Physiological and genomic consequences of intermittent hypoxia: Invited review: Intermittent hypoxia and respiratory plasticity

Journal of Applied Physiology

Volumn 90, Issue 6, 2001, Pages 2466-2475

  Mitchell, Gordon S ^a,c   Baker, Tracy L ^a,c   Nanda, Steven A ^b,c   Fuller, David D ^a   Zabka, Andrea G ^a   Hodgeman, Brad A ^a   Bavis, Ryan W ^a   Mack, Kenneth J ^b,c   Olson Jr , E B ^c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Brain derived neurotrophic factor; Episodic hypoxia; Neurotrophins; Respiratory control; Serotonin

Indexed keywords

NEUROTROPHIC FACTOR; NEUROTROPHIN; SEROTONIN RECEPTOR;

AGE; GENETIC ANALYSIS; HUMAN; HYPOXIA; INSPIRATORY CAPACITY; MOTONEURON; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RESPIRATION CONTROL; REVIEW; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SYNAPSE; ANIMAL; ANOXIA; INNERVATION; NERVE CELL PLASTICITY; PATHOPHYSIOLOGY; PHYSIOLOGY; RESPIRATORY FUNCTION; RESPIRATORY SYSTEM;

ANIMALS; ANOXIA; HUMANS; NEURONAL PLASTICITY; RESPIRATORY PHYSIOLOGY; RESPIRATORY SYSTEM;

EID: 0035374489     PISSN: 87507587     EISSN: None     Source Type: Journal    
DOI: 10.1152/jappl.2001.90.6.2466     Document Type: Review

References (112)

1. Abraham WC and Bear MF. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19: 126-130, 1996.
2. Altar CA, Boylan CB, Fritsche M, Jackson C, Hyman C, and Lindsay RM. The neurotrophins NT-4/5 and BDNF augment serotonin, dopamine, and GABAergic systems during behaviorally effective infusions to the substantia nigra. Exp Neurol 130: 31-40, 1994.
3. Babcock MA and Badr MS. Long-term facilitation of ventilation in humans during NREM sleep. Sleep 21: 709-716, 1998.
4. Bach KB, Johnson RA, Kinkead R, Fuller DD, Zhan W, Mantilla C, Sieck GC, and Mitchell GS. Cervical dorsal rhizotomy enhances serotonin-dependent long-term facilitation of hypoglossal motor output in rats. FASEB J 14: A77, 2000.
5. Bach KB, Kinkead R, Ling L, Olson EB, and Mitchell GS. Ketanserin blocks the effects of chronic intermittent hypoxia on the short term hypoxic phrenic response but not long term facilitation (Abstract). FASEB J 13: A166, 1999.
6. 2-adrenoreceptor antagonism. Brain Res 817: 25-33, 1999.
7. Bach KB and Mitchell GS. Effects of phrenicotomy and exercise on hypoxia-induced changes in phrenic motor output. J Appl Physiol 89: 1884-1891, 2000.
8. Bach KB and Mitchell GS. Hypoxia-induced long-term facilitation of respiratory activity is serotonin dependent. Respir Physiol 104: 251-260, 1996.
9. Baker TL and Mitchell GS. Episodic but not continuous hypoxia elicits long-term facilitation of phrenic motor output in rats. J Physiol (Lond) 15: 215-219, 2000.
10. Baker TL and Mitchell GS. Spinal protein synthesis inhibition attenuates serotonin dependent long-term facilitation of phrenic motor output. Soc Neurosci Abstr 26: 1458, 2000.
11. Baker TL and Mitchell GS. Spinal serotonin receptor activation is necessary for phrenic long-term facilitation following episodic hypoxia (Abstract). FASEB J 15: A422, 2001.
12. Balkowiec A and Katz DM. Activity-dependent release of endogenous brain derived neurotrophic factor from primary sensory neurons detected by ELISA in situ. J Neurosci 20: 7417-7423, 2000.
