Calcium cycling proteins in heart failure, cardiomyopathy and arrhythmias

Experimental and Molecular Medicine

Volumn 36, Issue 3, 2004, Pages 193-203

  Minamisawa, Susumu ^a   Sato, Yoji ^b   Cho, Myeong Chan ^c  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

^c Chungbuk National University College of Medicine   (South Korea)

Author keywords

Calcium ATPase; Calcium homeostasis; Cardiomyopathy; Heart failure; Phospholamban; Ryanodine receptor; Sarcoplasmic reticulum

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); CALCIUM BINDING PROTEIN; CALCIUM ION; PHOSPHOLAMBAN; RYANODINE RECEPTOR;

CALCIUM HOMEOSTASIS; CALCIUM MOBILIZATION; CALCIUM SIGNALING; CARDIOMYOPATHY; HEART ARRHYTHMIA; HEART FAILURE; HUMAN; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN EXPRESSION; REVIEW; SARCOPLASMIC RETICULUM; TRANSGENE;

EID: 3242772173     PISSN: 12263613     EISSN: 20926413     Source Type: Journal    
DOI: 10.1038/emm.2004.27     Document Type: Review

References (81)

1. Baker DL, Hashimoto K, Grupp IL, Ji Y, Reed T, Loukianov E, Grupp G, Bhagwhat A, Hoit B, Walsh R, Marban E, Periasamy M. Targeted overexpression of the sarcoplasmic reticulum Ca2+-ATPase increases cardiac contractility in transgenic mouse hearts. Circ Res 1998;83:1205-14
2. Bauce B, Rampazzo A, Basso C, Bagattin A, Daliento L, Tiso N, Turrini P, Thiene G, Danieli GA, Nava A. Screening for ryanodine receptor type 2 mutations in families with effort-induced polymorphic ventricular arrhythmias and sudden death: early diagnosis of asymptomatic carriers. J Am Coll Cardiol 2002;40:341-9
3. Brittsan AG, Carr AN, Schmidt AG, Kranias EG. Maximal inhibition of SERCA2 Ca(2+) affinity by phospholamban in transgenic hearts overexpressing a non-phosphorylatable form of phospholamban. J Biol Chem 2000;275:12129-35
4. Caswell AH, Brandt NR, Brunschwig JP, Purkerson S. Localization and partial characterization of the oligomeric disulfide-linked molecular weight 95,000 protein (triadin) which binds the ryanodine and dihydropyridine receptors in skeletal muscle triadic vesicles. Biochemistry 1991;30:7507-13
5. Chien KR. Genomic circuits and the integrative biology of cardiac diseases. Nature 2000;407:227-32
6. Cho MC, Rapacciuolo A, Koch WJ, Kobayashi Y, Jones LR, Rockman HA. Defective beta-adrenergic receptor signaling precedes the development of dilated cardiomyopathy in transgenic mice with calsequestrin overexpression. J Biol Chem 1999;274:22251-6
7. Cho MC, Choi SY, Kim YH, Kwon JS, Youn TJ, Kim DW, Hong CS, Kim DH. J Am Coll Cardiol 2003;41 (Supplement): 313A
8. Chu G, Li L, Sato Y, Harrer JM, Kadambi VJ, Hoit BD, Bers D, Mand Kranias EG. Pentameric assembly of phospholamban facilitates inhibition of cardiac function in vivo. J Biol Chem 1998;273:33674-80
9. Colyer J. Phosphorylation states of phospholamban. Ann N Y Acad Sci 1998;853:79-91
10. Dash R, Kadambi V, Schmidt AG, Tepe NM, Biniakiewicz D, Gerst MJ, Canning AM, Abraham WT, Hoit BD, Liggett SB, Lorenz JN, Dorn GW, 2nd, Kranias EG. Interactions between phospholamban and beta-adrenergic drive may lead to cardiomyopathy and early mortality. Circulation 2001;103: 889-96
