Differential positive selection of malaria resistance genes in three indigenous populations of Peninsular Malaysia

Human Genetics

Volumn 134, Issue 4, 2015, Pages 375-392

  Liu, Xuanyao ^a   Yunus, Yushimah ^b   Lu, Dongsheng ^c   Aghakhanian, Farhang ^d   Saw, Woei Yuh ^a   Deng, Lian ^c   Ali, Mohammad ^a   Wang, Xu ^a   Ghazali, Fadzilah ^b   Abdul Rahman, Thuhairah ^b   Shaari, Shahrul Azlin ^b   Salleh, Mohd Zaki ^b   Phipps, Maude E ^d   Ong, Rick Twee Hee ^a   Xu, Shuhua ^c   Teo, Yik Ying ^a,e   Hoh, Boon Peng ^b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b UNIVERSITI TEKNOLOGI MARA   (Malaysia)

^c Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^d MONASH UNIVERSITY MALAYSIA   (Malaysia)

^e GENOME INSTITUTE OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; ETHNIC GROUP; FEMALE; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC HETEROGENEITY; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HAPLOTYPE MAP; HUMAN; MALARIA; MALE; NATURAL SELECTION; ORANG ASLI; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; URBAN POPULATION; ADAPTATION; DISEASE RESISTANCE; ETHNOLOGY; GENETIC SELECTION; GENETICS; MALAYSIA; POPULATION GROUP;

CADHERIN; FAS ANTIGEN; FAS PROTEIN, HUMAN; H-CADHERIN; HEME OXYGENASE 1; HMOX1 PROTEIN, HUMAN; INDUCIBLE NITRIC OXIDE SYNTHASE; LYMPHOTOXIN; NOS2 PROTEIN, HUMAN; TRANSCRIPTOME; TUMOR NECROSIS FACTOR ALPHA;

ADAPTATION, BIOLOGICAL; ANTIGENS, CD95; CADHERINS; DISEASE RESISTANCE; GENOME-WIDE ASSOCIATION STUDY; HEME OXYGENASE-1; HUMANS; LYMPHOTOXIN-ALPHA; MALARIA; MALAYSIA; NITRIC OXIDE SYNTHASE TYPE II; POLYMORPHISM, SINGLE NUCLEOTIDE; POPULATION GROUPS; SELECTION, GENETIC; TRANSCRIPTOME; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84925484528     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-014-1525-2     Document Type: Article

References (77)

1. Agarwal A, Guindo A, Cissoko Y, Taylor JG, Coulibaly D, Kone A, Kayentao K, Djimde A, Plowe CV, Doumbo O, Wellems TE, Diallo D (2000) Hemoglobin C associated with protection from severe malaria in the Dogon of Mali, a West African population with a low prevalence of hemoglobin S. Blood 96:2358–2363.
2. Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664. doi:10.1101/gr.094052.109.
3. Altshuler DM, Gibbs RA, Peltonen L, Dermitzakis E, Schaffner SF, Yu F, Bonnen PE, de Bakker PI, Deloukas P, Gabriel SB, Gwilliam R, Hunt S, Inouye M, Jia X, Palotie A, Parkin M, Whittaker P, Chang K, Hawes A, Lewis LR, Ren Y, Wheeler D, Muzny DM, Barnes C, Darvishi K, Hurles M, Korn JM, Kristiansson K, Lee C, McCarrol SA, Nemesh J, Keinan A, Montgomery SB, Pollack S, Price AL, Soranzo N, Gonzaga-Jauregui C, Anttila V, Brodeur W, Daly MJ, Leslie S, McVean G, Moutsianas L, Nguyen H, Zhang Q, Ghori MJ, McGinnis R, McLaren W, Takeuchi F, Grossman SR, Shlyakhter I, Hostetter EB, Sabeti PC, Adebamowo CA, Foster MW, Gordon DR, Licinio J, Manca MC, Marshall PA, Matsuda I, Ngare D, Wang VO, Reddy D, Rotimi CN, Royal CD, Sharp RR, Zeng C, Brooks LD, McEwen JE (2010) Integrating common and rare genetic variation in diverse human populations. Nature 467:52–58. doi:10.1038/nature09298.
