Autophagy and the kidney: Implications for ischemia-reperfusion injury and therapy

American Journal of Kidney Diseases

Volumn 66, Issue 4, 2015, Pages 699-709

  Decuypere, Jean Paul ^a,b   Ceulemans, Laurens J ^a,b   Agostinis, Patrizia ^c   Monbaliu, Diethard ^a,b   Naesens, Maarten ^b,d   Pirenne, Jacques ^a,b   Jochmans, Ina ^a,b  

^a REGA INSTITUTE   (Belgium)

^b UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^c LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

^d UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

acute kidney injury (AKI); animal model; Autophagy; cell death; delayed graft function; immunosuppression; ischemia reperfusion injury (IRI); kidney transplantation; macroautophagy; renal IRI; review; stress response

Indexed keywords

DIURETIC AGENT; IMMUNOSUPPRESSIVE AGENT; MYCOPHENOLATE MOFETIL; STEROID; TACROLIMUS;

ACUTE GRAFT REJECTION; ACUTE KIDNEY FAILURE; ACUTE KIDNEY TUBULE NECROSIS; ADULT; ARTICLE; AUTOPHAGY; CASE REPORT; DELAYED GRAFT FUNCTION; DISEASE EXACERBATION; DRUG MEGADOSE; END STAGE RENAL DISEASE; HOMEOSTASIS; HUMAN; HUMAN TISSUE; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY BIOPSY; KIDNEY ISCHEMIA; KIDNEY TRANSPLANTATION; LYSOSOME; MALE; MIDDLE AGED; RENAL PROTECTION; REPERFUSION INJURY; SURVIVAL; ADVERSE EFFECTS; ANIMAL; APOPTOSIS; CELL CULTURE; DISEASE MODEL; DRUG EFFECTS; FEMALE; GRAFT REJECTION; GRAFT SURVIVAL; KNOCKOUT MOUSE; MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; RAT; RISK ASSESSMENT; SENSITIVITY AND SPECIFICITY;

ANIMALS; APOPTOSIS; AUTOPHAGY; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; GRAFT REJECTION; GRAFT SURVIVAL; HUMANS; IMMUNOSUPPRESSIVE AGENTS; KIDNEY TRANSPLANTATION; MALE; MICE; MICE, KNOCKOUT; RATS; REPERFUSION INJURY; RISK ASSESSMENT; SENSITIVITY AND SPECIFICITY;

EID: 84942294096     PISSN: 02726386     EISSN: 15236838     Source Type: Journal    
DOI: 10.1053/j.ajkd.2015.05.021     Document Type: Article

References (84)