13. Beck CDO, Schroeder B, and Davis L. Learning performance of normal and mutant Drosophila after repeated conditioning trials with discrete stimuli. J Neurosci 20: 2944-2953, 2000.
14. Bisgard GE. Carotid body mechanisms in acclimatization to hypoxia. Respir Physiol 121: 237-246, 2000.
15. Bisgard GE and Forster HV. Ventilatory responses to acute and chronic hypoxia. In: Handbook of Physiology. Environmental Physiology. Bethesda, MD: Am. Physiol. Soc., 1996, sect. 4, vol V, chapt, 52, p. 1207-1239.
16. Bisgard GE and Neubauer JA. Peripheral and central effects of hypoxia. In: Lung Biology in Health and Disease. Regulation of Breathing: Central Nervous System, edited by Dempsey JA and Pack AI. New York: Marcel Dekker, 1995, vol. 79, p. 617-668.
17. Bixler EO, Vgontzas AN, Lin H-M, Have TT, Rein J, Vela-Bueno A, and Kales A. Prevalence of sleep disordered breathing in women: effects of gender. Am J Resp Crit Care Med 163: 608-613, 2001.
18. Black IB. Trophic regulation of synaptic plasticity. J Neurobiol 41: 108-118, 1999.
19. Byrne JH. Plastic plasticity. Nature 389: 791-792, 1997.
20. Byrne JH and Kandel ER. Presynaptic facilitation revisited: state and time dependence. J Neurosci 16: 425-435, 1996.
21. Cao K-Y, Zwillich CW, Berthon-Jones M, and Sullivan CE. Increased normoxic ventilation induced by repetitive hypoxia in conscious dogs. J Appl Physiol 73: 2083-2088, 1992.
22. Clark FM and Proudfit HK. Anatomical evidence for genetic differences in the innervation of the rat spinal cord by noradrenergic locus coeruleus. Brain Res 591: 44-53, 1992.
23. Coplan JD and Lydiard RB. Brain circuits in panic disorder. Biol Psychiatry 44: 1264-1276, 1998.
24. Dolmetsch RE, Xu K, and Lewis RS. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392: 933-936, 1998.
25. Dwinell MR, Janssen PL, and Bisgard GE. Lack of long term facilitation of ventilation after exposure to hypoxia in goats. Respir Physiol 108: 1-9, 1997.
26. Dwinell MR and Powell FL. Chronic hypoxia enhances the phrenic nerve response to arterial chemoreceptor stimulation in anesthetized rats. J Appl Physiol 87: 817-823, 1999.
27. Dwinell MR and Powell FL. Long-term facilitation can be elicited following chronic hypoxia in rats (Abstract). FASEB J 13: A166, 1999.
28. Engwall MJ and Bisgard GE. Ventilatory responses to chemoreceptor stimulation after hypoxic acclimatization in awake goats. J Appl Physiol 69: 1236-1243, 1990.
29. Fitzgerald RS and Lahiri S. Reflex responses to chemoreceptor stimulation. In: Handbook of Physiology. The Respiratory System. Control of Breathing. Bethesda, MD: Am. Physiol. Soc., 1986, sect. 3, vol. 2, pt, 1, chapt. 10, p. 313-362.
30. Fregosi RF and Mitchell GS. Long-term facilitation of inspiratory intercostal nerve activity following carotid sinus nerve stimulation in cats. J Physiol (Lond) 477: 469-479, 1994.
31. Freudenthal R and Romano A. Participation of Rel/NF-κB transcription factors in long-term memory in the crab Chasmagnathus. Brain Res 855: 274-281, 2000.
32. Fuller DD, Bach KB, Baker TL, Kinkead R, and Mitchell GS. Long term facilitation of phrenic motor output. Respir Physiol 121: 135-146, 2000.
33. Fuller DD, Baker TL, Behan M, and Mitchell GS. Expression of hypoglossal long-term facilitation differs between substrains of Sprague-Dawley rat. Physiol Genomics 4: 175-181, 2001.
34. Fuller DD, Zabka AZ, Baker TL, and Mitchell GS. Phrenic long-term facilitation requires 5-HT receptor activation during but not following episodic hypoxia. J Appl Physiol In press.
