Insulin resistance in chronic kidney disease: New lessons from experimental models

Nephrology Dialysis Transplantation

Volumn 29, Issue 9, 2014, Pages 1666-1674

  Koppe, Laetitia ^a,b   Pelletier, Caroline C ^a,b   Alix, Pascaline M ^a,b   Kalbacher, Emilie ^a,b   Fouque, Denis ^a,b   Soulage, Christophe O ^b   Guebre Egziabher, Fitsum ^a,b  

^a UNIVERSITÉ DE LYON   (France)

^b EDOUARD HERRIOT HOSPITAL   (France)

Author keywords

Chronic kidney disease; Inflammation; Insulin resistance; Lipotoxicity; Uraemic toxins

Indexed keywords

INSULIN; UREMIC TOXIN; CALCITRIOL; PSEUDOURIDINE; URIC ACID;

ACIDOSIS; CARBAMOYLATION; CHRONIC KIDNEY DISEASE; DISEASE ASSOCIATION; HORMONE ACTION; HUMAN; HYPERPARATHYROIDISM; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; INTESTINE FLORA; KIDNEY FUNCTION; LIPOTOXICITY; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN MODIFICATION; REVIEW; SIGNAL TRANSDUCTION; UREMIA; VITAMIN D DEFICIENCY; WHITE ADIPOSE TISSUE; ANIMAL; ANIMAL MODEL; CHRONIC KIDNEY FAILURE; ENERGY METABOLISM; HOMEOSTASIS; INTESTINE; LIVER; MICROBIOLOGY; OBESITY; PATHOPHYSIOLOGY; PHYSIOLOGY; SKELETAL MUSCLE; ADIPOSE TISSUE; ARTICLE; CARDIOVASCULAR MORTALITY; CLINICAL FEATURE; DYSBIOSIS; EXPERIMENTAL MODEL; FATTY ACID OXIDATION; KIDNEY DYSFUNCTION; LIPID STORAGE; LIPOATROPHY; METABOLIC ACIDOSIS;

ADIPOSE TISSUE, WHITE; ANIMALS; ENERGY METABOLISM; HOMEOSTASIS; HUMANS; INFLAMMATION; INSULIN RESISTANCE; INTESTINES; LIVER; MODELS, ANIMAL; MUSCLE, SKELETAL; OBESITY; RENAL INSUFFICIENCY, CHRONIC; SIGNAL TRANSDUCTION; UREMIA;

EID: 84907413131     PISSN: 09310509     EISSN: 14602385     Source Type: Journal    
DOI: 10.1093/ndt/gft435     Document Type: Review

References (62)

