Autophagy in renal diseases

Pediatric Nephrology

Volumn 31, Issue 5, 2016, Pages 737-752

  De Rechter, Stéphanie ^a,b   Decuypere, Jean Paul ^a,c   Ivanova, Ekaterina ^b   van den Heuvel, Lambertus P ^b,d   De Smedt, Humbert ^b   Levtchenko, Elena ^a,b   Mekahli, Djalila ^a,b  

^a UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c REGA INSTITUTE   (Belgium)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Apoptosis; Autophagy; Cystinosis; Diabetic nephropathy; Fibrosis; Glomerulosclerosis; Ischemia reperfusion injury; Polycystic kidney disease

Indexed keywords

3 METHYLADENINE; BAFILOMYCIN; CHLOROQUINE; RAPAMYCIN; URINARY TRACT AGENT;

ACTIN FILAMENT; ACUTE KIDNEY FAILURE; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL DEATH; CELL DIFFERENTIATION; CELL ENERGY; CELL GROWTH; CHAPERONE-MEDIATED AUTOPHAGY; CHRONIC KIDNEY DISEASE; CYSTINOSIS; DIABETIC NEPHROPATHY; ENDOPLASMIC RETICULUM STRESS; EUKARYOTIC FLAGELLUM; GLOMERULOSCLEROSIS; GLUCOSE METABOLISM; KIDNEY DISEASE; KIDNEY FIBROSIS; KIDNEY FUNCTION; KIDNEY ISCHEMIA; KIDNEY POLYCYSTIC DISEASE; KIDNEY TRANSPLANTATION; LIPOGENESIS; MACROAUTOPHAGY; MICROAUTOPHAGY; OXIDATIVE STRESS; PODOCYTE; PRIORITY JOURNAL; PROTEIN CONFORMATION; RENAL PROTECTION; SIGNAL TRANSDUCTION; THERAPEUTIC INDEX; TURNOVER TIME; ANIMAL; DRUG EFFECTS; EPITHELIUM CELL; HUMAN; KIDNEY; KIDNEY DISEASES; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; AUTOPHAGY; EPITHELIAL CELLS; HUMANS; KIDNEY; KIDNEY DISEASES; MOLECULAR TARGETED THERAPY; SIGNAL TRANSDUCTION; UROLOGICAL AGENTS;

EID: 84936804753     PISSN: 0931041X     EISSN: 1432198X     Source Type: Journal    
DOI: 10.1007/s00467-015-3134-2     Document Type: Article

References (86)

