Nitric oxide synthase and NADPH-diaphorase after acute hypobaric hypoxia in the rat caudate putamen

Experimental Neurology

Volumn 186, Issue 1, 2004, Pages 33-45

  Encinas, Juan Manuel ^a   Fernández, Ana Patricia ^a   Salas, Eduardo ^a   Castro Blanco, Susana ^a   Muñoz, Priscila ^a   Rodrigo, José ^a   Serrano, Julia ^a  

^a CSIC   (Spain)

Author keywords

Endothelial and inducible nitric oxide synthase; High altitude; Neuronal; Striatum

Indexed keywords

3 NITROTYROSINE; CAUDATE PUTAMEN; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; UNCLASSIFIED DRUG;

ALTITUDE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL; CONTROLLED STUDY; ENDOTHELIUM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; EVALUATION; EXPOSURE; HYPOBARISM; HYPOXIA; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NITRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUTAMEN; RAT; SIMULATION; STAINING; STIMULATION; SYNTHESIS; TIME; WESTERN BLOTTING;

EID: 1242316348     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.expneurol.2003.09.024     Document Type: Article

References (62)

1. Adachi N., Lei B., Soutani M., Arai T. Different roles of neuronal and endothelial nitric oxide synthases on ischemic nitric oxide production in gerbil striatum. Neurosci. Lett. 288:2000;151-154.
2. Alonso D., Serrano J., Rodriguez I., Ruiz-Cabello J., Fernández A.P., Encinas J.M., Castro-Blanco S., Bentura M.L., Santacana M., Richart A., Fernandez-Vizarra P., Uttenthal L.O., Rodrigo J. Effects of oxygen and glucose deprivation on the expression and distribution of neuronal and inducible nitric oxide synthases and on protein nitration in rat cerebral cortex. J. Comp. Neurol. 443:2002;183-200.
3. Arregui A., Hollingsworth Z., Penney J.B., Young A.B. Autoradiographic evidence for increased dopamine uptake sites in striatum of hypoxic mice. Neurosci. Lett. 167:1994;195-197.
4. Bahrke M.S., Shukitt-Hale B. Effects of altitude on mood, behaviour and cognitive functioning. A review. Sports Med. 16:1993;97-125.
5. Berndt C., Henke W., Gross J. Hypoxia induces different responses of striatal high- and low-affinity dopamine uptake sites. Mol. Chem. Neuropathol. 18:1993;179-187.
6. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254.
7. Castro-Blanco S., Encinas J.M., Serrano J., Alonso D., Gómez M.B., Sánchez J., Rios-Tejada F., Fernández-Vizzara P., Fernández A.P., Martinez-Murillo R., Rodrigo J. Expression of the nitrergic system and protein nitration in adult rat brains submitted to hypobaric hypoxia. Nitric Oxide. 2003;. (in press).
8. Dawson V.L., Dawson T.M. Nitric oxide neurotoxicity. J. Chem. Neuroanat. 10:1996;179-190.
9. Dawson T.M., Bredt D.S., Fotuhi M., Hwang P.M., Snyder S.H. Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc. Natl. Acad. Sci. U. S. A. 88:1991;7797-7801.
10. Descarries L., Bosler O., Berthelet F., Des Rosiers M.H. Dopaminergic nerve endings visualized by high-resolution autoradiography in adult rat neostriatum. Nature. 284:1980;620-622.
11. Forman L.J., Liu P., Nagele R.G., Yin K., Wong P.Y. Augmentation of nitric oxide, superoxide, and peroxynitrite production during cerebral ischemia and reperfusion in the rat. Neurochem. Res. 23:1998;141-148.
