The genetic architecture of lipoprotein subclasses in Gullah-speaking African American families enriched for type 2 diabetes: The Sea Islands Genetic African American Registry (Project SuGAR)

Journal of Lipid Research

Volumn 51, Issue 3, 2010, Pages 586-597

  Divers, Jasmin ^a,b   Sale, Michèle M ^a,c,d   Lu, Lingyi ^a   Chen, Wei Min ^a,e   Lok, Kerry H ^c   Spruill, Ida J ^f   Fernandes, Jyotika K ^f   Langefeld, Carl D ^a,b   Garvey, W Timothy ^c,g  

^a Center for Public Health Genomics   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

^c Department of Medicine ^*  (United States)

^d UNIVERSITY OF VIRGINIA   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^f MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^g BIRMINGHAM VA MEDICAL CENTER   (United States)

Author keywords

Genetic correlation; Heritability; Linkage analysis; Lipids; Lipoproteins

Indexed keywords

LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; VERY LOW DENSITY LIPOPROTEIN;

ADULT; AFRICAN AMERICAN; ARTICLE; CHROMOSOME 20P; CHROMOSOME 6P; FAMILIAL DISEASE; FEMALE; GENE STRUCTURE; GENETIC LINKAGE; GENETIC VARIABILITY; GENOTYPE; HERITABILITY; HUMAN; MAJOR CLINICAL STUDY; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; PARTICLE SIZE; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM;

ADULT; AFRICAN AMERICANS; ANALYSIS OF VARIANCE; DIABETES MELLITUS, TYPE 2; FEMALE; HUMANS; LIPOPROTEINS; MALE; MIDDLE AGED; PARTICLE SIZE; PHENOTYPE; REGISTRIES; UNITED STATES;

EID: 77950608687     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M001842     Document Type: Article

References (79)

