Alteration of fatty acid oxidation in tubular epithelial cells: From acute kidney injury to renal fibrogenesis

Frontiers in Medicine

Volumn 2, Issue AUG, 2015, Pages

  Simon, Noémie ^a   Hertig, Alexandre ^a,b  

^a HÔPITAL TENON   (France)

^b Urgences Néphrologiques et Transplantation Rénale Hôpital Tenon 4   (France)

Author keywords

Acute kidney injury; Chronic kidney diseases; Epithelium; Fatty acid oxidation; Fibroblasts; Fibrosis

Indexed keywords

EID: 84966528862     PISSN: None     EISSN: 2296858X     Source Type: Journal    
DOI: 10.3389/fmed.2015.00052     Document Type: Short Survey

References (59)

1. Nangaku M. Chronic hypoxia and tubulointerstitial injury: a final common pathway to end-stage renal failure. J Am Soc Nephrol (2005) 17(1):17-25. doi: 10.1681/ASN.2005070757
2. Nadasdy T, Laszik Z, Blick KE, Johnson DL, Burst-Singer K, Nast C, et al. Human acute tubular necrosis: a lectin and immunohistochemical study. Hum Pathol (1995) 26(2):230-9. doi:10.1016/0046-8177(95)90042-X
3. Rastaldi MP, Ferrario F, Giardino L, Dell'Antonio G, Grillo C, Grillo P, et al. Epithelial-mesenchymal transition of tubular epithelial cells in human renal biopsies. Kidney Int (2002) 62(1):137-46. doi:10.1046/j.1523-1755.2002.00430.x
4. Xu-Dubois Y-C, Baugey E, Peltier J, Colombat M, Ouali N, Jouanneau C, et al. Epithelial phenotypic changes are associated with a tubular active fibrogenic process in human renal grafts. Hum Pathol (2013) 44(7):1251-61. doi:10.1016/j.humpath.2012.10.010
5. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest (2009) 119(6):1420-8. doi:10.1172/JCI39104
6. Galichon P, Finianos S, Hertig A. EMT-MET in renal disease: should we curb our enthusiasm? Cancer Lett (2013) 341(1):24-9. doi:10.1016/j.canlet.2013.04.018
7. Duffield JS. Cellular and molecular mechanisms in kidney fibrosis. J Clin Invest (2014) 124(6):2299-306. doi:10.1172/JCI72267
8. Humphreys BD, Lin S-L, Kobayashi A, Hudson TE, Nowlin BT, Bonventre JV, et al. Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am J Pathol (2010) 176(1):85-97. doi:10.2353/ajpath.2010.090517
9. Galichon P, Hertig A. Epithelial to mesenchymal transition as a biomarker in renal fibrosis: are we ready for the bedside? Fibrogenesis Tissue Repair (2011) 4:11. doi:10.1186/1755-1536-4-11
10. Venkatachalam MA, Bernard DB, Donohoe JF, Levinsky NG. Ischemic damage and repair in the rat proximal tubule: differences among the S1, S2, and S3 segments. Kidney Int (1978) 14(1):31-49. doi:10.1038/ki.1978.87
11. Shanley PF, Brezis M, Spokes K, Silva P, Epstein FH, Rosen S. Hypoxic injury in the proximal tubule of the isolated perfused rat kidney. Kidney Int (1986) 29(5):1021-32. doi:10.1038/ki.1986.102
12. Sugden MC, Holness MJ, Donald E, Lall H. Substrate interactions in the short-and long-term regulation of renal glucose oxidation. Metabolism (1999) 48(6):707-15. doi:10.1016/S0026-0495(99)90169-5
13. Meyer C, Nadkarni V, Stumvoll M, Gerich J. Human kidney free fatty acid and glucose uptake: evidence for a renal glucose-fatty acid cycle. Am J Physiol (1997) 273(3):E650-4
14. Kang HM, Ahn SH, Choi P, Ko Y-A, Han SH, Chinga F, et al. Defective fatty acid oxidation in renal tubular epithelial cells has a key role in kidney fibrosis development. Nat Med (2014) 21(1):37-46. doi:10.1038/nm.3762
