The role of adipose tissue asymmetric dimethylarginine/dimethylarginine dimethylaminohydrolase pathway in adipose tissue phenotype and metabolic abnormalities in subtotally nephrectomized rats

Nephrology Dialysis Transplantation

Volumn 31, Issue 3, 2016, Pages 413-423

  Minakuchi, Hitoshi ^a   Wakino, Shu ^a   Hosoya, Kozi ^a   Sueyasu, Keiko ^a   Hasegawa, Kazuhiro ^a   Shinozuka, Keisuke ^a   Yoshifuji, Ayumi ^a   Futatsugi, Koji ^a   Komatsu, Motoaki ^a   Kanda, Takeshi ^a   Tokuyama, Hirobumi ^a   Hayashi, Koichi ^a   Itoh, Hiroshi ^a  

^a KEIO UNIVERSITY   (Japan)

Author keywords

ADMA; chronic kidney disease; indoxyl sulfate; insulin resistance; uremic toxins

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; CCAAT ENHANCER BINDING PROTEIN ALPHA; CCAAT ENHANCER BINDING PROTEIN BETA; CELL PROTEIN; CREATININE; CYCLIC GMP; DIMETHYLARGININASE; DIMETHYLARGININE DIMETHYLAMINOHYDROLASE 1; DIMETHYLARGININE DIMETHYLAMINOHYDROLASE 2; FATTY ACID; GLUCOSE; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 4; INDICAN; INSULIN; LIPID; MALONALDEHYDE; MESSENGER RNA; N(G),N(G) DIMETHYLARGININE; NITRIC OXIDE SYNTHASE INHIBITOR; NITROGEN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PROTEIN AP2; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; UREA; UREMIC TOXIN; AMIDASE; ARGININE; N,N-DIMETHYLARGININE; RNA;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; ADIPOSE TISSUE ATROPHY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATROPHY; BLOOD PRESSURE; BODY WEIGHT; CELL COUNT; CELL DIFFERENTIATION; CELL MATURATION; CELL SIZE; CHRONIC KIDNEY DISEASE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DISEASE SEVERITY; DOWN REGULATION; DYSLIPIDEMIA; ENZYME ACTIVITY; ENZYME DEGRADATION; EPIDIDYMIS FAT; FATTY ACID BLOOD LEVEL; FIBROBLAST; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HISTOPATHOLOGY; IMPAIRED GLUCOSE TOLERANCE; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; KIDNEY FAILURE; LIPID LIVER LEVEL; LIPID STORAGE; LIPODYSTROPHY; MALE; METABOLIC DISORDER; MUSCLE LEVEL; NEPHRECTOMY; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PERIRENAL FAT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION; TRIACYLGLYCEROL BLOOD LEVEL; UREA BLOOD LEVEL; VASCULAR ENDOTHELIUM; ADVERSE EFFECTS; ANALOGS AND DERIVATIVES; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CHRONIC KIDNEY FAILURE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE; REAL TIME POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT; TRANSGENIC MOUSE; WESTERN BLOTTING;

ADIPOSE TISSUE; AMIDOHYDROLASES; ANIMALS; ARGININE; BLOTTING, WESTERN; CELLS, CULTURED; GENE EXPRESSION REGULATION; MALE; MICE; MICE, TRANSGENIC; NEPHRECTOMY; OXIDATIVE STRESS; PHENOTYPE; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; RENAL INSUFFICIENCY, CHRONIC; RNA; SIGNAL TRANSDUCTION;

EID: 84960087554     PISSN: 09310509     EISSN: 14602385     Source Type: Journal    
DOI: 10.1093/ndt/gfv367     Document Type: Article

References (65)

