Impaired acclimatization to chronic hypoxia in adult male and female rats following neonatal hypoxia

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 297, Issue 2, 2009, Pages

  Lumbroso, Delphine ^a   Joseph, Vincent ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b Université Laval   (Canada)

Author keywords

Chronic mountain sickness; Hypoxic ventilatory acclimatization; Neonatal hypoxia

Indexed keywords

ACCLIMATIZATION; ADOLESCENT; ALTITUDE DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREATHING PATTERN; CONTROLLED STUDY; FEMALE; GENDER; HEART RIGHT VENTRICLE HYPERTROPHY; HEMATOCRIT; HEMOGLOBIN BLOOD LEVEL; HYPOXIA; LUNG MINUTE VOLUME; MALE; METABOLIC RATE; NEWBORN; NEWBORN HYPOXIA; NONHUMAN; PRIORITY JOURNAL; PULMONARY HYPERTENSION; RAT;

ACCLIMATIZATION; AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; ANOXIA; BASAL METABOLISM; BODY TEMPERATURE; BODY WEIGHT; CHRONIC DISEASE; FEMALE; HEART; HEMATOCRIT; HEMOGLOBINS; HYPERTROPHY, RIGHT VENTRICULAR; MALE; ORGAN SIZE; PULMONARY GAS EXCHANGE; PULMONARY VENTILATION; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY MECHANICS; SEX CHARACTERISTICS; TIDAL VOLUME;

EID: 68049092131     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00068.2009     Document Type: Article

References (54)

