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Endoplasmic reticulum in the heart, a forgotten organelle?

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Abstract

Our hypothesis is that sarcoplasmic and endoplasmic reticulum Ca2+ stores may be functionally distinct compartments in cardiomyocytes. Sarcoplasmic reticulum Ca2+ store is responsible for control of excitation-contraction coupling whereas endoplasmic reticulum compartment may provide Ca2+ for housekeeping and transcriptional functions.

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References

  1. Chien KR, Zhu H, Knowlton KU, Miller-Hance W, van-Bilsen M, O'Brien TX, Evans SM: Transcriptional regulation during cardiac growth and development. Annu Rev Physiol 55: 77–95, 1993

    Google Scholar 

  2. Olson EN, Srivastava D: Molecular pathways controlling heart development. Science 272: 671–676, 1996

    Google Scholar 

  3. Sucov HM: Molecular insights into cardiac development. Annu Rev Physiol 60: 287–308, 1998

    Google Scholar 

  4. Harvey RP: NK-2 homeobox genes and heart development. Dev Biol 178: 203–216, 1996

    Google Scholar 

  5. Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, Robbins J, Grant SR, Olson EN: A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93: 215–228, 1998

    Google Scholar 

  6. Crabtree GR: Generic signals and specific outcomes: Signaling through Ca2+, calcineurin, and NF-AT. Cell 96: 611–614, 1999

    Google Scholar 

  7. Pozzan T, Rizzuto R, Volpe P, Meldolesi J: Molecular and cellular physiology of intracellular calcium stores. Physiol Rev 74: 595–636, 1994

    Google Scholar 

  8. Clapham DE: Calcium signaling. Cell 80: 259–268, 1995

    Google Scholar 

  9. Krause K-H, Michalak M: Calreticulin. Cell 88: 439–443, 1997

    Google Scholar 

  10. Meldolesi J, Pozzan T: The endoplasmic reticulum Ca2+ store: A view from the lumen. TiBS 23: 10–14, 1998

    Google Scholar 

  11. Mesaeli N, Nakamura K, Zvaritch E, Dickie P, Dziak E, Krause K-H, Opas M, MacLennan DH, Michalak M: Calreticulin is essential for cardiac development. J Cell Biol 144: 857–868, 1999

    Google Scholar 

  12. Rauch F, Prud'homme J, Arabian A, Dedhar S, St-Arnaud R: Heart, brain, and body wall defects in mice lacking calreticulin. Exp Cell Res 256: 105–111, 2000

    Google Scholar 

  13. Michalak M, Corbett EF, Mesaeli N, Nakamura K, Opas M: Calreticulin: One protein, one gene, many functions. Biochem J 344: 281–292, 1999

    Google Scholar 

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

    Google Scholar 

  15. Fliegel L, Burns K, Opas M, Michalak M: The high-affinity calcium binding protein of sarcoplasmic reticulum. Tissue distribution, and homology with calregulin. Biochim Biophys Acta 982: 1–8, 1989

    Google Scholar 

  16. 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 

  17. Tharin S, Hamel PA, Conway EM, Michalak M, Opas M: Regulation of calcium binding proteins calreticulin and calsequestrin during differentiation in the myogenic cell line L6. J Cell Physiol 166: 547–560, 1996

    Google Scholar 

  18. Bergeron JJM, Brenner MB, Thomas DY, Williams DB: Calnexin: A membrane-bound chaperone of the endoplasmic reticulum. TiBS 19: 124–128, 1994

    Google Scholar 

  19. Helenius A, Trombetta ES, Hebert DN, Simons JF: Calnexin, calreticulin and the folding of glycoproteins. Trends Cell Biol 7: 193–200, 1997

    Google Scholar 

  20. Bastianutto C, Clementi E, Codazzi F, Podini P, De Giorgi F, Rizzuto R, Meldolesi J, Pozzan T: Overexpression of calreticulin increases the Ca2+ capacity of rapidly exchanging Ca2+ stores and reveals aspects of their lumenal microenvironment and function. J Cell Biol 130: 847–855, 1995

