Chronic intermittent but not constant hypoxia decreases NAA/Cr ratios in neonatal mouse hippocampus and thalamus

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 292, Issue 3, 2007, Pages

  Douglas, Robert M ^a,b   Miyasaka, Naoyuki ^a   Takahashi, Kan ^a   Latuszek Barrantes, Adrianna ^a   Haddad, Gabriel G ^a,c   Hetherington, Hoby P ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Energy metabolism; Magnetic resonance imaging; Oxygen deprivation

Indexed keywords

CREATINE; N ACETYLASPARTIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN REGION; COGNITION; CONTROLLED STUDY; HIPPOCAMPUS; HYPOXIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SLEEP APNEA SYNDROME; THALAMUS;

ANIMALS; ANIMALS, NEWBORN; ASPARTIC ACID; CREATINE; FEMALE; HIPPOCAMPUS; HYPOXIA, BRAIN; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MICE, INBRED STRAINS; PREGNANCY; THALAMUS; TIME FACTORS;

EID: 33847703319     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00404.2006     Document Type: Article

References (66)

1. Arnold DL, Riess GT, Matthews PM, Francis GS, Collins DL, Wolfson C, Antel JP. Use of proton magnetic resonance spectroscopy for monitoring disease progression in multiple sclerosis. Ann Neurol 36: 76-82, 1994.
2. Attwell D, Laughlin SB. An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21: 1133-1145, 2001.
3. Baslow MH. A review of phylogenetic and metabolic relationships between the acylamino acids, N-acetyl-L-aspartic acid and N-acetyl-L-histidine, in the vertebrate nervous system. J Neurochem 68: 1335-1344, 1997.
4. Bass JL, Corwin M, Gozal D, Moore C, Nishida H, Parker S, Schonwald A, Wilker RE, Stehle S, Kinane TB. The effect of chronic or intermittent hypoxia on cognition in childhood: a review of the evidence. Pediatrics 114: 805-816, 2004.
5. Bates TE, Strangward M, Keelan J, Davey GP, Munro PM, Clark JB. Inhibition of N-acetylaspartate production: implications for 1H MRS studies in vivo. Neuroreport 7: 1397-1400, 1996.
6. Birken DL, Oldendorf WH. N-acetyl-L-aspartic acid: a literature review of a compound prominent in 1H-NMR spectroscopic studies of brain. Neurosci Biobehav Rev 13: 23-31, 1989.
7. Brooks KJ, Hargreaves I, Bhakoo K, Sellwood M, O'Brien F, Noone M, Sakata Y, Cady E, Wylezinska M, Thornton J, Ordidge R, Nguyen Q, Clemence M, Wyatt J, Bates TE. Delayed hypothermia prevents decreases in N-acetylaspartate and reduced glutathione in the cerebral cortex of the neonatal pig following transient hypoxia-ischaemia. Neurochem Res 27: 1599-1604, 2002.
8. Brulatout S, Meric P, Loubinoux I, Borredon J, Correze JL, Roucher P, Gillet B, Berenger G, Beloeil JC, Tiffon B, Mispelter J, Seylaz J. A one-dimensional (proton and phosphorus) and two-dimensional (proton) in vivo NMR spectroscopic study of reversible global cerebral ischemia. J Neurochem 66: 2491-2499, 1996.
9. Bunn HF, Poyton RO. Oxygen sensing and molecular adaptation to hypoxia. Physiol Rev 76: 839-885, 1996.
10. Cendes F, Andermann F, Dubeau F, Matthews PM, Arnold DL. Normalization of neuronal metabolic dysfunction after surgery for temporal lobe epilepsy. Evidence from proton MR spectroscopic imaging. Neurology 49: 1525-1533, 1997.
11. Cendes F, Caramanos Z, Andermann F, Dubeau F, Arnold DL. Proton magnetic resonance spectroscopic imaging and magnetic resonance imaging volumetry in the lateralization of temporal lobe epilepsy: a series of 100 patients. Ann Neurol 42: 737-746, 1997.
