MTORC2 regulates cardiac response to stress by inhibiting MST1

Cell Reports

Volumn 11, Issue 1, 2015, Pages 125-136

  Sciarretta, Sebastiano ^a,b   Zhai, Peiyong ^a   Maejima, Yasuhiro ^a   DelRe, Dominic P ^a   Nagarajan, Narayani ^a   Yee, Derek ^a   Liu, Tong ^c   Magnuson, Mark A ^d   Volpe, Massimo ^b,e   Frati, Giacomo ^b,f   Li, Hong ^c   Sadoshima, Junichi ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b IRCCS NEUROMED   (Italy)

^c The State University of New Jersey   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e SAPIENZA UNIVERSITY OF ROME   (Italy)

^f SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; MST1 KINASE; PHOSPHOTRANSFERASE; SERINE; UNCLASSIFIED DRUG; CARRIER PROTEIN; MACROPHAGE STIMULATING PROTEIN; MULTIPROTEIN COMPLEX; ONCOPROTEIN; RICTOR PROTEIN, MOUSE; SCATTER FACTOR; TARGET OF RAPAMYCIN KINASE; TOR COMPLEX 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL GROWTH; CELL SURVIVAL; CONTROLLED STUDY; DIMERIZATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE DELETION; GENE DISRUPTION; HEART DEVELOPMENT; HEART DISEASE; HEART FAILURE; HEART FUNCTION; HEART MUSCLE; HEART MUSCLE CELL; HEART SIZE; HIPPO PATHWAY; HOMODIMERIZATION; MECHANICAL STRESS; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; REGULATORY MECHANISM; SARAH DOMAIN; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CARDIAC MUSCLE; CELL PROLIFERATION; GENETICS; HEART; HUMAN; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PROTEIN MULTIMERIZATION;

ANIMALS; CARRIER PROTEINS; CELL PROLIFERATION; CELL SURVIVAL; HEART; HEPATOCYTE GROWTH FACTOR; HUMANS; MICE; MICE, KNOCKOUT; MULTIPROTEIN COMPLEXES; MYOCARDIUM; PROTEIN MULTIMERIZATION; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; STRESS, MECHANICAL; TOR SERINE-THREONINE KINASES;

EID: 84927695687     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.03.010     Document Type: Article

References (51)

