Neuronal nitric oxide synthase expression is induced in neocortical astrocytes after spreading depression

Journal of Cerebral Blood Flow and Metabolism

Volumn 18, Issue 1, 1998, Pages 75-87

  Caggiano, Anthony O ^a   Kraig, Richard P ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Astrogliosis; Ischemia; Nitric oxide synthase; Spreading depression; Superoxide dismutase

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN ISCHEMIA; CELL SPECIFICITY; COMPUTER ANALYSIS; CONTROLLED STUDY; ENZYME ASSAY; ENZYME INDUCTION; IMAGE ANALYSIS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPREADING CORTICAL DEPRESSION;

EID: 0031985062     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1097/00004647-199801000-00008     Document Type: Article

References (79)

1. Bailey MS, Shipley MT (1993) Astrocyte subtypes in the rat olfactory bulb: morphological heterogeneity and differential laminar distribution. J Comp Neurol 328:501-526
2. Black JA, Friedman B, Waxman SG, Elmer LW, Angelides KL (1989) Immunoultrastructural localization of sodium channels at nodes of Ranvier and perinodal astrocytes in rat optic nerve. Proc R Soc London B Biol Sci 238:39-51
3. Beckman JS, Chen J, Crow JP, Ye YZ (1994) Reactions of nitric oxide, superoxide and peroxynitrite with superoxide dismutase in neurodegeneration. Prog Brian Res 103:366-380
4. Biber K, Walden J, Gebicke-Harter P, Berger M, van Calker D (1996) Carbamazepine inhibits the potentiation by adenosine analogues of agonist induced inoitolphosphate formation in hippocampal astrocyte cultures. Biol Phychiatry 40:563-7
5. Bo L, Dawson TM, Wesselingh S, Mork S, Choi S, King PA, Hanley D, Trapp BD (1994) Induction of nitric oxide synthase in demyelinating regions of multiple sclerosis brains. Ann Neurol 36:778-786
6. Boje KM, Arora PK (1992) Microglial-produced nitric oxide and reactive oxides mediate neuronal cell death. Brain Res 587:250-256
7. Breder CD, Dewitt D, Kraig RP (1995) Characterization of inducible cyclooxygenase in rat brain. J Comp Neurol 322:296-315
8. Breder CD, Smith WL, Raz A, Masferer JL, Seibert K, Needleman P, Saper CB (1992) The distribution and characterization of cyclooxygenase-like immunoreactivity in ovine brain. J Comp Neurol 322:409-438
9. Bredt DS, Glatt CE, Hwang PM, Fotuhi M, Dawson TM, Snyder SH (1991) Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron 7:615-624
10. Bredt DS, Snyder SH (1989) Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc Natl Acad Sci USA 86:9030-9033
11. Bredt DS, Snyder SH (1990) Isolation of nitric oxide synthetase, a calmoudulin-requiring enzyme. Proc Natl Acad Sci USA 87:682-685
12. Bretag AH (1969) Synthetic interstitial fluids for isolated mammalian tissue. Life Sci 8:319-329
13. Busch E, Gyngell ML, Eis M, Hoehn-Berlage M, Hossmann KA (1996) Potassium-induced cortical spreading depression during focal cerebral ischemia in rats: contribution to lesion growth assessed by diffusion-weighted NMR and biochemical imaging. J Cereb Blood Flow Metab 16:1090-1099
14. Caggiano AO, Breder CD, Kraig RP (1996) Long-term elevation of cyclooxygenase-2 by not lipoxygenase, in regions synaptically distant from spreading depression. J Comp Neurol 376:447-462
15. Caggiano AO, Kraig RP (1996) Eicosanoids and nitric oxide influence induction of reactive gliosis from spreading depression in microglia but not astrocytes. J Comp Neurol 369:93-108
16. Caggiano AO, Kraig RP (1997) Expression pattern of superoxide dismutase following neocortical spreading depression [Abstr]. J Cereb Blood Flow Metab 17:S553
