Ablation of phospholamban and sarcolipin results in cardiac hypertrophy and decreased cardiac contractility

Cardiovascular Research

Volumn 89, Issue 2, 2011, Pages 353-361

  Shanmugam, Mayilvahanan ^a   Gao, Shumin ^a   Hong, Chull ^a   Fefelova, Nadezhda ^a   Nowycky, Martha C ^a   Xie, Lai Hua ^a   Periasamy, Muthu ^b   Babu, Gopal J ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Aortic banding; Calcium; Calcium transient; Cardiac function; Double knockout; Phospholamban; Sarcolipin; SERCA

Indexed keywords

ALPHA ACTIN; CALCIUM; PHOSPHOLAMBAN; REGULATOR PROTEIN; SARCOLIPIN; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; UNCLASSIFIED DRUG;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; ECHOCARDIOGRAPHY; HEART FAILURE; HEART FUNCTION; HEART MUSCLE CONTRACTILITY; HEART VENTRICLE HYPERTROPHY; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL;

AGE FACTORS; AGING; ANIMALS; AORTA; CALCIUM; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; CARDIOMEGALY; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION REGULATION; LIGATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE PROTEINS; MYOCARDIAL CONTRACTION; MYOCARDIUM; PROTEOLIPIDS; SARCOPLASMIC RETICULUM; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; STROKE VOLUME; VENTRICULAR FUNCTION, LEFT;

EID: 78751532739     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvq294     Document Type: Article

References (42)

