Natural selection on EPAS1 (HIF2α) associated with low hemoglobin concentration in Tibetan highlanders

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 25, 2010, Pages 11459-11464

  Beall, Cynthia M ^a   Cavalleri, Gianpiero L ^b   Deng, Libin ^c,q   Elston, Robert C ^a   Gao, Yang ^c   Knight, Jo ^d,e   Li, Chaohua ^c   Li, Jiang Chuan ^f   Liang, Yu ^g   McCormack, Mark ^b   Montgomery, Hugh E ^h   Pan, Hao ^c   Robbins, Peter A ⁱ   Shianna, Kevin V ^j   Tam, Siu Cheung ^k   Tsering, Ngodrop ^l   Veeramah, Krishna R ^m   Wang, Wei ^g   Wangdui, Puchung ^l   Weale, Michael E ^d   Xu, Yaomin ⁿ   Xu, Zhe ^c   Yang, Ling ^g   Zaman, M Justin ^o   Zeng, Changqing ^c   Zhang, Li ⁿ   Zhang, Xianglong ^c   Zhaxi, Pingcuo ^g,r   Zheng, Yong Tang ^p   more..

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b BEAUMONT HOSPITAL   (Ireland)

^c Chinese Academy of Sciences and China National Center for Bioinformation   (China)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e GUY'S AND ST THOMAS' NHS FOUNDATION TRUST   (United Kingdom)

^f Yunnan Research Institute of Family Planning   (China)

^g BGI SHENZHEN   (China)

^h ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

ⁱ UNIVERSITY OF OXFORD   (United Kingdom)

^j DUKE UNIVERSITY   (United States)

^k CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^l Tibet Academy of Agriculture and Animal Sciences   (China)

^m UNIVERSITY OF CALIFORNIA   (United States)

ⁿ LERNER RESEARCH INSTITUTE   (United States)

^o UNIVERSITY COLLEGE LONDON   (United Kingdom)

^p KUNMING INSTITUTE OF ZOOLOGY   (China)

^q NANCHANG UNIVERSITY   (China)

^r People's Hospital of Tibet Autonomous Region   (China)

more..

Author keywords

Chronic mountain sickness; High altitude; Human genome variation; Hypoxia; Hypoxia inducible factor

Indexed keywords

HEMOGLOBIN; HYPOXIA INDUCIBLE FACTOR 2ALPHA; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ENDOTHELIAL PAS DOMAIN CONTAINING PROTEIN 1; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1;

ALTITUDE DISEASE; ARTICLE; CHINA; CONTROLLED STUDY; FEMALE; GENE FREQUENCY; GENE FUNCTION; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; GEOGRAPHIC DISTRIBUTION; HAPLOTYPE MAP; HEMOGLOBIN BLOOD LEVEL; HETEROZYGOTE; HOMOZYGOTE; HUMAN; INDIGENOUS PEOPLE; MAJOR CLINICAL STUDY; MALE; NATURAL SELECTION; PHENOTYPE; PRIORITY JOURNAL; SEX DIFFERENCE; SINGLE NUCLEOTIDE POLYMORPHISM; ALLELE; ALTITUDE; ANOXIA; GENETIC SELECTION; GENETICS; HUMAN GENOME; METABOLISM; PHYSIOLOGY;

ALLELES; ALTITUDE; ALTITUDE SICKNESS; ANOXIA; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; GENETIC VARIATION; GENOME, HUMAN; HEMOGLOBINS; HOMOZYGOTE; HUMANS; LINKAGE DISEQUILIBRIUM; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC; TIBET;

EID: 77954926596     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1002443107     Document Type: Article

References (59)