17. Chao CC, Hu S, Molitor TW, Shaskan EG, Peterson PK (1992) Activated microglia mediate neuronal injury via a nitric oxide mechanism. J Immunol 149:2736-2741
18. Chesler M, Kraig RP (1989) Intracellular pH transients of mammalian astrocytes. J Neurosci 9:2011-2019
19. Dani JW, Chernjavsky A, Smith SJ (1992) Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron 8:429-440
20. Dawson TM, Snyder SH (1994) Gases as biological messengers: nitric oxide and carbon monoxide in the brain. J Neurosci 14:5147-5159
21. Dawson TM, Zhang J, Dawson VL, Snyder SH (1994) Nitric oxide: cellular regulation and neuronal injury. Prog Brain Res 103:365-369
22. Dawson VL, Dawson TM, London ED, Bredt DS, Snyder SH (1991) Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc Natl Acad Sci USA 88:6368-6371
23. Dawson VL, Kizushi VM, Huang PL, Snyder SH, Dawson TM (1996) Resistance to neurotoxicity in cortical cultures from neuronal nitric oxide synthase-deficient mice. J Neurosci 16:2479-2487
24. Endoh M, Maiese K, Wagner J (1994) Expression of the inducible form of nitric oxide synthase by reactive astrocytes after transient global ischemia. Brain Res 651:92-100
25. 2+ in primary rat astrocytes. Glia 2:397-402
26. 2+ and fura-2. Brain Res 500:46-54
27. Feinstein DL, Galea E, Reis DJ (1993) Norepinephrine suppresses inducible nitric oxide synthase activity in rat astroglial cultures. J Neurochem 60:1945-1948
28. Fiallos-Estrada CE, Kummer W, Mayer B, Bravo R, Zimmermann M, Herdegen T (1993) Long-lasting increase of nitric oxide synthase immunoreactivity, NADPH-diaphorase reaction and c-jun co-expression in rat dorsal root ganglion neurons following sciatic nerve transection. Neurosci Lett 150:169-173
29. Garthwaite J, Charles SL, Chess-Williams R (1988) Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 336: 385-388
30. Garthwaite J, Garthwaite G, Palmer RMJ, Moncada S (1989) NMDA receptor mediated activation induces nitric oxide synthesis from arginine in rat brain slices. Eur J Pharmacol 172:413-416
31. Geller DA, Nussler AK, Di Silvio M, Lowenstein CJ, Shapiro RA, Wang SC, Simmons RL, Billiar TR (1993) Cytokines, endotoxin, and glucocorticoids regulate expression of inducible nitric oxide synthase in hepatocytes. Proc Natl Acad Sci USA 90:522-526
32. Gehrmann J, Miles G, Bonnekoh P, Banati R, Iijima T, Kreutzberg GW, Hossmann KA (1993) Microglial reaction in the rat cerebral cortex induced by cortical spreading depression. Brain Pathol 3: 11-17
33. 2+ influx into astrocytes. Proc Natl Acad Sci USA 87:3454-3458
34. Griffith R, Sutin J (1996) Reactive astrocyte formation in vivo is regulated by noradrenergic axons. J Comp Neurol 371:362-75
35. Guo FH, DeRaeve HR, Rice TW, Stuehr DJ, Thunnissen FBJM, Erzurum SC (1995) Continuous nitric oxide synthesis by inducible nitric oxide synthase in normal human airway epithelium in vivo. Proc Natl Acad Sci USA 92:7809-7813
36. Hara H, Huang PL, Panahian N, Fishman MC, Moskowitz MA (1996) Reduced brain edema and infarction volume in mice lacking the neuronal isoform of nitric oxide synthase after transient MCA occlusion. J Cereb Blood Flow Metab 16:605-611
37. Hewett SJ, Csemansky CA, Choi DW (1994) Selective potentiation of NMDA-induced neuronal injury following induction of astrocytic iNOS. Neuron 13:487-494
38. Hodges-Savola C, Rogers SD, Ghilardi JR, Timm DR, Mantyh PW (1996) Beta-adrenergic receptors regulate astrogliosis and cell proliferation in the central nervous system in vivo. Glia 17:52-62
