Targeting mTOR signaling can prevent the progression of FSGS

Journal of the American Society of Nephrology

Volumn 28, Issue 7, 2017, Pages 2144-2157

  Zschiedrich, Stefan ^a   Bork, Tillmann ^a   Liang, Wei ^a,b   Wanner, Nicola ^a   Eulenbruch, Kristina ^a   Munder, Stefan ^a   Hartleben, Björn ^a   Kretz, Oliver ^a,c   Gerber, Simon ^d   Simons, Matias ^d   Viau, Amandine ^a   Burtin, Martine ^e   Wei, Changli ^f   Reiser, Jochen ^f   Herbach, Nadja ^g   Rastaldi, Maria Pia ^h   Cohen, Clemens D ⁱ   Tharaux, Pierre Louis ^j   Terzi, Fabiola ^e   Walz, Gerd ^a   Gödel, Markus ^a   Huber, Tobias B ^a,c,k   more..

^a UNIVERSITY OF FREIBURG   (Germany)

^b RENMIN HOSPITAL OF WUHAN UNIVERSITY   (China)

^c UNIVERSITY OF FREIBURG   (Germany)

^d IMAGINE INSTITUTE   (France)

^e INSTITUT NECKER ENFANTS MALADES   (France)

^f RUSH UNIVERSITY MEDICAL CENTER   (United States)

^g UNIVERSITY OF MUNICH   (Germany)

^h NATIONAL CANCER INSTITUTE   (Italy)

ⁱ Institute of Clinical Chemistry and Immunology   (Germany)

^j INSERM   (France)

^k UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; PROTEIN S6; REACTIVE OXYGEN METABOLITE; IMMUNOSUPPRESSIVE AGENT; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; RAPAMYCIN; TARGET OF RAPAMYCIN KINASE;

ALLELE; ANAEROBIC GLYCOLYSIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DEDIFFERENTIATION; CELL ENERGY; CELL STRESS; CONTROLLED STUDY; DISEASE COURSE; ENERGY METABOLISM; FOCAL GLOMERULOSCLEROSIS; GLOMERULOPATHY; GLOMERULOSCLEROSIS; GLOMERULUS; HUMAN; HUMAN CELL; HUMAN TISSUE; MICRODISSECTION; MITOCHONDRIAL BIOGENESIS; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; OXIDATIVE PHOSPHORYLATION; PODOCYTE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TITRIMETRY; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; PHYSIOLOGY;

ANIMALS; DISEASE PROGRESSION; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; HUMANS; IMMUNOSUPPRESSIVE AGENTS; MICE; MULTIPROTEIN COMPLEXES; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES;

EID: 85017435939     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2016050519     Document Type: Article

References (55)

