Biomarkers of Adiponectin: Plasma Protein Variation and Genomic DNA Polymorphisms

Biomarker Insights

Volumn 4, Issue , 2009, Pages

  Gu, Harvest F ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

adiponectin; biomarker; genetic polymorphism; protein variation

Indexed keywords

EID: 77955488122     PISSN: None     EISSN: 11772719     Source Type: Journal    
DOI: 10.4137/BMI.S3453     Document Type: Review

References (99)

1. Kershaw E.E., Flier J.S. Adipose tissue as an endocrine organ. J Clin Endocrinol Metab. 2004; 89(6): 2548–56.
2. http://www.ncbi.nlm.nih.gov/entrez/dispomim.cgi?id=164160
3. http://www.ncbi.nlm.nih.gov/entrez/dispomim.cgi?id=134350
4. http://www.ncbi.nlm.nih.gov/entrez/dispomim.cgi?id=191160
5. http://www.ncbi.nlm.nih.gov/entrez/dispomim.cgi?id=605441
6. Zhang Y., Proenca R., Maffei M., Barone M., Leopold L., Friedman J.M. Positional cloning of the mouse obese gene and its human homologue. Nature. 1994; 1; 372(6505): 425–32.
7. Scherer P.E., Williams S., Fogliano M., Baldini G., Lodish H.F. A novel serum protein similar to C1q, produced exclusively in adipocytes. J Biol Chem. 1995; 270: 26746–9.
8. Maeda K., Okubo K., Shimomura I., Funahashi T., Matsuzawa Y., Matsubara K. cDNA cloning and expression of a novel adipose collagen-like factor, apM1. Biochem Biophys Res Commun. 1996; 221: 286–9.
9. Hu E., Liang P., Spiegelman B.M. AdipoQ is a novel adipose-specific gene dysregulated in obesity. J Biol Chem. 1996; 271: 10697–703.
10. Nakano Y., Tobe T., Choi-Miura N.H., Mazda T., Tomita M. Isolation and characterization of GBP28, a novel gelatin-binding protein purified from human plasma. J Biochem. 1996; 120: 803–12.
11. Saito K., Tobe T., Minoshima S. et al. Organization of the gene for gelatin-binding protein (GBP28). Gene. 1999; 229: 67–73.
12. Schaffler A., Orso E., Palitzsch K.D. et al. The human apM-1, an adipocyte-specific gene linked to the family of TNF's and to genes expressed in activated T cells, is mapped to chromosome 1q21.3-q23, a susceptibility locus identified for familial combined hyperlipidaemia (FCH). Biochem Biophys Res Commun. 1999; 260: 416–25.
13. Das K., Lin Y., Widen E., Zhang Y., Scherer P.E. Chromosomal localization, expression pattern, and promoter analysis of the mouse gene encoding adipocyte-specific secretory protein Acrp30. Biochem Biophys Res Commun. 2001; 280: 1120–9.
14. Tsao T.S., Murrey H.E., Hug C., Lee D.H., Lodish H.F. Oligomerization state-dependent activation of NF-κB signaling pathway by adipocyte complement-related protein of 30 kDa(Acrp30). J Biol Chem. 2002; 277: 29359–62.
15. Wang Y., Xu A., Knight C., Xu L.Y., Cooper G.J. Hydroxylation and glycosylation of the four conserved lysine residues in the collagenous domain of adiponectin. Potential role in the modulation of its insulin-sensitizing activity. J Biol Chem. 2002; 277: 19521–9.
16. Tsao T.S., Tomas E., Murrey H.E. 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: 50810–7.
17. Pajvani U.B., Du X., Combs T.P. et al. Structure-function studies of the adipocyte-secreted hormone Acrp30/adiponectin. Implications for metabolic regulation and bioactivity. J Biol Chem. 2003; 278: 9073–85.
18. Wong G.W., Wang J., Hug C., Tsao T.S., Lodish H.F. A family of Acrp30/adiponectin structural and functional paralogs. Proc Natl Acad Sci USA. 2004; 101: 10302–7.