1. MacLennan DH, Kranias EG. Phospholamban: a crucial regulator of cardiac contractility. Nat Rev Mol Cell Biol 2003;4:566-577.
2. Bhupathy P, Babu GJ, Periasamy M. Sarcolipin and phospholamban as regulators of cardiac sarcoplasmic reticulum Ca2+ ATPase. J Mol Cell Cardiol 2007;42:903-911.
3. Periasamy M, Bhupathy P, Babu GJ. Regulation of sarcoplasmic reticulum Ca2+ ATPase pump expression and its relevance to cardiac muscle physiology and pathology. Cardiovasc Res 2008; 77:265-273.
4. Inesi G, Prasad AM, Pilankatta R. The Ca2+ ATPase of cardiac sarcoplasmic reticulum: Physiological role and relevance to diseases. Biochem Biophys Res Commun 2008;369:182-187.
5. Arai M, Alpert NR, MacLennan DH, Barton P, Periasamy M. Alterations in sarcoplasmic reticulum gene expression in human heart failure. A possible mechanism for alterations in systolic and diastolic properties of the failing myocardium. Circ Res 1993;72:463-469.
6. Frank KF, Bolck B, Brixius K, Kranias EG, Schwinger RH. Modulation of SERCA: implications for the failing human heart. Basic Res Cardiol 2002;97 Suppl 1:I72-I78.
7. 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 2003;278:9570-9575.
8. Uemura N, Ohkusa T, Hamano K, Nakagome M, Hori H, Shimizu M et al. Down-regulation of sarcolipin mRNA expression in chronic atrial fibrillation. Eur J Clin Invest 2004;34:723-730.
9. Belke DD, Dillmann WH. Altered cardiac calcium handling in diabetes. Curr Hypertens Rep 2004;6:424-429.
10. Babu GJ, Bhupathy P, Carnes CA, Billman GE, Periasamy M. Differential expression of sarcolipin protein during muscle development and cardiac pathophysiology. J Mol Cell Cardiol 2007;43: 215-222.
11. del Monte F, Harding SE, Schmidt U, Matsui T, Kang ZB, Dec GW et al. Restoration of contractile function in isolated cardiomyocytes from failing human hearts by gene transfer of SERCA2a. Circulation 1999;100:2308-2311.
12. Ito K, Yan X, Feng X, Manning WJ, Dillmann WH, Lorell BH. Transgenic expression of sarcoplasmic reticulum Ca2+ ATPase modifies the transition from hypertrophy to early heart failure. Circ Res 2001;89:422-429.
13. Trost SU, Belke DD, Bluhm WF, Meyer M, Swanson E, Dillmann WH. Overexpression of the sarcoplasmic reticulum Ca2+-ATPase improves myocardial contractility in diabetic cardiomyopathy. Diabetes 2002;51:1166-1171.
14. Kawase Y, Hajjar RJ. The cardiac sarcoplasmic/endoplasmic reticulum calcium ATPase: a potent target for cardiovascular diseases. Nat Clin Pract Cardiovasc Med 2008;5:554-565.
15. Byrne MJ, Power JM, Preovolos A, Mariani JA, Hajjar RJ, Kaye DM. Recirculating cardiac delivery of AAV2/1SERCA2a improves myocardial function in an experimental model of heart failure in large animals. Gene Ther 2008;15:1550-1557.
16. Suarez J, Hu Y, Makino A, Fricovsky E, Wang H, Dillmann WH. Alterations in mitochondrial function and cytosolic calcium induced by hyperglycemia are restored by mitochondrial transcription factorA in cardiomyocytes. Am J Physiol Cell Physiol 2008;295:C1561-C1568.
17. Kaye DM, Hoshijima M, Chien KR. Reversing advanced heart failure by targeting Ca2+ cycling. Annu Rev Med 2008;59:13-28.
18. del Monte F, Harding SE, Dec GW, Gwathmey JK, Hajjar RJ. Targeting phospholamban by gene transfer in human heart failure. Circulation 2002;105:904-907.
19. Tsuji T, Del Monte F, Yoshikawa Y, Abe T, Shimizu J, Nakajima-Takenak C et al. Rescue of Ca2+ overload-induced left ventricular dysfunction by targeted ablation of phospholamban. Am J Physiol Heart Circ Physiol 2009;296:H310-H317.
20. Chen Y, Escoubet B, Prunier F, Amour J, Simonides WS, Vivien B et al. Constitutive cardiac overexpression of sarcoplasmic/endoplasmic reticulum Ca2+-ATPase delays myocardial failure after myocardial infarction in rats at a cost of increased acute arrhythmias. Circulation 2004;109:1898-1903.
21. Song Q, Schmidt AG, Hahn HS, Carr AN, Frank B, Peter L et al. Rescue of cardiomyocyte dysfunction by phospholamban ablation does not prevent ventricular failure in genetic hypertrophy. J Clin Invest 2003;111:859-867.
22. Haghighi K, Kolokathis F, Pater L, Lynch RA, Asahi M, Gramolini AO 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.
23. Teucher N, Prestle J, Seidler T, Currie S, Elliott EB, Reynolds DF et al. Excessive sarcoplasmic/endoplasmic reticulum Ca2+-ATPase expression causes increased sarcoplasmic reticulum Ca2+ uptake but decreases myocyte shortening. Circulation 2004;110: 3553-3559.
24. Vangheluwe P, Tjwa M, Van Den Bergh A, Louch WE, Beullens M, Dode L et al. SERCA2 pump with an increased Ca2+ affinity can lead to severe cardiac hypertrophy, stress intolerance and reduced life span. J Mol Cell Cardiol 2006;41:308-317.
25. Vangheluwe P, Sipido KR, Raeymaekers L, Wuytack F. New perspectives on the role of SERCA2's Ca2+ affinity in cardiac function. Biochim Biophys Acta 2006;1763:1216-1228.
26. LuoW, Grupp IL, Harrer J, Ponniah S, Grupp G, Duffy JJ 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.
27. Babu GJ, Bhupathy P, Timofeyev V, Petrashevskaya NN, Reiser PJ, Chiamvimonvat N et al. Ablation of sarcolipin enhances sarcoplasmic reticulum calcium transport and atrial contractility. Proc Natl Acad Sci USA 2007;104:17867-17872.
28. Goldhaber JI, Parker JM, Weiss JN. Mechanisms of excitation- contraction coupling failure during metabolic inhibition in guineapig ventricular myocytes. J Physiol 1991;443:371-386.
29. Xie LH, Chen F, Karagueuzian HS, Weiss JN. Oxidative-stressinduced afterdepolarizations and calmodulin kinaseII signaling. Circ Res 2009;104:79-86.
30. Williams DA, Fogarty KE, Tsien RY, Fay FS. Calcium gradients in single smooth muscle cells revealed by the digital imaging microscope using Fura-2. Nature 1985;318:558-561.
31. Ward ML, Pope AJ, Loiselle DS, Cannell MB. Reduced contraction strength with increased intracellular [Ca2+] in left ventricular trabeculae from failing rat hearts. J Physiol 2003;546:537-550.
32. Sadoshima J, Montagne O, Wang Q, Yang G, Warden J, Lui J et al. The MEKK1-JNK pathway plays a protective role in pressure overload but does not mediate cardiac hypertrophy. J Clin Invest 2002;110:271-279.
33. Okumura S, Vatner DE, Kurotani R, Bai Y, Gao SM, Yuan ZR et al. Disruption of type5 adenylyl cyclase enhances desensitization of cyclic adenosine monophosphate signal and increases Akt signal with chronic catecholamine stress. Circulation 2007;116:1776-1783.
34. Lehnart SE, Wehrens XH, Kushnir A, Marks AR. Cardiac ryanodine receptor function and regulation in heart disease. Ann N Y Acad Sci 2004;1015:144-159.
35. van der Heyden MA, Wijnhoven TJ, Opthof T. Molecular aspects of adrenergic modulation of cardiac L-type Ca2+ channels. Cardiovasc Res 2005;65:28-39.
36. Hoit BD, Khoury SF, Kranias EG, Ball N, Walsh RA. In vivo echocardiographic detection of enhanced left ventricular function in gene-targeted mice with phospholamban deficiency. Circ Res 1995;77:632-637.
37. Chu G, Luo W, Slack JP, Tilgmann C, Sweet WE, Spindler M et al. Compensatory mechanisms associated with the hyperdynamic function of phospholamban-deficient mouse hearts. Circ Res 1996;79:1064-1076.
38. Masaki H, Sato Y, Luo W, Kranias EG, Yatani A. Phospholamban deficiency alters inactivation kinetics of L-type Ca2+ channels in mouse ventricular myocytes. Am J Physiol 1997;272: H606-H612.
39. Shiojima I, Walsh K. Regulation of cardiac growth and coronary angiogenesis by the Akt/PKB signaling pathway. Genes Dev 2006; 20:3347-3365.
40. DeBosch B, Treskov I, Lupu TS, Weinheimer C, Kovacs A, Courtois M et al. Akt1 is required for physiological cardiac growth. Circulation 2006;113:2097-2104.
41. Braz JC, Gill RM, Corbly AK, Jones BD, Jin N, Vlahos CJ et al. Selective activation of PI3Ka/Akt/GSK-3b signalling and cardiac compensatory hypertrophy during recovery from heart failure. Eur J Heart Fail 2009;11:739-748.
42. Damilano F, Perino A, Hirsch E. PI3K kinase and scaffold functions in heart. Ann N Y Acad Sci 2010;188:39-45.