11. del Monte F, Williams E, Lebeche D, Schmidt U, Rosenzweig A, Gwathmey JK, Lewandowski ED, Hajjar RJ. Improvement in survival and cardiac metabolism after gene transfer of sarcoplasmic reticulum Ca(2+)-ATPase in a rat model of heart failure. Circulation 2001;104:1424-9
12. del Monte F, Lebeche D, Guerrero JL, Tsuji T, Doye AA, Gwathmey JK, Hajjar RJ. Abrogation of ventricular arrhythmias in a model of ischemia and reperfusion by targeting myocardial calcium cycling. Proc Natl Acad Sci USA 2004; 101:5622-7
13. Dillmann WH. Calcium regulatory proteins and their alteration by transgenic approaches. Am J Cardiol 1999;83:89H-91H
14. Eizema K, Fechner H, Bezstarosti K, Schneider-Rasp S, van der Laarse A, Wang H, Schultheiss HP, Poller WC, Lamers JM. Adenovirus-based phospholamban antisense expression as a novel approach to improve cardiac contractile dysfunction: comparison of a constitutive viral versus an endothelin-1- responsive cardiac promoter. Circulation 2000;101: 2193-9
15. Frank K, Kranias EG. Phospholamban and cardiac contractility. Ann Med 2000;32:572-8
16. Greene AL, Lalli MJ, Ji Y, Babu GJ, Grupp I, Sussman M, Periasamy M. Overexpression of SERCA2b in the heart leads to an increase in sarcoplasmic reticulum calcium transport function and increased cardiac contractility. J Biol Chem 2000;275:24722-7
17. Haghighi K, Schmidt AG, Hoit BD, Brittsan AG, Yatani A, Lester JW, Zhai J, Kimura Y, Dorn GW 2nd, MacLennan DH, Kranias EG. Superinhibition of sarcoplasmic reticulum function by phospholamban induces cardiac contractile failure. J Biol Chem 2001;276:24145-52
18. Haghighi K, Kolokathis K, Pater L, Lynch RA, Asahi M, Gramolini AO, Fan G, Tsiapras D, Hahn HS, Adamopoulos S, Liggett SB, Dorn II GW, MacLennan DH, Kremastinos DT, Kranias EG. Human phospholamban null results in lethal dilated cardiomyopathy revealing a critical difference between mouse and human. J Clin Invest 2003;111:869-876
19. He H, Giordano FJ, Hilal-Dandan R, Choi DJ, Rockman HA, McDonough PM, Bluhm WF, Meyer M, Sayen MR, Swanson E, Dillmann WH. Overexpression of the rat sarcoplasmic reticulum Ca2+ ATPase gene in the heart of transgenic mice accelerates calcium transients and cardiac relaxation. J Clin Invest 1997:100:380-9
20. He H, Meyer M, Martin JL, McDonough PM, Ho P, Lou X, Lew WY, Hilal-Dandan R, Dillmann WH. Effects of mutant and antisense RNA of phospholamban on SR Ca(2+)-ATPase activity and cardiac myocyte contractility. Circulation 1999;100:974-80
21. Hong CS, Kwak YG, Ji JH, Chae SW, Kim do H. Molecular cloning and characterization of mouse cardiac junctate isoforms. Biochem Biophys Res Commun 2001;289:882-7
22. Hong CS, Cho MC, Kwak YG, Song CH, Lee YH, Lim JS, Kwon YK, Chae SW, Kim do H. Cardiac remodeling and atrial fibrillation in transgenic mice overexpressing junctin. Faseb J 2002;16:1310-2
23. Hoshijima M, Ikeda Y, Iwanaga Y, Minamisawa S, Date MO, Gu Y, Iwatate M, Li M, Wang L, Wilson JM, Wang Y, Ross J Jr, Chien KR. Chronic suppression of heart-failure progression by a pseudophosphorylated mutant of phospholamban via in vivo cardiac rAAV gene delivery. Nat Med 2002;8:864-71
24. Houser SR, Piacentino V 3rd, Weisser J. Abnormalities of calcium cycling in the hypertrophied and failing heart. J Mol Cell Cardiol 2000;32:1595-607
25. Ito K, Komazaki S, Sasamoto K, Yoshida M, Nishi M, Kitamura K, Takeshima H. Deficiency of triad junction and contraction in mutant skeletal muscle lacking junctophilin type 1. J Cell Biol 2001;154:1059-67