12. Forstermann U., Schmidt H.W., Pollock J.S., Sheng H., Mitchell J.A., Warner T.D., Nakane M., Murad F. Isoforms of nitric oxide synthase. Characterization and purification from different cell types. Biochem. Pharmacol. 42:1991;1849-1857.
13. Fujiyama F., Masuko S. Association of dopaminergic terminals and neurons releasing nitric oxide in the rat striatum: an electron microscopic study using NADPH-diaphorase histochemistry and tyrosine hydroxylase immunohistochemistry. Brain Res. Bull. 40:1996;121-127.
14. Hamilton A.J., Trad L.A., Cymerman A. Alterations in human upper extremity motor function during acute exposure to simulated altitude. Aviat. Space Environ. Med. 62:1991;759-764.
15. Hatton W.J., von Bartheld C.S. Analysis of cell death in the trochlear nucleus of the chick embryo: calibration of the optical disector counting method reveals systematic bias. J. Comp. Neurol. 409:1999;169-186.
16. Holtz M.L., Craddock S.D., Pettigrew L.C. Rapid expression of neuronal and inducible nitric oxide synthases during post-ischemic reperfusion in rat brain. Brain Res. 898:2001;49-60.
17. Hope B.T., Michael G.J., Knigge K.M., Vincent S.R. Neuronal NADPH diaphorase is a nitric oxide synthase. Proc. Natl. Acad. Sci. U. S. A. 88:1991;2811-2814.
18. Iadecola C. Bright and dark sides of nitric oxide in ischemic brain injury. Trends Neurosci. 20:1997;132-139.
19. Ignarro L.J., Buga G.M., Wood K.S., Byrns R.E., Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. U. S. A. 84:1987;9265-9269.
20. Ischiropoulos H., al-Mehdi A.B. Peroxynitrite-mediated oxidative protein modifications. FEBS Lett. 364:1995;279-282.
21. Kader A., Frazzini V.I., Solomon R.A., Trifiletti R.R. Nitric oxide production during focal cerebral ischemia in rats. Stroke. 24:1993;1709-1716.
22. Kahn R.A., Weinberger J., Brannan T., Prikhojan A., Reich D.L. Nitric oxide modulates dopamine release during global temporary cerebral ischemia. Anesth. Analg. 80:1995;1116-1121.
23. Kelly P.A., Ritchie I.M., Arbuthnott G.W. Inhibition of neuronal nitric oxide synthase by 7-nitroindazole: effects upon local cerebral blood flow and glucose use in the rat. J. Cereb. Blood Flow Metab. 15:1995;766-773.
24. Kiss J.P., Vizi E.S. Nitric oxide: a novel link between synaptic and nonsynaptic transmission. Trends Neurosci. 24:2001;211-215.
25. Koppenol W.H., Moreno J.J., Pryor W.A., Ischiropoulos H., Beckman J.S. Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide. Chem. Res. Toxicol. 5:1992;834-842.
26. Lafuente J.V., Adan B., Cervos-Navarro J. Effects of chronic deep hypoxia on the expression of nitric oxide synthase in the rat brain. Acta Neurochir., Suppl. 76:2000;111-113.
27. Light K.E., Shetlar D., Strahlendorf J.C., Hughes M.J., Barnes C.D. Alterations in norepinephrine and dopamine content in selected brain areas of guinea pigs adapted to simulated high altitude. J. Neurochem. 36:1981;773-775.
28. Lonart G., Cassels K.L., Johnson K.M. Nitric oxide induces calcium-dependent [3H]dopamine release from striatal slices. Neurosci. Res. 35:1993;192-198.
29. Luo Y., Kaur C., Ling E.A. Hypobaric hypoxia induces fos and neuronal nitric oxide synthase expression in the paraventricular and supraoptic nucleus in rats. Neurosci. Lett. 296:2000;145-148.
30. Malinski T., Bailey F., Zhang Z.G., Chopp M. Nitric oxide measured by a porphyrinic microsensor in rat brain after transient middle cerebral artery occlusion. J. Cereb. Blood Flow Metab. 13:1993;355-358.
