Phospholamban interactome in cardiac contractility and survival: A new vision of an old friend

Journal of Molecular and Cellular Cardiology

Volumn 77, Issue , 2014, Pages 160-167

  Haghighi, Kobra ^a   Bidwell, Philip ^a   Kranias, Evangelia G ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Calcium; Contractility; Heart failure; Human variants; Phospholamban; Sarcoplasmic reticulum

Indexed keywords

4 AMINO 7 TERT BUTYL 5 (4 METHYLPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; CALCIUM BINDING PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; HEAT SHOCK PROTEIN 20; HISTIDINE RICH CALCIUM BINDING PROTEIN; MITOCHONDRIAL PROTEIN; PHOSPHOLAMBAN; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN HAX1; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE 2A; UNCLASSIFIED DRUG; CALCIUM;

BINDING AFFINITY; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CARDIOVASCULAR RESPONSE; CELL DEATH; CELL SURVIVAL; CONGESTIVE CARDIOMYOPATHY; DOWN REGULATION; ENZYME ACTIVITY; GENE; GENETIC VARIABILITY; HEART FAILURE; HEART FUNCTION; HEART INFARCTION SIZE; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; NONHUMAN; PATHOGENESIS; PLN GENE; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; REVIEW; SERCA2A GENE; SUMOYLATION; ANIMAL; EXCITATION CONTRACTION COUPLING; HEART CONTRACTION; HUMAN; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROTEIN PROTEIN INTERACTION; SARCOPLASMIC RETICULUM;

ANIMALS; CALCIUM; CALCIUM-BINDING PROTEINS; CELL SURVIVAL; EXCITATION CONTRACTION COUPLING; HEART FAILURE; HUMANS; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PROTEIN INTERACTION MAPS; SARCOPLASMIC RETICULUM;

EID: 84910093555     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.10.005     Document Type: Review

References (74)