1. Aragona M., Panciera T., Manfrin A., Giulitti S., Michielin F., Elvassore N., Dupont S., Piccolo S. A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 2013, 154:1047-1059.
2. Boulbés D.R., Shaiken T., Sarbassov D. Endoplasmic reticulum is a main localization site of mTORC2. Biochem. Biophys. Res. Commun. 2011, 413:46-52.
3. Braz J.C., Gregory K., Pathak A., Zhao W., Sahin B., Klevitsky R., Kimball T.F., Lorenz J.N., Nairn A.C., Liggett S.B., et al. PKC-alpha regulates cardiac contractility and propensity toward heart failure. Nat. Med. 2004, 10:248-254.
4. Cinar B., Collak F.K., Lopez D., Akgul S., Mukhopadhyay N.K., Kilicarslan M., Gioeli D.G., Freeman M.R. MST1 is a multifunctional caspase-independent inhibitor of androgenic signaling. Cancer Res. 2011, 71:4303-4313.
5. Collak F.K., Yagiz K., Luthringer D.J., Erkaya B., Cinar B. Threonine-120 phosphorylation regulated by phosphoinositide-3-kinase/Akt and mammalian target of rapamycin pathway signaling limits the antitumor activity of mammalian sterile 20-like kinase 1. J.Biol. Chem. 2012, 287:23698-23709.
6. Das S., Aiba T., Rosenberg M., Hessler K., Xiao C., Quintero P.A., Ottaviano F.G., Knight A.C., Graham E.L., Boström P., et al. Pathological role of serum- and glucocorticoid-regulated kinase 1 in adverse ventricular remodeling. Circulation 2012, 126:2208-2219.
7. DeBosch B., Treskov I., Lupu T.S., Weinheimer C., Kovacs A., Courtois M., Muslin A.J. Akt1 is required for physiological cardiac growth. Circulation 2006, 113:2097-2104.
8. Del Re D.P., Matsuda T., Zhai P., Gao S., Clark G.J., Van Der Weyden L., Sadoshima J. Proapoptotic Rassf1A/Mst1 signaling in cardiac fibroblasts is protective against pressure overload in mice. J.Clin. Invest. 2010, 120:3555-3567.
9. Del Re D.P., Yang Y., Nakano N., Cho J., Zhai P., Yamamoto T., Zhang N., Yabuta N., Nojima H., Pan D., Sadoshima J. Yes-associated protein isoform 1 (Yap1) promotes cardiomyocyte survival and growth to protect against myocardial ischemic injury. J.Biol. Chem. 2013, 288:3977-3988.
10. Del Re D.P., Matsuda T., Zhai P., Maejima Y., Jain M.R., Liu T., Li H., Hsu C.P., Sadoshima J. Mst1 promotes cardiac myocyte apoptosis through phosphorylation and inhibition of Bcl-xL. Mol. Cell 2014, 54:639-650.
11. Dibble C.C., Asara J.M., Manning B.D. Characterization of Rictor phosphorylation sites reveals direct regulation of mTOR complex 2 by S6K1. Mol. Cell. Biol. 2009, 29:5657-5670.
12. Facchinetti V., Ouyang W., Wei H., Soto N., Lazorchak A., Gould C., Lowry C., Newton A.C., Mao Y., Miao R.Q., et al. The mammalian target of rapamycin complex 2 controls folding and stability of Akt and protein kinase C. EMBO J. 2008, 27:1932-1943.
13. Fernández B.G., Gaspar P., Brás-Pereira C., Jezowska B., Rebelo S.R., Janody F. Actin-Capping Protein and the Hippo pathway regulate F-actin and tissue growth in Drosophila. Development 2011, 138:2337-2346.
14. García-Martínez J.M., Alessi D.R. mTOR complex 2 (mTORC2) controls hydrophobic motif phosphorylation and activation of serum- and glucocorticoid-induced protein kinase 1 (SGK1). Biochem. J. 2008, 416:375-385.
15. Guertin D.A., Stevens D.M., Thoreen C.C., Burds A.A., Kalaany N.Y., Moffat J., Brown M., Fitzgerald K.J., Sabatini D.M. Ablation in mice of the mTORC components raptor, rictor, or mLST8 reveals that mTORC2 is required for signaling to Akt-FOXO and PKCalpha, but not S6K1. Dev. Cell 2006, 11:859-871.
16. Hayashi S., Tamura K., Yokoyama H. Yap1, transcription regulator in the Hippo signaling pathway, is required for Xenopus limb bud regeneration. Dev. Biol. 2014, 388:57-67.