1. Engelgau, M. M., L. S. Geiss, J. B. Saaddine, J. P. Boyle, S. M. Benjamin, E. W. Gregg, E. F. Tierney, N. Rios-Burrows, A. H. Mokdad, E. S. Ford, et al. 2004. The evolving diabetes burden in the United States. Ann. Intern. Med. 140: 945-950.
2. Haffner, S. M., S. Lehto, T. Ronnemaa, K. Pyorala, and M. Laakso. 1998. Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myo-cardial infarction. N. Engl. J. Med. 339: 229-234.
3. Casiglia, E., G. Zanette, A. Mazza, V. Donadon, C. Donada, A. Pizziol, V. Tikhonoff, P. Palatini, and A. C. Pessina. 2000. Cardiovascular mortality in non-insulin-dependent diabetes mellitus. A controlled study among 683 diabetics and 683 age-and sex-matched normal subjects. Eur. J. Epidemiol. 16: 677-684.
4. Klein, B. E., R. Klein, P. E. McBride, K. J. Cruickshanks, M. Palta, M. D. Knudtson, S. E. Moss, and J. O. Reinke. 2004. Cardiovascular disease, mortality, and retinal microvascular characteristics in type 1 diabetes: Wisconsin epidemiologic study of diabetic retinopathy. Arch. Intern. Med. 164: 1917-1924.
5. Eckel, R. H., R. Kahn, R. M. Robertson, and R. A. Rizza. 2006. Preventing cardiovascular disease and diabetes. Diabetes Care. 29: 1697-1699.
6. Fox, C. S., S. Coady, P. D. Sorlie, R. B. D'Agostino, Sr., M. J. Pencina, R. S. Vasan, J. B. Meigs, D. Levy, and P. J. Savage. 2007. Increasing cardiovascular disease burden due to diabetes mellitus: the Framingham Heart Study. Circulation. 115: 1544-1550.
7. Fox, C. S., S. Coady, P. D. Sorlie, D. Levy, J. B. Meigs, R. B. D'Agostino, Sr., P. W. Wilson, and P. J. Savage. 2004. Trends in cardiovascular complications of diabetes. JAMA. 292: 2495-2499.
8. He, Z., and G. L. King. 2004. Microvascular complications of diabe-tes. Endocrinol. Metab. Clin. North Am. 33: 215-238.
9. Bloomgarden, Z. T. 2007. Insulin resistance, dyslipidemia, and car-diovascular disease. Diabetes Care. 30: 2164-2170.
10. Watkins, P. J. 2003. ABC of diabetes: cardiovascular disease, hyper-tension, and lipids. BMJ. 326: 874-876.
11. Sandhu, M. S., D. M. Waterworth, S. L. Debenham, E. Wheeler, K. Papadakis, J. H. Zhao, K. Song, X. Yuan, T. Johnson, S. Ashford, et al. 2008. LDL-cholesterol concentrations: a genome-wide association study. Lancet. 371: 483-491.
12. Ober, C., A. S. Nord, E. E. Thompson, L. Pan, Z. Tan, D. Cusanovich, Y. Sun, R. Nicolae, C. Edelstein, D. H. Schneider, et al. 2009. Genome-wide association study of plasma lipoprotein(a) levels identifies multiple genes on chromosome 6q. J. Lipid Res. 50: 798-806.
13. Knoblauch, H., A. Busjahn, S. Munter, Z. Nagy, H. D. Faulhaber, H. Schuster, and F. C. Luft. 1997. Heritability analysis of lipids and three gene loci in twins link the macrophage scavenger receptor to HDL cholesterol concentrations. Arterioscler. Thromb. Vasc. Biol. 17: 2054-2060.
14. Edwards, K. L., M. C. Mahaney, A. G. Motulsky, and M. A. Austin. 1999. Pleiotropic genetic effects on LDL size, plasma triglyceride, and HDL cholesterol in families. Arterioscler. Thromb. Vasc. Biol. 19: 2456-2464.
15. Kullo, I. J., M. de Andrade, E. Boerwinkle, J. P. McConnell, S. L. Kardia, and S. T. Turner. 2005. Pleiotropic genetic effects contribute to the correlation between HDL cholesterol, triglycerides, and LDL particle size in hypertensive sibships. Am. J. Hypertens. 18: 99-103. (Pubitemid 40187355)
16. McFarlane, S. I., M. Banerji, and J. R. Sowers. 2001. Insulin re-sistance and cardiovascular disease. J. Clin. Endocrinol. Metab. 86: 713-718.
17. Ayyobi, A. F., and J. D. Brunzell. 2003. Lipoprotein distribution in the metabolic syndrome, type 2 diabetes mellitus, and familial combined hyperlipidemia. Am. J. Cardiol. 92: J27-33.
