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An Evolutionary Model for Identifying Genetic Adaptation to High Altitude

  • Conference paper
Hypoxia and Exercise

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 588))

Abstract

Coordinated maternal/fetal responses to pregnancy are required to ensure continuous O2 delivery to the developing organism. Mammals employ distinctive reproductive strategies that afford their young an improved chance of survival through the completion or the reproductive period. Thus, mortality prior to the end of the reproductive period is concentrated in the earliest phases of the lifecycle. At high altitude, fetal growth restriction reduces birth weight and likely compromises survival during the early postnatal period. Population variation in the frequency of the altitude-associated increase in intrauterine growth restriction (IUGR) demonstrates that multigenerational Tibetan and Andean high-altitude populations are protected compared with shorter duration, European or Han (Chinese) residents. This experiment of nature permits testing the hypothesis that genetic factors (a) influence susceptibility to altitude-associated IUGR, (b) act on maternal vascular adjustments to pregnancy determining uteroplacental blood flow, and (c) involve genes which regulate and/or are regulated by hypoxia-inducible factors (HIFs). Serial, studies during pregnancy as well as postpartum in Andean and European residents of high (3600 m) and low (300 m) altitude will permit evaluation of whether uteroplacental O2 delivery is lower in the European than Andean women and, if so, the physiological factors responsible. Comparisons of HIF-targeted vasoactive substances and SNPs in or near HIF-regulatory or targeted genes will permit determination of whether these regions are distinctive in the Andean population. Studies coupling genetic and genomic approaches with more traditional physiological measures may be productively employed for determining the genetic mechanisms influencing physiological adaptation to high altitude.

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References

  1. Abbott BD and Buckalew AR. Placental defects in ARNT-knockout conceptus correlate with localized decreases in VEGF-R2, Ang-1, and Tie-2. Developmental Dynamics 219: 526–538, 2000.

    Article  PubMed  CAS  Google Scholar 

  2. Angrimsson R, Hayward C, Nadaud S, Baldursdottir A, Walker JJ, Liston WA, Bjarnadottir RI, Brock DJH, Geirsson RT, Connor JM, and Soubrier F. Evidence for a familial pregnancy-induced hypertension locus in the eNOS-gene region. American Journal of Human Genetics 61: 354–362, 1997.

    Google Scholar 

  3. Bae MK, Ahn MY, Jeong JW, Bae MH, Lee YM, Bae SK, Park JW, Kim KR, and Kim KW. Jab1 interacts directly with HIF-1 alpha and regulates its stability. Journal of Biological Chemistry 277: 9–12, 2002.

    Article  PubMed  CAS  Google Scholar 

  4. Barker DJ. Fetal origins of cardiovascular disease. Ann Med 31Suppl 1: 3–6, 1999.

    PubMed  Google Scholar 

  5. Black WC, Baer CF, Antolin MF, and DuTeau NM. Population genomics: genome-wide sampling of insect populations. Annu Rev Entomol 46: 441–469, 2001.

    Article  PubMed  CAS  Google Scholar 

  6. Bodi I, Bishopric NH, Discher DJ, Wu X, and Webster KA. Cell-specificity and signaling pathway of endothelin-1 gene regulation by hypoxia. Cardiovascular Research 30: 975–984, 1995.

    Article  PubMed  CAS  Google Scholar 

  7. Bolivia. Encuesta Nacional de Demografía y Salud. Calverton, MD USA: Macro International/DHS+Program, 1998.

    Google Scholar 

  8. Brutsaert T. Spanish genetic admixture is associated with larger VO2 max decrement from sea level to 4,338 m in Peruvian Quechua. Journal of Applied Physiology 95: 519–528, 2003.

    PubMed  Google Scholar 

  9. Brutsaert T. Limits on inferring genetic adaptation to high altitude in Himalayan and Andean populations. High Altitude Medicine & Biology 2: 211–225, 2001.

