A functional ABCA1 gene variant is associated with low HDL-cholesterol levels and shows evidence of positive selection in Native Americans

Human Molecular Genetics

Volumn 19, Issue 14, 2010, Pages 2877-2885

  Acuña Alonzo, Víctor ^a,c   Flores Dorantes, Teresa ^a   Kruit, Janine K ^d   Villarreal Molina, Teresa ^a   Arellano Campos, Olimpia ^b   Hünemeier, Tábita ^e   Moreno Estrada, Andrés ^f   Ortiz López, Ma Guadalupe ^a,g   Villamil Ramírez, Hugo ^a   León Mimila, Paola ^a   Villalobos Comparan, Marisela ^a   Jacobo Albavera, Leonor ^a   Ramírez Jiménez, Salvador ^a   Sikora, Martin ^h   Zhang, Lin Hua ^d   Pape, Terry D ^d   de Ángeles Granados Silvestre, Ma ^a,g   Montufar Robles, Isela ^a,g   Tito Alvarez, Ana M ⁱ   Zurita Salinas, Camilo ⁱ   Bustos Arriaga, José ^j   Cedillo Barrón, Leticia ^j   Gómez Trejo, Celta ^c   Barquera Lozano, Rodrigo ^c   Vieira Filho, Joao P ^k   Granados, Julio ^b   Romero Hidalgo, Sandra ^l   Huertas Vázquez, Adriana ^m   González Martín, Antonio ⁿ   Gorostiza, Amaya ^c,n   Bonatto, Sandro L ^o   Rodríguez Cruz, Maricela ^p   Wang, Li ^q   Tusié Luna, Teresa ^a   Aguilar Salinas, Carlos A ^b   Lisker, Ruben ^b   Moises, Regina S ^k   Menjivar, Marta ^a   Salzano, Francisco M ^e   Knowler, William C ^r   Bortolini, M Cátira ^e   Hayden, Michael R ^d   Baier, Leslie J ^r   Canizales Quinteros, Samuel ^a   more..

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b INSTITUTO NACIONAL DE CIENCIAS MÉDICAS Y NUTRICIÓN SALVADOR ZUBIRÁN   (Mexico)

^c INSTITUTO NACIONAL DE ANTROPOLOGÍA E HISTORIA   (Mexico)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^f STANFORD UNIVERSITY   (United States)

^g HOSPITAL JUÁREZ DE MÉXICO   (Mexico)

^h INSTITUTE OF EVOLUTIONARY BIOLOGY CSIC UNIVERSITAT POMPEU FABRA   (Spain)

ⁱ Laboratorios Zurita and Zurita   (Ecuador)

^j DEPARTAMENTO DE FÍSICA   (Mexico)

^k FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^l INSTITUTO NACIONAL DE MEDICINA GENÓMICA   (Mexico)

^m CEDARS SINAI MEDICAL CENTER   (United States)

ⁿ UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^o PONTIFICAL CATHOLIC UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^p INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^q INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^r NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER A1; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; ABC TRANSPORTER; ABCA1 PROTEIN, HUMAN;

ADULT; ARTICLE; BODY MASS; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; ETHNIC DIFFERENCE; GENETIC ASSOCIATION; GENETIC SELECTION; GENETIC VARIABILITY; HAPLOTYPE; HUMAN; IN VITRO STUDY; INDIGENOUS PEOPLE; METABOLISM; POPULATION GENETICS; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; UNITED STATES; ALLELE; AMERICAN INDIAN; BLOOD; FEMALE; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENETICS; GEOGRAPHY; MALE; PHYSIOLOGY;

ADULT; ALLELES; ATP BINDING CASSETTE TRANSPORTER 1; ATP-BINDING CASSETTE TRANSPORTERS; CHOLESTEROL, HDL; FEMALE; GENE FREQUENCY; GENETICS, POPULATION; GENOME-WIDE ASSOCIATION STUDY; GEOGRAPHY; HAPLOTYPES; HUMANS; INDIANS, NORTH AMERICAN; LINKAGE DISEQUILIBRIUM; MALE; SELECTION, GENETIC;

EID: 77954145711     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq173     Document Type: Article

References (54)