1. R. Bellomo, J.A. Kellum, and C. Ronco Acute kidney injury Lancet 380 9843 2012 756 766
2. M. Jiang, K. Liu, J. Luo, and Z. Dong Autophagy is a renoprotective mechanism during in vitro hypoxia and in vivo ischemia-reperfusion injury Am J Pathol 176 3 2010 1181 1192
3. T. Kimura, Y. Takabatake, A. Takahashi, and et al. Autophagy protects the proximal tubule from degeneration and acute ischemic injury J Am Soc Nephrol 22 5 2011 902 913
4. S. Liu, B. Hartleben, O. Kretz, and et al. Autophagy plays a critical role in kidney tubule maintenance, aging and ischemia-reperfusion injury Autophagy 8 5 2012 826 837
5. M. Jiang, Q. Wei, G. Dong, M. Komatsu, Y. Su, and Z. Dong Autophagy in proximal tubules protects against acute kidney injury Kidney Int 82 12 2012 1271 1283
6. J. Lempiainen, P. Finckenberg, E.E. Mervaala, S. Sankari, J. Levijoki, and E.M. Mervaala Caloric restriction ameliorates kidney ischaemia/reperfusion injury through PGC-1alpha-eNOS pathway and enhanced autophagy Acta Physiol (Oxf) 208 4 2013 410 421
7. N. Pallet, M. Livingston, and Z. Dong Emerging functions of autophagy in kidney transplantation Am J Transplant 14 1 2013 13 20
8. C.T. Chien, S.K. Shyue, and M.K. Lai Bcl-xL augmentation potentially reduces ischemia/reperfusion induced proximal and distal tubular apoptosis and autophagy Transplantation 84 9 2007 1183 1190
9. Y. Isaka, C. Suzuki, T. Abe, and et al. Bcl-2 protects tubular epithelial cells from ischemia/reperfusion injury by dual mechanisms Transplant Proc 41 1 2009 52 54
10. H.H. Wu, T.Y. Hsiao, C.T. Chien, and M.K. Lai Ischemic conditioning by short periods of reperfusion attenuates renal ischemia/reperfusion induced apoptosis and autophagy in the rat J Biomed Sci 16 2009 19
11. C.H. Yeh, S.P. Hsu, C.C. Yang, C.T. Chien, and N.P. Wang Hypoxic preconditioning reinforces HIF-alpha-dependent HSP70 signaling to reduce ischemic renal failure-induced renal tubular apoptosis and autophagy Life Sci 86 3-4 2010 115 123
12. S. Nakagawa, K. Nishihara, K. Inui, and S. Masuda Involvement of autophagy in the pharmacological effects of the mTOR inhibitor everolimus in acute kidney injury Eur J Pharmacol 696 1-3 2012 143 154
13. J.A. Funk, and R.G. Schnellmann Persistent disruption of mitochondrial homeostasis after acute kidney injury Am J Physiol Renal Physiol 302 7 2012 F853 F864
14. L. Li, Z.V. Wang, J.A. Hill, and F. Lin New autophagy reporter mice reveal dynamics of proximal tubular autophagy J Am Soc Nephrol 25 2 2014 305 315
15. C. Suzuki, Y. Isaka, Y. Takabatake, and et al. Participation of autophagy in renal ischemia/reperfusion injury Biochem Biophys Res Commun 368 1 2008 100 106
16. K. Turkmen, J. Martin, A. Akcay, and et al. Apoptosis and autophagy in cold preservation ischemia Transplantation 91 11 2011 1192 1197
17. M. Ishihara, M. Urushido, K. Hamada, and et al. Sestrin-2 and BNIP3 regulate autophagy and mitophagy in renal tubular cells in acute kidney injury Am J Physiol Renal Physiol 305 4 2013 F495 F509
18. J.P. Decuypere, J. Pirenne, and I. Jochmans Autophagy in renal ischemia-reperfusion injury: friend or foe? Am J Transplant 14 6 2014 1464 1465
19. D.J. Klionsky, F.C. Abdalla, H. Abeliovich, and et al. Guidelines for the use and interpretation of assays for monitoring autophagy Autophagy 8 4 2012 445 544
20. A.S. Levey, L.A. Stevens, C.H. Schmid, and et al. A new equation to estimate glomerular filtration rate Ann Intern Med 150 9 2009 604 612
21. V. Todde, M. Veenhuis, and I.J. van der Klei Autophagy: principles and significance in health and disease Biochim Biophys Acta 1792 1 2009 3 13