18. Cromwell, W. C., J. D. Otvos, M. J. Keyes, M. J. Pencina, L. Sullivan, R. S. Vasan, P. W. F. Wilson, and R. B. D'Agostino. 2007. LDL particle number and risk of future cardiovascular disease in the Framingham Offspring Study: implications for LDL management. J. Clin. Lipidol. 1: 583-592.
19. Reaven, G. M. 2004. Insulin resistance, cardiovascular disease, and the metabolic syndrome: how well do the emperor's clothes fit? Diabetes Care. 27: 1011-1012.
20. Gardner, C. D., S. P. Fortmann, and R. M. Krauss. 1996. Association of small low-density lipoprotein particles with the incidence of coronary artery disease in men and women. JAMA. 276: 875-881.
21. Lamarche, B., A. Tchernof, S. Moorjani, B. Cantin, G. R. Dagenais, P. J. Lupien, and J. P. Despres. 1997. Small, dense low-density lipo-protein particles as a predictor of the risk of ischemic heart disease in men. Prospective results from the Quebec Cardiovascular Study. Circulation. 95: 69-75.
22. Assmann, G., and A. M. Gotto, Jr. 2004. HDL cholesterol and pro-tective factors in atherosclerosis. Circulation. 109: III8-III14.
23. Rosenson, R. S., J. D. Otvos, and D. S. Freedman. 2002. Relations of lipoprotein subclass levels and low-density lipoprotein size to progression of coronary artery disease in the Pravastatin Limitation of Atherosclerosis in the Coronary Arteries (PLAC-I) trial. Am. J. Cardiol. 90: 89-94.
24. Otvos, J. D. 2002. Measurement of lipoprotein subclass profiles by nuclear magnetic resonance spectroscopy. Clin. Lab. 48: 171-180.
25. Shao, B., and J. W. Heinecke. 2009. HDL, lipid peroxidation, and atherosclerosis. J. Lipid Res. 50: 599-601.
26. Freedman, D. S., J. D. Otvos, E. J. Jeyarajah, J. J. Barboriak, A. J. Anderson, and J. A. Walker. 1998. Relation of lipoprotein subclasses as measured by proton nuclear magnetic resonance spec-troscopy to coronary artery disease. Arterioscler. Thromb. Vasc. Biol. 18: 1046-1053.
27. Garvey, W. T., S. Kwon, D. Zheng, S. Shaughnessy, P. Wallace, A. Hutto, K. Pugh, A. J. Jenkins, R. L. Klein, and Y. Liao. 2003. Effects of insulin resistance and type 2 diabetes on lipoprotein subclass particle size and concentration determined by nuclear magnetic resonance. Diabetes. 52: 453-462.
28. Liao, Y., S. Kwon, S. Shaughnessy, P. Wallace, A. Hutto, A. J. Jenkins, R. L. Klein, and W. T. Garvey. 2004. Critical evaluation of adult treatment panel III criteria in identifying insulin resistance with dyslipidemia. Diabetes Care. 27: 978-983.
29. Kullo, I. J., K. Ding, E. Boerwinkle, S. T. Turner, and M. de Andrade. 2006. Quantitative trait loci infl uencing low density lipoprotein particle size in African Americans. J. Lipid Res. 47: 1457-1462.
30. Oberman, A. 2000. Hypertriglyceridemia and coronary heart dis-ease. J. Clin. Endocrinol. Metab. 85: 2098-2105.
31. Austin, M. A. 1996. Genetic epidemiology of dyslipidaemia and atherosclerosis. Ann. Med. 28: 459-463.
32. Opala, J. A. 1987. The Gullah: rice, slavery, and the Sierra Leone-American connection. United States Information Service, Freetown, Sierra Leone.
33. Parra, E. J., R. A. Kittles, G. Argyropoulos, C. L. Pfaff, K. Hiester, C. Bonilla, N. Sylvester, D. Parrish-Gause, W. T. Garvey, L. Jin, et al. 2001. Ancestral proportions and admixture dynamics in geographically defined African Americans living in South Carolina. Am. J. Phys. Anthropol. 114: 18-29.