15. Lameire NH, Bagga A, Cruz D, De Maeseneer J, Endre Z, Kellum JA, et al. Acute kidney injury: an increasing global concern. Lancet (2013) 382(9887):170-9. doi:10.1016/S0140-6736(13)60647-9
16. Colvin RB. Chronic allograft nephropathy. N Engl J Med (2003) 349(24):2288-90. doi:10.1056/NEJMp038178
17. Bechtel W, McGoohan S, Zeisberg EM, Müller GA, Kalbacher H, Salant DJ, et al. Methylation determines fibroblast activation and fibrogenesis in the kidney. Nat Med (2010) 16(5):544-50. doi:10.1038/nm.2135
18. Yang L, Besschetnova TY, Brooks CR, Shah JV, Bonventre JV. Epithelial cell cycle arrest in G2/M mediates kidney fibrosis after injury. Nat Med (2010) 16(5):535-43; 1p following 143. doi:10.1038/nm.2144
19. Weidemann MJ, Krebs HA. The fuel of respiration of rat kidney cortex. Biochem J (1969) 112(2):149-66
20. Iwao Y, Nakajou K, Nagai R, Kitamura K, Anraku M, Maruyama T, et al. CD36 is one of important receptors promoting renal tubular injury by advanced oxidation protein products. Am J Physiol Renal Physiol (2008) 295(6):F1871-80. doi:10.1152/ajprenal.00013.2008
21. Johnson ACM, Stahl A, Zager RA. Triglyceride accumulation in injured renal tubular cells: alterations in both synthetic and catabolic pathways. Kidney Int (2005) 67(6):2196-209. doi:10.1111/j.1523-1755.2005.00325.x
22. Zager RA, Johnson ACM, Hanson SY. Renal tubular triglyercide accumulation following endotoxic, toxic, and ischemic injury. Kidney Int (2005) 67(1):111-21. doi:10.1111/j.1523-1755.2005.00061.x
23. Ruidera E, Irazu CE, Rajagopalan PR, Orak JK, Fitts CT, Singh I. Fatty acid metabolism in renal ischemia. Lipids (1988) 23(9):882-4. doi:10.1007/BF02536209
24. Portilla D. Role of fatty acid beta-oxidation and calcium-independent phospholipase A2 in ischemic acute renal failure. Curr Opin Nephrol Hypertens (1999) 8(4):473-7. doi:10.1097/00041552-199907000-00012
25. Gulati S, Ainol L, Orak J, Singh AK, Singh I. Alterations of peroxisomal function in ischemia-reperfusion injury of rat kidney. Biochim Biophys Acta (1993) 1182(3):291-8. doi:10.1016/0925-4439(93)90071-8
26. Idrovo J-P, Yang W-L, Nicastro J, Coppa GF, Wang P. Stimulation of carnitine palmitoyltransferase 1 improves renal function and attenuates tissue damage after ischemia/reperfusion. J Surg Res (2012) 177(1):157-64. doi:10.1016/j.jss.2012.05.053
27. Feldkamp T, Kribben A, Roeser NF, Senter RA, Weinberg JM. Accumulation of nonesterified fatty acids causes the sustained energetic deficit in kidney proximal tubules after hypoxia-reoxygenation. Am J Physiol Renal Physiol (2006) 290(2):F465-77. doi:10.1152/ajprenal.00305.2005
28. Lefebvre P. Sorting out the roles of PPAR in energy metabolism and vascular homeostasis. J Clin Invest (2006) 116(3):571-80. doi:10.1172/JCI27989
29. Portilla D, Dai G, Mcclure T, Bates L, Kurten R, Megyesi J, et al. Alterations of PPARalpha and its coactivator PGC-1 in cisplatin-induced acute renal failure. Kidney Int (2002) 62(4):1208-18. doi:10.1111/j.1523-1755.2002.kid553.x
30. Takahashi K, Kamijo Y, Hora K, Hashimoto K, Higuchi M, Nakajima T, et al. Pretreatment by low-dose fibrates protects against acute free fatty acid-induced renal tubule toxicity by counteracting PPARa deterioration. Toxicol Appl Pharmacol (2011) 252(3):237-49. doi:10.1016/j.taap.2011.02.012
