A genome-wide association study reveals variants in ARL15 that influence adiponectin levels

PLoS Genetics

Volumn 5, Issue 12, 2009, Pages

  Brent Richards, J ^a,b   Waterworth, Dawn ^c   O'Rahilly, Stephen ^d   Hivert, Marie France ^e,f   Loos, Ruth J F ^g   Perry, John R B ^h   Tanaka, Toshiko ^i,j   Timpson, Nicholas John ^k   Semple, Robert K ^d   Soranzo, Nicole ^b,l   Song, Kijoung ^c   Rocha, Nuno ^d   Grundberg, Elin ^a,m   Dupuis, Josée ⁿ   Florez, Jose C ^e,f,o   Langenberg, Claudia ^g   Prokopenko, Inga ^p,q   Saxena, Richa ^e,o   Sladek, Robert ^a   Aulchenko, Yurii ^r   Evans, David ^k   Waeber, Gerard ^s   Erdmann, Jeanette ^t   Burnett, Mary Susan ^u   Sattar, Naveed ^v   Devaney, Joseph ^u   Willenborg, Christina ^t   Hingorani, Aroon ^w   Witteman, Jaquelin C M ^r   Vollenweider, Peter ^s   Glaser, Beate ^k   Hengstenberg, Christian ^x   Ferrucci, Luigi ⁱ   Melzer, David ^h   Stark, Klaus ^x   Deanfield, John ^y   Winogradow, Janina ^x   Grassl, Martina ^x   Hall, Alistair S ^z   Egan, Josephine M ⁱ   Thompson, John R ^aa   Ricketts, Sally L ^ab   König, Inke R ^t   Reinhard, Wibke ^x   Grundy, Scott ^ac   Wichmann, H Erich ^ad,ae   Barter, Phil ^af   Mahley, Robert ^ag   Kesaniemi, Y Antero ^ah   Rader, Daniel J ^ai   Reilly, Muredach P ^ai   Epstein, Stephen E ^u   Stewart, Alexandre F R ^aj   Van Duijn, Cornelia M ^r   Schunkert, Heribert ^t   Burling, Keith ^d   Deloukas, Panos ^l   Pastinen, Tomi ^a,o   Samani, Nilesh J ^ak   McPherson, Ruth ^aj   Smith, George Davey ^k   Frayling, Timothy M ^h   Wareham, Nicholas J ^g   Meigs, James B ^e,f   Mooser, Vincent ^c   Spector, Tim D ^b   more..

^a MCGILL UNIVERSITY   (Canada)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c GLAXOSMITHKLINE   (United States)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

^f HARVARD MEDICAL SCHOOL   (United States)

^g ADDENBROOKE S HOSPITAL   (United Kingdom)

^h PENINSULA MEDICAL SCHOOL   (United Kingdom)

ⁱ NATIONAL INSTITUTE ON AGING   (United States)

^j MEDSTAR RESEARCH INSTITUTE   (United States)

^k MEDICAL RESEARCH COUNCIL   (United Kingdom)

^l WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^m MCGILL UNIVERSITY   (Canada)

ⁿ BOSTON UNIVERSITY   (United States)

^o MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^p UNIVERSITY OF OXFORD   (United Kingdom)

^q UNIVERSITY OF OXFORD   (United Kingdom)

^r ERASMUS MEDICAL CENTER   (Netherlands)

^s LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^t UNIVERSITY OF LÜBECK   (Germany)

^u WASHINGTON HOSPITAL CENTER   (United States)

^v UNIVERSITY OF GLASGOW   (United Kingdom)

^w UNIVERSITY COLLEGE LONDON   (United Kingdom)

^x UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^y GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^z UNIVERSITY OF LEEDS   (United Kingdom)

^aa UNIVERSITY OF LEICESTER   (United Kingdom)

^ab UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^ac UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^ad INSTITUTE OF EPIDEMIOLOGY   (Germany)

^ae UNIVERSITY OF MUNICH   (Germany)

^af HEART RESEARCH INSTITUTE   (Australia)

^ag GLADSTONE INSTITUTE OF NEUROLOGICAL DISEASE   (United States)

^ah UNIVERSITY OF OULU   (Finland)

^ai UNIVERSITY OF PENNSYLVANIA   (United States)

^aj UNIVERSITY OF OTTAWA HEART INSTITUTE   (Canada)

^ak UNIVERSITY OF LEICESTER   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 15; ADIPONECTIN; UNCLASSIFIED DRUG;