1. United States Renal Data System: 2016 USRDS Annual Data Report: Epidemiology of Kidney Disease in the United States, Bethesda, MD, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, 2016
2. D'Agati VD, Kaskel FJ, Falk RJ: Focal segmental glomerulosclerosis. N Engl J Med 365: 2398-2411, 2011
3. Dantal J, Bigot E, Bogers W, Testa A, Kriaa F, Jacques Y, Hurault de Ligny B, Niaudet P, Charpentier B, Soulillou JP: Effect of plasma protein adsorption on protein excretion in kidney-transplant recipients with recurrent nephrotic syndrome. N Engl J Med 330: 7-14, 1994
4. Ponticelli C, Moroni G, Glassock RJ: De novo glomerular diseases after renal transplantation. Clin J Am Soc Nephrol 9: 1479-1487, 2014
5. Schachter ME, Monahan M, Radhakrishnan J, Crew J, Pollak M, Ratner L, Valeri AM, Stokes MB, Appel GB: Recurrent focal segmental glomerulosclerosis in the renal allograft: Single center experience in the era of modern immunosuppression. Clin Nephrol 74: 173-181, 2010
6. Grahammer F, Schell C, Huber TB: The podocyte slit diaphragm-froma thin grey line to a complex signalling hub. Nat Rev Nephrol 9: 587-598, 2013
7. Wiggins JE, GoyalM, Sanden SK, WharramBL, Shedden KA,Misek DE, Kuick RD, Wiggins RC: Podocyte hypertrophy, "adaptation," and "decompensation" associated with glomerular enlargement and glomerulosclerosis in the aging rat: Prevention by calorie restriction. J Am Soc Nephrol 16: 2953-2966, 2005
8. Deegens JK, Steenbergen EJ, Wetzels JF: Review on diagnosis and treatment of focal segmental glomerulosclerosis. Neth JMed 66: 3-12, 2008
9. Jafar TH, Schmid CH, LandaM,Giatras I, Toto R, RemuzziG,MaschioG, Brenner BM, Kamper A, Zucchelli P, Becker G, Himmelmann A, Bannister K, Landais P, Shahinfar S, de Jong PE, de Zeeuw D, Lau J, Levey AS: Angiotensin-converting enzyme inhibitors and progression of nondiabetic renal disease. Ameta-analysis of patient-level data. Ann Intern Med 135: 73-87, 2001
10. Fukuda A, Chowdhury MA, Venkatareddy MP, Wang SQ, Nishizono R, Suzuki T, Wickman LT, Wiggins JE, Muchayi T, Fingar D, Shedden KA, Inoki K, Wiggins RC: Growth-dependent podocyte failure causes glomerulosclerosis. J Am Soc Nephrol 23: 1351-1363, 2012
11. Inoki K, Huber TB: Mammalian target of rapamycin signaling in the podocyte. Curr Opin Nephrol Hypertens 21: 251-257, 2012
12. Inoki K, Mori H, Wang J, Suzuki T, Hong S, Yoshida S, Blattner SM, Ikenoue T, R?egg MA, Hall MN, Kwiatkowski DJ, Rastaldi MP, Huber TB, KretzlerM, Holzman LB,Wiggins RC, Guan KL: mTORC1 activation in podocytes is a critical step in the development of diabetic nephropathy in mice. J Clin Invest 121: 2181-2196, 2011
13. G?del M, Hartleben B, Herbach N, Liu S, Zschiedrich S, Lu S, Debreczeni-M?r A, LindenmeyerMT, RastaldiMP, Hartleben G, Wiech T, Fornoni A,Nelson RG, KretzlerM, Wanke R, Pavenst?dt H, Kerjaschki D, Cohen CD, Hall MN, R?egg MA, Inoki K, Walz G, Huber TB: Role of mTOR in podocyte function and diabetic nephropathy in humans and mice. J Clin Invest 121: 2197-2209, 2011
14. Mao J, Zeng Z, Xu Z, Li J, Jiang L, Fang Y, Xu X, Hu Z, HeW, Yang J, Dai C: Mammalian target of rapamycin complex 1 activation in podocytes promotes cellular crescent formation. Am J Physiol Renal Physiol 307: F1023-F1032, 2014
15. Laplante M, Sabatini DM: mTOR signaling in growth control and disease. Cell 149: 274-293, 2012
16. 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
17. Holz MK, Ballif BA, Gygi SP, Blenis J: mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 123: 569-580, 2005
18. Ma XM, Blenis J: Molecular mechanisms of mTOR-mediated translational control. Nat RevMol Cell Biol 10: 307-318, 2009
19. Tumlin JA, Miller D, Near M, Selvaraj S, Hennigar R, Guasch A: A prospective, open-label trial of sirolimus in the treatment of focal segmental glomerulosclerosis. Clin J Am Soc Nephrol 1: 109-116, 2006