1. Zhao M, et al. (2009) Mitochondrial genome evidence reveals successful Late Paleolithic settlement on the Tibetan Plateau. Proc Natl Acad Sci USA 106:21230-21235.
2. Aldenderfer M (2003) Moving up in the world: Archaeologists seek to understand how and when people came to occupy the Andean and Tibetan plateaus. Am Sci 91:542-549.
3. Wu T, Miao C (2002) High altitude heart disease in children in Tibet. High Alt Med Biol 3:323-325.
4. León-Velarde F, et al. (2005) Consensus statement on chronic and subacute high altitude diseases. High Alt Med Biol 6:147-157.
5. Wu T (2004) Life on the high Tibetan plateau. High Alt Med Biol 5:1-2.
6. Julian CG, Wilson MJ, Moore LG (2009) Evolutionary adaptation to high altitude: A view from in utero. Am J Hum Biol 21:614-622.
7. Monge C (1973) Acclimatization in the Andes (Johns Hopkins University Press, Baltimore).
8. Moore LG, Young D, McCullough RE, Droma T, Zamudio S (2001) Tibetan protection from intrauterine growth restriction (IUGR) and reproductive loss at high altitude. Am J Hum Biol 13:635-644. (Pubitemid 32771407)
9. Moore LG, Zamudio S, Zhuang J, Sun S, Droma T (2001) Oxygen transport in tibetan women during pregnancy at 3,658 m. Am J Phys Anthropol 114:42-53. (Pubitemid 32047317)
10. Monge-M C, Encinas E, Heraud C, Hurtado A (1928) La Enfermedad de los Andes (Sindromes Eritemicos) (Imprenta Americana, Lima).
11. Pei SX, et al. (1989) Chronic mountain sickness in Tibet. Q J Med 71:555-574.
12. Beall CM (2007) Two routes to functional adaptation: Tibetan and Andean high-altitude natives. Proc Natl Acad Sci USA 104 (Suppl 1):8655-8660.
13. Beall CM (2002) Biodiversity of Human Populations in Mountain Environments. Mountain Biodiversity: A Global Assessment, eds Korner C, Spehn EM (The Parthenon Publishing Group, New York), pp 199-210.
14. Winslow RM, et al. (1989) Different hematologic responses to hypoxia in Sherpas and Quechua Indians. J Appl Physiol 66:1561-1569.
15. Beall CM, et al. (1998) Hemoglobin concentration of high-altitude Tibetans and Bolivian Aymara. Am J Phys Anthropol 106:385-400.
16. Beall CM (2002) Biodiversity of Human Populations in Moutain Environments. Mountain Biodiversity: A Global Assessment, eds Korner C, Spehn EM (The Parthenon Publishing Group, New York), pp 199-210.
17. Garruto RM, et al. (2003) Hematological differences during growth among Tibetans and Han Chinese born and raised at high altitude in Qinghai, China. Am J Phys Anthropol 122:171-183.
18. Ward MP, Milledge JS, West JB (1995) High Altitude Medicine and Physiology (Chapman and Hall Medical, London).
19. Zhuang J, et al. (1996) Smaller alveolar-arterial O2 gradients in Tibetan than Han residents of Lhasa (3658 m). Respir Physiol 103:75-82. (Pubitemid 26049037)
20. Moore LG, et al. (1992) Are Tibetans better adapted? Int J Sports Med 13(Suppl 1): S86-S88.
21. Droma T, et al. (1991) Increased vital and total lung capacities in Tibetan compared to Han residents of Lhasa (3,658 m). Am J Phys Anthropol 86:341-351.
22. 2 uptakes and vital capacities in Tibetan than Han residents of Lhasa. Respir Physiol 79:151-161.
23. Zhuang J, et al. (1993) Hypoxic ventilatory responsiveness in Tibetan compared with Han residents of 3,658 m. J Appl Physiol 74:303-311. (Pubitemid 23059761)
24. Chi JT, et al. (2006) Gene expression programs in response to hypoxia: Cell type specificity and prognostic significance in human cancers. PLoS Med 3:e47.
25. Rankin EB, et al. (2007) Hypoxia-inducible factor-2 (HIF-2) regulates hepatic erythropoietin in vivo. J Clin Invest 117:1068-1077.
26. Su B, et al. (2000) Y chromosome haplotypes reveal prehistorical migrations to the Himalayas. Hum Genet 107:582-590.
27. Qian Y, et al. (2000) Multiple origins of Tibetan Y chromosomes. Hum Genet 106:453-454.
28. Gayden T, et al. (2009) Genetic insights into the origins of Tibeto-Burman populations in the Himalayas. J Hum Genet 54:216-223.
29. Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: Analysis and visualization of LD and haplotype maps. Bioinformatics 21:263-265. (Pubitemid 40202029)
30. Devlin B, Roeder K, Wasserman L (2001) Genomic control, a new approach to genetic-based association studies. Theor Popul Biol 60:155-166. (Pubitemid 34235086)
31. Benyamin B, et al. (2009) Common variants in TMPRSS6 are associated with iron status and erythrocyte volume. Nat Genet 41:1173-1175.
32. Chambers JC, et al. (2009) Genome-wide association study identifies variants in TMPRSS6 associated with hemoglobin levels. Nat Genet 41:1170-1172.