26. Iwanaga Y, Hoshijima M, Gu Y, Iwatate M, Dieterle T, Ikeda Y, Date MO, Chrast J, Matsuzaki M, Peterson KL, Chien KR, Ross J Jr. Chronic phospholamban inhibition prevents progressive cardiac dysfunction and pathological remodeling after infarction in rats. J Clin Invest 2004;113:727-36
27. Ji Y, Lalli MJ, Babu GJ, Xu Y, Kirkpatrick DL, Liu LH, Chiamvimonvat N, Walsh RA, Shull GE, Periasamy M. Disruption of a single copy of the SERCA2 gene results in altered Ca2+ homeostasis and cardiomyocyte function. J Biol Chem 2000;275:38073-80
28. Jones LR, Zhang L, Sanborn K, Jorgensen AO and Kelley, J. Purification, primary structure, and immunological characterization of the 26-kDa calsequestrin binding protein (junctin) from cardiac junctional sarcoplasmic reticulum. J Biol Chem 1995;270:30787-96
29. Jones LR, Suzuki YJ, Wang W, Kobayashi YM, Ramesh V, Franzini-Armstrong C, Cleemann Land Morad M. Regulation of Ca2+ signaling in transgenic mouse cardiac myocytes overexpressing calsequestrin. J Clin Invest 1998;101:1385-93
30. Kadambi VJ, Ponniah S, Harrer JM, Hoit BID, Dorn GW 2nd, Walsh RA, Kranias EG. Cardiac-specific overexpression of phospholamban alters calcium kinetics and resultant cardiomyocyte mechanics in transgenic mice. J Clin Invest 1996; 97:533-9
31. Kadambi VJ, Kranias EG. Genetically engineered mice: model systems for left ventricular failure. J Card Fail 1998; 4:349-61
32. Kirchhefer U, Neumann J, Bers DM, Buchwalow IB, Fabritz L, Hanske G, Justus I, Riemann B, Schmitz W, Jones LR. Impaired relaxation in transgenic mice overexpressing junctin. Cardiovasc Res 2003;59:369-79
33. Kirchhefer U, Neumann J, Baba HA, Begrow F, Kobayashi YM, Reinke U, Schmitz W, Jones LR. Cardiac hypertrophy and impaired relaxation in transgenic mice overexpressing triadin 1. J Biol Chem 2001;276:4142-9.
34. Komazaki S, Nishi M, Takeshima H. Abnormal junctional membrane structures in cardiac myocytes expressing ectopic junctophilin type 1. FEBS Lett 2003;542:69-73.
35. Lahat H, Pras E, Olender T, Avidan N, Ben-Asher E, Man O, Levy-Nissenbaum E, Khoury A, Lorber A, Goldman B, Lancet D, Eldar M. A missense mutation in a highly conserved region of CASQ2 is associated with autosomal recessive catecholamine-induced polymorphic ventricular tachycardia in Bedouin families from Israel. Am J Hum Genet 2001;69:1378-84
36. Lahat H, Pras E, Eldar M. RYR2 and CASQ2 mutations in patients suffering from catecholaminergic polymorphic ventricular tachycardia. Circulation 2003;107, e29; author reply e29.
37. Laitinen PJ, Brown KM, Piippo K, Swan H, Devaney JM, Brahmbhatt B, Donarum EA, Marino M, Tiso N, Viitasalo M, Toivonen L, Stephan DA, Kontula K. Mutations of the cardiac ryanodine receptor (RyR2) gene in familial polymorphic ventricular tachycardia. Circulation 2001;103:485-90
38. Leberer E, Timms BG, Campbell KP, MacLennan DH. Purification, calcium binding properties, and ultrastructural localization of the 53,000- and 160,000 (sarcalumenin)-dalton glycoproteins of the sarcoplasmic reticulum. J Biol Chem 1990;265:10118-24
