Genetic adaptation to high altitude in the Ethiopian highlands

Genome Biology

Volumn 13, Issue 1, 2012, Pages

  Scheinfeldt, Laura B ^a   Soi, Sameer ^a   Thompson, Simon ^a   Ranciaro, Alessia ^a   Woldemeskel, Dawit ^b   Beggs, William ^a   Lambert, Charla ^a,c   Jarvis, Joseph P ^a   Abate, Dawit ^b   Belay, Gurja ^b   Tishkoff, Sarah A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b ADDIS ABABA UNIVERSITY   (Ethiopia)

^c Simons Center for Quantitative Biology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOGLOBIN; ARNT2 PROTEIN, HUMAN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CALCIUM BINDING PROTEIN; CARRIER PROTEIN; CATION TRANSPORT PROTEIN; HYPOXIA INDUCIBLE FACTOR 1BETA; MICU1 PROTEIN, HUMAN; THYROID HORMONE RECEPTOR BETA; VAV PROTEIN; VAV3 PROTEIN, HUMAN;

ALTITUDE; ARNT2 GENE; ARTICLE; CBARA1 GENE; CONTROLLED STUDY; ETHIOPIA; EVOLUTIONARY ADAPTATION; GENE; GENE IDENTIFICATION; GENETIC ASSOCIATION; GENOTYPE; HEMOGLOBIN BLOOD LEVEL; HUMAN; MALE; SINGLE NUCLEOTIDE POLYMORPHISM; THRB GENE; VAV3 GENE; ADAPTATION; FEMALE; GENETICS; METABOLISM; METHODOLOGY;

ADAPTATION, PHYSIOLOGICAL; ALTITUDE; ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CALCIUM-BINDING PROTEINS; CATION TRANSPORT PROTEINS; ETHIOPIA; FEMALE; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HEMOGLOBINS; HUMANS; MALE; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTO-ONCOGENE PROTEINS C-VAV; THYROID HORMONE RECEPTORS BETA;

EID: 84856022397     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2012-13-1-r1     Document Type: Article

References (43)