35. Gallman EA and Millhorn DE. Two long-lasting central respiratory responses following acute hypoxia in glomectomized cats. J Physiol (Lond) 395: 333-347, 1988.
36. Garcia N, Hopkins SR, and Powell FL. Effects of intermittent hypoxia on the isocapnic hypoxic ventilatory response and erythropoiesis in humans. Respir Physiol 123: 39-49, 2000.
37. Gardiol A, Racca C, and Triller A. Dendritic and postsynaptic protein synthetic machinery. J Neurosci 19: 168-179, 1999.
38. Gerhardt CC and van Heerikhuizen H. Functional characteristics of heterologously expressed 5-HT receptors. Eur J Pharmacol 334: 1-23, 1997.
39. Ghirardi Montarolo M, PG, and Kandel ER. A novel intermediate stage in the transition between short and long-term facilitation in the sensory to motor neuron synapse of aplysia. Neuron 14: 413-420, 1995.
40. Gozal E and Gozal D. Respiratory plasticity following intermittent hypoxia: developmental interactions. J Appl Physiol 90: 1995-1999, 2001.
41. Gozal D and Gozal E. Episodic hypoxia enhances late hypoxic ventilation in developing rat: putative role of neuronal NO synthase. Am J Physiol Regulatory Integrative Comp Physiol 276: R17-R22, 1999.
42. Hayashi F, Coles SK, Bach KB, Mitchell GS, and McCrimmon DR. Time-dependent phrenic nerve responses to carotid afferent activation: intact vs. decerebellate rate. Am J Physiol Regulatory Integrative Comp Physiol 265: R811-R819, 1993.
43. Hermitte Pedreira G, ME, Tomsic D, and Maldonado H. Context shift and protein synthesis inhibition disrupt long-term habituation after spaced, but not massed training in the crab Chasmagnathus. Neurobiol Learn Mem 71: 34-49, 1999.
44. Hoyer D, Clarke DE, Fozard JR, Hartig PR, Martin GR, Mylacharane EJ, Saxena PR, and Humphrey PPA. International union of pharmacology classification of receptors for 5-hydroxytryptamine (serotonin). Pharmacol Rev 46: 157-203, 1994.
45. Hoyer D and Martin G. 5-HT receptor classification and nomenclature: towards a harmonization with the human genome. Neuropharmacology 36: 419-428, 1997.
46. Huang YY and Kandel ER. Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization. Learn Mem 1: 74-82, 1994.
47. Janssen PL and Fregosi RF. No evidence for long-term facilitation after episodic hypoxia in spontaneously breathing, anesthetized rats. J Appl Physiol 89: 1345-1351, 2000.
48. Jiang C, Mitchell GS, and Lipski J. Prolonged augmentation of respiratory discharge in hypoglossal motoneurons following superior laryngeal nerve stimulation. Brain Res 538: 215-225, 1991.
49. Johnson RA and Mitchell GS. Exercise increases brain-derived neurotrophic factor (BDNF) and decreases neurotrophin-3 (NT-3) in the rat ventral spinal cord. Federation Proc 15: A428, 2001.
50. Johnson RA, Okragly AJ, Haak-Frendscho M and Mitchell GS. Spinal sensory denervation increases BDNF and NT-3 expression in the ventral spinal cord. J Neurosci 20: 1-5, 2000.
51. Katayama K, Sato Y, Ishida K, Mori S, and Miyamura M. The effects of intermittent exposure to hypoxia during endurance exercise training on the ventilatory responses to hypoxia and hypercapnia in humans. Eur J Appl Physiol 78: 189-194, 1998.
52. Katz PS and Edwards DH. Metamodulation: the control and modulation of neuromodulation. In: Beyond Neurotransmission, edited by Katz PS. New York: Oxford Univ. Press, 1999, p. 349-381.