1. Chmielewski M, Carrero JJ, Stenvinkel P, et al. Metabolic abnormalities in chronic kidney disease that contribute to cardiovascular disease, and nutritional initiatives that may diminish the risk. Curr Opin Lipidol 2009; 20: 3-9
2. Becker B, Kronenberg F, Kielstein JT, et al. Renal insulin resistance syndrome, adiponectin and cardiovascular events in patients with kidney disease: the mild and moderate kidney disease study. J Am Soc Nephrol 2005; 16: 1091-1098
3. Vaziri ND, Yuan J, Ni Z, et al. Lipoprotein lipase deficiency in chronic kidney disease is accompanied by down-regulation of endothelial GPIHBP1 expression. Clin Exp Nephrol 2012; 16: 238-243
4. Guebre-Egziabher F, Alix PM, Koppe L, et al. Ectopic lipid accumulation: a potential cause for metabolic disturbances and a contributor to the alteration of kidney function. Biochimie 2013; 95: 1971-1979
5. Vigouroux C, Caron-Debarle M, Le Dour C, et al. Molecular mechanisms of human lipodystrophies: fromadipocyte lipid droplet to oxidative stress and lipotoxicity. Int J Biochem Cell Biol 2011; 43: 862-876
6. Zhao HL, Sui Y, He L, et al. Lipid partitioning after uninephrectomy. Acta Diabetol 2011; 48: 317-328
7. Zhao HL, Sui Y, Guan J, et al. Fat redistribution and adipocyte transformation in uninephrectomized rats. Kidney Int 2008; 74: 467-477
8. Speer T, Zewinger S, Fliser D. Uraemic dyslipidaemia revisited: role of highdensity lipoprotein. Nephrol Dial Transplant 2013; 28: 2456-2463
9. Pelletier CC, Koppe L, Croze ML, et al. White adipose tissue overproduces the lipid-mobilizing factor zinc a2-glycoprotein in chronic kidney disease. Kidney Int 2013; 83: 878-886
10. Koppe L, Pillon NJ, Vella RE, et al. p-Cresyl sulfate promotes insulin resistance associated with CKD. J Am Soc Nephrol 2013; 24: 88-99
11. Teerlink T, Luo Z, Palm F, et al. Cellular ADMA: regulation and action. Pharmacol Res 2009; 60: 448-460
12. Okubo K, Hayashi K, Wakino S, et al. Role of asymmetrical dimethylarginine in renal microvascular endothelial dysfunction in chronic renal failure with hypertension. Hypertens Res 2005; 28: 181-189
13. Tatematsu S, Wakino S, Kanda T, et al. Role of nitric oxide-producing and -degrading pathways in coronary endothelial dysfunction in chronic kidney disease. J Am Soc Nephrol 2007; 18: 741-749
14. Andreozzi F, Presta I, Mannino GC, et al. A functional variant of the dimethylarginine dimethylaminohydrolase-2 gene is associated with insulin sensitivity. PLoS One 2012; 7: e36224
15. CaglarK, Yilmaz MI, Sonmez Aetal.ADMA, proteinuria, andinsulin resistance in non-diabetic stage I chronic kidney disease. Kidney Int 2006; 70: 781-787
16. Stühlinger MC, Abbasi F, Chu JWet al. Relationship between insulin resistance and an endogenous nitric oxide synthase inhibitor. JAMA 2002; 287: 1420-1426
17. Sydow K, Mondon CE, Schrader J, et al. Dimethylarginine dimethylaminohydrolase overexpression enhances insulin sensitivity. Arterioscler Thromb Vasc Biol 2008; 28: 692-697
18. Spoto B, Parlongo RM, Parlongo G, et al. The enzymatic machinery for ADMA synthesis and degradation is fully expressed in human adipocytes. J Nephrol 2007; 20: 554-559
19. Zheng J, Wang K, Jin P, et al. The association of adipose-derived dimethylarginine dimethylaminohydrolase-2 with insulin sensitivity in experimental type 2 diabetes mellitus. Acta Biochim Biophys Sin (Shanghai) 2013; 45: 641-648
20. Kanda T, Wakino S, Hayashi K, et al. Effect of fasudil on Rho-kinase and nephropathy in subtotally nephrectomized spontaneously hypertensive rats. Kidney Int 2003; 64: 2009-2019
21. Kaku K, Fiedorek FT, Jr, Province M, et al. Genetic analysis of glucose tolerance in inbred mouse strains. Evidence for polygenic control. Diabetes 1988; 37: 707-713
22. Kaku K, Fiedorek FT, Jr, Province M, et al. Enhanced endothelial adhesiveness in hypercholesterolemia is attenuated by L-arginine. Circulation 1994; 89: 2176-2182