34. Mclean, D. C., G. P. Page, and W. T. Garvey. 2001. Mitochondrial DNA and Y-chromosome haplotypes of Gullah-speaking African Americans show closer genetic distance to Sierra Leoneans and lower Caucasian admixture than other new world African populations. Am. J. Hum. Genet. 69: 227-227
35. McLean, D. C., Jr., I. Spruill, G. Argyropoulos, G. P. Page, M. D. Shriver, and W. T. Garvey. 2005. Mitochondrial DNA (mtDNA) haplotypes reveal maternal population genetic affinities of Sea Island Gullah-speaking African Americans. Am. J. Phys. Anthropol. 127: 427-438.
36. Parra, E. J., A. Marcini, L. Akey, J. Martinson, M. A. Batzer, R. Cooper, T. Forrester, D. B. Allison, R. Deka, R. E. Ferrell, et al. 1998. Estimating African American admixture proportions by use of population-specific alleles. Am. J. Hum. Genet. 63: 1839-1851.
37. Garvey WT, McClean DC, and, S. I. 2003. The search for obesity genes in isolated populations: Gullah-speaking African Americans and the role of Uncoupling Protein 3 as a thrifty gene. In Progress in Obesity Research. Madeiros G, Halpern A, and Bouchards C. John Libbey Eurotext Ltd., London. 373-380.
38. Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus 2003. Diabetes Care. 26: S5-S20.
39. Otvos, J. D. 2000. Measurement of lipoprotein subclass profiles by nuclear magnetic resonance spectroscopy. In Handbook of Lipoprotein Testing. American Association for Clinical Chemistry., Washington (DC). 609-623.
40. Sun, L., K. Wilder, and M. S. McPeek. 2002. Enhanced pedigree error detection. Hum. Hered. 54: 99-110.
41. McPeek, M. S., and L. Sun. 2000. Statistical tests for detection of misspecified relationships by use of genome-screen data. Am. J. Hum. Genet. 66: 1076-1094.
42. O'Connell, J. R., and D. E. Weeks. 1998. PedCheck: a program for identification of genotype incompatibilities in linkage analysis. Am. J. Hum. Genet. 63: 259-266.
43. Kong, X., K. Murphy, T. Raj, C. He, P. S. White, and T. C. Matise. 2004. A combined linkage-physical map of the human genome. Am. J. Hum. Genet. 75: 1143-1148.
44. Almasy, L., and J. Blangero. 1998. Multipoint quantitative-trait linkage analysis in general pedigrees. Am. J. Hum. Genet. 62: 1198-1211.
45. Abecasis, G. R., S. S. Cherny, W. O. Cookson, and L. R. Cardon. 2002. Merlin: rapid analysis of dense genetic maps using sparse gene fl ow trees. Nat. Genet. 30: 97-101.
46. Comuzzie, A. G., M. C. Mahaney, L. Almasy, T. D. Dyer, and J. Blangero. 1997. Exploiting pleiotropy to map genes for oligogenic phenotypes using extended pedigree data. Genet. Epidemiol. 14: 975-980.
47. Almasy, L., T. D. Dyer, and J. Blangero. 1997. Bivariate quantitative trait linkage analysis: pleiotropy versus co-incident linkages. Genet. Epidemiol. 14: 953-958.
48. Lander, E., and L. Kruglyak. 1995. Genetic dissection of complex traits: guidelines for interpreting and reporting linkage results. Nat. Genet. 11: 241-247.
49. Conneally, P. M., J. H. Edwards, K. K. Kidd, J. M. Lalouel, N. E. Morton, J. Ott, and R. White. 1985. Report of the Committee on Methods of Linkage Analysis and Reporting. Cytogenet. Cell Genet. 40: 356-359.
50. van Ooijen, J. W. 1999. LOD significance thresholds for QTL analysis in experimental populations of diploid species. Heredity. 83: 613-624.
51. Xu, Z., and J. A. Taylor. 2009. SNPinfo: integrating GWAS and can-didate gene information into functional SNP selection for genetic association studies. Nucleic Acids Res. 37: W600-W605.
52. Sale, M. M., L. Lu, I. J. Spruill, J. K. Fernandes, K. H. Lok, J. Divers, C. D. Langefeld, and W. T. Garvey. 2009. Genome-wide linkage scan in Gullah-speaking African American families with type 2 diabetes. Diabetes. 58: 260-267.