    Article  CAS  Google Scholar 

  10. Caniggia I and Winter JL. Hypoxia inducible factor-1: oxygen regulation of trophoblast differentiation in normal and pre-eclamptic pregnancies-a review. Placenta 23: S47–S57, 2002.

    Article  PubMed  Google Scholar 

  11. Chapman AB, Abraham WT, Osorio FV, Merouani A, Zamudio S, Young DA, Johnson A, Coffin C, Goldberg C, Moore LG, Dahms T, and Schrier RW. Temporal relationships between hormonal and hemodynamic changes in early human pregnancy. Kidney International 54: 2056–2063, 1998.

    Article  PubMed  CAS  Google Scholar 

  12. Chen D, Zhou X, Zhu Y, Zhu T, and Wang J. Comparison study on uterine and umbilical artery blood flow during pregnancy at high altitude and at low altitude. Zhonghua Fu Chan Ke Za Zhi 37: 69–71, 2002.

    PubMed  Google Scholar 

  13. Cipolla M and Osol G. Hypertrophic and hyperplastic effects of pregnancy on the rat uterine arterial wall. American Journal of Obstetrics and Gynecology 171: 805–811, 1994.

    PubMed  CAS  Google Scholar 

  14. Clifford SC, Cockman ME, Smallwood AC, Mole DR, Woodward ER, Maxwell PH, Ratcliffe PJ, and Maher ER. Contrasting effects on HIF-1 alpha regulation by disease-causing pVHL mutations correlate with patterns of tumourigenesis in von Hippel-Lindau disease. Hum Mol Genet 10: 1029–1038, 2001.

    Article  PubMed  CAS  Google Scholar 

  15. Cope GA, Suh GS, Aravind L, Schwarz SE, Zipursky SL, Koonin EV, and Deshaies RJ. Role of predicted metalloprotease motif of Jab1/Csn5 in cleavage of Nedd8 from Cul1. Science 298: 608–611, 2002.

    Article  PubMed  CAS  Google Scholar 

  16. Coussons-Read ME, Mazzeo RS, Whitford MH, Schmitt M, Moore LG, and Zamudio S. High altitude residence during pregnancy alters cytokine and catecholamine levels. American Journal of Reproductive Immunology 48: 344–354, 2002.

    Article  PubMed  Google Scholar 

  17. Dobzhansky T. Adaptedness and fitness. In: Population Biology and Evolution, edited by Lewontin RC. Syracuse, NY: Syracuse University Press, 1968, p. 111–205.

    Google Scholar 

  18. Eremina V, Sood M, Haigh J, Nagy A, Lajoie G, Ferrara N, Gerber H-P, Kikkawa Y, Miner JH, and Quaggin SE. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. Journal of Clinical Investigation 111: 707–716, 2003.

    Article  PubMed  CAS  Google Scholar 

  19. Frisancho AR, Frisancho HG, Albalak R, Villain M, Vargas E, and Soria R. Developmental, genetic, and environmental components of lung volumes at high altitude. American Journal of Human Biology 9: 191–203, 1997.

    Article  Google Scholar 

  20. Furuhashi N, Kimura H, Nagae H, and Yajima A. Maternal plasma endothelin levels and fetal status in normal and preeclamptic pregnancies. Gynecologic and Obstetric Investigation 39: 88–92, 1995.

    Article  PubMed  CAS  Google Scholar 

  21. Gage T. Demography. In: Human Biology: an evolutionary and biocultural perspective, edited by Stinson S, Bogin B, Huss-Ashmore R and O”Rourke D. New York: John Wiley & Sons, 2000, p. 507–551.

    Google Scholar 

  22. Genbacev O, Krtolica A, Kaelin W, and Fisher SJ. Human cytotrophoblast expression of the von Hippel-Lindau protein is downregulated during uterine invasion in situ and upregulated by hypoxia in vitro. Developmental Biology 233: 526–536, 2001.

    Article  PubMed  CAS  Google Scholar 

  23. Genbacev O, Zhou Y, Ludlow JW, and Fisher SJ. Regulation of human placental development by oxygen tension. Science 277: 1669–1672, 1997.

