Fatty kidney: Emerging role of ectopic lipid in obesity-related renal disease

The Lancet Diabetes and Endocrinology

Volumn 2, Issue 5, 2014, Pages 417-426

  De Vries, Aiko P J ^a   Ruggenenti, Piero ^b,c   Ruan, Xiong Z ^d,e   Praga, Manuel ^f   Cruzado, Josep M ^g   Bajema, Ingeborg M ^a   D'Agati, Vivette D ^h   Lamb, Hildo J ^a   Barlovic, Drazenka Pongrac ⁱ   Hojs, Radovan ^j   Abbate, Manuela ^b   Rodriquez, Rosa ^k   Mogensen, Carl Erik ^l   Porrini, Esteban ^m  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^c Azienda Ospedaliera Papa Giovanni XXIII   (Italy)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e SHENZHEN UNIVERSITY   (China)

^f UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^g HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^h New York Presbyterian Morgan Stanley Children's Hospital   (United States)

ⁱ UNIVERSITY MEDICAL CENTRE LJUBLJANA   (Slovenia)

^j UNIVERSITY OF MARIBOR   (Slovenia)

^k HOSPITAL UNIVERSITARIO DE CANARIAS   (Spain)

^l AARHUS UNIVERSITY HOSPITAL   (Denmark)

^m UNIVERSIDAD DE LA LAGUNA   (Spain)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; FATTY ACID; LIPID; ALBUMIN; DOXERCALCIFEROL; FENOFIBRATE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; RAMIPRIL;

CELL TRANSFORMATION; CHRONIC KIDNEY DISEASE; DISEASE ASSOCIATION; DISEASE COURSE; FATTY KIDNEY; GLOMERULOPATHY; GLOMERULUS FILTRATION; GLUCONEOGENESIS; HUMAN; INSULIN RESISTANCE; KIDNEY DISEASE; LIPID STORAGE; MESANGIUM CELL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OBESITY; OBESITY RELATED GLOMERULOPATHY; PATHOPHYSIOLOGY; PODOCYTE; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; ALBUMINURIA; BODY MASS; ECTOPIC LIPID; GLOMERULOMEGALY; GLOMERULUS FILTRATION RATE; HYPERLIPIDEMIA; KIDNEY PLASMA FLOW; KIDNEY TUBULE; NEPHROTOXICITY; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; RISK FACTOR; WEIGHT REDUCTION; CHRONIC KIDNEY FAILURE; COMPLICATION; FEMALE; LIPID METABOLISM; MALE; METABOLISM; PATHOLOGY;

FEMALE; HUMANS; LIPID METABOLISM; MALE; OBESITY; RENAL INSUFFICIENCY, CHRONIC; RISK FACTORS;

EID: 84899697896     PISSN: 22138587     EISSN: None     Source Type: Journal    
DOI: 10.1016/S2213-8587(14)70065-8     Document Type: Review

References (107)

