Induction of heme oxygenase-1 and major histocompatibility complex antigens in transient forebrain ischemia

Journal of Cerebral Blood Flow and Metabolism

Volumn 18, Issue 8, 1998, Pages 824-832

  Matsuoka, Yasuji ^a   Kitamura, Yoshihisa ^a   Okazaki, Mitsuhiro ^a   Sakata, Masahiro ^a   Tsukahara, Tetsuya ^b   Taniguchi, Takashi ^a  

^a KYOTO PHARMACEUTICAL UNIVERSITY   (Japan)

^b NATIONAL HOSPITAL ORGANIZATION KYOTO MEDICAL CENTER   (Japan)

Author keywords

Heme oxygenase; Hippocampus; Ischemia; Major histocompatibility complex; Microglia; Neuroimmunology

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; HEAT SHOCK PROTEIN; HEME OXYGENASE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; ENZYME INDUCTION; FOREBRAIN; GLIA CELL; HIPPOCAMPUS; MALE; MICROGLIA; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; TRANSIENT ISCHEMIC ATTACK;

EID: 0031855776     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1097/00004647-199808000-00002     Document Type: Article

References (54)

1. Akiyama H, Itagaki S, McGeer PL (1988) Major histocompatibility complex antigen expression on rat microglia following epidural kainic acid lesions. J Neurosci Res 20:147-157
2. Applegate LA, Luscher P, Tyrell RM (1991) Induction of heme oxygenase: a general response to oxidant stress in cultured mammalian cells. Cancer Res 51:974-978
3. Brüne B, Dimmeler S, Molinay L, Vedia LM, Lapetina EG (1994) Nitric oxide: a signal for ADP-ribosylation of proteins. Life Sci 54:61-70
4. Buttini M, Appel K, Sauter A, Gebicke-Haerter P-J, Boddeke HWGM (1996) Expression of tumor necrosis factor alpha after focal cerebral ischemia in the rat. Neuroscience 71:1-16
5. Dickson DW, Lee SC, Mattiace LA, Yen SC, Brosnan C (1993) Microglia and cytokines in neurological disease, with special reference to AIDS and Alzheimer's disease. Glia 7:75-83
6. Endoh M, Maiese K, Wagner J (1994) Expression of the inducible form of the nitric oxide synthase by reactive astrocytes after transient global ischemia. Brain Res 651:92-100
7. Ewing JF, Maines MD (1991) Rapid Induction of heme oxygenase-1 mRNA and protein by hyperthermia in rat brain: heme oxygenase-2 is not a heat shock protein. Proc Natl Acad Sci USA 88: 5364-5368
8. Ewing JF, Harber SN, Maines MD (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 JF, Weber CM, Maines MD (1993) Biliverdin reductase is heat resistant and expressed with constitutive and heat shock form of heme oxygenase. J Neurochem 61:1015-1023
10. Gavrieli Y, Sherman Y, Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493-501
11. Hayashi T, Morimoto C, Burks JS, Kerr C, Hauser SL (1988) Dual-labeled immunocytochemistry of the active multiple sclerosis lesion: major histocompatibility complex and activation antigens. Ann Neurol 24:523-531
12. Iadecola C, Zhang F, Xu S, Casey R, Ross ME (1995) Inducible nitric oxide synthase gene expression in brain following cerebral ischemia. J Cereb Blood Flow Metab 15:378-384
13. Jørgensen MB, Finsen BR, Jensen MB, Castellano B, Diemer NH, Zimmer J (1993) Microglial and astroglial reactions to ischemic and kainic acid-induced lesions of the adult rat hippocampus. Exp Neurol 120:70-88
14. Kaku Y, Yonekawa Y, Tsukahara T, Ogata N, Kimura T, Taniguchi T (1993) Alternation of a 200kDa neurofilament in the rat hippocampus after forebrain ischemia. J Cereb Blood Flow Metab 13: 402-408