22. X.H. Liang, S. Jackson, M. Seaman, and et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1 Nature 402 6762 1999 672 676
23. D.J. Klionsky Autophagy: from phenomenology to molecular understanding in less than a decade Nat Rev Mol Cell Biol 8 11 2007 931 937
24. A.M. Choi, S.W. Ryter, and B. Levine Autophagy in human health and disease N Engl J Med 368 7 2013 651 662
25. P. Jiang, and N. Mizushima Autophagy and human diseases Cell Res 24 1 2014 69 79
26. G. Marino, F. Madeo, and G. Kroemer Autophagy for tissue homeostasis and neuroprotection Curr Opin Cell Biol 23 2 2011 198 206
27. G. Kroemer, and B. Levine Autophagic cell death: the story of a misnomer Nat Rev Mol Cell Biol 9 12 2008 1004 1010
28. S. Shen, O. Kepp, and G. Kroemer The end of autophagic cell death? Autophagy 8 1 2012 1 3
29. P.G. Clarke, and J. Puyal Autophagic cell death exists Autophagy 8 6 2012 867 869
30. E. Wirawan, L. Vande Walle, K. Kersse, and et al. Caspase-mediated cleavage of Beclin-1 inactivates Beclin-1-induced autophagy and enhances apoptosis by promoting the release of proapoptotic factors from mitochondria Cell Death Dis 1 2010 e18
31. L. Yu, F. Wan, S. Dutta, and et al. Autophagic programmed cell death by selective catalase degradation Proc Natl Acad Sci U S A 103 13 2006 4952 4957
32. D.R. Green, L. Galluzzi, and G. Kroemer Cell biology. Metabolic control of cell death Science 345 6203 2014 1250256
33. +-ATPase-regulated form of cell death triggered by autophagy-inducing peptides, starvation, and hypoxia-ischemia Proc Natl Acad Sci U S A 110 51 2013 20364 20371
34. S. Pattingre, A. Tassa, X. Qu, and et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy Cell 122 6 2005 927 939
35. B. Ravikumar, S. Sarkar, J.E. Davies, and et al. Regulation of mammalian autophagy in physiology and pathophysiology Physiol Rev 90 4 2010 1383 1435
36. 2+ signaling and autophagy induction are interrelated Autophagy 7 12 2011 1472 1489
37. E.L. Axe, S.A. Walker, M. Manifava, and et al. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum J Cell Biol 182 4 2008 685 701
38. N. Mizushima, A. Yamamoto, M. Matsui, T. Yoshimori, and Y. Ohsumi In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker Mol Biol Cell 15 3 2004 1101 1111
39. B. Hartleben, M. Godel, C. Meyer-Schwesinger, and et al. Autophagy influences glomerular disease susceptibility and maintains podocyte homeostasis in aging mice J Clin Invest 120 4 2010 1084 1096
40. E. Morselli, M.C. Maiuri, M. Markaki, and et al. Caloric restriction and resveratrol promote longevity through the sirtuin-1-dependent induction of autophagy Cell Death Dis 1 2010 e10
41. Y. Takabatake, T. Kimura, A. Takahashi, and Y. Isaka Autophagy and the kidney: health and disease Nephrol Dial Transplant 29 9 2014 1639 1647
42. A. Takahashi, T. Kimura, Y. Takabatake, and et al. Autophagy guards against cisplatin-induced acute kidney injury Am J Pathol 180 2 2012 517 525
43. B. Levine, N. Mizushima, and H.W. Virgin Autophagy in immunity and inflammation Nature 469 7330 2011 323 335
44. P. Bizargity, and B. Schroppel Autophagy: basic principles and relevance to transplant immunity Am J Transplant 14 8 2014 1731 1739
45. C. Chen, L.X. Hu, T. Dong, and et al. Apoptosis and autophagy contribute to gender difference in cardiac ischemia-reperfusion induced injury in rats Life Sci 93 7 2013 265 270
46. S. Sciarretta, N. Hariharan, Y. Monden, D. Zablocki, and J. Sadoshima Is autophagy in response to ischemia and reperfusion protective or detrimental for the heart? Pediatr Cardiol 32 3 2011 275 281
47. G. Sener, H. Tugtepe, M. Yuksel, S. Cetinel, N. Gedik, and B.C. Yegen Resveratrol improves ischemia/reperfusion-induced oxidative renal injury in rats Arch Med Res 37 7 2006 822 829
