Augmenter of liver regeneration regulates autophagy in renal ischemia–reperfusion injury via the AMPK/mTOR pathway

Springer Science and Business Media LLC - Tập 22 Số 7 - Trang 955-969 - 2017
Tao Pu1, Xiaohui Liao2, Hang Sun1, Hui Guo1, Xiao Jiang1, Junbo Peng1, Ling Zhang2, Qi Liu1
1Key Laboratory of Molecular Biology for Infectious Diseases (Ministry of Education), Institute for Viral Hepatitis, Department of Infectious Diseases, The Second Affiliated Hospital, Chongqing Medical University, Chongqing, People’s Republic of China
2Department of Nephrology, The Second Affiliated Hospital, Chongqing Medical University, Chongqing, People’s Republic of China

Tóm tắt

Từ khóa


Tài liệu tham khảo

Basile DP, Yoder MC (2014) Renal endothelial dysfunction in acute kidney ischemia reperfusion injury. Cardiovasc Hematol Disord Drug Targets 14(1):3–14

Yeh CH, Hsu SP, Yang CC, Chien CT, Wang NP (2010) Hypoxic preconditioning reinforces HIF-alpha-dependent HSP70 signaling to reduce ischemic renal failure-induced renal tubular apoptosis and autophagy. Life Sci 86(3–4):115–123. doi: 10.1016/j.lfs.2009.11.022

Nakagawa S, Nishihara K, Inui K, Masuda S (2012) Involvement of autophagy in the pharmacological effects of the mTOR inhibitor everolimus in acute kidney injury. Eur J Pharmacol 696(1–3):143–154. doi: 10.1016/j.ejphar.2012.09.010

Turkmen K, Martin J, Akcay A, Nguyen Q, Ravichandran K, Faubel S, Pacic A, Ljubanovic D, Edelstein CL, Jani A (2011) Apoptosis and autophagy in cold preservation ischemia. Transplantation 91(11):1192–1197. doi: 10.1097/TP.0b013e31821ab9c8

Kimura T, Takabatake Y, Takahashi A, Kaimori JY, Matsui I, Namba T, Kitamura H, Niimura F, Matsusaka T, Soga T, Rakugi H, Isaka Y (2011) Autophagy protects the proximal tubule from degeneration and acute ischemic injury. J Am Soc Nephrol 22(5):902–913. doi: 10.1681/ASN.2010070705

Liu S, Hartleben B, Kretz O, Wiech T, Igarashi P, Mizushima N, Walz G, Huber TB (2012) Autophagy plays a critical role in kidney tubule maintenance, aging and ischemia-reperfusion injury. Autophagy 8(5):826–837. doi: 10.4161/auto.19419

Jiang M, Wei Q, Dong G, Komatsu M, Su Y, Dong Z (2012) Autophagy in proximal tubules protects against acute kidney injury. Kidney Int 82(12):1271–1283. doi: 10.1038/ki.2012.261

Morselli E, Maiuri MC, Markaki M, Megalou E, Pasparaki A, Palikaras K, Criollo A, Galluzzi L, Malik SA, Vitale I, Michaud M, Madeo F, Tavernarakis N, Kroemer G (2010) Caloric restriction and resveratrol promote longevity through the Sirtuin-1-dependent induction of autophagy. Cell Death Dis 1:e10. doi: 10.1038/cddis.2009.8

Lieberthal W, Fuhro R, Andry CC, Rennke H, Abernathy VE, Koh JS, Valeri R, Levine JS (2001) Rapamycin impairs recovery from acute renal failure: role of cell-cycle arrest and apoptosis of tubular cells. Am J Physiol Renal Physiol 281(4):F693–F706

Lieberthal W, Fuhro R, Andry C, Patel V, Levine JS (2006) Rapamycin delays but does not prevent recovery from acute renal failure: role of acquired tubular resistance. Transplantation 82(1):17–22