1. Moore LG, Shriver M, Bemis L, Hickler B, Wilson M, Brutsaert T, Parra E, Vargas E. Maternal adaptation to high-altitude pregnancy: an experiment of nature - a review. Placenta 2004, 25(Suppl A):S60-71.
2. Scheinfeldt LB, Tishkoff SA. Living the high life: high-altitude adaptation. Genome Biol 2010, 11:133. 10.1186/gb-2010-11-9-133, 2965377, 20979669.
3. Moore LG. Human genetic adaptation to high altitude. High Alt Med Biol 2001, 2:257-279. 10.1089/152702901750265341, 11443005.
4. Beall CM, Decker MJ, Brittenham GM, Kushner I, Gebremedhin A, Strohl KP. An Ethiopian pattern of human adaptation to high-altitude hypoxia. Proc Natl Acad Sci USA 2002, 99:17215-17218. 10.1073/pnas.252649199, 139295, 12471159.
5. Beall CM. Andean, Tibetan, and Ethiopian patterns of adaptation to high-altitude hypoxia. Integr Comp Biol 2006, 46:18-24. 10.1093/icb/icj004, 21672719.
6. Beall CM, Song K, Elston RC, Goldstein MC. Higher offspring survival among Tibetan women with high oxygen saturation genotypes residing at 4,000 m. Proc Natl Acad Sci USA 2004, 101:14300-14304. 10.1073/pnas.0405949101, 521103, 15353580.
7. Julian CG, Wilson MJ, Lopez M, Yamashiro H, Tellez W, Rodriguez A, Bigham AW, Shriver MD, Rodriguez C, Vargas E, Moore LG. Augmented uterine artery blood flow and oxygen delivery protect Andeans from altitude-associated reductions in fetal growth. Am J Physiol Regul Integr Comp Physiol 2009, 296:R1564-1575. 10.1152/ajpregu.90945.2008, 2689835, 19244584.
8. Bigham AW, Mao X, Mei R, Brutsaert T, Wilson MJ, Julian CG, Parra EJ, Akey JM, Moore LG, Shriver MD. Identifying positive selection candidate loci for high-altitude adaptation in Andean populations. Hum Genomics 2009, 4:79-90. 2857381, 20038496.
9. Simonson TS, Yang Y, Huff CD, Yun H, Qin G, Witherspoon DJ, Bai Z, Lorenzo FR, Xing J, Jorde LB, Prchal JT, Ge R. Genetic evidence for high-altitude adaptation in Tibet. Science 2010, 329:72-75. 10.1126/science.1189406, 20466884.
10. Xu S, Li S, Yang Y, Tan J, Lou H, Jin W, Yang L, Pan X, Wang J, Shen Y, Wu B, Wang H, Jin L. A genome-wide search for signals of high-altitude adaptation in Tibetans. Mol Biol Evol 2011, 28:1003-1011. 10.1093/molbev/msq277, 20961960.
11. Yi X, Liang Y, Huerta-Sanchez E, Jin X, Cuo ZXP, Pool JE, Xu X, Jiang H, Vinckenbosch N, Korneliussen TS, Zheng H, Liu T, He W, Li K, Luo R, Nie X, Wu H, Zhao M, Cao H, Zou J, Shan Y, Li S, Yang Q, Asan, Ni P, Tian G, Xu J, Liu X, Jiang T, Wu R, Zhou G, et al. Sequencing of 50 human exomes reveals adaptation to high altitude. Science 2010, 329:75-78. 10.1126/science.1190371, 20595611.
12. Beall CM, Cavalleri GL, Deng L, Elston RC, Gao Y, Knight J, Li C, Li JC, Liang Y, McCormack M, Montgomery HE, Pan H, Robbins PA, Shianna KV, Tam SC, Tsering N, Veeramah KR, Wang W, Wangdui P, Weale ME, Xu Y, Xu Z, Yang L, Zaman MJ, Zeng C, Zhang L, Zhang X, Zhaxi P, Zheng YT. Natural selection on EPAS1 (HIF2alpha) associated with low hemoglobin concentration in Tibetan highlanders. Proc Natl Acad Sci USA 2010, 107:11459-11464. 10.1073/pnas.1002443107, 2895075, 20534544.
13. Bigham A, Bauchet M, Pinto D, Mao X, Akey JM, Mei R, Scherer SW, Julian CG, Wilson MJ, López Herráez D, Brutsaert T, Parra EJ, Moore LG, Shriver MD. Identifying signatures of natural selection in Tibetan and Andean populations using dense genome scan data. PLoS Genet 2010, 6:e1001116.
14. Weir BS. Genetic Data Analysis II: Methods for Discrete Population Genetic Data 1996, Sinauer Associates.
15. International HapMap Consortium A haplotype map of the human genome. Nature 2005, 437:1299-1320. 10.1038/nature04226, 1880871, 16255080, International HapMap Consortium.
16. Shriver MD, Kennedy GC, Parra EJ, Lawson HA, Sonpar V, Huang J, Akey JM, Jones KW. The genomic distribution of population substructure in four populations using 8,525 autosomal SNPs. Hum Genomics 2004, 1:274-286.
17. Perocchi F, Gohil VM, Girgis HS, Bao XR, McCombs JE, Palmer AE, Mootha VK. MICU1 encodes a mitochondrial EF hand protein required for Ca(2+) uptake. Nature 2010, 467:291-296. 10.1038/nature09358, 2977980, 20693986.
18. Leikauf GD, Concel VJ, Liu P, Bein K, Berndt A, Ganguly K, Jang AS, Brant KA, Dietsch M, Pope-Varsalona H, Dopico RAJ, Di YPP, Li Q, Vuga LJ, Medvedovic M, Kaminski N, You M, Prows DR. Haplotype association mapping of acute lung injury in mice implicates activin a receptor, type 1. Am J Respir Crit Care Med 2011, 183:1499-1509. 10.1164/rccm.201006-0912OC, 21297076.
19. Miah SMS, Purdy AK, Rodin NB, MacFarlane AW4, Oshinsky J, Alvarez-Arias DA, Campbell KS. Ubiquitylation of an internalized killer cell Ig-like receptor by Triad3A disrupts sustained NF-κB signaling. J Immunol 2011, 186:2959-2969. 10.4049/jimmunol.1000112, 21270397.
20. Jung Y, Isaacs JS, Lee S, Trepel J, Neckers L. Microtubule disruption utilizes an NFkappa B-dependent pathway to stabilize HIF-1alpha protein. J Biol Chem 2003, 278:7445-7452. 10.1074/jbc.M209804200, 12488445.
