Interleukin 3 prevents delayed neuronal death in the hippocampal CA1 field

Journal of Experimental Medicine

Volumn 188, Issue 4, 1998, Pages 635-649

  Wen, Tong Chun ^a   Tanaka, Junya ^a   Peng, Hui ^a   Desaki, Junzo ^a   Matsuda, Seiji ^a   Maeda, Nobuji ^a   Fujita, Hiroko ^a   Sato, Kohji ^a   Sakanaka, Masahiro ^a  

^a EHIME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Bcl x(L); DNA fragmentation; Interleukin 3; Receptor; Transient forebrain ischemia

Indexed keywords

BIOTIN; DEOXYURIDINE PHOSPHATE; DNA FRAGMENT; DNA NUCLEOTIDYLEXOTRANSFERASE; INTERLEUKIN 3; INTERLEUKIN 3 RECEPTOR; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 2; ONCOPROTEIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CONTROLLED STUDY; GERBIL; HIPPOCAMPUS; HISTOCHEMISTRY; HISTOPATHOLOGY; IMMUNOBLOTTING; IN SITU HYBRIDIZATION; LEARNING DISORDER; MALE; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BCL-X PROTEIN; CELL DEATH; CELLS, CULTURED; CEREBRAL CORTEX; FERROUS COMPOUNDS; GENE EXPRESSION; GERBILLINAE; HIPPOCAMPUS; INTERLEUKIN-3; MALE; NEURONS; NEUROPROTECTIVE AGENTS; OXIDANTS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; REACTIVE OXYGEN SPECIES; RECEPTORS, INTERLEUKIN-3; SYNAPSES;

EID: 0032541386     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.188.4.635     Document Type: Article

References (62)