1. Dong Z (2014) Introduction: autophagy in kidneys. Semin Nephrol 34:1
2. Choi AM, Ryter SW, Levine B (2013) Autophagy in human health and disease. N Engl J Med 368:651–662
3. Fougeray S, Pallet N (2015) Mechanisms and biological functions of autophagy in diseased and ageing kidneys. Nat Rev Nephrol 11:34–45
4. Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW, Jimenez-Sanchez M, Korolchuk VI, Lichtenberg M, Luo S, Massey DC, Menzies FM, Moreau K, Narayanan U, Renna M, Siddiqi FH, Underwood BR, Winslow AR, Rubinsztein DC (2010) Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev 90:1383–1435
5. Inoki K (2014) mTOR signaling in autophagy regulation in the kidney. Semin Nephrol 34:2–8
6. Huber TB, Edelstein CL, Hartleben B, Inoki K, Jiang M, Koya D, Kume S, Lieberthal W, Pallet N, Quiroga A, Ravichandran K, Susztak K, Yoshida S, Dong Z (2012) Emerging role of autophagy in kidney function, diseases and aging. Autophagy 8:1009–1031
7. Simonsen A, Stenmark H (2008) Self-eating from an ER-associated cup. J Cell Biol 182:621–622
8. Polson HE, de Lartigue J, Rigden DJ, Reedijk M, Urbe S, Clague MJ, Tooze SA (2010) Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy 6:506–522
9. Kang R, Zeh HJ, Lotze MT, Tang D (2011) The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 18:571–580
10. Decuypere JP, Parys JB, Bultynck G (2012) Regulation of the autophagic bcl-2/beclin 1 interaction. Cells 1:284–312
11. Klionsky DJ, Baehrecke EH, Brumell JH, Chu CT, Codogno P, Cuervo AM, Debnath J, Deretic V, Elazar Z, Eskelinen EL, Finkbeiner S, Fueyo-Margareto J, Gewirtz D, Jaattela M, Kroemer G, Levine B, Melia TJ, Mizushima N, Rubinsztein DC, Simonsen A, Thorburn A, Thumm M, Tooze SA (2011) A comprehensive glossary of autophagy-related molecules and processes (2nd edition). Autophagy 7:1273–1294
12. Mizushima N (2010) The role of the Atg1/ULK1 complex in autophagy regulation. Curr Opin Cell Biol 22:132–139
13. Ganley IG, du Lam H, Wang J, Ding X, Chen S, Jiang X (2009) ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy. J Biol Chem 284:12297–12305
14. Decleves AE, Sharma K, Satriano J (2014) Beneficial effects of amp-activated protein kinase agonists in kidney ischemia-reperfusion: autophagy and cellular stress markers. Nephron Exp Nephrol 128:98–110
15. Settembre C, Di Malta C, Polito VA, Garcia Arencibia M, Vetrini F, Erdin S, Erdin SU, Huynh T, Medina D, Colella P, Sardiello M, Rubinsztein DC, Ballabio A (2011) TFEB links autophagy to lysosomal biogenesis. Science 332:1429–1433
16. Kaushik S, Cuervo AM (2012) Chaperone-mediated autophagy: a unique way to enter the lysosome world. Trends Cell Biol 22:407–417
17. Franch HA (2014) Chaperone-mediated autophagy in the kidney: the road more traveled. Semin Nephrol 34:72–83
18. Martinez-Vicente M, Talloczy Z, Kaushik S, Massey AC, Mazzulli J, Mosharov EV, Hodara R, Fredenburg R, Wu DC, Follenzi A, Dauer W, Przedborski S, Ischiropoulos H, Lansbury PT, Sulzer D, Cuervo AM (2008) Dopamine-modified alpha-synuclein blocks chaperone-mediated autophagy. J Clin Invest 118:777–788
19. Wang Y, Martinez-Vicente M, Kruger U, Kaushik S, Wong E, Mandelkow EM, Cuervo AM, Mandelkow E (2009) Tau fragmentation, aggregation and clearance: the dual role of lysosomal processing. Hum Mol Genet 18:4153–4170
20. Kon M, Kiffin R, Koga H, Chapochnick J, Macian F, Varticovski L, Cuervo AM (2011) Chaperone-mediated autophagy is required for tumor growth. Sci Transl Med 3:109–117