1. Eckardt KU, Coresh J, Devuyst O, et al. Evolving importance of kidney disease: from subspecialty to global health burden. Lancet 2013, 382:158-169.
2. USRDS 2012 annual data report: atlas of chronic kidney disease and end-stage renal disease in the United States 2012, US Renal Data System, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Disease, Bethesda, MD.
3. Alberti KGMM, Zimmet P, Shaw J Metabolic syndrome-a new world-wide definition. A consensus statement from the International Diabetes Federation. Diabet Med 2006, 23:469-480.
4. Thomas G, Sehgal AR, Kashyap SR, et al. Metabolic syndrome and kidney disease: a systematic review and meta-analysis. Clin J Am Soc Nephrol 2011, 6:2364-2373.
5. Blüher M The distinction of metabolically 'healthy' from 'unhealthy' obese individuals. Curr Opin Lipidol 2010, 21:38-43.
6. Kwakernaak AJ, Zelle DM, Bakker SJL, Navis G Central body fat distribution associates with unfavorable renal hemodynamics independent of body mass index. J Am Soc Nephrol 2013, 24:987-994.
7. Elsayed EF, Sarnak MJ, Tighiouart H, et al. Waist-to-hip ratio, body mass index, and subsequent kidney disease and death. Am J Kidney Dis 2008, 52:29-38.
8. Reaven GM Banting lecture 1988. Role of insulin resistance in human disease. Diabetes 1988, 37:1595-1607.
9. Hsu CY, McCulloch CE, Iribarren C, Darbinian J, Go AS Body mass index and risk for end-stage renal disease. Ann Intern Med 2006, 144:21-28.
10. Waist circumference and waist-hip ratio: report of a WHO expert consultation 2011, WHO, World Health Organization, Geneva.
11. Tan CE, Ma S, Wai D, Chew SK, Tai ES Can we apply the National Cholesterol Education Program Adult Treatment Panel definition of the metabolic syndrome to Asians?. Diabetes Care 2004, 27:1182-1186.
12. Lean MEJ, Han TS, Morrison CE Waist circumference as a measure for indicating need for weight management. BMJ 1995, 311:158-161.
13. Munkhaugen J, Lydersen S, Widerøe TE, Hallan S Prehypertension, obesity, and risk of kidney disease: 20-year follow-up of the HUNT I study in Norway. Am J Kidney Dis 2009, 54:638-646.
14. Wahba IM, Mak RH Obesity and obesity-initiated metabolic syndrome: mechanistic links to chronic kidney disease. Clin J Am Soc Nephrol 2007, 2:550-562.
15. Griffin KA, Kramer H, Bidani AK Adverse renal consequences of obesity. Am J Physiol Renal Physiol 2008, 294:F685-F696.
16. Bonnet F, Deprele C, Sassolas A, et al. Excessive body weight as a new independent risk factor for clinical and pathological progression in primary IgA nephritis. Am J Kidney Dis 2001, 37:720-727.
17. Praga M, Hernández E, Herrero JC, et al. Influence of obesity on the appearance of proteinuria and renal insufficiency after unilateral nephrectomy. Kidney Int 2000, 58:2111-2118.
18. Kurella M Metabolic syndrome and the risk for chronic kidney disease among nondiabetic adults. J Am Soc Nephrol 2005, 16:2134-2140.
19. Oterdoom LH, de Vries APJ, Gansevoort RT, et al. Fasting insulin modifies the relation between age and renal function. Nephrol Dial Transplant 2007, 22:1587-1592.
20. Tomaszewski M, Charchar FJ, Maric C, et al. Glomerular hyperfiltration: a new marker of metabolic risk. Kidney Int 2007, 71:816-821.
21. Helal I, Fick-Brosnahan GM, Reed-Gitomer B, Schrier RW Glomerular hyperfiltration: definitions, mechanisms and clinical implications. Nat Rev Nephrol 2012, 8:293-300.
22. Kwakernaak AJ, Toering TJ, Navis G Body mass index and body fat distribution as renal risk factors: a focus on the role of renal haemodynamics. Nephrol Dial Transplant 2013, 28(suppl 4):iv42-iv49.