1. Schrader, J.W. 1986. The pan specific hemopoietin of activated T-lymphocytes (interleukin-3). Annu. Rev. Immunol. 4: 205-230.
2. Frendl, G., and D.I. Beller. 1990. Regulation of macrophage activation by IL-3. J. Immunol. 144:3392-3399.
3. Frendl, G. 1992. Interleukin-3: from colony-stimulating factor to pluripotent immunoregulatory cytokine. J. Immunol. 14:421-430.
4. Ihle, J.N., and Y. Weinstein. 1986. Immunological regulation of hematopoietic/lymphoid stem cell differentiation by interleukin 3. Adv. Immunol. 39:1-50.
5. Clarke, S.C., and R. Kamen. 1987. The human hematopoietic colony-stimulating factors. Science. 236:1229-1237.
6. Park, L.S., D. Friend, S. Gillis, and D.L. Urdal. 1986. Characterization of the cell surface receptor for a multi-lineage colony-stimulating factor (CSF-2). J. Biol. Chem. 261:205-210.
7. Appel, K., M. Buttini, A. Sauter, and P.J. Gebicke-Haerter. 1995. Cloning of rat interleukin-3 receptor beta-subunit from cultured microglia and its mRNA expression in vivo. J. Neurosci. 15:5800-5809.
8. Frei, K., S. Bodmer, C. Schwerdel, and A. Fontana. 1983. Astrocytes of the brain synthesize interleukin-3-like factors. J. Immunol. 135:4044-4047.
9. Frei, K., S. Bodmer, C. Schwerdel, and A. Fontana. 1986. Astrocyte-derived interleukin-3 as a growth factor for microglia cells and peritoneal macrophages. J. Immunol. 137:3521-3527.
10. Moroni, S.C., and A. Rossi. 1995. Enhanced survival and differentiation in vitro of different neuronal populations by some interleukins. Int. J. Dev. Neurosci. 13:41-49.
11. Kamegai, M., K. Niijima, T. Kunishita, M. Nishizawa, M. Ogawa, M. Araki, A. Ueki, Y. Konishi, and T. Tabira. 1990. Interleukin-3 as a trophic factor for central cholinergic neurons in vitro and in vivo. Neuron. 2:429-436.
12. Farrar, W.L., M. Vinocour, and J.M. Hill. 1988. In situ hybridization histochemistry localization of interleukin-3 mRNA in mouse brain. Blood. 73:137-140.
13. Konishi, Y., D.H. Chui, T. Kunishita, T. Yamamura, Y. Higashi, and T. Tabira. 1995. Demonstration of interleukin-3 receptor-associated antigen in the central nervous system. J. Neurosci. Res. 41:572-582.
14. Konishi, Y., M. Kamegai, K. Takahashi, T. Kunishita, and T. Tabira. 1994. Production of interleukin-3 by murine central nervous system neurons. Neurosci. Lett. 182:271-274.
15. Rinaudo, M.S., K. Su, L.A. Falk, S. Halder, and R.A. Mufson. 1995. Human interleukin-3 receptor modulates bcl-2 mRNA and protein levels through protein kinase C in TF-1 cells. Blood. 86:80-88.
16. Hockenbery, D.M., Z.N. Oltvai, X.-M. Yin, C.L. Milliman, and S.J. Korsmeyer. 1993. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell. 75:241-251.
17. Kane, D.J., T.A. Sarafian, R. Anton, H. Hahn, E.B. Gralla, J.S. Valentine, T. Ord, and D.E. Bredesen. 1993. Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science. 262:1274-1277.
18. Boise, L.H., M. Gonzalez-Garcia, C.E. Postema, L. Ding, T. Lindsten, L.A. Turka, X. Mao, G. Nunez, and C.B. Thompson. 1993. Bcl-x, bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell. 74:597-608.
19. Gottschalk, A.R., L.H. Boise, C.B. Thompson, and J. Quintans. 1994. Identification of immunosuppressant-induced apoptosis in a murine B-cell line and its prevention by bcl-x but not bcl-2. Proc. Natl. Acad. Sci. USA. 91:7350-7354.
20. Gonzalez-Garcia, M., I. Garcia, L. Ding, S. O'Shea, L.H. Boise, C.B. Thompson, and G. Nunez. 1995. Bcl-x is expressed in embryonic and postnatal neural tissues and functions to prevent cell death. Proc. Natl. Acad. Sci. USA. 92: 4304-4308.
21. L is the major Bcl-x mRNA form expressed during murine development and its product localization to mitochondria. Development (Camb.). 120:3033-3042.