1. Aaron E, Powell F. Effect of chronic hypoxia on hypoxic ventilatory response in awake rats. J Appl Physiol 74: 1635-1640, 1993.
2. Baig MS, Joseph V. Activation of NMDA receptors prevents excessive metabolic decrease in hypoxic rat pups. Respir Physiol Neurobiol 152: 61-71, 2006.
3. Barker DJ. The origins of the developmental origins theory. J Intern Med 261: 412-417, 2007.
4. Bartlett D, Tenney SM. Control of breathing in experimental anemia. Respir Physiol 10: 384-395, 1970.
5. Bavis RW, Mitchell GS. Long-term effects of the perinatal environment on respiratory control. J Appl Physiol 104: 1220-1229, 2008.
6. Bavis RW, Olson EB Jr, Vidruk EH, Fuller DD, Mitchell GS. Developmental plasticity of the hypoxic ventilatory response in rats induced by neonatal hypoxia. J Physiol 557: 645-660, 2004.
7. Bayliss DA, Cidlowski JA, Millhorn DE. The stimulation of respiration by progesterone in ovariectomized cat is mediated by an estrogen-dependent hypothalamic mechanism requiring gene expression. Endocrinology 126: 519-527, 1990.
8. Bayliss DA, Millhorn DE, Gallman EA, Cidlowski JA. Progesterone stimulates ventilation through a central nervous system steroid receptor-mediated mechanism in the cat. Proc Natl Acad Aci USA 84: 7788-7792, 1987.
9. Beall CM. Two routes to functional adaptation: Tibetan and Andean high-altitude natives. Proc Natl Acad Sci USA 104, Suppl 1: 8655-8660, 2007.
10. Bee D, Pallot DJ. Acute hypoxic ventilation, carotid body cell division, and dopamine content during early hypoxia in rats. J Appl Physiol 79: 1504-1511, 1995.
11. Bernardi L, Roach RC, Keyl C, Spicuzza L, Passino C, Bonfichi M, Gamboa A, Gamboa J, Malcovati L, Schneider A, Casiraghi N, Mori A, Leon-Velarde F. Ventilation, autonomic function, sleep and erythropoietin Chronic mountain sickness of Andean natives. Adv Exp Med Biol 543: 161-175, 2003.
12. Busch MA, Bisgard GE, Forster HV. Ventilatory acclimatization to hypoxia is not dependant on arterial hypoxemia. J Appl Physiol 58: 1874-1880, 1985.
13. Carroll JL. Plasticity in respiratory motor control: developmental plasticity in respiratory control. J Appl Physiol 94: 375-389, 2003.
14. Chiodi H. Respiratory adaptations to chronic high altitude hypoxia. J Appl Physiol 10: 81-87, 1957.
15. Doan VD, Gagnon S, Joseph V. Prenatal blockade of estradiol synthesis impairs respiratory and metabolic responses to hypoxia in newborn and adult rats. Am J Physiol Regul Integr Comp Physiol 287: R612-R618, 2004.
16. Genest SE, Gulemetova R, Laforest S, Drolet G, Kinkead R. Neonatal maternal separation and sex-specific plasticity of the hypoxic ventilatory response in awake rat. J Physiol 554: 543-557, 2004.
17. Hannhart B, Pickett CK, Moore LG. Effects of estrogen and progesterone on carotid body neural output responsiveness to hypoxia. J Appl Physiol 68: 1909-1916, 1990.
18. He L, Chen J, Dinger B, Stensaas L, Fidone S. Effect of chronic hypoxia on purinergic synaptic transmission in rat carotid body. J Appl Physiol 100: 157-162, 2006.
19. He L, Dinger B, Fidone S. Effect of chronic hypoxia on cholinergic chemotransmission in rat carotid body. J Appl Physiol 98: 614-619, 2005.
20. Heinicke K, Baum O, Ogunshola OO, Vogel J, Stallmach T, Wolfer DP, Keller S, Weber K, Wagner PD, Gassmann M, Djonov V. Excessive erythrocytosis in adult mice overexpressing erythropoietin leads to hepatic, renal, neuronal, and muscular degeneration. Am J Physiol Regul Integr Comp Physiol 291: R947-R956, 2006.
21. Huey KA, Brown IP, Jordan MC, Powell FL. Changes in dopamine D(2)-receptor modulation of the hypoxic ventilatory response with chronic hypoxia. Respir Physiol 123: 177-187, 2000.
22. Jefferson JA, Escudero E, Hurtado ME, Pando J, Tapia R, Swenson ER, Prchal J, Schreiner GF, Schoene RB, Hurtado A, Johnson RJ. Excessive erythrocytosis, chronic mountain sickness, and serum cobalt levels. Lancet 359: 407-408, 2002.
23. Joseph V, Doan VD, Morency CE, Lajeunesse Y, Bairam A. Expression of sex-steroid receptors and steroidogenic enzymes in the carotid body of adult and newborn male rats. Brain Res 1073-1074: 71-82, 2006.
24. Joseph V, Pequignot JM. Neurochemical processes involved in acclimatization to long term hypoxia. In: Oxygen sensing: Responses and adaptation to hypoxia, edited by Lahiri S, Semenza GL, and Prabhakar NR. New York: Dekker, 2003, p. 467-488.
25. Joseph V, Soliz J, Pequignot J, Sempore B, Cottet-Emard JM, Dalmaz Y, Favier R, Spielvogel H, Pequignot JM. Gender differentiation of the chemoreflex during growth at high altitude: functional and neurochemical studies. Am J Physiol Regul Integr Comp Physiol 278: R806-R816, 2000.
26. Joseph V, Soliz J, Soria R, Pequignot J, Favier R, Spielvogel H, Pequignot JM. Dopaminergic metabolism in carotid bodies and high altitude acclimatization in female rats. Am J Physiol Regul Integr Comp Physiol 282: R765-R773, 2002.