15. Keyse SM, Tyrrell RM (1989) Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblast by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci USA 86:99-103
16. Kiessling M, Dienel GA, Jacewicz M, Pulsineli WA (1986) Protein synthesis in postischemic rat brain: a two-dimensional electrophoretic analysis. J Cereb Blood Flow Metab 6:642-649
17. Kinouchi H, Sharp FR, Hill MP, Koistinaho J, Sagar SM, Chan PH (1993) Induction of 70-kDa heat shock protein and hsp70 mRNA following transient focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 13:105-115
18. Kitamura Y, Takahashi H, Matsuoka Y, Tooyama I, Kimura H, Nomura Y, Taniguchi T (1996) In vivo induction of inducible nitric oxide synthase by microinjection with interferon-γ and lipopolysaccharide in rat hippocampus. Glia 18:233-243
19. Kondo T, Reaume AG, Huang TT, Carlson E, Murakami K, Chen SF, Hoffman EK, Scott RW, Epstein CJ, Chan PH (1997) Reduction of CuZn-superoxide dismutase activity exacerbates neuronal cell injury and edema formation after transient focal cerebral ischemia. J Neurosci 17:4180-4189
20. Lavrosky Y, Schwartzman ML, Abraham NG (1993) Novel regulatory sites of the human heme oxygenase-1 promoter region. Biochem Biophys Res Commun 196:336-341
21. Lee PJ, Alam J, Wiegand GW, Choi MK (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
22. Llesuy SF, Tomaro ML (1994) Heme oxygenase and oxidative stress: evidence of involvement of bilirubin as physiological protector against oxidative damage. Biochim Biophys Acta 1223:9-14
23. MacGregor DG, Higgins MJ, Jones PA, Maxwell WL, Watson MW, Graham DL, Stone TW (1996) Ascorbate attenuates the systemic kainate-induced neurotoxicity in the rat hippocampus. Brain Res 727:133-144
24. Maines MD (1988) Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J 2:2557-2568
25. Maines MD (1993) Carbon monoxide: an emerging regulator of cGMP in the brain. Mol Cell Neurosci 4:389-397
26. Matz PG, Massa SM, Weinstein PR, Turner C, Panter SS, Sharp FR (1996a) Focal hyperexpression of hemeoxygenase-1 protein and messenger RNA in rat brain caused by cellular stress following subarachnoid injections of lysed blood. J Neurosurg 85:892-900
27. Matz P, Turner C, Weinstein PR, Massa SM, Panter SS, Sharp FR (1996b) Heme oxygenase-1 induction in glia throughout rat brain following experimental subarachnoid hemorrhage. Brain Res 713: 211-222
28. Matz PG, Weinstein PR, Sharp FR (1997) Heme oxygenase-1 and heat shock protein 70 induction in glia and neurons throughout rat brain after experimental intracerebral hemorrhage. Neurosurgery 40: 152-160
29. McCoubrey WK Jr, Ewing JF, Maines MD (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
30. McGeer PL, Kawamata T, Walker DG, Akiyama H, Tooyama I, McGeer ED (1993) Microglia in degenerative neurological disease. Glia 7:84-92
31. Murphy BJ, Laderoute KR, Short SM, Sutgerland RM (1991) The identification of heme oxygenase as a major hypoxic stress protein in Chinese hamster ovary cells. Br J Cancer 64:69-73
32. Nath KA, Balla G, Vercellotti GM, Balla J, Jacob HS, Levitt MD, Rosenberg ME (1992) Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. J Clin Invest 90:267-270
33. Nimura T, Weinstein PR, Massa SM, Panter S, Sharp FR (1996) Heme oxygenase-1 (HO-1) protein in rat brain following focal ischemia. Mol Brain Res 37:201-208
34. Nitatori T, Sato N, Waguri S, Karasawa Y, Araki H, Shibanal K, Kominami E, Uchiyama Y (1995) Delayed neuronal death in the CA1 pyramidal cells layer of the gerbil hippocampus following transient ischemia is apoptosis. J Neurosci 15:1001-1011