1. Lorenzo, C., Serrano-Rios, M., Martinez-Larrad, M.T., Gabriel, R., Williams, K., Gonzalez-Villalpando, C., Stern, M.P., Hazuda, H.P. and Haffner, S.M. (2001) Was the historic contribution of Spain to the Mexican gene pool partially responsible for the higher prevalence of type 2 diabetes in Mexican-origin populations? The Spanish Insulin Resistance Study Group, the San Antonio Heart Study, and the Mexico City Diabetes Study. Diabetes Care, 24, 2059-2064.
2. Cossrow, N. and Falkner, B. (2004) Race/ethnic issues in obesity and obesity-related comorbidities. J. Clin. Endocrinol. Metab., 89, 2590-2594.
3. Aguilar-Salinas, C.A., Canizales-Quinteros, S., Rojas-Martínez, R., Mehta, R., Villarreal-Molina, M.T., Arellano-Campos, O., Riba, L., Gómez-Pérez, F.J. and Tusié-Luna, M.T. (2009) Hypoalphalipoproteinemia in the populations with Native American origin: an opportunity to assess the interaction of genes and environment. Curr. Opin. Lipidol., 20, 92-97.
4. Villarreal-Molina, M.T., Aguilar-Salinas, C.A., Rodriguez-Cruz, M., Riaño, D., Villalobos-Comparan, M., Coral-Vazquez, R., Menjivar, M., Yescas-Gomez, P., Königsoerg-Fainstein, M., Romero-Hidalgo, S. et al. (2007) The ATP-binding cassette transporter A1 R230C variant affects HDL cholesterol levels and BMI in the Mexican population: association with obesity and obesity-related comorbidities. Diabetes, 56, 1881-1887.
5. Villarreal-Molina, M.T., Flores-Dorantes, M.T., Arellano-Campos, O., Villalobos-Comparan, M., Rodríguez-Cruz, M., Miliar-García, A., Huertas-Vazquez, A., Menjivar, M., Romero-Hidalgo, S., Wacher, N.H. et al. (2008) Association of the ATP-binding cassette transporter A1 R230C variant with early-onset type 2 diabetes in a Mexican population. Diabetes, 57, 509-513.
6. Attie, A.D., Kastelein, J.P. and Hayden, M.R. (2001) Pivotal role of ABCA1 in reverse cholesterol transport influencing HDL levels and susceptibility to atherosclerosis. J. Lipid Res., 42, 1717-1726.
7. Oram, J.F. and Vaughan, A.M. (2006) ATP-binding cassette cholesterol transporters and cardiovascular disease. Circ. Res., 99, 1031-1043.
8. Wang, J., Burnett, J.R., Near, S., Young, K., Zinman, B., Hanley, A.J., Connelly, P.W., Harris, S.B. and Hegele, R.A. (2000) Common and rare ABCA1 variants affecting plasma HDL cholesterol. Arterioscler. Thromb. Vasc. Biol., 20, 1983-1989.
9. Kooner, J.S., Chambers, J.C., Aguilar-Salinas, C.A., Hinds, D.A., Hyde, C.L., Warnes, G.R., Gómez-Pérez, 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., 4, 149-151.
10. Hu, S., Zhong, Y., Hao, Y., Luo, M., Zhou, Y., Guo, H., Liao, W., Wan, D., Wei, H., Gao, Y. et al. (2009) Novel rare alleles of ABCA1 are exclusively associated with extreme high-density lipoprotein-cholesterol levels among the Han Chinese. Clin. Chem. Lab. Med., 47, 1239-1245.
11. Frikke-Schmidt, R., Nordestgaard, B.G., Jensen, G.B. and Tybjaerg-Hansen, A. (2004) Genetic variation in ABC transporter A1 contributes to HDL cholesterol in the general population. J. Clin. Invest., 114, 1343-1353.
12. González-José, R., Bortolini, M.C., Santos, F.R. and Bonatto, S.L. (2008) The peopling of America: craniofacial shape variation on a continental scale and its interpretation from an interdisciplinary view. Am. J. Phys. Anthropol., 137, 175-187.
13. Kitchen, A., Miyamoto, M.M. and Mulligan, C.J. (2008) A three-stage colonization model for the peopling of the Americas. PLoS ONE, 3, e1596.
14. Fagundes, N.J.R., Kanitz, R. and Bonatto, S.L. (2008) A reevaluation of the Native American mtDNA genome diversity and its bearing on the models of early colonization of Beringia. PLoS ONE, 3, e3157.
15. Williams, R.C. and McAuley, J.E. (1992) HLA class I variation controlled for genetic admixture in the Gila River Indian community of Arizona: a model for the Paleo-Indians. Hum. Immunol., 33, 39-46.
16. Salzano, F.M. (2002) Molecular variability in Amerindians: widespread but uneven information. An. Acad. Bras. Cienc., 74, 223-263.