20. Tsagalis G, Psimenou E, Iliadis A, Nakopoulou L, Laggouranis A: Rapamycin for focal segmental glomerulosclerosis: A report of 3 cases. Am J Kidney Dis 54: 340-344, 2009
21. Cho ME, Hurley JK, Kopp JB: Sirolimus therapy of focal segmental glomerulosclerosis is associated with nephrotoxicity. AmJ Kidney Dis 49: 310-317, 2007
22. Letavernier E, Pe'raldi MN, Pariente A, Morelon E, Legendre C: Proteinuria following a switch from calcineurin inhibitors to sirolimus. Transplantation 80: 1198-1203, 2005
23. Letavernier E, Bruneval P, Mandet C, Duong Van Huyen JP, P?raldi MN, Helal I, No?l LH, Legendre C: High sirolimus levels may induce focal segmental glomerulosclerosis de novo. Clin J AmSoc Nephrol 2: 326-333, 2007
24. Liern M, De Reyes V, Fayad A, Vallejo G: Use of sirolimus in patients with primary steroid-resistant nephrotic syndrome. Nefrologia 32: 321-328, 2012
25. Fervenza FC, Fitzpatrick PM,Mertz J, Erickson SB, Liggett S, PophamS, Wochos DN, Synhavsky A, Hippler S, Larson TS, Bagniewski SM, Velosa JA; Mayo Nephrology Collaborative Committee: Acute rapamycin nephrotoxicity in native kidneys of patients with chronic glomerulopathies. Nephrol Dial Transplant 19: 1288-1292, 2004
26. Wiggins RC: The spectrum of podocytopathies: A unifying view of glomerular diseases. Kidney Int 71: 1205-1214, 2007
27. Wharram BL, Goyal M, Wiggins JE, Sanden SK, Hussain S, Filipiak WE, Saunders TL, Dysko RC, Kohno K, Holzman LB, Wiggins RC: Podocyte depletion causes glomerulosclerosis: Diphtheria toxin-induced podocyte depletion in rats expressing human diphtheria toxin receptor transgene. J Am Soc Nephrol 16: 2941-2952, 2005
28. Sato Y, Wharram BL, Lee SK, Wickman L, Goyal M, Venkatareddy M, Chang JW, Wiggins JE, Lienczewski C, Kretzler M, Wiggins RC: Urine podocyte mRNAsmark progression of renal disease. J AmSocNephrol 20: 1041-1052, 2009
29. Grahammer F,Wanner N, Huber TB: mTOR controls kidney epithelia in health and disease. Nephrol Dial Transplant 29[Suppl 1]: i9-i18, 2014
30. Eid AA, Ford BM, Bhandary B, de Cassia Cavaglieri R, Block K, Barnes JL, Gorin Y, Choudhury GG, Abboud HE: Mammalian target of rapamycin regulates Nox4-mediated podocyte depletion in diabetic renal injury. Diabetes 62: 2935-2947, 2013
31. Hartleben B, G?del M, Meyer-Schwesinger C, Liu S, Ulrich T, K?bler S, Wiech T, Grahammer F, Arnold SJ, Lindenmeyer MT, Cohen CD, Pavenst?dt H, Kerjaschki D, Mizushima N, Shaw AS, Walz G, Huber TB: Autophagy influences glomerular disease susceptibility and maintains podocyte homeostasis in aging mice. J Clin Invest 120: 1084-1096, 2010
32. Vogelbacher R, Wittmann S, Braun A, Daniel C, Hugo C: The mTOR inhibitor everolimus induces proteinuria and renal deterioration in the remnant kidney model in the rat. Transplantation 84: 1492-1499, 2007
33. Amer H, Cosio FG: Significance and management of proteinuria in kidney transplant recipients. J Am Soc Nephrol 20: 2490-2492, 2009
34. Torras J, Herrero-Fresneda I,GuliasO, Flaquer M, Vidal A, Cruzado JM, Lloberas N, Franquesa M, Griny? JM: Rapamycin has dual opposing effects on proteinuric experimental nephropathies: Is it a matter of podocyte damage? Nephrol Dial Transplant 24: 3632-3640, 2009
35. Munivenkatappa R, Haririan A, Papadimitriou JC, Drachenberg CB, Dinits-Pensy M, Klassen DK: Tubular epithelial cell and podocyte apoptosis with de novo sirolimus based immunosuppression in renal allograft recipients with DGF. Histol Histopathol 25: 189-196, 2010
36. Canaud G, Bienaim? F, Viau A, Treins C, BaronW, Nguyen C, BurtinM, Berissi S, Giannakakis K, Muda AO, Zschiedrich S, Huber TB, Friedlander G, Legendre C, Pontoglio M, Pende M, Terzi F: AKT2 is essential to maintain podocyte viability and function during chronic kidney disease. Nat Med 19: 1288-1296, 2013
37. Dayel MJ, Holleran EA, Mullins RD: Arp2/3 complex requires hydrolyzable ATP for nucleation of new actin filaments. Proc Natl Acad Sci USA 98: 14871-14876, 2001