21. Li WW, Li J, Bao JK (2012) Microautophagy: lesser-known self-eating. Cell Mol Life Sci 69:1125–1136
22. Liu Y, Levine B (2015) Autosis and autophagic cell death: the dark side of autophagy. Cell Death Differ 22:367–376
23. Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35:495–516
24. Chan FK, Luz NF, Moriwaki K (2015) Programmed necrosis in the cross talk of cell death and inflammation. Annu Rev Immunol 33:79–106
25. Li M, Tan J, Miao Y, Lei P, Zhang Q (2015) The dual role of autophagy under hypoxia-involvement of interaction between autophagy and apoptosis. Apoptosis 20:769–777
26. Tait SW, Ichim G, Green DR (2014) Die another way–non-apoptotic mechanisms of cell death. J Cell Sci 127:2135–2144
27. Grahammer F, Wanner N, Huber TB (2014) mTOR controls kidney epithelia in health and disease. Nephrol Dial Transplant 29(Suppl 1):i9–i18
28. Shaw RJ (2013) Cell biology. GATORs take a bite out of mTOR. Science 340:1056–1057
29. Mekahli D, Decuypere JP, Sammels E, Welkenhuyzen K, Schoeber J, Audrezet MP, Corvelyn A, Dechenes G, Ong AC, Wilmer MJ, van den Heuvel L, Bultynck G, Parys JB, Missiaen L, Levtchenko E, De Smedt H (2014) Polycystin-1 but not polycystin-2 deficiency causes upregulation of the mTOR pathway and can be synergistically targeted with rapamycin and metformin. Pflugers Arch 466:1591–1604
30. Betz C, Hall MN (2013) Where is mTOR and what is it doing there? J Cell Biol 203:563–574
31. Jewell JL, Guan KL (2013) Nutrient signaling to mTOR and cell growth. Trends Biochem Sci 38:233–242
32. Wang S, Tsun ZY, Wolfson RL, Shen K, Wyant GA, Plovanich ME, Yuan ED, Jones TD, Chantranupong L, Comb W, Wang T, Bar-Peled L, Zoncu R, Straub C, Kim C, Park J, Sabatini BL, Sabatini DM (2015) Metabolism. Lysosomal amino acid transporter SLC38A9 signals arginine sufficiency to mTORC1. Science 347:188–194
33. Ogmundsdottir MH, Heublein S, Kazi S, Reynolds B, Visvalingam SM, Shaw MK, Goberdhan DC (2012) Proton-assisted amino acid transporter PAT1 complexes with Rag GTPases and activates TORC1 on late endosomal and lysosomal membranes. PLoS One 7, e36616
34. Rebsamen M, Pochini L, Stasyk T, de Araujo ME, Galluccio M, Kandasamy RK, Snijder B, Fauster A, Rudashevskaya EL, Bruckner M, Scorzoni S, Filipek PA, Huber KV, Bigenzahn JW, Heinz LX, Kraft C, Bennett KL, Indiveri C, Huber LA, Superti-Furga G (2015) SLC38A9 is a component of the lysosomal amino acid sensing machinery that controls mTORC1. Nature 519:477–481
35. Hartleben B, Wanner N, Huber TB (2014) Autophagy in glomerular health and disease. Semin Nephrol 34:42–52
36. Oliva Trejo JA, Asanuma K, Kim EH, Takagi-Akiba M, Nonaka K, Hidaka T, Komatsu M, Tada N, Ueno T, Tomino Y (2014) Transient increase in proteinuria, poly-ubiquitylated proteins and ER stress markers in podocyte-specific autophagy-deficient mice following unilateral nephrectomy. Biochem Biophys Res Commun 446:1190–1196
37. Liebau MC, Braun F, Hopker K, Weitbrecht C, Bartels V, Muller RU, Brodesser S, Saleem MA, Benzing T, Schermer B, Cybulla M, Kurschat CE (2013) Dysregulated autophagy contributes to podocyte damage in Fabry’s disease. PLoS One 8, e63506
38. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 15:1101–1111
39. Livingston MJ, Dong Z (2014) Autophagy in acute kidney injury. Semin Nephrol 34:17–26
40. Orhon I, Dupont N, Pampliega O, Cuervo AM, Codogno P (2015) Autophagy and regulation of cilia function and assembly. Cell Death Differ 22:389–397
41. Ravichandran K, Edelstein CL (2014) Polycystic kidney disease: a case of suppressed autophagy? Semin Nephrol 34:27–33