19. Waki H., Yamauchi T., Kamon J. et al. Generation of globular fragment of adiponectin by leukocyte elastase secreted by monocytic cell line THP-1. Endocrinology. 2005; 146: 790–6.
20. Sato C., Yasukawa Z., Honda N., Matsuda T., Kitajima K. Identification and adipocyte differentiation-dependent expression of the unique disialic acid residue in an adipose tissue-specific glycoprotein, adipo Q. J Biol Chem. 2001; 3; 276(31): 28849–56.
21. Wang Y., Lam K.S., Chan L. et al. Post-translational modifications of the four conserved lysine residues within the collagenous domain of adiponectin are required for the formation of its high molecular weight oligomeric complex. J Biol Chem. 2006; 16; 281(24): 16391–400.
22. Waki H., Yamauchi T., Kamon J. et al. Impaired multimerization of human adiponectin mutants associated with diabetes. Molecular structure and multimer formation of adiponectin. J Biol Chem. 2003; 278(41): 40352–63.
23. Ouchi N., Kihara S., Arita Y. et al. Novel modulator for endothelial adhesion molecules: adipocyte-derived plasma protein adiponectin. Circulation. 1999; 100(25): 2473–6.
24. Das K., Lin Y., Widen E., Zhang Y., Scherer P.E. Chromosomal localization, expression pattern, and promoter analysis of the mouse gene encoding adipocyte-specific secretory protein Acrp30. Biochem Biophys Res Commun. 2001; 2; 280(4): 1120–9.
25. Yu S., Matsusue K., Kashireddy P. et al. Adipocyte-specific gene expression and adipogenic steatosis in the mouse liver due to peroxisome proliferator-activated receptor gamma1 (PPARgamma1) overexpression. J Biol Chem. 2003; 278(1): 498–505.
26. Kubota N., Terauchi Y., Miki H. et al. PPAR gamma mediates high-fat diet-induced adipocyte hypertrophy and insulin resistance. Mol Cell. 1999; 4(4): 597–609.
27. Yamauchi T., Kamon J., Waki H. et al. The mechanisms by which both heterozygous peroxisome proliferator-activated receptor gamma (PPARgamma) deficiency and PPARgamma agonist improve insulin resistance. J Biol Chem. 2001; 276(44): 41245–54.
28. Sivan E., Mazaki-Tovi S., Pariente C. et al. Adiponectin in human cord blood: relation to fetal birth weight and gender. J Clin Endocrinol Metab. 2003; 88(12): 5656–60.
29. Kamoda T., Saitoh H., Saito M., Sugiura M., Matsui A. Serum adiponectin concentrations in newborn infants in early postnatal life. Pediatr Res. 2004; 56(5): 690–3.
30. Tsai P.J., Yu C.H., Hsu S.P. et al. Cord plasma concentrations of adiponectin and leptin in healthy term neonates: positive correlation with birthweight and neonatal adiposity. Clin Endocrinol (Oxf). 2004; 61(1): 88–93.
31. Kotani Y., Yokota I., Kitamura S., Matsuda J., Naito E., Kuroda Y. Plasma adiponectin levels in newborns are higher than those in adults and positively correlated with birth weight. Clin Endocrinol (Oxf). 2004; 61(4): 418–23.
32. Tsou P.L., Jiang Y.D., Chang C.C. et al. Sex-related differences between adiponectin and insulin resistance in schoolchildren. Diabetes Care. 2004; 27(2): 308–13.
33. Nishimura R., Sano H., Matsudaira T. et al. Changes in body mass index, leptin and adiponectin in Japanese children during a three-year follow-up period: a population-based cohort study. Cardiovasc Diabetol. 2009; 8: 30.
34. Woo J.G., Dolan L.M., Daniels S.R., Goodman E., Martin L.J. Adolescent sex differences in adiponectin are conditional on pubertal development and adiposity. Obes Res. 2005; 13(12): 2095–101.