39. Loukianov E, Ji Y, Grupp IL, Kirkpatrick DL, Baker DL, Loukianova T, Grupp G, Lytton J, Walsh RA, Periasamy M. Enhanced myocardial contractility and increased Ca2+ transport function in transgenic hearts expressing the fast-twitch skeletal muscle sarcoplasmic reticulum Ca2+-ATPase. Circ Res 1998;83:889-97
40. Luo W, Grupp IL, Harrer J, Ponniah S, Grupp G, Duffy JJ, Doetschman T, Kranias EG. Targeted ablation of the phospholamban gene is associated with markedly enhanced myocardial contractility and loss of beta-agonist stimulation. Circ Res 1994;75:401-9
41. Marks AR, Marx SO, Reiken S. Regulation of ryanodine receptors via macromolecular complexes: a novel role for leucine/isoleucine zippers. Trends Cardiovasc Med 2002a;12: 166-70
42. Marks AR, Priori S, Memmi M, Kontula K, Laitinen PJ. Involvement of the cardiac ryanodine receptor/calcium release channel in catecholaminergic polymorphic ventricular tachycardia. J Cell Physiol 2002b;190:1-6
43. Martin DW. High efficiency Ca2+ transport by the sarcoplasmic reticulum Ca2(+)-ATPase in the absence of the 53-kilodalton glycoprotein. J Biol Chem 1990;265:20946-51
44. Marx SO, Reiken S, Hisamatsu Y, Jayaraman T, Burkhoff D, Rosemblit N, Marks AR. PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 2000;101: 365-76
45. Meyers MB, Fischer A, Sun YJ, Lopes CM, Rohacs T, Nakamura TY, Zhou YY, Lee PC, Altschuld RA, McCune SA, Coetzee WA, Fishman GI. Sorcin regulates excitation-contraction coupling in the heart. J Biol Chem 2003;278: 28865-71
46. Minamisawa S, Hoshijima M, Chu G, Ward CA, Frank K, Gu Y, Martone ME, Wang Y, Ross J Jr, Kranias EG, Giles WR, Chien KR. Chronic phospholamban- sarcoplasmic reticulum calcium ATPase interaction is the critical calcium cycling defect in dilated cardiomyopathy. Cell 1999;99:313-22
47. Minamisawa S, Sato Y, Tatsuguchi Y, Fujino T, Imamura S, Uetsuka Y, Nakazawa M, Matsuoka R. Mutation of the phospholanbam promoter associated with hypertrophic cardiomyopathy. Biochem Biophys Res Commun 2003a
48. Minamisawa S, Wang Y, Chen J, Ishikawa Y, Chien KR, Matsuoka R. Atrial-chamber specific expression of sarcolipin is regulated during development and hypertrophic remodeling. J Biol Chem 2003b;278:9570-9575
49. Miyamoto MI, del Monte F, Schmidt U, DiSalvo TS, Kang ZB, Matsui T, Guerrero JL, Gwathmey JK, Rosenzweig A, Hajjar RJ. Adenoviral gene transfer of SERCA2a improves left-ventricular function in aortic-banded rats in transition to heart failure. Proc Natl Acad Sci USA 2000;97:793-8
50. Muller FU, Kirchhefer U, Begrow F, Reinke U, Neumann J, Schmitz W. Junctional sarcoplasmic reticulum transmembrane proteins in the heart. Basic Res Cardiol 2002;97 Suppl 1:152-5
51. Nakayama H, Otsu K, Yamaguchi O, Nishida K, Date MO, Hongo K, Kusakari Y, Toyofuku T, Hikoso S, Kashiwase K, Takeda T, Matsumura Y, Kurihara S, Hori M, Tada M. Cardiac-specific overexpression of a high Ca2+ affinity mutant of SERCA2a attenuates in vivo pressure overload cardiac hypertrophy. Faseb J 2003;17:61-3
52. Odermatt A, Becker S, Khanna VK, Kurzydlowski K, Leisner E, Pette D, MacLennan DH. Sarcolipin regulates the activity of SERCA1, the fast-twitch skeletal muscle sarcoplasmic reticulum Ca2+-ATPase. J Biol Chem 1998;273:12360-9
53. Olson EN, Williams RS. Calcineurin signaling and muscle remodeling. Cell 2000;101:689-92