1. Kranias E.G., Hajjar R.J. Modulation of cardiac contractility by the phospholamban/SERCA2a regulatome. Circ Res 2012, 110:1646-1660.
2. Steenaart N.A., Ganim J.R., Di Salvo J., Kranias E.G. The phospholamban phosphatase associated with cardiac sarcoplasmic reticulum is a type 1 enzyme. Arch Biochem Biophys 1992, 293(1):17-24.
3. Carr A.N., Schmidt A.G., Suzuki Y., del Monte F., Sato Y., Lanner C., et al. Type 1 phosphatase, a negative regulator of cardiac function. Mol Cell Biol 2002, 22(12):4124-4135.
4. Pathak A., del Monte F., Zhao W., Shultz J.E., Lorenz J.N., Bodi I., et al. Enhancement of cardiac function and suppression of heart failure progression by inhibition of protein phosphatase 1. Circ Res 2005, 96(7):756-766.
5. Zhao W., Waggoner J.R., Zhang Z.G., Lam C.K., Han P., Qian J., et al. The anti-apoptotic protein HAX-1 is a regulator of cardiac function. Proc Natl Acad Sci 2009, 106(49):20776-20781.
6. 2+-ATPase. Am J Physiol Heart Circ Physiol 2007, 293:H1581-H1589.
7. 2+-cycling and severe pathology under pressure-overload stress. Basic Res Cardiol 2013, 108(3):344.
8. Vafiadaki E., Arvanitis D.A., Sanoudou D., Kranias E.G. Identification of a protein phosphatase 1/phospholamban interactome that is regulated by cAMP-dependent phosphorylation. PLoS ONE 2013, 8(11):e80867.
9. Meyer M., Schillinger W., Pieske B., Holubarsch C., Heilmann C., Posival H., et al. Alterations of sarcoplasmic reticulum proteins in failing human dilated cardiomyopathy. Circulation 1995, 92:778-784.
10. 2+ ATPase gene in the heart of transgenic mice accelerates calcium transients and cardiac relaxation. J Clin Invest 1997, 100:380-389.
11. 2+ homeostasis and cardiomyocyte function. J Biol Chem 2000, 275:38073-38080.
12. Anderson K.B., Birkeland J.A.K., Finsen A.V., Louch W.E., Sjaastad I., Wang Y., et al. Moderate heart dysfunction in mice with inducible cardiomyocyte-specific excision of the Serca2 gene. J Mol Cell Cardiol 2009, 47:180-187.
13. Heinis F.I., Andersson K.B., Christensen G., Metzger J.M. Prominent heart organ-level performance deficits in a genetic model of targeted severe and progressive SERCA2 deficiency. PLoS ONE 2013, 8(11):e79609.
14. Louch W.E., Hougen K., Mørk H.K., Swift F., Aronsen J.M., Sjaastad I., et al. Sodium accumulation promotes diastolic dysfunction in end-stage heart failure following Serca2 knockout. J Physiol 2010, 588:465-478.
15. 2+-handling in failing human myocardium. J Mol Cell Cardiol 2001, 33(7):1345-1353.
16. 2+-ATPase in a rat model of heart. Circulation 2001, 104:1424-1429.
17. Kawase Y., Ly H.Q., Prunier F., Lebeche D., Shi Y., Jin H., et al. Reversal of cardiac dysfunction after long-term expression of SERCA2a by gene transfer in a pre-clinical model of heart failure. J Am Coll Cardiol 2008, 51:1112-1119.
18. 2+-ATPase in patients with advanced heart failure. Circulation 2011, 124:304-313.
19. Zsebo K.M., Yaroshinsky A., Rudy J.J., Wagner K., Greenberg B., Jessup M., et al. Long-term effects of AAV1/SERCA2a gene transfer in patients with severe heart failure: analysis of recurrent cardiovascular events and mortality. Circ Res 2014, 114:101-108.
20. Jaski B.E., Jessup M.L., Mancini D.M., Cappola T.P., Pauly D.F., Greenberg B., et al. Calcium upregulation by percutaneous administration of gene therapy in cardiac disease (CUPID trial), a first-in-human phase 1/2 clinical trial. J Card Fail 2009, 15:171-181.
21. Kho C., Lee A., Jeong D., Oh J.G., Chaanine A.H., Kizana E., et al. SUMO1-dependent modulation of SERCA2a in heart failure. Nature 2011, 477(7366):601-605.
22. Tilemann L., Lee A., Ishikawa K., Aguero J., Rapti K., Santos-Gallego C., et al. SUMO-1 gene transfer improves cardiac function in a large-animal model of heart failure. Sci Transl Med 2013, 5:211ra159.