17. Hwang E., Ryu K.S., Pääkkönen K., Güntert P., Cheong H.K., Lim D.S., Lee J.O., Jeon Y.H., Cheong C. Structural insight into dimeric interaction of the SARAH domains from Mst1 and RASSF family proteins in the apoptosis pathway. Proc. Natl. Acad. Sci. USA 2007, 104:9236-9241.
18. Ikenoue T., Inoki K., Yang Q., Zhou X., Guan K.L. Essential function of TORC2 in PKC and Akt turn motif phosphorylation, maturation and signalling. EMBO J. 2008, 27:1919-1931.
19. Ikenoue T., Hong S., Inoki K. Monitoring mammalian target of rapamycin (mTOR) activity. Methods Enzymol. 2009, 452:165-180.
20. Jacinto E., Loewith R., Schmidt A., Lin S., Rüegg M.A., Hall A., Hall M.N. Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat. Cell Biol. 2004, 6:1122-1128.
21. Jacinto E., Facchinetti V., Liu D., Soto N., Wei S., Jung S.Y., Huang Q., Qin J., Su B. SIN1/MIP1 maintains rictor-mTOR complex integrityand regulates Akt phosphorylation and substrate specificity. Cell 2006, 127:125-137.
22. Lamming D.W., Ye L., Katajisto P., Goncalves M.D., Saitoh M., Stevens D.M., Davis J.G., Salmon A.B., Richardson A., Ahima R.S., et al. Rapamycin-induced insulin resistance is mediated by mTORC2 loss and uncoupled from longevity. Science 2012, 335:1638-1643.
23. Lamming D.W., Mihaylova M.M., Katajisto P., Baar E.L., Yilmaz O.H., Hutchins A., Gultekin Y., Gaither R., Sabatini D.M. Depletion of Rictor, an essential protein component of mTORC2, decreases male lifespan. Aging Cell 2014, 13:911-917.
24. Laplante M., Sabatini D.M. mTOR signaling in growth control and disease. Cell 2012, 149:274-293.
25. Maejima Y., Kyoi S., Zhai P., Liu T., Li H., Ivessa A., Sciarretta S., Del Re D.P., Zablocki D.K., Hsu C.P., et al. Mst1 inhibits autophagy by promoting the interaction between Beclin1 and Bcl-2. Nat. Med. 2013, 19:1478-1488.
26. Morisco C., Seta K., Hardt S.E., Lee Y., Vatner S.F., Sadoshima J. Glycogen synthase kinase 3beta regulates GATA4 in cardiac myocytes. J.Biol. Chem. 2001, 276:28586-28597.
27. O'Neill E., Rushworth L., Baccarini M., Kolch W. Role of the kinase MST2 in suppression of apoptosis by the proto-oncogene product Raf-1. Science 2004, 306:2267-2270.
28. Oppermann F.S., Gnad F., Olsen J.V., Hornberger R., Greff Z., Kéri G., Mann M., Daub H. Large-scale proteomics analysis of the human kinome. Mol. Cell. Proteomics 2009, 8:1751-1764.
29. Pan D. The hippo signaling pathway in development and cancer. Dev. Cell 2010, 19:491-505.
30. Praskova M., Khoklatchev A., Ortiz-Vega S., Avruch J. Regulation of the MST1 kinase by autophosphorylation, by the growth inhibitory proteins, RASSF1 and NORE1, and by Ras. Biochem. J. 2004, 381:453-462.
31. Sarbassov D.D., Ali S.M., Kim D.H., Guertin D.A., Latek R.R., Erdjument-Bromage H., Tempst P., Sabatini D.M. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr. Biol. 2004, 14:1296-1302.
32. Sarbassov D.D., Guertin D.A., Ali S.M., Sabatini D.M. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005, 307:1098-1101.
33. Sarbassov D.D., Ali S.M., Sengupta S., Sheen J.H., Hsu P.P., Bagley A.F., Markhard A.L., Sabatini D.M. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol. Cell 2006, 22:159-168.
34. Sciarretta S., Volpe M., Sadoshima J. Mammalian target of rapamycin signaling in cardiac physiology and disease. Circ. Res. 2014, 114:549-564.
35. Shende P., Plaisance I., Morandi C., Pellieux C., Berthonneche C., Zorzato F., Krishnan J., Lerch R., Hall M.N., Rüegg M.A., et al. Cardiac raptor ablation impairs adaptive hypertrophy, alters metabolic gene expression, and causes heart failure in mice. Circulation 2011, 123:1073-1082.