27. Lahiri S, Edelman NH. Peripheral chemoreflexes in the regulation of breathing of high altitude natives. Respir Physiol 6: 375-385, 1969.
28. Lahiri S, Edelman NH, Cherniack NS, Fishman AP. Role of carotid chemoreflex in respiratory acclimatization to hypoxemia in goat and sheep. Respir Physiol 46: 367-382, 1981.
29. Leon-Velarde F, Maggiorini M, Reeves JT, Aldashev A, Asmus I, Bernardi L, Ge RL, Hackett P, Kobayashi T, Moore LG, Penaloza D, Richalet JP, Roach R, Wu T, Vargas E, Zubieta-Castillo G, Zubieta-Calleja G. Consensus statement on chronic and subacute high altitude diseases. High Alt Med Biol 6: 147-157, 2005.
30. León-Velarde F, Ramos MA, Hernández JA, De Idiáquez D, Muñoz LS, Gaffo A, Córdova S, Durand D, Monge-CC. The role of menopause in the development of chronic mountain sickness. Am J Physiol Regul Integr Comp Physiol 272: R90-R94, 1997.
31. León-Velarde F, Rivera-Chira M, Tapia R, Huicho L, Monge-CC. Relationship of ovarian hormones to hypoxemia in women residents of 4,300 m. Am J Physiol Regul Integr Comp Physiol 280: R488-R493, 2001.
32. Montandon G, Bairam A, Kinkead R. Neonatal caffeine induces sex-specific developmental plasticity of the hypoxic respiratory chemoreflex in adult rats. Am J Physiol Regul Integr Comp Physiol 295: R922-R934, 2008.
33. Moore LG, Niermeyer S, Vargas E. Does chronic mountain sickness (CMS) have perinatal origins? Respir Physiol Neurobiol 158: 180-189, 2007.
34. Mortola JP, Saiki C. Ventilatory response to hypoxia in rats: gender differences. Respir Physiol 106: 21-34, 1996.
35. Mukundan H, Resta TC, Kanagy NL. 17β-Estradiol decreases hypoxic induction of erythropoietin gene expression. Am J Physiol Regul Integr Comp Physiol 283: R496-R504, 2002.
36. Okubo S, Mortola JP. Control of ventilation in adult rats hypoxic in the neonatal period. Am J Physiol Regul Integr Comp Physiol 259: R836-R841, 1990.
37. Olson EB Jr., Dempsey JA. Rat as a model for humanlike ventilatory adaptation to chronic hypoxia. J Appl Physiol 44: 763-769, 1978.
38. Olson LG, Saunders NA. Effect of a dopamine antagonist on ventilation during sustained hypoxia in mice. J Appl Physiol 62: 1222-1226, 1987.
39. Ou LC, Sardella GL, Leiter JC, Brinck-Johnsen, Smith RP. Role of sex hormones in the development of chronic mountain sickness in rats. J Appl Physiol 77: 427-433, 1994.
40. Ou LC, Smith RP. Strain and sex difference in the cardiopulmonary adaptation of rats to high altitude. Proc Soc Exp Biol Med 177: 308-311, 1984.
41. Powell FL, Huey KA, Dwinell MR. Central nervous system mechanisms of ventilatory acclimatization to hypoxia. Respir Physiol 121: 223-236., 2000.
42. Powell FL, Milsom WK, Mitchell GS. Time domains of the hypoxic ventilatory response. Respir Physiol 112: 123-134, 1998.
43. Rabinovitch M, Gamble WJ, Miettinen OL, Reid L. Age and sex influence on pulmonary hypertension of chronic hypoxia and on recovery. Am J Physiol Heart Circ Physiol 240: H62-H72, 1981.
44. Schmitt P, Soulier V, Pequignot JM, Pujol JF, Denavit-Saubie M. Ventilatory acclimatization to chronic hypoxia: relationship to noradrenaline metabolism in the rat solitary complex. J Physiol (Lond) 477: 331-337, 1994.
45. Severinghaus JW, Bainton GR, Carcelen A. Respiratory insensitivity to hypoxia in chronically hypoxic man. Respir Physiol 1: 308-334, 1966.
46. Sladek M, Parker RA, Grogaard JB, Sundell HW. Long-lasting effect of prolonged hypoxemia after birth on the immediate ventilatory response to changes in arterial partial pressure of oxygen in young lambs. Pediatr Res 34: 821-828, 1993.
47. Smith C, Bisgard G, Nielsen A, Daristotle L, Kressin N, Forster H, Dempsey J. Carotid bodies are requiered for ventilatory acclimatization to chronic hypoxia. J Appl Physiol 60: 1003-1010, 1986.
48. Soliz J, Gassmann M, Joseph V. Soluble erythropoietin receptor is present in the mouse brain and is required for the ventilatory acclimatization to hypoxia. J Physiol 583: 329-336, 2007.
49. Tatsumi K, Pickett CK, Jacoby CR, Weil JV, Moore LG. Role of endogenous female hormones in hypoxic chemosensitivity. J Appl Physiol 83: 1706-1710, 1997.
50. Tatsumi K, Pickett CK, Weil JV. Decreased carotid body hypoxic sensitivity in chronic hypoxia: role of dopamine. Respir Physiol 101: 47-57, 1995.
51. Tatsumi K, Pickett CK, Weil JV. Possible role of dopamine in ventilatory acclimatization to high altitude. Respir Physiol 99: 63-73, 1995.
52. Tenney SM, Ou LC. Hypoxic ventilatory response of cats at high altitude: an interpretation of "blunting." Respir Physiol 30: 185-199, 1977.
53. Vargas E, Spielvogel H. Chronic mountain sickness, optimal hemoglobin, and heart disease. High Alt Med Biol 7: 138-149, 2006.
54. Weil JV. Ventilatory control at high altitude. In: Handbook of Physiology: The Respiratory System. Control of Breathing. Bethesda, MD: Am Physiol Soc, 1986, sec. 3, vol. II, pt. 2, chapt. 21, p. 703-728.