    Article  PubMed  CAS  Google Scholar 

  24. Giussani D. High altitude and rural living are associated with increased infant mortality in Bolivia. J Soc Cynecol Investig 9: 292A, 2002.

    Google Scholar 

  25. Giussani DA, Seamus P, Anstee S, and Barker DJP. Effects of altitude versus economic status on birth weight and body shape at birth. Pediatric Research 49: 490–494, 2001.

    PubMed  CAS  Google Scholar 

  26. Gonzales GF. Determinantes biomedicos de la fertilidad humana en la altura. In: Reproduccion Humana en la Altura, edited by Gonzales GF. Lima, Peru: Consejo Nacional de Ciencia y Tecnologica, 1993, p. 73–87.

    Google Scholar 

  27. Granger JP. Maternal and fetal adaptations during pregnancy: lessons in regulatory and integrative physiology. American Journal of Physiology Regulatory, integrative and comparative physiology 283: R1289–R1292, 2002.

    PubMed  CAS  Google Scholar 

  28. Haas J, Balcazar H, and Caulfield L. Variation in early neonatal mortality for different types of fetal growth restriction. American Journal of Physical Anthropology 73: 467–473, 1987.

    Article  PubMed  CAS  Google Scholar 

  29. Haas JD. Human adaptability approach to nutritional assessment: a Bolivian example. Federation Proceedings 40: 2577–2582, 1981.

    PubMed  CAS  Google Scholar 

  30. Haas JD, Frongillo EJ, Stepcik C, Beard J, and Hurtado L. Altitude, ethnic and sex differences in birth weight and length in Bolivia. Human Biology 52: 459–477, 1980.

    Google Scholar 

  31. Halushka MK, Fan J-B, Bentley K, Hsie L, Shen N, Weder A, Cooper R, Lipshutz R, and Chakravarti A. Patterns of single-nucleotide polymorphisms in candidate genes for blood-pressure homeostasis. Nature Genetics 22: 239–247, 1999.

    Article  PubMed  CAS  Google Scholar 

  32. Hanaoka M, Droma Y, Hotta J, Matsuzawa Y, Kobayashi T, Kubo K, and Ota M. Polymorphisms of the tyrosine hydroxylase gene in subjects susceptible to high-altitude pulmonary edema. Chest 123: 54–58, 2003.

    Article  PubMed  CAS  Google Scholar 

  33. Hellwig-Bürgel T, Rutkowski K, Metzen E, Fandrey J, and Jelkmann W. Interleukin-lb and tumor necrosis factor-a stimulate DNA binding of hypoxia-inducible factor-1. Blood 94: 1561–1567, 1999.

    PubMed  Google Scholar 

  34. Howell WM, Bateman AC, Turner SJ, Collins A, and Theaker JM. Influence of vascular endothelial growth factor single nucleotide polymorphisms on tumour development in cutaneous malignant melanoma. Genes and Immunity 3: 229–232, 2002.

    Article  PubMed  CAS  Google Scholar 

  35. Hu XQ, Longo LD, Gilbert RD, and Zhang L. Effects of long-term high-altitude hypoxemia on alpha 1-adrenergic receptors in the ovine uterine artery. American Journal of Physiology 270: H1001–H1007, 1996.

    PubMed  CAS  Google Scholar 

  36. Hubel CA, Roberts JM, and Ferrell RE. Association of pre-eclampsia with common coding sequence variations in the lipoprotein lipase gene. Clin Genet 56: 289–296, 1999.

    Article  PubMed  CAS  Google Scholar 

  37. Jensen GM and Moore LG. The effect of high altitude and other risk factors on birthweight: independent or interactive effects? American Journal of Public Health 87: 1003–1007, 1997.

    Article  PubMed  CAS  Google Scholar 

  38. Jeong JW, Bae MK, Ahn MY, Kim SH, Sohn TK, Bae MH, Yoo MA, Song EJ, Lee K, and Kim KW. Regulation and Destabilization of HIF-1alpha by ARD1-Mediated Acetylation. Cell 111: 709–720, 2002.