12. Chavez JC, Agani F, Pichiule P, LaManna JC. Expression of hypoxia-inducible factor-1alpha in the brain of rats during chronic hypoxia. J Appl Physiol 89: 1937-1942, 2000.
13. Chu WJ, Mason GF, Pan JW, Hetherington HP, Liu HG, San Pedro EC, Mountz JM. Regional cerebral blood flow and magnetic resonance spectroscopic imaging findings in diaschisis from stroke. Stroke 33: 1243-1248, 2002.
14. Cohen-Gadol AA, Pan JW, Kim JH, Spencer DD, Hetherington HH. Mesial temporal lobe epilepsy: a proton magnetic resonance spectroscopy study and a histopathological analysis. J Neurosurg 101: 613-620, 2004.
15. 1H magnetic resonance spectroscopy of chronic cerebral white matter lesions and normal appearing white matter in multiple sclerosis. J Neurol Neurosurg Psychiatry 63: 736-742, 1997.
16. De Stefano N, Matthews PM, Arnold DL. Reversible decreases in N-acetylaspartate after acute brain injury. Magn Reson Med 34: 721-727, 1995.
17. Dixon JC, Cady EB, Priest AN, Thornton JS, Peebles DM. Growth restriction and the cerebral metabolic response to acute hypoxia of chick embryos in-ovo: A proton magnetic resonance spectroscopy study. Brain Res Dev Brain Res 160: 203-210, 2005.
18. -dependent transporters in mouse CNS. J Appl Physiol 95: 292-299, 2003.
19. Dyugovskaya L, Lavie P, Lavie L. Increased adhesion molecules expression and production of reactive oxygen species in leukocytes of sleep apnea patients. Am J Respir Crit Care Med 165: 934-939, 2002.
20. Fan C, Iacobas DA, Zhou D, Chen Q, Lai JK, Gavrialov O, Haddad GG. Gene expression and phenotypic characterization of mouse heart after chronic constant or intermittent hypoxia. Physiol Genomics 22: 292-307, 2005.
21. Foster GE, McKenzie DC, Milsom WK, Sheel AW. Effects of two protocols of intermittent hypoxia on human ventilatory, cardiovascular and cerebral responses to hypoxia. J Physiol 567: 689-699, 2005.
22. Gibson GE, Pulsinelli W, Blass JP, Duffy TE. Brain dysfunction in mild to moderate hypoxia. Am J Med 70: 1247-1254, 1981.
23. Goldstein FB. The enzymatic synthesis of N-acetyl- L-aspartic acid by subcellular preparations of rat brain. J Biol Chem 244: 4257-4260, 1969.
24. Govindaraju V, Young K, Maudsley AA. Proton NMR chemical shifts and coupling constants for brain metabolites. NMR Biomed 13: 129-153, 2000.
25. Gozal D. Sleep-disordered breathing and school performance in children. Pediatrics 102: 616-620, 1998.
26. Gozal D, Daniel JM, Dohanich GP. Behavioral and anatomical correlates of chronic episodic hypoxia during sleep in the rat. J Neurosci 21: 2442-2450, 2001.
27. Gozal E, Row BW, Schurr A, Gozal D. Developmental differences in cortical and hippocampal vulnerability to intermittent hypoxia in the rat. Neurosci Lett 305: 197-201, 2001.
28. Gozal E, Sachleben LR Jr, Rane MJ, Vega C, Gozal D. Mild sustained and intermittent hypoxia induce apoptosis in PC-12 cells via different mechanisms. Am J Physiol Cell Physiol 288: C535-C542, 2005.
29. 2 deprivation in the central nervous system: on mechanisms of neuronal response, differential sensitivity and injury. Prog Neurobiol 40: 277-318, 1993.
30. Heales SJ, Davies SE, Bates TE, Clark JB. Depletion of brain glutathione is accompanied by impaired mitochondrial function and decreased N-acetyl aspartate concentration. Neurochem Res 20: 31-38, 1995.