    Google Scholar 

  21. Mery L, Mesaeli N, Michalak M, Opas M, Lew DP, Krause K-H: Overexpression of calreticulin increases intracellular Ca2+ storage and decreases store-operated Ca2+ influx. J Biol Chem 271: 9332–9339, 1996

    Google Scholar 

  22. Fasolato C, Pizzo P, Pozzan T: Delayed activation of the store-operated calcium current induced by calreticulin overexpression in RBL-1 cells. Mol Biol Cell 9: 1513–1522, 1998

    Google Scholar 

  23. Camacho P, Lechleiter JD: Calreticulin inhibits repetitive intracellular Ca2+ waves. Cell 82: 765–771, 1995

    Google Scholar 

  24. John LM, Lechleiter JD, Camacho P: Differential modulation of SERCA2 isoforms by calreticulin. J Cell Biol 142: 963–973, 1998

    Google Scholar 

  25. Coppolino MG, Woodside MJ, Demaurex N, Grinstein S, St-Arnaud R, Dedhar S: Calreticulin is essential for integrin-mediated calcium signalling and cell adhesion. Nature 386: 843–847, 1997

    Google Scholar 

  26. Imanaka-Yoshida K, Amitani A, Ioshii SO, Koyabu S, Yamakado T, Yoshida T: Alterations of expression and distribution of the Ca2+-storing proteins in endo/sarcoplasmic reticulum during differentiation of rat cardiomyocytes. J Mol Cell Cardiol 28: 553–562, 1996

    Google Scholar 

  27. Barnes JA, Smoak IW: Immunolocalization and heart levels of GRP94 in the mouse during post-implantation development. Anat Embryol 196: 335–341, 1997

    Google Scholar 

  28. Vitadello M, Colpo P, Gorza L: Rabbit cardiac and skeletal myocytes differ in constitutive and inducible expression of the glucose-regulated protein GRP94. Biochem J 332: 351–359, 1998

    Google Scholar 

  29. Sussman MA, Lim HW, Gude N, Taigen T, Olson EN, Robbins J, Colbert MC, Gualberto A, Wieczorek DF, Molkentin JD: Prevention of cardiac hypertrophy in mice by calcineurin inhibition. Science 281: 1690–1693, 1998

    Google Scholar 

  30. Nolan GP: Cardiac development. Transcription and the broken heart. Nature 392: 129–130, 1998

    Google Scholar 

  31. Thibault G, Amiri F, Garcia R: Regulation of natriuretic peptide secretion by the heart. Annu Rev Physiol 61: 193–217, 1999

    Google Scholar 

  32. Sutko JL, Airey JA: Ryanodine receptor Ca2+ release channels: Does diversity in form equal diversity in function? Physiol Rev 76: 1027–1071, 1996

    Google Scholar 

  33. 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 

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

    Google Scholar 

  35. Cala SE, Ulbright C, Kelley JS, Jones LR: Purification of a 90-kDa protein (Band VII) from cardiac sarcoplasmic reticulum. Identification as calnexin and localization of casein kinase II phosphorylation sites. J Biol Chem 268: 2969–2975, 1993

    Google Scholar 

  36. Villa A, Podini P, Panzeri MC, Söling H-D, Volpe P, Meldolesi J: The endoplasmic-sarcoplasmic reticulum of smooth muscle: Immunocytochemistry of vas deferens fibers reveals specialized subcompartments differently equipped for the control of Ca2+ homeostasis. J Cell Biol 121: 1041–1051, 1993

    Google Scholar 

  37. Volpe P, Villa A, Podini P, Martini A, Nori A, Panzeri MC, Meldolesi J: The endoplasmic reticulum-sarcoplasmic reticulum connection: Distribution of endoplasmic reticulum markers in the sarcoplasmic reticulum of skeletal muscle fibers. Proc Natl Acad Sci USA 89: 6142–6146, 1992

    Google Scholar 

  38. Cala SE, Jones LR: GRP94 resides within cardiac sarcoplasmic reticulum vesicles and is phosphorylated by casein kinase II. J Biol Chem 269: 5926–5931, 1994