48. X. Zhang, S. Chen, L. Song, and et al. mTOR-independent, autophagic enhancer trehalose prolongs motor neuron survival and ameliorates the autophagic flux defect in a mouse model of amyotrophic lateral sclerosis Autophagy 10 4 2014 588 602
49. M. Bahro, G. Gertig, and U. Pfeifer Short-term stimulation of cellular autophagy by furosemide in the thick ascending limb of Henle's loop in the rat kidney Cell Tissue Res 253 3 1988 625 629
50. K. Inoki mTOR signaling in autophagy regulation in the kidney Semin Nephrol 34 1 2014 2 8
51. T. Nakagaki, K. Satoh, D. Ishibashi, and et al. FK506 reduces abnormal prion protein through the activation of autolysosomal degradation and prolongs survival in prion-infected mice Autophagy 9 9 2013 1386 1394
52. U. Bandyopadhyay, S. Sridhar, S. Kaushik, R. Kiffin, and A.M. Cuervo Identification of regulators of chaperone-mediated autophagy Mol Cell 39 4 2010 535 547
53. S. Swerdlow, K. McColl, Y. Rong, M. Lam, A. Gupta, and C.W. Distelhorst Apoptosis inhibition by Bcl-2 gives way to autophagy in glucocorticoid-treated lymphocytes Autophagy 4 5 2008 612 620
54. E. Laane, K.P. Tamm, E. Buentke, and et al. Cell death induced by dexamethasone in lymphoid leukemia is mediated through initiation of autophagy Cell Death Differ 16 7 2009 1018 1029
55. D. Yamamoto, T. Maki, E.H. Herningtyas, and et al. Branched-chain amino acids protect against dexamethasone-induced soleus muscle atrophy in rats Muscle Nerve 41 6 2010 819 827
56. X. Xia, R. Kar, J. Gluhak-Heinrich, and et al. Glucocorticoid-induced autophagy in osteocytes J Bone Miner Res 25 11 2010 2479 2488
57. N. Liu, W. Wang, Z. Zhao, T. Zhang, and Y. Song Autophagy in human articular chondrocytes is cytoprotective following glucocorticoid stimulation Mol Med Rep 9 6 2014 2166 2172
58. J. Jia, W. Yao, M. Guan, and et al. Glucocorticoid dose determines osteocyte cell fate FASEB J 25 10 2011 3366 3376
59. H.C. Chen, T.H. Fong, A.W. Lee, and W.T. Chiu Autophagy is activated in injured neurons and inhibited by methylprednisolone after experimental spinal cord injury Spine (Phila Pa 1976) 37 6 2012 470 475
60. B. Hernandez-Breijo, J. Monserrat, I.D. Roman, and et al. Azathioprine desensitizes liver cancer cells to insulin-like growth factor 1 and causes apoptosis when it is combined with bafilomycin A1 Toxicol Appl Pharmacol 272 3 2013 568 578
61. D. Bani, F. Filipponi, L. Magnani, D. Houssin, and P. Romagnoli Morphological changes in rat pancreatic acinar cells induced by long-term treatment with cyclosporine and their reversal after withdrawal Transplantation 50 5 1990 830 834
62. Y.M. Yoo, and E.B. Jeung Melatonin suppresses cyclosporine A-induced autophagy in rat pituitary GH3 cells J Pineal Res 48 3 2010 204 211
63. S.W. Lim, B.J. Hyoung, S.G. Piao, K.C. Doh, B.H. Chung, and C.W. Yang Chronic cyclosporine nephropathy is characterized by excessive autophagosome formation and decreased autophagic clearance Transplantation 94 3 2012 218 225
64. I.A. Ciechomska, K. Gabrusiewicz, A.A. Szczepankiewicz, and B. Kaminska Endoplasmic reticulum stress triggers autophagy in malignant glioma cells undergoing cyclosporine A-induced cell death Oncogene 32 12 2013 1518 1529
65. H.S. Kim, S.I. Choi, E.B. Jeung, and Y.M. Yoo Cyclosporine A induces apoptotic and autophagic cell death in rat pituitary GH3 cells PLoS One 9 10 2014 e108981
66. N. Aravindan, and A. Shaw Effect of furosemide infusion on renal hemodynamics and angiogenesis gene expression in acute renal ischemia/reperfusion Ren Fail 28 1 2006 25 35