23. MacLennan D.H., Kimura Y., Toyofuku T. Sites of regulatory interaction between calcium ATPases and phospholamban. Ann N Y Acad Sci 1998, 853:31-42.
24. 2+ pump in cardiac sarcoplasmic reticulum to probe spatial and functional interactions within the transmembrane domain. J Biol Chem 2006, 281(20):14163-14172.
25. 2+-ATPase by protein kinase A and by anti-phospholamban monoclonal antibody 2D12. J Biol Chem 2007, 282(29):20968-20976.
26. Hou Z., Kelly E.M., Robia S.L. Phosphomimetic mutations increase phospholamban oligomerization and alter the structure of its regulatory complex. J Biol Chem 2008, 283(43):28996-29003.
27. Pallikkuth S., Blackwell D.J., Hu Z., Hou Z., Zieman D.T., Svensson B., et al. Phosphorylated phospholamban stabilizes a compact conformation of the cardiac calcium-ATPase. Biophys J 2013, 105(8):1812-1821.
28. Glaves J.P., Trieber C.A., Ceholski D.K., Stokes D.L., Young H.S. Phosphorylation and mutation of phospholamban alter physical interactions with the sarcoplasmic reticulum calcium pump. J Mol Biol 2011, 405(3):707-723.
29. Kadambi V.J., Ponniah S., Harrer J.M., Hoit B.D., Dorn G.W., Walsh R.A., et al. Cardiac-specific overexpression of phospholamban alters calcium kinetics and resultant cardiomyocyte mechanics in transgenic mice. J Clin Invest 1996, 97:533-539.
30. Luo W., Grupp I.L., Harrer J., Ponniah S., Grupp G., Duffy J.J., et al. Targeted ablation of the phospholamban gene is associated with markedly enhanced myocardial contractility and loss of beta-agonist stimulation. Circ Res 1994, 75:401-409.
31. Slack J.P., Grupp I.L., Dash R., Holder D., Schmidt A., Gerst M.J., et al. The enhanced contractility of the phospholamban-deficient mouse heart persists with aging. J Mol Cell Cardiol 2001, 33:1031-1040.
32. Lorenz J.N., Kranias E.G. Regulatory effects of phospholamban on cardiac function in intact mice. Am J Physiol 1997, 273:H2826-H2831.
33. del Monte F., Harding S.E., Dec G.W., Gwathmey J.K., Hajjar R.J. Targeting phospholamban by gene transfer in human heart failure. Circulation 2002, 105:904-907.
34. 2+ affinity by phospholamban in transgenic hearts overexpressing a non-phosphorylatable form of phospholamban. J Biol Chem 2000, 275:12129-12135.
35. Ziolo M.T., Martin J.L., Bossuyt J., Bers D.M., Pogwizs S.M. Adenoviral gene transfer of mutant phospholamban rescues contractile dysfunction in failing rabbit myocytes with relatively preserved SERCA function. Circ Res 2005, 96:815-817.
36. Schmitt J.P., Kamisago M., Asahi M., Li G.H., Ahmad F., Mende U., et al. Dilated cardiomyopathy and heart failure caused by a mutation in phospholamban. Science 2003, 299(5611):1410-1413.
37. Haghighi K., Kolokathis F., Pater L., Lynch R.A., Asahi M., Gramolini A.O., et al. Human phospholamban null results in lethal dilated cardiomyopathy revealing a critical difference between mouse and human. J Clin Invest 2003, 111:869-876.
38. Haghighi K., Kolokathis F., Gramolini A.O., Waggoner J.R., Pater L., Lynch R.A., et al. A mutation in the human phospholamban gene, deleting arginine 14, results in lethal, hereditary cardiomyopathy. Proc Natl Acad Sci U S A 2006, 103:1388-1393.
39. Medeiros A., Biagi D.G., Sobreira T.J., de Oliveira P.S., Negrao C.E., Mansur A.J., et al. Mutations in the human phospholamban gene in patients with heart failure. Am Heart J 2011, 162:1088-1095.
40. van der Zwaag P.A., van Rijsingen I.A., Asimaki A., Jongbloed J.D., van Veldhuisen D.J., Wiesfeld A.C., et al. Phospholamban R14del mutation in patients diagnosed with dilated cardiomyopathy or arrhythmogenic right ventricular cardiomyopathy: evidence supporting the concept of arrhythmogenic cardiomyopathy. Eur J Heart Fail 2012, 14(11):1199-1207.