22. Krajewski, S., M. Krajewska, A. Shabaik, H.G. Wang, S. Irie, L. Fong, and J.C. Reed. 1994. Immunohistochemical analysis of in vivo patterns of Bcl-x expression. Cancer Res. 54:5501-5507.
23. Wen, T.-C., S. Matsuda, H. Yoshimura, J. Aburaya, F. Kushihata, and M. Sakanaka. 1995. Protective effect of basic fibroblast growth factor-heparin and neurotoxic effect of platelet factor 4 on ischemic neuronal loss and learning disability in gerbils. Neuroscience. 65:513-521.
24. Wen, T.-C., S. Matsuda, H. Yoshimura, T. Kawabe, and M. Sakanaka. 1995. Ciliary neurotrophic factor prevents ischemia-induced learning disability and neuronal loss in gerbils. Neurosci. Lett. 191:55-58.
25. Kotani, Y., S. Matsuda, T.-C. Wen, M. Sakanaka, J. Tanaka, N. Maeda, K. Kondon, S. Ueno, and A. Sano. 1996. A hydrophilic peptide comprising 18 amino acid residues of the prosaposin sequence has neurotrophic activity in vitro and in vivo. J. Neurochem. 66:2197-2200.
26. Roberts-Lewis, J.M., V.R. Marcy, Y. Zhao, J.L. Vaught, R. Siman, and M.E. Lewis. 1993. Aurintricarboxylic acid protects hippocampal neurons from NMDA- and ischemia-induced toxicity in vivo. J. Neurochem. 61:378-381.
27. Stein-Behrens, B., M.P. Mattson, I. Chang, M. Yeh, and R. Sapolsky. 1994. Stress exacerbates neuron loss and cytoskeletal pathology in the hippocampus. J. Neurosci. 14:5373-5380.
28. Flamm, E.S., H.B. Demopoulos, M.L. Seligman, R.G. Poser, and J. Ransohoff. 1978. Free radicals in cerebral ischemia. Stroke. 9:445-447.
29. Chan, P.H., J.W. Schmidley, R.A. Fishman, and S.M. Longar. 1984. Brain injury, edema, and vascular permeability changes induced by oxygen-derived free radicals. Neurology. 34:315-320.
30. Choi, D.W. 1995. Calcium: still center-stage in hypoxicischemic neuronal death. Trends Neurosci. 18:58-60.
31. Siesjö, B.K. 1981. Cell damage in the brain: a speculative synthesis. J. Cereb. Blood Flow Metab. 1:155-185.
32. Cao, W., J.M. Carney, A. Duchon, R.A. Floyd, and M. Chevion. 1988. Oxygen free radical involvement in ischemia and reperfusion injury to brain. Neurosci. Lett. 88:233-238.
33. Oliver, C.N., P.E. Starke-Reed, E.R. Stadtman, G.J. Liu, J.M. Carney, and R.A. Floyd. 1990. Oxidative damage to brain protein, loss of glutamine synthetase activity, and production of free oxygen radicals during ischemia/reperfusion-induced injury to gerbil brain. Proc. Natl. Acad. Sci. USA. 87: 5144-5147.
34. Asano, T., T. Koide, O. Gotoh, H. Joshita, T. Hanamura, T. Shigeno, and H. Maeda. 1990. Free radical generation during brief period of cerebral ischemia may trigger delayed neuronal death. Neuroscience. 35:551-558.
35. Thiessen, D., and P. Yahr. 1977. A stereo-taxic brain atlas of the gerbil. In The Gerbil in Behavioral Investigations, Mechanisms of Territoriality and Olfactory Communication. University of Texas, Austin TX. 138 pp.
36. Sano, A., S. Matsuda, T.-C. Wen, Y. Kotani, K. Kondoh, S. Ueno, Y. Kakimoto, H. Yoshimura, and M. Sakanaka. 1994. Protection by prosaposin against ischemia-induced learning disability and neuronal loss. Biochem. Biophys. Res. Commun. 204:994-1000.
37. 2 analog, TEI-7165, on ischemic neuronal damage in gerbils. Brain Res. 769:321-328.
38. Wen, T.-C., S. Matsuda, H. Yoshimura, J.-H. Lim, and M. Sakanaka. 1996. Ginseng root prevents learning disability and neuronal loss in gerbils with 5-minute forebrain ischemia. Acta Neuropathol. 91:15-22.
39. Mitani, A., Y. Andou, S. Matsuda, and K. Kataoka. 1991. Transient forebrain ischemia of three-minute duration consistently induces severe neuronal damage in field CA1 of the hippocampus in the normothermic gerbil. Neurosci. Lett. 131: 171-174.
40. Araki, H., M. Nojiri, K. Kawashima, M. Kimura, and H. Aihara. 1986. Behavioral, electroencephalographic and histopathological studies on Mongolian gerbils with occluded common carotid arteries. Physiol. Behav. 38:89-94.
