Genetic adaptation of the hypoxia-inducible factor pathway to oxygen pressure among eurasian human populations

Molecular Biology and Evolution

Volumn 29, Issue 11, 2012, Pages 3359-3370

  Ji, Lin Dan ^a,b,c   Qiu, Yu Qing ^b,d   Xu, Jin ^a,b,c   Irwin, David M ^a,e,f   Tam, Siu Cheung ^g   Tang, Nelson L S ^b,d,g   Zhang, Ya Ping ^a,b,h  

^a KUNMING INSTITUTE OF ZOOLOGY   (China)

^b KIZ/CUHK Joint Laboratory of Bioresources and Molecular Research in Common Diseases   (China)

^c NINGBO UNIVERSITY   (China)

^d and Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics   (Hong Kong)

^e UNIVERSITY OF TORONTO   (Canada)

^f UNIVERSITY OF TORONTO   (Canada)

^g CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^h YUNNAN UNIVERSITY   (China)

Author keywords

adaptive evolution; Eurasian populations; human genetic variation; hypoxia; hypoxia inducible factor pathway; oxygen pressure

Indexed keywords

HYPOXIA INDUCIBLE FACTOR; MU OPIATE RECEPTOR;

ALTITUDE; ARTICLE; BREATHING; CARDIOPULMONARY HEMODYNAMICS; CHINA; CHINESE; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; GENE; GENE FREQUENCY; GENE IDENTIFICATION; GENE LOCUS; GENETIC ASSOCIATION; GENETIC CODE; GENETIC VARIABILITY; HUMAN; HYPOXIA; MAJOR CLINICAL STUDY; OXYGEN TENSION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM;

ADAPTATION, PHYSIOLOGICAL; ALLELES; ALTITUDE; ANOXIA; ASIAN CONTINENTAL ANCESTRY GROUP; ECOSYSTEM; ETHNIC GROUPS; EUROPE; GENE FREQUENCY; GENETIC ASSOCIATION STUDIES; GENETICS, POPULATION; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; OXYGEN; POLYMORPHISM, SINGLE NUCLEOTIDE; PRESSURE; PRINCIPAL COMPONENT ANALYSIS; PROCOLLAGEN-PROLINE DIOXYGENASE; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; TIBET;

EID: 84867776802     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mss144     Document Type: Article

References (71)