4. Ang KC, Ngu MS, Reid KP, Teh MS, Aida ZS, Koh DX, Berg A, Oppenheimer S, Salleh H, Clyde MM, Md-Zain BM, Canfield VA, Cheng KC (2012) Skin color variation in Orang Asli tribes of Peninsular Malaysia. PLoS One 7:e42752. doi:10.1371/journal.pone.0042752.
5. Baer A (1999) Health, disease and survival: a biomedical and genetic analysis of the Orang Asli of Malaysia. Center for Orang Asli Concerns, Kuala Lumpur.
6. Baer A, Lie-Injo LE, Welch QB, Lewis AN (1976) Genetic factors and malaria in the Temuan. Am J Hum Genet 28:179–188.
7. Band G, Le QS, Jostin L, Pirinen M, Kivinen K, Jallow M et al (2012) Imputation-based meta-analysis of severe malaria in three African populations. PLoS Genet 9(5):e1003509. doi:10.1371/journal.pgen.1003509.
8. Barker G, Barton H, Bird M, Daly P, Datan I et al (2007) The ‘human revolution’ in lowland tropical Southeast Asia: the antiquity and behavior of anatomically modern humans at Niah Cave (Sarawak, Borneo). J Hum Evol 52:243–261.
9. Bellwood P (2007) Prehistory of the Indo-Malaysian archipelago, 4th edn. ANU E Press, Canberra.
10. Bidere N, Su HC, Lenardo MJ (2006) Genetic disorders of programmed cell death in the immune system. Annu Rev Immunol 24:321–352.
11. Browning SR, Browning BL (2007) Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet 81:1084–1097.
12. Bustamante CD, Burchard EG, De La Vega FM (2011) Genomics for the world. Nature 475:163–165.
13. Campbell MC, Tishkoff SA (2008) African Genetic Diversity: implications for human demographic history, modern human origins, and complex disease mapping. Annu Rev Genomics Hum Genet 9:403–433.
14. Clark TG, Fry AE, Auburn S, Campino S, Diakite M, Green A, Richardson A, Teo YY, Small K, Wilson J, Jallow M, Sisay-Joof F, Pinder M, Sabeti P, Kwiatkowski DP, Rockett KA (2009) Allelic heterogeneity of G6PD deficiency in West Africa and severe malaria susceptibility. Eur J Hum Genet 17:1080–1085. doi:10.1038/ejhg.2009.8.
15. Comuzzie AG, Cole SA, Laston SL, Voruganti VS, Haack K et al (2012) Novel Genetic Loci Identified for the Pathophysiology of Childhood Obesity in the Hispanic Population. PLoS One 7(12):e51954. doi:10.1371/journal.pone.0051954.
16. Dastani Z, Hivert MF, Timpson N, Perry JR, Yuan X et al (2012) Novel loci for adiponectin levels and their influence on type 2 diabetes and metabolic traits: a multi-ethnic meta-analysis of 45,891 individuals. PLoS Genet 8:e1002607. doi:10.1371/journal.pgen.1002607.
17. Delahaye NF, Coltel N, Puthier D, Barbier M, Benech P, Joly F, Iraqi FA, Grau GE, Nguyen C, Rihet P (2007) Gene expression analysis reveals early changes in several molecular pathways in cerebral malaria-susceptible mice versus cerebral malaria-resistant mice. BMC Genom 8:452. doi:10.1186/1471-2164-8-452.
18. Deng L, Hoh BP, Lu D, Fu R, Phipps ME, Li S, Nur-Shafawati AR, Hatin WI, Ismail E, Siti Shuhada M, Jin L, Zilfalil BA, Marshall CR, Scherer SW, Al-Mulla F, Shuhua XuS (2014) The population genomic landscape of human genetic structure, admixture history and local adaptation in Peninsular Malaysia. DOI, Huma Genetic. doi:10.1007/s00439-014-1459-8.
19. Eng LI, Baer A, Lewis AN, Welch QB (1973) Hemoglobin Constant Spring (slow-moving hemoglobin X components) and hemoglobin e in Malayan aborigines. Am J Hum Genet 25:382–387.
20. Faucher JF, Milama EN, Missinou MA et al (2002) The impact of malaria on common lipid parameters. Parasitol Res 88:1040–1043.