    Article  PubMed  CAS  Google Scholar 

  39. Keyes LE, Armaza JF, Niermeyer S, Vargas E, Young D, Villena M, and Moore LG. Intrauterine growth restriction, preeclampsia and intrauterine mortality at high altitude in Bolivia. Pediatric Research 54: 20–25, 2003.

    Article  PubMed  Google Scholar 

  40. Kitanaka T, Gilbert RD, and Longo LD. Maternal responses to long-term hypoxemia in sheep. American Journal of Physiology 256: R1340–R1347, 1989.

    PubMed  CAS  Google Scholar 

  41. Krampl E. Pregnancy at high altitude. Ultrasound Obstet Gynecol 19: 535–539, 2002.

    Article  PubMed  CAS  Google Scholar 

  42. Krampl E, Espinoza-Dorado J, Lees CC, Moscoso G, and Bland JM. Maternal uterine artery Doppler studies at high altitude and sea level. Ultrasound in Obstetrics and Gynecology 18: 578–582, 2001.

    Article  PubMed  CAS  Google Scholar 

  43. Krampl E, Lees C, Bland JM, Dorado JE, Gonzalo M, and Campbell S. Fetal biometry at 4300 m compared to sea level in Peru. Ultrasound in Obstetrics and Gynecology 16: 9–18, 2000.

    Article  PubMed  CAS  Google Scholar 

  44. Kublickiene KR, Lindblom B, Kruger K, and Nisell H. Preeclampsia: evidence for impaired shear stress-mediated nitiric oxide release in uterine circulation. American Journal of Obstetrics and Gynecology 183: 160–166, 2000.

    PubMed  CAS  Google Scholar 

  45. Lea RG, Riley SC, Antipatis C, Hannah L, Ashworth CJ, Clark DA, and Critchley HO. Cytokines and the regulation of apoptosis in reproductive tissues: a review. Am J Reprod Immunol 42: 100–109, 1999.

    PubMed  CAS  Google Scholar 

  46. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH, Sibai BM, Sukhatme VP, and Karumanchi SA. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 350: 672–683, 2004.

    Article  PubMed  CAS  Google Scholar 

  47. Lewontin R. The triple helix: gene, organism and environment. Cambridge: Harvard University Press, 2001.

    Google Scholar 

  48. Lewontin RC. Ken-Ichi Kojima September 17, 1930-November 14, 1971. Genetics 71:Suppl 2:s89–90, 1972.

    Google Scholar 

  49. Lichty JL, Ting R, Bruns PD, and Dyar E. Studies of babies born at high altitude. American Journal of Diseases of Children 93: 666–669, 1957.

    CAS  Google Scholar 

  50. Lie RT, Rasmussen S, Brunborg H, Gjessing HK, Lie-Nielsen E, and Irgens LM. Fetal and maternal contributions to risk of pre-eclampsia: population based study. BMJ 316: 1343–1347, 1998.

    PubMed  CAS  Google Scholar 

  51. Lindsay RS, Kobes S, Knowler WC, and Hanson RL. Genome-wide linkage analysis assessing parent-of-origin effects in the inheritance of birth weight. Hum Genet 110: 503–509, 2002.

    Article  PubMed  CAS  Google Scholar 

  52. Lubchenco LO, Searls DT, and Brazie JV. Neonatal mortality rate: relationship to birth weight and getational age. Journal of Pediatrics 81: 814–822, 1972.

    Article  PubMed  CAS  Google Scholar 

  53. Magness RR. Maternal cardiovascular and other physiologic responses to the endocrinology of pregnancy. In: The Endocrinology of Pregnancy, edited by Bazer FW. Totowas, NJ: Humana Press, 1998, p. 507–539.

    Google Scholar 

  54. Mahfouz AA and al-Erian RA. Hypertension in Asir region, southwestern Saudi Arabia: an epidemiologic study. Southeast Asian Journal of Tropical Medicine and Public Health 24:284–286, 1993.