41. Sakanaka, M., T. Shibasaki, and K. Lederis. 1991. Improved fixation and cobalt-glucose oxidase-diaminobenzidine intensification for immunohistochemical demonstration of corticotropin-releasing factor in rat brain. J. Histochem. Cytochem. 35:207-212.
42. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227: 680-685.
43. Towbin, H., T. Staehelin, and J. Goudon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheet: procedure and some applications. Proc. Natl. Acad. Sci. USA. 76:4350-4354.
44. Kira, M., J. Tanaka, and K. Sobue. 1995. Caldesmon and low Mr isoform of tropomyosin are localized in neuronal growth cones. J. Neurosci. Res. 40:294-305.
45. Tanaka, J., and N. Maeda. 1996. Microglial ramification requires non-diffusible factors derived from astrocytes. Exp. Neurol. 137:367-375.
46. Tanaka, J., H. Fijita, S. Matsuda, K. Toku, M. Sakanaka, and N. Maeda. 1997. Glucocorticoid- and mineralocorticoid receptors in microglial cells: the two receptors mediate differential effects of corticosteroids. Glia. 20:23-37.
47. Braughler, J.M., L.A. Duncan, and R.L. Chase. 1986. The involvement of iron in lipid peroxidation: importance of ferric to ferrous ratios in initiation. J. Biol. Chem. 261:10282-10289.
48. Floyd, R.A. 1990. Role of oxygen free radicals in carcinogenesis and brain ischemia. FASEB (Fed. Am. Soc. Exp. Biol.) J. 4:2587-2597.
49. Stadtman, E.R., and C.N. Oliver. 1991. Metal-catalyzed oxidation of proteins: physiological consequences. J. Biol. Chem. 266:2005-2008.
50. Zhang, Y., T. Tatsuno, J. Carney, and M.P. Mattson. 1993. Basic FGF, NGF and IGFs protect hippocampal neurons against iron-induced degeneration. J. Cereb. Blood Flow Metab. 13:378-388.
51. Lim, J.-H., T.-C. Wen, S. Matsuda, J. Tanaka, N. Maeda, H. Peng, J. Aburaya, K. Ishihara, and M. Sakanaka. 1997. Protection of ischemic hippocampal neurons by ginsenoside Rb1, a main ingredient of ginseng root. Neurosci. Res. 28: 191-200.
52. Kirino, T. 1982. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res. 239:57-69.
53. Sapolsky, R.M., and W.A. Pulsinelli. 1985. Glucocorticoids potentiate ischemic injury to neurons: therapeutic implications. Science. 229:1379-1400.
54. Sapolsky, R.M., L.C. Krey, and B.S. McEwen. 1985. Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J. Neurosci. 5:1222-1227.
55. Rothman, S.M., and J.W. Olney. 1986. Glutamate and pathophysiology of hypoxic brain damage. Ann. Neurol. 19: 105-111.
56. Siesjö, B.K., and F. Bengtsson. 1989. Calcium fluxes, calcium antagonists, and calcium-related pathology in brain ischemia, hypoglycemia, and spreading depression: a unifying hypothesis. J. Cereb. Blood Flow Metab. 9:127-140.
57. Siesjö, B.K., K. Katsura, and T. Kristian. 1995. The biochemical basis of cerebral ischemic damage. J. Neurosurg. Anesthesiol. 7:47-52.
58. Mattson, M.P., B. Cheng, and V.L. Smith-Swintosky. 1993. Growth factor-mediated protection from excitotoxicity and disturbances in calcium and free radical metabolism. Semin. Neurosci. 5:295-307.
59. Maeda, Y., M. Matsumoto, O. Hori, K. Kuwabara, S. Ogawa, S.D. Yan, T. Ohtsuki, T. Kinoshita, T. Kamada, and D.M. Stern. 1994. Hypoxia/reoxygenation-mediated induction of astrocyte interleukin 6: a paracrine mechanism potentially enhancing neuron survival. J. Exp. Med. 180:2297-2308.
60. Lindvall, O., Z Kokaia, J. Bengzon, E. Elmer, and M. Kokaia. 1994. Neurotrophins and brain insults. Trends Neurosci. 17:490-496.
61. Rothwell, N.J., and S.J. Hopkins. 1995. Cytokines and the nervous system II: actions and mechanisms of action. Trends Neurosci. 18:130-136.
62. Nitatori, T., N. Sato, S. Waguri, Y. Karasawa, H. Araki, K. Shibanai, E. Kominami, and Y. Uchiyama. 1995. Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J. Neurosci. 15:1001-1011.