31. Malyshev I.Y., Zenina T.A., Golubeva L.Y., Saltykova V.A., Manukhina E.B., Mikoyan V.D., Kubrina L.N., Vanin A.F. NO-dependent mechanisms of adaptation to hypoxia. Nitric Oxide. 3:1999;105-113.
32. Marletta M.A., Yoon P.S., Iyengar R., Leaf C.D., Wishnok J.S. Macrophage oxidation of L-arginine to nitrite and nitrate: nitric oxide is an intermediate. Biochemistry. 27:1988;8706-8711.
33. Martínez-Murillo R., Semenenko F., Cuello A.C. The origin of tyrosine hydroxylase-immunoreactive fibers in the regions of the nucleus basalis magnocellularis of the rat. Brain Res. 451:1988;227-236.
34. Matsuoka Y., Kitamura Y., Tooyama I., Kimura H., Taniguchi T. In vivo hypoxia-induced neuronal damage with an enhancement of neuronal nitric oxide synthase immunoreactivity in hippocampus. Exp. Neurol. 146:1997;57-66.
35. Moncada S., Higgs E.A. Endogenous nitric oxide: physiology, pathology and clinical relevance. Eur. J. Clin. Invest. 21:1991;361-374.
36. Moro M.A., De Alba J., Leza J.C., Lorenzo P., Fernández A.P., Bentura M.L., Bosca L., Rodrigo J., Lizasoain I. Neuronal expression of inducible nitric oxide synthase after oxygen and glucose deprivation in rat forebrain slices. Eur. J. Neurosci. 10:1998;445-456.
37. Nakashima M.N., Yamashita K., Kataoka Y., Yamashita Y.S., Niwa M. Time course of nitric oxide synthase activity in neuronal, glial, and endothelial cells of rat striatum following focal cerebral ischemia. Cell. Mol. Neurobiol. 15:1995;341-349.
38. Palmer R.J., Ferrige A.G., Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 327:1987;524-526.
39. Prabhakar N.R., Pieramici S.F., Premkumar D.R., Kumar G.K., Kalaria R.N. Activation of nitric oxide synthase gene expression by hypoxia in central and peripheral neurons. Brain Res., Mol. Brain Res. 43:1996;341-346.
40. Prioux-Guyonneau M., Mocaer-Cretet E., Redjimi-Hafsi F., Jacquot C. Changes in brain 5-hydroxytryptamine metabolism induced by hypobaric hypoxia. Gen. Pharmacol. 13:1982;251-254.
41. Pryor W.A., Squadrito G.L. The chemistry of peroxynitrite: a product from the reaction of nitric oxide with superoxide. Am. J. Physiol. 268:1995;699-722.
42. Radomski M.W., Vallance P.J., Whitely G., Foxwell N., Moncada S. Modulation of platelet adhesion to human vascular endothelium by the constitutive and cytokine-inducible nitric oxide synthases. Cardiovasc. Res. 27:1993;1380-1382.
43. Robertson S.C., Loftus C.M. Effect of N-methyl-D-aspartate and inhibition of neuronal nitric oxide on collateral cerebral blood flow after middle cerebral artery occlusion. Neurosurgery. 42:1998;117-124.
44. Rodrigo J., Springall D.R., Uttenthal O., Bentura M.L., Abadia-Molina F., Riveros-Moreno V., Martinez-Murillo R., Polak J.M., Moncada S. Localization of nitric oxide synthase in the adult rat brain. Philos. Trans. R. Soc. Lond., B Biol. Sci. 345:1994;175-221.
45. Rodrigo J., Fernández A.P., Bentura M.L., Martínez de Velasco J., Serrano J., Uttenthal L.O., Martínez-Murillo R. Distribution of catecholaminergic afferent fibres in the rat globus pallidus and their relations with cholinergic neurons. J. Chem. Neuroanat. 15:1998;1-20.
46. Rodrigo J., Alonso A., Fernández A.P., Serrano J., Richart A., López J.C., Santacana M., Martínez-Murillo R., Ventura M.L., Ghiglione M., Uttenthal L.O. Neuronal and inducible nitric oxide synthase expression and protein nitration in rat cerebellum after oxygen and glucose deprivation. Brain Res. 909:2001;20-45.