    PubMed  CAS  Google Scholar 

  55. Mahfouz AA, el-Said MM, Alakija W, and al-Erian RA. Altitude and socio-biological determinants of pregnancy-associated hypertension. International Journal of Gynaecology and Obstetrics AA: 135–138, 1994.

    Google Scholar 

  56. Maloney J, Wang D, Duncan T, Voelkel N, and Ruoss S. Plasma vascular endothelial growth factor in acute mountain sickness. Chest 118: 47–52, 2000.

    Article  PubMed  CAS  Google Scholar 

  57. Mateev S, Sillau AH, Mouser R, McCullough RE, White MM, Young DA, and Moore LG. Chronic hypoxia opposes pregnancy-induced increase in uterine artery vasodilator response to flow. American Journal of Physiology Heart and Circulatory Physiology 284: H820–H829, 2003.

    PubMed  CAS  Google Scholar 

  58. Mayhew TM, Jackson MR, and Haas JD. Oxygen diffusive conductances of human placentae from term pregnancies at low and high altitudes. Placenta 11: 493–503, 1990.

    Article  PubMed  CAS  Google Scholar 

  59. Maynard SE, Min J-Y, Merchan J, Lim K-H, Li J, Mondai S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, Epstein FH, Sukhatme VP, and Karumanchi SA. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. Journal of Clinical Investigation 111: 6 9-658, 2003.

    Google Scholar 

  60. Mazzeo RS, Brooks GA, Butterfield GE, Podolin DA, Wolfel EE, and Reeves JT. Acclimatization to high altitude increase muscle sympathetic activity both at rest and during exercise. American Journal of Physiology 269: R201–R207, 1995.

    PubMed  CAS  Google Scholar 

  61. McAuliffe F, Kametas N, Krampl E, Ernsting J, and Nicolaides K. Blood gases in pregnancy at sea level and at high altitude. British Journal of Obstetrics and Gynaecology 108: 980–985, 2001.

    Article  PubMed  CAS  Google Scholar 

  62. McCullough RE, Reeves JT, and Liljegren RL. Fetal growth retardation and increased infant mortality at high altitude. Archives of Environmental Health 32: 36–40, 1977.

    PubMed  CAS  Google Scholar 

  63. Moll W and Kunzel W. The blood pressure in arteries entering the placentae of guinea pigs, rats, rabbits, and sheep. Pflugers Archiv European Journal of Physiology 338: 125–131, 1973.

    Article  PubMed  CAS  Google Scholar 

  64. Moore LG. Human genetic adaptation to high altitude. High Altitude Medicine & Biology 2:257–279, 2001.

    Article  CAS  Google Scholar 

  65. Moore LG. Small babies and big mountains: John Lichty solves a Colorado mystery in Leadville. In: Attitudes on Altitude, edited by Reeves JT and Grover FT. Boulder: Univ Colorado Press, 2001, p. 137–159.

    Google Scholar 

  66. Moore LG, Hershey DW, Jahnigen D, and Bowes W, Jr. The incidence of pregnancy-induced hypertension is increased among Colorado residents at high altitude. American Journal of Obstetrics and Gynecology 144: 423–429, 1982.

    PubMed  CAS  Google Scholar 

  67. Moore LG, Jahnigen D, Rounds SS, Reeves JT, and Grover RF. Maternal hyperventilation helps preserve arterial oxygenation during high-altitude pregnancy. Journal of Applied Physiology: Respiratory, Environmental and Exercise Physiology 52: 690–694, 1982.

    CAS  Google Scholar 

  68. Moore LG, McCullough RE, and Weil JV. Increased HVR in pregnancy: relationship to hormonal and metabolic changes. Journal of Applied Physiology 62: 158–163, 1987.