Mordas A, Tokatlidis K (2015) The MIA pathway: a key regulator of mitochondrial oxidative protein folding and biogenesis. Acc Chem Res 48(8):2191–2199. doi: 10.1021/acs.accounts.5b00150

Gandhi CR (2012) Augmenter of liver regeneration. Fibrogenesis Tissue Repair 5(1):10. doi: 10.1186/1755-1536-5-10

Polimeno L, Pesetti B, De Santis F, Resta L, Rossi R, De Palma A, Girardi B, Amoruso A, Francavilla A (2012) Decreased expression of the augmenter of liver regeneration results in increased apoptosis and oxidative damage in human-derived glioma cells. Cell Death Dis 3:e289. doi: 10.1038/cddis.2012.25

Liao XH, Zhang L, Tang XP, Liu Q, Sun H (2009) Expression of augmenter of liver regeneration in rats with gentamicin-induced acute renal failure and its protective effect on kidney. Ren Fail 31(10):946–955. doi: 10.3109/08860220903216154

Liao XH, Zhang L, Liu Q, Sun H, Peng CM, Guo H (2010) Augmenter of liver regeneration protects kidneys from ischaemia/reperfusion injury in rats. Nephrology Dial Transpl Off Publ Eur Dial Transpl Assoc Eur Renal Assoc 25(9):2921–2929. doi: 10.1093/ndt/gfq151

Xia N, Yan RY, Liu Q, Liao XH, Sun H, Guo H, Zhang L (2015) Augmenter of liver regeneration plays a protective role against hydrogen peroxide-induced oxidative stress in renal proximal tubule cells. Apoptosis 20(4):423–432. doi: 10.1007/s10495-015-1096-2

Rambold AS, Lippincott-Schwartz J (2011) Mechanisms of mitochondria and autophagy crosstalk. Cell Cycle 10(23):4032–4038. doi: 10.4161/cc.10.23.18384

Todd LR, Gomathinayagam R, Sankar U (2010) A novel Gfer-Drp1 link in preserving mitochondrial dynamics and function in pluripotent stem cells. Autophagy 6(6):821–822. doi: 10.1091/mbc.E09-11-0937

Shi HB, Sun HQ, Shi HL, Ren F, Chen Y, Chen DX, Lou JL, Duan ZP (2015) Autophagy in anti-apoptotic effect of augmenter of liver regeneration in HepG2 cells. World J Gastroenterol 21(17):5250–5258. doi: 10.3748/wjg.v21.i17.5250

Chien CT, Shyue SK, Lai MK (2007) Bcl-xL augmentation potentially reduces ischemia/reperfusion induced proximal and distal tubular apoptosis and autophagy. Transplantation 84(9):1183–1190. doi: 10.1097/01.tp.0000287334.38933.e3

Isaka Y, Suzuki C, Abe T, Okumi M, Ichimaru N, Imamura R, Kakuta Y, Matsui I, Takabatake Y, Rakugi H, Shimizu S, Takahara S (2009) Bcl-2 protects tubular epithelial cells from ischemia/reperfusion injury by dual mechanisms. Transplant Proc 41(1):52–54. doi: 10.1016/j.transproceed.2008.10.026

Wu HH, Hsiao TY, Chien CT, Lai MK (2009) Ischemic conditioning by short periods of reperfusion attenuates renal ischemia/reperfusion induced apoptosis and autophagy in the rat. J Biomed Sci 16:19. doi: 10.1186/1423-0127-16-19

Sciarretta S, Hariharan N, Monden Y, Zablocki D, Sadoshima J (2011) Is autophagy in response to ischemia and reperfusion protective or detrimental for the heart? Pediatr Cardiol 32(3):275–281. doi: 10.1007/s00246-010-9855-x

Liao XH, Chen GT, Li Y, Zhang L, Liu Q, Sun H, Guo H (2012) Augmenter of liver regeneration attenuates tubular cell apoptosis in acute kidney injury in rats: the possible mechanisms. Ren Fail 34(5):590–599. doi: 10.3109/0886022x.2012.664470

