Rapamycin protection of livers from ischemia and reperfusion injury is dependent on both autophagy induction and mammalian target of rapamycin complex 2-akt activation

Transplantation

Volumn 99, Issue 1, 2015, Pages 48-55

  Zhu, Jianjun ^a,b   Lu, Tianfei ^a,b   Yue, Shi ^a   Shen, Xiuda ^a   Gao, Feng ^a   Busuttil, Ronald W ^a   Kupiec Weglinski, Jerzy W ^a   Xia, Qiang ^b   Zhai, Yuan ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROQUINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; PROTEIN KINASE B; RAPAMYCIN; TORIN 1; TRICIRIBINE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; 1-(4-(4-PROPIONYLPIPERAZIN-1-YL)-3-(TRIFLUOROMETHYL)PHENYL)-9-(QUINOLIN-3-YL)BENZO(H)(1,6)NAPHTHYRIDIN-2(1H)-ONE; MULTIPROTEIN COMPLEX; NAPHTHYRIDINE DERIVATIVE; PROTECTIVE AGENT; PROTEIN KINASE INHIBITOR; TARGET OF RAPAMYCIN KINASE; TOR COMPLEX 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CELL DEATH; CELL PROTECTION; CELL STRESS; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; INNATE IMMUNITY; LIVER CELL; LIVER ISCHEMIA; LIVER PROTECTION; MALE; MOUSE; NONHUMAN; PATHOGENESIS; REGULATORY MECHANISM; REPERFUSION INJURY; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL LINE; DISEASE MODEL; DRUG EFFECTS; ENDOPLASMIC RETICULUM STRESS; ENZYMOLOGY; ISCHEMIA; LIVER; LIVER DISEASES; METABOLISM; PATHOLOGY;

ANIMALS; AUTOPHAGY; CELL LINE; CYTOPROTECTION; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; HEPATOCYTES; LIVER; LIVER DISEASES; MALE; MICE, INBRED C57BL; MULTIPROTEIN COMPLEXES; NAPHTHYRIDINES; PROTECTIVE AGENTS; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; REPERFUSION INJURY; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES; TUMOR NECROSIS FACTOR-ALPHA; WARM ISCHEMIA;

EID: 84920155065     PISSN: 00411337     EISSN: None     Source Type: Journal    
DOI: 10.1097/TP.0000000000000476     Document Type: Article

References (53)