17. Schroeder, K.B., Jakobsson, M., Crawford, M.H., Schurr, T.G., Boca, S.M., Conrad, D.F., Tito, R.Y., Osipova, L.P., Tarskaia, L.A., Zhadanov, S.I. et al. (2009) Haplotypic background of a private allele at high frequency in the Americas. Mol. Biol. Evol., 26, 995-1016.
18. Fagundes, N.J.R., Ray, N., Beaumont, M., Neuenschwander, S., Salzano, F.M., Bonatto, S.L. and Excoffier, L. (2007) Statistical evaluation of alternative models of human evolution. Proc. Natl Acad. Sci. USA, 104, 17614-17619.
19. Fagundes, N.J.R., Kanitz, R., Eckert, R., Valls, A.C., Bogo, M.R., Salzano, F.M., Smith, D.G., Silva, W.A. Jr, Zago, M.A., Ribeiro-dos-Santos, A.K. et al. (2008) Mitochondrial population genomics supports a single pre-Clovis origin with a coastal route for the peopling of the Americas. Am. J. Hum. Genet., 8, 583-592.
20. Brunham, L.R., Singaraja, R.R., Pape, T.D., Kejariwal, A., Thomas, P.D. and Hayden, M.R. (2005) Accurate prediction of the functional significance of single nucleotide polymorphisms and mutations in the ABCA1 gene. PLoS Genet., 1, e83.
21. Clark, A.G., Glanowski, S., Nielsen, R., Thomas, P.D., Kejariwal, A., Todd, M.A., Tanenbaum, D.M., Civello, D., Lu, F., Murphy, B. et al. (2003) Inferring nonneutral evolution from human-chimp-mouse orthologous gene trios. Science, 302, 1960-1963.
22. Wang, S., Lewis, C.M., Jakobsson, M., Ramachandran, S., Ray, N., Bedoya, G., Rojas, W., Parra, M.V., Molina, J.A., Gallo, C. et al. (2007) Genetic variation and population structure in native Americans. PLoS Genet., 3, e185.
23. Hancock, A.M., Witonsky, D.B., Gordon, A.S., Eshel, G., Pritchard, J.K., Coop, G. and Di Rienzo, A. (2008) Adaptations to climate in candidate genes for common metabolic disorders. PLoS Genet., 4, e32.
24. Neel, J.V. (1962) Diabetes mellitus: a 'thrifty' genotype rendered detrimental by 'progress'? Am. J. Hum. Genet., 14, 353-362.
25. Prentice, A.M., Rayco-Solon, P. and Moore, S.E. (2005) Insights from the developing world: thrifty genotypes and thrifty phenotypes. Proc. Nutr. Soc., 64, 153-161.
26. Wells, J.C. (2009) Ethnic variability in adiposity and cardiovascular risk: the variable disease selection hypothesis. Int. J. Epidemiol., 38, 63-71.
27. Lee, C.J., Lin, H.R., Liao, C.L. and Lin, Y.L. (2008) Cholesterol effectively blocks entry of flavivirus. J. Virol., 82, 6470-6480.
28. Simons, K. and Toomre, D. (2000) Lipid rafts and signal transduction. Nat. Rev. Mol. Cell. Biol., 1, 31-39.
29. Combes, V., Coltel, N., Alibert, M., van Eck, M., Raymond, C., Juhan-Vague, I., Grau, G.E. and Chimini, G. (2005) ABCA1 gene deletion protects against cerebral malaria: potential pathogenic role of microparticles in neuropathology. Am. J. Pathol., 166, 295-302.
30. Rogers, D.J. and Randolph, S.E. (2000) The global spread of malaria in a future, warmer world. Science., 289, 1763-1766.
31. Howard, B.V., Davis, M.P., Pettitt, D.J., Knowler, W.C. and Bennett, P.H. (1983) Plasma and lipoprotein cholesterol and triglyceride concentrations in the Pima Indians: distributions differing from those of Caucasians. Circulation., 68, 714-724.
32. Clee, S.M., Kastelein, J.J., van Dam, M., Marcil, M., Roomp, K., Zwarts, K.Y., Collins, J.A., Roelants, R., Tamasawa, N., Stulc, T. et al. (2000) Age and residual cholesterol efflux affect HDL cholesterol levels and coronary artery disease in ABCA1 heterozygotes. J. Clin. Invest., 106, 1263-1270.
33. Helgason, A., Pálsson, S., Thorleifsson, G., Grant, S.F., Emilsson, V., Gunnarsdottir, S., Adeyemo, A., Chen, Y., Chen, G., Reynisdottir, I. et al. (2007) Refining the impact of TCF7L2 gene variants on type 2 diabetes and adaptive evolution. Nat. Genet., 39, 218-225.
34. Browning, J.D., Szczepaniak, L.S., Dobbins, R., Nuremberg, P., Horton, J.D., Cohen, J.C., Grundy, S.M. and Hobbs, H.H. (2004) Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology, 40, 1387-1395.
35. Guerrero, R., Vega, G.L., Grundy, S.M. and Browning, J.D. (2009) Ethic differences in hepatic steatosis: an insulin resistance paradox? Hepatology, 49, 791-801.