ADULT; AGED; ALLELE; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; GENE EXPRESSION; GENE LOCUS; GENETIC VARIABILITY; HUMAN; HUMAN EXPERIMENT; HUMAN GENOME; ISCHEMIC HEART DISEASE; MALE; METABOLIC DISORDER; NON INSULIN DEPENDENT DIABETES MELLITUS; NORMAL HUMAN; RISK ASSESSMENT; SINGLE NUCLEOTIDE POLYMORPHISM; BLOOD; CORONARY ARTERY DISEASE; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENETICS; META ANALYSIS; PHYSIOLOGY;

ADIPONECTIN; CORONARY DISEASE; DIABETES MELLITUS, TYPE 2; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 74249100913     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000768     Document Type: Article

References (59)

1. Hivert MF, Sullivan LM, Fox CS, Nathan DM, D'Agostino RB Sr, et al. (2008) Associations of adiponectin, resistin, and tumor necrosis factor-alpha with insulin resistance. J Clin Endocrinol Metab 93: 3165-3172.
2. Hung J, McQuillan BM, Thompson PL, Beilby JP (2008) Circulating adiponectin levels associate with inflammatory markers, insulin resistance and metabolic syndrome independent of obesity. Int J Obes (Lond) 32: 772-779.
3. Wannamethee SG, Tchernova J, Whincup P, Lowe GD, Rumley A, et al. (2007) Associations of adiponectin with metabolic and vascular risk parameters in the British Regional Heart Study reveal stronger links to insulin resistance-related than to coronory heart disease risk-related parameters. Int J Obes (Lond) 31: 1089-1098.
4. Lindsay RS, Funahashi T, Hanson RL, Matsuzawa Y, Tanaka S, et al. (2002) Adiponectin and development of type 2 diabetes in the Pima Indian population. The Lancet 360: 57-58.
5. Weyer C, Funahashi T, Tanaka S, Hotta K, Matsuzawa Y, et al. (2001) Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. J Clin Endocrinol Metab 86: 1930-1935.
6. Spranger J, Kroke A, Mohlig M, Bergmann MM, Ristow M, et al. (2003) Adiponectin and protection against type 2 diabetes mellitus. Lancet 361: 226-228.
7. Pischon T, Girman CJ, Hotamisligil GS, Rifai N, Hu FB, et al. (2004) Plasma Adiponectin Levels and Risk of Myocardial Infarction in Men. JAMA: The Journal of the American Medical Association 291: 1730-1737.
8. Hoffstedt J, Arvidsson E, Sjolin E, Wahlen K, Arner P (2004) Adipose tissue adiponectin production and adiponectin serum concentration in human obesity and insulin resistance. J Clin Endocrinol Metab 89: 1391-1396.
9. Peake PW, Kriketos AD, Campbell LV, Shen Y, Charlesworth JA (2005) The metabolism of isoforms of human adiponectin: studies in human subjects and in experimental animals. Eur J Endocrinol 153: 409-417.
10. Comuzzie AG, Funahashi T, Sonnenberg G, Martin LJ, Jacob HJ, et al. (2001) The genetic basis of plasma variation in adiponectin, a global endophenotype for obesity and the metabolic syndrome. Journal of Clinical Endocrinology and Metabolism 86: 4321-4325.
11. Vasseur F, Helbecque N, Dina C, Lobbens S, Delannoy V, et al. (2002) Singlenucleotide polymorphism haplotypes in the both proximal promoter and exon 3 of the APM1 gene modulate adipocyte-secreted adiponectin hormone levels and contribute to the genetic risk for type 2 diabetes in French Caucasians. Hum Mol Genet 11: 2607-2614.
12. Menzaghi C, Trischitta V, Doria A (2007) Genetic influences of adiponectin on insulin resistance, type 2 diabetes, and cardiovascular disease. Diabetes 56: 1198-1209.
13. Hivert MF, Manning AK, McAteer JB, Florez JC, Dupuis J, et al. (2008) Common variants in the adiponectin gene (ADIPOQ) associated with plasma adiponectin levels, type 2 diabetes, and diabetes-related quantitative traits: the Framingham Offspring Study. Diabetes.
14. Ling H, Waterworth DM, Stirnadel HA, Pollin TI, Barter PJ, et al. (2009) Genome-wide Linkage and Association Analyses to Identify Genes Influencing Adiponectin Levels: The GEMS Study Obesity (Silver Spring).
15. Zeggini E, Scott LJ, Saxena R, Voight BF, Marchini JL, et al. (2008) Metaanalysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes. Nat Genet 40: 638-645.