21. Field L, Tobias R, Thomson G, Plon S (1996) Susceptibility to insulin-dependent diabetes mellitus maps to a locus (IDDM11) on human chromosome 14q24.3–q31. Genomics 33:1–8.
22. Fox CS, Liu Y, White CC, Feitosa M, Smith AV et al (2012) Genome-wide association for abdominal subcutaneous and visceral adipose reveals a novel locus for visceral fat in women. PLoS Genet 8(5):e1002695. doi:10.1371/journal.pgen.1002695.
23. Franke B, Faraone SV, Asherson P, Buitelaar J, Bau CHD, Ramos-Quiroga JA, Mick E, Grevet EH, Johansson S, Haavik J et al (2012) The genetics of attention deficit/hyperactivity disorder in adults, a review. Mol Psychiatry 17:960–987.
24. Fumagalli M, Sironi M (2014) Human genome variability, natural selection and infectious diseases. Curr Opin Immunol 30:9–16.
25. Fumagalli M, Sironi M, Pozzoli U, Ferrer-Admettla A, Pattini L et al (2011) Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution. PLoS Genet 7(11):e1002355. doi:10.1371/journal.pgen.1002355.
26. Hamblin MT, Di Rienzo A (2000) Detection of the signature of natural selection in humans: evidence from the Duffy blood group locus. Am J Hum Genet 66:1669–1679. doi:10.1086/302879.
27. Hamblin MT, Thompson EE, Di Rienzo A (2002) Complex signatures of natural selection at the Duffy blood group locus. Am J Hum Genet 70:369–383. doi:10.1086/338628.
28. Hanchard N, Elzein A, Trafford C, Rockett K, Pinder M, Jallow M, Harding R, Kwiatkowski D, McKenzie C (2007) Classical sickle beta-globin haplotypes exhibit a high degree of long-range haplotype similarity in African and Afro-Caribbean populations. BMC Genet 8:52. doi:10.1186/1471-2156-8-52.
29. Harper K, Armelagos G (2011) The changing disease-scape in the third epidemiological transition. Int J Environ Res Public Health 7:675–697.
30. Hatin WI, Nur-Shafawati AR, Zahri M et al (2011) Population genetic structure of Peninsular Malaysia Malay sub-ethnic groups. Plos One 6:e18312.
31. Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J (2008) Helminth infections: the great neglected tropical diseases. J Clin Invest 118:1311–1321. doi:10.1172/JCI34261.
32. Jakobsson M, Scholz SW, Scheet P, Gibbs JR, VanLiere JM, Fung HC, Szpiech ZA, Degnan JH, Wang K, Guerreiro R, Bras JM, Schymick JC, Hernandez DG, Traynor BJ, Simon-Sanchez J, Matarin M, Britton A, van de Leemput J, Rafferty I, Bucan M, Cann HM, Hardy JA, Rosenberg NA, Singleton AB (2008) Genotype, haplotype and copy-number variation in worldwide human populations. Nature 451:998–1003. doi:10.1038/nature06742.
33. Jamieson SE, Miller EN, Black GF, Peacock CS, Cordell HJ, Howson JM, Shaw MA, Burgner D, Xu W, Lins-Lainson Z, Shaw JJ, Ramos F, Silveira F, Blackwell JM (2004) Evidence for a cluster of genes on chromosome 17q11-q21 controlling susceptibility to tuberculosis and leprosy in Brazilians. Genes Immun 5:46–57.
34. Jarvis JP, Scheinfeldt LB, Soi S, Lambert C, Omberg L et al (2012) Patterns of ancestry, signatures of natural selection, and genetic association with stature in western African pygmies. PLoS Genet 8(4):e1002641. doi:10.1371/journal.pgen.1002641.
35. Jha AN, Singh VK, Kumari N, Singh A, Antony J, van Tong H, Singh S, Pati SS, Patra PK, Singh R, Toan NL, le Song H, Assaf A, Messias-Reason IJ, Velavan TP, Singh L, Thangaraj K (2012) IL-4 haplotype -590T, -34T and intron-3 VNTR R2 is associated with reduced malaria risk among ancestral indian tribal populations. PLoS One 7:e48136. doi:10.1371/journal.pone.0048136.
36. Kwiatkowski DP (2005) How malaria has affected the human genome and what human genetics can teach us about malaria. Am J Hum Genet 77: 171–92. doi:10.1086/432519.
