,4,5-trisphophate-sensitive Ca2+ store of nonmuscle cells? Proc Natl Acad Sci USA 85: 1091–1095, 1988

    Google Scholar 

  73. Michalak M, Baksh S, Opas M: Identification and immunolocalization of calreticulin in pancreatic cells: no evidence for ‘calcio-somes’. Exp Cell Res 179: 91–99, 1991

    Google Scholar 

  74. Opas M, Dziak E, Fliegel L, Michalak M: Regulation of expression and intracellular distribution of calreticulin, a major calcium binding protein of nonmuscle cells. J Cell Physiol 149: 160–171, 1991

    Google Scholar 

  75. Van PN, Peter F, Söling H-D: Four intracisternal calcium-binding glycoproteins from rat liver microsomes with high affinity for calcium. J Biol Chem 264: 17494–17501, 1989

    Google Scholar 

  76. Rossier MF, Bird GSJ, Putney Jr JW: Subcellular distribution of the calcium-storing inositol 1,4,5-trisphosphate-sensitive organelle in rat liver. Biochem J 274: 643–650, 1991

    Google Scholar 

  77. Baksh S, Michalak M: Expression of calreticulin in Escherichia coli and identification of its Caz+ binding domains. J Biol Chem 266: 21458–21465, 1991

    Google Scholar 

  78. Ostwald TJ, MacLennan DH, Dorrington KJ: Effects of cation binding on the conformation of calsequestrin and the high affinity calcium-binding protein of sarcoplasmic reticulum. J Biol Chem 249: 5867–5871, 1974

    Google Scholar 

  79. Krause K-H, Simmerman HKB, Jones LR, Campbell KP: Sequence similarity of calreticulin with a Ca2+-binding protein that co-purifies with an Ins(1,4,5)P3-sensitive Ca2+ store in HL-60 cells. Biochem J 270: 545–548, 1990

    Google Scholar 

  80. Khanna NC, Tokuda M, Waisman DM: Conformational changes induced by binding of divalent cations to calregulin. J Biol Chem 261: 8883–8887, 1986

    Google Scholar 

  81. Murthy KK, Banville D, Srikant CB, Carrier F, Holmes C, Bell A, Patel YC: Structural homology between the rat calreticulin gene product and the Onchocerca volvulus antigen Ral-1. Nuc Acid Res 18: 4933, 1990

    Google Scholar 

  82. McCauliffe DP, Lux F, Liu TS, San I, Hanke J, Newkirk MM, Bachinski LL, Itch Y, Sicilino MJ, Reichlin M, Sontheimer RD, Capra JD: Molecular cloning, expression and chromosome 19 localization of a human Ro/SS-A auto antigen. J Clin Invest 85: 1379–1391, 1990

    Google Scholar 

  83. Zarain-Herzberg A, Fliegel L, MacLennan DH: Structure of the rabbit fast-twitch skeletal muscle calsequestrin gene. J Biol Chem 263: 4807–4812, 1988

    Google Scholar 

  84. Fujii J, Willard HF, MacLennan DH: Characterization and localization to human chromosome 1 of human fast-twitch skeletal muscle calsequestrin gene. Somatic Cell Mol Genetics 16: 18518, 1990

    Google Scholar 

  85. Khanna NC, Tokuda M, Waisman DM: Comparison of calregulins from vertebrate livers. Biochem J 242: 245–251, 1987

    Google Scholar 

  86. Kulomaa MS, Weigel NL, Kleinsek DA, Beattie WG, Conneely OM, March C, Zarucki-Schulz T, Schrader WT, O'Malley BW: Amino acid sequence of a chicken heat shock protein derived from the complementary DNA nucleotide sequence. Biochemistry 25: 6244–6251, 1986

    Google Scholar 

  87. Mazzarella RA, Green M: ERp99, an abundant, conserved glycoprotein of the endoplasmic reticulum, is homologous to the 90-kDa heat shock protein (hsp 90) and the 94-kDa glucose regulated protein (Grp94). J Biol Chem 262: 8875–8883, 1987

    Google Scholar 

  88. Pelham HRB: Activation of the heat-shock genes in eukaryotes. Trends Genet 1: 31–35, 1985

    Google Scholar 

  89. Munro S, Pelham HRB: An hsp 70-like protein in the ER: Identity with the 78kd glucose-regulated protein and immuno-globulin heavy chain binding protein. Cell 46: 291–300, 1986

    Google Scholar 

  90. Kelly RB: Tracking an elusive receptor. Nature 345: 480–481, 1990

    Google Scholar 

  91. Volpe P, Alderson-Lang BH, Madeddu L, Damiani E, Collins JH, Margreth A: Calsequestrin, a component of the inositol 1,4,5-trisphosphate-sensitive Ca2+ store of chicken cerebellum. Neuron 5: 713–721, 1990

    Google Scholar 

  92. Villa A, Podini P, Clegg DO, Pozzan T, Meldolesi J: Intracellular Ca2+ stores in chicken purkinje neurons: differential distribution of the low affinity-high capacity Ca2+ binding protein, calsequestrin, of Ca2+ ATPase and of the ER lumenal protein, BiP. J Cell Biol 113: 779–791, 1991

    Google Scholar 

  93. McPherson PS, Campbell KP: Solubilization and biochemical characterization of the high affinity [3H]ryanodine receptor from rabbit brain membranes. J Biol Chem 265: 18454–18460, 1990

    Google Scholar 

  94. McPherson PS, Kim YK, Valdivia H, Knudson CM, Takekura H, Franzini-Armstrong C, Coronado R, Campbell KP: The brain ryanodine receptor: a caffeine-sensitive calcium release channel. Neuron 7: 17–25, 1991

    Google Scholar 

  95. Damiani E, Tobaldin G, Volpe P, Margreth A: Quantitation of ryanodine receptor of rabbit skeletal muscle, heart and brain. Biochem Biophys Res Commun 175: 858–865, 1991

    Google Scholar 

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  1. Cardiovascular Disease Research Group, Department of Biochemistry, 417 Heritage Medical Research Center, University of Alberta, T6G 2S2, Edmonton, Alberta, Canada

    Rachel E. Milner, Konrad S. Famulski & Marek Michalak

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  1. Rachel E. Milner
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  2. Konrad S. Famulski
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Milner, R.E., Famulski, K.S. & Michalak, M. Calcium binding proteins in the sarcoplasmic/endoplasmic reticulum of muscle and nonmuscle cells. Mol Cell Biochem 112, 1–13 (1992). https://doi.org/10.1007/BF00229637

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