1. Adams WH, Strang LJ. 1975. Hemoglobin levels in persons of Tibetan ancestry living at high altitude. Proc Soc Exp Biol Med. 149: 1036-1039.
2. Ashburner M, Ball CA, Blake JA, et al. (20 co-authors). 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 25:25-29.
3. Beall CM. 2000. Tibetan and Andean contrasts in adaptation to high-altitude hypoxia. Adv Exp Med Biol. 475:63-74.
4. Beall CM. 2007. Two routes to functional adaptation: Tibetan and Andean high-altitude natives. Proc Natl Acad Sci USA. 104(Suppl. 1), 8655-8660.
5. Beall CM, Brittenham GM, Macuaga F, Barragan M. 1990. Variation in hemoglobin concentration among samples of high altitude natives in the Andes and the Himalayas. Am J Hum Biol. 2:639-651.
6. Beall CM, Brittenham GM, Strohl KP, et al. (12 co-authors). 1998. Hemoglobin concentration of high-altitude Tibetans and Bolivian Aymara. Am J Phys Anthropol. 106:385-400.
7. Beall CM, Cavalleri GL, Deng L, et al. (29 co-authors). 2010. Natural selection on EPAS1 (HIF2alpha) associated with low hemoglobin concentration in Tibetan highlanders. Proc Natl Acad Sci USA. 107:11459-11464.
8. Beall CM, Goldstein MC. 1987. Hemoglobin concentration of pastoral nomads permanently resident at 4,850-5,450 meters in Tibet. Am J Phys Anthropol. 73:433-438.
9. Beall CM, Reichsman AB. 1984. Hemoglobin levels in a Himalayan high altitude population. Am J Phys Anthropol. 63:301-306.
10. Beall CM, Strohl KP, Blangero J, et al. (13 co-authors). 1997. Ventilation and hypoxic ventilatory response of Tibetan and Aymara high altitude natives. Am J Phys Anthropol. 104:427-447.
11. Bigham A, Bauchet M, Pinto D, et al. (14 co-authors). 2010. Identifying signatures of natural selection in Tibetan and Andean populations using dense genome scan data. PLoS Genet. 6:e1001116.
12. Bigham AW, Mao X, Mei R, Brutsaert T, Wilson MJ, Julian CG, Parra EJ, Akey JM, Moore LG, Shriver MD. 2009. Identifying positive selection candidate loci for high-altitude adaptation in Andean populations. Hum Genomics. 4:79-90.
13. Bitner-Mathe BC, Peixoto AA, Klaczko LB. 1995. Morphological variation in a natural population of Drosophila mediopunctata: altitudinal cline, temporal changes and influence of chromosome inversions. Heredity 75:54-61.
14. Boucher O. 2010. Stratospheric ozone, ultraviolet radiation and climate change. Weather 65:105-110.
15. Brown KA, Laferriere A, Moss IR. 2004. Recurrent hypoxemia in young children with obstructive sleep apnea is associated with reduced opioid requirement for analgesia. Anesthesiology 100:806-810.
16. Brunsdon C, McClatchey J, Unwin DJ. 2001. Spatial variations in the average rainfall-altitude relationship in Great Britain: an approach using geographically weighted regression. Int J Climatol. 21:455-466.
17. Calbet JA, Boushel R, Radegran G, Sondergaard H, Wagner PD, Saltin B. 2003. Why is VO2 max after altitude acclimatization still reduced despite normalization of arterial O2 content? Am J Physiol Regul Integr Comp Physiol. 284:R304-R316.
18. Chen YR, Dai AG, Hu RC, Jiang YL. 2006. Differential and reciprocal regulation between hypoxia-inducible factor-alpha subunits and their prolyl hydroxylases in pulmonary arteries of rat with hypoxia-induced hypertension. Acta Biochim Biophys Sin. 38: 423-434.
19. Collinge JE, Hoffmann AA, McKechnie SW. 2006. Altitudinal patterns for latitudinally varying traits and polymorphic markers in Drosophila melanogaster from eastern Australia. J Evol Biol. 19:473-482.
20. Davis WB, Rennard SI, Bitterman PB, Crystal RG. 1983. Pulmonary oxygen toxicity. Early reversible changes in human alveolar structures induced by hyperoxia. N Engl J Med. 309:878-883.
21. Farmer EW, Lupa HT, Dunlop F, McGowan FF. 1992. Task learning under mild hypoxia. In: Sutton JR, Coates G, Houston CS, editors. Hypoxia and mountain medicine. Burlington (VT): Queen City Printers. p. 1-8.