37. Kwiatkowski DP, Luoni G (2006) Host genetic factors in resistance and susceptibility to malaria. Parassitologia 48:450–467.
38. Lee JH, Shin D-J, Park S, Kang S-M, Jang Y, Lee S-H (2013) Association between CDH13 Variants and Cardiometabolic and Vascular Phenotypes in a Korean Population. Yonsei Med J 54(6):1305–1312.
39. Li J, Liu J, Zhao L, Ma Y, Jia M, Lu T, Ruan Y, Li Q, Yue W, Zhang D, Lifang Wang L (2013) Association study between genes in Reelin signaling pathway and autism identifies DAB1 as a susceptibility gene in a Chinese Han population. Prog Neuropsychopharmacol Biol Psychiatry 44(2013):226–232.
40. Liu X, Ong RT, Pillai EN, Elzein AM, Small KS, Clark TG, Kwiatkowski DP, Teo YY (2013) Detecting and characterizing genomic signatures of positive selection in global populations. Am J Hum Genet. doi:10.1016/j.ajhg.2013.04.021.
41. Liu X, Saw W-Y, Ali M, Rick Ong T-H, Teo Y-Y (2014) Evaluating the possibility of detecting evidence of positive selection across Asia with sparse genotype data from the HUGO Pan-Asian SNP Consortium. BMC Genom 15:332.
42. Lokossou AG, Dechavanne C, Bouraïma A, Courtin D, Le Port A, Ladékpo R, Noukpo J, Bonou D, Ahouangninou C, Sabbagh A, Fayomi B, Massougbodji A, Garcia A, Migot-Nabias F (2013) Association of IL-4 and IL-10 maternal haplotypes with immune responses to P. falciparum in mothers and newborns. BMC Infect Dis. doi: 10.1186/1471-2334-13-215.
43. Luoni G, Verra F, Arca B, Sirima BS, Troye-Blomberg M, Coluzzi M, Kwiatkowski D, Modiano D (2001) Antimalarial antibody levels and IL4 polymorphism in the Fulani of West Africa. Genes Immun 2:411–414. doi:10.1038/sj.gene.6363797.
44. Macaulay V, Hill C, Achilli A, Rengo C, Clarke D et al (2005) Single, rapid coastal settlement of Asia revealed by analysis of complete mitochondrial genomes. Science 308:1034–1036.
45. Malaria Genomic Epidemiology Network (2014) Reappraisal of known malaria resistance loci in a large multicenter study: doi:10.1038/ng.2107.
46. Mangano VD, Modiano D (2014) An evolutionary perspective of how infection drives human genome diversity: the case of malaria. Curr Opin Immunol 30:39–47.
47. Manning AK, Hilvert MF, Scott RA, Grimsby JL, Bouatia-Naji N, Chen H et al (2012) A genome-wide approach accounting for body mass index identifies genetic variants influencing fasting glycemic traits and insulin resistance. Nat Genet 44:659–669.
48. Meyer CG, Calixto Fernandes MH, Intemann CD, Kreuels B, Kobbe R, Kreuzberg C, Ayim M, Ruether A, Loag W, Ehmen C, Adjei S, Adjei O, Horstmann RD, May J (2011) IL3 variant on chromosomal region 5q31-33 and protection from recurrent malaria attacks. Hum Mol Genet 20:1173–1181. doi:10.1093/hmg/ddq562.
49. Modiano D, Luoni G, Sirima BS, Simpore J, Verra F, Konate A, Rastrelli E, Olivieri A, Calissano C, Paganotti GM, D’Urbano L, Sanou I, Sawadogo A, Modiano G, Coluzzi M (2001) Haemoglobin C protects against clinical Plasmodium falciparum malaria. Nature 414:305–308. doi:10.1038/35104556.
50. Mokhtar SS, Marshall CR, Phipps ME, Thiruvahindrapuram B, Lionel AC et al (2014) Novel population specific autosomal copy number variation and its functional analysis amongst negritos from Peninsular Malaysia. PLoS One 9(6):e100371. doi:10.1371/journal.pone.0100371.
51. Nandi S, Ma L, Denis M, Karwatsky J, Li Z, Jiang XC, Zha X (2009) ABCA1-mediated cholesterol efflux generates microparticles in addition to HDL through processes governed by membrane rigidity. J Lipid Res 50:456–466.