21. Thomas PD, Campbell MJ, Kejariwal A, Mi H, Karlak B, Daverman R, Diemer K, Muruganujan A, Narechania A. PANTHER: a library of protein families and subfamilies indexed by function. Genome Res 2003, 13:2129-2141. 10.1101/gr.772403, 403709, 12952881.
22. Voight BF, Kudaravalli S, Wen X, Pritchard JK. A map of recent positive selection in the human genome. PLoS Biol 2006, 4:e72. 10.1371/journal.pbio.0040072, 1382018, 16494531.
23. Thirunavukkarasu N, Ghosal KJ, Kukreja R, Zhou Y, Dombkowski A, Cai S, Singh BR. Microarray analysis of differentially regulated genes in human neuronal and epithelial cell lines upon exposure to type A botulinum neurotoxin. Biochem Biophys Res Commun 2011, 405:684-690. 10.1016/j.bbrc.2011.01.102, 21291863.
24. Ben Mahmoud L, Ghozzi H, Kamoun A, Hakim A, Hachicha H, Hammami S, Sahnoun Z, Zalila N, Makni H, Zeghal K. Polymorphism of the N-acetyltransferase 2 gene as a susceptibility risk factor for antituberculosis drug-induced hepatotoxicity in Tunisian patients with tuberculosis. Pathol Biol (Paris) 2011,
25. Park SG, Kang YS, Kim JY, Lee CS, Ko YG, Lee WJ, Lee K, Yeom YI, Kim S. Hormonal activity of AIMP1/p43 for glucose homeostasis. Proc Natl Acad Sci USA 2006, 103:14913-14918. 10.1073/pnas.0602045103, 1595450, 17001013.
26. Chen H, Patterson N, Reich D. Population differentiation as a test for selective sweeps. Genome Res 2010, 20:393-402. 10.1101/gr.100545.109, 2840981, 20086244.
27. Thein SL, Menzel S, Lathrop M, Garner C. Control of fetal hemoglobin: new insights emerging from genomics and clinical implications. Hum Mol Genet 2009, 18:R216-23. 10.1093/hmg/ddp401, 2758709, 19808799.
28. Zeng L, Sachdev P, Yan L, Chan JL, Trenkle T, McClelland M, Welsh J, Wang LH. Vav3 mediates receptor protein tyrosine kinase signaling, regulates GTPase activity, modulates cell morphology, and induces cell transformation. Mol Cell Biol 2000, 20:9212-9224. 10.1128/MCB.20.24.9212-9224.2000, 102179, 11094073.
29. Quevedo C, Sauzeau V, Menacho-Márquez M, Castro-Castro A, Bustelo XR. Vav3-deficient mice exhibit a transient delay in cerebellar development. Mol Biol Cell 2010, 21:1125-1139. 10.1091/mbc.E09-04-0292, 2836963, 20089829.
30. Kang HM, Zaitlen NA, Wade CM, Kirby A, Heckerman D, Daly MJ, Eskin E. Efficient control of population structure in model organism association mapping. Genetics 2008, 178:1709-1723. 10.1534/genetics.107.080101, 2278096, 18385116.
31. Semenza GL. HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J Appl Physiol 2000, 88:1474-1480.
32. Flamant F, Gauthier K, Samarut J. Thyroid hormones signaling is getting more complex: STORMs are coming. Mol Endocrinol 2007, 21:321-333.
33. Semenza GL. Hypoxia-inducible factor 1: regulator of mitochondrial metabolism and mediator of ischemic preconditioning. Biochim Biophys Acta 2011, 1813:1263-1268. 10.1016/j.bbamcr.2010.08.006, 20732359.
34. Rey S, Semenza GL. Hypoxia-inducible factor-1-dependent mechanisms of vascularization and vascular remodelling. Cardiovasc Res 2010, 86:236-242. 10.1093/cvr/cvq045, 2856192, 20164116.
35. Lewis P. Ethnologue: Languages of the World 2009, Dallas, TX: SIL International, 16.
36. Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 1988, 16:1215. 10.1093/nar/16.3.1215, 334765, 3344216.
37. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, de Bakker PIW, Daly MJ, Sham PC. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 2007, 81:559-575. 10.1086/519795, 1950838, 17701901.
38. McVean G. A genealogical interpretation of principal components analysis. PLoS Genet 2009, 5:e1000686. 10.1371/journal.pgen.1000686, 2757795, 19834557.
39. R Development Core Team R: A Language and Environment for Statistical Computing 2009, R Foundation for Statistical Computing, R Development Core Team.
40. Scheet P, Stephens M. A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet 2006, 78:629-644. 10.1086/502802, 1424677, 16532393.
41. McVean GAT, Myers SR, Hunt S, Deloukas P, Bentley DR, Donnelly P. The fine-scale structure of recombination rate variation in the human genome. Science 2004, 304:581-584. 10.1126/science.1092500, 15105499.
42. Fujita PA, Rhead B, Zweig AS, Hinrichs AS, Karolchik D, Cline MS, Goldman M, Barber GP, Clawson H, Coelho A, Diekhans M, Dreszer TR, Giardine BM, Harte RA, Hillman-Jackson J, Hsu F, Kirkup V, Kuhn RM, Learned K, Li CH, Meyer LR, Pohl A, Raney BJ, Rosenbloom KR, Smith KE, Haussler D, Kent WJ. The UCSC Genome Browser database: update 2011. Nucleic Acids Res 2011, 39:D876-882. 10.1093/nar/gkq963, 3242726, 20959295.
43. Myers S, Bottolo L, Freeman C, McVean G, Donnelly P. A fine-scale map of recombination rates and hotspots across the human genome. Science 2005, 310:321-324. 10.1126/science.1117196, 16224025.