53. Snieder, H., L. J. P. van Doornen, and D. I. Boomsma. 1999. Dissecting the genetic architecture of lipids, lipoproteins, and apo-lipoproteins: lessons from twin studies. Arterioscler. Thromb. Vasc. Biol. 19: 2826-2834.
54. Bosse, Y., M. C. Vohl, J. P. Despres, B. Lamarche, T. Rice, D. C. Rao, C. Bouchard, and L. Perusse. 2003. Heritability of LDL peak particle diameter in the Quebec Family Study. Genet. Epidemiol. 25: 375-381.
55. Otvos JD. 2004. NMR LipoProfile test Subclass Particle Analysis. LipoScience, Inc.
56. Kazumi, T., A. Kawaguchi, T. Hozumi, M. Nagao, M. Iwahashi, M. Hayakawa, K. Ishihara, and G. Yoshino. 1999. Low density li-poprotein particle diameter in young, nonobese, normolipidemic Japanese men. Atherosclerosis. 142: 113-119.
57. Jakobsson, A., R. Westerberg, and A. Jacobsson. 2006. Fatty acid elongases in mammals: their regulation and roles in metabolism. Prog. Lipid Res. 45: 237-249.
58. Wu, J., M. A. Province, H. Coon, S. C. Hunt, J. H. Eckfeldt, D. K. Arnett, G. Heiss, C. E. Lewis, R. C. Ellison, D. C. Rao, et al. 2007. An investigation of the effects of lipid-lowering medications: genome-wide linkage analysis of lipids in the HyperGEN study. BMC Genet. 8: 60.
59. Broadbent, H. M., Peden, J. F., Lorkowski, S., Goel, A., Ongen, H., Green, F., Clarke, R., Collins, R., Franzosi, M. G., Tognoni, G., et al. 2008. Susceptibility to coronary artery disease and diabetes is encoded by distinct, tightly linked SNPs in the ANRIL locus on chromosome 9p. Hum. Mol. Genet. 17: 806-814.
60. Coon, H., Leppert, M. F., Eckfeldt, J. H., Oberman, A., Myers, R. H., Peacock, J. M., Province, M. A., Hopkins, P. N., and Heiss, G. 2001. Genome-Wide Linkage Analysis of Lipids in the Hypertension Genetic Epidemiology Network (HyperGEN) Blood Pressure Study. Arterioscler. Thromb. Vasc. Biol. 21: 1969-1976.
61. Malhotra, A., J. K. Wolford, and the American Diabetes Association GENNID Study Group. 2005. Analysis of Quantitative Lipid Traits in the Genetics of NIDDM (GENNID) Study. Diabetes. 54: 3007-3014.
62. Feitosa, M. F., I. B. Borecki, T. Rankinen, T. Rice, J. P. Despres, Y. C. Chagnon, J. Gagnon, A. S. Leon, J. S. Skinner, C. Bouchard, et al. 2005. Evidence of QTLs on chromosomes 1q42 and 8q24 for LDL-cholesterol and apoB levels in the HERITAGE Family Study. J. Lipid Res. 46: 281-286. (Pubitemid 40271092)
63. Li, W. D., C. Dong, D. Li, C. Garrigan, and R. A. Price. 2005. A ge-nome scan for serum triglyceride in obese nuclear families. J. Lipid Res. 46: 432-438.
64. Adeyemo, A. A., Johnson, T., Acheampong, J., Oli, J., Okafor, G., Amoah, A., Owusu, S., Gyenim-Boateng, K., Eghan, B. A., Jr., Abbiyesuku, F., et al. 2005. A genome wide quantitative trait linkage analysis for serum lipids in type 2 diabetes in an African population. Atherosclerosis. 181: 389-397.
65. Badzioch, M. D., R. P. Igo, Jr., F. Gagnon, J. D. Brunzell, R. M. Krauss, A. G. Motulsky, E. M. Wijsman, and G. P. Jarvik. 2004. Low-density lipoprotein particle size loci in familial combined hyperlip-idemia: evidence for multiple loci from a genome scan. Arterioscler. Thromb. Vasc. Biol. 24: 1942-1950.
66. Kaess, B., M. Fischer, A. Baessler, K. Stark, F. Huber, W. Kremer, H. R. Kalbitzer, H. Schunkert, G. Riegger, and C. Hengstenberg. 2008. The lipoprotein subfraction profile: heritability and identification of quantitative trait loci. J. Lipid Res. 49: 715-723.
67. Cupples, L. A., H. Arruda, E. Benjamin, R. D'Agostino, S. Demissie, A. DeStefano, J. Dupuis, K. Falls, C. Fox, D. Gottlieb, et al. 2007. The Framingham Heart Study 100K SNP genome-wide association study resource: overview of 17 phenotype working group reports. BMC Med. Genet. 8: S1.
