Targeted deletion of PTEN in cardiomyocytes renders cardiac contractile dysfunction through interruption of Pink1-AMPK signaling and autophagy

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1852, Issue 2, 2015, Pages 290-298

  Roe, Nathan D ^a   Xu, Xihui ^a   Kandadi, Machender R ^a   Hu, Nan ^a   Pang, Jiaojiao ^a,b   Weiser Evans, Mary C M ^c   Ren, Jun ^a  

^a UNIVERSITY OF WYOMING COLLEGE OF HEALTH SCIENCES   (United States)

^b SHANDONG UNIVERSITY   (China)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

AMPK; Cardiac hypertrophy; Contractile function; Pink1; PTEN

Indexed keywords

DRINKING WATER; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; METFORMIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P62; PTEN INDUCIBLE KINASE 1; RAPAMYCIN; SUPEROXIDE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; PROTEIN KINASE; PTEN PROTEIN, MOUSE; PTEN-INDUCED PUTATIVE KINASE;

ANIMAL CELL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CALCIUM CELL LEVEL; CONTROLLED STUDY; GEOMETRY; HEART FUNCTION; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; IN VIVO STUDY; MOUSE; MYOBLAST; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEIN QUALITY; QUALITY CONTROL; RAT; RNA INTERFERENCE; ANIMAL; CARDIOMEGALY; DEFICIENCY; DRUG EFFECTS; ENZYME ACTIVATION; ENZYMOLOGY; GENE DELETION; GENE INACTIVATION; HEART CONTRACTION; INTRACELLULAR SPACE; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

MURINAE;

ADENOSINE TRIPHOSPHATE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; AUTOPHAGY; CARDIOMEGALY; ENZYME ACTIVATION; GENE DELETION; GENE KNOCKOUT TECHNIQUES; INTRACELLULAR SPACE; METFORMIN; MICE, KNOCKOUT; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PHOSPHORYLATION; PROTEIN KINASES; PTEN PHOSPHOHYDROLASE; RATS; SIGNAL TRANSDUCTION; SUPEROXIDES;

EID: 84919797562     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2014.09.002     Document Type: Article

References (52)