54. Periasamy M, Reed TD, Liu LH, Ji Y, Loukianov E, Paul RJ, Nieman ML, Riddle T, Duffy JJ, Doetschman T, Lorenz JN, Shull GE. Impaired cardiac performance in heterozygous mice with a null mutation in the sarco(endo)plasmic reticulum Ca2+-ATPase isoform 2 (SERCA2) gene. J Biol Chem 1999; 274:2556-62
55. Periasamy M, Huke S. SERCA pump level is a critical determinant of Ca(2+)homeostasis and cardiac contractility. J Mol Cell Cardiol 2001;33:1053-63
56. Postma AV, Denjoy I, Hoorntje TM, Lupoglazoff JM, Da Costa A, Sebillon P, Mannens MM, Wilde AA, Guicheney P. Absence of calsequestrin 2 causes severe forms of catecholaminergic polymorphic ventricular tachycardia. Circ Res 2002;91:e21-6.
57. Prestle J, Janssen PM, Janssen AP, Zeitz O, Lehnart SE, Bruce L, Smith GL, Hasenfuss G. Overexpression of FK506-binding protein FKBP12.6 in cardiomyocytes reduces ryanodine receptor-mediated Ca(2+) leak from the sarcoplasmic reticulum and increases contractility. Circ Res 2001;88:188-94
58. Priori SG, Napolitano C, Memmi M, Colombi B, Drago F, Gasparini M, DeSimone L, Coltorti F, Bloise R, Keegan R, Cruz Filho FE, Vignati G, Benatar A, DeLogu A. Clinical and molecular characterization of patients with catecholaminergic polymorphic ventricular tachycardia. Circulation 2002;106:69-74
59. Sande JB, Sjaastad I, Hoen IB, Bokenes J, Tonnessen T, Holt E, Lunde PK, Christensen G. Reduced level of serine (16) phosphorylated phospholamban in the failing rat myocardium: a major contributor to reduced SERCA2 activity. Cardiovasc Res 2002;53:382-91
60. Sato Y, Ferguson DG, Sako H, Dorn GW 2nd, Kadambi VJ, Yatani A, Hoit BD, Walsh RA, Kranias EG. Cardiac-specific overexpression of mouse cardiac calsequestrin is associated with depressed cardiovascular function and hypertrophy in transgenic mice. J Biol Chem 1998;273:28470-7
61. Schmidt AG, Zhai J, Carr AN, Gerst MJ, Lorenz JN, Pollesello P, Annila A, Hoit BD, Kranias EG. Structural and functional implications of the phospholamban hinge domain: impaired SR Ca2+ uptake as a primary cause of heart failure. Cardiovasc Res 2002;56:248-59
62. Schmidt U, Hajjar RJ, Kim CS, Lebeche D, Doye AA, Gwathmey JK. Human heart failure: cAMP stimulation of SR Ca(2+)-ATPase activity and phosphorylation level of phospholamban. Am J Physiol 1999;277:H474-80
63. Schmitt JP, Kamisago M, Asahi M, Li GH, Ahmad F, Mende U, Kranias EG, MacLennan DH, Seidman JG, Seidman CE. Dilated cardiomyopathy and heart failure caused by a mutation in phospholamban. Science 2003;299:1410-3
64. Scoote M, Williams AJ. The cardiac ryanodine receptor (calcium release channel): emerging role in heart failure and arrhythmia pathogenesis. Cardiovasc Res 2002;56:359-72
65. Seidman JG, Seidman C. The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms. Cell 2001;104:557-67
66. 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 1998;391:489-92
67. Sitsapesan R, Williams AJ. Regulation of current flow through ryanodine receptors by luminal Ca2+. J Membr Biol 1997;159:179-85
68. Takeshima H, Komazaki S, Hirose K, Nishi M, Noda T, Iino M. Embryonic lethality and abnormal cardiac myocytes in mice lacking ryanodine receptor type 2. Embo J 1998;17: 3309-16
69. Takeshima H, Komazaki S, Nishi M, Iino M, Kangawa K. Junctophilins: a novel family of junctional membrane complex proteins. Mol Cell 2000;6:11-22