53. Kim JJ and Yoon KS. Stress: metaplastic effects in the hippocampus. Trends Neurosci 21: 505-509, 1998.
54. Kinkead R and Mitchell GS. Time-dependent hypoxic ventilatory responses in rats: effects of ketansterin and 5-carboxyamidotryptamine. Am J Physiol Regulatory Integrative Comp Physiol 277: R658-R666, 1999.
55. Kinkead R, Zhan WZ, Prakash YS, Bach KB, Sieck GC, and Mitchell GS. Cervical dorsal rhizotomy enhances serotonergic innervation of phrenic motoneurons and serotonin-dependent long-term facilitation of respiratory motor output in rats. J Neurosci 18: 8436-8443, 1998.
56. Kline DD and Prabhakar NR. Importance of nitric oxide from NOS-1 in short and long-term potentiation of respiration following hypoxia. FASEB J 14: A78, 2000.
57. Kogan JH, Frankland PW, Blendy JA, Coblentz J, Marowitz Z, Schutz G, and Silva AJ. Spaced training induces normal long-term memory in CREB mutant mice. Curr Biol 1: 1-11, 1997.
58. Lindholm D. Neurotrophic factors and neuronal plasticity: is there a link? Adv Neurol 73: 1-6, 1997.
59. Ling L, Olson EB, Johnson SM, and Mitchell GS. Phrenic responses to electrical stimulation of carotid sinus nerve in rats following chronic intermittent hypoxia (Abstract). FASEB J 14: A77, 2000.
60. Ling L, Bach KB, Kinkead R, Olson, EB Jr, and Mitchell GS. Enhancement of the hypoxic ventilatory responses following chronic intermittent hypoxia is serotonin dependent (Abstract). FASEB J 13: A166, 1999.
61. Ling L, Olson EB, and Mitchell GS. Chronic intermittent hypoxia enhances the hypoxic ventilatory control system (Abstract). FASEB J 12: A781, 1998.
62. Ling L, Olson EB, Vidruk EH, and Mitchell GS. Integrated phrenic responses to carotid afferent stimulation in adult rats following perinatal hyperoxia. J Physiol (Lond) 500: 787-796, 1997.
63. Mamounas LA, Altar CA, Blue ME, Kaplan DR, Tessarollo L, and Lyons WE. BDNF promotes the regenerative sprouting, but not survival, of injured serotonergic axons in the adult rat brain. J Neurosci 20: 771-782, 2000.
64. Mamounas LA, Blue ME, and Siusiak JA. Brain-derived neurotrophic factor promotes the survival and sprouting of serotonergic axons in rat brain. J Neurosci 15: 7929-7939, 1995.
65. Martin PA and Mitchell GS. Long term modulation of the exercise ventilatory response. J Physiol (Lond) 470: 601-617, 1993.
66. Mateika JH and Fregosi RF. Long-term facilitation of upper airway muscle activities in vagotomized and vagally intact cats. J Appl Physiol 82: 419-425, 1997.
67. Mauelshagen J, Sherff CM, and Carew TJ. Differential induction of long-term synaptic facilitation by spaced and massed applications of serotonin at sensory neuron synapses of Aplysia californica. Learn Mem 5: 246-256, 1998.
68. Mauelshagen J, Parker GR, and Carew TJ. Dynamics of induction and expression of long-term synaptic facilitation in Aplysia. J Neurosci 16: 7099-7108, 1996.
69. McCrimmon DR, Dekin MS, and Mitchell GS. Glutamate, GABA, and serotonin in ventilatory control. In: Lung Biology in Health and Disease. Regulation of Breathing: Central Nervous System, edited by Dempsey JA and Pack AI. New York: Marcel Dekker, 1995, vol. 79, p. 151-218.
70. McEvoy RD, Popovic RM, Saunders NA, and White DP. Effects of sustained and repetitive isocapnic hypoxia on ventilation and gengiolossal and diaphragmatic EMGs. J Appl Physiol 81: 866-875, 1996.
71. McNamara SG, Aarts MJ, Becker H, Cao K, Polo OJ, and Sullivan CE. Ventilatory responses to repetitive hypoxia in subjects with obstructive sleep apnea (Abstract). Am J Respir Crit Care Med 151: A100, 1995.
