Hypoxia-induced ventilatory responses in conscious mice: Gender differences in ventilatory roll-off and facilitation

Respiratory Physiology and Neurobiology

Volumn 185, Issue 3, 2013, Pages 497-505

  Palmer, Lisa A ^a   May, Walter J ^a   deRonde, Kimberly ^a   Brown Steinke, Kathleen ^a   Gaston, Benjamin ^a   Lewis, Stephen J ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Hypercapnia; Hypoxia; Male and female mice; Minute ventilation

Indexed keywords

AMBIENT AIR; ANIMAL MODEL; ARTICLE; ARTIFICIAL VENTILATION; BREATHING; FEMALE; HYPERCAPNIA; HYPOXIA; LUNG FUNCTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEX DIFFERENCE; TIDAL VOLUME;

ANIMALS; ANOXIA; CONSCIOUSNESS; FEMALE; HYPERCAPNIA; MALE; MICE; MICE, INBRED C57BL; PULMONARY VENTILATION; SEX CHARACTERISTICS;

EID: 84871732185     PISSN: 15699048     EISSN: 18781519     Source Type: Journal    
DOI: 10.1016/j.resp.2012.11.010     Document Type: Article

References (64)

1. Aitken M.L., Franklin J.L., Pierson D.J., Schoene R.B. Influence of body size and gender on control of ventilation. Journal of Applied Physiology 1986, 60:1894-1899.
2. Ainslie P.N., Ogoh S. Regulation of cerebral blood flow in mammals during chronic hypoxia: a matter of balance. Experimental Physiology 2010, 95:251-262.
3. Behan M., Wenninger J.M. Sex steroidal hormones and respiratory control. Respiratory Physiology and Neurobiology 2008, 164:213-221.
4. Biscoe T.J., Pallot D.J. The carotid body chemoreceptor: an investigation in the mouse. Quarterly Journal of Experimental Physiology 1982, 67:557-576.
5. Card J.W., Carey M.A., Bradbury J.A., DeGraff L.M., Morgan D.L., Moorman M.P., Flake G.P., Zeldin D.C. Gender differences in murine airway responsiveness and lipopolysaccharide-induced inflammation. Journal of Immunology 2006, 177:621-630.
6. Carey M.A., Card J.W., Bradbury J.A., Moorman M.P., Haykal-Coates N., Gavett S.H., Graves J.P., Walker V.R., Flake G.P., Voltz J.W., Zhu D., Jacobs E.R., Dakhama A., Larsen G.L., Loader J.E., Gelfand E.W., Germolec D.R., Korach K.S., Zeldin D.C. Spontaneous airway hyperresponsiveness in estrogen receptor-alpha-deficient mice. American Journal of Respiratory and Critical Care Medicine 2007, 175:126-135.
7. Dahan A., Sarton E., Teppema L., Olievier C. Sex-related differences in the influence of morphine on ventilatory control in humans. Anesthesiology 1998, 88:903-913.
8. 2 concentration on short term potentiation of breathing in humans. The Journal of Physiology (London) 1995, 488:803-813.
9. Dempsey J.A., Veasey S.C., Morgan B.J., O'Donnell C. Pathophysiology of sleep apnea. Physiological Reviews 2010, 90:47-112.
10. Donnelly D.F., Rigual R. Single-unit recordings of arterial chemoreceptors from mouse petrosal ganglia in vitro. Journal of Applied Physiology 2000, 88:1489-1495.
11. Fatemian M., Nieuwenhuijs D.J., Teppema L.J., Meinesz S., van der Mey A.G., Dahan A., Robbins P.A. The respiratory response to carbon dioxide in humans with unilateral and bilateral resections of the carotid bodies. The Journal of Physiology 2003, 549:965-973.
12. Fewell J.E., Konduri G.G. Repeated exposure to rapidly developing hypoxemia influences the interaction between oxygen and carbon dioxide in initiating arousal from sleep in lambs. Pediatric Research 1998, 24:28-33.
13. Fournier S., Allard M., Gulemetova R., Joseph V., Kinkead R. Chronic corticosterone elevation and sex-specific augmentation of the hypoxic ventilatory response in awake rats. The Journal of Physiology 2007, 584:951-962.
14. +. Journal of Applied Physiology 2010, 108:989-994.
15. Fuchs B., Dietrich A., Gudermann T., Kalwa H., Grimminger F., Weissmann N. The role of classical transient receptor potential channels in the regulation of hypoxic pulmonary vasoconstriction. Advances in Experimental Medicine and Biology 2010, 661:187-200.
16. Gonzalez C., Almaraz L., Obeso A., Rigual R. Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiological Reviews 1994, 74:829-898.
17. Guyenet P.G., Stornetta R.L., Bayliss D.A. Central respiratory chemoreception. Journal of Comparative Neurology 2010, 518:3883-3906.
18. Gassmann M., Tissot van Patot M., Soliz J. The neuronal control of hypoxic ventilation: erythropoietin and sexual dimorphism. Annals of the New York Academy of Sciences 2009, 1177:151-161.