67. N. Aravindan, S. Aravindan, B.J. Riedel, H.R. Weng, and A.D. Shaw Furosemide prevents apoptosis and associated gene expression in a rat model of surgical ischemic acute renal failure Ren Fail 29 4 2007 399 407
68. C. Fleck, and J. Heller Age-dependent differences in the effect of ischaemia on the rat kidney: prevention of the postischaemic damage by different drugs Exp Toxicol Pathol 45 5-6 1993 381 387
69. A.A. Ejaz, and R. Mohandas Are diuretics harmful in the management of acute kidney injury? Curr Opin Nephrol Hypertens 23 2 2014 155 160
70. C. Esposito, F. Grosjean, M. Torreggiani, and et al. Sirolimus prevents short-term renal changes induced by ischemia-reperfusion injury in rats Am J Nephrol 33 3 2011 239 249
71. F. Cicora, N. Lausada, D.N. Vasquez, and et al. Protective effect of immunosuppressive treatment before orthotopic kidney autotransplantation Transpl Immunol 24 2 2011 107 112
72. B. Yang, S. Jain, I.Z. Pawluczyk, and et al. Inflammation and caspase activation in long-term renal ischemia/reperfusion injury and immunosuppression in rats Kidney Int 68 5 2005 2050 2067
73. T.F. Fuller, C.E. Freise, N. Serkova, C.U. Niemann, J.L. Olson, and S. Feng Sirolimus delays recovery of rat kidney transplants after ischemia-reperfusion injury Transplantation 76 11 2003 1594 1599
74. W. Lieberthal, R. Fuhro, C.C. Andry, and et al. Rapamycin impairs recovery from acute renal failure: role of cell-cycle arrest and apoptosis of tubular cells Am J Physiol Renal Physiol 281 4 2001 F693 F706
75. S.L. Lui, K.W. Chan, R. Tsang, S. Yung, K.N. Lai, and T.M. Chan Effect of rapamycin on renal ischemia-reperfusion injury in mice Transpl Int 19 10 2006 834 839
76. D. Ninova, M. Covarrubias, D.J. Rea, W.D. Park, J.P. Grande, and M.D. Stegall Acute nephrotoxicity of tacrolimus and sirolimus in renal isografts: differential intragraft expression of transforming growth factor-beta1 and alpha-smooth muscle actin Transplantation 78 3 2004 338 344
77. E. Suyani, U.B. Derici, T. Sahin, and et al. Effects of everolimus on cytokines, oxidative stress, and renal histology in ischemia-reperfusion injury of the kidney Ren Fail 31 8 2009 698 703
78. M. Liu, P. Agreda, M. Crow, L. Racusen, and H. Rabb Effects of delayed rapamycin treatment on renal fibrosis and inflammation in experimental ischemia reperfusion injury Transplant Proc 41 10 2009 4065 4071
79. F. Cicora, J. Roberti, D. Vasquez, and et al. Preconditioning donor with a combination of tacrolimus and rapamacyn to decrease ischaemia-reperfusion injury in a rat syngenic kidney transplantation model Clin Exp Immunol 167 1 2012 169 177
80. E.M. Jolicoeur, S. Qi, D. Xu, L. Dumont, P. Daloze, and H. Chen Combination therapy of mycophenolate mofetil and rapamycin in prevention of chronic renal allograft rejection in the rat Transplantation 75 1 2003 54 59
81. B. Yang, S. Jain, S.Y. Ashra, P.N. Furness, and M.L. Nicholson Apoptosis and caspase-3 in long-term renal ischemia/reperfusion injury in rats and divergent effects of immunosuppressants Transplantation 81 10 2006 1442 1450
82. M. Sabbatini, F. Uccello, V. Serio, and et al. Effects of mycophenolate mofetil on acute ischaemia-reperfusion injury in rats and its consequences in the long term Nephrol Dial Transplant 25 5 2010 1443 1450
83. Y.X. Zhang, J.R. Zhang, and Z.G. Wang Mycophenolate mofetil affects monocyte Toll-like receptor 4 signaling during mouse renal ischemia/reperfusion injury Chin Med J (Engl) 126 7 2013 1224 1229
84. L. Yan, D.E. Vatner, S.J. Kim, and et al. Autophagy in chronically ischemic myocardium Proc Natl Acad Sci U S A 102 39 2005 13807 13812