Low plasma adiponectin concentrations predict increases in visceral adiposity and insulin resistance

Journal of Clinical Endocrinology and Metabolism

Volumn 102, Issue 12, 2017, Pages 4626-4633

  Han, Seung Jin ^a,b,c   Boyko, Edward J ^b,c   Fujimoto, Wilfred Y ^c   Kahn, Steven E ^b,c   Leonetti, Donna L ^d  

^a Ajou University School of Medicine   (South Korea)

^b VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; ADIPOQ PROTEIN, HUMAN;

ABDOMINAL OBESITY; ABDOMINAL RADIOGRAPHY; ABDOMINAL SUBCUTANEOUS FAT; ADULT; AGE; ARTICLE; ASIAN AMERICAN; BODY COMPOSITION; BODY FAT DISTRIBUTION; BODY MASS; BODY WEIGHT CHANGE; COHORT ANALYSIS; COMPUTER ASSISTED TOMOGRAPHY; CONCENTRATION (PARAMETERS); FEMALE; FOLLOW UP; HOMEOSTASIS MODEL ASSESSMENT; HORMONE BLOOD LEVEL; HUMAN; HUMAN TISSUE; INSULIN RESISTANCE; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; PREDICTION; PRIORITY JOURNAL; PROSPECTIVE STUDY; RADIOIMMUNOASSAY; SEX; THIGH; BLOOD; BODY WEIGHT; DEFICIENCY; DIAGNOSTIC IMAGING; GENETICS; INTRAABDOMINAL FAT; METABOLISM; OBESITY; PATHOLOGY; SUBCUTANEOUS FAT; X-RAY COMPUTED TOMOGRAPHY;

ADIPONECTIN; ADIPOSITY; ADULT; ASIAN AMERICANS; BODY MASS INDEX; BODY WEIGHT; COHORT STUDIES; FEMALE; FOLLOW-UP STUDIES; HUMANS; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; MALE; MIDDLE AGED; PROSPECTIVE STUDIES; SUBCUTANEOUS FAT; TOMOGRAPHY, X-RAY COMPUTED;

EID: 85038254482     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2017-01703     Document Type: Article

References (41)