1. Kawahara T, Asthana S, Kneteman NM. m-TOR inhibitors: what role in liver transplantation? J Hepatol 2011;55:1441.
2. Otto G. Liver transplantation: an appraisal of the present situation. Dig Dis 2013;31:164.
3. Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell 2012;149:274.
4. Saemann MD, Haidinger M, Hecking M, et al. The multifunctional role of mTOR in innate immunity: implications for transplant immunity. Am J Transplant 2009;9:2655.
5. Thoreen CC, Kang SA, Chang JW, et al. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J Biol Chem2009;284:8023.
6. Weichhart T, Costantino G, Poglitsch M, et al. The TSC-mTOR signaling pathway regulates the innate inflammatory response. Immunity 2008;29:565.
7. Schmitz F, Heit A, Dreher S, et al. Mammalian target of rapamycin (mTOR) orchestrates the defense program of innate immune cells. Eur J Immunol 2008;38:2981.
8. Inoki K, KimJ, Guan KL. AMPK and mTOR in cellular energy homeostasis and drug targets. Annu Rev Pharmacol Toxicol 2012;52:381.
9. Kroemer G, Marino G, Levine B. Autophagy and the integrated stress response. Mol Cell 2010;40:280.
10. Gottlieb RA, Mentzer RM. Autophagy during cardiac stress: joys and frustrations of autophagy. Annu Rev Physiol 2010;72:45.
11. Murrow L, Debnath J. Autophagy as a stress-response and qualitycontrol mechanism: implications for cell injury and human disease. Annu Rev Pathol 2013;8:105.
12. Fang H, Liu A, Dahmen U, et al. Dual role of chloroquine in liver ischemia reperfusion injury: reduction of liver damage in early phase, but aggravation in late phase. Cell Death Dis 2013;4:e694.
13. Hwang SK, Kim HH. The functions of mTOR in ischemic diseases. BMB Rep 2011;44:506.
14. Sarbassov DD, Ali SM, Sengupta S, et al. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 2006;22:159.
15. Puglisi RN, Strande L, Santos M, et al. Beneficial effects of cyclosporine and rapamycin in small bowel ischemic injury. J Surg Res 1996;65:115.
16. Matsuda T, Yamaguchi Y, Matsumura F, et al. Immunosuppressants decrease neutrophil chemoattractant and attenuate ischemia/reperfusion injury of the liver in rats. J Trauma 1998;44:475.
17. Inman SR, Davis NA, Olson KM, et al. Rapamycin preserves renal function compared with cyclosporine A after ischemia/reperfusion injury. Urology 2003;62:750.
18. Lieberthal W, Fuhro R, Andry CC, et al. Rapamycin impairs recovery from acute renal failure: role of cell-cycle arrest and apoptosis of tubular cells. Am J Physiol Renal Physiol 2001;281:F693.
19. Loverre A, Ditonno P, Crovace A, et al. Ischemia-reperfusion induces glomerular and tubular activation of proinflammatory and antiapoptotic pathways: differential modulation by rapamycin. J Am Soc Nephrol 2004;15:2675.
20. Lui SL, Chan KW, Tsang R, et al. Effect of rapamycin on renal ischemiareperfusion injury in mice. Transpl Int 2006;19:834.
21. Serr F, Lauer H, Armann B, et al. Sirolimus improves earlymicrocirculation, but impairs regeneration after pancreatic ischemia-reperfusion injury. Am J Transplant 2007;7:48.
22. Khan S, Salloum F, Das A, et al. Rapamycin confers preconditioning-like protection against ischemia-reperfusion injury in isolated mouse heart and cardiomyocytes. J Mol Cell Cardiol 2006;41:256.
23. Das A, Salloum FN, Durrant D, et al. Rapamycin protects against myocardial ischemia-reperfusion injury through JAK2-STAT3 signaling pathway. J Mol Cell Cardiol 2012;53:858.
24. Fuller TF, Freise CE, Serkova N, et al. Sirolimus delays recovery of rat kidney transplants after ischemia-reperfusion injury. Transplantation 2003;76:1594.
25. Gonçalves GM, Cenedeze MA, Feitoza CQ, et al. The role of heme oxygenase 1 in rapamycin-induced renal dysfunction after ischemia and reperfusion injury. Kidney Int 2006;70:1742.
26. Chen L-P, Zhang Q-H, Chen G, et al. Rapamycin inhibits cholangiocyte regeneration by blocking interleukin-6-induced activation of signal transducer and activator of transcription 3 after liver transplantation. Liver Transpl 2010;16:204.
27. Carloni S, Buonocore G, Balduini W. Protective role of autophagy in neonatal hypoxia-ischemia induced brain injury. Neurobiol Dis 2008;32:329.