31. Tran M, Tam D, Bardia A, Bhasin M, Rowe GC, Kher A, et al. PGC-1a promotes recovery after acute kidney injury during systemic inflammation in mice. J Clin Invest (2011) 121(10):4003-14. doi:10.1172/JCI58662
32. Zhong X, Chung ACK, Chen H-Y, Meng X-M, Lan HY. Smad3-mediated upregulation of miR-21 promotes renal fibrosis. J Am Soc Nephrol (2011) 22(9):1668-81. doi:10.1681/ASN.2010111168
33. Chau BN, Xin C, Hartner J, Ren S, Castano AP, Linn G, et al. MicroRNA-21 promotes fibrosis of the kidney by silencing metabolic pathways. Sci Transl Med (2012) 4(121):ra18-121. doi:10.1126/scitranslmed.3003205
34. Kato M. Reduction of fatty acid oxidation and responses to hypoxia correlate with the progression of de-differentiation in HCC. Mol Med Rep (2012) 7:1-6. doi:10.3892/mmr.2012.1201
35. Xu Y, Huang J, Xin W, Chen L, Zhao X, Lv Z, et al. Lipid accumulation is ahead of epithelial-to-mesenchymal transition and therapeutic intervention by acetyl-CoA carboxylase 2 silence in diabetic nephropathy. Metabolism (2014) 63(5):716-26. doi:10.1016/j.metabol.2014.02.010
36. Bobulescu IA. Renal lipid metabolism and lipotoxicity. Curr Opin Nephrol Hypertens (2010) 19(4):393-402. doi:10.1097/MNH.0b013e32833aa4ac
37. Wahba IM, Mak RH. Obesity and obesity-initiated metabolic syndrome: mechanistic links to chronic kidney disease. Clin J Am Soc Nephrol (2007) 2(3):550-62. doi:10.2215/CJN.04071206
38. Jiang T, Wang Z, Proctor G, Moskowitz S, Liebman SE, Rogers T, et al. Diet-induced obesity in C57BL/6J mice causes increased renal lipid accumulation and glomerulosclerosis via a sterol regulatory element-binding protein-1c dependent pathway. J Biol Chem (2005) 280(37):32317-25. doi:10.1074/jbc.M500801200
39. Proctor G, Jiang T, Iwahashi M, Wang Z, Li J, Levi M. Regulation of renal fatty acid and cholesterol metabolism, inflammation, and fibrosis in Akita and OVE26 mice with type 1 diabetes. Diabetes (2006) 55(9):2502-9. doi:10.2337/db05-0603
40. Arici M. Stimulation of proximal tubular cell apoptosis by albumin-bound fatty acids mediated by peroxisome proliferator activated receptor-gamma. J Am Soc Nephrol (2003) 14(1):17-27. doi:10.1097/01.ASN.0000042167.66685.EA
41. Ruggiero C, Elks CM, Kruger C, Cleland E, Addison K, Noland RC, et al. Albumin-bound fatty acids but not albumin itself alter redox balance in tubular epithelial cells and induce a peroxide-mediated redox-sensitive apoptosis. Am J Physiol Renal Physiol (2014) 306(8):F896-906. doi:10.1152/ajprenal.00484.2013
42. Kees-Folts D, Sadow JL, Schreiner GF. Tubular catabolism of albumin is associated with the release of an inflammatory lipid. Kidney Int (1994) 45(6):1697-709. doi:10.1038/ki.1994.222
43. Soumura M, Kume S, Isshiki K, Takeda N, Araki S, Tanaka Y, et al. Oleate and eicosapentaenoic acid attenuate palmitate-induced inflammation and apoptosis in renal proximal tubular cell. Biochem Biophys Res Commun (2010) 402(2):265-71. doi:10.1016/j.bbrc.2010.10.012
44. Katsoulieris E, Mabley JG, Samai M, Sharpe MA, Green IC, Chatterjee PK. Lipotoxicity in renal proximal tubular cells: relationship between endoplasmic reticulum stress and oxidative stress pathways. Free Radic Biol Med (2010) 48(12):1654-62. doi:10.1016/j.freeradbiomed.2010.03.021
45. Weinberg JM. Lipotoxicity. Kidney Int (2006) 70(9):1560-6. doi:10.1038/sj.ki.5001834
