Decoy peptides targeted to protein phosphatase 1 inhibit dephosphorylation of phospholamban in cardiomyocytes

Journal of Molecular and Cellular Cardiology

Volumn 56, Issue 1, 2013, Pages 63-71

  Oh, Jae Gyun ^a   Kim, Jihwa ^a   Jang, Seung Pil ^a   Nguen, Mai ^a   Yang, Dong Kwon ^a   Jeong, Dongtak ^b   Park, Zee Yong ^a   Park, Sung Gyoo ^a   Hajjar, Roger J ^b   Park, Woo Jin ^a  

^a Gwangju Institute of Science and Technology (GIST)   (South Korea)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Decoy; Peptide; Phospholamban; Protein phosphatase 1; SERCA2a

Indexed keywords

CALCIUM ION; DECOY PEPTIDE; GLUTAMINE; PHOSPHOLAMBAN; PHOSPHOPROTEIN PHOSPHATASE 1; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE 2A; SERINE; SYNTHETIC PEPTIDE; THREONINE; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

ADULT ANIMAL; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; COMPETITIVE INHIBITION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; EX VIVO STUDY; HEART FAILURE; HEART FUNCTION; HEART LEFT VENTRICLE PRESSURE; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART PERFUSION; IN VITRO STUDY; ISOLATED HEART; MALE; MOLECULAR MIMICRY; NEWBORN; NONHUMAN; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; RAT;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM; CALCIUM-BINDING PROTEINS; CARDIOTONIC AGENTS; CELLS, CULTURED; HEART FAILURE; KINETICS; MALE; MOLECULAR SEQUENCE DATA; MYOCARDIAL CONTRACTION; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN PHOSPHATASE 1; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, SPRAGUE-DAWLEY; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES;

RATTUS;

EID: 84873170957     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2012.12.005     Document Type: Article

References (51)

