Dose-dependent, protective effect of FK506 against white matter changes in the rat brain after chronic cerebral ischemia

Brain Research

Volumn 792, Issue 1, 1998, Pages 105-113

  Wakita, Hideaki ^a   Tomimoto, Hidekazu ^a   Akiguchi, Ichiro ^a   Kimura, Jun ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Chronic cerebral ischemia; FK506; Microglia; Rat; White matter change

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CD45 ANTIGEN; CREATININE; DRUG VEHICLE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; IMMUNOSUPPRESSIVE AGENT; MAJOR HISTOCOMPATIBILITY ANTIGEN; TACROLIMUS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR COMMISSURE; ARTICLE; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN PROTECTION; CAPSULA INTERNA; COMMON CAROTID ARTERY; CONTROLLED STUDY; CORPUS CALLOSUM; DOSE RESPONSE; IMMUNOHISTOCHEMISTRY; INTRAMUSCULAR DRUG ADMINISTRATION; MACROGLIA; MACROPHAGE; MALE; MICROGLIA; NONHUMAN; OPTIC NERVE; OPTIC TRACT; PRIORITY JOURNAL; RAT; WHITE MATTER;

ANIMALS; BLOOD GLUCOSE; BLOOD UREA NITROGEN; BRAIN; BRAIN ISCHEMIA; CHRONIC DISEASE; DOSE-RESPONSE RELATIONSHIP, DRUG; IMMUNOHISTOCHEMISTRY; MALE; NEUROPROTECTIVE AGENTS; OPTIC NERVE; RATS; RATS, WISTAR; TACROLIMUS; TIME FACTORS; TRANSAMINASES;

EID: 0032482134     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(98)00126-7     Document Type: Article

References (54)