Yan R, Li Y, Zhang L, Xia N, Liu Q, Sun H, Guo H (2015) Augmenter of liver regeneration attenuates inflammation of renal ischemia/reperfusion injury through the NF-kappa B pathway in rats. Int Urol Nephrol 47(5):861–868. doi: 10.1007/s11255-015-0954-8

Jiang M, Liu K, Luo J, Dong Z (2010) Autophagy is a renoprotective mechanism during in vitro hypoxia and in vivo ischemia-reperfusion injury. Am J Pathol 176(3):1181–1192. doi: 10.2353/ajpath.2010.090594

Dong W, Wang H, Shahzad K, Bock F, Al-Dabet MM, Ranjan S, Wolter J, Kohli S, Hoffmann J, Dhople VM, Zhu C, Lindquist JA, Esmon CT, Grone E, Grone HJ, Madhusudhan T, Mertens PR, Schluter D, Isermann B (2015) Activated protein C ameliorates renal ischemia-reperfusion injury by restricting Y-box binding protein-1 ubiquitination. J Am Soc Nephrol 26(11):2789–2799. doi: 10.1681/ASN.2014080846

Zhang ZS, Yang DY, Fu YB, Zhang L, Zhao QP, Li G (2015) Knockdown of CkrL by shRNA deteriorates hypoxia/reoxygenation-induced H9C2 cardiomyocyte apoptosis and survival inhibition Via Bax and downregulation of P-Erk1/2. Cell Biochem Funct 33(2):80–88. doi: 10.1002/cbf.3093

Wang LT, Chen BL, Wu CT, Huang KH, Chiang CK, Hwa Liu S (2013) Protective role of AMP-activated protein kinase-evoked autophagy on an in vitro model of ischemia/reperfusion-induced renal tubular cell injury. PloS One 8(11):e79814. doi: 10.1371/journal.pone.0079814

Dayoub R, Vogel A, Schuett J, Lupke M, Spieker SM, Kettern N, Hildt E, Melter M, Weiss TS (2013) Nrf2 activates augmenter of liver regeneration (ALR) via antioxidant response element and links oxidative stress to liver regeneration. Mol Med 19:237–244. doi: 10.2119/molmed.2013.00027

Liu M, Grigoryev DN, Crow MT, Haas M, Yamamoto M, Reddy SP, Rabb H (2009) Transcription factor Nrf2 is protective during ischemic and nephrotoxic acute kidney injury in mice. Kidney Int 76(3):277–285. doi: 10.1038/ki.2009.157

Cao Y, Fu YL, Yu M, Yue PB, Ge CH, Xu WX, Zhan YQ, Li CY, Li W, Wang XH, Wang ZD, Li YH, Yang XM (2009) Human augmenter of liver regeneration is important for hepatoma cell viability and resistance to radiation-induced oxidative stress. Free Rad Biol Med 47(7):1057–1066. doi: 10.1016/j.freeradbiomed.2009.07.017

Sun GY, Dong LY, An W (2014) Involvement of hepatic stimulator substance in the regulation of hepatoblast maturation into hepatocytes in vitro. Stem Cells Dev 23(14):1675–1687. doi: 10.1089/scd.2013.0468

Li Y, Farooq M, Sheng D, Chandramouli C, Lan T, Mahajan NK, Kini RM, Hong Y, Lisowsky T, Ge R (2012) Augmenter of liver regeneration (alr) promotes liver outgrowth during zebrafish hepatogenesis. PloS One 7(1):e30835. doi: 10.1371/journal.pone.0030835

Grahammer F, Haenisch N, Steinhardt F, Sandner L, Roerden M, Arnold F, Cordts T, Wanner N, Reichardt W, Kerjaschki D, Ruegg MA, Hall MN, Moulin P, Busch H, Boerries M, Walz G, Artunc F, Huber TB (2014) mTORC1 maintains renal tubular homeostasis and is essential in response to ischemic stress. Proc Natl Acad Sci USA 111(27):E2817–E2826. doi: 10.1073/pnas.1402352111