19. Giannoni A., Emdin M., Bramanti F., Iudice G., Francis D.P., Barsotti A., Piepoli M., Passino C. Combined increased chemosensitivity to hypoxia and hypercapnia as a prognosticator in heart failure. Journal of the American College of Cardiology 2009, 53:1975-1980.
20. Gozal D., Gozal E., Simakajornboon N. Signaling pathways of the acute hypoxic ventilatory response in the nucleus tractus solitarius. Respiration Physiology 2000, 121:209-221.
21. Han F., Subramanian S., Dick T.E., Dreshaj I.A., Strohl K.P. Ventilatory behavior after hypoxia in C57BL/6J and A/J mice. Applied Physiology 2001, 91:1962-1970.
22. 2-ventilatory response of the anesthetized rat by rebreathing technique. Pflugers Archiv 1982, 393:77-82.
23. He L., Chen J., Dinger B., Fidone S. Characteristics of carotid body chemosensitivity in the mouse. Baseline studies for future experiments with knockout animals. Advances in Experimental Medicine and Biology 2000, 475:697-704.
24. He L., Chen J., Dinger B., Sanders K., Sundar K., Hoidal J., Fidone S. Characteristics of carotid body chemosensitivity in NADPH oxidase-deficient mice. American Journal of Physiology Cell Physiology 2002, 282:C27-C33.
25. 2 receptors. Journal of Applied Physiology 2000, 89:1142-1150.
26. Izumizaki M., Pokorski M., Homma I. Role of the carotid bodies in chemosensory ventilatory responses in the anesthetized mouse. Journal of Applied Physiology 2004, 97:1401-1407.
27. Joseph V., Soliz J., Soria R., Pequignot J., Favier R., Spielvogel H., Pequignot J.M. Dopaminergic metabolism in carotid bodies and high-altitude acclimatization in female rats. American Journal of Physiology Regulatory, Integrative and Comparative Physiology 2002, 282:R765-R773.
28. Kanbar R., Stornetta R.L., Cash D.R., Lewis S.J., Guyenet P.G. Photostimulation of Phox2b medullary neurons activates cardiorespiratory function in conscious rats. American Journal of Respiratory and Critical Care Medicine 2010, 182:1184-1194.
29. Kline D.D., Peng Y.J., Manalo D.J., Semenza G.L., Prabhakar N.R. Defective carotid body function and impaired ventilatory responses to chronic hypoxia in mice partially deficient for hypoxia-inducible factor 1 alpha. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:821-826.
30. Lahiri S., Roy A., Baby S.M., Hoshi T., Semenza G.L., Prabhakar N.R. Oxygen sensing in the carotid body. Progress in Biophysics and Molecular Biology 2006, 91:249-286.
31. Lahm T., Crisostomo P.R., Markel T.A., Wang M., Weil B.R., Novotny N.M., Meldrum D.R. The effects of estrogen on pulmonary artery vasoreactivity and hypoxic pulmonary vasoconstriction: potential new clinical implications for an old hormone. Critical Care Medicine 2008, 36:2174-2183.
32. Lindeman K.S., Freed A.N. Lemakalim attenuates hypocapnia- and dry air-induced bronchoconstriction in canine peripheral airways. Journal of Applied Physiology 1993, 75:86-92.
33. Liu L., Yan Y., Zeng M., Ahang J., Hanes M.A., Ahearn G., McMahon T.J., Dickfeld T., Marshall H.E., Que L.G., Stamler J.S. Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock. Cell 2004, 116:617-628.
34. Marcus C.L., Glomb W.B., Basinski D.J., Davidson S.L., Keens T.G. Developmental pattern of hypercapnic and hypoxic ventilatory responses from childhood to adulthood. Journal of Applied Physiology 1994, 76:314-320.
35. Martin-Body R.L. Brain transections demonstrate the central origin of hypoxic ventilatory depression in carotid body-denervated rats. The Journal of Physiology 1988, 407:41-52.
36. Massaro G.D., Mortola J.P., Massaro D. Sexual dimorphism in the architecture of the lung's gas-exchange region. Proceedings of the National Academy of Sciences of the United States of America 1995, 92:1105-1107.
37. Mellen N.M., Mishra D. Functional anatomical evidence for respiratory rhythmogenic function of endogenous bursters in rat medulla. Journal of Neuroscience 2010, 30:8383-8392.
38. Millhorn D.E., Eldridge F.L., Waldrop T.G. Prolonged stimulation of respiration by a new central neural mechanism. Respiration Physiology 1980, 41:87-103.
39. Mortola J.R., Saiki C. Ventilatory response to hypoxia in rats: gender differences. Respiration Physiology 1996, 106:21-34.