1. I. Akiguchi, H. Tomimoto, T. Suenaga, H. Wakita, H. Budka, Alterations in glia and axons in the brains of Binswanger's disease patients, Stroke 28 (1997) 1423-1429.
2. R.B. Banati, P. Schubert, G. Rothe, J. Gehrmann, K. Rudolphi, G. Valet, G.W. Kreutzberg, Modulation of intracellular formation of reactive oxygen intermediates in peritoneal macrophages and microglia/brain macrophages by propentofylline, J. Cereb. Blood Flow Metab. 14 (1994) 145-149.
3. A. Benson, H.K. Ziegler, Macrophage as targets for inhibition by cyclosporine, Transplantation 47 (1989) 696-703.
4. D. Burnett, D.H. Adams, T.J.M. Martin, Q. Liu, R.A. Grant, R.A. Stockley, J.M. Lord, Inhibition by FK506 of formyl peptide-induced neutrophil activation and associated protein synthesis, Biochem. Pharmacol. 48 (1994) 1081-1088.
5. R. Busto, W.D. Dietrich, M.Y.T. Globus, M.D. Ginsberg, The importance of brain temperature in cerebral ischemic injury, Stroke 20 (1989) 1113-1114.
6. M. Conde, J. Andrade, F.J. Bedoya, C. Santa Maria, F. Sobrino, Inhibitory effect of cyclosporin A and FK506 on nitric oxide production by cultured macrophages. Evidence of a direct effect on nitric oxide synthase activity, Immunology 84 (1995) 476-481.
7. T.M. Dawson, J.P. Steiner, V.L. Dawson, J.L. Dinerman, G.R. Uhl, S.H. Snyder, Immunosuppressant FK506 enhances phosphorylation of nitric oxide synthase and protects against glutamate neurotoxicity, Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 9808-9812.
8. V.L. Dawson, T.M. Dawsom, D.A. Bartley, G.R. Uhl, S.H. Snyder, Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures, J. Neurosci. 13 (1993) 2651-2661.
9. J. DeLeo, L. Toth, P. Schubert, K. Rudolphi, G.W. Kreutzberg, Ischemia-induced neuronal cell death, calcium accumulation and glial response in the hippocampus of the Mongolian gerbil and protection by propentofylline (HWA 285), J. Cereb. Blood Flow Metab. 7 (1987) 745-751.
10. M. Drake, H. Friberg, F. Boris-Mšller, K. Sakata, T. Wieloch, The immunosuppressant FK506 ameliorates ischaemic damage in the rat brain, Acta Physiol. Scand. 158 (1996) 155-159.
11. D.A. Fruman, P.E. Mather, S.J. Burakoff, B.E. Bierer, Correlation of calcineurin phosphatase activity and programmed cell death in murine T cell hybridomas, Eur. J. Immunol. 22 (1992) 2513-2517.
12. J. Gehrmann, P. Bonnekoh, T. Miyazawa, K.A. Hossman, G.W. Kreutzberg, Immunocytochemical study of an early microglial activation in ischemia, J. Cereb. Blood Flow Metab. 12 (1992) 257-269.
13. D. Giulian, T.J. Baker, Characterization of ameboid microglia isolated from developing mammalian brain, J. Neurosci. 6 (1986) 2163-2178.
14. E.J. Griffiths, A.P. Halestrap, Protection by cyclosporin A of ischemia/reperfusion-induced damage in isolated rat hearts, J. Mol. Cell Cardiol. 25 (1993) 1461-1469.
15. R.P. Hellendall, J.P.Y. Ting, Differential regulation of cytokine-induced major histocompatibility complex class II expression and nitric oxide release in rat microglia and astrocytes by effectors of tyrosine kinase, protein kinase C, and cAMP, J. Neuroimmunol. 74 (1997) 19-29.
16. Y. Hirano, T. Mitamura, T. Tamura, K. Ohara, Y. Mine, H. Noguchi H, Mechanism of FK506-induced glucose intolerance in rats, J. Toxicol. Sci. 19 (1994) 61-65.
17. T. Ide, E. Morikawa, T. Kirino, An immunosuppressant, FK506, protects hippocampal neurons from forebrain ischemia in the mongolian gerbil, Neurosci. Lett. 204 (1996) 157-160.
18. K. Kawano, Y.I. Kim, T. Kai, T. Ishi, T. Tatsuma, A. Morimoto, Y. Tamura, M. Kobayashi, Evidence that FK506 alleviates ischemia/reperfusion injury to the rat liver: in vivo demonstration for suppression of TNF-α production in response to endotoxemia, Eur. Surg. Res. 26 (1994) 108-115.
19. N. Keicho, S. Sawada, K. Kitamura, H. Yotsumoto, F. Takaku, Effects of an immunosuppressant, FK506, on interleukin 1 alpha production by human macrophages and a macrophage-like cell line, U937, Cell Immunol. 132 (1991) 285-294.
20. T. Kino, H. Hatanaka, M. Hashimoto, M. Nishiyama, T. Goto, M. Okuhara, M. Kohsaka, H. Aoki, H. Imanaka, FK-506, a novel immunosuppressant isolated from a Streptomyces: I. Fermentation, isolation, and physico-chemical and biological characteristics, J. Antibiot. Tokyo 40 (1987) 1249-1255.
21. B. Klun, Spinal fluid and blood serum enzyme activity in brain injuries, J. Neurosurg. 41 (1974) 224-228.
22. Y. Kondo, N. Ogawa, M. Asanuma, S. Nishibayashi, E. Iwata, A. Mori, Cyclosporin A prevents ischemia-induced reduction of mus-carinic acetylcholine receptors with suppression of microglial activation in gerbil hippocampus, Neurosci. Res. 22 (1995) 123-127.
23. K. Kumano, G. Wang, T. Endo, S. Kuwao, FK506-induced nephrotoxicity in rats, Transplant. Proc. 23 (1991) 512-515.
24. S.C. Lee, W. Liu, D.W. Dickson, C.F. Brosnan, J.W. Berman, Cytokine production by human fetal microglia and astrocytes. Differential induction by lipopolysaccharide and IL-1β, J. Immunol. 150 (1993) 2659-2667.
25. G.J. Lees, The possible contribution of microglia and macrophages to delayed neuronal death after ischemia, J. Neurol. Sci. 114 (1993) 119-122.
26. T. Liu, P.C. McDonnell, P.R. Young, R.F. White, A.L. Siren, J.M. Hallenbeck, F.C. Barone, G.Z. Feuerstein, Interleukin-1β mRNA expression in ischemic rat cortex, Stroke 24 (1993) 1746-1751.