1. Aroor A.R., Mandavia C.H., Sowers J.R. Insulin resistance and heart failure: molecular mechanisms. Heart Fail. Clin. 2012, 8:609-617.
2. Abel E.D., O'Shea K.M., Ramasamy R. Insulin resistance: metabolic mechanisms and consequences in the heart. Arterioscler. Thromb. Vasc. Biol. 2012, 32:2068-2076.
3. Ren J., Pulakat L., Whaley-Connell A., Sowers J.R. Mitochondrial biogenesis in the metabolic syndrome and cardiovascular disease. J. Mol. Med. (Berl.) 2010, 88:993-1001.
4. Jay M.A., Ren J. Peroxisome proliferator-activated receptor (PPAR) in metabolic syndrome and type 2 diabetes mellitus. Curr. Diabetes Rev. 2007, 3:33-39.
5. Maehama T., Dixon J.E. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 1998, 273:13375-13378.
6. Pal A., Barber T.M., Van de Bunt M., Rudge S.A., Zhang Q., Lachlan K.L., Cooper N.S., Linden H., Levy J.C., Wakelam M.J., Walker L., Karpe F., Gloyn A.L. PTEN mutations as a cause of constitutive insulin sensitivity and obesity. N. Engl. J. Med. 2012, 367:1002-1011.
7. Crackower M.A., Oudit G.Y., Kozieradzki I., Sarao R., Sun H., Sasaki T., Hirsch E., Suzuki A., Shioi T., Irie-Sasaki J., Sah R., Cheng H.Y., Rybin V.O., Lembo G., Fratta L., Oliveira-dos-Santos A.J., Benovic J.L., Kahn C.R., Izumo S., Steinberg S.F., Wymann M.P., Backx P.H., Penninger J.M. Regulation of myocardial contractility and cell size by distinct PI3K-PTEN signaling pathways. Cell 2002, 110:737-749.
8. Oudit G.Y., Kassiri Z., Zhou J., Liu Q.C., Liu P.P., Backx P.H., Dawood F., Crackower M.A., Scholey J.W., Penninger J.M. Loss of PTEN attenuates the development of pathological hypertrophy and heart failure in response to biomechanical stress. Cardiovasc. Res. 2008, 78:505-514.
9. Xu X., Roe N.D., Weiser-Evans M.C., Ren J. Inhibition of mammalian target of rapamycin with rapamycin reverses hypertrophic cardiomyopathy in mice with cardiomyocyte-specific knockout of PTEN. Hypertension 2014, 63:729-739.
10. Matsui T., Nagoshi T., Hong E.G., Luptak I., Hartil K., Li L., Gorovits N., Charron M.J., Kim J.K., Tian R., Rosenzweig A. Effects of chronic Akt activation on glucose uptake in the heart. Am. J. Physiol. Endocrinol. Metab. 2006, 290:E789-E797.
11. Billia F., Hauck L., Konecny F., Rao V., Shen J., Mak T.W. PTEN-inducible kinase 1 (PINK1)/Park6 is indispensable for normal heart function. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:9572-9577.
12. Unoki M., Nakamura Y. Growth-suppressive effects of BPOZ and EGR2, two genes involved in the PTEN signaling pathway. Oncogene 2001, 20:4457-4465.
13. Zaha V.G., Young L.H. AMP-activated protein kinase regulation and biological actions in the heart. Circ. Res. 2012, 111:800-814.
14. Carling D., Sanders M.J., Woods A. The regulation of AMP-activated protein kinase by upstream kinases. Int. J. Obes. (Lond.) 2008, 32(Suppl. 4):S55-S59.
15. Mughal W., Dhingra R., Kirshenbaum L.A. Striking a balance: autophagy, apoptosis, and necrosis in a normal and failing heart. Curr. Hypertens. Rep. 2012, 14:540-547.
16. Xie Z., Lau K., Eby B., Lozano P., He C., Pennington B., Li H., Rathi S., Dong Y., Tian R., Kem D., Zou M.H. Improvement of cardiac functions by chronic metformin treatment is associated with enhanced cardiac autophagy in diabetic OVE26 mice. Diabetes 2011, 60:1770-1778.
17. Roe N.D., Ren J. Akt2 knockout mitigates chronic iNOS inhibition-induced cardiomyocyte atrophy and contractile dysfunction despite persistent insulin resistance. Toxicol. Lett. 2011, 207:222-231.
18. Xu X., Pacheco B.D., Leng L., Bucala R., Ren J. Macrophage migration inhibitory factor plays a permissive role in the maintenance of cardiac contractile function under starvation through regulation of autophagy. Cardiovasc. Res. 2013, 99:412-421.
19. Bhamra G.S., Hausenloy D.J., Davidson S.M., Carr R.D., Paiva M., Wynne A.M., Mocanu M.M., Yellon D.M. Metformin protects the ischemic heart by the Akt-mediated inhibition of mitochondrial permeability transition pore opening. Basic Res. Cardiol. 2008, 103:274-284.
20. 2+ transients in adult rat ventricular myocytes. Diabetes 1999, 48:2059-2065.
21. Wang Q., Yang L., Hua Y., Nair S., Xu X., Ren J. AMP-activated protein kinase deficiency rescues paraquat-induced cardiac contractile dysfunction through an autophagy-dependent mechanism. Toxicol. Sci. 2014.
22. Roe N.D., Thomas D.P., Ren J. Inhibition of NADPH oxidase alleviates experimental diabetes-induced myocardial contractile dysfunction. Diabetes Obes. Metab. 2011, 13:465-473.
23. Wang D., Patel V.V., Ricciotti E., Zhou R., Levin M.D., Gao E., Yu Z., Ferrari V.A., Lu M.M., Xu J., Zhang H., Hui Y., Cheng Y., Petrenko N., Yu Y., FitzGerald G.A. Cardiomyocyte cyclooxygenase-2 influences cardiac rhythm and function. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:7548-7552.
24. Xu X., Bucala R., Ren J. Macrophage migration inhibitory factor deficiency augments doxorubicin-induced cardiomyopathy. J. Am. Heart Assoc. 2013, 2:e000439.
25. Xu X., Hueckstaedt L.K., Ren J. Deficiency of insulin-like growth factor 1 attenuates aging-induced changes in hepatic function: role of autophagy. J. Hepatol. 2013, 59:308-317.
26. Xu X., Hua Y., Nair S., Zhang Y., Ren J. Akt2 knockout preserves cardiac function in high-fat diet-induced obesity by rescuing cardiac autophagosome maturation. J. Mol. Cell Biol. 2013, 5:61-63.