16. Prokopenko I, Langenberg C, Florez JC, Saxena R, Soranzo N, et al. (2008) Variants in MTNR1B influence fasting glucose levels. Nat Genet.
17. Willer CJ, Speliotes EK, Loos RJ, Li S, Lindgren CM, et al. (2009) Six new loci associated with body mass index highlight a neuronal influence on body weight regulation. Nat Genet 41: 25-34.
18. Loos RJ, Lindgren CM, Li S, Wheeler E, Zhao JH, et al. (2008) Common variants near MC4R are associated with fat mass, weight and risk of obesity. Nat Genet 40: 768-775.
19. Gillingham AK, Munro S (2007) The small G proteins of the Arf family and their regulators. Annu Rev Cell Dev Biol 23: 579-611.
20. Thierry-Mieg D, Thierry-Mieg J (2006) AceView: a comprehensive cDNAsupported gene and transcripts annotation. Genome Biology 7: S12.
21. Hofmann I, Thompson A, Sanderson CM, Munro S (2007) The Arl4 family of small G proteins can recruit the cytohesin Arf6 exchange factors to the plasma membrane. Curr Biol 17: 711-716.
22. Fuss B, Becker T, Zinke I, Hoch M (2006) The cytohesin Steppke is essential for insulin signalling in Drosophila. Nature 444: 945-948.
23. Ishiki M, Klip A (2005) Minireview: recent developments in the regulation of glucose transporter-4 traffic: new signals, locations, and partners. Endocrinology 146: 5071-5078.
24. Hou JC, Pessin JE (2007) Ins (endocytosis) and outs (exocytosis) of GLUT4 trafficking. Curr Opin Cell Biol 19: 466-473.
25. Pollin TI, Tanner K, O'Connell JR, Ott SH, Damcott CM, et al. (2005) Linkage of plasma adiponectin levels to 3q27 explained by association with variation in the APM1 gene. Diabetes 54: 268-274.
26. Basu R, Pajvani UB, Rizza RA, Scherer PE (2007) Selective downregulation of the high molecular weight form of adiponectin in hyperinsulinemia and in type 2 diabetes: differential regulation from nondiabetic subjects. Diabetes 56: 2174-2177.
27. Blumer RM, van der Crabben SN, Stegenga ME, Tanck MW, Ackermans MT, et al. (2008) Hyperglycemia prevents the suppressive effect of hyperinsulinemia on plasma adiponectin levels in healthy humans. Am J Physiol Endocrinol Metab 295: E613-617.
28. Brame LA, Considine RV, Yamauchi M, Baron AD, Mather KJ (2005) Insulin and endothelin in the acute regulation of adiponectin in vivo in humans. Obes Res 13: 582-588.
29. Imagawa A, Funahashi T, Nakamura T, Moriwaki M, Tanaka S, et al. (2002) Elevated serum concentration of adipose-derived factor, adiponectin, in patients with type 1 diabetes. Diabetes Care 25: 1665-1666.
30. Lindstrom T, Frystyk J, Hedman CA, Flyvbjerg A, Arnqvist HJ (2006) Elevated circulating adiponectin in type 1 diabetes is associated with long diabetes duration. Clin Endocrinol (Oxf) 65: 776-782.
31. Galler A, Gelbrich G, Kratzsch J, Noack N, Kapellen T, et al. (2007) Elevated serum levels of adiponectin in children, adolescents and young adults with type 1 diabetes and the impact of age, gender, body mass index and metabolic control: a longitudinal study. Eur J Endocrinol 157: 481-489.
32. Leth H, Andersen KK, Frystyk J, Tarnow L, Rossing P, et al. (2008) Elevated levels of high-molecular-weight adiponectin in type 1 diabetes. J Clin Endocrinol Metab 93: 3186-3191.
33. Semple RK, Soos MA, Luan J, Mitchell CS, Wilson JC, et al. (2006) Elevated plasma adiponectin in humans with genetically defective insulin receptors. J Clin Endocrinol Metab 91: 3219-3223.
34. Semple RK, Halberg NH, Burling K, Soos MA, Schraw T, et al. (2007) Paradoxical elevation of high-molecular weight adiponectin in acquired extreme insulin resistance due to insulin receptor antibodies. Diabetes 56: 1712-1717.
35. Bluher M, Michael MD, Peroni OD, Ueki K, Carter N, et al. (2002) Adipose tissue selective insulin receptor knockout protects against obesity and obesityrelated glucose intolerance. Dev Cell 3: 25-38.
36. Firmann M, Mayor V, Vidal PM, Bochud M, Pecoud A, et al. (2008) The CoLaus study: a population-based study to investigate the epidemiology and genetic determinants of cardiovascular risk factors and metabolic syndrome. BMC Cardiovasc Disord 8: 6.