1. Lopez A.D., Mathers C.D., Ezzati M., Jamison D.T., Murray C.J. Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. Lancet May 27 2006, 367(9524):1747-1757.
2. Mathers C.D., Loncar D. Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med Nov 2006, 3(11):e442.
3. Mathers C.D., Boerma T., Ma Fat D. Global and regional causes of death. Br Med Bull 2009, 92:7-32.
4. Houser S.R., Piacentino V., Weisser J. Abnormalities of calcium cycling in the hypertrophied and failing heart. J Mol Cell Cardiol Sep 2000, 32(9):1595-1607.
5. Houser S.R., Margulies K.B. Is depressed myocyte contractility centrally involved in heart failure?. Circ Res Mar 7 2003, 92(4):350-358.
6. Lehnart S.E., Maier L.S., Hasenfuss G. Abnormalities of calcium metabolism and myocardial contractility depression in the failing heart. Heart Fail Rev Dec 2009, 14(4):213-224.
7. Bers D.M., Guo T. Calcium signaling in cardiac ventricular myocytes. Ann N Y Acad Sci Jun 2005, 1047:86-98.
8. Schaub M.C., Hefti M.A., Zaugg M. Integration of calcium with the signaling network in cardiac myocytes. J Mol Cell Cardiol Aug 2006, 41(2):183-214.
9. MacLennan D.H., Kranias E.G. Phospholamban: a crucial regulator of cardiac contractility. Nat Rev Mol Cell Biol Jul 2003, 4(7):566-577.
10. Arai M., Matsui H., Periasamy M. Sarcoplasmic reticulum gene expression in cardiac hypertrophy and heart failure. Circ Res Apr 1994, 74(4):555-564.
11. Hasenfuss G., Reinecke H., Studer R., Meyer M., Pieske B., Holtz J., et al. Relation between myocardial function and expression of sarcoplasmic reticulum Ca(2+)-ATPase in failing and nonfailing human myocardium. Circ Res Sep 1994, 75(3):434-442.
12. 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 Aug 15 1995, 92(4):778-784.
13. Miyamoto M.I., del Monte F., Schmidt U., DiSalvo T.S., Kang Z.B., Matsui T., et al. Adenoviral gene transfer of SERCA2a improves left-ventricular function in aortic-banded rats in transition to heart failure. Proc Natl Acad Sci U S A Jan 18 2000, 97(2):793-798.
14. del Monte F., Hajjar R.J., Harding S.E. Overwhelming evidence of the beneficial effects of SERCA gene transfer in heart failure. Circ Res Jun 8 2001, 88(11):E66-E67.
15. Sakata S., Lebeche D., Sakata Y., Sakata N., Chemaly E.R., Liang L., et al. Transcoronary gene transfer of SERCA2a increases coronary blood flow and decreases cardiomyocyte size in a type 2 diabetic rat model. Am J Physiol Heart Circ Physiol Feb 2007, 292(2):H1204-H1207.
16. 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 Mar 18 2008, 51(11):1112-1119.
17. 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 Apr 2009, 15(3):171-181.
18. Jessup M., Greenberg B., Mancini D., Cappola T., Pauly D.F., Jaski B., et al. Calcium upregulation by percutaneous administration of gene therapy in cardiac disease (CUPID): a phase 2 trial of intracoronary gene therapy of sarcoplasmic reticulum Ca2+-ATPase in patients with advanced heart failure. Circulation Jul 19 2011, 124(3):304-313.
19. Le Peuch C.J., Haiech J., Demaille J.G. Concerted regulation of cardiac sarcoplasmic reticulum calcium transport by cyclic adenosine monophosphate dependent and calcium-calmodulin-dependent phosphorylations. Biochemistry Nov 13 1979, 18(23):5150-5157.
20. James P., Inui M., Tada M., Chiesi M., Carafoli E. Nature and site of phospholamban regulation of the Ca2+ pump of sarcoplasmic reticulum. Nature Nov 2 1989, 342(6245):90-92.
21. Mattiazzi A., Mundina-Weilenmann C., Guoxiang C., Vittone L., Kranias E. Role of phospholamban phosphorylation on Thr17 in cardiac physiological and pathological conditions. Cardiovasc Res Dec 1 2005, 68(3):366-375.
22. MacDougall L.K., Jones L.R., Cohen P. Identification of the major protein phosphatases in mammalian cardiac muscle which dephosphorylate phospholamban. Eur J Biochem Mar 28 1991, 196(3):725-734.
23. 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 Feb 14 1992, 293(1):17-24.
24. Schwinger R.H., Munch G., Bolck B., Karczewski P., Krause E.G., Erdmann E. Reduced Ca(2+)-sensitivity of SERCA 2a in failing human myocardium due to reduced serin-16 phospholamban phosphorylation. J Mol Cell Cardiol Mar 1999, 31(3):479-491.
25. Mishra S., Gupta R.C., Tiwari N., Sharov V.G., Sabbah H.N. Molecular mechanisms of reduced sarcoplasmic reticulum Ca(2+) uptake in human failing left ventricular myocardium. J Heart Lung Transplant Mar 2002, 21(3):366-373.
26. Sande J.B., Sjaastad I., Hoen I.B., Bokenes J., Tonnessen T., Holt E., et al. Reduced level of serine(16) phosphorylated phospholamban in the failing rat myocardium: a major contributor to reduced SERCA2 activity. Cardiovasc Res Feb 1 2002, 53(2):382-391.
27. 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 Jan 1997, 29(1):265-272.
28. Huang B., Wang S., Qin D., Boutjdir M., El-Sherif N. Diminished basal phosphorylation level of phospholamban in the postinfarction remodeled rat ventricle: role of beta-adrenergic pathway, G(i) protein, phosphodiesterase, and phosphatases. Circ Res Oct 29 1999, 85(9):848-855.