28. Carloni S, Buonocore G, Longini M, et al. Inhibition of rapamycin-induced autophagy causes necrotic cell death associated with Bax/Bad mitochondrial translocation. Neuroscience 2012;203:160.
29. Jiang M, Wei Q, Dong G, et al. Autophagy in proximal tubules protects against acute kidney injury. Kidney Int 2012;82:1271.
30. Nakagawa S, Nishihara K, Inui K-i, et al. Involvement of autophagy in the pharmacological effects of the mTOR inhibitor everolimus in acute kidney injury. Eur J Pharmacol 2012;696:143.
31. Kang J-W, Cho H-I, Lee S-M. Melatonin Inhibits mTOR-dependent autophagy during liver ischemia/reperfusion. Cell Physiol Biochem 2014;33:23.
32. Li Q, Zhang T, Wang J, et al. Rapamycin attenuates mitochondrial dysfunction via activation of mitophagy in experimental ischemic stroke. Biochem Biophys Res Commun 2014;444:182.
33. Przyklenk K, Dong Y, Undyala VV, et al. Autophagy as a therapeutic target for ischaemia /reperfusion injury? Concepts, controversies, and challenges. Cardiovasc Res 2012;94:197.
34. Yan L, Vatner DE, Kim SJ, et al. Autophagy in chronically ischemic myocardium. Proc Natl Acad Sci U S A 2005;102:13807.
35. Matsui Y, Takagi H, Qu X, et al. Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ Res 2007;100:914.
36. French CJ, Taatjes DJ, Sobel BE. Autophagy in myocardium of murine hearts subjected to ischemia followed by reperfusion. Histochem Cell Biol 2010;134:519.
37. Loos B, Genade S, Ellis B, et al. At the core of survival: autophagy delays the onset of both apoptotic and necrotic cell death in a model of ischemic cell injury. Exp Cell Res 2011;317:1437.
38. Kim JS, Nitta T, Mohuczy D, et al. Impaired autophagy: a mechanism of mitochondrial dysfunction in anoxic rat hepatocytes. Hepatology 2008;47:1725.
39. Hamacher-Brady A, Brady NR, Gottlieb RA. Enhancing macroautophagy protects against ischemia/reperfusion injury in cardiac myocytes. J Biol Chem 2006;281:29776.
40. Gurusamy N, Lekli I, Gorbunov NV, et al. Cardioprotection by adaptation to ischaemia augments autophagy in association with BAG-1 protein. J Cell Mol Med 2009;13:373.
41. Hariharan N, Zhai P, Sadoshima J. Oxidative stress stimulates autophagic flux during ischemia/reperfusion. Antioxid Redox Signal 2011;14:2179.
42. Zhai P, Sciarretta S, Galeotti J, et al. Differential roles of GSK-3beta during myocardial ischemia and ischemia/reperfusion. Circ Res. 2011;109:502.
43. TanemuraM, Ohmura Y, Deguchi T, et al. Rapamycin causes upregulation of autophagy and impairs islets function both in vitro and in vivo. Am J Transplant 2012;12:102.
44. Wang JH, Ahn IS, Fischer TD, et al. Autophagy suppresses agedependent ischemia and reperfusion injury in livers of mice. Gastroenterology 2011;141:2188.
45. Ni HM, Bockus A, Boggess N, et al. Activation of autophagy protects against acetaminophen-induced hepatotoxicity. Hepatology 2012;55:222.
46. Volkers M, Konstandin MH, Doroudgar S, et al. Mechanistic target of rapamycin complex 2 protects the heart from ischemic damage. Circulation 2013;128:2132.
47. Vasudevan KM, Garraway LA. AKT signaling in physiology and disease. Curr Top Microbiol Immunol 2010;347:105.
48. Zhu M, Feng J, Lucchinetti E, et al. Ischemic postconditioning protects remodeled myocardium via the PI3K-PKB/Akt reperfusion injury salvage kinase pathway. Cardiovasc Res 2006;72:152.
49. Kamo N, Ke B, Busuttil RW, et al. PTEN-mediated Akt/beta-catenin/ Foxo1 signaling regulates innate immune responses in mouse liver ischemia/reperfusion injury. Hepatology 2013;57:289.
50. Julien LA, Carriere A, Moreau J, et al. mTORC1-activated S6K1 phosphorylates Rictor on threonine 1135 and regulates mTORC2 signaling. Mol Cell Biol 2010;30:908.
51. Shen XD, Ke B, Zhai Y, et al. CD154-CD40 T-cell costimulation pathway is required in the mechanism of hepatic ischemia/reperfusion injury, and its blockade facilitates and depends on heme oxygenase-1 mediated cytoprotection. Transplantation 2002;74:315.
52. Suzuki S, Toledo-Pereyra LH, Rodriguez FJ, et al. Neutrophil infiltration as an important factor in liver ischemia and reperfusion injury. Modulating effects of FK506 and cyclosporine. Transplantation 1993;55:1265.
53. Zhai Y, Shen XD, Gao F, et al. CXCL10 regulates liver innate immune response against ischemia and reperfusion injury. Hepatology 2008;47:207.