In vitro and in vivo induction of heme oxygenase-1 in rat glial cells: Possible involvement of nitric oxide production from inducible nitric oxide synthase

GLIA

Volumn 22, Issue 2, 1998, Pages 138-148

  Kitamura, Yoshihisa ^a   Furukawa, Muneki ^a   Matsuoka, Yasuji ^a   Tooyama, Ikuo ^b   Kimura, Hiroshi ^b   Nomura, Yasuyuki ^c   Taniguchi, Takashi ^a  

^a KYOTO PHARMACEUTICAL UNIVERSITY   (Japan)

^b SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Astrocyte; Interferon ; Lipopolysaccharide; Microglia

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); DRUG DERIVATIVE; ENDOTOXIN; ENDOTOXIN, ESCHERICHIA COLI; ENZYME INHIBITOR; HEME OXYGENASE; HEME OXYGENASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPOLYSACCHARIDE; N ACETYL S NITROSOPENICILLAMINE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NOS2 PROTEIN, RAT; PENICILLAMINE; RECOMBINANT GAMMA INTERFERON;

ANIMAL; ARTICLE; BIOSYNTHESIS; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GLIA; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MICROINJECTION; PHYSIOLOGY; RAT; WESTERN BLOTTING; WISTAR RAT;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; ENDOTOXINS; ENZYME INHIBITORS; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTERFERON-GAMMA, RECOMBINANT; LIPOPOLYSACCHARIDES; MICROINJECTIONS; NA(+)-K(+)-EXCHANGING ATPASE; NEUROGLIA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; PENICILLAMINE; RATS; RATS, WISTAR; S-NITROSO-N-ACETYLPENICILLAMINE;

EID: 0032005858     PISSN: 08941491     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-1136(199802)22:2<138::AID-GLIA5>3.0.CO;2-3     Document Type: Article

References (52)