1. DeFronzo RA, Alvestrand A, Smith D et al. Insulin resistance in uremia. J. Clin. Invest. 1981; 67: 563-568
2. Chen J, Muntner P, Hamm LL, Fonseca V, Batuman V, Whelton PK et al. Insulin resistance and risk of chronic kidney disease in nondiabetic US adults. J. Am. Soc. Nephrol. 2003; 14: 469-477
3. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 1993; 259: 87-91
4. Turnbaugh PJ, Ley RE, Mahowald MA et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006; 444: 1027-1031
5. Bammens B, Evenepoel P, Verbeke K et al. Impairment of small intestinal protein assimilation in patients with end-stage renal disease: extending the malnutrition-inflammation-atherosclerosis concept. Am. J. Clin. Nutr. 2004; 80: 1536-1543
6. Vaziri ND, Wong J, Pahl M et al. Chronic kidney disease alters intestinal microbial flora. Kidney Int. 2013; 83: 308-315
7. Aronov PA, Luo FJ-G, Plummer NS et al. Colonic contribution to uremic solutes. J. Am. Soc. Nephrol. 2011; 22: 1769-1776
8. D'Apolito M, Du X, Zong H et al. Urea-induced ROS generation causes insulin resistance in mice with chronic renal failure. J. Clin. Invest. 2010; 120: 203-213
9. 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
10. Zhao H-L, Sui Y, Guan J et al. Fat redistribution and adipocyte transformation in uninephrectomized rats. Kidney Int. 2008; 74: 467-477
11. Samuel VT, Shulman GI. Mechanisms for insulin resistance: common threads and missing links. Cell 2012; 148: 852-871
12. Fox TE, Houck KL, O'Neill SM et al. Ceramide recruits and activates protein kinase C zeta (PKC zeta) within structured membrane microdomains. J. Biol. Chem. 2007; 282: 12450-12457
13. Plomgaard P, Fischer CP, Ibfelt T et al. Tumor necrosis factor-alpha modulates human in vivo lipolysis. J. Clin. Endocrinol. Metab. 2008; 93: 543-549
14. Tuncman G, Hirosumi J, Solinas G et al. Functional in vivo interactions between JNK1 and JNK2 isoforms in obesity and insulin resistance. Proc. Natl. Acad. Sci. USA 2006; 103: 10741-10746
15. Rabkin R, Simon NM, Steiner S et al. Effect of renal disease on renal uptake and excretion of insulin in man. N. Engl. J. Med. 1970; 282: 182-187
16. DeFronzo RA, Ferrannini E, Sato Y et al. Synergistic interaction between exercise and insulin on peripheral glucose uptake. J. Clin. Invest. 1981; 68: 1468-1474
17. DeFronzo RA, Gunnarsson R, Björkman O et al. Effects of insulin on peripheral and splanchnic glucose metabolism in noninsulin-dependent (type II) diabetes mellitus. J. Clin. Invest. 1985; 76: 149-155
18. Friedman JE, Dohm GL, Elton CW et al. Muscle insulin resistance in uremic humans: glucose transport, glucose transporters, and insulin receptors. Am. J. Physiol. 1991; 261: E87-E94
19. Bak JF, Schmitz O, Sørensen SS et al. Activity of insulin receptor kinase and glycogen synthase in skeletal muscle from patients with chronic renal failure. Acta Endocrinol. 1989; 121: 744-750
20. Rubenfeld S, Garber AJ. Abnormal carbohydrate metabolism in chronic renal failure. The potential role of accelerated glucose production, increased gluconeogenesis, and impaired glucose disposal. J. Clin. Invest. 1978; 62: 20-28
21. Cecchin F, Ittoop O, Sinha MK et al. Insulin resistance in uremia: insulin receptor kinase activity in liver and muscle from chronic uremic rats. Am. J. Physiol. 1988; 254: E394-E401
22. Aksentijević D, Bhandari S, Seymour A-ML. Insulin resistance and altered glucose transporter 4 expression in experimental uremia. Kidney Int. 2009; 75: 711-718
23. Witasp A, Carrero JJ, Heimbürger O et al. Increased expression of pro-inflammatory genes in abdominal subcutaneous fat in advanced chronic kidney disease patients. J. Intern. Med. 2011; 269: 410-419
24. Bailey JL, Zheng B, Hu Z et al. Chronic kidney disease causes defects in signaling through the insulin receptor substrate/phosphatidylinositol 3-kinase/Akt pathway: implications for muscle atrophy. J. Am. Soc. Nephrol. 2006; 17: 1388-1394
25. Thomas SS, Dong Y, Zhang L et al. Signal regulatory protein-α interacts with the insulin receptor contributing to muscle wasting in chronic kidney disease. Kidney Int. 2013; 84: 308-316
26. McCaleb ML, Mevorach R, Freeman RB et al. Induction of insulin resistance in normal adipose tissue by uremic human serum. Kidney Int. 1984; 25: 416-421
27. McCaleb ML, Izzo MS, Lockwood DH. Characterization and partial purification of a factor from uremic human serum that induces insulin resistance. J. Clin. Invest. 1985; 75: 391-396
28. Franch HA, Raissi S, Wang X et al. Acidosis impairs insulin receptor substrate-1-associated phosphoinositide 3-kinase signaling in muscle cells: consequences on proteolysis. Am. J. Physiol. Renal. Physiol. 2004; 287: F700-F706
29. Kobayashi S, Maesato K, Moriya H et al. Insulin resistance in patients with chronic kidney disease. Am. J. Kidney Dis. 2005; 45: 275-280
30. Pittas AG, Dawson-Hughes B. Vitamin D and diabetes. J. Steroid Biochem. Mol. Biol. 2010; 121: 425-429
31. Mak RH. 1,25-Dihydroxyvitamin D3 corrects insulin and lipid abnormalities in uremia. Kidney Int. 1998; 53: 1353-1357
32. Chang E, Donkin SS, Teegarden D. Parathyroid hormone suppresses insulin signaling in adipocytes. Mol. Cell. Endocrinol. 2009; 307: 77-82