36. Shiota C., Woo J.T., Lindner J., Shelton K.D., Magnuson M.A. Multiallelic disruption of the rictor gene in mice reveals that mTOR complex 2 is essential for fetal growth and viability. Dev. Cell 2006, 11:583-589.
37. Tamai T., Yamaguchi O., Hikoso S., Takeda T., Taneike M., Oka T., Oyabu J., Murakawa T., Nakayama H., Uno Y., et al. Rheb (Ras homologue enriched in brain)-dependent mammalian target of rapamycin complex 1 (mTORC1) activation becomes indispensable for cardiac hypertrophic growth after early postnatal period. J.Biol. Chem. 2013, 288:10176-10187.
38. Thoreen C.C., Kang S.A., Chang J.W., Liu Q., Zhang J., Gao Y., Reichling L.J., Sim T., Sabatini D.M., Gray N.S. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J.Biol. Chem. 2009, 284:8023-8032.
39. Treins C., Warne P.H., Magnuson M.A., Pende M., Downward J. Rictor is a novel target of p70 S6 kinase-1. Oncogene 2010, 29:1003-1016.
40. Tumaneng K., Schlegelmilch K., Russell R.C., Yimlamai D., Basnet H., Mahadevan N., Fitamant J., Bardeesy N., Camargo F.D., Guan K.L. YAP mediates crosstalk between the Hippo and PI(3)K-TOR pathways by suppressing PTEN via miR-29. Nat. Cell Biol. 2012, 14:1322-1329.
41. Völkers M., Konstandin M.H., Doroudgar S., Toko H., Quijada P., Din S., Joyo A., Ornelas L., Samse K., Thuerauf D.J., et al. Mechanistic target of rapamycin complex 2 protects the heart from ischemic damage. Circulation 2013, 128:2132-2144.
42. Wullschleger S., Loewith R., Hall M.N. TOR signaling in growth and metabolism. Cell 2006, 124:471-484.
43. Xie X., Zhang D., Zhao B., Lu M.K., You M., Condorelli G., Wang C.Y., Guan K.L. IkappaB kinase epsilon and TANK-binding kinase 1 activate AKT by direct phosphorylation. Proc. Natl. Acad. Sci. USA 2011, 108:6474-6479.
44. Yamamoto S., Yang G., Zablocki D., Liu J., Hong C., Kim S.J., Soler S., Odashima M., Thaisz J., Yehia G., et al. Activation of Mst1 causes dilated cardiomyopathy by stimulating apoptosis without compensatory ventricular myocyte hypertrophy. J.Clin. Invest. 2003, 111:1463-1474.
45. Yang Q., Inoki K., Ikenoue T., Guan K.L. Identification of Sin1 as an essential TORC2 component required for complex formation and kinase activity. Genes Dev. 2006, 20:2820-2832.
46. Yano T., Ferlito M., Aponte A., Kuno A., Miura T., Murphy E., Steenbergen C. Pivotal role of mTORC2 and involvement of ribosomal protein S6 in cardioprotective signaling. Circ. Res. 2014, 114:1268-1280.
47. Yu F.X., Guan K.L. The Hippo pathway: regulators and regulations. Genes Dev. 2013, 27:355-371.
48. Zhang D., Contu R., Latronico M.V., Zhang J., Rizzi R., Catalucci D., Miyamoto S., Huang K., Ceci M., Gu Y., et al. MTORC1 regulates cardiac function and myocyte survival through 4E-BP1 inhibition in mice. J.Clin. Invest. 2010, 120:2805-2816.
49. Zhao B., Li L., Wang L., Wang C.Y., Yu J., Guan K.L. Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis. Genes Dev. 2012, 26:54-68.
50. Zhu Y., Pires K.M., Whitehead K.J., Olsen C.D., Wayment B., Zhang Y.C., Bugger H., Ilkun O., Litwin S.E., Thomas G., et al. Mechanistic target of rapamycin (Mtor) is essential for murine embryonic heart development and growth. PLoS ONE 2013, 8:e54221.
51. Zi M., Maqsood A., Prehar S., Mohamed T.M., Abou-Leisa R., Robertson A., Cartwright E.J., Ray S.G., Oh S., Lim D.S., et al. The mammalian Ste20-like kinase 2 (Mst2) modulates stress-induced cardiac hypertrophy. J.Biol. Chem. 2014, 289:24275-24288.