29. Ta H.M., Nguyen G.T., Jin H.M., Choi J., Park H., Kim N., et al. Structure-based development of a receptor activator of nuclear factor-kappaB ligand (RANKL) inhibitor peptide and molecular basis for osteopetrosis. Proc Natl Acad Sci U S A Nov 23 2010, 107(47):20281-20286.
30. Law J.H., Li Y., To K, Wang M., Astanehe A., Lambie K., et al. Molecular decoy to the Y-box binding protein-1 suppresses the growth of breast and prostate cancer cells whilst sparing normal cell viability. PLoS One 2010, 5(9).
31. Yamaguchi H., Durell S.R., Feng H., Bai Y., Anderson C.W., Appella E. Development of a substrate-based cyclic phosphopeptide inhibitor of protein phosphatase 2Cdelta, Wip1. Biochemistry Nov 7 2006, 45(44):13193-13202.
32. Hayashi R., Tanoue K., Durell S.R., Chatterjee D.K., Jenkins L.M., Appella D.H., et al. Optimization of a cyclic peptide inhibitor of Ser/Thr phosphatase PPM1D (Wip1). Biochemistry May 31 2011, 50(21):4537-4549.
33. Ren J., Wold L.E. Measurement of cardiac mechanical function in isolated ventricular myocytes from rats and mice by computerized video-based imaging. Biol Proced Online Dec 11 2001, 3:43-53.
34. Zhou Y.Y., Wang S.Q., Zhu W.Z., Chruscinski A., Kobilka B.K., Ziman B., et al. Culture and adenoviral infection of adult mouse cardiac myocytes: methods for cellular genetic physiology. Am J Physiol Heart Circ Physiol Jul 2000, 279(1):H429-H436.
35. 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 Sep 1994, 75(3):401-409.
36. Capogrossi M.C., Kaku T., Filburn C.R., Pelto D.J., Hansford R.G., Spurgeon H.A., et al. Phorbol ester and dioctanoylglycerol stimulate membrane association of protein kinase C and have a negative inotropic effect mediated by changes in cytosolic Ca2+ in adult rat cardiac myocytes. Circ Res Apr 1990, 66(4):1143-1155.
37. Ward C.A., Moffat M.P. Positive and negative inotropic effects of phorbol 12-myristate 13-acetate: relationship to PKC-dependence and changes in [Ca2+]i. J Mol Cell Cardiol Sep 1992, 24(9):937-948.
38. Braz J.C., Gregory K., Pathak A., Zhao W., Sahin B., Klevitsky R., et al. PKC-alpha regulates cardiac contractility and propensity toward heart failure. Nat Med Mar 2004, 10(3):248-254.
39. Shintani-Ishida K., Yoshida K. Ischemia induces phospholamban dephosphorylation via activation of calcineurin, PKC-alpha, and protein phosphatase 1, thereby inducing calcium overload in reperfusion. Biochim Biophys Acta Jul 2011, 1812(7):743-751.
40. He H., Meyer M., Martin J.L., McDonough P.M., Ho P., Lou X., et al. Effects of mutant and antisense RNA of phospholamban on SR Ca(2+)-ATPase activity and cardiac myocyte contractility. Circulation Aug 31 1999, 100(9):974-980.
41. Watanabe A., Arai M., Yamazaki M., Koitabashi N., Wuytack F., Kurabayashi M. Phospholamban ablation by RNA interference increases Ca2+ uptake into rat cardiac myocyte sarcoplasmic reticulum. J Mol Cell Cardiol Sep 2004, 37(3):691-698.
42. Hoshijima M., Ikeda Y., Iwanaga Y., Minamisawa S., Date M.O., Gu Y., et al. Chronic suppression of heart-failure progression by a pseudophosphorylated mutant of phospholamban via in vivo cardiac rAAV gene delivery. Nat Med Aug 2002, 8(8):864-871.
43. Iwanaga Y., Hoshijima M., Gu Y., Iwatate M., Dieterle T., Ikeda Y., et al. Chronic phospholamban inhibition prevents progressive cardiac dysfunction and pathological remodeling after infarction in rats. J Clin Invest Mar 2004, 113(5):727-736.
44. Kaye D.M., Preovolos A., Marshall T., Byrne M., Hoshijima M., Hajjar R., et al. Percutaneous cardiac recirculation-mediated gene transfer of an inhibitory phospholamban peptide reverses advanced heart failure in large animals. J Am Coll Cardiol Jul 17 2007, 50(3):253-260.
45. Hou Z., Kelly E.M., Robia S.L. Phosphomimetic mutations increase phospholamban oligomerization and alter the structure of its regulatory complex. J Biol Chem Oct 24 2008, 283(43):28996-29003.
46. Chu G., Lester J.W., Young K.B., Luo W., Zhai J., Kranias E.G. A single site (Ser16) phosphorylation in phospholamban is sufficient in mediating its maximal cardiac responses to beta-agonists. J Biol Chem Dec 8 2000, 275(49):38938-38943.
47. Luo W., Chu G., Sato Y., Zhou Z., Kadambi V.J., Kranias E.G. Transgenic approaches to define the functional role of dual site phospholamban phosphorylation. J Biol Chem Feb 20 1998, 273(8):4734-4739.
48. Yoshida Y., Shiga T., Imai S. Degradation of sarcoplasmic reticulum calcium-pumping ATPase in ischemic-reperfused myocardium: role of calcium-activated neutral protease. Basic Res Cardiol Sep-Oct 1990, 85(5):495-507.
49. Singh R.B., Chohan P.K., Dhalla N.S., Netticadan T. The sarcoplasmic reticulum proteins are targets for calpain action in the ischemic-reperfused heart. J Mol Cell Cardiol Jul 2004, 37(1):101-110.
50. 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 Apr 24 2009, 104(8):1012-1020.
51. 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 Jun 10 2011, 108(12):1429-1438.