Adiponectin in chronic kidney disease has an opposite impact on protein-energy wasting and cardiovascular risk: Two sides of the same coin

Clinical Nephrology

Volumn 72, Issue 2, 2009, Pages 87-96

  Park, S H ^a,b   Carrero, J J ^a   Lindholm, B ^a   Stenvinkel, Peter ^a,c  

^a KAROLINSKA INSTITUTE   (Sweden)

^b Kyungpook National University Hospital   (South Korea)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Adiponectin; Chronic kidney disease; Inflammation; Protein energy wasting

Indexed keywords

ADIPONECTIN; ADIPONECTIN RECEPTOR 1; ADIPONECTIN RECEPTOR 2; C REACTIVE PROTEIN; INTERLEUKIN 10; INTERLEUKIN 6; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA;

ALBUMINURIA; CARDIOVASCULAR RISK; CHRONIC KIDNEY DISEASE; FATTY ACID OXIDATION; GENE EXPRESSION; GLOMERULUS FILTRATION RATE; GLUCOSE TRANSPORT; HUMAN; INFLAMMATION; METABOLIC DISORDER; MOLECULAR INTERACTION; MORTALITY; NONHUMAN; OBESITY; PROTEIN BLOOD LEVEL; PROTEIN CALORIE MALNUTRITION; REVIEW; UREMIA;

EID: 70350416632     PISSN: 03010430     EISSN: None     Source Type: Journal    
DOI: 10.5414/cnp72087     Document Type: Review

References (92)