33. Moxley MA, Bell NH, Wagle SR et al. Parathyroid hormone stimulation of glucose and urea production in isolated liver cells. Am. J. Physiol. 1974; 227: 1058-1061
34. Mak RH, Turner C, Haycock GB et al. Secondary hyperparathyroidism and glucose intolerance in children with uremia. Kidney Int. Suppl. 1983; 16: S128-S133
35. Kraus LM, Traxinger R, Kraus AP. Uremia and insulin resistance: N-carbamoyl-asparagine decreases insulin-sensitive glucose uptake in rat adipocytes. Kidney Int. 2004; 65: 881-887
36. DeFronzo RA, Tobin JD, Rowe JW et al. Glucose intolerance in uremia. Quantification of pancreatic beta cell sensitivity to glucose and tissue sensitivity to insulin. J. Clin. Invest. 1978; 62: 425-435
37. Sydow K, Mondon CE, Schrader J et al. Dimethylarginine dimethyl-aminohydrolase overexpression enhances insulin sensitivity. Arterioscler. Thromb. Vasc. Biol. 2008; 28: 692-697
38. Dzúrik R, Spustová V, Lajdová I. Inhibition of glucose utilization in isolated rat soleus muscle by pseudouridine: implications for renal failure. Nephron. 1993; 65: 108-110
39. Johnson RJ, Perez-Pozo SE, Sautin YY et al. Hypothesis: could excessive fructose intake and uric acid cause type 2 diabetes? Endocrine Rev. 2009; 30: 96-116
40. Sánchez-Lozada LG, Tapia E, Bautista-García P et al. Effects of febuxostat on metabolic and renal alterations in rats with fructose-induced metabolic syndrome. Am. J. Physiol. Renal Physiol. 2008; 294: F710-F718
41. Anderstam B, Bragfors-Helin A-C, Axelsson J et al. Differences in acute metabolism of fructose between hemodialysis patients and healthy subjects. Scand. J. Clin. Lab. Invest. 2013; 73: 154-160
42. Rigalleau V, Blanchetier V, Combe C et al. A low-protein diet improves insulin sensitivity of endogenous glucose production in predialytic uremic patients. Am. J. Clin. Nutr. 1997; 65: 1512-1516
43. Okada K, Takahashi Y, Okawa E et al. Relationship between insulin resistance and uremic toxins in the gastrointestinal tract. Nephron. 2001; 88: 384-386
44. Vaziri ND, Yuan J, Rahimi A et al. Disintegration of colonic epithelial tight junction in uremia: a likely cause of CKD-associated inflammation. Nephrol. Dial. Transplant 2012; 27: 2686-2693
45. Caricilli AM, Picardi PK, de Abreu LL et al. Gut microbiota is a key modulator of insulin resistance in TLR 2 knockout mice. Vidal-Puig AJ, éditeur. PLoS Biol. 2011; 9: e1001212
46. Cani PD, Amar J, Iglesias MA et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007; 56: 1761-1772
47. Vaziri ND, Yuan J, Khazaeli M et al. Oral activated charcoal adsorbent (AST-120) ameliorates chronic kidney disease-induced intestinal epithelial barrier disruption. Am. J. Nephrol. 2013; 37: 518-525
48. McIntyre CW, Harrison LEA, Eldehni MT et al. Circulating endotoxemia: a novel factor in systemic inflammation and cardiovascular disease in chronic kidney disease. Clin. J. Am. Soc. Nephrol. 2011; 6: 133-141
49. Vaziri ND, Goshtasbi N, Yuan J et al. Uremic plasma impairs barrier function and depletes the tight junction protein constituents of intestinal epithelium. Am. J. Nephrol. 2012; 36: 438-443
50. Vaziri ND, Yuan J, Norris K. Role of urea in intestinal barrier dysfunction and disruption of epithelial tight junction in chronic kidney disease. Am. J. Nephrol. 2013; 37: 1-6
51. Banerjee D, Recio-Mayoral A, Chitalia N et al. Insulin resistance, inflammation, and vascular disease in nondiabetic predialysis chronic kidney disease patients. Clin. Cardiol. 2011; 34: 360-365
52. Gotoh H, Gohda T, Tanimoto M et al. Contribution of subcutaneous fat accumulation to insulin resistance and atherosclerosis in haemodialysis patients. Nephrol. Dial. Transplant. 2009; 24: 3474-3480
53. Kalbacher E, Koppe L, Zarrouki B et al. Human uremic plasma and not urea induces exuberant secretion of leptin in 3T3-L1 adipocytes. J. Ren. Nutr. 2011; 21: 72-75
54. Roubicek T, Bartlova M, Krajickova J et al. Increased production of proinflammatory cytokines in adipose tissue of patients with end-stage renal disease. Nutrition 2009; 25: 762-768
55. Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 2006; 440: 944-948
56. Xue P, Hou Y, Chen Y et al. Adipose deficiency of Nrf2 in ob/ob mice results in severe metabolic syndrome. Diabetes 2013; 62: 845-854
57. Ruiz S, Pergola PE, Zager RA et al. Targeting the transcription factor Nrf2 to ameliorate oxidative stress and inflammation in chronic kidney disease. Kidney Int. 2013; 83: 1029-1041
58. Axelsson J, Aström G, Sjölin E et al. Uraemic sera stimulate lipolysis in human adipocytes: role of perilipin. Nephrol. Dial. Transplant. 2011; 26: 2485-2491
59. Pelletier CC, Koppe L, Croze ML et al. White adipose tissue overproduces the lipid-mobilizing factor zinc α2-glycoprotein in chronic kidney disease. Kidney Int. 2013; 83: 878-886
60. Jin K, Norris K, Vaziri ND. Dysregulation of hepatic fatty acid metabolism in chronic kidney disease. Nephrol. Dial. Transplant. 2013; 28: 313-320
61. Barazzoni R, Zhu X, DeBoer M et al. Combined effects of ghrelin and higher food intake enhance skeletal muscle mitochondrial oxidative capacity and AKT phosphorylation in rats with chronic kidney disease. Kidney Int. 2010; 77: 23-28
62. Rao M, Li L, Demello C et al. Mitochondrial DNA injury and mortality in hemodialysis patients. J. Am. Soc. Nephrol. 2009; 20: 189-196