    PubMed  CAS  Google Scholar 

  69. Moore LG, Rounds SS, Jahnigen D, Grover RF, and Reeves JT. Infant birth weight is related to maternal arterial oxygenation at high altitude. Journal of Applied Physiology: Respiratory, Environmental and Exercise Physiology 52: 695–699, 1982.

    CAS  Google Scholar 

  70. Moore LG, Shriver M, Bemis L, Hickler B, Wilson M, Brutsaert T, Parra E, and Vargas E. Maternal adaptation to high-altitude pregnancy: an experiment of nature. Placenta 25Suppl: S60–S71, 2004.

    Article  PubMed  CAS  Google Scholar 

  71. Moore LG, Zamudio S, Zhuang J, Sun S, and Droma T. Oxygen transport in Tibetan women during pregnancy at 3658 m. American Journal of Physical Anthropology 114: 42–53, 2001.

    Article  PubMed  CAS  Google Scholar 

  72. Morganti A, Giussani M, Sala C, Gazzano G, Marana I, Pierini A, Savoia MT, Ghio F, Cogo A, and Zanchetti A. Effects of exposure to high altitude on plasma endothelin-1 levels in normal subjects. Journal of Hypertension 13: 859–865, 1995.

    Article  PubMed  CAS  Google Scholar 

  73. Mortola JP, Frappell PB, Aguero L, and Armstrong K. Birth weight and altitude: a study in Peruvian communities. Journal of Pediatrics 136: 324–329, 2000.

    Article  PubMed  CAS  Google Scholar 

  74. Mulvany MJ, Baumbach GL, Aalkjaer C, Heagerty AM, Korsgaard N, Schiffrin EL, and Heistad DD. Vascular remodeling. Hypertension 28: 505–506, 1996.

    PubMed  CAS  Google Scholar 

  75. NCBI. LocusLink, 2003.

    Google Scholar 

  76. Ng DP, Canani L, Araki S, Smiles A, Moczulski D, Warram JH, and Krolewski AS. Minor effect of GLUT1 polymorphisms on susceptibility to diabetic nephropathy in type 1 diabetes. Diabetes 51: 2264–2269, 2002.

    Article  PubMed  CAS  Google Scholar 

  77. NIEHS. Environmental Genome Project, 2003.

    Google Scholar 

  78. Niermeyer S, Williford D, Asmus I, Honigman B, Moore LG, and Egbert M. Low birth weight in Colorado: analysis using geographic information systems. Adv Exp Med Biol (this volume): page 327 (abstract), 2006.

    Google Scholar 

  79. Niermeyer S, Zamudio S, and Moore LG. The People. In: Adaptations to Hypoxia, edited by Hornbein T and Schoene RB. New York, NY: Marcel Dekker and Co., 2001, p. 43–100.

    Google Scholar 

  80. PAHO. Epidemiological Bulletin 20(3): 14–19, 1999.

    Google Scholar 

  81. Palmer SK, Moore LG, Young DA, Cregger B, Berman JC, and Zamudio S. Altered blood pressure course during normal pregnancy and increased preeclampsia at high altitude (3100 meters) in Colorado. American Journal of Obstetrics and Gynecology 180: 1161–1168, 1999.

    Article  PubMed  CAS  Google Scholar 

  82. Palmer SK, Zamudio S, Coffin C, Parker S, Stamm E, and Moore LG. Quantitative estimation of human uterine artery blood flow and pelvic blood flow redistribution in pregnancy. Obstetrics and Gynecology 80: 1000–1006, 1992.

    PubMed  CAS  Google Scholar 

  83. Rajakumar A. The hypoxia inducible transcription factor, HIF-la, overexpressed in preeclamptic placentas is capable of binding to the hypoxia response element. Journal of the Society for Gynecologic Investigation 10: 304A, 2003.

    Article  Google Scholar 

  84. Rajakumar A, Doty K, Daftary A, Harger G, and Conrad KP. Impaired oxygen-dependent reduction of HIF-1alpha and-2alpha proteins in pre-eclamptic placentae. Placenta 24: 199–208, 2003.