23. Ter Maaten JC, Bakker SJ, Serné EH, et al. Insulin's acute effects on glomerular filtration rate correlate with insulin sensitivity whereas insulin's acute effects on proximal tubular sodium reabsorption correlation with salt sensitivity in normal subjects. Nephrol Dial Transplant 1999, 14:2357-2363.
24. Rüster C, Wolf G The role of the renin-angiotensin-aldosterone system in obesity-related renal diseases. Semin Nephrol 2013, 33:44-53.
25. Brenner BM Hemodynamically mediated glomerular injury and the progressive nature of kidney disease. Kidney Int 1983, 23:647-655.
26. Ruggenenti P, Porrini EL, Gaspari F, et al. Glomerular hyperfiltration and renal disease progression in type 2 diabetes. Diabetes Care 2012, 35:2061-2068.
27. Kambham N, Markowitz G, Valeri A, Lin J, D'Agati VD Obesity-related glomerulopathy: an emerging epidemic. Kidney Int 2001, 59:1498-1509.
28. Chen HM, Liu ZH, Zeng CH, et al. Podocyte lesions in patients with obesity-related glomerulopathy. Am J Kidney Dis 2006, 48:772-779.
29. Verani RR Obesity-associated focal segmental glomerulosclerosis: pathological features of the lesion and relationship with cardiomegaly and hyperlipidemia. Am J Kidney Dis 1992, 20:629-634.
30. Kato S, Nazneen A, Nakashima Y, et al. Pathological influence of obesity on renal structural changes in chronic kidney disease. Clin Exp Nephrol 2009, 13:332-340.
31. Serra A, Romero R, Lopez D, et al. Renal injury in the extremely obese patients with normal renal function. Kidney Int 2008, 73:947-955.
32. Bidani AK, Mitchell KD, Schwartz MM, Navar LG, Lewis EJ Absence of glomerular injury or nephron loss in a normotensive rat remnant kidney model. Kidney Int 1990, 38:28-38.
33. Kriz W, Elger M, Mundel P, Lemley KV Structure-stabilizing forces in the glomerular tuft. J Am Soc Nephrol 1995, 5:1731-1739.
34. D'Agati VD, Kaskel FJ, Falk RJ Focal segmental glomerulosclerosis. N Engl J Med 2011, 365:2398-2411.
35. Wu Y, Liu Z, Xiang Z, et al. Obesity-related glomerulopathy: insights from gene expression profiles of the glomeruli derived from renal biopsy samples. Endocrinology 2006, 147:44-50.
36. Ruan XZ, Varghese Z, Moorhead JF An update on the lipid nephrotoxicity hypothesis. Nat Rev Nephrol 2009, 5:713-721.
37. Unger RH, Clark GO, Scherer PE, Orci L Lipid homeostasis, lipotoxicity and the metabolic syndrome. Biochim Biophys Acta 2010, 1801:209-214.
38. Bjárntorp P "Portal" adipose tissue as a generator of risk factors for cardiovascular disease and diabetes. Arteriosclerosis 1990, 10:493-496.
39. Steinberg D, Parthasarathy S, Carew TE, Khoo JC, Witztum JL Beyond cholesterol. Modifications of low-density lipoprotein that increase its atherogenicity. N Engl J Med 1989, 320:915-924.
40. Straub BK, Gyoengyoesi B, Koenig M, et al. Adipophilin/perilipin-2 as a lipid droplet-specific marker for metabolically active cells and diseases associated with metabolic dysregulation. Histopathology 2013, 62:617-631.
41. Bozza PT, Magalhães KG, Weller PF Leukocyte lipid bodies-biogenesis and functions in inflammation. Biochim Biophys Acta 2009, 1791:540-551.
42. Shashkin P, Dragulev B, Ley K Macrophage differentiation to foam cells. Curr Pharm Des 2005, 11:3061-3072.
43. Unger RH, Orci L Lipotoxic diseases of nonadipose tissues in obesity. Int J Obes Relat Metab Disord 2000, 24(suppl 4):S28-S32.