1. Tilg H, Moschen AR. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol. 2006;6(10): 772-783.
2. Cnop M, Havel PJ, Utzschneider KM, Carr DB, Sinha MK, Boyko EJ, Retzlaff BM, Knopp RH, Brunzell JD, Kahn SE. Relationship of adiponectin to body fat distribution, insulin sensitivity and plasma lipoproteins: evidence for independent roles of age and sex. Diabetologia. 2003;46(4):459-469.
3. Lim S, Quon MJ, Koh KK. Modulation of adiponectin as a potential therapeutic strategy. Atherosclerosis. 2014;233(2): 721-728.
4. Weyer C, Funahashi T, Tanaka S, Hotta K, Matsuzawa Y, Pratley RE, Tataranni PA. Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. J Clin Endocrinol Metab. 2001;86(5):1930-1935.
5. Yang WS, Lee WJ, Funahashi T, Tanaka S, Matsuzawa Y, Chao CL, Chen CL, Tai TY, Chuang LM. Weight reduction increases plasma levels of an adipose-derived anti-inflammatory protein, adiponectin. J Clin Endocrinol Metab. 2001;86(8):3815-3819.
6. Ma W, Huang T, Zheng Y, Wang M, Bray GA, Sacks FM, Qi L. Weight-loss diets, adiponectin, and changes in cardiometabolic risk in the 2-year POUNDS Lost Trial. J Clin Endocrinol Metab. 2016; 101(6):2415-2422.
7. Fruebis J, Tsao TS, Javorschi S, Ebbets-Reed D, Erickson MR, Yen FT, Bihain BE, Lodish HF. Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proc Natl Acad Sci USA. 2001;98(4):2005-2010.
8. Vozarova B, Stefan N, Lindsay RS, Krakoff J, Knowler WC, Funahashi T, Matsuzawa Y, Stumvoll M, Weyer C, Tataranni PA. Low plasma adiponectin concentrations do not predict weight gain in humans. Diabetes. 2002;51(10):2964-2967.
9. Langenberg C, Bergstrom J, Laughlin GA, Barrett-Connor E. Ghrelin, adiponectin, and leptin do not predict long-termchanges in weight and body mass index in older adults: longitudinal analysis of the Rancho Bernardo cohort. Am J Epidemiol. 2005;162(12): 1189-1197.
10. Bennett NR, Boyne MS, Cooper RS, Royal-Thomas TY, Bennett FI, Luke A, Wilks RJ, Forrester TE. Impact of adiponectin and ghrelin on incident glucose intolerance and on weight change. Clin Endocrinol (Oxf). 2009;70(3):408-414.
11. Hivert MF, Sun Q, Shrader P, Mantzoros CS, Meigs JB, Hu FB. Higher adiponectin levels predict greater weight gain in healthy women in the Nurses' Health Study. Obesity (Silver Spring). 2011; 19(2):409-415.
12. Drolet R, Bélanger C, Fortier M, Huot C, Mailloux J, Ĺegaŕe D, Tchernof A. Fat depot-specific impact of visceral obesity on adipocyte adiponectin release in women. Obesity (Silver Spring). 2009; 17(3):424-430.
13. Park KG, Park KS, Kim MJ, Kim HS, Suh YS, Ahn JD, Park KK, Chang YC, Lee IK. Relationship between serum adiponectin and leptin concentrations and body fat distribution. Diabetes Res Clin Pract. 2004;63(2):135-142.
14. Frederiksen L, Nielsen TL, Wraae K, Hagen C, Frystyk J, Flyvbjerg A, Brixen K, Andersen M. Subcutaneous rather than visceral adipose tissue is associated with adiponectin levels and insulin resistance in young men. J Clin Endocrinol Metab. 2009;94(10): 4010-4015.
15. Fujikawa R, Ito C, Nakashima R, Orita Y, Ohashi N. Is there any association between subcutaneous adipose tissue area and plasma total and high molecular weight adiponectin levels? Metabolism. 2008;57(4):506-510.
16. Borges MC, Oliveira IO, Freitas DF, Horta BL, Ong KK, Gigante DP, Barros AJ. Obesity-induced hypoadiponectinaemia: the opposite influences of central and peripheral fat compartments [published online ahead of print March 27, 2017]. Int J Epidemiol.
17. Nawrocki AR, Rajala MW, Tomas E, Pajvani UB, Saha AK, Trumbauer ME, Pang Z, Chen AS, Ruderman NB, Chen H, Rossetti L, Scherer PE. Mice lacking adiponectin show decreased hepatic insulin sensitivity and reduced responsiveness to peroxisome proliferator-activated receptor gamma agonists. J Biol Chem. 2006;281(5):2654-2660.
18. Kim JY, van de Wall E, Laplante M, Azzara A, Trujillo ME, Hofmann SM, Schraw T, Durand JL, Li H, Li G, Jelicks LA, Mehler MF, Hui DY, Deshaies Y, Shulman GI, Schwartz GJ, Scherer PE. Obesity-associated improvements in metabolic profile through expansion of adipose tissue. J Clin Invest. 2007;117(9):2621-2637.
19. Cook JR, Semple RK. Hypoadiponectinemia-cause or consequence of human "insulin resistance"? J Clin Endocrinol Metab. 2010; 95(4):1544-1554.
20. Fujimoto WY, Leonetti DL, Kinyoun JL, Shuman WP, Stolov WC, Wahl PW. Prevalence of complications among second-generation Japanese-American men with diabetes, impaired glucose tolerance, or normal glucose tolerance. Diabetes. 1987;36(6):730-739.
21. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2004;27(Suppl 1):S5-S10.
22. Levy JC, Matthews DR, Hermans MP. Correct homeostasis model assessment (HOMA) evaluation uses the computer program. Diabetes Care. 1998;21(12):2191-2192.