41. Haghighi K., Pritchard T., Bossuyt J., Waggoner J.R., Yuan Q., Fan G.C., et al. The human phospholamban Arg14-deletion mutant localizes to plasma membrane and interacts with the Na/K-ATPase. J Mol Cell Cardiol 2012, 52(3):773-782.
42. Minamisawa S., Sato Y., Tatsuguchi Y., Fujino T., Imamura S., Uetsuka Y., et al. Mutation of the phospholamban promoter associated with hypertrophic cardiomyopathy. Biochem Biophys Res Commun 2003, 304:1-4.
43. Haghighi K., Chen G., Sato Y., Fan G.C., He S., Kolokathis F., et al. A human phospholamban promoter polymorphism in dilated cardiomyopathy alters transcriptional regulation by glucocorticoids. Hum Mutat 2008, 29:640-647.
44. Medin M., Hermida-Prieto M., Monserrat L., Laredo R., Rodriguez-Rey J.C., Fernandez X., et al. Mutational screening of phospholamban gene in hypertrophic and idiopathic dilated cardiomyopathy and functional study of the PLN -42 C>G mutation. Eur J Heart Fail 2007, 9:37-43.
45. Vafiadaki E., Sanoudou D., Arvanitis D.A., Catino D.H., Kranias E.G., Kontrogianni-Konstantopoulos A. Phospholamban interacts with HAX-1, a mitochondrial protein with anti-apoptotic function. J Mol Biol 2007, 367:65-79.
46. Chao J.R., Parganas E., Boyd K., Hong C.Y., Opferman J.T., Ihle J.N. Hax1-mediated processing of HtrA2 by Parl allows survival of lymphocytes and neurons. Nature 2008, 452(7183):98-102.
47. Lam C.K., Zhao W., Cai W., Vafiadaki E., Zhang Z., Ren X., et al. Novel role of HAX-1 in ischemic injury protection: involvement of Hsp90. Circ Res 2013, 112(1):79-89.
48. Neumann J., Eschenhagen T., Jones L.R., Linck B., Schmitz W., Scholz H., et al. Increased expression of cardiac phosphatases in patients with end-stage heart failure. J Mol Cell Cardiol 1997, 29(1):265-272.
49. Huang F.L., Glinsmann W.H. Separation and characterization of two phosphorylase phosphatase inhibitors from rabbit skeletal muscle. Eur J Biochem 1976, 70:419-426.
50. Picking W.D., Kudlicki W., Kramer G., Hardesty B., Vandenheede J.R., Merlvede W., et al. Fluorescence studies on the interaction of inhibitor 2 and okadaic acid with the catalytic subunit of type 1 phosphoprotein phosphatases. Biochemistry 1991, 30:10280-10287.
51. Sakashita G., Shima H., Komatsu M., Urano T., Kikuchi A., Kikuchi K. Regulation of type 1 protein phosphatase/inhibitor-2 complex by glycogen synthase kinase-3beta in intact cells. J Biochem 2003, 133:165-171.
52. Kirchhefer U., Baba H.A., Boknik P., Breeden K.M., Mavila N., Bruchert N., et al. Enhanced cardiac function in mice overexpressing protein phosphatase inhibitor-2. Cardiovasc Res 2005, 68:98-108.
53. Yamada M., Ikeda Y., Yano M., Yoshimura K., Nishino S., Aoyama H., et al. Inhibition of protein phosphatase 1 by inhibitor-2 gene delivery ameliorates heart failure progression in genetic cardiomyopathy. FASEB J 2006, 20(8):1197-1199.
54. El-Armouche A., Bednorz A., Pamminger T., Ditz D., Didie M., Dobrev D., et al. Role of calcineurin and protein phosphatase-2A in the regulation of phosphatase inhibitor-1 in cardiac myocytes. Biochem Biophys Res Commun 2006, 346(3):700-706.
55. Rodriguez P., Mitton B., Nicolaou P., Chen G., Kranias E.G. Phosphorylation of human inhibitor-1 at Ser67 and/or Thr75 attenuates stimulatory effects of protein kinase A signaling in cardiac myocytes. Am J Physiol Heart Circ Physiol 2007, 293(1):H762-H769.
56. Nicolaou P., Rodriguez P., Ren X., Zhou X., Qian J., Sadayappan S., et al. Inducible expression of active protein phosphatase-1 inhibitor-1 enhances basal cardiac function and protects against ischemia/reperfusion injury. Circ Res 2009, 104:1012-1020.
57. Pritchard T.J., Kawase Y., Haghighi K., Anjak A., Cai W., Jiang M., et al. Active inhibitor-1 maintains protein hyper-phosphorylation in aging hearts and halts remodeling in failing hearts. PLoS ONE 2013, 8(12):e80717.
