Ancestry explains the blunted ventilatory response to sustained hypoxia and lower exercise ventilation of Quechua altitude natives

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 289, Issue 1 58-1, 2005, Pages

  Brutsaert, Tom D ^a   Parra, Esteban J ^b   Shriver, Mark D ^c   Gamboa, Alfredo ^d   Rivera Ch, Maria ^d   León Velarde, Fabiola ^d  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d UNIVERSIDAD PERUANA CAYETANO HEREDIA   (Peru)

Author keywords

Admixture; Andes; Arterial saturation; Genetic markers

Indexed keywords

ADULT; ALTITUDE; AMERICAN INDIAN; ANTHROPOMETRY; ARTERIAL OXYGEN SATURATION; ARTERIAL OXYGEN TENSION; ARTICLE; CHEMOSENSITIVITY; CLINICAL ARTICLE; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; EXERCISE; FEMALE; GENETIC MARKER; GENETIC TRAIT; GENOTYPE; HUMAN; HYPOVENTILATION; HYPOXIA; LUNG GAS EXCHANGE; LUNG VENTILATION; MALE; PRIORITY JOURNAL; RESPIRATORY FUNCTION;

ADULT; ALTITUDE; ANOXIA; ARTERIES; EUROPEAN CONTINENTAL ANCESTRY GROUP; EXERCISE; EXERCISE TEST; HUMANS; INDIANS, SOUTH AMERICAN; MALE; OXYGEN; OXYGEN CONSUMPTION; PERU; PULMONARY VENTILATION; SPAIN; TIME FACTORS;

EID: 21044451773     PISSN: 03636119     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpregu.00105.2005     Document Type: Article

References (75)