1. Boje, K.M. and Arora, P.K. (1992) Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death. Brain Res., 587:250-256.
2. Bredt, D.S., Glatt, C.E., Hwang, P.M., Fotuhi, M., Dawson, T.M., and Snyder, S.H. (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.
3. Brüne, B., Dimmeler, S., Molinay, L., Vedia, L.M., and Lapetina, E.G. (1993) Nitric oxide: A signal for ADP-ribosylation of proteins. Life Sci., 54:61-70.
4. Dalton, T.P., Li, Q., Bittel, D., Liang, L., and Andrews, G.K. (1996) Oxidative stress activates metal-responsive transcription factor-1: Occupancy in vivo of metal response elements in the metallothionein-I gene promoter. J. Biol. Chem., 271:26233-26241.
5. Dawson, T.M. and Snyder, S.H. (1994) Gases as biological messengers: Nitric oxide and carbon monoxide in the brain. J. Neurosci., 14:5147-5159.
6. Dwyer, B.E., Nishimura, R.N., and Lu, S.-Y. (1995) Differential expression of heme oxygenase-1 in cultured cortical neurons and astrocytes determined by the aid of new heme oxygenase antibody: Response to oxidative stress. Mol. Brain Res., 30:37-47.
7. Endoh, M., Maiese, K., and Wagner, J. (1994) Expression of the inducible form of nitric oxide synthase by reactive astrocytes after transient global ischemia. Brain Res., 651:92-100.
8. Ewing, J.F., Harber, S.N., and Maines, M.D. (1992) Normal and heat-induced patterns of expression of heme oxygenase-1 (HSP32) in rat brain: Hyperthermia causes rapid induction of mRNA and protein. J. Neurochem., 58:1140-1149.
9. Ewing, J.F., Weber, C.M., and Maines, M.D. (1993) Biliverdin reductase is heat resistant and expressed with constitutive and heat shock form of heme oxygenase. J. Neurochem., 61:1015-1023.
10. Feinstein, D.L., Galea, E., Roberts, S., Berquist, H., Wang, H., and Reis, D.J. (1994) Induction of nitric oxide synthase in rat C6 glioma cells. J. Neurochem., 62:315-321.
11. Fujisawa, H., Ogura, T., Hokari, A., Weisz, A., Yamashita, J., and Esumi, H. (1995) Inducible nitric oxide synthase in a human glioblastoma cell line. J. Neurochem., 64:85-91.
12. Fukuda, K., Richmon, J.D., Sato, M., Sharp, F.R., Panter, S.S., and Noble, L.J. (1996) Induction of heme oxygenase-1 (HO-1) in glia after traumatic brain injury. Brain Res., 736:68-75.
13. Galea, E., Feinstein, D.L., and Reis, D.J. (1992) Induction of calcium-independent nitric oxide synthase activity in primary rat glial cells. Proc. Natl. Acad. Sci. USA, 89:10945-10949.
14. Galea, E., Feinstein, D.L., and Reis, D.J. (1994) Cloning and expression of inducible nitric oxide synthase from rat astrocytes. J. Neurosci. Res., 37:406-414.
15. Geddes, J.W., Pettigrew, L.C., Holtz, M.L., Craddock, S.D., and Maines, M.D. (1996) Permanent focal transient global cerebral ischemia increase glial and neuronal expression of heme oxygenase-1, but not heme oxygenase-2, protein in rat brain. Neurosci. Lett., 210:205-208.
16. Giulian, D. and Baker, T.J. (1986) Characterization of ameboid microglia isolated from developing mammalian brain. J. Neurosci., 6:2163-2178.
17. 15N]nitrate in biological fluids. Anal. Biochem., 126:131-138.
18. Kim, Y-M., Bergonia, H.A., Müller, C., Pitt, B.R., Watkins, W.D. and Lancaster, J.R. Jr. (1995a) Loss and degradation of enzyme-bound heme induced by cellular nitric oxide synthesis. J. Biol. Chem., 270:5710-5713.
19. Kim, Y.-M., Bergonia, H., and Lancaster, J.R. Jr. (1995b) Nitrogen oxide-induced autoprotection in isolated rat hepatocytes. FEBS Lett., 374:228-232.
20. 2+-insensitive but calmodulin-coupling nitric oxide synthase in rat glial cells. J. Neurosci. Res., 43:235-245.
21. Kitamura, Y., Takahashi, H., Nomura, Y., and Taniguchi, T. (1996b) Possible involvement of Janus kinase Jak2 in interferon-γ induction of nitric oxide synthase in rat glial cells. Eur. J. Pharmacol., 18:233-243.
22. Kitamura, Y., Takahashi, H., Matsuoka, Y., Tooyama, I., Kimura, H., Nomura, Y., and Taniguchi, T. (1996c) In vivo induction of inducible nitric oxide synthase by microinjection with interferon-γ and lipopolysaccharide in rat hippocampus. Glia, 18:233-243.
23. Koprowski, H., Zheng, Y.M., Heber-Katz, E., Fraser, N., Rorke, L., Fu, Z.F., Hanlon, C., and Dietzshold, B. (1993) In vivo expression of inducible nitric oxide synthase in experimentally induced neurologic diseases. Proc. Natl. Acad. Sci. USA, 90:3024-3027.
24. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227:680-685.
25. Lee, P.J., Alam, J., Wiegand, G.W., and Choi, M.K. (1996) Overexpression of heme oxygenase-1 in human pulmonary epithelial cells results in cell growth arrest and increased resistance to hyperoxia. Proc. Natl. Acad. Sci. USA, 93:10393-10398.
26. Llesuy, S.F. and Tomaro, M.L. (1994) Heme oxygenase and oxidative stress: Evidence of involvement of bilirubin as physiological protector against oxidative damage. Biochim. Biophys. Acta, 1223:9-14.
27. Maeshima, H., Sato, M., Ishikawa, K., Katagata, Y., and Yoshida, T. (1996) Participation of altered upstream stimulatory factor in the induction of rat heme oxygenase-1 by cadmium. Nucleic Acids Res., 24:2959-2965.