31. Hetherington H, Kuzniecky R, Pan J, Mason G, Morawetz R, Harris C, Faught E, Vaughan T, Pohost G. Proton nuclear magnetic resonance spectroscopic imaging of human temporal lobe epilepsy at 4.1 T. Ann Neurol 38: 396-404, 1995.
32. 31P spectroscopic imaging of epilepsy: spectroscopic and histologic correlations. Epilepsia 45 Suppl 4: 17-23, 2004.
33. Hochachka PW, Buck LT, Doll CJ, Land SC. Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci USA 93: 9493-9498, 1996.
34. Hochachka PW, Clark CM, Monge C, Stanley C, Brown WD, Stone CK, Nickles RJ, Holden JE. Sherpa brain glucose metabolism and defense adaptations against chronic hypoxia. J Appl Physiol 81: 1355-1361, 1996.
35. 1H magnetic resonance spectroscopic imaging. Ann Neurol 40: 236-239, 1996.
36. Kamba M, Suto Y, Ohta Y, Inoue Y, Matsuda E. Cerebral metabolism in sleep apnea. Evaluation by magnetic resonance spectroscopy. Am J Respir Crit Care Med 156: 296-298, 1997.
37. Kanaan A, Farahani R, Douglas RM, Lamanna JC, Haddad GG. Effect of chronic continuous or intermittent hypoxia and reoxygenation on cerebral capillary density and myelination. Am J Physiol Regul Integr Comp Physiol 290: R1105-R1114, 2006.
38. Kantarci K, Jack CR Jr. Neuroimaging in Alzheimer disease: an evidence-based review. Neuroimaging Clin N Am 13: 197-209, 2003.
39. Kreisman NR, Soliman S, Gozal D. Regional differences in hypoxic depolarization and swelling in hippocampal slices. J Neurophysiol 83: 1031-1038, 2000.
40. Kuzniecky R, Hetherington H, Pan J, Hugg J, Palmer C, Gilliam F, Faught E, Morawetz R. Proton spectroscopic imaging at 4.1 tesla in patients with malformations of cortical development and epilepsy. Neurology 48: 1018-1024, 1997.
41. LaManna JC, Vendel LM, Farrell RM. Brain adaptation to chronic hypobaric hypoxia in rats. J Appl Physiol 72: 2238-2243, 1992.
42. Macey PM, Henderson LA, Macey KE, Alger JR, Frysinger RC, Woo MA, Harper RK, Yan-Go FL, Harper RM. Brain morphology associated with obstructive sleep apnea. Am J Respir Crit Care Med 166: 1382-1387, 2002.
43. Monge C, Leon-Velarde F. Physiological adaptation to high altitude: oxygen transport in mammals and birds. Physiol Rev 71: 1135-1172, 1991.
44. Morrell MJ, McRobbie DW, Quest RA, Cummin AR, Ghiassi R, Corfield DR. Changes in brain morphology associated with obstructive sleep apnea. Sleep Med 4: 451-454, 2003.
45. Nagata N, Saji M, Ito T, Ikeno S, Takahashi H, Terakawa N. Repetitive intermittent hypoxia-ischemia and brain damage in neonatal rats. Brain Dev 22: 315-320, 2000.
46. Neubauer JA. Invited review: Physiological and pathophysiological responses to intermittent hypoxia. J Appl Physiol 90: 1593-1599, 2001.
47. O'Reilly JP, Jiang C, Haddad GG. Major differences in response to graded hypoxia between hypoglossal and neocortical neurons. Brain Res 683: 179-186, 1995.
48. 1H spectroscopic imaging at 4.1 T. Magn Reson Med 36: 72-77, 1996.
49. Pan JW, Kim JH, Cohen-Gadol A, Pan C, Spencer DD, Hetherington HP. Regional energetic dysfunction in hippocampal epilepsy. Acta Neurol Scand 111: 218-224, 2005.
50. Pan JW, Krupp LB, Elkins LE, Coyle PK. Cognitive dysfunction lateralizes with NAA in multiple sclerosis. Appl Neuropsychol 8: 155-160, 2001.
51. Pan JW, Takahashi K. Interdependence of N-acetyl aspartate and high-energy phosphates in healthy human brain. Ann Neurol 57: 92-97, 2005.