52. Ohashi J, Naka I, Patarapotikul J, Hananantachai H, Brittenham G, Looareesuwan S, Clark AG, Tokunaga K (2004) Extended linkage disequilibrium surrounding the hemoglobin E variant due to malarial selection. Am J Hum Genet 74:1198–1208. doi:10.1086/421330.
53. Org E, Eyheramendy S, Juhanson P, Gieger C, Lichtner P, Klopp N et al (2009) Genome-wide scan identifies CDH13 as a novel susceptibility locus contributing to blood pressure determination in two European populations. Hum Mol Genet 18:2288–2296.
54. Panda AK, Panda M, Tripathy R, Pattanaik SS, Ravindran B, Das BK (2012) Complement receptor 1 variants confer protection from severe malaria in Odisha, India. PLoS One 7:e49420. doi:10.1371/journal.pone.0049420.
55. Pickrell JK, Coop G, Novembre J, Kudaravalli S, Li JZ, Absher D, Srinivasan BS, Barsh GS, Myers RM, Feldman MW, Pritchard JK (2009) Signals of recent positive selection in a worldwide sample of human populations. Genome Res 19: 826–37. doi: 10.1101/gr.087577.108.
56. Pozzoli U, Fumagalli M, Cagliani R, Comi GP, Bresolin N, Clerici M, Sironi M (2010) The role of protozoa-driven selection in shaping human genetic variability. Trends Genet 26:95–99.
57. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38: 904–9. doi:10.1038/ng1847.
58. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81: 559–75. doi:10.1086/519795.
59. Qian W, Deng L, Lu D, Xu S (2013) Genome-wide landscapes of human local adaptation in asia. PLoS One 8:e54224.
60. Rout R, Dhangadamajhi G, Mohapatra BN, Kar SK, Ranjit M (2011) High CR1 level and related polymorphic variants are associated with cerebral malaria in eastern-India. Infect Genet Evol 11:139–144. doi:10.1016/j.meegid.2010.09.009.
61. Ruwende C, Khoo SC, Snow RW, Yates SN, Kwiatkowski D, Gupta S, Warn P, Allsopp CE, Gilbert SC, Peschu N et al (1995) Natural selection of hemi- and heterozygotes for G6PD deficiency in Africa by resistance to severe malaria. Nature 376:246–249. doi:10.1038/376246a0.
62. Sabeti PC, Varilly P, Fry B, Lohmueller J, Hostetter E, Cotsapas C, Xie X, Byrne EH, McCarroll SA, Gaudet R, Schaffner SF, Lander ES, Frazer KA, Ballinger DG, Cox DR, Hinds DA, Stuve LL, Gibbs RA, Belmont JW, Boudreau A, Hardenbol P, Leal SM, Pasternak S, Wheeler DA, Willis TD, Yu F, Yang H, Zeng C, Gao Y, Hu H, Hu W, Li C, Lin W, Liu S, Pan H, Tang X, Wang J, Wang W, Yu J, Zhang B, Zhang Q, Zhao H, Zhou J, Gabriel SB, Barry R, Blumenstiel B, Camargo A, Defelice M, Faggart M, Goyette M, Gupta S, Moore J, Nguyen H, Onofrio RC, Parkin M, Roy J, Stahl E, Winchester E, Ziaugra L, Altshuler D, Shen Y, Yao Z, Huang W, Chu X, He Y, Jin L, Liu Y, Sun W, Wang H, Wang Y, Xiong X, Xu L, Waye MM, Tsui SK, Xue H, Wong JT, Galver LM, Fan JB, Gunderson K, Murray SS, Oliphant AR, Chee MS, Montpetit A, Chagnon F, Ferretti V, Leboeuf M, Olivier JF, Phillips MS, Roumy S, Sallee C, Verner A, Hudson TJ, Kwok PY, Cai D, Koboldt DC, Miller RD, Pawlikowska L, Taillon-Miller P, Xiao M, Tsui LC et al (2007) Genome-wide detection and characterization of positive selection in human populations. Nature 449:913–918. doi:10.1038/nature06250.