35. Kern P.A., Di Gregorio G.B., Lu T., Rassouli N., Ranganathan G. Adiponectin expression from human adipose tissue: relation to obesity, insulin resistance, and tumor necrosis factor-alpha expression. Diabetes. 2003; 52(7): 1779–85.
36. Mannucci E., Ognibene A., Cremasco F. et al. Plasma adiponectin and hyperglycaemia in diabetic patients. Clin Chem Lab Med. 2003; 41(9): 1131–5.
37. Silha J.V., Krsek M., Skrha J., Sucharda P., Nyomba B.L., Murphy L.J. Plasma resistin, leptin and adiponectin levels in non-diabetic and diabetic obese subjects. Diabet Med. 2004; 21(5): 497–9.
38. Schulze M.B., Rimm E.B., Shai I., Rifai N., Hu F.B. Relationship between adiponectin and glycemic control, blood lipids, and inflammatory markers in men with type 2 diabetes. Diabetes Care. 2004; 27(7): 1680–7.
39. Shetty G.K., Economides P.A., Horton E.S., Mantzoros C.S., Veves A. Circulating adiponectin and resistin levels in relation to metabolic factors, inflammatory markers, and vascular reactivity in diabetic patients and subjects at risk for diabetes. Diabetes Care. 2004; 27(10): 2450–7.
40. Mojiminiyi O.A., Abdella N.A., Al Arouj M., Ben Nakhi A. Adiponectin, insulin resistance and clinical expression of the metabolic syndrome in patients with Type 2 diabetes. Int J Obes (Lond). 2007; 31(2): 213–20.
41. Aguilar-Salinas C.A., Garcia E.G., Robles L. et al. High adiponectin concentrations are associated with the metabolically healthy obese phenotype. J Clin Endocrinol Metab. 2008; 93(10): 4075–9.
42. Lindsay R.S., Funahashi T., Krakoff J. et al. Genome-wide linkage analysis of serum adiponectin in the Pima Indian population. Diabetes. 2003; 52(9): 2419–25.
43. Costacou T., Bosnyak Z., Harger G.F., Markovic N., Silvers N., Orchard T.J. Postpartum adiponectin concentration, insulin resistance and metabolic abnormalities among women with pregnancy-induced disturbances. Prev Cardiol. 2008; 11(2): 106–15.
44. Heitritter S.M., Solomon C.G., Mitchell G.F., Skali-Ounis N., Seely E.W. Sub-clinical inflammation and vascular dysfunction in women with previous gestational diabetes mellitus. J Clin Endocrinol Metab. 2005; 90(7): 3983–8.
45. Retnakaran R., Hanley A.J., Raif N. et al. Adiponectin and beta cell dysfunction in gestational diabetes: pathophysiological implications. Diabetologia. 2005; 48(5): 993–1001.
46. Osei K., Gaillard T., Schuster D. Plasma adiponectin levels in high risk African-Americans with normal glucose tolerance, impaired glucose tolerance, and type 2 diabetes. Obes Res. 2005; 13(1): 179–85.
47. Furuhashi M., Ura N., Moniwa N. et al. Possible impairment of transcardiac utilization of adiponectin in patients with type 2 diabetes. Diabetes Care. 2004; 27(9): 2217–21.
48. Takano H., Kodama Y., Kitta Y. et al. Transcardiac adiponectin gradient is independently related to endothelial vasomotor function in large and resistance coronary arteries in humans. Am J Physiol Heart Circ Physiol. 2006; 291(6): H2641–6.
49. Perseghin G., Lattuada G., Danna M. et al. Insulin resistance, intramyocellular lipid content, and plasma adiponectin in patients with type 1 diabetes. Am J Physiol Endocrinol Metab. 2003; 285(6): E1174–81.
50. Morales A., Wasserfall C., Brusko T. et al. Adiponectin and leptin concentrations may aid in discriminating disease forms in children and adolescents with type 1 and type 2 diabetes. Diabetes Care. 2004; 27(8): 2010–4.
51. Schäffler A., Herfarth H., Paul G. et al. Identification of influencing variables on adiponectin serum levels in diabetes mellitus type 1 and type 2. Exp Clin Endocrinol Diabetes. 2004; 112(7): 383–9.