1. Himmelfarb J, Stenvinkel P, Ikizler TA, Hakim RM. The elephant in uremia: oxidant stress as a unifying concept of cardiovascular disease in uremia. Kidney Int. 2002; 62: 1524-1538.
2. Carrero JJ, Stenvinkel P, Fellstrom B, Qureshi AR et al. Telomere attrition is associated with inflammation, low fetuin-A levels and high mortality in prevalent hemodialysis patients. J Intern Med. 2008; 263: 302-312.
3. Stenvinkel P, Carrero JJ, Axelsson J, Lindholm B et al. Emerging biomarkers for evaluating cardiovascular risk in the chronic kidney disease patient: how do new pieces fit into the uremic puzzle? Clin J Am Soc Nephrol. 2008; 3: 505-521.
4. Arita Y, Kihara S, Ouchi N, Takahashi M et al. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun. 1999; 257: 79-83.
5. Pajvani UB, Hawkins M, Combs TP, Rajala MW et al. Complex distribution, not absolute amount of adiponectin, correlates with thiazolidinedione-mediated improvement in insulin sensitivity. J Biol Chem. 2004; 279: 12152-12162.
6. Nishizawa H, Shimomura I, Kishida K, Maeda N et al. Androgens decrease plasma adiponectin, an insulin-sensitizing adipocyte-derived protein. Diabetes. 2002; 51: 2734-2741.
7. Pischon T, Girman CJ, Rifai N, Hotamisligil GS et al. Association between dietary factors and plasma adiponectin concentrations in men. Am J Clin Nutr. 2005; 81: 780-786.
8. Tsukinoki R, Morimoto K, Nakayama K. Association between lifestyle factors and plasma adiponectin levels in Japanese men. Lipids Health Dis. 2005; 4: 27.
9. Zoccali C, Mallamaci F, Tripepi G, Benedetto FA et al. Adiponectin, metabolic risk factors, and cardiovascular events among patients with end-stage renal disease. J Am Soc Nephrol. 2002; 13: 134-141.
10. Becker B, Kronenberg F, Kielstein JT, Haller H 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.
11. Iwashima Y, Horio T, Kumada M, Suzuki Y et al. Adiponectin and renal function, and implication as a risk of cardiovascular disease. Am J Cardiol. 2006; 98: 1603-1608.
12. Ignacy W, Chudek J, Adamczak M, Funahashi T et al. Reciprocal association of plasma adiponectin and serum C-reactive protein concentration in haemodialysis patients with end-stage kidney disease - a follow-up study. Nephron. 2005; 101: c18-24.
13. Nishimura M, Hashimoto T, Kobayashi H, Yamazaki S et al. Association of the circulating adiponectin concentration with coronary in-stent restenosis in hemodialysis patients. Nephrol Dial Transplant. 2006; 21: 1640-1647.
14. Cavusoglu E, Ruwende C, Chopra V, Yanamadala S et al. Adiponectin is an independent predictor of all-cause mortality, cardiac mortality, and myocardial infarction in patients presenting with chest pain. Eu Heart J. 2006; 27: 2300-2309.
15. Kistorp C, Faber J, Galatius S, Gustafsson F et al. Plasma adiponectin, body mass index, and mortality in patients with chronic heart failure. Circulation. 2005; 112: 1756-1762.
16. Pilz S, Mangge H, Wellnitz B, Seelhorst U et al. Adiponectin and mortality in patients undergoing coronary angiography. J Clin Endocrinol Metab. 2006; 91: 4277-4286.
17. Menon V, Li L, Wang X, Greene T et al. Adiponectin and mortality in patients with chronic kidney disease. J Am Soc Nephrol. 2006; 17: 2599-2606.
18. Ohashi N, Kato A, Misaki T, Sakakima M et al. Association of serum adiponectin levels with all-cause mortality in hemodialysis patients. Intern Med (Tokyo, Japan). 2008; 47: 485-491.
19. Matsumoto M, Ishikawa S, Kajii E. Adiponectin and non cardiovascular death: a nested case-control study. Metabolism. 2008; 57: 811-818.
20. Weyer C, Funahashi T, Tanaka S, Hotta K et al. Hypoadiponectinemia in obesity and Type 2 diabetes: close association with insulin resistance and hyperinsulinemia. J Clin Endocrinol Metab. 2001; 86: 1930-1935.
21. Kumada M, Kihara S, Sumitsuji S, Kawamoto T et al. Association of hypoadiponectinemia with coronary artery disease in men. Arterioscler Throm Vasc Biol. 2003; 23 85-89.
22. Kaser S, Moschen A, Cayon A, Kaser A et al. Adiponectin and its receptors in non-alcoholic steatohepatitis. Gut. 2005; 54: 117-121.
23. Barb D, Williams CJ, Neuwirth AK, Mantzoros CS. Adiponectin in relation to malignancies: a review of existing basic research and clinical evidence. Am J Clin Nutr. 2007; 86: s858-866.
24. Yilmaz MI, Saglam M, Qureshi AR, Carrero JJ et al. Endothelial dysfunction in type-2 diabetics with early diabetic nephropathy is associated with low circulating adiponectin. Nephrol Dial Transplant. 2008; 23: 1621-1627.