23. Dayoub H, Achan V, Adimoolam S, et al. Dimethylarginine dimethylaminohydrolase regulates nitric oxide synthesis: genetic and physiological evidence. Circulation 2003; 108: 3042-3047
24. Hasegawa K, Wakino S, Tatematsu S, et al. Role of asymmetric dimethylarginine in vascular injury in transgenic mice overexpressing dimethylarginie dimethylaminohydrolase 2. Circ Res 2007; 101: e2-e10
25. Hara Y, Wakino S, Tanabe Y, et al. Rho and Rho-kinase activity in adipocytes contributes to a vicious cycle in obesity that may involve mechanical stretch. Sci Signal 2011; 4: ra3
26. Shimizu H, Yisireyili M, Nishijima F, et al. Stat3 contributes to indoxyl sulfate-induced inflammatory and fibrotic gene expression and cellular senescence. Am J Nephrol 2012; 36: 184-189
27. Smith PJ, Wise LS, Berkowitz R, et al. Insulin-like growth factor-I is an essential regulator of the differentiation of 3T3-L1 adipocytes. J Biol Chem 1988; 263: 9402-9408
28. Accili D, Taylor SI. Targeted inactivation of the insulin receptor gene in mouse 3T3-L1 fibroblasts via homologous recombination. Proc Natl Acad Sci USA 1991; 88: 4708-4712
29. Rieusset J, Auwerx J, Vidal H. Regulation of gene expression by activation of the peroxisome proliferator-activated receptor gamma with rosiglitazone (BRL 49653) in human adipocytes. Biochem Biophys Res Commun 1999; 265: 265-271
30. Kim SH, Yu MA, Ryu ES, et al. Indoxyl sulfate-induced epithelial-tomesenchymal transition and apoptosis of renal tubular cells as novel mechanisms of progression of renal disease. Lab Invest 2012; 92: 488-498
31. Adiels M, Taskinen MR, Packard C, et al. Overproduction of large VLDL particles is driven by increased liver fat content in man. Diabetologia 2006; 49: 755-765
32. Vaziri ND, Liang KH. Down-regulation of hepatic LDL receptor expression in experimental nephrosis. Kidney Int 1996; 50: 887-893
33. Vaziri ND, Liang K. Down-regulation of VLDL receptor expression in chronic experimental renal failure. Kidney Int 1997; 51: 913-919
34. Blüher M, Michael MD, Peroni OD, et al. Adipose tissue selective insulin receptor knockout protects against obesity and obesity-related glucose intolerance. Dev Cell 2002; 3: 25-38
35. Barsotti G, Cupisti A, Gervasi GB, et al. Effects of oral administration of heparin sulphate in the rat remnant kidney model. Nephron 1999; 81: 310-316
36. Adamczak M, Gross ML, Amann K, et al. Reversal of glomerular lesions involves coordinated restructuring of glomerular microvasculature. J Am Soc Nephrol 2004; 15: 3063-3072
37. Hosoya K, Minakuchi H, Wakino S, et al. Insulin resistance in chronic kidney disease is ameliorated by spironolactone in rats and humans. Kidney Int 2015; 87: 749-760
38. Thomas SS, Dong Y, Zhang L, et al. Signal regulatory protein-A interacts with the insulin receptor contributing to muscle wasting in chronic kidney disease. Kidney Int 2013; 84: 308-316
39. DeFronzo RA. Insulin resistance: a multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidaemia and atherosclerosis. Neth J Med 1997; 50: 191-197
40. James DE, Burleigh KM, Kraegen EW. Time dependence of insulin action in muscle and adipose tissue in the rat in vivo. An increasing response in adipose tissue with time. Diabetes 1985; 34: 1049-1054
41. Kopelman PG. Obesity as a medical problem. Nature 2000; 404: 635-643
42. Joffe BI, Panz VR, Raal FJ. From lipodystrophy syndromes to diabetes mellitus. Lancet 2001; 357: 1379-1381
43. Abel ED, Peroni O, Kim JK, et al. Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver. Nature 2001; 409: 729-733
44. McLaughlin T, Sherman A, Tsao P, et al. Enhanced proportion of small adipose cells in insulin-resistant vs insulin-sensitive obese individuals implicates impaired adipogenesis. Diabetologia 2007; 50: 1707-1715