33. Ganesh SK, et al. (2009) Multiple loci influence erythrocyte phenotypes in the CHARGE Consortium. Nat Genet 41:1191-1198.
34. Soranzo N, et al. (2009) A genome-wide meta-analysis identifies 22 loci associated with eight hematological parameters in the HaemGen consortium. Nat Genet 41:1182-1190.
35. Bigham AW, et al. (2009) Identifying positive selection candidate loci for high-altitude adaptation in Andean populations. Hum Genomics 4:79-90.
36. Beall CM, Blangero J, Williams-Blangero S, Goldstein MC (1994) Major gene for percent of oxygen saturation of arterial hemoglobin in Tibetan highlanders. Am J Phys Anthropol 95:271-276. (Pubitemid 24332502)
37. Percy MJ, et al. (2008) A gain-of-function mutation in the HIF2A gene in familial erythrocytosis. N Engl J Med 358:162-168.
38. Percy MJ, et al. (2008) Novel exon 12 mutations in the HIF2A gene associated with erythrocytosis. Blood 111:5400-5402.
39. Gale DP, Harten SK, Reid CDL, Tuddenham EGD, Maxwell PH (2008) Autosomal dominant erythrocytosis and pulmonary arterial hypertension associated with an activating HIF2 α mutation. Blood 112:919-921.
40. Martini M, et al. (2008) A novel heterozygous HIF2AM535I mutation reinforces the role of oxygen sensing pathway disturbances in the pathogenesis of familial erythrocytosis. Haematologica 93:1068-1071. (Pubitemid 351957024)
41. Ang SO, et al. (2002) Disruption of oxygen homeostasis underlies congenital Chuvash polycythemia. Nat Genet 32:614-621.
42. Gordeuk VR, et al. (2004) Congenital disorder of oxygen sensing: Association of the homozygous Chuvash polycythemia VHL mutation with thrombosis and vascular abnormalities but not tumors. Blood 103:3924-3932.
43. Sergeyeva A, et al. (1997) Congenital polycythemia in Chuvashia. Blood 89:2148-2154.
44. Smith TG, et al. (2006) Mutation of von Hippel-Lindau tumour suppressor and human cardiopulmonary physiology. PLoS Med 3:e290.
45. Bushuev VI, et al. (2006) Endothelin-1, vascular endothelial growth factor and systolic pulmonary artery pressure in patients with Chuvash polycythemia. Haematologica 91:744-749.
46. Ren YH, et al. (2010) Incidence of high altitude illnesses among unacclimatized persons who acutely ascended to Tibet. High Alt Med Biol 11:39-42.
47. Monge-C C, Arregui A, León-Velarde F (1992) Pathophysiology and epidemiology of chronic mountain sickness. Int J Sports Med 13 (Suppl 1):S79-S81.
48. Penaloza D, Arias-Stella J (2007) The heart and pulmonary circulation at high altitudes: Healthy highlanders and chronic mountain sickness. Circulation 115:1132-1146. (Pubitemid 46673174)
49. Jaillard AS, Hommel M, Mazetti P (1995) Prevalence of stroke at high altitude (3380 m) in Cuzco, a town of Peru. A population-based study. Stroke 26:562-568.
50. Gonzales GF, Steenland K, Tapia V (2009) Maternal hemoglobin level and fetal outcome at low and high altitudes. Am J Physiol Regul Integr Comp Physiol 297:R1477-R1485.
51. Pringle KG, Kind KL, Sferruzzi-Perri AN, Thompson JG, Roberts CT (2009) Beyond oxygen: Complex regulation and activity of hypoxia inducible factors in pregnancy. Hum Reprod Update, 10.1093/humupd/dmp046.
52. Dunwoodie SL (2009) The role of hypoxia in development of the Mammalian embryo. Dev Cell 17:755-773.
53. Meade ES, Ma YY, Guller S (2007) Role of hypoxia-inducible transcription factors 1alpha and 2alpha in the regulation of plasminogen activator inhibitor-1 expression in a human trophoblast cell line. Placenta 28:1012-1019.
54. Cowden Dahl KD, et al. (2005) Hypoxia-inducible factors 1alpha and 2alpha regulate trophoblast differentiation. Mol Cell Biol 25:10479-10491.
55. Dai SY, Kanenishi K, Ueno M, Sakamoto H, Hata T (2004) Hypoxia-inducible factor-2alpha is involved in enhanced apoptosis in the placenta from pregnancies with fetal growth restriction. Pathol Int 54:843-849. (Pubitemid 40065090)
56. Moore LG, Young D, McCullough RE, Droma T, Zamudio S (2001) Tibetan protection from intrauterine growth restriction (IUGR) and reproductive loss at high altitude. Am J Hum Biol 13:635-644. (Pubitemid 32771407)
57. Xing Y, et al. (2009) Hemoglobin levels and anemia evaluation during pregnancy in the highlands of Tibet: A hospital-based study. BMC Public Health 9:336.
58. Hoit BD, et al. (2005) Nitric oxide and cardiopulmonary hemodynamics in Tibetan highlanders. J Appl Physiol 99:1796-1801. (Pubitemid 41547177)
59. Wellcome Trust Case Control Consortium (2007) Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447:661-678.