25. Stenvinkel P, Marchlewska A, Pecoits-Filho R, Heimburger O et al. Adiponectin in renal disease: relationship to phenotype and genetic variation in the gene encoding adiponectin. Kidney Int. 2004; 65: 274-281.
26. Chudek J, Adamczak M, Karkoszka H, Budzinski G et al. Plasma adiponectin concentration before and after successful kidney transplantation. Transplant Proc. 2003; 35: 2186-2189.
27. Yang WS, Lee WJ, Funahashi T, Tanaka S et al. Weight reduction increases plasma levels of an adipose-derived anti-inflammatory protein, adiponectin. J Clin Endocrinol Metab. 2001; 86: 3815-3819.
28. Fouque D, Kalantar-Zadeh K, Kopple J, Cano N et al. Aproposed nomenclature and diagnostic criteria for protein-energywasting in acute and chronic kidney disease. Kidney Int. 2008; 73: 391-398.
29. Marchlewska A, Stenvinkel P, Lindholm B,Danielsson A et al. Reduced gene expression of adiponectin in fat tissue from patients with end-stage renal disease. Kidney Int. 2004; 66: 46-50.
30. Bauche IB, Ait El Mkadem S, Rezsohazy R, Funahashi T et al. Adiponectin down regulates its own production and the expression of its AdipoR2 receptor in transgenic mice. Biochem Biophys Res Commun. 2006; 345: 1414-1424.
31. Bruun JM, Lihn AS, Verdich C, Pedersen SB et al. Regulation of adiponectin by adipose tissue-derived cytokines: in vivo and in vitro investigations in humans. AmJ Physiol. 2003; 285: E527-533.
32. Ebinc H, Ozkurt ZN, Ebinc FA, Ucardag D et al. Effects of sympatholytic therapy with moxonidine on serum adiponectin levels in hypertensive women. J Int Med Res. 2008; 36: 80-87.
33. Richards AA, Stephens T, Charlton HK, Jones A et al. Adiponectin multimerization is dependent on conserved lysines in the collagenous domain: evidence for regulation of multimerization by alterations in posttranslational modifications. Mol Endocrinol. (Baltimore, Md). 2006; 20: 1673-1687.
34. Tsao TS, Tomas E, Murrey HE, Hug C et al. Role of disulfide bonds in Acrp30/adiponectin structure and signaling specificity. Different oligomers activate different signal transduction pathways. J Biol Chem. 2003; 278: 50810-50817.
35. Shen YY, Charlesworth JA, Kelly JJ, Loi KW et al. Up-regulation of adiponectin, its isoforms and receptors in end-stage kidney disease. Nephrol Dial Transplant. 2007; 22: 171-178.
36. Hada Y, Yamauchi T, Waki H, Tsuchida A et al. Selective purification and characterization of adiponectin multimer species from human plasma. Biochem Biophys Res Commun. 2007; 356: 487-493.
37. Yamauchi T, Kamon J, Ito Y, Tsuchida A et al. Cloning of adiponectin receptors thatmediate antidiabetic metabolic effects. Nature. 2003; 423: 762-769.
38. Kadowaki T, Yamauchi T. Adiponectin and adiponectin receptors. Endocr Rev. 2005; 26: 439-451.
39. Hug C, Wang J, Ahmad NS, Bogan JS et al. T-cadherin is a receptor for hexameric and high-molecular-weight forms of Acrp30/adiponectin. Proc Natl Acad Sci USA. 2004; 101: 10308-10313.
40. Tan GD, Debard C, Funahashi T, Humphreys SM et al. Changes in adiponectin receptor expression in muscle and adipose tissue of type 2 diabetic patients during rosiglitazone therapy. Diabetologia. 2005; 48: 1585-1589.
41. Mullen KL, Smith AC, Junkin KA, Dyck DJ. Globular adiponectin resistance develops independently of impaired insulin-stimulated glucose transport in soleus muscle from high-fat-fed rats. Am J Physiol. 2007; 293: E83-90.
42. Shen YY, Charlesworth JA, Kelly JJ, Peake PW. The effect of renal transplantation on adiponectin and its isoforms and receptors. Metabolism. 2007; 56: 1201-1208.
43. Ouchi N, Kihara S, Funahashi T, Nakamura T et al. Reciprocal association of C-reactive protein with adiponectin in blood stream and adipose tissue. Circulation. 2003; 107: 671-674.
44. Huang JW, Yen CJ, Chiang HW, Hung KY et al. Adiponectin in peritoneal dialysis patients: a comparison with hemodialysis patients and subjects with normal renal function. Am J Kidney Dis. 2004; 43: 1047-1055.
45. Kern PA, Di Gregorio GB, Lu T, Rassouli N et al. Adiponectin expression from human adipose tissue: relation to obesity, insulin resistance, and tumor necrosis factor-alpha expression. Diabetes. 2003; 52: 1779-1785.
46. Ouchi N, Kihara S, Arita Y, Maeda K et al. Novel modulator for endothelial adhesion molecules: adipocyte-derived plasma protein adiponectin. Circulation. 1999; 100: 2473-2476.
47. Ouchi N, Kihara S, Arita Y, Okamoto Y et al. Adiponectin, an adipocyte-derived plasma protein, inhibits endothelial NF-κB signaling through a cAMP-dependent pathway. Circulation. 2000; 102: 1296-1301.
48. Wolf AM, Wolf D, Rumpold H, Enrich B et al. Adiponectin induces the anti-inflammatory cytokines IL-10 and IL-1RA in human leukocytes. Biochem Biophys Res Commun. 2004; 323: 630-635.