Hardie DG (2011) AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev 25(18):1895–1908. doi: 10.1101/gad.17420111

Kim TW, Kim YJ, Kim HT, Park SR, Lee MY, Park YD, Lee CH, Jung JY (2016) NQO1 deficiency leads enhanced autophagy in cisplatin-induced acute kidney injury through the AMPK/TSC2/mTOR signaling pathway. Antioxid Redox Signal 24(15):867–883. doi: 10.1089/ars.2015.6386

Duan P, Hu C, Quan C, Yu T, Zhou W, Yuan M, Shi Y, Yang K (2016) 4-Nonylphenol induces apoptosis, autophagy and necrosis in Sertoli cells: involvement of ROS-mediated AMPK/AKT-mTOR and JNK pathways. Toxicology 341–343:28–40. doi: 10.1016/j.tox.2016.01.004

Alers S, Loffler AS, Wesselborg S, Stork B (2012) Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks. Mol Cell Biol 32(1):2–11. doi: 10.1128/MCB.06159-11

Kim J, Kundu M, Viollet B, Guan KL (2011) AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 13(2):132–141. doi: 10.1038/ncb2152

Polimeno L, Rossi R, Mastrodonato M, Montagnani M, Piscitelli D, Pesetti B, De Benedictis L, Girardi B, Resta L, Napoli A, Francavilla A (2013) Augmenter of liver regeneration, a protective factor against ROS-induced oxidative damage in muscle tissue of mitochondrial myopathy affected patients. Int J Biochem Cell Biol 45(11):2410–2419. doi: 10.1016/j.biocel.2013.07.010

Bolisetty S, Traylor AM, Kim J, Joseph R, Ricart K, Landar A, Agarwal A (2010) Heme oxygenase-1 inhibits renal tubular macroautophagy in acute kidney injury. J Am Soc Nephrol 21(10):1702–1712. doi: 10.1681/ASN.2010030238

Maiuri MC, Zalckvar E, Kimchi A, Kroemer G (2007) Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8(9):741–752. doi: 10.1038/nrm2239

Yang C, Kaushal V, Shah SV, Kaushal GP (2008) Autophagy is associated with apoptosis in cisplatin injury to renal tubular epithelial cells. Am J Physiol Renal Physiol 294(4):F777–F787. doi: 10.1152/ajprenal.00590.2007

Zeng Y, Li S, Wu J, Chen W, Sun H, Peng W, Yu X, Yang X (2014) Autophagy inhibitors promoted aristolochic acid I induced renal tubular epithelial cell apoptosis via mitochondrial pathway but alleviated nonapoptotic cell death in mouse acute aritolochic acid nephropathy model. Apoptosis Int J Program Cell Death 19(8):1215–1224. doi: 10.1007/s10495-014-0996-x

Guan X, Qian Y, Shen Y, Zhang L, Du Y, Dai H, Qian J, Yan Y (2015) Autophagy protects renal tubular cells against ischemia / reperfusion injury in a time-dependent manner. Cell Physiol Biochem 36(1):285–298. doi: 10.1159/000374071

Gandhi CR, Chaillet JR, Nalesnik MA, Kumar S, Dangi A, Demetris AJ, Ferrell R, Wu T, Divanovic S, Stankeiwicz T, Shaffer B, Stolz DB, Harvey SA, Wang J, Starzl TE (2015) Liver-specific deletion of augmenter of liver regeneration accelerates development of steatohepatitis and hepatocellular carcinoma in mice. Gastroenterology 148(2):379–391 e374. doi: 10.1053/j.gastro.2014.10.008

Ilowski M, Kleespies A, de Toni EN, Donabauer B, Jauch KW, Hengstler JG, Thasler WE (2011) Augmenter of liver regeneration (ALR) protects human hepatocytes against apoptosis. Biochem Biophys Res Commun 404(1):148–152. doi: 10.1016/j.bbrc.2010.11.083