27. T. Liu, R.K. Clark, P.C. McDonnell, P.R. Young, R.F. White, F.C. Barone, G.Z. Feuerstein, Tumor necrosis factor-α expression in ischemic neurons, Stroke 25 (1994) 1481-1488.
28. M. Nedergaard, Transient focal ischemia in hyperglycemic rats is associated with increased cerebral infarction, Brain Res. 408 (1987) 79-85.
29. Y. Nishinaka, S. Sugiyama, M. Yokota, H. Saito, T. Ozawa, Protective effect of FK506 on ischemia/reperfusion-induced myocardial damage in canine heart, J. Cardivasc. Pharmacol. 21 (1993) 448-454.
30. H. Ohta, H. Nishikawa, H. Kimura, H. Anayama, M. Miyamoto, Chronic cerebral hypoperfusion by permanent internal carotid ligation produces learning impairment without brain damage in rats, Neuroscience 79 (1997) 1039-1050.
31. T. Otori, T. Katsumata, F. Kashiwagi, Y. Katayama, A. Terashi, Measurement of regional cerebral blood flow (rCBF) and glucose utilization (rCGU) in rat brain under chronic hypoperfusion following bilateral carotid occlusion, Cerebrovasc. Dis. 6 (1996) 71, Suppl.
32. L. Pantoni, J.H. Garcia, Pathogenesis of leukoaraiosis: a review, Stroke 28 (1997) 652-659.
33. H.M. Payan, S. Levine, R. Strebel, Effect of cerebral ischemia in various strains of rats, Proc. Soc. Exp. Biol. Med. 120 (1965) 208-209.
34. R. Prado, M.D. Ginsberg, W.D. Dietrich, B.D. Watson, R. Busto, Hyperglycemia increases infarct size in collaterally perfused but not end-arterial vascular territories, J. Cereb. Blood Flow Metab. 8 (1988) 186-192.
35. M. Sakr, G. Zetti, C. McClain, J. Gavaler, M. Nalesnik, S. Todo, T. Starzl, D.V. Thiel, The protective effect of FK506 pretreatment against renal ischemia/reperfusion injury in rats, Transplantation 53 (1992) 987-991.
36. M. Sawada, N. Kondo, A. Suzumura, T. Marunouchi, Production of tumor necrosis factor-alpha by microglia and astrocytes in culture, Brain Res. 491 (1989) 394-397.
37. J. Sharkey, S.P. Butcher, Immunophilins mediate the neuroprotective effects of FK506 in focal cerebral ischaemia, Nature 371 (1994) 336-339.
38. J. Sharkey, J.H. Crawford, S.P. Butcher, H.M. Marston, Tacrolimus (FK506) ameliorates skilled motor deficits produced by middle cerebral artery occlusion in rats, Stroke 27 (1996) 2282-2286.
39. Y. Shiga, H. Onodera, Y. Matsuo, K. Kogure, Cyclosporin A protects against ischemia-reperfusion injury in the brain, Brain Res. 595 (1992) 145-148.
40. T.E. Starzl, S. Todo, J. Fung, A.J. Demetris, R. Venkataramman, A. Jain, FK506 for liver, kidney, and pancreas transplantation, Lancet 2 (1989) 1000-1004.
41. J.P. Steiner, T.M. Dawson, M. Fotuhi, C.E. Glatt, A.M. Snowman, N. Cohen, S.H. Snyder, High brain densities of the immunophilin FKBP colocalized with calcineurin, Nature 358 (1992) 584-587.
42. S. Suzuki, L.H. Toledo-Pereyra, F.J. Rodriguez, D. Cejalvo, Neutrophil infiltration as an important factor in liver ischemia and reperfusion injury. Modulating effects of FK506 and cyclosporine, Transplantation 55 (1993) 1265-1272.
43. C. Théry, B. Chamak, M. Mallat, Cytotoxic effect of brain macrophages on developing neurons, Eur. J. Neurosci. 3 (1991) 1155-1164.
44. A.W. Thomson, T.E. Starzl, New immunosuppressive drugs: mechanistic insights and potential therapeutic advances, Immunol. Rev. 136 (1993) 71-98.
45. M.J. Tocci, D.A. Matkovich, K.A. Collier, P. Kwok, F. Dumont, S. Lin, S. Degudicibus, J.J. Siekierka, J. Chin, N.I. Hutchinson, The immunosuppressant FK506 selectively inhibits expression of early T cell activation genes, J. Immunol. 143 (1989) 718-726.
46. T. Tokime, K. Nozaki, H. Kikuchi, Neuroprotective effect of FK506, an immunosuppressant, on transient global ischemia in gerbil, Neurosci. Lett. 206 (1996) 81-84.
47. H. Tomimoto, I. Akiguchi, H. Akiyama, J. Kimura, T. Yanagihara, T cell infiltration and expression of MHC class II antigen by macrophage and microglia in a heterogeneous group in leukoencephalopathy, Am. J. Pathol. 143 (1993) 579-586.
48. H. Tomimoto, I. Akiguchi, H. Wakita, J. Kimura, White matter lesions after occlusion of the bilateral carotid arteries in the rat: temporal profile of cerebral blood flow (CBF), oligodendroglia and myelin, Brain Nerve 49 (1997) 639-644.
49. M. Tsuchiya, K. Sako, S. Yura, Y. Yonemasu, Cerebral blood flow and histopathological changes following permanent bilateral carotid artery ligation in Wistar rats, Exp. Brain Res. 89 (1992) 87-92.
50. S. Umemura, T. Yoshida, K. Iwayama, H. Mabe, H. Nagai, Experimental study of ischemic rat brain: correlation of pathological findings with rCBF, Brain Nerve 34 (1982) 179-185.
51. T. Vartanian, Y. Li, M. Zhao, K. Stefansson, Interferon-gamma-induced oligodendrocyte cell death: implications for the pathogenesis of multiple sclerosis, Mol. Med. 1 (1995) 732-743.
52. H. Wakita, H. Tomimoto, I. Akiguchi, J. Kimura, Glial activation and white matter changes in the rat brain induced by chronic cerebral hypoperfusion: an immunohistochemical study, Acta Neuropathol. (Berl.) 87 (1994) 484-492.
53. H. Wakita, H. Tomimoto, I. Akiguchi, J. Kimura, Protective effect of cyclosporin A on the white matter changes in the rat brain after chronic cerebral hypoperfusion, Stroke 26 (1995) 1415-1422.
54. Y. Yagita, K. Kitagawa, K. Matsushita, A. Taguchi, T. Mabuchi, T. Ohtsuki, T. Yanagihara, M. Matsumoto, Effect of immunosuppressant FK506 on ischemia-induced degeneration of hippocampal neurons in gerbils, Life Sci. 59 (1996) 1643-1650.