1. Akey JM, Sosnoski D, Parra E, Dios S, Hiester K, Su B, Bonilla C, Jin L, and Shriver MD. Melting curve analysis of SNPs (McSNP): a gel-free and inexpensive approach for SNP genotyping. Biotechniques 30: 358-362, 364, 366-357, 2001.
2. Beall CM, Strohl KP, Blangero J, Williams-Blangero S, Almasy LA, Decker MJ, Worthman CM, Goldstein MC, Vargas E, Villena M, Soria R, Alarcon AM, and Gonzales C. Ventilation and hypoxic ventilatory response of Tibetan and Aymara high-altitude natives. Am J Phys Anthropol 104: 427-447, 1997.
3. Bonilla C, Shriver MD, Parra EJ, Jones A, and Fernandez JR. Ancestral proportions and their association with skin pigmentation and bone mineral density in Puerto Rican women from New York City. Hum Genet 115: 57-68, 2004.
4. Brutsaert T, Parra E, Shriver M, Gamboa A, Palacios J, Rivera M, Rodriquez I, and Leaon-Velarde F. Effects of birth place and individual admixture on lung volume and exercise phenotypes of Peruvian Quechua Am J Phys Anthropol 123: 390-398, 2004.
5. 2 max decrement from sea level to 4338 m in Peruvan Quechua. J Appl Physiol 95: 519-528, 2003.
6. Brutsaert TD. Limits on inferring genetic adaptation to high altitude in Himalayan and Andean populations. High Alt Med Biol 2: 211-225, 2001.
7. Brutsaert TD, Araoz M, Soria R, Spielvogel H, and Haas JD. Higher arterial oxygen saturation during submaximal exercise in Bolivian Aymara compared to European sojourners and Europeans born and raised at high altitude. Am J Phys Anthropol 113: 169-181, 2000.
8. Brutsaert TD, Soria R, Caceres E, Spielvogel H, and Haas JD. Effect of developmental and ancestral high-altitude exposure on chest morphology and pulmonary function in Andean and European/North American natives. Am J Hum Biol 11: 383-395, 1999.
9. Byrne-Quinn E, Sodal IE, and Weil JV. Hypoxic and hypercapnic ventilatory drives in children native to high altitude. J Appl Physiol 32: 44-46, 1972.
10. Chiodi H. Respiratory adaptations to chronic high-altitude hypoxia. J Appl Physiol 10: 81-87, 1957.
11. Cudkowicz L, Spielvogel H, and Zubieta G. Respiratory studies in women at high altitude (3.600 m or 12,200 ft and 5,200 m or 17,200 ft). Respiration 29: 393-426, 1972.
12. Durnin JV and Womersley J. Body fat assessed from total body density and its estimation from skinfold thickness: measurements on 481 men and women aged from 16 to 72 years. Br J Nutr 32: 77-97, 1974.
13. Easton PA, Slykerman LJ, and Anthonisen NR. Ventilatory response to sustained hypoxia in normal adults. J Appl Physiol 61: 906-911, 1986.
14. Falush D, Stephens M, and Pritchard JK. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567-1587, 2003.
15. Fernandez JR, Shriver MD, Beasley TM, Rafla-Demetrious N, Parra E, Albu J, Nicklas B, Ryan AS, McKeigue PM, Hoggart CL, Weinsier RL, and Allison DB. Association of African genetic admixture with resting metabolic rate and obesity among women. Obes Res 11: 904-911, 2003.
16. 2 and hypoxia. J Appl Physiol 31: 586-592, 1971.
17. Frisancho AR. Developmental adaptation to high altitude hypoxia. Int J Biometeorol 21: 135-146, 1977.
18. Frisancho AR, Frisancho HG, Albalak R, Villena M, Vargas E, and Soria R. Developmental, genetic and environmental components of lung volumes at high altitude. Am J Hum Biol 9: 191-203, 1997.
19. Gale GE, Torre-Bueno JR, Moon RE, Saltzman HA, and Wagner PD. Ventilation-perfusion inequality in normal humans during exercise at sea level and simulated altitude. J Appl Physiol 58: 978-988, 1985.
20. Gamboa A, Leon-Velarde F, Rivera-Ch M, Palacios JA, Pragnell TR, O'Connor DF, and Robbins PA. Selected contribution: Acute and sustained ventilatory responses to hypoxia in high-altitude natives living at sea level. J Appl Physiol 94: 1255-1262; discussion 1253-1254, 2003.
21. Ge RL, Chen QH, and He LG. Characteristics of hypoxic ventilatory response in Tibetan living at moderate and high altitudes. Chung Hua Chieh Ho Ho Hu Hsi Tsa Chih 17: 364-366, 384, 1994.
22. Gorodezky C, Alaez C, Vazquez-Garcia MN, de la Rosa G, Infante E, Balladares S, Toribio R, Perez-Luque E, and Munoz L. The genetic structure of Mexican Mestizos of different locations: tracking back their origins through MHC genes, blood group systems, and microsatellites. Hum Immunol 62: 979-991, 2001.
23. Gower BA, Fernandez JR, Beasley TM, Shriver MD, and Goran MI. Using genetic admixture to explain racial differences in insulin-related phenotypes. Diabetes 52: 1047-1051, 2003.
24. Greksa LP. Evidence for a genetic basis to the enhanced total lung capacity of Andean highlanders. Hum Biol 68: 119-129, 1996.