38. RoscaMG, Tandler B, Hoppel CL:Mitochondria in cardiac hypertrophy and heart failure. J Mol Cell Cardiol 55: 31-41, 2013
39. Sharov VG, Todor AV, SilvermanN,Goldstein S, Sabbah HN: Abnormal mitochondrial respiration in failed human myocardium. J Mol Cell Cardiol 32: 2361-2367, 2000
40. Rosca MG, Vazquez EJ, Kerner J, Parland W, Chandler MP, Stanley W, Sabbah HN, Hoppel CL: Cardiac mitochondria in heart failure: Decrease in respirasomes and oxidative phosphorylation. Cardiovasc Res 80: 30-39, 2008
41. Abe Y, Sakairi T, Beeson C, Kopp JB: TGF-b1 stimulates mitochondrial oxidative phosphorylation and generation of reactive oxygen species in cultured mouse podocytes, mediated in part by the mTOR pathway. Am J Physiol Renal Physiol 305: F1477-F1490, 2013
42. James AM, Collins Y, Logan A, Murphy MP: Mitochondrial oxidative stress and the metabolic syndrome. Trends EndocrinolMetab 23: 429-434, 2012
43. Guzy RD, Sharma B, Bell E, Chandel NS, Schumacker PT: Loss of the SdhB, but Not the SdhA, subunit of complex II triggers reactive oxygen species-dependent hypoxia-inducible factor activation and tumorigenesis. Mol Cell Biol 28: 718-731, 2008
44. Stylianou K, Petrakis I, Mavroeidi V, Stratakis S, Kokologiannakis G, Lioudaki E, Liotsi C, Kroustalakis N, Vardaki E, Stratigis S, Perakis K, Kyriazis J, Nakopoulou L, Daphnis E: Rapamycin induced ultrastructural and molecular alterations in glomerular podocytes in healthy mice. Nephrol Dial Transplant 27: 3141-3148, 2012
45. Cohen CD, Klingenhoff A, Boucherot A, Nitsche A, Henger A, Brunner B, Schmid H, Merkle M, Saleem MA, Koller KP, Werner T, Gr?ne HJ, Nelson PJ, Kretzler M: Comparative promoter analysis allows de novo identification of specialized cell junction-associated proteins. Proc Natl Acad Sci USA 103: 5682-5687, 2006
46. Polak P, Cybulski N, Feige JN, Auwerx J, R?eggMA, HallMN: Adiposespecific knockout of raptor results in lean mice with enhanced mitochondrial respiration. Cell Metab 8: 399-410, 2008
47. MoellerMJ,SandenSK,Soofi A,Wiggins RC,Holzman LB: Podocyte-specific expression of cre recombinase in transgenic mice. Genesis 35: 39-42, 2003
48. Eremina V, Jefferson JA, Kowalewska J, Hochster H, Haas M,Weisstuch J, Richardson C, Kopp JB, Kabir MG, Backx PH, Gerber HP, Ferrara N, Barisoni L, Alpers CE, Quaggin SE: VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med 358: 1129-1136, 2008
49. Hodgin JB, Bitzer M, Wickman L, Afshinnia F, Wang SQ, O'Connor C, Yang Y, Meadowbrooke C, Chowdhury M, Kikuchi M, Wiggins JE, Wiggins RC: Glomerular aging and focal global glomerulosclerosis: A podometric perspective. J Am Soc Nephrol 26: 3162-3178, 2015
50. el Nahas AM, Bassett AH, Cope GH, Le Carpentier JE: Role of growth hormone in the development of experimental renal scarring. Kidney Int 40: 29-34, 1991
51. Herbach N, Schairer I, Blutke A, Kautz S, Siebert A, G?ke B, Wolf E, Wanke R: Diabetic kidney lesions of GIPRdn transgenic mice: Podocyte hypertrophy and thickening of the GBM precede glomerular hypertrophy and glomerulosclerosis. Am J Physiol Renal Physiol 296: F819-F829, 2009
52. Weibel ER, Gomez DM: A principle for counting tissue structures on random sections. J Appl Physiol 17: 343-348, 1962
53. Hoeflich A, Weber MM, Fisch T, Nedbal S, Fottner C, Elmlinger MW, Wanke R, Wolf E: Insulin-like growth factor binding protein 2 (IGFBP-2) separates hypertrophic and hyperplastic effects of growth hormone (GH)/IGF-I excess on adrenocortical cells in vivo. FASEB J 16: 1721-1731, 2002
54. Sterio DC: The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134: 127-136, 1984
55. Schell C, Baumhakl L, Salou S, Conzelmann AC, Meyer C, Helmst?dter M, Wrede C, Grahammer F, Eimer S, Kerjaschki D, Walz G, Snapper S, Huber TB: N-wasp is required for stabilization of podocyte foot processes. J Am Soc Nephrol 24: 713-721, 2013