42. Pampliega O, Orhon I, Patel B, Sridhar S, Diaz-Carretero A, Beau I, Codogno P, Satir BH, Satir P, Cuervo AM (2013) Functional interaction between autophagy and ciliogenesis. Nature 502:194–200
43. Tang Z, Lin MG, Stowe TR, Chen S, Zhu M, Stearns T, Franco B, Zhong Q (2013) Autophagy promotes primary ciliogenesis by removing OFD1 from centriolar satellites. Nature 502:254–257
44. Mekahli D, Parys JB, Bultynck G, Missiaen L, De Smedt H (2013) Polycystins and cellular Ca2+ signaling. Cell Mol Life Sci 70:2697–2712
45. Decuypere JP, Kindt D, Luyten T, Welkenhuyzen K, Missiaen L, De Smedt H, Bultynck G, Parys JB (2013) mTOR-Controlled autophagy requires intracellular Ca(2+) signaling. PLoS One 8, e61020
46. Decuypere JP, Bultynck G, Parys JB (2011) A dual role for Ca(2+) in autophagy regulation. Cell Calcium 50:242–250
47. Delling M, DeCaen PG, Doerner JF, Febvay S, Clapham DE (2013) Primary cilia are specialized calcium signalling organelles. Nature 504:311–314
48. DeCaen PG, Delling M, Vien TN, Clapham DE (2013) Direct recording and molecular identification of the calcium channel of primary cilia. Nature 504:315–318
49. Zeng C, Fan Y, Wu J, Shi S, Chen Z, Zhong Y, Zhang C, Zen K, Liu Z (2014) Podocyte autophagic activity plays a protective role in renal injury and delays the progression of podocytopathies. J Pathol 234:203–213
50. Kawakami T, Gomez IG, Ren S, Hudkins K, Roach A, Alpers CE, Shankland SJ, D’Agati VD, Duffield JS (2014) Deficient autophagy results in mitochondrial dysfunction and FSGS. J Am Soc Nephrol 26:1040–1052
51. Ding Y, Choi ME (2014) Regulation of autophagy by TGF-beta: emerging role in kidney fibrosis. Semin Nephrol 34:62–71
52. Kim H, Moon SY, Kim JS, Baek CH, Kim M, Min JY, Lee SK (2015) Activation of AMP-activated protein kinase inhibits ER stress and renal fibrosis. Am J Physiol Ren Physiol 308:226–236
53. Kume S, Yamahara K, Yasuda M, Maegawa H, Koya D (2014) Autophagy: emerging therapeutic target for diabetic nephropathy. Semin Nephrol 34:9–16
54. Pallet N (2014) Emerging roles of autophagy in the stressed kidney allograft. Semin Nephrol 34:34–41
55. 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 8:826–837
56. 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 22:902–913
57. Jiang M, Wei Q, Dong G, Komatsu M, Su Y, Dong Z (2012) Autophagy in proximal tubules protects against acute kidney injury. Kidney Int 82:1271–1283
58. 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 176:1181–1192
59. 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 86:115–123
60. 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
61. Suzuki C, Isaka Y, Takabatake Y, Tanaka H, Koike M, Shibata M, Uchiyama Y, Takahara S, Imai E (2008) Participation of autophagy in renal ischemia/reperfusion injury. Biochem Biophys Res Commun 368:100–106
62. 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 696:143–154
63. 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 41:52–54
64. Chien CT, Shyue SK, Lai MK (2007) Bcl-xL augmentation potentially reduces ischemia/reperfusion induced proximal and distal tubular apoptosis and autophagy. Transplantation 84:1183–1190
65. Kher A, Meldrum KK, Wang M, Tsai BM, Pitcher JM, Meldrum DR (2005) Cellular and molecular mechanisms of sex differences in renal ischemia-reperfusion injury. Cardiovasc Res 67:594–603
66. Kang KP, Lee JE, Lee AS, Jung YJ, Kim D, Lee S, Hwang HP, Kim W, Park SK (2014) Effect of gender differences on the regulation of renal ischemia-reperfusion-induced inflammation in mice. Mol Med Rep 9:2061–2068