25. Hackett PH, Reeves JT, Reeves CD, Grover RF, and Rennie D. Control of breathing in Sherpas at low and high altitude. J Appl Physiol 49: 374-379, 1980.
26. Hochachka PW. Balancing conflicting metabolic demands of exercise and diving. Fed Proc 45: 2948-2952, 1986.
27. Hoggart CJ, Parra EJ, Shriver MD, Bonilla C, Kittles RA, Clayton DG, and McKeigue PM. Control of confounding of genetic associations in stratified populations. Am J Hum Genet 72: 1492-1504, 2003.
28. Hoggart CJ, Shriver MD, Kittles RA, Clayton DG, and McKeigue PM. Design and analysis of admixture mapping studies. Am J Hum Genet 74: 965-978, 2004.
29. Huang SY, Alexander JK, Grover RF, Maher JT, McCullough RE, McCullough RG, Moore LG, Sampson JB, Weil JV, and Reeves JT. Hypocapnia and sustained hypoxia blunt ventilation on arrival at high altitude. J Appl Physiol 56: 602-606, 1984.
30. Kashiwazaki H, Dejima Y, Orias-Rivera J, and Coward W. Validity of published prediction equations for body composition in high-altitude Bolivian Aymara as evaluated by doubly labeled water. Am J Hum Biol 10: 371-384, 1998.
31. Kazemi H and Hoop B. Glutamic acid and gamma-aminobutyric acid neurotransmitters in central control of breathing. J Appl Physiol 70: 1-7, 1991.
32. Kollias J, Buskirk ER, Akers RF, Prokop EK, Baker PT, and Picon-Reategui E. Work capacity of long-time residents and newcomers to altitude. J Appl Physiol 24: 792-799, 1968.
33. Kreuzer F, Tenney SM, Mithoefer JC, and Remmers J. Alveolar-arterial oxygen gradient in Andean natives at high altitude. J Appl Physiol 19: 13-16, 1964.
34. Lahiri S. Alveolar gas pressures in man with life-time hypoxia. Respir Physiol 4: 373-386, 1968.
35. Lahiri S, DeLaney RG, Brody JS, Simpser M, Velasquez T, Motoyama EK, and Polgar C. Relative role of environmental and genetic factors in respiratory adaptation to high altitude. Nature 261: 133-135, 1976.
36. Lahiri S, Kao FF, Velasquez T, Martinez C, and Pezzia W. Irreversible blunted respiratory sensitivity to hypoxia in high-altitude natives. Respir Physiol 6: 360-374, 1969.
37. Lahiri S and Milledge JS. Acid-base in Sherpa altitude residents and lowlanders at 4880 m. Respir Physiol 2: 323-334, 1967.
38. Lee SD, Nakano H, and Farkas GA. GABAergic modulation of ventilation and peak oxygen consumption in obese Zucker rats. J Appl Physiol 90: 1707-1713, 2001.
39. Leon-Velarde F, Gamboa A, Rivera-Ch M, Palacios JA, and Robbins PA. Selected contribution: Peripheral chemoreflex function in high-altitude natives and patients with chronic mountain sickness. J Appl Physiol 94: 1269-1278; discussion 1253-1264, 2003.
40. Lisker R, Ramirez E, Briceno RP, Granados J, and Babinsky V. Gene frequencies and admixture estimates in four Mexican urban centers. Hum Biol 62: 791-801, 1990.
41. Molokhia M, Hoggart C, Patrick AL, Shriver M, Parra E, Ye J, Silman AJ, and McKeigue PM. Relation of risk of systemic lupus erythematosus to west African admixture in a Caribbean population. Hum Genet 112: 310-318, 2003.
42. Moore LG. Comparative aspects of high altitude adaptation in human populations. In: Oxygen Sensing: Molecule to Man, edited by Lahiri S, Prabhakar NR, and Forster RE. Norwell, MA: Kluwer Academic/Plenum Publishers, 2000, p. 45-62.
43. Moore LG. Comparative human ventilatory adaptation to high altitude. Respir Physiol 121: 257-276, 2000.
44. Moore LG. Women at Altitude: Overview. In: Hypoxia: Women at Altitude, edited by Houston CS, and G. Coates. Burlington: Queen City Printer, 1997, p. 1-7.
45. Mou XB, Howard LS, and Robbins PA. A protocol for determining the shape of the ventilatory response to hypoxia in humans. Respir Physiol 101: 139-143, 1995.
46. Papadimitriou GN, Dikeos DG, Karadima G, Avramopoulos D, Daskalopoulou EG, and Stefanis CN. GABA-A receptor beta3 and alpha5 subunit gene cluster on chromosome 15q11-q13 and bipolar disorder: a genetic association study. Am J Med Genet 105: 317-320, 2001.
47. Parra EJ, Kittles RA, and Shriver MD. Implications of correlations between skin color and genetic ancestry for biomedical research. Nat Genet 36: S54-S60, 2004.
48. Patterson N, Hattangadi N, Lane B, Lohmueller KE, Hafler DA, Oksenberg JR, Hauser SL, Smith MW, O'Brien SJ, Altshuler D, Daly MJ, and Reich D. Methods for high-density admixture mapping of disease genes. Am J Hum Genet 74: 979-1000, 2004.
49. Powell FL, Milsom WK, and Mitchell GS. Time domains of the hypoxic ventilatory response. Respir Physiol 112: 123-134, 1998.
50. Pritchard JK, Stephens M, and Donnelly P. Inference of population structure using multilocus genotype data. Genetics 155: 945-959, 2000.