35. Okinaga S, Shibahara S (1993) Identification of a nuclear protein that constitutive recognizes the sequence containing a heat-shock element. Its binding properties and possible function modulating heat-shock induction of the rat heme oxygenase gene. Eur J Biochem 212:167-175
36. Paschen W, Uto A, Djuricic B, Schmitt J (1994) Hemeoxygenase expression after reversible ischemia of rat brain. Neurosci Lett 180:5-8
37. Rao K, Lund RD (1993) Optic nerve degeneration induces the expression of MHC antigens in rat visual system. J Camp Neurol 33: 613-627
38. Rotenberg MO, Maines MD (1990) Isolation, characterization, and expression in Escherichia coli of a cDNA encoding rat heme oxygenase-2. J Biol Chem 265:7501-7506
39. Salminen A, Liu PK, Hsu CY (1995) Alternation of transcription factor binding activities in the ischemic rat brain. Biochem Biophysic Res Commun 212:939-944
40. Sauders EL, Maines MD, Meredith MJ, Freeman ML (1991) Enhancement of heme oxygenase-1 synthesis by glutathione depletion in Chinese hamster ovary cells. Arch Biochem Biophys 288:268-373
41. Sharp FR, Kinouchi H, Koistinaho J, Chan PH, Sagar SM (1993) HSP70 heat shock gene regulation during ischemia. Stroke 24(12 Suppl): 172-175
42. Shibahara S, Müller R, Taguchi H, Yoshida T (1985) Cloning and expression of cDNA for rat heme oxygenase. Proc Natl Acad Sci USA 82:7865-7869
43. Shibahara S, Müller RM, Taguchi H (1987) Transcription control of the rat heme oxygenase by heat shock. J Biol Chem 262:12889-12892
44. Smith ML, Auer RN, Siesjo BK (1984) The density and distribution of ischemic brain injury in the rat following 2-10 min of forebrain ischemia. Acta Neuropathol (Berl) 64:319-332
45. Stocker P, Glazer AN, Ames BN (1987a) Antioxidant activity of albumin bound bilirubin. Proc Natl Acad Sci USA 84:5918-5923
46. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN (1987b) Bilirubin is an antioxidant of possible physiological importance. Science 235:1043-1046
47. Takeda A, Onodera H, Sugimoto A, Itoyama Y, Kogure K, Shibahara S (1994) Increased expression of heme oxygenase mRNA in rat brain following transient forebrain ischemia. Brain Res 666:120-124
48. Terai K, Matsuo A, McGeer EG, McGeer PL (1996) Enhancement of immunoreactivity for NF-κB in human cerebral infarctions. Brain Res 739:343-349
49. Tooyama I, Kimura H, Akiyama H, McGeer PL (1990) Reactive microglia express class I and class II major histocompatibility complex antigen in Alzheimer's disease. Brain Res 523:273-280
50. Traugott U, Lebon P (1988) Interferon-γ and la antigen are present on astrocytes in active chronic multiple sclerosis lesions. J Neurosci Res 84:257-264
51. Uemura Y, Kowall NW, Moskowitz MA (1991) Focal ischemia in rats causes time-dependent expression of c-fos protein immunoreactivity in wide spread regions of ipsilateral cortex. Brain Res 552:99-105
52. Vincent SR, Das S, Maines MD (1994) Brain heme oxygenase isozymes and nitric oxide synthase are co-localized in select neurons. Neuroscience 63:223-231
53. Widera G (1986) Molecular biology of the histocompatibility complex. Science 233:437-443
54. Zhang J, Dawson VL, Dawson TM, Snyder SH (1994) ADP-ribosylation as a cGMP-independent pathway to mediate nitric oxide effects. In: Nitric Oxide: Roles in Neuronal Communication and Neurotoxicity (Takagi H, Toda N, Hawkins RD, eds), Tokyo, Japan Scientific Societies Press and CRC Press, pp 223-234