52. Imagawa A., Funahashi T., Nakamura T. et al. Elevated serum concentration of adipose-derived factor, adiponectin, in patients with type 1 diabetes. Diabetes Care. 2002; 25(9): 1665–6.
53. Lindstrom T., Frystyk J., Hedman C.A., Flyvbjerg A., Arnqvist H.J. Elevated circulating adiponectin in type 1 diabetes is associated with long diabetes duration. Clin Endocrinol (Oxf). 2006; 65(6): 776–82.
54. Saraheimo M., Forsblom C., Fagerudd J. et al. FinnDiane study group. Serum adiponectin is increased in type 1 diabetic patients with nephropathy. Diabetes Care. 2005 Jun; 28(6): 1410–4.
55. Frystyk J., Tarnow L., Hansen T.K., Parving H.H., Flyvbjerg A. Increased serum adiponectin levels in type 1 diabetic patients with microvascular complications. Diabetologia. 2005; 48(9): 1911–8.
56. Ljubic S., Boras J., Jazbec A. et al. Adiponectin has different mechanisms in type 1 and type 2 diabetes with C-peptide link. Clin Invest Med. 2009; 1; 32(4): E271–9.
57. Goldberg R.B. Cytokine and Cytokine-like Inflammation Markers, Endothelial Dysfunction and Imbalanced Coagulation in Development of Diabetes and Its Complications. J Clin Endocrinol Metab. 2009 Jun 9. [Epub ahead of print].
58. Nayak S., Soon S.Q., Kunjal R. et al. Relationship between adiponectin, inflammatory markers and obesity in type 2 diabetic and non-diabetic Trinidadians. Arch Physiol Biochem. 2009; 115(1): 28–33.
59. Waki H., Yamauchi T., Kamon J. et al. Impaired multimerization of human adiponectin mutants associated with diabetes: Molecular structure and multimer formation of adiponectin. J Biol Chem. 2003; 278: 40352–63.
60. Pajvani U.B., Du X., Combs T.P. et al. Structure-function studies of the adipocyte-secreted hormone Acrp30/adiponectin. Implications for metabolic regulation and bioactivity. J Biol Chem. 2003; 278: 9073–85.
61. Iwase M., Iino K., Oku M. et al. Serum high-molecular weight adiponectin is related to early postprandial glycemic increases and gastric emptying in patients with type 2 diabetes mellitus. Diabetes Metab Res Rev. 2009; 25(4): 344–50.
62. Blüher M., Brennan A.M., Kelesidis T. et al. Total and high-molecular weight adiponectin in relation to metabolic variables at baseline and in response to an exercise treatment program: comparative evaluation of three assays. Diabetes Care. 2007; 30(2): 280–5.
63. Vionnet N., Hani ElH, Dupont S. et al. Genomewide search for T2D-susceptibility genes in French whites: evidence for a novel susceptibility locus for early-onset diabetes on chromosome 3q27-qter and independent replication of a type 2-diabetes locus on chromosome 1q21–q24. Am J Hum Genet. 2000; 67: 1470–80.
64. Francke S., Manraj M., Lacquemant C. et al. A genome-wide scan for coronary heart disease suggests in Indo-Mauritians a susceptibility locus on chromosome 16p13 and replicates linkage with the metabolic syndrome on 3q27. Hum Mol Genet. 2001; 10: 2751–65.
65. Francke S., Manraj M., Lacquemant C. et al. A genome-wide scan for coronary heart disease suggests in Indo-Mauritians a susceptibility locus on chromosome 16p13 and replicates linkage with the metabolic syndrome on 3q27. Hum Mol Genet. 2001; 10: 2751–65.
66. Chiodini B.D., Lewis C.M. Meta-analysis of 4 coronary heart disease genome-wide linkage studies confirms a susceptibility locus on chromosome 3q. Arterioscler Thromb Vasc Biol. 2003; 23: 1863–8.