46. Okamura DM, Pennathur S, Pasichnyk K, Lopez-Guisa JM, Collins S, Febbraio M, et al. CD36 regulates oxidative stress and inflammation in hypercholesterolemic CKD. J Am Soc Nephrol (2009) 20(3):495-505. doi:10.1681/ASN.2008010009
47. Li S, Nagothu KK, Desai V, Lee T, Branham W, Moland C, et al. Transgenic expression of proximal tubule peroxisome proliferator-activated receptor-a in mice confers protection during acute kidney injury. Kidney Int (2009) 76(10):1049-62. doi:10.1038/ki.2009.330
48. Nagothu KK, Bhatt R, Kaushal GP, Portilla D. Fibrate prevents cisplatin-induced proximal tubule cell death. Kidney Int (2005) 68(6):2680-93. doi:10.1111/j.1523-1755.2005.00739.x
49. Sivarajah A, Chatterjee PK, Hattori Y, Brown PA, Stewart KN, Todorovic Z, et al. Agonists of peroxisome-proliferator activated receptor-alpha (clofibrate and WY14643) reduce renal ischemia/reperfusion injury in the rat. Med Sci Monit (2002) 8(12):BR532-9
50. Portilla D, Dai G, Peters JM, Gonzalez FJ, Crew MD, Proia AD. Etomoxir-induced PPARa-modulated enzymes protect during acute renal failure. Am J Physiol Renal Physiol (2000) 278(4):F667-75
51. Patel NSA, di Paola R, Mazzon E, Britti D, Thiemermann C, Cuzzocrea S. Peroxisome proliferator-activated receptor-alpha contributes to the resolution of inflammation after renal ischemia/reperfusion injury. J Pharmacol Exp Ther (2009) 328(2):635-43. doi:10.1124/jpet.108.146191
52. Tanaka Y, Kume S, Araki S, Isshiki K, Chin-Kanasaki M, Sakaguchi M, et al. Fenofibrate, a PPARa agonist, has renoprotective effects in mice by enhancing renal lipolysis. Kidney Int (2011) 79(8):871-82. doi:10.1038/ki.2010.530
53. Chung HW, Lim JH, Kim MY, Shin SJ, Chung S, Choi BS, et al. High-fat diet-induced renal cell apoptosis and oxidative stress in spontaneously hypertensive rat are ameliorated by fenofibrate through the PPAR-FoxO3a-PGC-1 pathway. Nephrol Dial Transplant (2012) 27(6):2213-25. doi:10.1093/ndt/gfr613
54. Keech A, Simes RJ, Barter P, Best J, Scott R, Taskinen MR, et al. Effects of long-term fenofibrate therapy on cardiovascular events in 9795 people with type 2 diabetes mellitus (the FIELD study): randomised controlled trial. Lancet (2005) 366(9500):1849-61. doi:10.1016/S0140-6736(05)67667-2
55. Cases A, Coll E. Dyslipidemia and the progression of renal disease in chronic renal failure patients. Kidney Int (2005) 68(S99):S87-93. doi:10.1111/j.1523-1755.2005.09916.x
56. Hottelart C, el Esper N, Achard JM, Pruna A, Fournier A. [Fenofibrate increases blood creatinine, but does not change the glomerular filtration rate in patients with mild renal insufficiency]. Nephrologie (1999) 20(1):41-4
57. Jun M, Zhu B, Tonelli M, Jardine MJ, Patel A, Neal B, et al. Effects of fibrates in kidney disease. J Am Coll Cardiol (2012) 60(20):2061-71. doi:10.1016/j.jacc.2012.07.049
58. Decleves A-E, Zolkipli Z, Satriano J, Wang L, Nakayama T, Rogac M, et al. Regulation of lipid accumulation by AMK-activated kinase in high fat diet-induced kidney injury. Kidney Int (2013) 85(3):611-23. doi:10.1038/ki.2013.462
59. Mister M, Noris M, Szymczuk J, Azzollini N, Aiello S, Abbate M, et al. Propionyl-l-carnitine prevents renal function deterioration due to ischemia/reperfusion. Kidney Int (2002) 61(3):1064-78. doi:10.1046/j.1523-1755.2002.00212.x