58. Fish K.M., Ladage D., Kawase Y., Karakikes I., Jeong D., Ly H., et al. AAV9.I-1c delivered via direct coronary infusion in a porcine model of heart failure improves contractility and mitigates adverse remodeling. Circ Heart Fail 2013, 6:310-317.
59. Chen G., Zhou X., Nicolaou P., Rodriguez P., Song G., Mitton B., et al. A human polymorphism of protein phosphatase-1 inhibitor-1 is associated with attenuated contractile response of cardiomyocytes to beta-adrenergic stimulation. FASEB J 2008, 22(6):1790-1796.
60. Chu G., Egnaczyk G.F., Zhao W., Jo S.H., Fan G.C., Maggio J.E., et al. Phosphoproteome analysis of cardiomyocytes subjected to beta-adrenergic stimulation: identification and characterization of a cardiac heat shock protein p20. Circ Res 2004, 94(2):184-193.
61. Fan G.C., Ren X., Qian J., Yuan Q., Nicolaou P., Wang Y., et al. Novel cardioprotective role of a small heat-shock protein, Hsp20, against ischemia/reperfusion injury. Circulation 2005, 111(14):1792-1799.
62. Dreiza C.M., Komalavilas P., Furnish E.J., Flynn C.R., Sheller M.R., Smoke C.C., et al. The small heat shock protein, HSPB6, in muscle function and disease. Cell Stress Chaperones 2010, 15(1):1-11.
63. Qian J., Vafiadaki E., Florea S.M., Singh V.P., Song W., Lam C.K., et al. Small heat shock protein 20 interacts with protein phosphatase-1 and enhances sarcoplasmic reticulum calcium cycling. Circ Res 2011, 108:1429-1438.
64. Fan G.C., Chu G., Kranias E.G. Hsp20 and its cardioprotection. Trends Cardiovasc Med 2005, 15(4):138-141.
65. Qian J., Ren X., Wang X., Zhang P., Jones W.K., Molkentin J.D., et al. Blockade of Hsp20 phosphorylation exacerbates cardiac ischemia/reperfusion injury by suppressed autophagy and increased cell death. Circ Res 2009, 105(12):1223-1231.
66. Nicolaou P., Knöll R., Haghighi K., Fan G.C., Dorn G.W., Hasenfub G., et al. Human mutation in the anti-apoptotic heat shock protein 20 abrogates its cardioprotective effects. J Biol Chem 2008, 283(48):33465-33471.
67. 2+-binding protein of sarcoplasmic reticulum that contains highly conserved repeated elements. J Biol Chem 1989, 264:18083-18090.
68. 2+-binding protein at the triadic junction in skeletal muscle fibers. J Muscle Res Cell Motil 1999, 20(4):403-415.
69. Zhang L., Kelley J., Schmeisser G., Kobayashi Y.M., Jones L.R. Complex formation between junctin, triadin, calsequestrin, and the ryanodine receptor. Proteins of the cardiac junctional sarcoplasmic reticulum membrane. J Biol Chem 1997, 272:23389-23397.
70. 2+-binding protein) and triadin in the lumen of sarcoplasmic reticulum. J Biol Chem 2001, 276:39533-39538.
71. Gyorke I., Hester N., Jones L.R., Gyorke S. The role of calsequestrin, triadin, and junctin in conferring cardiac ryanodine receptor responsiveness to luminal calcium. Biophys J 2004, 86:2121-2128.
72. Gregory K.N., Ginsburg K.S., Bodi I., Hahn H., Marreez Y.M., Song Q., et al. Histidine-rich Ca binding protein: a regulator of sarcoplasmic reticulum calcium sequestration and cardiac function. J Mol Cell Cardiol 2006, 40(5):653-665.
73. Arvanitis D.A., Sanoudou D., Kolokathis F., Vafiadaki E., Papalouka V., Kontrogianni-Konstantopoulos A., et al. The Ser96Ala variant in histidine-rich calcium-binding protein is associated with life-threatening ventricular arrhythmias in idiopathic dilated cardiomyopathy. Eur Heart J 2008, 29(20):2514-2525.
74. Singh V.P., Arvanitis D.A., Ren X., Gao X., Haghighi K., Gilbert M., et al. Abnormal calcium cycling and cardiac arrhythmias associated with the human Ser96Ala genetic variant of histidine-rich calcium-binding protein. J Am Heart Assoc 2013, 2(5):e000460.