44. Savage DB, Petersen KF, Shulman GI Disordered lipid metabolism and the pathogenesis of insulin resistance. Physiol Rev 2007, 87:507-520.
45. Befroy DE, Petersen KF, Dufour S, et al. Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients. Diabetes 2007, 56:1376-1381.
46. Montani JP, Carroll JF, Dwyer TM, et al. Ectopic fat storage in heart, blood vessels and kidneys in the pathogenesis of cardiovascular diseases. Int J Obes Relat Metab Disord 2004, 28(suppl 4):S58-S65.
47. Armstrong MJ, Adams LA, Canbay A, Syn WK Extrahepatic complications of nonalcoholic fatty liver disease. Hepatology 2014, 59:1174-1197.
48. Ruan XZ, Moorhead JF, Varghese Z Lipid redistribution in renal dysfunction. Kidney Int 2008, 74:407-409.
49. Rickards E Remarks on the fatty transformation of the kidney. BMJ 1883, 2:2-3.
50. Schlöndorff D, Banas B The mesangial cell revisited: no cell is an island. J Am Soc Nephrol 2009, 20:1179-1187.
51. Lindahl P, Johansson BR, Levéen P, Betsholtz C Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 1997, 277:242-245.
52. Ruan XZ, Varghese Z, Powis SH, Moorhead JF Human mesangial cells express inducible macrophage scavenger receptor. Kidney Int 1999, 56:440-451.
53. Takemura T, Yoshioka K, Aya N, et al. Apolipoproteins and lipoprotein receptors in glomeruli in human kidney diseases. Kidney Int 1993, 43:918-927.
54. Li J, Li H, Wen YB, Li XW Very-low-density lipoprotein-induced triglyceride accumulation in human mesangial cells is mainly mediated by lipoprotein lipase. Nephron Physiol 2008, 110:p1-10.
55. Chen Y, Ruan XZ, Li Q, et al. Inflammatory cytokines disrupt LDL-receptor feedback regulation and cause statin resistance: a comparative study in human hepatic cells and mesangial cells. Am J Physiol Renal Physiol 2007, 293:F680-F687.
56. Berfield AK, Andress DL, Abrass CK IGF-1-induced lipid accumulation impairs mesangial cell migration and contractile function. Kidney Int 2002, 62:1229-1237.
57. Ruan XZ, Varghese Z, Powis SH, Moorhead JF Dysregulation of LDL receptor under the influence of inflammatory cytokines: a new pathway for foam cell formation. Kidney Int 2001, 60:1716-1725.
58. Li Z, Woollard JR, Wang S, et al. Increased glomerular filtration rate in early metabolic syndrome is associated with renal adiposity and microvascular proliferation. Am J Physiol Renal Physiol 2011, 301:F1078-F1087.
59. Matsusaka T, Sandgren E, Shintani A, et al. Podocyte injury damages other podocytes. J Am Soc Nephrol 2011, 22:1275-1285.
60. Lasagni L, Romagnani P Glomerular epithelial stem cells: the good, the bad, and the ugly. J Am Soc Nephrol 2010, 21:1612-1619.
61. Fukuda A, Chowdhury MA, Venkatareddy MP, et al. Growth-dependent podocyte failure causes glomerulosclerosis. J Am Soc Nephrol 2012, 23:1351-1363.
62. Lieberthal W, Levine JS Mammalian target of rapamycin and the kidney. I. The signaling pathway. Am J Physiol Renal Physiol 2012, 303:F1-10.
63. Laplante M, Sabatini DM mTOR signaling in growth control and disease. Cell 2012, 149:274-293.
64. Gödel M, Hartleben B, Herbach N, et al. Role of mTOR in podocyte function and diabetic nephropathy in humans and mice. J Clin Invest 2011, 121:2197-2209.
65. Inoki K, Mori H, Wang J, et al. mTORC1 activation in podocytes is a critical step in the development of diabetic nephropathy in mice. J Clin Invest 2011, 121:2181-2196.
66. Um SH, Frigerio F, Watanabe M, et al. Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 2004, 431:200-205.
67. Hale LJ, Coward RJ The insulin receptor and the kidney. Curr Opin Nephrol Hypertens 2013, 22:100-106.
