mTOR attenuates the inflammatory response in cardiomyocytes and prevents cardiac dysfunction in pathological hypertrophy

American Journal of Physiology - Cell Physiology

Volumn 299, Issue 6, 2010, Pages

  Song, Xiaoxiao ^a,b   Kusakari, Yoichiro ^a   Xiao, Chun Yang ^a   Kinsella, Stuart D ^a   Rosenberg, Michael A ^a   Scherrer Crosbie, Marielle ^c   Hara, Kenta ^d   Rosenzweig, Anthony ^a   Matsui, Takashi ^a,e  

^a HARVARD MEDICAL SCHOOL   (United States)

^b ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d KOBE UNIVERSITY   (Japan)

^e UNIVERSITY OF HAWAII   (United States)

Author keywords

Cardiac hypertrophy; Heart failure; Inflammation; Mammalian target of rapamycin; Transgenic mice

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MAMMALIAN TARGET OF RAPAMYCIN; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; FIBROSING ALVEOLITIS; HEART FAILURE; HEART HYPERTROPHY; HEART LEFT VENTRICLE PRESSURE; HEART MUSCLE CELL; HEART PROTECTION; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; CARDIOMEGALY; FEMALE; HEART; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-6; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MIDDLE AGED; MYOCYTES, CARDIAC; RATS; TOR SERINE-THREONINE KINASES;

MAMMALIA; MUS; MUS MUSCULUS;

EID: 78649668307     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00338.2010     Document Type: Article

References (59)