36. Fagot-Campagna, A., Narayan, K.M., Hanson, R.L., Imperatore, G., Howard, B.V., Nelson, R.G., Pettitt, D.J. and Knowler, W.C. (1997) Plasma lipoproteins and incidence of non-insulin-dependent diabetes mellitus in Pima Indians: protective effect of HDL cholesterol in women. Atherosclerosis, 128, 113-119.
37. Brunham, L.R., Kruit, J.K., Verchere, C.B. and Hayden, M.R. (2008) Cholesterol in islet dysfunction and type 2 diabetes. J. Clin. Invest., 118, 403-408.
38. Knowler, W.C., Bennett, P.H., Hamman, R.F. and Miller, M. (1978) Diabetes incidence and prevalence in Pima Indians: a 19-fold greater incidence than in Rochester, Minnesota. Am. J. Epidemiol., 108, 497-505.
39. Vieira-Filho, J.P., Reis, A.F., Kasamatsu, T.S., Tavares, E.F., Franco, L.J., Matioli, S.R. and Moisés, R.S. (2004) Influence of the polymorphisms Tpr64Arg in the beta 3-adrenergic receptor gene and Pro12Ala in the PPAR gamma 2 gene on metabolic syndrome-related phenotypes in an indigenous population of the Brazilian Amazon. Diabetes Care, 27, 621-622.
40. The Expert Committee on the Diagnosis Classification of Diabetes Mellitus (2003) Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Diabetes Care, 26, S5-S20.
41. Expert Panel on Detection, Evaluation and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) (2001) Executive summary of the Third Report of the National Cholesterol Education Program (NCEP). JAMA, 285, 2486-2497.
42. See, R.H., Caday-Malcolm, R.A., Singaraja, R.R., Zhou, S., Silverston, A., Huber, M.T., Moran, J., James, E.R., Janoo, R., Savill, J.M. et al. (2002) Protein kinase A site-specific phosphorylation regulates ATP-binding cassette A1 (ABCA1)-mediated phospholipid efflux. J. Biol. Chem., 277, 41835-41842.
43. Singaraja, R.R., Van Eck, M., Bissada, N., Zimetti, F., Collins, H.L., Brunham, L.R., Kang, M.H., Zannis, V.I., Chimini, G. and Hayden, M.R. (2006) Specific mutations in ABCA1 have discrete effects on ABCA1 function and lipid phenotypes both in vivo and in vitro. Circ. Res., 99, 389-397.
44. Wellington, C.L. (2002) ABCA1 mRNA and protein distribution patterns predict multiple different roles and levels of regulation. Lab. Invest., 82, 273-283.
45. Excoffier, L., Laval, G. and Schneider, S. (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol. Bioinform. Online, 1, 47-50.
46. Campbell, L. (1997) American Indian languages: the historical linguistics of Native America. Oxford University Press, New York.
47. Bandelt, H.J., Forster, P. and Rohl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol., 16, 37-48.
48. Sabeti, P.C., Reich, D.E., Higgins, J.M., Levine, H.Z., Richter, D.J., Schaffner, S.F., Gabriel, S.B., Platko, J.V., Patterson, N.J., McDonald, G.J. et al. (2002) Detecting recent positive selection in the human genome from haplotype structure. Nature, 419, 832-837.
49. Moreno-Estrada, A., Tang, K., Sikora, M., Marquès-Bonet, T., Casals, F., Navarro, A., Calafell, F., Bertranpetit, J., Stoneking, M. and Bosch, E. (2009) Interrogating 11 fast-evolving genes for signatures of recent positive selection in worldwide human populations. Mol. Biol. Evol., 26, 2285-2297.
50. Voight, B.F., Kudaravalli, S., Wen, X. and Pritchard, J.K. (2006) A map of recent positive selection in the human genome. PLoS Biol., 4, e72.
51. Pickrell, J.K., Coop, G., Novembre, J., Kudaravalli, S., Li, J.Z., Absher, D., Srinivasan, B.S., Barsh, G.S., Myers, R.M., Feldman, M.W. et al. (2009) Signals of recent positive selection in a worldwide sample of human populations. Genome Res., 19, 826-837.
52. Li, J.Z., Absher, D.M., Tang, H., Southwick, A.M., Casto, A.M., Ramachandran, S., Cann, H.M., Barsh, G.S., Feldman, M., Cavalli-Sforza, L.L. et al. (2008) Worldwide human relationships inferred from genome-wide patterns of variation. Science, 22, 1100-1104.
53. Nielsen, R., Williamson, S., Kim, Y., Hubisz, M.J., Clark, A.G. and Bustamante, C. (2005) Genomic scans for selective sweeps using SNP data. Genome Res., 15, 1566-1575.
54. Mantel, N. and Haenszel, W. (1959) Statistical aspects of the analysis of data from retrospective studies of disease. J. Natl Cancer Inst., 22, 719-748.