28. Maines, M.D. (1988) Heme oxygenase: Function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J., 2:2557-2568.
29. Maines, M.D. (1993) Carbon monoxide: An emerging regulator of cGMP in the brain. Mol. Cell. Neurosci., 4:389-397.
30. Matz, P., Turner, C., Weinstein, P.R., Massa, S.M., Panter, S.S., and Sharp, F.R. (1996) Heme-oxygenase-1 induction in glia throughout rat brain following experimental subarachnoid hemorrhage. Brain Res., 713:211-222.
31. McCoubrey, W.K. Jr., Ewing, J.F., and Maines, M.D. (1992) Human heme oxygenase-2: Characterization and expression of a full-length cDNA and evidence suggesting that the two HO-2 transcripts may differ by choice of polyadenylation signal. Arch. Biochem. Biophys., 295:13-20.
32. Monta, T., Perrella, M.A., Lee, M.-E., and Kourembanas, S. (1995) Smooth muscle cell-derived carbon monoxide is a regulator of vascular cGMP. Proc Natl. Acad. Sci. USA, 92:1475-1479.
33. Motterlini, R, Foresti, R., Intaglietta, M., and Winslow, R.M. (1996) NO-mediated activation of heme oxygenase: Endogenous cytoprotection against oxidative stress to endothelium. Am. J. Physiol., 270:H107-H114.
34. Müller, R., Taguchi, H., and Shibahara, S. (1987) Nucleotide sequence and organization of rat heme oxygenase gene. J. Biol. Chem., 262:6795-6802.
35. Murphy, S., Simons, M.L., Agullo, L., Garcia, A., Feinstein, D.L., Galea, E., Reis, D.J., Minc-Golomb, D., and Schwartz, J.P. (1993) Synthesis of nitric oxide in CNS glial cells. Trends Neurosci., 16:323-328.
36. Nathan, C. (1992) Nitric oxide as a secretory product of mammalian cells. FASEB J., 6:3051-3064.
37. Nimura, T., Weinstein, P.R., Massa, S.M., Panter, S., and Sharp, F.R. (1996) Heme oxygenase-1 (HO-1) protein induction in rat brain following focal ischemia. Mol. Brain Res., 37:201-208.
38. Ohshima, H., Brouet, I.M., Bandaletova, T., Adachi, H., Oguchi, S., Iida, S., Kurashima, Y., Morishita, Y., Sugimura, T., and Esumi, H. (1992) Polyclonal antibody against an inducible form of nitric oxide synthase purified from the liver of rats treated with Propionibacterium acnes and lipopolysaccharide. Biochem. Biophys. Res. Commun., 187:1291-1297.
39. O'Neill, L.A.J. and Kaltschmidt, C. (1997) NF-κB: A crucial transcription factor for glial and neuronal cell function. Trends Ncurosci., 20:252-258.
40. Paxinos, G. and Watson, C. (eds.) (1986) The Rat Brain in Stereotaxic Coordinates. 2nd ed. Academic Press, New York.
41. Peunova, N. and Enikolopov. G. (1993) Amplification of calcium-induced gene transcription by nitric oxide in neuronal cells. Nature, 364:450-453.
42. Rotenberg, M.O. and Maines, M.D. (1990) Isolation, characterization, and expression in Escherichia coli of a cDNA encoding rat heme oxygenase-2. J. Biol. Chem., 265:7501-7506.
43. Shibahara, S. (1988) Regulation of heme oxygenase gene expression. Semin. Hematol., 25:370-376.
44. Stocker, R., Yamamoto, Y., McDonagh, A.F., Glazer, A.N., and Ames, B.N. (1987) Bilirubin is an antioxidant of possible physiological importance. Science, 235:1043-1046.
45. Stone, J.R. and Marietta, M.A. (1994) Soluble guanylate cyclase from bovine lung: Activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states. Biochemistry, 33:5636-5640.
46. Takahashi, K., Hara, E., Suzuki, H., Sasano, H., and Shibahara, S. (1996) Expression of heme oxygenase isozyme mRNAs in the human brain and induction of heme oxygenase-1 by nitric oxide donors. J. Neurochem., 67:482-489.
47. Takeda, A., Onodera, H., Sugimoto, A., Itoyama, Y., Kogure, K., and Shibahara, S. (1994) Increased expression of heme oxygenase mRNA in rat brain following transient forebrain ischemia. Brain Res., 666:120-124.
48. Tyrrell, R.M. and Basu-Modak, S. (1994) Transient enhancement of heme oxygenase-1 mRNA accumulation: A marker of oxidative stress to eukaryotic cells. Methods Enzymol., 234:224-235.
49. Van Dam, A.-M., Bauer, J., Man-A-Hing, W.K.H., Marquette, C., Tilders, F.J.H., and Berkenbosch, F. (1995) Appearance of inducible nitric oxide synthase in rat central nervous system after rabies virus infection and during experimental allergic encephalomyelitis but not after periferal administration of endotoxin. J. Neurosci. Res., 40:251-260.
50. Vincent, S.R., Das, S., and Maines, M.D. (1994) Brain heme oxygenase isozymes and nitric oxide synthase are co-localized in select neurons. Neuroscience, 63:223-231.
51. Willis, D., Frederick, A.T.R., Paul-Clark, M.J., and Willoughby, D.A. (1995) Modulation of heme oxygenase activity in rat brain and spleen by inhibitors and donors of nitric oxide. Biochem. Biophys. Res. Commun., 214:1152-1156.
52. Zhang, J., Dawson, V.L., Dawson, T.M., and Snyder, S.H. (1994) ADP-ribosylation as a cGMP-independent pathway to mediate nitric oxide effects. In: Nitric Oxide: Roles in Neuronal Communication and Neurotoxicity. H. Takagi, N. Toda, and R.D. Hawkins, eds. Japan Scientific Societies Press and CRC Press, Tokyo, pp. 223-234.