1. Asehnoune K, Strassheim D, Mitra S, Kim JY, Abraham E. Involvement of reactive oxygen species in Toll-like receptor 4-dependent activation of NF-kappa B. J Immunol 172: 2522-2529, 2004.
2. Aukrust P, Gullestad L, Ueland T, Damas JK, Yndestad A. Inflammatory and anti-inflammatory cytokines in chronic heart failure: potential therapeutic implications. Ann Med 37: 74-85, 2005.
3. Avruch J, Hara K, Lin Y, Liu M, Long X, Ortiz-Vega S, Yonezawa K. Insulin and amino-acid regulation of mTOR signaling and kinase activity through the Rheb GTPase. Oncogene 25: 6361-6372, 2006. (Pubitemid 44596154)
4. Berenji K, Drazner MH, Rothermel BA, Hill JA. Does load-induced ventricular hypertrophy progress to systolic heart failure? Am J Physiol Heart Circ Physiol 289: H8-H16, 2005.
5. Chen MM, Lam A, Abraham JA, Schreiner GF, Joly AH. CTGF expression is induced by TGF- beta in cardiac fibroblasts and cardiac myocytes: a potential role in heart fibrosis. J Mol Cell Cardiol 32: 1805-1819, 2000.
6. Claycomb WC, Lanson NA Jr, Stallworth BS, Egeland DB, Delcarpio JB, Bahinski A, Izzo NJ Jr. HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci USA 95: 2979-2984, 1998.
7. Diaz JA, Booth AJ, Lu G, Wood SC, Pinsky DJ, Bishop DK. Critical role for IL-6 in hypertrophy and fibrosis in chronic cardiac allograft rejection. Am J Transplant 9: 1773-1783, 2009.
8. Diwan A, Tran T, Misra A, Mann DL. Inflammatory mediators and the failing heart: a translational approach. Curr Mol Med 3: 161-182, 2003.
9. El-Menyar AA. Cytokines and myocardial dysfunction: state of the art. J Card Fail 14: 61-74, 2008.
10. Feldman ME, Apsel B, Uotila A, Loewith R, Knight ZA, Ruggero D, Shokat KM. Active-site inhibitors of mTOR target rapamycin-resistant outputs of mTORC1 and mTORC2. PLoS Biol 7: e38, 2009.
11. Ferrari R. Interleukin-6: a neurohumoral predictor of prognosis in patients with heart failure: light and shadow. Eur Heart J 23: 9-10, 2002.
12. Frantz S, Kobzik L, Kim YD, Fukazawa R, Medzhitov R, Lee RT, Kelly RA. Toll4 (TLR4) expression in cardiac myocytes in normal and failing myocardium. J Clin Invest 104: 271-280, 1999.
13. Fredj S, Bescond J, Louault C, Delwail A, Lecron JC, Potreau D. Role of interleukin-6 in cardiomyocyte/cardiac fibroblast interactions during myocyte hypertrophy and fibroblast proliferation. J Cell Physiol 204: 428-436, 2005. (Pubitemid 40934637)
14. Frey N, Katus HA, Olson EN, Hill JA. Hypertrophy of the heart: a new therapeutic target? Circulation 109: 1580-1589, 2004.
15. Gerdes AM, Iervasi G. Thyroid replacement therapy and heart failure. Circulation 122: 385-393, 2010.
16. Gu JQ, Ikuyama S, Wei P, Fan B, Oyama J, Inoguchi T, Nishimura J. Pycnogenol, an extract from French maritime pine, suppresses Toll-like receptor 4-mediated expression of adipose differentiation-related protein in macrophages. Am J Physiol Endocrinol Metab 295: E1390-E1400, 2008.
17. Gunther S, Grossman W. Determinants of ventricular function in pressure-overload hypertrophy in man. Circulation 59: 679-688, 1979. (Pubitemid 9154960)
18. Hara K, Maruki Y, Long X, Yoshino K, Oshiro N, Hidayat S, Tokunaga C, Avruch J, Yonezawa K. Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 110: 177-189, 2002.
19. Harrington LS, Findlay GM, Lamb RF. Restraining PI3K: mTOR signalling goes back to the membrane. Trends Biochem Sci 30: 35-42, 2005.
20. Hedayat M, Mahmoudi MJ, Rose NR, Rezaei N. Proinflammatory cytokines in heart failure: double-edged swords. Heart Fail Rev 15: 543-562, 2010.
21. Herskowitz A, Choi S, Ansari AA, Wesselingh S. Cytokine mRNA expression in postischemic/reperfused myocardium. Am J Pathol 146: 419-428, 1995.
22. Jacinto E, Facchinetti V, Liu D, Soto N, Wei S, Jung SY, Huang Q, Qin J, Su B. SIN1/MIP1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificity. Cell 127: 125-137, 2006.
23. Janes MR, Limon JJ, So L, Chen J, Lim RJ, Chavez MA, Vu C, Lilly MB, Mallya S, Ong ST, Konopleva M, Martin MB, Ren P, Liu Y, Rommel C, Fruman DA. Effective and selective targeting of leukemia cells using a TORC1/2 kinase inhibitor. Nat Med 16: 205-213, 2010.