22. Fu D, Dai A, Hu R, Chen Y, Zhu L. 2008. Expression and role of factor inhibiting hypoxia-inducible factor-1 in pulmonary arteries of rat with hypoxia-induced hypertension. Acta Biochim Biophys Sin. 40: 883-892.
23. Ge D, Zhang K, Need AC, Martin O, Fellay J, Urban TJ, Telenti A, Goldstein DB. 2008. WGAViewer: software for genomic annotation of whole genome association studies. Genome Res. 18:640-643.
24. Greer JJ, Carter JE, al-Zubaidy Z. 1995. Opioid depression of respiration in neonatal rats. J Physiol. 485(Pt 3):845-855.
25. Grocott M, Richardson A, Montgomery H, Mythen M. 2007. Caudwell Xtreme Everest: a field study of human adaptation to hypoxia. Crit Care 11:151.
26. Hannon JP, Sudman DM. 1973. Basal metabolic and cardiovascular function of women during altitude acclimatization. J Appl Physiol. 34: 471-477.
27. Hayes MA, Timmins AC, Yau EH, Palazzo M, Hinds CJ, Watson D. 1994. Elevation of systemic oxygen delivery in the treatment of critically ill patients. N Engl J Med. 330:1717-1722.
28. Hornbein TF, Schoene RB. 2001. High altitude: an exploration of human adaptation. New York: Marcel Dekker.
29. Houston CS, Riley RL. 1947. Respiratory and circulatory changes during acclimatization to high altitude. Am J Physiol. 149:565-588.
30. Huang da W, Sherman BT, Lempicki RA. 2009a. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37:1-13.
31. Huang da W, Sherman BT, Lempicki RA. 2009b. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protocols. 4:44-57.
32. Hunley K, Healy M. 2011. The impact of founder effects, gene flow, and European admixture on native American genetic diversity. Am J Phys Anthropol. 146:530-538.
33. Ji L, Xu J, Wu D, Xie S, Tang NLS, Zhang Y. 2010. Association of diseasepredisposition polymorphisms of the melatonin receptors and sunshine duration in the global human populations. J Pineal Res. 48: 133-141.
34. Johnson SM, Kinney ME, Wiegel LM. 2008. Inhibitory and excitatory effects of micro-, delta-, and kappa-opioid receptor activation on breathing in awake turtles, Trachemys scripta. Am J Physiol Regul Integr Comp Physiol. 295:R1599-R1612.
35. Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, Kawashima S, Katayama T, Araki M, Hirakawa M. 2006. From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res. 34:D354-D357.
36. Kiritsy-Roy JA, Appel NM, Bobbitt FG, Van Loon GR. 1986. Effects of mu-opioid receptor stimulation in the hypothalamic paraventricular nucleus on basal and stress-induced catecholamine secretion and cardiovascular responses. J Pharmacol Exp Ther. 239:814-822.
37. Lando D, Peet DJ, Gorman JJ, Whelan DA,WhitelawML, Bruick RK. 2002. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 16: 1466-1471.
38. Lendahl U, Lee KL, Yang H, Poellinger L. 2009. Generating specificity and diversity in the transcriptional response to hypoxia. Nat Rev Genet. 10:821-832.
39. Li JZ, Absher DM, Tang H, et al. (11 co-authors). 2008. Worldwide human relationships inferred from genome-wide patterns of variation. Science 319:1100-1104.
40. Martin D, Windsor J. 2008. From mountain to bedside: understanding the clinical relevance of human acclimatisation to high-altitude hypoxia. Postgrad Med J. 84:622-627.
41. Mason NP. 2000. The physiology of high altitude: an introduction to the cardio-respiratory changes occurring on ascent to altitude. Curr Anaesthesia Crit Care. 11:34-41.
42. Moore LG, Brodeur P, Chumbe O, D'Brot J, Hofmeister S,Monge C. 1986. Maternal hypoxic ventilatory response, ventilation, and infant birth weight at 4,300 m. J Appl Physiol. 60:1401-1406.
43. Moore LG, Shriver M, Bemis L, Hickler B, Wilson M, Brutsaert T, Parra E, Vargas E. 2004. Maternal adaptation to high-altitude pregnancy: an experiment of nature-a review. Placenta 25(Suppl. A), S60-S71.
44. 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.
45. Mortola JP, Frappell PB, Aguero L, Armstrong K. 2000. Birth weight and altitude: a study in Peruvian communities. J Pediatr. 136:324-329.