51. Remmers JE and Mithoefer JC. The carbon monoxide diffusing capacity in permanent residents at high altitude. Respir Physiol 6: 233-244, 1969.
52. Robbins PA. Hypoxic ventilatory decline: site of action. J Appl Physiol 79: 373-374, 1995.
53. Robbins PA, Swanson GD, and Howson MG. A prediction-correction scheme for forcing alveolar gases along certain time courses. J Appl Physiol 52: 1353-1357, 1982.
54. Schoene RB. Control of ventilation in climbers to extreme altitude. J Appl Physiol 53: 886-890, 1982.
55. Schoene RB, Roach RC, Lahiri S, Peters RM, Hackett PH, and Santolaya R. Increased diffusion capacity maintains arterial saturation during exercise in the Quechua Indians of the Chilean Altiplano. Am J Hum Biol 2: 663-668, 1990.
56. 2 dissociation computations. J Appl Physiol 46: 599-602, 1979.
57. Severinghaus JW, Bainton CR, and Carcelen A. Respiratory insensitivity to hypoxia in chronically hypoxic man. Respir Physiol 1: 308-334, 1966.
58. Shriver M, Mei P, Parra E, Sonpar V, Halder I, Tishkoft S, Schurr T, Zhadanov S, Osipova L, Brutsaert T, Friedlander J, Jorde L, Watkins W, Bamshad M, Gutierrez G, Loi H, Matsuzaki H, Kittles R, Argyropoulos G, Fernandez J, Akey J, and Jones K. Large-scale SNP analysis reveals clustered and continuous human genetic variation. Hum Genomics, in press.
59. Shriver MD, Parra EJ, Dios S, Bonilla C, Norton H, Jovel C, Pfaff C, Jones C, Massac A, Cameron N, Baron A, Jackson T, Argyropoulos G, Jin L, Hoggart CJ, McKeigue PM, and Kittles RA. Skin pigmentation, biogeographical ancestry and admixture mapping. Hum Genet 112: 387-399, 2003.
60. Smith C, Dempsey J, and Hornbein T. Control of breathing at high altitude. In: High Altitude: An Exploration of Human Adaptation, edited by Hornbein T and Schoene R. New York: Marcel Dekker AG, 2001, p. 139-173.
61. Sorensen SC and Severinghaus JW. Irreversible respiratory insensitivity to acute hypoxia in man born at high altitude. J Appl Physiol 25: 217-220, 1968.
62. Sorensen SC and Severinghaus JW. Respiratory sensitivity to acute hypoxia in man born at sea level living at high altitude. J Appl Physiol 25: 211-216, 1968.
63. Vargas M, Leon-Velarde F, Monge CC, Palacios JA, and Robbins PA. Similar hypoxic ventilatory responses in sea-level natives and high-altitude Andean natives living at sea level. J Appl Physiol 84: 1024-1029, 1998.
64. Velasquez T, Martinez C, Pezzia W, and Gallardo N. Ventilatory effects of oxygen in high-altitude natives. Respir Physiol 5: 211-220, 1968.
65. Vincent J, Hellot MF, Vargas E, Gautier H, Pasquis P, and Lefrancois R. Pulmonary gas exchange, diffusing capacity in natives and newcomers at high altitude. Respir Physiol 34: 219-231, 1978.
66. Wagner PD, Araoz M, Boushel R, Calbet JA, Jessen B, Radegran G, Spielvogel H, Sondegaard H, Wagner H, and Saltin B. Pulmonary gas exchange and acid-base state at 5,260 m in high-altitude Bolivians and acclimatized lowlanders. J Appl Physiol 92: 1393-1400, 2002.
67. Wagner PD, Gale GE, Moon RE, Torre-Bueno JR, Stolp BW, and Saltzman HA. Pulmonary gas exchange in humans exercising at sea level and simulated altitude. J Appl Physiol 61: 260-270, 1986.
68. Weil JV. Variation in human ventilatory control-genetic influence on the hypoxic ventilatory response. Respir Physiol Neurobiol 135: 239-246, 2003.
69. 2 and hypoxia after sustained hypoxia in awake cats. J Appl Physiol 76: 2251-2252, 1994.
70. Weil JV, Byrne-Quinn E, Sodal IE, Filley GF, and Grover RF. Acquired attenuation of chemoreceptor function in chronically hypoxic man at high altitude. J Clin Invest 50: 186-195, 1971.
71. Weil JV, Byrne-Quinn E, Sodal IE, Friesen WO, Underbill B, Filley GF, and Grover RF. Hypoxic ventilatory drive in normal man. J Clin Invest 49: 1061-1072, 1970.
72. Williams RC, Long JC, Hanson RL, Sievers ML, and Knowler WC. Individual estimates of European genetic admixture associated with lower body-mass index, plasma glucose, and prevalence of type 2 diabetes in Pima Indians. Am J Hum Genet 66: 527-538, 2000.
73. Yamada KA, Hamosh P, and Gillis RA. Respiratory depression produced by activation of GABA receptors in hindbrain of cat. J Appl Physiol 51: 1278-1286, 1981.
74. Zhang S and Robbins PA. Methodological and physiological variability within the ventilatory response to hypoxia in humans. J Appl Physiol 88: 1924-1932, 2000.
75. Zhuang J, Droma T, Sun S, Janes C, McCullough RE, McCullough RG, Cymerman A, Huang SY, Reeves JT, and Moore LG. Hypoxic ventilatory responsiveness in Tibetan compared with Han residents of 3,658 m. J Appl Physiol 74: 303-311, 1993.