49. Takemura Y, Ouchi N, Shibata R, Aprahamian T et al. Adiponectin modulates inflammatory reactions via calreticulin receptor-dependent clearance of early apoptotic bodies. J Clin Invest. 2007; 117: 375-386.
50. Maeda N, Shimomura I, Kishida K, Nishizawa H et al. Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat Med. 2002; 8: 731-737.
51. Ohashi K, Iwatani H, Kihara S, Nakagawa Y et al. Exacerbation of albuminuria and renal fibrosis in subtotal renal ablation model of adiponectin-knockout mice. Arterioscler Thromb Vasc Biol. 2007; 27: 1910-1917.
52. Lihn AS, Richelsen B, Pedersen SB, Haugaard SB et al. Increased expression of TNF-alpha, IL-6, and IL-8 in HALS: implications for reduced adiponectin expression and plasma levels. Am J Physiol. 2003; 285: E1072-1080.
53. Ouchi N, Kihara S, Arita Y, Nishida M et al. Adipocyte-derived plasma protein, adiponectin, suppresses lipid accumulation and class A scavenger receptor expression in human monocyte-derived macrophages. Circulation. 2001; 103: 1057-1063.
54. Chen H, Montagnani M, Funahashi T, Shimomura I et al. Adiponectin stimulates production of nitric oxide in vascular endothelial cells. J Biol Chem. 2003; 278: 45021-45026.
55. Kobayashi H, Ouchi N, Kihara S, Walsh K et al. Selective suppression of endothelial cell apoptosis by the high molecular weight form of adiponectin. Circ Res. 2004; 94: e27-31.
56. Arita Y, Kihara S, Ouchi N, Maeda K et al. Adipocyte-derived plasma protein adiponectin acts as a platelet-derived growth factor-BB-binding protein and regulates growth factor-induced common postreceptor signal in vascular smooth muscle cell. Circulation. 2002; 105: 2893-2898.
57. Kumada M, Kihara S, Ouchi N, Kobayashi H et al. Adiponectin specifically increased tissue inhibitor of metalloproteinase-1 through interleukin-10 expression in human macrophages. Circulation. 2004; 109: 2046-2049.
58. Okamoto Y, Kihara S, Ouchi N, Nishida M et al. Adiponectin reduces atherosclerosis in apolipoprotein E-deficient mice. Circulation. 2002; 106: 2767-2770.
59. Combs TP, Berg AH, Obici S, Scherer PE et al. Endogenous glucose production is inhibited by the adipose-derived protein Acrp30. J Clin Invest. 2001; 108: 1875-1881.
60. Ravussin E. Adiponectin enhances insulin action by decreasing ectopic fat deposition. Pharmacogenomics J. 2002; 2: 4-7.
61. Cnop M, Havel PJ, Utzschneider KM, Carr DB et al. Relationship of adiponectin to body fat distribution, insulin sensitivity and plasma lipoproteins: evidence for independent roles of age and sex. Diabetologia. 2003; 46: 459-469.
62. Sharma K, Ramachandrarao S, Qiu G, Usui HK et al. Adiponectin regulates albuminuria and podocyte function in mice. J Clin Invest. 2008; 118: 1645-1656.
63. Jorsal A, Tarnow L, Frystyk J, Lajer M et al. Serum adiponectin predicts all-cause mortality and end stage renal disease in patients with type I diabetes and diabetic nephropathy. Kidney Int. 2008; 74: 649-654.
64. Kollerits B, Fliser D, Heid IM, Ritz E et al. Gender-specific association of adiponectin as a predictor of progression of chronic kidney disease: the Mild to Moderate Kidney Disease Study. Kidney Int. 2007; 71: 1279-1286.
65. Saraheimo M, Forsblom C, Thorn L, Waden J et al. Serum adiponectin and progression of diabetic nephropathy in patients with type 1 diabetes. Diabetes care. 2008; 31: 1165-1169.
66. Leth H, Andersen KK, Frystyk J, Tarnow L et al. Elevated levels of high-molecular-weight adiponectin in type 1 diabetes. J Clin Endocrinol Metab. 2008; 93: 3186-3191.
67. Carrero JJ, Qureshi AR, Axelsson J, Avesani CM et al. Comparison of nutritional and inflammatory markers in dialysis patients with reduced appetite. Am J Clin Nutr 2007; 85: 695-701.
68. Carrero JJ. Identification of patients with eating disorders: clinical and biochemical signs of appetite loss in dialysis patients. J Ren Nutr. 2009; 19: 10-15.
69. Qi Y, Takahashi N, Hileman SM, Patel HR et al. Adiponectin acts in the brain to decrease body weight. Nat Med. 2004; 10: 524-529.
70. Yamauchi T, Kamon J, Waki H, Terauchi Y et al. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat Med. 2001; 7: 941-946.
71. Fruebis J, Tsao TS, Javorschi S, Ebbets-Reed D et al. Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation inmuscle and causesweight loss inmice. Proc Natl Acad Sci USA. 2001; 98: 2005-2010.
72. Castaneda-Sceppa C, Sarnak MJ, Wang X, Greene T et al. Role of adipose tissue in determining muscle mass in patients with chronic kidney disease. J Ren Nutr. 2007; 17: 314-322.