46. Moss IR, Brown KA, Laferriere A. 2006. Recurrent hypoxia in rats during development increases subsequent respiratory sensitivity to fentanyl. Anesthesiology 105:715-718.
47. Nei M. 1973. Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA. 70:3321-3323.
48. Oelz O, Howald H, Di Prampero PE, et al. (12 co-authors). 1986. Physiological profile of world-class high-altitude climbers. J Appl Physiol. 60:1734-1742.
49. Patterson N, Price AL, Reich D. 2006. Population structure and eigenanalysis. PLoS Genet. 2:e190.
50. Penaloza D, Arias-Stella J. 2007. The heart and pulmonary circulation at high altitudes: healthy highlanders and chronic mountain sickness. Circulation 115:1132-1146.
51. Peng Y, Yang Z, Zhang H, et al. (15 co-authors). 2011. Genetic variations in Tibetan populations and high-altitude adaptation at the Himalayas. Mol Biol Evol. 28:1075-1081.
52. 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. 38:904-909.
53. Purcell S, Cherny SS, Sham PC. 2003. Genetic Power Calculator: design of linkage and association genetic mapping studies of complex traits. Bioinformatics 19:149-150.
54. Purcell S, Neale B, Todd-Brown K, et al. (11 co-authors). 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 81:559-575.
55. Rabbitts JA, Groenewald CB, Dietz NM, Morales C, Rasanen J. 2010. Perioperative opioid requirements are decreased in hypoxic children living at altitude. Paediatr Anaesth. 20:1078-1083.
56. Reich D, Price AL, Patterson N. 2008. Principal component analysis of genetic data. Nat Genet. 40:491-492.
57. Reynafarje C, Hurtado A. 1971. Adaptation to high altitude. N Engl J Med. 285:862.
58. Sherry ST, Ward MH, Kholodov M, Baker J, Phan L, Smigielski EM, Sirotkin K. 2001. dbSNP: the NCBI database of genetic variation. Nucleic Acids Res. 29:308-311.
59. Shook JE, Watkins WD, Camporesi EM. 1990. Differential roles of opioid receptors in respiration, respiratory disease, and opiate-induced respiratory depression. Am Rev Respir Dis. 142:895-909.
60. Simonson TS, Yang Y, Huff CD, et al. (12 co-authors). 2010. Genetic evidence for high-altitude adaptation in Tibet. Science 329:72-75.
61. Sorensen JG, Norry FM, Scannapieco AC, Loeschcke V. 2005. Altitudinal variation for stress resistance traits and thermal adaptation in adult Drosophila buzzatii from the NewWorld. J Evol Biol. 18: 829-837.
62. Soto IM, Soto EM, Carreira VP, Hurtado J, Fanara JJ, Hasson E. 2010. Geographic patterns of inversion polymorphismin the second chromosome of the cactophilic Drosophila buzzatii from northeastern Argentina. J Insect Sci. 10:181.
63. Virues-Ortega J, Buela-Casal G, Garrido E, Alcazar B. 2004. Neuropsychological functioning associated with high-altitude exposure. Neuropsychol Rev. 14:197-224.
64. Vogel JA, Harris CW. 1967. Cardiopulmonary responses of resting man during early exposure to high altitude. J Appl Physiol. 22: 1124-1128.
65. Wang D, Teichtahl H. 2007. Opioids, sleep architecture and sleep-disordered breathing. Sleep Med Rev. 11:35-46.
66. West JB. 1998. High life: a history of high-altitude physiology and medicine. Oxford: Oxford University Press.
67. Xu S, Li S, Yang Y, et al. (13 co-authors). 2011. A genome-wide search for signals of high-altitude adaptation in Tibetans. Mol Biol Evol. 28: 1003-1011.
68. Yi X, Liang Y, Huerta-Sanchez E, et al. (70 co-authors). 2010. Sequencing of 50 human exomes reveals adaptation to high altitude. Science 329:75-78.
69. Yip R. 1987. Altitude and birth weight. J Pediatr. 111:869-876.
70. Zamudio S, Palmer SK, Droma T, Stamm E, Coffin C, Moore LG. 1995. Effect of altitude on uterine artery blood flow during normal pregnancy. J Appl Physiol. 79:7-14.
71. Zhao M, Kong QP, Wang HW, et al. (16 co-authors). 2009. Mitochondrial genome evidence reveals successful Late Paleolithic settlement on the Tibetan Plateau. Proc Natl Acad Sci USA. 106: 21230-21235.