72. Meldolesi J. Oscillation, activation, expression. Nature 392: 863-866, 1998.
73. Mellins RB, Balfour HH, Turino GM, and Winters RW. Failure of automatic control of ventilation (Ondine's curse). Medicine 49: 487-504, 1990.
74. Millhorn DE. Stimulation of raphe (obscurus) nucleus causes long-term potentiation of phrenic nerve activity in cat. J Physiol (Lond) 381: 169-179, 1986.
75. Millhorn DE, Eldridge FL, and Waldrop TG. Prolonged stimulation of respiration by a new central neural mechanism. Respir Physiol 41: 87-103, 1980.
76. Millhorn DE, Eldridge FL, and Waldrop TG. Prolonged stimulation of respiration by endogenous central serotonin. Respir Physiol 42: 171-198, 1980.
77. Mitchell GS, Bach KB, Martin PA, and Foley KT. Modulation and plasticity of the exercise ventilatory response. Functionsanalyse Biologischer Systeme 23: 269-277, 1993.
78. Mitchell GS, Powell FL, Hopkins SR, and Milsom WK. Time domains of the hypoxic ventilatory response in ducks: short-term and episodic hypoxia. Respir Physiol 124: 117-128, 2001.
79. Morris KF, Arata A, Shannon R, Lindsey BG. Long-term facilitation of phrenic nerve activity in cats: responses and short time scale correlations of medullary neurones. J Physiol (Lond) 490: 463-480, 1996.
80. Morris KF, Baekey DM, Shannon R, and Lindsey BG. Respiratory neural activity during long-term facilitation. Respir Physiol 121: 119-33, 2000.
81. Moss IR. Respiratory responses to single and episodic hypoxia during development: mechanisms of adaptation. Respir Physiol 121: 185-197, 2000.
82. Muzzio IA, Ramirez RR, Talk AC, and Matzel LD. Interactive contributions of intracellular calcium and protein phosphatases to massed-trials learning deficits in Hermissenda. Behav Neurosci 113: 103-117, 1999.
83. Olson E Jr, Bohne C, Dwinell M, Podolsky A, Vidruk E, Fuller D, Powell F, and Mitchell G. Ventilatory long-term facilitation in unanesthetized rats. J Appl Physiol In press.
84. Olson EB. Ventilatory adaptation to hypoxia occurs in serotonin-depleted rats. Respir Physiol 69: 227-235, 1987.
85. Papp LA, Klein DF, and Gorman JM. Carbon dioxide hyposensitivity, hyperventilation and panic disorder. Am J Psychiatry 150: 1149-1157, 1993.
86. Poo M-M. Neurotrophins as synaptic modulators. Nat Neurosci 2: 1-9, 2001.
87. Powell FL, Huey KA, and Dwinell MR. Central nervous system mechanisms of ventilatory acclimatization to hypoxia. Respir Physiol 121: 223-236, 2000.
88. Powell FL, Milsom WK, and Mitchell GS. Time domains of the hypoxic ventilatory response. Respir Physiol 112: 123-134, 1998.
89. Putney JW. Calcium signaling: up, down, up, down . . . what's the point? Science 279: 191-192, 1998.
90. Richerson GB. Sudden infant death syndrome: the role of central chemosensitivity. Neuroscientist 3: 3-7, 1997.
91. Sabban EL and Kvetnansky R. Stress-triggered activation of gene expression in catecholaminergic systems: dynamics of transcriptional events. Trends Neurosci 24: 91-98, 2001.
92. Sandoz JC, Roger B, and Pham-Delegue MH. Olfactory learning and memory in the honeybee: comparison of different classical conditioning procedures of the proboscis extension response. CR Acad Sci 318: 749-755, 1995.
93. Schinder AF and Poo M-M. The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci 23: 639-645, 2000.
94. Serebrovskaya TV, Karaban IN, Kolesnikova EE, Mishunina TM, Kuzminskaya LA, Serebrovsky AN, and Swanson RJ. Human hypoxic ventilatory response with blood dopamine content under intermittent hypoxic training. Can J Pharmacol 77: 967-973, 1999.