23. Shuman WP, Morris LL, Leonetti DL, Wahl PW, MoceriVM, Moss AA, Fujimoto WY. Abnormal body fat distribution detected by computed tomography in diabetic men. Invest Radiol. 1986;21(6): 483-487.
24. Kutner M, Nachtsheim C, Neter J. Applied Linear Statistical Models. 4th ed. Chicago, IL: McGraw-Hill; 2004.
25. Amato MC, Guarnotta V, Giordano C. Body composition assessment for the definition of cardiometabolic risk. J Endocrinol Invest. 2013;36(7):537-543.
26. Hayashi T, Boyko EJ, McNeely MJ, Leonetti DL, Kahn SE, Fujimoto WY. Visceral adiposity, not abdominal subcutaneous fat area, is associated with an increase in future insulin resistance in Japanese Americans. Diabetes. 2008;57(5):1269-1275.
27. Neeland IJ, Turer AT, Ayers CR, Berry JD, Rohatgi A, Das SR, Khera A, Vega GL, McGuire DK, Grundy SM, de Lemos JA. Body fat distribution and incident cardiovascular disease in obese adults. J Am Coll Cardiol. 2015;65(19):2150-2151.
28. Lear SA, Humphries KH, Kohli S, Chockalingam A, Frohlich JJ, Birmingham CL. Visceral adipose tissue accumulation differs according to ethnic background: results of the Multicultural Community Health Assessment Trial (M-CHAT). Am J Clin Nutr. 2007;86(2):353-359.
29. Kim JY, Ahn SV, Yoon JH, Koh SB, Yoon J, Yoo BS, Lee SH, Park JK, Choe KH, Guallar E. Prospective study of serum adiponectin and incident metabolic syndrome: the ARIRANG study. Diabetes Care. 2013;36(6):1547-1553.
30. Hanley AJ, Wagenknecht LE. Abdominal adiposity and diabetes risk: the importance of precise measures and longitudinal studies. Diabetes. 2008;57(5):1153-1155.
31. Stefan N, Vozarova B, Funahashi T, Matsuzawa Y, Weyer C, Lindsay RS, Youngren JF, Havel PJ, Pratley RE, Bogardus C, Tataranni PA. Plasma adiponectin concentration is associated with skeletal muscle insulin receptor tyrosine phosphorylation, and low plasma concentration precedes a decrease in whole-body insulin sensitivity in humans. Diabetes. 2002;51(6):1884-1888.
32. Hanley AJ, Connelly PW, Harris SB, Zinman B. Adiponectin in a native Canadian population experiencing rapid epidemiological transition. Diabetes Care. 2003;26(12):3219-3225.
33. Yamamoto Y, Hirose H, Saito I, Nishikai K, Saruta T. Adiponectin, an adipocyte-derived protein, predicts future insulin resistance: two-year follow-up study in Japanese population. J Clin Endocrinol Metab. 2004;89(1):87-90.
34. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, Yamashita S, Noda M, Kita S, Ueki K, Eto K, Akanuma Y, Froguel P, Foufelle F, Ferre P, Carling D, Kimura S, Nagai R, Kahn BB, Kadowaki T. Adiponectin stimulates glucose utilization and fattyacid oxidation by activating AMP-activated protein kinase. Nat Med. 2002;8(11):1288-1295.
35. Combs TP, Pajvani UB, Berg AH, Lin Y, Jelicks LA, Laplante M, Nawrocki AR, Rajala MW, Parlow AF, Cheeseboro L, Ding YY, Russell RG, Lindemann D, Hartley A, Baker GR, Obici S, Deshaies Y, Ludgate M, Rossetti L, Scherer PE. A transgenic mouse with a deletion in the collagenous domain of adiponectin displays elevated circulating adiponectin and improved insulin sensitivity. Endocrinology. 2004;145(1):367-383.
36. Awazawa M, Ueki K, Inabe K, Yamauchi T, Kubota N, Kaneko K, KobayashiM, Iwane A, Sasako T, OkazakiY, OhsugiM, Takamoto I, Yamashita S, Asahara H, Akira S, Kasuga M, Kadowaki T. Adiponectin enhances insulin sensitivity by increasing hepatic IRS-2 expression via a macrophage-derived IL-6-dependent pathway. Cell Metab. 2011;13(4):401-412.
37. Holland WL, Miller RA, Wang ZV, Sun K, Barth BM, Bui HH, Davis KE, Bikman BT, Halberg N, Rutkowski JM, Wade MR, Tenorio VM, Kuo MS, Brozinick JT, Zhang BB, Birnbaum MJ, Summers SA, Scherer PE. Receptor-mediated activation of ceramidase activity initiates the pleiotropic actions of adiponectin. Nat Med. 2011;17(1):55-63.
38. Funahashi T, Matsuzawa Y. Adiponectin and the cardiometabolic syndrome: an epidemiological perspective. Best Pract Res Clin Endocrinol Metab. 2014;28(1):93-106.
39. Kang ES, Yun YS, Park SW, Kim HJ, Ahn CW, Song YD, Cha BS, Lim SK, Kim KR, Lee HC. Limitation of the validity of the homeostasis model assessment as an index of insulin resistance in Korea. Metabolism. 2005;54(2):206-211.
40. Pisprasert V, Ingram KH, Lopez-Davila MF, Munoz AJ, Garvey WT. Limitations in the use of indices using glucose and insulin levels to predict insulin sensitivity: impact of race and gender and superiority of the indices derived from oral glucose tolerance test in African Americans. Diabetes Care. 2013;36(4):845-853.
41. Wallace TM, Levy JC, Matthews DR. Use and abuse of HOMA modeling. Diabetes Care. 2004;27(6):1487-1495.