39. Huang R, Hertz L (1995) Noradrenaline-induced stimulation of glutamine metabolism in primary cultures of astrocytes. J Neurosci Res 41:677-683
40. Huang Z, Huang PL, Panahian N, Dalkara T, Fishman MC, Moskowitz MA (1994) Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 265:1883-1885
41. Huie RE, Padmaja S (1993) The reaction rate of nitric oxide with superoxide. Free Radical Res Commun 18:195-199
42. Iadecola C (1997) Bright and dark sides of nitric oxide in ischemic brain injury. TINS 20:132-139
43. Iadecola C, Zhang F, Sherry X, Casey R, Ross ME (1995) Inducible nitric oxide synthase gene expression in brain following cerebral ischemia. J Cereb Blood Flow Metab 15:378-384
44. Jensen AM, Chiu SY (1991) Differential intracellular calcium responses to glutamate in type 1 and type 2 cultured brain astrocytes. J Neurosci 11:1674-1684
45. Jensen AM, Chiu SY (1990) Fluorescence measurement of changes in intracellular calcium induced by excitatory amino acids in cultured cortical astrocytes. J Neurosci 10:1165-1175
46. Kawahara N, Ruetzler CA, Klatzo I (1995) Protective effect of spreading depression against neuronal damage following cardiac arrest cerebral ischaemia. Neurol Res 17:9-16
47. Kobayashi S, Harris VA, Welsh FA (1995) Spreading depression induces tolerance of cortical neurons to ischemia in rat brain. J Cereb Blood Flow Metab 15:721-727
48. Kraig RP, Chester M (1988) Dynamics of volatile buffers in brain cells during spreading depression. In: Mechanisms of Cerebral Hypoxia and Stroke (Somjen G, ed), New York, Plenum Press, pp 279-289
49. Kraig RP, Dong L, Thisted R, Jaeger CB (1991) Spreading depression increases immunohistochemical staining of glial fibrillary acidic protein. J Neurosci 11:2187-2198
50. 2+ changes: implication for ischemic brain injury. In: Cerebral Ischemia and Basic Mechanisms (Hartmann A, Yatsu F, Kuschinsky W, eds), Heidelberg, Berlin, Springer-Verlag, pp 64-76
51. Kraig RP, Lascola CD, Caggiano, AO (1995) Glial response to brain ischemia. In: Neuroglia (Kettenmann H, Ransom BR, eds), New York, Oxford Press, pp 964-976
52. Kraig RP, Pulsinelli WA, Plum F (1986) Carbonic acid buffer changes during complete brain ischemia. Am J Physiol 250:R348-R357
53. Kugler P, Drenckhahn D.(1996) Astrocytes and bergmann glia as an important site of nitric oxide synthase I. Glia 16:165-173
54. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
55. Leao AAP (1944) Spreading depression of activity in the cerebral cortex. J Neurophysiol 7:359-390
56. Lipton SA, Choi Y, Pan Z, Lei SZ, Chen HV, Sucher NJ, Loscalzo J, Singel DJ, Stamler JS (1993) A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364:626-632
57. Lipton SA, Singel DJ, Stamler JS (1994) Nitric oxide in the central nervous system. Prog Brain Res 103:359-364
58. Liu S, Adcock IM, Old RW, Barnes PJ, Evans TW (1993) Lipopolysaccharide treatment in vivo induces widespread tissue expression of inducible nitric oxide synthase mRNA. Biochem Biophys Res Comm 196:1208-1213
59. Matsushima K, Hogan MJ, Hakim AM (1996) Cortical spreading depression protects against subsequent focal cerebral ischemia in rats. J Cereb Blood Flow Metab 16:221-226
60. Mies G, Iijima T, Hossmann KA (1993) Correlation between periinfarct DC shifts and ischaemic neuronal damage in rat. Neuroreport 4:709-711
61. Minc-Golomb D, Schwartz JP (1992) Transcription of the brain nitric oxide synthase gene in neural cell cultures [Abstr] Soc Neurosci Abstr 18:1004
62. Moskowitz MA, Nozaki K, Kraig RP (1993) Neocortical spreading depression provokes the expression of c-fos protein-like immunoreactivity within trigeminal nucleus caudalis via trigeminovascular mechanisms. J Neurosci 13:1167-1177.