24. Jug B, Salobir BG, Vene N, Sebestjen M, Sabovic M, Keber I. Interleukin-6 is a stronger prognostic predictor than high-sensitive C-reactive protein in patients with chronic stable heart failure. Heart Vessels 24: 271-276, 2009.
25. Khaper N, Bryan S, Dhingra S, Singal R, Bajaj A, Pathak CM, Singal PK. Targeting the vicious inflammation-oxidative stress cycle for the management of heart failure. Antioxid Redox Signal 13: 1033-1049, 2010.
26. Koitabashi N, Arai M, Kogure S, Niwano K, Watanabe A, Aoki Y, Maeno T, Nishida T, Kubota S, Takigawa M, Kurabayashi M. Increased connective tissue growth factor relative to brain natriuretic peptide as a determinant of myocardial fibrosis. Hypertension 49: 1120-1127, 2007.
27. Kurt-Jones EA, Chan M, Zhou S, Wang J, Reed G, Bronson R, Arnold MM, Knipe DM, Finberg RW. Herpes simplex virus 1 interaction with Toll-like receptor 2 contributes to lethal encephalitis. Proc Natl Acad Sci USA 101: 1315-1320, 2004.
28. Kuzman JA, O'Connell TD, Gerdes AM. Rapamycin prevents thyroid hormone-induced cardiac hypertrophy. Endocrinology 148: 3477-3484, 2007.
29. Kuzman JA, Vogelsang KA, Thomas TA, Gerdes AM. L-Thyroxine activates Akt signaling in the heart. J Mol Cell Cardiol 39: 251-258, 2005.
30. Makarenko I, Opitz CA, Leake MC, Neagoe C, Kulke M, Gwathmey JK, del Monte F, Hajjar RJ, Linke WA. Passive stiffness changes caused by upregulation of compliant titin isoforms in human dilated cardiomyopathy hearts. Circ Res 95: 708-716, 2004.
31. Mao JH, Kim IJ, Wu D, Climent J, Kang HC, DelRosario R, Balmain A. FBXW7 targets mTOR for degradation and cooperates with PTEN in tumor suppression. Science 321: 1499-1502, 2008.
32. Matsui T, Li L, Wu JC, Cook SA, Nagoshi T, Picard MH, Liao R, Rosenzweig A. Phenotypic spectrum caused by transgenic overexpression of activated Akt in the heart. J Biol Chem 277: 22896-22901, 2002.
33. Matsui T, Nagoshi T, Hong EG, Luptak I, Hartil K, Li L, Gorovits N, Charron MJ, Kim JK, Tian R, Rosenzweig A. Effects of chronic Akt activation on glucose uptake in the heart. Am J Physiol Endocrinol Metab 290: E789-E797, 2006.
34. Matsui T, Tao J, del Monte F, Lee KH, Li L, Picard M, Force TL, Franke TF, Hajjar RJ, Rosenzweig A. Akt activation preserves cardiac function and prevents injury after transient cardiac ischemia in vivo. Circulation 104: 330-335, 2001.
35. Matsui Y, Sadoshima J. Rapid upregulation of CTGF in cardiac myocytes by hypertrophic stimuli: implication for cardiac fibrosis and hypertrophy. J Mol Cell Cardiol 37: 477-481, 2004.
36. McMullen JR, Sherwood MC, Tarnavski O, Zhang L, Dorfman AL, Shioi T, Izumo S. Inhibition of mTOR signaling with rapamycin regresses established cardiac hypertrophy induced by pressure overload. Circulation 109: 3050-3055, 2004.
37. McMullen JR, Shioi T, Zhang L, Tarnavski O, Sherwood MC, Dorfman AL, Longnus S, Pende M, Martin KA, Blenis J, Thomas G, Izumo S. Deletion of ribosomal S6 kinases does not attenuate pathological, physiological, or insulin-like growth factor 1 receptor-phosphoinositide 3-kinase-induced cardiac hypertrophy. Mol Cell Biol 24: 6231-6240, 2004.
38. Medzhitov R. Origin and physiological roles of inflammation. Nature 454: 428-435, 2008.
39. Medzhitov R, Preston-Hurlburt P, Janeway CA Jr. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388: 394-397, 1997.
40. Minhajuddin M, Bijli KM, Fazal F, Sassano A, Nakayama KI, Hay N, Platanias LC, Rahman A. Protein kinase C-delta and phosphatidylinositol 3-kinase/Akt activate mammalian target of rapamycin to modulate NF-kappaB activation and intercellular adhesion molecule-1 (ICAM-1) expression in endothelial cells. J Biol Chem 284: 4052-4061, 2009.
41. Ng SB, Tan YH, Guy GR. Differential induction of the interleukin-6 gene by tumor necrosis factor and interleukin-1. J Biol Chem 269: 19021-19027, 1994.
42. Rudolph A, Abdel-Aty H, Bohl S, Boye P, Zagrosek A, Dietz R, Schulz-Menger J. Noninvasive detection of fibrosis applying contrast-enhanced cardiac magnetic resonance in different forms of left ventricular hypertrophy relation to remodeling. J Am Coll Cardiol 53: 284-291, 2009.