67. Schiebler TH, Danner KG (1978) The effect of sex hormones on the proximal tubules in the rat kidney. Cell Tissue Res 192:527–549
68. Rubinsztein DC, Marino G, Kroemer G (2011) Autophagy and aging. Cell 146:682–695
69. Reutzel-Selke A, Jurisch A, Denecke C, Pascher A, Martins PN, Kessler H, Tamura A, Utku N, Pratschke J, Neuhaus P, Tullius SG (2007) Donor age intensifies the early immune response after transplantation. Kidney Int 71:629–636
70. Decuypere JP, Pirenne J, Jochmans I (2014) Autophagy in renal ischemia-reperfusion injury: friend or foe? Am J Transplant 14:1464–1465
71. Bizargity P, Schroppel B (2014) Autophagy: basic principles and relevance to transplant immunity. Am J Transplant 14:1731–1739
72. Leuenroth SJ, Bencivenga N, Chahboune H, Hyder F, Crews CM (2010) Triptolide reduces cyst formation in a neonatal to adult transition Pkd1 model of ADPKD. Nephrol Dial Transplant 25:2187–2194
73. Belibi F, Zafar I, Ravichandran K, Segvic AB, Jani A, Ljubanovic DG, Edelstein CL (2011) Hypoxia-inducible factor-1alpha (HIF-1alpha) and autophagy in polycystic kidney disease (PKD). Am J Physiol Ren Physiol 300:F1235–F1243
74. Rowe I, Chiaravalli M, Mannella V, Ulisse V, Quilici G, Pema M, Song XW, Xu H, Mari S, Qian F, Pei Y, Musco G, Boletta A (2013) Defective glucose metabolism in polycystic kidney disease identifies a new therapeutic strategy. Nat Med 19:488–493
75. Cebotaru V, Cebotaru L, Kim H, Chiaravalli M, Boletta A, Qian F, Guggino WB (2014) Polycystin-1 negatively regulates polycystin-2 expression via the aggresome/autophagosome pathway. J Biol Chem 289:6404–6414
76. Gahl WA, Thoene JG, Schneider JA (2002) Cystinosis. N Engl J Med 347:111–121
77. Levtchenko E, Monnens L (2006) Development of Fanconi syndrome during infancy in a patient with cystinosis. Acta Paediatr 95:379–380
78. Wilmer MJ, Christensen EI, van den Heuvel LP, Monnens LA, Levtchenko EN (2008) Urinary protein excretion pattern and renal expression of megalin and cubilin in nephropathic cystinosis. Am J Kidney Dis 51:893–903
79. Ivanova E, De Leo MG, De Matteis MA, Levtchenko E (2014) Cystinosis: clinical presentation, pathogenesis and treatment. Pediatr Endocrinol Rev 12(Suppl 1):176–184
80. Kogan K, Spear ED, Kaiser CA, Fass D (2010) Structural conservation of components in the amino acid sensing branch of the TOR pathway in yeast and mammals. J Mol Biol 402:388–398
81. Dubouloz F, Deloche O, Wanke V, Cameroni E, De Virgilio C (2005) The TOR and EGO protein complexes orchestrate microautophagy in yeast. Mol Cell 19:15–26
82. Sansanwal P, Yen B, Gahl WA, Ma Y, Ying L, Wong LJ, Sarwal MM (2010) Mitochondrial autophagy promotes cellular injury in nephropathic cystinosis. J Am Soc Nephrol 21:272–283
83. Sansanwal P, Sarwal MM (2010) Abnormal mitochondrial autophagy in nephropathic cystinosis. Autophagy 6:971–973
84. Sansanwal P, Sarwal MM (2012) p62/SQSTM1 prominently accumulates in renal proximal tubules in nephropathic cystinosis. Pediatr Nephrol 27:2137–2144
85. Sansanwal P, Li L, Sarwal MM (2015) Inhibition of intracellular clusterin attenuates cell death in nephropathic cystinosis. J Am Soc Nephrol 26:612–625
86. Napolitano G, Johnson JL, He J, Rocca CJ, Monfregola J, Pestonjamasp K, Cherqui S, Catz SD (2015) Impairment of chaperone-mediated autophagy leads to selective lysosomal degradation defects in the lysosomal storage disease cystinosis. EMBO Mol Med 7:158–174