37. Andrew T, Hart DJ, Snieder H, de LM, Spector TD, et al. (2001) Are twins and singletons comparable? A study of disease-related and lifestyle characteristics in adult women. Twin Res 4: 464-477.
38. Richards JB, Valdes AM, Burling K, Perks UC, Spector TD (2007) Serum adiponectin and bone mineral density in women. J Clin Endocrinol Metab 92: 1517-1523.
39. Stirnadel H, Lin X, Ling H, Song K, Barter P, et al. (2008) Genetic and phenotypic architecture of metabolic syndrome-associated components in dyslipidemic and normolipidemic subjects: the GEMS Study. Atherosclerosis 197: 868-876.
40. Richards JB, Rivadeneira F, Inouye M, Pastinen TM, Soranzo N, et al. (2008) Bone mineral density, osteoporosis, and osteoporotic fractures: a genome-wide association study. Lancet 371: 1505-1512.
41. Shock NW, Greulich RC, Andres RA, Arenberg D, Costa PT, et al. (1984) Normal Human Aging: The Baltimore Longitudinal Study of Aging. NIH Publication No 84-2450.
42. Ferrucci L, Bandinelli S, Benvenuti E, Di Iorio A, Macchi C, et al. (2000) Subsystems contributing to the decline in ability to walk: bridging the gap between epidemiology and geriatric practice in the InCHIANTI study. J Am Geriatr Soc 48: 1618-1625.
43. Melzer D, Perry JR, Hernandez D, Corsi AM, Stevens K, et al. (2008) A genome-wide association study identifies protein quantitative trait loci (pQTLs). PLoS Genet 4: e1000072.
44. Golding J, Pembrey M, Jones R (2001) ALSPAC-the Avon Longitudinal Study of Parents and Children. I. Study methodology. Paediatr Perinat Epidemiol 15: 74-87.
45. Harding AH, Sargeant LA, Welch A, Oakes S, Luben RN, et al. (2001) Fat consumption and HbA(1c) levels: the EPIC-Norfolk study. Diabetes Care 24: 1911-1916.
46. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, et al. (1985) Homeostasis Model Assessment - Insulin Resistance and Beta-Cell Function from Fasting Plasma-Glucose and Insulin Concentrations in Man. Diabetologia 28: 412-419.
47. Rafiq S, Melzer D, Weedon MN, Lango H, Saxena R, et al. (2008) Gene variants influencing measures of inflammation or predisposing to autoimmune and inflammatory diseases are not associated with the risk of type 2 diabetes. Diabetologia 51: 2205-2213.
48. Helgadottir A, Manolescu A, Helgason A, Thorleifsson G, Thorsteinsdottir U, et al. (2006) A variant of the gene encoding leukotriene A4 hydrolase confers ethnicity-specific risk of myocardial infarction. Nat Genet 38: 68-74.
49. McPherson R, Pertsemlidis A, Kavaslar N, Stewart A, Roberts R, et al. (2007) A common allele on chromosome 9 associated with coronary heart disease. Science 316: 1488-1491.
50. Samani NJ, Erdmann J, Hall AS, Hengstenberg C, Mangino M, et al. (2007) Genomewide association analysis of coronary artery disease. N Engl J Med 357: 443-453.
51. Consortium WTCC (2007) Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447: 661-678.
52. Sandhu MS, Waterworth DM, Debenham SL, Wheeler E, Papadakis K, et al. (2008) LDL-cholesterol concentrations: a genome-wide association study. Lancet 371: 483-491.
53. Erdmann J, Großhennig A, Braund P, König I, Hengstenberg C, et al. (2009) New susceptibility locus for coronary artery disease on chromosome 3q22.3. Nature Genetics, In Press.
54. Hofman A, Breteler MM, van Duijn CM, Krestin GP, Pols HA, et al. (2007) The Rotterdam Study: objectives and design update. Eur J Epidemiol 22: 819-829.
55. Abecasis GR, Cherny SS, Cookson WO, Cardon LR (2002) Merlin-rapid analysis of dense genetic maps using sparse gene flow trees. Nat Genet 30: 97-101.
56. Folks JL (1984) Combination of independent tests; Krishnaiah PR, Sen PK, eds. Amsterdam, North-Holland: Elsevier Science Publ Co.
57. Frazer KA, Ballinger DG, Cox DR, Hinds DA, Stuve LL, et al. (2007) A second generation human haplotype map of over 3.1 million SNPs. Nature 449: 851-861.
58. Nyholt DR (2004) A simple correction for multiple testing for single-nucleotide polymorphisms in linkage disequilibrium with each other. Am J Hum Genet 74: 765-769.
59. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. Bmj 327: 557-560.