    Google Scholar 

  39. Franzini-Armstrong C, Jorgensen AO: Structure and development of E-C coupling units in skeletal muscle. Annu Rev Physiol 56: 509–534, 1994

    Google Scholar 

  40. Flucher BE, Franzini-Armstrong C: Formation of junctions involved in excitation-contraction coupling in skeletal and cardiac muscle. Proc Natl Acad Sci USA 93: 8101–8106, 1996

    Google Scholar 

  41. Jaconi M, Bony C, Richards SM, Terzic A, Arnaudeau S, Vassort G, Puceat M: Inositol 1,4,5-trisphosphate directs Ca2+ flow between mitochondria and the endoplasmic/sarcoplasmic reticulum: A role in regulating cardiac autonomic Ca2+ spiking. Mol Biol Cell 11: 1845–1858, 2000

    Google Scholar 

  42. Lipp P, Laine M, Tovey SC, Burrell KM, Berridge MJ, Li W, Bootman MD: Functional InsP3 receptors that may modulate excitation-contraction coupling in the heart. Curr Biol 10: 939–942, 2000

    Google Scholar 

  43. Jayaraman T, Brillantes AM, Timerman AP, Fleischer S, Erdjument-Bromage H, Tempst P, Mark AR: FK506 binding protein associated with the calcium release channel (ryanodine receptor). J Biol Chem 267: 9474–9477, 1992

    Google Scholar 

  44. Brillantes AB, Ondrias K, Scott A, Kobrinsky E, Ondriasova E, Moschella MC, Jayaraman T, Landers M, Ehrlich BE, Marks AR: Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77: 513–523, 1994

    Google Scholar 

  45. Cameron AM, Steiner JP, Sabatini DM, Kaplin AI, Walensky LD, Snyder SH: Immunophilin FK506 binding protein associated with inositol 1,4,5-trisphosphate receptor modulates calcium flux. Proc Natl Acad Sci USA 92: 1784–1788, 1995

    Google Scholar 

  46. McCall E, Li L, Satoh H, Shannon TR, Blatter LA, Bers DM: Effects of FK-506 on contraction and Ca2+ transients in rat cardiac myocytes. Circ Res 79: 1110–1121, 1996

    Google Scholar 

  47. Cameron AM, Nucifora FC Jr, Fung ET, Livingston DJ, Aldape RA, Ross CA, Snyder SH: FKBP12 binds the inositol 1,4,5-trisphosphate receptor at leucine-proline (1400-1401) and anchors calcineurin to this FK506-like domain. J Biol Chem 272: 27582–27588, 1997

    Google Scholar 

  48. Shou W, Aghdasi B, Armstrong DL, Guo Q, Bao S, Charng MJ, Mathews LM, Schneider MD, Hamilton SL, Matzuk MM: Cardiac defects and altered ryanodine receptor function in mice lacking FKBP12. Nature 391: 489–492, 1998

    Google Scholar 

  49. Burns K, Helgason CD, Bleackley RC, Michalak M: Calreticulin in Tlymphocytes. Identification of calreticulin in T-lymphocytes and demonstration that activation of T cells correlates with increased levels of calreticulin mRNA and protein. J Biol Chem 267: 19039–19042, 1992

    Google Scholar 

  50. Dupuis M, Schaerer E, Krause K-H, Tschopp J: The calcium-binding protein calreticulin is a major constituent of lytic granules in cytolytic T lymphocytes. J Exp Med 177: 1–7, 1993

    Google Scholar 

  51. Andrin C, Pinkoski MJ, Burns K, Atkinson EA, Krahenbuhl O, Hudig D, Fraser SA, Winkler U, Tschopp J, Opas M, Bleackley RC, Michalak M: Interaction between a Ca2+-binding protein calreticulin and perforin, a component of the cytotoxic T-cell granules. Biochemistry 37: 10386–10394, 1998

    Google Scholar 

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Correspondence to Marek Michalak.

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Mesaeli, N., Nakamura, K., Opas, M. et al. Endoplasmic reticulum in the heart, a forgotten organelle?. Mol Cell Biochem 225, 1–6 (2001). https://doi.org/10.1023/A:1012209923231

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