45. Yang X, Jansson PA, Nagaev I, et al. Evidence of impaired adipogenesis in insulin resistance. Biochem Biophys Res Commun 2004; 317: 1045-1051
46. Liu A, Sonmez A, Yee G, et al. Differential adipogenic and inflammatory properties of small adipocytes in Zucker Obese and Lean rats. Diab Vasc Dis Res 2010; 7: 311-318
47. Engeli S, Janke J, Gorzelniak K, et al. Regulation of the nitric oxide system in human adipose tissue. J Lipid Res 2004; 45: 1640-1648
48. YanH, Aziz E, ShillabeerGet al. Nitric oxide promotes differentiation of rat white preadipocytes in culture. J Lipid Res 2002; 43: 2123-2129
49. Gagnon A, Chen CS, Sorisky A. Activation of protein kinase B and induction of adipogenesis by insulin in 3T3-L1 preadipocytes: contribution of phosphoinositide-3, 4, 5-trisphosphate versus phosphoinositide-3, 4-bisphosphate. Diabetes 1999; 48: 691-698
50. Kawasaki K, Smith RS, Jr, Hsieh CM, et al. Activation of the phosphatidylinositol 3-kinase/protein kinase Akt pathway mediates nitric oxideinduced endothelial cell migration and angiogenesis. Mol Cell Biol 2003; 23: 5726-5737
51. Doronzo G, Viretto M, Russo I, et al. Nitric oxide activates PI3-K and MAPK signalling pathways in human and rat vascular smooth muscle cells: influence of insulin resistance and oxidative stress. Atherosclerosis 2011; 216: 44-53
52. Bayascas JR. Dissecting the role of the 3-phosphoinositide-dependent protein kinase-1 (PDK1) signalling pathways. Cell Cycle 2008; 7: 2978-2982
53. Luo Z, Teerlink T, Griendling K, et al. Angiotensin II and NADPH oxidase increaseADMAin vascular smoothmuscle cells.Hypertension 2010; 56: 498-504
54. Furukawa S, Fujita T, Shimabukuro M, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 2004; 114: 1752-1761
55. Findeisen HM, Pearson KJ, Gizard F, et al. Oxidative stress accumulates in adipose tissue during aging and inhibits adipogenesis. PLoS One 2011; 6: e18532
56. Lahera V, Goicoechea M, de Vinuesa SG, et al. Oxidative stress in uremia: the role of anemia correction. J Am Soc Nephrol 2006; 17: S174-S177
57. Kim YH, Kwak KA, Gil HW, et al. Indoxyl sulfate promotes apoptosis in cultured osteoblast cells. BMC Pharmacol Toxicol 2013; 14: 60
58. Gondouin B, Cerini C, Dou L, et al. Indolic uremic solutes increase tissue factor production in endothelial cells by the aryl hydrocarbon receptor pathway. Kidney Int 2013; 84: 733-744
59. Muteliefu G, Enomoto A, Jiang P, et al. Indoxyl sulphate induces oxidative stress and the expression of osteoblast-specific proteins in vascular smooth muscle cells. Nephrol Dial Transplant 2009; 24: 2051-2058
60. Ito S, Osaka M, Higuchi Y, et al. Indoxyl sulfate induces leukocyteendothelial interactions through up-regulation of E-selectin. J Biol Chem 2010; 285: 38869-38875
61. Shimba S, Wada T, Tezuka M. Arylhydrocarbon receptor (AhR) is involved in negative regulation of adipose differentiation in 3T3-L1 cells: AhR inhibits adipose differentiation independently of dioxin. J Cell Sci 2001; 114: 2809-2817
62. Kharait S, Haddad DJ, Springer ML. Nitric oxide counters the inhibitory effects of uremic toxin indoxyl sulfate on endothelial cells by governing ERK MAP kinase and myosin light chain activation. Biochem Biophys Res Commun 2011; 409: 758-763
63. Targher G, Chonchol M, Zoppini G, et al. Risk of chronic kidney disease in patients with non-alcoholic fatty liver disease: is there a link? J Hepatol 2011; 54: 1020-1029
64. Zoppini G, Targher G, Chonchol M, et al. Predictors of estimated GFR decline in patients with type 2 diabetes and preserved kidney function. Clin J Am Soc Nephrol 2012; 7: 401-408
65. Sirota JC, McFann K, Targher G, et al. Association between nonalcoholic liver disease and chronic kidney disease: an ultrasound analysis from NHANES 1988-1994. Am J Nephrol 2012; 36: 466-471