67. DeWan A.T., Arnett D.K., Atwood L.D. et al. A genome scan for renal function among hypertensives: the HyperGEN study. Am J Hum Genet. 2001; 68: 136–44.
68. Moczulski D.K., Rogus J.J., Antonellis A., Warram J.H., Krolewski A.S. Major susceptibility locus for nephropathy in type 1 diabetes on chromosome 3q: results of novel discordant sib-pair analysis. Diabetes. 1998; 47(7): 1164–9.
69. Bowden D.W., Colicigno C.J., Langefeld C.D. et al. A genome scan for diabetic nephropathy in African Americans. Kidney Int. 2004; 66(4): 1517–26.
70. Chung K.W., Ferrell R.E., Ellis D. et al. African American hypertensive nephropathy maps to a new locus on chromosome 9q31–q32. Am J Hum Genet. 2003; 73(2): 420–9.
71. Imperatore G., Hanson R.L., Pettitt D.J., Kobes S., Bennett P.H., Knowler W.C. ; The Pima Diabetes Genes Group: Sib-pair linkage analysis for susceptibility genes for microvascular complications among Pima Indians with type 2 diabetes. Diabetes. 1998; 47: 821–30.
72. http://www.hapmap.org/cgi-perl/gbrowse/hapmap27_B36/
73. Heid I.M., Wagner S.A., Gohlke H. et al. Genetic architecture of the APM1 gene and its influence on adiponectin plasma levels and parameters of the metabolic syndrome in 1,727 healthy Caucasians. Diabetes. 2006; 55(2): 375–84.
74. Hara K., Boutin P., Mori Y. et al. Genetic variation in the gene encoding adiponectin is associated with an increased risk of type 2 diabetes in the Japanese population. Diabetes. 2002; 51: 536–40.
75. Vasseur F., Helbecque N., Dina C. et al. Single-nucleotide polymorphism haplotypes in the both proximal promoter and exon 3 of the AdipoQ gene modulate adipocyte-secreted adiponectin hormone levels and contribute to the genetic risk for type 2 diabetes in French Caucasians. Hum Mol Genet. 2002; 11: 2607–14.
76. Ohashi K., Ouchi N., Kihara S. et al. Adiponectin I164T mutation is associated with the metabolic syndrome and coronary artery disease. J Am Coll Cardiol. 2004; 7; 43(7): 1195–200.
77. Zacharova J., Chiasson J.L., Laakso M. ; STOP-NIDDM Study Group. The common polymorphisms (single nucleotide polymorphism [SNP] +45 and SNP +276) of the adiponectin gene predict the conversion from impaired glucose tolerance to type 2 diabetes: the STOP-NIDDM trial. Diabetes. 2005; 54(3): 893–9.
78. Schwarz P.E., Govindarajalu S., Towers W. et al. Haplotypes in the promoter region of the AdipoQ gene are associated with increased diabetes risk in a German Caucasian population. Horm Metab Res. 2006; 38(7): 447–51.
79. Bacci S., Menzaghi C., Ercolino T. et al. The +276G/T single nucleotide polymorphism of the adiponectin gene is associated with coronary artery disease in type 2 diabetic patients. Diabetes Care. 2004; 27(8): 2015–20.
80. Lee Y.Y., Lee N.S., Cho Y.M. et al. Genetic association study of adiponectin polymorphisms with risk of Type 2 diabetes mellitus in Korean population. Diabet Med. 2005; 22(5): 569–75.
81. González-Sánchez J.L., Martínez-Calatrava M.J., Martínez-Larrad M.T. et al. Interaction of the –308G/A promoter polymorphism of the tumor necrosis factor-alpha gene with single-nucleotide polymorphism 45 of the adiponectin gene: effect on serum adiponectin concentrations in a Spanish population. Clin Chem. 2006; 52(1): 97–103.
82. Menzaghi C., Ercolino T., Di Paola R. et al. A haplotype at the adiponectin locus is associated with obesity and other features of the insulin resistance syndrome. Diabetes. 2002; 51(7): 2306–12.