    Article  PubMed  CAS  Google Scholar 

  85. Ratcliffe PJ, O’Rourke JF, Maxwell PH, and Pugh CW. Oxygen sensing, hypoxia-inducible factor-1 and the regulation of mammalian gene expression. Journal of Experimental Biology 201: 1153–1162, 1998.

    PubMed  CAS  Google Scholar 

  86. Renner W, Kotschan S, Hoffmann C, Obermayer-Pietsch B, and Pilger E. A common 936 C/T mutation in the gene for vascular endothelial growth factor is associated with vascular endothelial growth factor plasma levels. J Vasc Res 37: 443–448, 2000.

    Article  PubMed  CAS  Google Scholar 

  87. Rinehart BK, Terrone DA, Lagoo-Deenadayalan S, Barber WH, Hale EA, Martin JN, Jr., and Bennett WA. Expression of the placental cytokines tumor necrosis factor alpha, interleukin 1beta, and interleukin 10 is increased in preeclampsia. Am J Obstet Gynecol 181: 915–920, 1999.

    Article  PubMed  CAS  Google Scholar 

  88. Rockwell LC, Keyes LE, and Moore LG. Chronic hypoxia diminishes pregnancy-associated DNA synthesis in guinea pig uteroplacental arteries. Placenta 21: 313–319, 2000.

    Article  PubMed  CAS  Google Scholar 

  89. Safran M and Kaelin WG, Jr. HIF hydroxylation and the mammalian oxygen-sensing pathway. J Clin Invest 111: 779–783, 2003.

    Article  PubMed  CAS  Google Scholar 

  90. Sawidou MD, Valance PJT, Nicolaides KH, and Hingorani AD. Endothelial nitric oxide synthase gene polymorphism and maternal vascular adaptation to pregnancy. Hypertension 38: 1289–1293, 2001.

    Google Scholar 

  91. Schlotterer C. Hitchhiking mapping-functional genomics from the population genetics perspective. Trends Genet 19: 32–38, 2003.

    Article  PubMed  CAS  Google Scholar 

  92. SeattleSNPs. NHLBI Program for Genomic Appications, UW-FHCRC, Seattle, WA, 2004.

    Google Scholar 

  93. Semenza GL. Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annual Review of Cell and Developmental Biology 15: 551–578, 1999.

    Article  PubMed  CAS  Google Scholar 

  94. Smiley RM and Finster M. Do receptors get pregnant too? Adrenergic receptor alterations in human pregnancy. J Matern Fetal Med 5: 106–114, 1996.

    Article  PubMed  CAS  Google Scholar 

  95. Solomon CG and Seely EW. Preeclampsia-searching for the cause. N Engl J Med 350: 641–642, 2004.

    Article  PubMed  CAS  Google Scholar 

  96. Stock M and Metcalfe J. Maternal physiology during gestation. In: The Physiology of Reproduction, edited by Knobil E and Neil J. New York: Raven Press, 1994, p. 947–983.

    Google Scholar 

  97. Thaete LG, Dewey ER, and Neerhof MG. Endothelin and the regulation of uterine and placental perfusion in hypoxia-induced fetal growth restriction. J Soc Gynecol Investig 11: 16–21, 2004.

    Article  PubMed  CAS  Google Scholar 

  98. Thaete LG and Neerhof MG. Contribution of endothelin to the regulation of uterine and placental blood flow during nitric oxide synthase inhibition in the pregnant rat. 7th International Conference on Endothelin: 222, 2001.

    Google Scholar 

  99. Thaete LG, Neerhof MG, and Caplan MS. Endothelin receptor A antagonism prevents hypoxia-induced intrauterine growth restriction in the rat. American Journal of Obstetrics and Gynecology 176: 73–76, 1997.

    Article  PubMed  CAS  Google Scholar 

  100. Thaete LG, Neerhof MG, and Silver RK. Differential effects of endothelin A and B receptor antagonism on fetal growth in normal and nitric oxide-deficient rats. J Soc Cynecol Investig 8: 18–23, 2001.