70. Tiso N, Stephan DA, Nava A, Bagattin A, Devaney JM, Stanchi F, Larderet G, Brahmbhatt B, Brown K, Bauce B, Muriago M, Basso C, Thiene G, Danieli GA, Rampazzo A. Identification of mutations in the cardiac ryanodine receptor gene in families affected with arrhythmogenic right ventricular cardiomyopathy type 2 (ARVD2). Hum Mol Genet 2001;10: 189-94
71. Treves S, Feriotto G, Moccagatta L, Gambari R, Zorzato F. Molecular cloning, expression, functional characterization, chromosomal localization, and gene structure of junctate, a novel integral calcium binding protein of sarco(endo)plasmic reticulum membrane. J Biol Chem 2000;275:39555-68
72. Ver Heyen M, Heymans S, Antoons G, Reed T, Periasamy M, Awede B, Lebacq J, Vangheluwe P, Dewerchin M, Collen D, Sipido K, Carmeliet P, Wuytack F. Replacement of the muscle-specific sarcoplasmic reticulum Ca(2+)-ATPase isoform SERCA2a by the nonmuscle SERCA2b homologue causes mild concentric hypertrophy and impairs contraction-relaxation of the heart. Circ Res 2001;89:838-46
73. Wehrens XH, Lehnart SE, Huang F, Vest JA, Reiken SR, Mohler PJ, Sun J, Guatimosim S, Song LS, Rosemblit N, D'Armiento JM, Napolitano C, Memmi M, Priori SG, Lederer WJ, Marks AR. FKBP12.6 deficiency and defective calcium release channel (ryanodine receptor) function linked to exercise-induced sudden cardiac death. Cell 2003;113:829-40
74. Wehrens XH, Lehnart SE, Reiken SR, Deng SX, Vest JA, Cervantes D, Coromilas J, Landry DW, Marks AR. Protection from cardiac arrhythmia through ryanodine receptor-stabilizing protein calstabin2. Science 2004;304:292-6
75. Wilkins BJ, Molkentin JD. Calcineurin and cardiac hypertrophy: where have we been? Where are we going? J Physiol 2002;541:1-8
76. Xin HB, Senbonmatsu T, Cheng DS, Wang YX, Copello JA, Ji GJ, Collier ML, Deng KY, Jeyakumar LH, Magnuson MA, Inagami T, Kotlikoff MI, Fleischer S. Oestrogen protects FKBP12.6 null mice from cardiac hypertrophy. Nature 2002;416:334-8
77. Yano M, Ono K, Ohkusa T, Suetsugu M, Kohno M, Hisaoka T, Kobayashi S, Hisamatsu Y, Yamamoto T, Noguchi N, Takasawa S, Okamoto H, Matsuzaki M. Altered stoichiometry of FKBP12.6 versus ryanodine receptor as a cause of abnormal Ca(2+) leak through ryanodine receptor in heart failure. Circulation 2000;102:2131-6
78. Yano M, Kobayashi S, Kohno M, Doi M, Tokuhisa T, Okuda S, Suetsugu M, Hisaoka T, Obayashi M, Ohkusa T, Matsuzaki M. FKBP12.6-mediated stabilization of calcium-release channel (ryanodine receptor) as a novel therapeutic strategy against heart failure. Circulation 2003;107:477-84
79. Zhang L, Kelley J, Schmeisser G, Kobayashi YM, Jones LR. Complex formation between junctin, triadin, calsequestrin, and the ryanodine receptor. Proteins of the cardiac junctional sarcoplasmic reticulum membrane. J Biol Chem 1997;272: 23389-97
80. Zhang L, Franzini-Armstrong C, Ramesh V, Jones LR. Structural alterations in cardiac calcium release units resulting from overexpression of junctin. J Mol Cell Cardiol 2001;33: 233-47
81. Zvaritch E, Backx PH, Jirik F, Kimura Y, de Leon S, Schmidt AG, Hoit BD, Lester JW, Kranias EG, MacLennan DH. The transgenic expression of highly inhibitory monomeric forms of phospholamban in mouse heart impairs cardiac contractility. J Biol Chem 2000;275:14985-91