68. Welsh GI, Hale LJ, Eremina V, et al. Insulin signaling to the glomerular podocyte is critical for normal kidney function. Cell Metab 2010, 12:329-340.
69. Lennon R, Pons D, Sabin MA, et al. Saturated fatty acids induce insulin resistance in human podocytes: implications for diabetic nephropathy. Nephrol Dial Transplant 2009, 24:3288-3296.
70. Sieber J, Lindenmeyer MT, Kampe K, et al. Regulation of podocyte survival and endoplasmic reticulum stress by fatty acids. Am J Physiol Renal Physiol 2010, 299:F821-F829.
71. Zhang G, Li Q, Wang L, et al. Interleukin-1β enhances the intracellular accumulation of cholesterol by up-regulating the expression of low-density lipoprotein receptor and 3-hydroxy-3-methylglutaryl coenzyme A reductase in podocytes. Mol Cell Biochem 2011, 346:197-204.
72. Quaschning T, Käniger M, Kråmer-Guth A, et al. Receptor-mediated lipoprotein uptake by human glomerular cells: comparison with skin fibroblasts and HepG2 cells. Nephrol Dial Transplant 1997, 12:2528-2536.
73. Mayrhofer C, Krieger S, Huttary N, et al. Alterations in fatty acid utilization and an impaired antioxidant defense mechanism are early events in podocyte injury: a proteomic analysis. Am J Pathol 2009, 174:1191-1202.
74. Gutwein P, Abdel-Bakky MS, Schramme A, et al. CXCL16 is expressed in podocytes and acts as a scavenger receptor for oxidized low-density lipoprotein. Am J Pathol 2009, 174:2061-2072.
75. Tobar A, Ori Y, Benchetrit S, et al. Proximal tubular hypertrophy and enlarged glomerular and proximal tubular urinary space in obese subjects with proteinuria. PloS One 2013, 8:e75547.
76. Brunskill NJ, Stuart J, Tobin AB, Walls J, Nahorski S Receptor-mediated endocytosis of albumin by kidney proximal tubule cells is regulated by phosphatidylinositide 3-kinase. J Clin Invest 1998, 101:2140-2150.
77. Yamahara K, Kume S, Koya D, et al. Obesity-mediated autophagy insufficiency exacerbates proteinuria-induced tubulointerstitial lesions. J Am Soc Nephrol 2013, 24:1769-1781.
78. Nieth H, Schollmeyer P Substrate-utilization of the human kidney. Nature 1966, 209:1244-1245.
79. Wirthensohn G, Guder WG Renal lipid metabolism. Miner Electrolyte Metab 1983, 9:203-211.
80. Furuhashi M, Hotamisligil GS Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets. Nat Rev Drug Discov 2008, 7:489-503.
81. Suzuki K, Babazono T, Murata H, Iwamoto Y Clinical significance of urinary liver-type fatty acid-binding protein in patients with diabetic nephropathy. Diabetes Care 2005, 28:2038-2039.
82. Thomas ME, Harris KPG, Walls J, Furness PN, Brunskill NJ Fatty acids exacerbate tubulointerstitial injury in protein-overload proteinuria. Am J Physiol Renal Physiol 2002, 283:F640-F647.
83. Mandel LJ Metabolic substrates, cellular energy production, and the regulation of proximal tubular transport. Annu Rev Physiol 1985, 47:85-101.
84. Gerich JE Role of the kidney in normal glucose homeostasis and in the hyperglycaemia of diabetes mellitus: therapeutic implications. Diabet Med 2010, 27:136-142.
85. Marsenic O Glucose control by the kidney: an emerging target in diabetes. Am J Kidney Dis 2009, 53:875-883.
86. Owen OE, Felig P, Morgan AP, Wahren J, Cahill GF Liver and kidney metabolism during prolonged starvation. J Clin Invest 1969, 48:574-583.
87. Meyer C, Dostou J, Nadkarni V, Gerich J Effects of physiological hyperinsulinemia on systemic, renal, and hepatic substrate metabolism. Am J Physiol 1998, 275(6 pt 2):F915-F921.