52. Penrice J, Lorek A, Cady EB, Amess PN, Wylezinska M, Cooper CE, D'Souza P, Brown GC, Kirkbride V, Edwards AD, Wyatt JS, Reynolds EO. Proton magnetic resonance spectroscopy of the brain during acute hypoxia-ischemia and delayed cerebral energy failure in the newborn piglet. Pediatr Res 41: 795-802, 1997.
53. Prabhakar NR, Kline DD. Ventilatory changes during intermittent hypoxia: importance of pattern and duration. High Alt Med Biol 3: 195-204, 2002.
54. 1H-MRS and un-biased stereology: Can non-invasive measures of N-acetyl-asparate following global ischemia be used as a reliable measure of neuronal damage? Brain Res 892: 166-175, 2001.
55. Sastre-Garriga J, Ingle GT, Chard DT, Ramio-Torrenta L, McLean MA, Miller DH, Thompson AJ. Metabolite changes in normal-appearing gray and white matter are linked with disability in early primary progressive multiple sclerosis. Arch Neurol 62: 569-573, 2005.
56. Schulz R, Mahmoudi S, Hattar K, Sibelius U, Olschewski H, Mayer K, Seeger W, Grimminger F. Enhanced release of superoxide from polymorphonuclear neutrophils in obstructive sleep apnea. Impact of continuous positive airway pressure therapy. Am J Respir Crit Care Med 162: 566-570, 2000.
57. Serles W, Li LM, Antel SB, Cendes F, Gotman J, Olivier A, Andermann F, Dubeau F, Arnold DL. Time course of postoperative recovery of N-acetyl-aspartate in temporal lobe epilepsy. Epilepsia 42: 190-197, 2001.
58. Sica AL, Greenberg HE, Scharf SM, Ruggiero DA. Chronic-intermittent hypoxia induces immediate early gene expression in the midline thalamus and epithalamus. Brain Res 883: 224-228, 2000.
59. Signoretti S, Marmarou A, Tavazzi B, Lazzarino G, Beaumont A, Vagnozzi R. N-Acetylaspartate reduction as a measure of injury severity and mitochondrial dysfunction following diffuse traumatic brain injury. J Neurotrauma 18: 977-991, 2001.
60. Truckenmiller ME, Namboodiri MA, Brownstein MJ, Neale JH. N-acetylation of L-aspartate in the nervous system: differential distribution of a specific enzyme. J Neurochem 45: 1658-1662, 1985.
61. Tsai G, Coyle JT. N-acetylaspartate in neuropsychiatric disorders. Prog Neurobiol 46: 531-540, 1995.
62. Twieg DB, Meyerhoff DJ, Hubesch B, Roth K, Sappey-Marinier D, Boska MD, Gober JR, Schaefer S, Weiner MW. Phosphorus-31 magnetic resonance spectroscopy in humans by spectroscopic imaging: localized spectroscopy and metabolite imaging. Magn Reson Med 12: 291-305, 1989.
63. Urenjak J, Williams SR, Gadian DG, Noble M. Specific expression of N-acetylaspartate in neurons, oligodendrocyte-type-2 astrocyte progenitors, and immature oligodendrocytes in vitro. J Neurochem 59: 55-61, 1992.
64. Waldman AD, Rai GS. The relationship between cognitive impairment and in vivo metabolite ratios in patients with clinical Alzheimer's disease and vascular dementia: a proton magnetic resonance spectroscopy study. Neuroradiology 45: 507-512, 2003.
65. Wardlaw JM, Marshall I, Wild J, Dennis MS, Cannon J, Lewis SC. Studies of acute ischemic stroke with proton magnetic resonance spectroscopy: relation between time from onset, neurological deficit, metabolite abnormalities in the infarct, blood flow, and clinical outcome. Stroke 29: 1618-1624, 1998.
66. Young T, Peppard PE, Gottlieb DJ. Epidemiology of obstructive sleep apnea: a population health perspective. Am J Respir Crit Care Med 165: 1217-1239, 2002.