63. Murphy S, Simmons ML, Agullo L, Garcia A, Feinstein DL, Galea E, Reis DJ, Minc-Golomb D, Schwartz JP (1993) Synthesis of nitric oxide in CNS glial cells. Trends Neurosci 16:323-328
64. Nakashima MN, Yamashita K, Kataoka Y, Yamashita YS, Niwa M (1995) Time course of nitric oxide synthase activity in neuronal, glial, and endothelial cells of rat striatum following focal cerebral ischemia. Cell Mol Neurobiol 15:341-349
65. Nedergaard M, Hansen AJ (1988) Spreading depression is not associated with neuronal injury in rat brain. Brain Res 449:395-398
66. Panahian N, Yoshida T, Huang PL, Hedley-Whyte ET, Dalkara T, Fishman MC, Moskowitz MA (1996) Attenuated hippocampal damage after global cerebral ischemia in mice mutant in neuronal nitric oxide synthase. Neuroscience 72:343-354
67. Rogers NE, Ignarro LJ (1993) Constitutive nitric oxide synthase from cerebellum is reversibly inhibited by nitric oxide formed from 1-arginine. Biochem Biophys Res Commun 189:242-249
68. Sambrook J (1989) Molecular Cloning: A Laboratory Manual (Fritsch EF, Maniatis T, eds), Plainview, NY, Cold Spring Harbor Laboratory Press, pp 18.47-18.75
69. Schmidt HHW, Gagne GD, Nakane M, Pollock JS, Miller MF, Murad F (1992) Mapping of neuronal nitric oxide synthase in the rat suggest frequent co-localization with NADPH diaphorase but not with soluble guanylyl cyclase, and novel paraneural functions for nitrinergic signal transduction. J Histochem Cytochem 40:1439-1456
70. Simmons ML, Murphy S (1992) Induction of nitric oxide synthase in glial cells. J Neurochem 59:897-905
71. Takano K, Latour LL, Formato JE, Carano RA, Helmer KG, Hasegawa Y, Sotak CH, Fisher M (1996) The role of spreading depression in focal ischemia evaluated by diffusion mapping. Ann Neurol 39: 308-318
72. van den Pol AN, Finkbeiner SM, Cornell-Bell AH (1992) Calcium excitability and oscillations in suprachiasmatic nucleus neurons and glia in vitro. J Neurosci 12:2648-2664
73. Van der Zee EA, de Jong GI, Strosberg AD, Luiten PG (1993) Muscarinic acetylcholine receptor-expression in astrocytes in the cortex of young and aged rats. Glia 8:42-50
74. Verge VMK, Xu Z, Xu X, Wiesenfeld-Hallin Z (1992) Marked increase in nitric oxide synthase mRNA in rat dorsal root ganglia after peripheral axotomy: in situ hybridization and functional studies. Proc Natl Acad Sci USA 89:11617-11621
75. Wu W, Liuzzi FJ, Schico FP, Depto AS, Li Y, Mong JA, Dawson TM, Snyder SH (1994) Neuronal nitric oxide synthase is induced in spinal neurons by traumatic injury. Neuroscience 61:719-726
76. Zhang ZG, Chopp M, Gautam S, Zaloga C, Zhang RL, Schmidt HHHW, Pollock JS, Förstermann U (1994a) Upregulation of neuronal nitric oxide synthase and mRNA, and selective sparing of nitric oxide synthase-containing neurons after focal cerebral ischemia in rat. Brain Res 654:85-95
77. Zhang ZG, Reif D, Macdonald J, Tang WX, Kamp DK, Gentile RJ, Shakespeare WC, Murray RJ, Chopp M (1996) ARL 17477, a potent and selective neuronal NOS inhibitor decreases infarct volume after transient middle cerebral artery occlusion in rats. J Cereb Blood Flow Metab 16:599-604
78. Zhang J, Snyder SH (1995) Nitric oxide in the nervous system. Annu Rev Pharmacol Toxicol 35:213-233
79. Zhang F, White JG, Iadecola C (1994b) Nitric oxide donors increase blood flow and reduce brain damage in focal ischemia: evidence that nitric oxide is beneficial in the early stages of cerebral ischemia. J Cereb Blood Flow Metab 14:217-226