88. Tiwari S, Singh RS, Li L, et al. Deletion of the insulin receptor in the proximal tubule promotes hyperglycemia. J Am Soc Nephrol 2013, 24:1209-1214.
89. Weisinger JR, Kempson RL, Eldridge FL, Swenson RS The nephrotic syndrome: a complication of massive obesity. Ann Intern Med 1974, 81:440-447.
90. Praga M, Morales E, Herrero JC, et al. Absence of hypoalbuminemia despite massive proteinuria in focal segmental glomerulosclerosis secondary to hyperfiltration. Am J Kidney Dis 1999, 33:52-58.
91. McLaughlin T, Reaven G, Abbasi F, et al. Is there a simple way to identify insulin-resistant individuals at increased risk of cardiovascular disease?. Am J Cardiol 2005, 96:399-404.
92. Rook M, Bosma RJ, van Son WJ, et al. Nephrectomy elicits impact of age and BMI on renal hemodynamics: lower postdonation reserve capacity in older or overweight kidney donors. Am J Transplant 2008, 8:2077-2085.
93. Rea DJ, Heimbach JK, Grande JP, et al. Glomerular volume and renal histology in obese and non-obese living kidney donors. Kidney Int 2006, 70:1636-1641.
94. Gaspari F, Ruggenenti P, Porrini E, et al. The GFR and GFR decline cannot be accurately estimated in type 2 diabetics. Kidney Int 2013, 84:164-173.
95. Rijzewijk LJ, van der Meer RW, Smit JWA, et al. Myocardial steatosis is an independent predictor of diastolic dysfunction in type 2 diabetes mellitus. J Am Coll Cardiol 2008, 52:1793-1799.
96. Thomas EL, Hamilton G, Patel N, et al. Hepatic triglyceride content and its relation to body adiposity: a magnetic resonance imaging and proton magnetic resonance spectroscopy study. Gut 2005, 54:122-127.
97. Hammer S, de Vries APJ, de Heer P, et al. Metabolic imaging of human kidney triglyceride content: reproducibility of proton magnetic resonance spectroscopy. PloS One 2013, 8:e62209.
98. Bobulescu IA Renal lipid metabolism and lipotoxicity. Curr Opin Nephrol Hypertens 2010, 19:393-402.
99. Peng XG, Bai YY, Fang F, et al. Renal lipids and oxygenation in diabetic mice: noninvasive quantification with MR imaging. Radiology 2013, 269:748-757.
100. Neubauer S The failing heart-an engine out of fuel. N Engl J Med 2007, 356:1140-1151.
101. Bizino MB, Hammer S, Lamb HJ Metabolic imaging of the human heart: clinical application of magnetic resonance spectroscopy. Heart 2013, published online one July 31. http://dx.doi.org/10.1136/heartjnl-2012-302546.
102. Navaneethan SD, Yehnert H, Moustarah F, et al. Weight loss interventions in chronic kidney disease: a systematic review and meta-analysis. Clin J Am Soc Nephrol 2009, 4:1565-1574.
103. Mallamaci F, Ruggenenti P, Perna A, et al. ACE inhibition is renoprotective among obese patients with proteinuria. J Am Soc Nephrol 2011, 22:1122-1128.
104. Tanaka Y, Kume S, Araki SI, et al. Fenofibrate, a PPARα agonist, has renoprotective effects in mice by enhancing renal lipolysis. Kidney Int 2011, 79:871-882.
105. Wang XX, Jiang T, Shen Y, et al. The farnesoid X receptor modulates renal lipid metabolism and diet-induced renal inflammation, fibrosis, and proteinuria. Am J Physiol Renal Physiol 2009, 297:F1587-F1596.
106. Wang XX, Jiang T, Shen Y, et al. Vitamin D receptor agonist doxercalciferol modulates dietary fat-induced renal disease and renal lipid metabolism. Am J Physiol Renal Physiol 2011, 300:F801-F810.
107. Lloberas N, Cruzado JM, Franquesa M, et al. Mammalian target of rapamycin pathway blockade slows progression of diabetic kidney disease in rats. J Am Soc Nephrol 2006, 17:1395-1404.