95. Serebrovskaya T, Karaban I, Mankovskaya I, Bernardt L, Passino C, and Appenzeller O. Hypoxic ventilatory responses and gas exchange in patients with Parkinson's disease. Respiration 65: 28-33, 1998.
96. Serebrovskaia TV, Man'kovskaia IN, Lysenko GI, Swanson R, Belinskaia IV, Oberenko OA, and Daniliuk SV. A method for intermittent hypoxic exposures in the combined treatment of bronchial asthma patients. [Russian] Lik Sprava 6: 104-108, 1998.
97. Serebrovskaya TV, Swanson RJ, Karaban IN, Serebrovskaya ZA, and Kolesnikova EE. Intermittent hypoxia alters hypoxic ventilatory responses. Fiziol Zh 45: 9-18, 1999.
98. Siuciak JA, Boylan C, Fritsche M, Altar CA, and Lindsay RM. BDNF increases monoaminergic activity in rat brain following intracerebroventricular or intraparenchymal administration. Brain Res 710: 11-20, 1996.
99. Siuciak JA, Clark MS, Rind HB, Whittemore SR, and Russo AF. BDNF induction of tryptophan hydroxylase mRNA levels in the rat brain. J Neurosci Res 52: 149-158, 1998.
100. Strohl KP and Redline S. Recognition of sleep apnea. Am J Respir Crit Care Med 154: 279-289, 1996.
101. Thoenen H. Neurotrophins and neuronal plasticity. Science 270: 104-107, 1995.
102. Tongiorgi E, Righi M, and Cattaneo A. Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons. J Neurosci 17: 9492-9505, 1997.
103. Tun Y, Hida W, Okabe S, Kikuchi Y, Kurosawa H, Tabata M, and Shirato K. Effects of nasal continuous positive airway pressure on awake ventilatory responses to hypoxia and hypercapnia in patients with obstructive sleep apnea. Tohoku J Exp Med 190: 157-168, 2000.
104. Turner DL and Mitchell GS. Long-term facilitation of ventilation following repeated hypoxic episodes in awake goats. J Physiol (Lond) 499: 543-550, 1997.
105. 2A receptor-mediated regulation of brain-derived neurotrophic factor mRNA in the hippocampus and the neocortex. J Neurosci 17: 2785-2795, 1997.
106. Wang ZY, Baker TL, Keith IM, Mitchell GS, Bisgard GE. Continuous but not episodic hypoxia induces CREB phosphorylation in rat carotid body. Adv Exp Med Biol 475: 631-635, 2000.
107. Waters KA, Beardsmore CS, Paquette J, Meehan B, Cote A, and Moss IR. Respiratory responses to rapid-onset, repetitive vs. continuous hypoxia in piglets. Respir Physiol 105: 135-142, 1996.
108. Weese-Mayer DE, Silvestri JM, Marazita ML, and Hoo JJ. Congenital central hypoventilation syndrome: inheritance and relation to sudden infant death syndrome. Am J Med Genet 47: 360-367, 1993.
109. Zabka AG, Behan M, and Mitchell GS. Serotonin-dependent long-term facilitation of respiratory motor output decreases with age in male rats. J Physiol (Lond) 531: 509-514, 2001.
110. Zabka AG, Fuller DD, Baker TL, Behan M, and Mitchell GS. Influence of estrus cycle on phrenic and hypoglossal long term facilitation in female rats (Abstract). FASEB J 14: A77, 2000.
111. Zetterstrom TSC, Pei Q, Madhav TR, Coppell AL, Lewis L, and Grahame-Smith DG. Manipulations of brain 5-HT levels affect gene expression for BDNF in rat brain. Neuropharmacology 38: 1063-1073, 1999.
112. Zifa E and Pillion G. 5-Hydroxytryptamine receptors. Pharmacol Rev 44: 401-458, 1992.