83. Bouatia-Naji N., Meyre D., Lobbens S. et al. ACDC/adiponectin polymorphisms are associated with severe childhood and adult obesity. Diabetes. 2006; 55(2): 545–50.
84. Gu H.F., Abulaiti A., Ostenson C.G. et al. Single nucleotide SNPs in the proximal promoter region of the adiponectin (APM1) gene are associated with T2D in Swedish caucasians. Diabetes. 2004; 53 Suppl 1: 31–5.
85. Vasseur F., Helbecque N., Lobbens S. et al. Hypoadiponectinaemia and high risk of type 2 diabetes are associated with adiponectin-encoding (AdipoQ) gene promoter variants in morbid obesity: evidence for a role of AdipoQ in diabesity. Diabetologia. 2005; 48: 892–9.
86. Laumen H., Saningong A.D., Heid I.M. et al. Functional characterization of promoter variants of the adiponectin gene complemented by epidemiological data. Diabetes. 2009; 58(4): 984–91.
87. Owecki M., Miczke A., Kaczmarek M. et al. The Y111 H (T415C) polymorphism in exon 3 of the gene encoding adiponectin is uncommon in Polish obese patients. Horm Metab Res. 2007; 39(11): 797–800.
88. Janghorbani M., Van Dam R.M., Willett W.C., Hu F.B. Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol. 2007; 166(5): 495–505.
89. Kharroubi I., Rasschaert J., Eizirik D.L., Cnop M. Expression of adiponectin receptors in pancreatic beta cells. Biochem Biophys Res Commun. 2003; 26; 312(4): 1118–22.
90. Thamer C., Haap M., Heller E. et al. Beta cell function, insulin resistance and plasma adiponectin concentrations are predictors for the change of postprandial glucose in non-diabetic subjects at risk for type 2 diabetes. Horm Metab Res. 2006; 38(3): 178–82.
91. Ma J., Möllsten A., Falhammar H. et al. Genetic association analysis of the adiponectin polymorphisms in type 1 diabetes with and without diabetic nephropathy. J Diabetes Complications. 2007; 21(1): 28–33.
92. Musso G., Gambino R., De Michieli F., Durazzo M., Pagano G., Cassader M. Adiponectin gene polymorphisms modulate acute adiponectin response to dietary fat: Possible pathogenetic role in NASH. Hepatology. 2008; 47(4): 1167–77.
93. Carninci P., Sandelin A., Lenhard B. et al. Genome-wide analysis of mammalian promoter architecture and evolution. Nat Genet. 2006; 38(6): 626–35.
94. Li L., He S., Sun J.M., Davie J.R. Gene regulation by Sp1 and Sp3. Biochem Cell Biol. 2004; 82(4): 460–71.
95. Barth N., langmann T., Scholmerich J., Schmitz G., Schaffler A. Identification of regulatory elements in the human adipose most abundant gene transcript-1 (apM-1) promoter: role of SP1/SP3 and TNF-alpha as regulatory pathways. Diabetologia. 2002; 45: 1425–33.
96. Zhang D., Ma J., Brismar K., Efendic S., Gu H.F. A single nucleotide polymorphism alters the sequence of SP1 binding site in the adiponectin promoter region and is associated with diabetic nephropathy among type 1 diabetic patients in the Genetics of Kidneys in Diabetes Study. J Diabetes Complications. 2009; 23(4): 265–72.
97. Vionnet N., Tregouet D., Kazeem G. et al. Analysis of 14 candidate genes for DN on chromosome 3q in European populations: strongest evidence for association with a variant in the promoter region of the adiponectin gene. Diabetes. 2006; 55: 3166–74.
98. Mousavinasab F., Tähtinen T., Jokelainen J. et al. Common polymorphisms in the PPARgamma2 and IRS-1 genes and their interaction influence serum adiponectin concentration in young Finnish men. Mol Genet Metab. 2005; 84(4): 344–8.
99. Menzaghi C., Ercolino T., Salvemini L. et al. Multigenic control of serum adiponectin levels: evidence for a role of the APM1 gene and a locus on 14q13. Physiol Genomics. 2004; 4; 19(2): 170–4.