63. Sahu U, Mohapatra BN, Kar SK, Ranjit M (2013) Promoter Polymorphisms in the ATP Binding Cassette Transporter Gene Influence Production of Cell-Derived Microparticles and Are Highly Associated with Susceptibility to Severe Malaria in Humans. Infect Immun 81:1287–1294.
64. Sambo MR, Trovoada MJ, Benchimol C, Quinhentos V, Goncalves L, Velosa R, Marques MI, Sepulveda N, Clark TG, Mustafa S, Wagner O, Coutinho A, Penha-Goncalves C (2010) Transforming growth factor beta 2 and heme oxygenase 1 genes are risk factors for the cerebral malaria syndrome in Angolan children. PLoS One 5:e11141. doi:10.1371/journal.pone.0011141.
65. Schuldt K, Kretz CC, Timmann C, Sievertsen J, Ehmen C et al (2011) A 2436C. A polymorphism in the human fas gene promoter associated with severe childhood malaria. PLoS Genet 7(5):e1002066. doi:10.1371/journal.pgen.1002066.
66. Shriver MD, Kennedy GC, Parra EJ, Lawson HA, Sonpar V, Huang J, Akey JM, Jones KW (2004) The genomic distribution of population substructure in four populations using 8,525 autosomal SNPs. Hum Genomics 1:274–286.
67. Strasser A, Jost PJ, Nagata S (2009) The many roles of FAS receptor signaling in the immune system. Immunity 30:180–192.
68. Stringer CB, Andrews P (1998) Genetic and fossil evidence for the origin of modern humans. Science 239:1263–1268.
69. Takeuchi T, Adachi Y, Furihata YOM (2007) Adiponectin receptors, with special focus on the role of the third receptor, T-cadherin, in vascular disease. Med Mol Morphol 40:115–120.
70. Teo YY, Sim X, Ong RT, Tan AK, Chen J, Tantoso E, Small KS, Ku CS, Lee EJ, Seielstad M, Chia KS (2009) Singapore Genome Variation Project: a haplotype map of three Southeast Asian populations. Genome Res 19:2154–2162. doi:10.1101/gr.095000.109.
71. The HUGO Pan-Asian SNP Consortium (2009) Mapping human genetic diversity in Asia. Science 326:1541–1545.
72. Vafa M, Maiga B, Berzins K, Hayano M, Bereczky S, Dolo A, Daou M, Arama C, Kouriba B, Farnert A, Doumbo OK, Troye-Blomberg M (2007) Associations between the IL-4 -590 T allele and Plasmodium falciparum infection prevalence in asymptomatic Fulani of Mali. Microbes Infect 9:1043–1048. doi:10.1016/j.micinf.2007.04.011.
73. Velez Edwards DR, Naj AC, Monda K, North KE, Neuhouser M, Magvanjav O, Kusimo I, Vitolins MZ, Manson JE, O’Sullivan MJ, Rampersaud E, Edwards TL (2012) Gene-environment interactions and obesity traits among postmenopausal African–American and Hispanic women in the Women’s Health Initiative SHARe Study. Hum Genet 132:323–336.
74. Verbrugghe P, Bouwer S, Wiltshire S, Carter K, Chandler D, Cooper M, Morar B, Razif MFM, Henders A, Badcock JC, Dragovic M, Carr V, Almeida OP, Flicker L, Montgomery G, Jablensky A, Kalaydjieva L (2012) Impact of the reelin signaling cascade (ligands–receptors–adaptor complex) on cognition in schizophrenia. Am J Med Genet Part B 159B:392–404.
75. Visser BJ, Wieten RW, Nagel IM, Grobusch MP (2013) Serum lipids and lipoproteins in malaria - a systematic review and meta-analysis. Malar J. 7(12):442. doi:10.1186/1475-2875-12-442.
76. Voight BF, Kudaravalli S, Wen X, Pritchard JK (2006) A map of recent positive selection in the human genome. PLoS Biol 4:e72. doi:10.1371/journal.pbio.0040072.
77. Wee YC, Tan KL, Kuldip K, Tai KS, George E, Tan PC, Chia P, Subramaniam R, Yap SF, Tan JA (2008) Alpha-thalassaemia in association with beta-thalassaemia patients in Malaysia: a study on the co-inheritance of both disorders. Community Genet 11:129–134. doi:10.1159/000113874.