27. Morlino G., Barreiro O., Baixauli F., Robles-Valero J., Gonzalez-Granado J.M., Villa-Bellosta R., Cuenca J., Sanchez-Sorzano C.O., Veiga E., Martin-Cofreces N.B., Sanchez-Madrid F. Miro-1 links mitochondria and microtubule Dynein motors to control lymphocyte migration and polarity. Mol. Cell. Biol. 2014, 34:1412-1426.
28. Scherz-Shouval R., Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem. Sci. 2011, 36:30-38.
29. Chen Y., Azad M.B., Gibson S.B. Superoxide is the major reactive oxygen species regulating autophagy. Cell Death Differ. 2009, 16:1040-1052.
30. Kaushik S., Cuervo A.M. Autophagy as a cell-repair mechanism: activation of chaperone-mediated autophagy during oxidative stress. Mol. Aspects Med. 2006, 27:444-454.
31. Stambolic V., Suzuki A., de la Pompa J.L., Brothers G.M., Mirtsos C., Sasaki T., Ruland J., Penninger J.M., Siderovski D.P., Mak T.W. Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell 1998, 95:29-39.
32. Matsui T., Li L., Wu J.C., Cook S.A., Nagoshi T., Picard M.H., Liao R., Rosenzweig A. Phenotypic spectrum caused by transgenic overexpression of activated Akt in the heart. J. Biol. Chem. 2002, 277:22896-22901.
33. Condorelli G., Drusco A., Stassi G., Bellacosa A., Roncarati R., Iaccarino G., Russo M.A., Gu Y., Dalton N., Chung C., Latronico M.V., Napoli C., Sadoshima J., Croce C.M., Ross J. Akt induces enhanced myocardial contractility and cell size in vivo in transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:12333-12338.
34. Valente E.M., Abou-Sleiman P.M., Caputo V., Muqit M.M., Harvey K., Gispert S., Ali Z., Del Turco D., Bentivoglio A.R., Healy D.G., Albanese A., Nussbaum R., Gonzalez-Maldonado R., Deller T., Salvi S., Cortelli P., Gilks W.P., Latchman D.S., Harvey R.J., Dallapiccola B., Auburger G., Wood N.W. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 2004, 304:1158-1160.
35. Anichtchik O., Diekmann H., Fleming A., Roach A., Goldsmith P., Rubinsztein D.C. Loss of PINK1 function affects development and results in neurodegeneration in zebrafish. J. Neurosci. 2008, 28:8199-8207.
36. Siddall H.K., Warrell C.E., Davidson S.M., Mocanu M.M., Yellon D.M. Mitochondrial PINK1-a novel cardioprotective kinase?. Cardiovasc. Drugs Ther. 2008, 22:507-508.
37. Beauloye C., Bertrand L., Horman S., Hue L. AMPK activation, a preventive therapeutic target in the transition from cardiac injury to heart failure. Cardiovasc. Res. 2011, 90:224-233.
38. Wang J., Yang L., Rezaie A.R., Li J. Activated protein C protects against myocardial ischemic/reperfusion injury through AMP-activated protein kinase signaling. J. Thromb. Haemost. 2011, 9:1308-1317.
39. Ma H., Wang J., Thomas D.P., Tong C., Leng L., Wang W., Merk M., Zierow S., Bernhagen J., Ren J., Bucala R., Li J. Impaired macrophage migration inhibitory factor-AMP-activated protein kinase activation and ischemic recovery in the senescent heart. Circulation 2010, 122:282-292.
40. Xie Z., He C., Zou M.H. AMP-activated protein kinase modulates cardiac autophagy in diabetic cardiomyopathy. Autophagy 2011, 7:1254-1255.
41. Oliveira S.M., Zhang Y.H., Solis R.S., Isackson H., Bellahcene M., Yavari A., Pinter K., Davies J.K., Ge Y., Ashrafian H., Walker J.W., Carling D., Watkins H., Casadei B., Redwood C. AMP-activated protein kinase phosphorylates cardiac troponin I and alters contractility of murine ventricular myocytes. Circ. Res. 2012, 110:1192-1201.
42. Li H.L., Yin R., Chen D., Liu D., Wang D., Yang Q., Dong Y.G. Long-term activation of adenosine monophosphate-activated protein kinase attenuates pressure-overload-induced cardiac hypertrophy. J. Cell. Biochem. 2007, 100:1086-1099.
43. Chan A.Y., Soltys C.L., Young M.E., Proud C.G., Dyck J.R. Activation of AMP-activated protein kinase inhibits protein synthesis associated with hypertrophy in the cardiac myocyte. J. Biol. Chem. 2004, 279:32771-32779.
44. Xu X., Ren J. Unmasking the janus faces of autophagy in obesity-associated insulin resistance and cardiac dysfunction. Clin. Exp. Pharmacol. Physiol. 2012, 39:200-208.
45. Inoki K., Zhu T., Guan K.L. TSC2 mediates cellular energy response to control cell growth and survival. Cell 2003, 115:577-590.
46. Gwinn D.M., Shackelford D.B., Egan D.F., Mihaylova M.M., Mery A., Vasquez D.S., Turk B.E., Shaw R.J. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol. Cell 2008, 30:214-226.
47. Xu X., Hua Y., Nair S., Bucala R., Ren J. Macrophage migration inhibitory factor deletion exacerbates pressure overload-induced cardiac hypertrophy through mitigating autophagy. Hypertension 2014, 63:490-499.
48. Kim J., Kundu M., Viollet B., Guan K.L. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 2011, 13:132-141.
49. Egan D.F., Shackelford D.B., Mihaylova M.M., Gelino S., Kohnz R.A., Mair W., Vasquez D.S., Joshi A., Gwinn D.M., Taylor R., Asara J.M., Fitzpatrick J., Dillin A., Viollet B., Kundu M., Hansen M., Shaw R.J. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 2011, 331:456-461.
50. Mizushima N. The role of the Atg1/ULK1 complex in autophagy regulation. Curr. Opin. Cell Biol. 2010, 22:132-139.
51. Meley D., Bauvy C., Houben-Weerts J.H., Dubbelhuis P.F., Helmond M.T., Codogno P., Meijer A.J. AMP-activated protein kinase and the regulation of autophagic proteolysis. J. Biol. Chem. 2006, 281:34870-34879.
52. Kane L.A., Youle R.J. PINK1 and Parkin flag Miro to direct mitochondrial traffic. Cell 2011, 147:721-723.