47. Rushlow W., Flumerfelt B.A., Naus C.C. Colocalization of somatostatin, neuropeptide Y, and NADPH-diaphorase in the caudate-putamen of the rat. J. Comp. Neurol. 351:1995;499-508.
48. Sandor N.T., Brassai A., Puskas A., Lendvai B. Role of nitric oxide in modulating neurotransmitter release from rat striatum. Brain Res. Bull. 36:1995;436-483.
49. Serrano J., Encinas J.M., Salas E., Fernández A.P., Castro-Blanco S., Fernández-Vizarra P., Bentura M.L., Rodrigo J. Hypobaric hypoxia modifies constitutive nitric oxide synthase activity and protein nitration in the rat cerebellum. Brain Res. 2003;. (in press).
50. Shu S., Ju G., Fan L. The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. Neurosci. Lett. 85:1988;169-171.
51. Shukitt-Hale B., Stillman M.J., Levy A., Devine J.A., Lieberman H.R. Nimodipine prevents the in vivo decrease in hippocampal extracellular acetylcholine produced by hypobaric hypoxia. Brain Res. 621:1993;291-295.
52. Spatz M., Yasuma Y., Strasser A., Kawai N., Stanimirovic D., McCarron R. Modulation of striatal dopamine release in cerebral ischemia by L-arginine. Neurochem. Res. 20:1995;491-496.
53. Thomas E., Pearse A.G. The fine localization of dehydrogenases in the nervous system. Z. Zellforch. Microsk. Anat. Histochem. 2:1961;266-282.
54. Trabace L., Kendrick K.M. Nitric oxide can differentially modulate striatal neurotransmitter concentrations via soluble guanylate cyclase and peroxynitrite formation. J. Neurochem. 75:2000;1664-1674.
55. Uttenthal L.O., Alonso D., Fernández A.P., Campbell R.O., Moro M.A., Leza J.C., Lizasoain I., Esteban F.J., Barroso J.B., Valderrama R., Pedrosa J.A., Peinado M.A., Serrano J., Richart A., Ventura M.L., Santacana M., Martinez-Murillo R., Rodrigo J. Neuronal and inducible nitric oxide synthase and nitrotyrosine immunoreactivities in the cerebral cortex of the aging rat. Microsc. Res. Tech. 43:1998;75-88.
56. Veltkamp R., Rajapakse N., Robins G., Puskar M., Shimizu K., Busija D. Transient focal ischemia increases endothelial nitric oxide synthase in cerebral blood vessels. Stroke. 33:2002;2704-2710.
57. Vincent S.R., Johansson O., Hokfelt T., Skirboll L., Elde R.P., Terenius L., Kimmel J., Goldstein M. NADPH-diaphorase: a selective histochemical marker for striatal neurons containing both somatostatin- and avian pancreatic polypeptide (APP)-like immunoreactivities. Comp. Neurol. 217:1983;252-263.
58. Wei G., Dawson V.L., Zweier J.L. Role of neuronal and endothelial nitric oxide synthase in nitric oxide generation in the brain following cerebral ischemia. Biochim. Biophys. Acta. 20(1455):1999;23-34.
59. West A.R., Galloway M.P. Endogenous nitric oxide facilitates striatal dopamine and glutamate efflux in vivo: role of ionotropic glutamate receptor-dependent mechanisms. Neuropharmacology. 36:1997;1571-1581.
60. Wustmann C., Fischer H.D., Schmidt J. Inhibitory effects of hypoxia on dopamine release. Acta Biol. Med. Ger. 41:1982;571-574.
61. Yan X.X., Garey L.J. Morphological diversity of nitric oxide synthesising neurons in mammalian cerebral cortex. J. Hirnforsch. 38:1997;165-172.
62. Zhang F., Iadecola C. Nitroprusside improves blood flow and reduces brain damage after focal ischemia. NeuroReport. 4:1993;559-562.