68. Kooner, J. S., Chambers, J. C., Guilar-Salinas, C. A., Hinds, D. A., Hyde, C. L., Warnes, G. R., Gomez Perez, F. J., Frazer, K. A., Elliott, P., Scott, J., et al. 2008. Genome-wide scan identifies variation in MLXIPL associated with plasma triglycerides. Nat. Genet. 40: 149-151.
69. Wallace, C., Newhouse, S. J., Braund, P., Zhang, F., Tobin, M., Falchi, M., Ahmadi, K., Dobson, R. J., Marrano, A. C., Hajat, C., et al. 2008. Genome-wide association study identifies genes for bio-markers of cardiovascular disease: serum urate and dyslipidemia. Am. J. Hum. Genet. 82: 139-149
70. Diabetes Genetics Initiative of Broad Institute of Harvard and MIT, Lund University, and Novartis Institutes of BioMedical Research, Saxena R, Voight BF, Lyssenko V, Burtt NP, de Bakker PI, Chen H, Roix JJ. 2007. Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. Science. 316: 1331-1336.
71. Willer, C. J., Sanna, S., Jackson, A. U., Scuteri, A., Bonnycastle, L. L., Clarke, R., Heath, S. C., Timpson, N. J., Najjar, S. S., Stringham, H. M., et al. 2008. Newly identified loci that infl uence lipid concentrations and risk of coronary artery disease. Nat. Genet. 40: 161-169.
72. Kathiresan, S., O. Melander, C. Guiducci, A. Surti, N. P. Burtt, M. J. Rieder, G. M. Cooper, C. Roos, B. F. Voight, A. S. Havulinna, et al. 2008. Six new loci associated with blood low-density lipoprotein cholesterol, high-density lipoprotein cholesterol or triglycerides in humans. Nat. Genet. 40: 189-197.
73. Lewis, J. P., N. D. Palmer, P. J. Hicks, M. M. Sale, C. D. Langefeld, B. I. Freedman, J. Divers, and D. W. Bowden. 2008. Association analysis of European-derived type 2 diabetes SNPs from whole genome association studies in African Americans. Diabetes. 57: 2220-2225.
74. Miljkovic-Gacic, I., C. H. Bunker, R. E. Ferrell, C. M. Kammerer, R. W. Evans, A. L. Patrick, and L. H. Kuller. 2006. Lipoprotein subclass and particle size differences in Afro-Caribbeans, African Americans, and white Americans: associations with hepatic lipase gene variation. Metabolism. 55: 96-102.
75. Lamarche, B., A. C. St-Pierre, I. L. Ruel, B. Cantin, G. R. Dagenais, and J. P. Després. 2001. A prospective, population-based study of low density lipoprotein particle size as a risk factor for ischemic heart disease in men. Can. J. Cardiol. 17: 859-865.
76. El Harchaoui K., W. A. van der Steeg, E. S. Stroes, J. A. Kuivenhoven, J. D. Otvos, N. J. Wareham, B. A. Hutten, J. J. Kastelein, K. T. Khaw, and S. M. Boekholdt. 2007. Value of low-density lipoprotein particle number and size as predictors of coronary artery disease in apparently healthy men and women: the EPIC-Norfolk Prospective Population Study. J. Am. Coll. Cardiol. 49: 547-553.
77. Kuller, L., A. Arnold, R. Tracy, J. Otvos, G. Burke, B. Psaty, D. Siscovick, D. S. Freedman, and R. Kronmal. 2002. Nuclear magnetic resonance spectroscopy of lipoproteins and risk of coronary heart disease in the cardiovascular health study. Arterioscler. Thromb. Vasc. Biol. 22: 1175-1180.
78. Stampfer, M. J., R. M. Krauss, J. Ma, P. J. Blanche, L. G. Holl, F. M. Sacks, and C. H. Hennekens. 1996. A prospective study of triglyc-eride level, low-density lipoprotein particle diameter, and risk of myocardial infarction. JAMA. 276: 882-888.
79. Adiels, M., S. O. Olofsson, M. R. Taskinen, and J. Boren. 2008. Overproduction of very low-density lipoproteins is the hallmark of the dyslipidemia in the metabolic syndrome. Arterioscler. Thromb. Vasc. Biol. 28: 1225-1236.