    Article  CAS  Google Scholar 

  101. Tissot Van Patot M, Grilli A, Chapman P, Broad E, Tyson W, Heller DS, Zwerdlinger L, and Zamudio S. Remodeling of uteroplacental arteries is decreased in high altitude placentae. Placenta 24: 326–335, 2003.

    Article  Google Scholar 

  102. Unger C, Weiser JK, McCullough RE, Keefer S, and Moore LG. Altitude, low birth weight, and infant mortality in Colorado. Journal of the American Medical Association 259: 3427–3432, 1988.

    Article  PubMed  CAS  Google Scholar 

  103. Vitzthum V and Wiley A. The proximate determinants of fertility in populations exposed to chronic hypoxia. High Alt Med Biol 4: 125–139, 2003.

    Article  PubMed  Google Scholar 

  104. Ward K, hata A, Jeunemaitre X, Helin C, Nelson L, Namikawa C, Farrinton PF, Ogasawara M, Suzumori K, Tomoda S, Berrebi S, Sasaki M, Corvol P, Lifton RP, and Lalouel J-M. A molecular variant of angiotensinogen associated with preeclampsia (see comments). Nat Genet 4: 59–61, 1993.

    Article  PubMed  CAS  Google Scholar 

  105. Weil A. Mammalian evolution: upwards and onwards. Nature 416: 798–799, 2002.

    Article  PubMed  CAS  Google Scholar 

  106. Weinstein RS and Haas JD. Early stress and later reproductive performance under conditions of malutrition and high altitude hypoxia. Medical Anthropology 1: 25–54, 1977.

    Article  Google Scholar 

  107. White MM, McCullough RE, Dyckes R, Robertson AD, and Moore LG. Chronic hypoxia, pregnancy, and endothelium-mediated relaxation in guinea pig uterine and thoracic arteries. Am J Physiol Heart Circ Physiol 278: H2069–H2075, 2000.

    PubMed  CAS  Google Scholar 

  108. White MM, McCullough RE, Dyckes R, Robertson AD, and Moore LG. Effects of pregnancy and chronic hypoxia on contractile responsiveness to a-1-adrenergic stimulation. Journal of Applied Physiology 85: 2322–2329, 1998.

    PubMed  CAS  Google Scholar 

  109. Wilcox AJ. Birth weight and perinatal mortality: the effect of maternal smoking. American Journal of Epidemiology 137: 1098–1104, 1993.

    PubMed  CAS  Google Scholar 

  110. Williams RL, Creasy RK, Cunningham GC, Hawes WE, Norris FD, and Tashiro M. Fetal growth and perinatal viability in California. Obstetrics and Gynecology 59: 624–632, 1982.

    PubMed  CAS  Google Scholar 

  111. Zamudio S, Palmer SK, Droma T, Stamm E, Coffin C, and Moore LG. Effect of altitude on uterine artery blood flow during normal pregnancy. Journal of Applied Physiology 79: 7–14, 1995.

    PubMed  CAS  Google Scholar 

  112. Zamudio S, Palmer SK, Stamm E, Coffin C, and Moore LG. Uterine blood flow at high altitude. In: Hypoxia and the Brain, edited by Sutton JR and Houston CS. Burlington, VT, USA: Queen City Press, 1995, p. 112–124.

    Google Scholar 

  113. Zhang L and Ziao D. Effects of chronic hypoxia on Ca2+ mobilization and Ca2+ sensitivity of myofilaments in uterine arteries. Am J Physiol Heart Circ Physiol 274: H132–H138, 1998.

    CAS  Google Scholar 

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© 2006 Springer Science+Business Media, LLC

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Moore, L.G., Shriver, M., Bemis, L., Vargas, E. (2006). An Evolutionary Model for Identifying Genetic Adaptation to High Altitude. In: Roach, R.C., Wagner, P.D., Hackett, P.H. (eds) Hypoxia and Exercise. Advances in Experimental Medicine and Biology, vol 588. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-34817-9_10

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