43. Saemann MD, Haidinger M, Hecking M, Horl WH, Weichhart T. The multifunctional role of mTOR in innate immunity: implications for transplant immunity. Am J Transplant 9: 2655-2661, 2009.
44. Saric J, Li JV, Swann JR, Utzinger J, Calvert G, Nicholson JK, Dirnhofer S, Dallman MJ, Bictash M, Holmes E. Integrated cytokine and metabolic analysis of pathological responses to parasite exposure in rodents. J Proteome Res 9: 2255-2264, 2010.
45. Schmitz F, Heit A, Dreher S, Eisenacher K, Mages J, Haas T, Krug A, Janssen KP, Kirschning CJ, Wagner H. Mammalian target of rapamycin (mTOR) orchestrates the defense program of innate immune cells. Eur J Immunol 38: 2981-2992, 2008.
46. Shen WH, Chen Z, Shi S, Chen H, Zhu W, Penner A, Bu G, Li W, Boyle DW, Rubart M, Field LJ, Abraham R, Liechty EA, Shou W. Cardiac restricted overexpression of kinase-dead mammalian target of rapamycin (mTOR) mutant impairs the mTOR-mediated signaling and cardiac function. J Biol Chem 283: 13842-13849, 2008.
47. Shioi T, Matsumori A, Kihara Y, Inoko M, Ono K, Iwanaga Y, Yamada T, Iwasaki A, Matsushima K, Sasayama S. Increased expression of interleukin-1 beta and monocyte chemotactic and activating factor/monocyte chemoattractant protein-1 in the hypertrophied and failing heart with pressure overload. Circ Res 81: 664-671, 1997.
48. Shioi T, McMullen JR, Tarnavski O, Converso K, Sherwood MC, Manning WJ, Izumo S. Rapamycin attenuates load-induced cardiac hypertrophy in mice. Circulation 107: 1664-1670, 2003.
49. Shiojima I, Sato K, Izumiya Y, Schiekofer S, Ito M, Liao R, Colucci WS, Walsh K. Disruption of coordinated cardiac hypertrophy and angio-genesis contributes to the transition to heart failure. J Clin Invest 115: 2108-2118, 2005.
50. Soesanto W, Lin HY, Hu E, Lefler S, Litwin SE, Sena S, Abel ED, Symons JD, Jalili T. Mammalian target of rapamycin is a critical regulator of cardiac hypertrophy in spontaneously hypertensive rats. Hypertension 54: 1321-1327, 2009.
51. Takimoto E, Champion HC, Li M, Ren S, Rodriguez ER, Tavazzi B, Lazzarino G, Paolocci N, Gabrielson KL, Wang Y, Kass DA. Oxidant stress from nitric oxide synthase-3 uncoupling stimulates cardiac pathologic remodeling from chronic pressure load. J Clin Invest 115: 1221-1231, 2005.
52. Timmers L, Sluijter JP, van Keulen JK, Hoefer IE, Nederhoff MG, Goumans MJ, Doevendans PA, van Echteld CJ, Joles JA, Quax PH, Piek JJ, Pasterkamp G, de Kleijn DP. Toll-like receptor 4 mediates maladaptive left ventricular remodeling and impairs cardiac function after myocardial infarction. Circ Res 102: 257-264, 2008.
53. Weichhart T, Costantino G, Poglitsch M, Rosner M, Zeyda M, Stuhlmeier KM, Kolbe T, Stulnig TM, Horl WH, Hengstschlager M, Muller M, Saemann MD. The TSC-mTOR signaling pathway regulates the innate inflammatory response. Immunity 29: 565-577, 2008.
54. Xia Y, Lee K, Li N, Corbett D, Mendoza L, Frangogiannis NG. Characterization of the inflammatory and fibrotic response in a mouse model of cardiac pressure overload. Histochem Cell Biol 131: 471-481, 2009.
55. Xiao CY, Chen M, Zsengeller Z, Li H, Kiss L, Kollai M, Szabo C. Poly(ADP-ribose) polymerase promotes cardiac remodeling, contractile failure, and translocation of apoptosis-inducing factor in a murine experimental model of aortic banding and heart failure. J Pharmacol Exp Ther 312: 891-898, 2005.
56. Yang Q, Guan KL. Expanding mTOR signaling. Cell Res 17: 666-681, 2007.
57. Youker K, Smith CW, Anderson DC, Miller D, Michael LH, Rossen RD, Entman ML. Neutrophil adherence to isolated adult cardiac myocytes. Induction by cardiac lymph collected during ischemia and reperfusion. J Clin Invest 89: 602-609, 1992.
58. Zhang D, Contu R, Latronico MV, Zhang JL, Rizzi R, Catalucci D, Miyamoto S, Huang K, Ceci M, Gu Y, Dalton ND, Peterson KL, Guan KL, Brown JH, Chen J, Sonenberg N, Condorelli G. MTORC1 regulates cardiac function and myocyte survival through 4E-BP1 inhibition in mice. J Clin Invest 120: 2805-2816, 2010.
59. Zhang P, Xu X, Hu X, van Deel ED, Zhu G, Chen Y. Inducible nitric oxide synthase deficiency protects the heart from systolic overload-induced ventricular hypertrophy and congestive heart failure. Circ Res 100: 1089-1098, 2007.