73. Carrero JJ, Chmielewski M, Axelsson J, Snaedal S et al. Muscle atrophy, inflammation and clinical outcome in incident and prevalent dialysis patients. Clin Nutr. 2008; 27: 557-564.
74. Liu YM, Lacorte JM, Viguerie N, Poitou C et al. Adiponectin gene expression in subcutaneous adipose tissue of obese women in response to shortterm very low calorie diet and refeeding. J Clin Endocrinol Metab. 2003; 88: 5881-5886.
75. Duda MK, O'Shea KM, Lei B, Barrows BR et al. Dietary supplementation with omega-3 PUFA increases adiponectin and attenuates ventricular remodeling and dysfunction with pressure overload. Cardiovasc Res. 2007; 76: 303-310.
76. Krebs JD, Browning LM, McLean NK, Rothwell JL et al. Additive benefits of long-chain n-3 polyunsaturated fatty acids and weight-loss in the management of cardiovascular disease risk in overweight hyperinsulinemic women. Int J Obes. (2005) 2006; 30: 1535-1544.
77. Shimada K, Kawarabayashi T, Tanaka A, Fukuda D et al. Oolong tea increases plasma adiponectin levels and low-density lipoprotein particle size in patients with coronary artery disease. Diabetes Res Clin Pract. 2004; 65: 227-234.
78. Hsu CH, Tsai TH, Kao YH, Hwang KC et al. Effect of green tea extract on obese women: a randomized, double-blind, placebo-controlled clinical trial. Clin Nutr (Edinburgh, Scotland). 2008; 27: 363-370.
79. Koh KK, Han SH, Quon MJ, Yeal Ahn J et al. Beneficial effects of fenofibrate to improve endothelial dysfunction and raise adiponectin levels in patients with primary hypertriglyceridemia. Diabetes care. 2005; 28: 1419-1424.
80. Choi KC, Ryu OH, Lee KW, Kim HY et al. Effect of PPAR-alpha and -gamma agonist on the expression of visfatin, adiponectin, and TNF-alpha in visceral fat of OLETF rats. Biochem Biophys Res Commun. 2005; 336: 747-753.
81. Tsuchida A, Yamauchi T, Takekawa S, Hada Y et al. Peroxisome proliferator-activated receptor (PPAR)alpha activation increases adiponectin receptors and reduces obesity-related inflammation in adipose tissue: comparison of activation of PPARalpha, PPARgamma, and their combination. Diabetes. 2005; 54: 3358-3370.
82. Furuhashi M, Ura N, Higashiura K, Murakami H et al. Blockade of the renin-angiotensin system increases adiponectin concentrations in patients with essential hypertension. Hypertension. 2003; 42: 76-81.
83. Nowak L, Adamczak M, Wiecek A. Blockade of sympathetic nervous system activity by rilmenidine increases plasma adiponectin concentration in patients with essential hypertension. Am J Hypertens. 2005; 18: 1470-1475.
84. Poyhonen-Alho MK, Manhem K, Katzman P, Kibarskis A et al. Central sympatholytic therapy has anti-inflammatory properties in hypertensive postmenopausal women. J Hypertens. 2008; 26: 2445-2449.
85. Nagasaka S, Taniguchi A, Aiso Y, Yatagai T et al. Effect of glimepiride on serum adiponectin level in subjects with type 2 diabetes. Diabetes care. 2003; 26: 2215-2216.
86. Despres JP, Golay A, Sjostrom L. Effects of rimonabant on metabolic risk factors in overweight patients with dyslipidemia. Engl J Med. 2005; 353: 2121-2134.
87. Celik T, Iyisoy A, Kursaklioglu H, Kardesoglu E et al. Comparative effects of nebivolol and metoprolol on oxidative stress, insulin resistance, plasma adiponectin and soluble P-selectin levels in hypertensive patients. J Hypertens. 2006; 24: 591-596.
88. Narasimhan ML, Coca MA, Jin J, Yamauchi T et al. Osmotin is a homolog of mammalian adiponectin and controls apoptosis in yeast through a homolog of mammalian adiponectin receptor. Mol Cell. 2005; 17: 171-180.
89. Barazzoni R, Stulle M, Panzetta G, Vasille A, Biolo G, Zanetti M, Guarnieri G.. Plasma high- but not low-molecular weight adiponectin is positively associated with resting energy expenditure in male non-diabetic hemodialysis patients. J Ren Nutr. 2008; 18: S1-S36.
90. Carrero JJ, Brodin L, Lindholm B, Stenvinkel P. Adiponectin in chronic kidney disease: Dr Jekyll and Mr Hyde. Kidney Int. 2009; 75: 120-121.
91. Adamczak M, Szotowska M, Chudek J, Karkosza H, Cierpka L, Wiecek A. Plasma adiponectin concentration in patients after successful kidney transplantation - a single center, observational study. Clin Nephrol. 2007; 67: 381-390.
92. Yilmaz MI, Saglam M, Carrero JJ, Qureshi AR, CAglar K, Eyileten T, Sonmez A, Oguz Y, Aslan I Vural A, Yenicesu M, Stenvinkel P, Lindholm B, Axelsson J. Normalization of endothelial dysfunction following renal transplantation is accompanied by a reduction of circulating visfatin/ NAMPT. A novel marker of endothelial damage? Clin Transplant. 2009; 23: 241-248.