40. Moss I.R., Bélisle M., Laferrière A. Long-term recurrent hypoxia in developing rat attenuates respiratory responses to subsequent acute hypoxia. Pediatric Research 2006, 59:525-530.
41. Palmer L.A., May W.J., deRonde K., Brown-Steinke K., Bates J.N., Gaston B., Lewis S.J. Ventilatory responses during and following exposure to a hypoxic challenge in conscious mice deficient or null in S-nitrosoglutathione reductase. Respiratory Physiology and Neurobiology 2012, 10.1016/j.resp.2012.11.009.
42. 2 inhalation in Caucasians. Respiration Physiology 1972, 16:337-350.
43. Powell F.L., Milsom W.K., Mitchell G.S. Time domains of the hypoxic ventilatory response. Respiration Physiology 1998, 112:123-134.
44. 2 receptors. Journal of Applied Physiology 2007, 103:1269-1275.
45. Reinhard C., Eder G., Fuchs H., Ziesenis A., Heyder J., Schulz H. Inbred strain variation in lung function. Mammalian Genome 2002, 13:429-437.
46. 2 chemoreflex after carotid sinus nerve transection in rat. The Journal of Physiology 2000, 522:493-501.
47. Saaresranta T., Polo O. Hormones and breathing. Chest 2002, 122:2165-2182.
48. Schlenker E.H., Goldman M. Aspartic acid administered neonatally affects ventilation of male and female rats differently. Journal of Applied Physiology 1986, 61:780-784.
49. Schulz H., Johner C., Eder G., Ziesenis A., Reitmeier P., Heyder J., Balling R. Respiratory mechanics in mice: strain and sex specific differences. Acta Physiologica Scandinavica 2002, 174:367-375.
50. Soliz J., Soulage C., Borter E., van Patot M.T., Gassmann M. Ventilatory responses to acute and chronic hypoxia are altered in female but not male Paskin-deficient mice. American Journal of Physiology Regulatory, Integrative and Comparative Physiology 2008, 295:R649-R658.
51. Soliz J., Thomsen J.J., Soulage C., Lundby C., Gassmann M. Sex-dependent regulation of hypoxic ventilation in mice and humans is mediated by erythropoietin. American Journal of Physiology Regulatory, Integrative and Comparative Physiology 2009, 296:R1837-R1846.
52. Tankersley C.G. Selected contribution: variation in acute hypoxic ventilatory response is linked to mouse chromosome 9. Journal of Applied Physiology 2001, 90:615-622.
53. Tankersley C.G. Genetic aspects of breathing: on interactions between hypercapnia and hypoxia. Respiratory Physiology and Neurobiology 2003, 135:167-178.
54. Tankersley C.G., Broman K.W. Interactions in hypoxic and hypercapnic breathing are genetically linked to mouse chromosomes 1 and 5. Journal of Applied Physiology 2004, 97:77-84.
55. Teppema L.J., Dahan A. The ventilatory response to hypoxia in mammals: mechanisms, measurement, and analysis. Physiological Reviews 2010, 90:675-754.
56. Timmers H.J., Wieling W., Karemaker J.M., Lenders J.W. Denervation of carotid baro- and chemoreceptors in humans. The Journal of Physiology 2003, 553:3-11.
57. Vizek M., Pickett C.K., Weil J.V. Biphasic ventilatory response of adult cats to sustained hypoxia has central origin. Journal of Applied Physiology 1987, 63:1658-1664.
58. Wagner P.G., Eldridge F.L. Development of short-term potentiation of respiration. Respiration Physiology 1991, 83:129-139.
59. Wenninger J.M., Olson E.B., Cotter C.J., Thomas C.F., Behan M. Hypoxic and hypercapnic ventilatory responses in aging male vs. aging female rats. Journal of Applied Physiology 2009, 106:1522-1528.
60. Wetzel R.C., Herold C.J., Zerhouni E.A., Robotham J.L. Hypoxic bronchodilation. Journal of Applied Physiology 1992, 73:1202-1206.
61. White D.P., Douglas N.J., Pickett C.K., Weil J.V., Zwillich C.W. Sexual influence on the control of breathing. Journal of Applied Physiology 1983, 54:874-879.
62. Xu F., Zhuang J., Wang R., Seagrave J.C., March T.H. Blunted ventilatory response to hypoxia/hypercapnia in mice with cigarette smoke-induced emphysema. Respiratory Physiology and Neurobiology 2007, 158:5-13.
63. Yamauchi M., Kimura H., Strohl K.P. Mouse models of apnea: strain differences in apnea expression and its pharmacologic and genetic modification. Advances in Experimental Medicine and Biology 2010, 669:303-307.
64. Zwemer C.F., Song M.Y., Carello K.A., D'Alecy L.G. Strain differences in response to acute hypoxia: CD-1 versus C57BL/6J mice. Journal of Applied Physiology 2007, 102:286-293.