Defects in cytokine-mediated neuroprotective glial responses to excitotoxic hippocampal injury in senescence-accelerated mouse

Brain, Behavior, and Immunity

Volumn 25, Issue 1, 2011, Pages 83-100

  Hasegawa Ishii, Sanae ^a   Takei, Shiro ^a   Inaba, Muneo ^b   Umegaki, Hiroyuki ^c   Chiba, Yoichi ^a   Furukawa, Ayako ^a   Kawamura, Noriko ^a   Hosokawa, Masanori ^a   Shimada, Atsuyoshi ^a  

^a INSTITUTE FOR DEVELOPMENTAL RESEARCH   (Japan)

^b KANSAI MEDICAL UNIVERSITY   (Japan)

^c NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Aging; Astrocyte; CD44; Cytokines; Microglia; Neurodegeneration; Osteopontin

Indexed keywords

CYTOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GAMMA INTERFERON RECEPTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HERMES ANTIGEN; KAINIC ACID; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; OSTEOPONTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CELL INTERACTION; CONTROLLED STUDY; EXCITOTOXICITY; GENE CONTROL; GENE EXPRESSION; GLIA CELL; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENESCENCE ACCELERATED MOUSE;

AGING; ANIMALS; ANTIGENS, CD44; ASTROCYTES; CELL SIZE; CYTOKINES; GENE EXPRESSION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; KAINIC ACID; MICE; MICE, NEUROLOGIC MUTANTS; MICROGLIA; NEUROGLIA; NEURONS; NEUROTOXINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 78649329486     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2010.08.006     Document Type: Article

References (82)

1. Alboni S., Cervia D., Sugama S., Conti B. Interleukin 18 in the CNS. J. Neuroinflammation 2010, 7:9.
2. Alonso R., Chaudieu I., Diorio J., Krishnamurthy A., Quirion R., Boksa P. Interleukin-2 modulates evoked release of [3H] dopamine in rat cultured mesencephalic cells. J. Neurochem. 1993, 61:1284-1290.
3. Amin D.N., Rottenberg M.E., Thomsen A.R., Mumba D., Fenger C., Kristensson K., Buscher P., Finsen B., Masocha W. Expression and role of CXCL10 during the encephalitic stage of experimental and clinical African trypanosomiasis. J. Infect. Dis. 2009, 200:1556-1565.
4. Auer R.N., Dunn J.F., Sutherland G.R. Hypoxia and related conditions. Greenfield's Neuropathology 2008, 63-119. Hodder Arnold, London. S. Love, D.N. Louis, D.W. Ellison (Eds.).
5. Baker B.J., Akhtar L.N., Benveniste E.N. SOCS1 and SOCS3 in the control of CNS immunity. Trends Immunol. 2009, 30:392-400.
6. Bakhiet M., Mousa A., Seiger A., Andersson J. Constitutive and inflammatory induction of alpha and beta chemokines in human first trimester forebrain astrocytes and neurons. Mol. Immunol. 2002, 38:921-929.
7. Bausch S.B. Potential roles for hyaluronan and CD44 in kainic acid-induced mossy fiber sprouting in organotypic hippocampal slice cultures. Neuroscience 2006, 143:339-350.
8. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 1985, 14:375-403.
9. Bessis A., Bechade C., Bernard D., Roumier A. Microglial control of neuronal death and synaptic properties. Glia 2007, 55:233-238.
10. Bhowmick S., Duseja R., Das S., Appaiahgiri M.B., Vrati S., Basu A. Induction of IP-10 (CXCL10) in astrocytes following Japanese encephalitis. Neurosci. Lett. 2007, 414:45-50.
11. Borges K., McDermott D.L., Dingledine R. Reciprocal changes of CD44 and GAP-43 expression in the dentate gyrus inner molecular layer after status epilepticus in mice. Exp. Neurol. 2004, 188:1-10.
12. Carr D.J., Chodosh J., Ash J., Lane T.E. Effect of anti-CXCL10 monoclonal antibody on herpes simplex virus type 1 keratitis and retinal infection. J. Virol. 2003, 77:10037-10046.
13. Chen K., Iribarren P., Huang J., Zhang L., Gong W., Cho E.H., Lockett S., Dunlop N.M., Wang J.M. Induction of the formyl peptide receptor 2 in microglia by IFN-gamma and synergy with CD40 ligand. J. Immunol. 2007, 178:1759-1766.
14. Chiba Y., Shimada A., Kumagai N., Yoshikawa K., Ishii S., Furukawa A., Takei S., Sakura M., Kawamura N., Hosokawa M. The senescence-accelerated mouse (SAM): a higher oxidative stress and age-dependent degenerative diseases model. Neurochem. Res. 2009, 34:679-687.
15. Choi J.S., Kim H.Y., Cha J.H., Choi J.Y., Lee M.Y. Transient microglial and prolonged astroglial upregulation of osteopontin following transient forebrain ischemia in rats. Brain Res. 2007, 1151:195-202.
16. Conde J.R., Streit W.J. Microglia in the aging brain. J. Neuropathol. Exp. Neurol. 2006, 65:199-203.
17. Dickstein D.L., Kabaso D., Rocher A.B., Luebke J.I., Wearne S.L., Hof P.R. Changes in the structural complexity of the aged brain. Aging Cell 2007, 6:275-284.
18. Dilger R.N., Johnson R.W. Aging, microglial cell priming, and the discordant central inflammatory response to signals from the peripheral immune system. J. Leukoc. Biol. 2008, 84:932-939.
19. Ellison J.A., Velier J.J., Spera P., Jonak Z.L., Wang X., Barone F.C., Feuerstein G.Z. Osteopontin and its integrin receptor alpha(v)beta3 are upregulated during formation of the glial scar after focal stroke. Stroke 1998, 29:1698-1706. discussion 1707.
20. Eriksson C., Tehranian R., Iverfeldt K., Winblad B., Schultzberg M. Increased expression of mRNA encoding interleukin-1beta and caspase-1, and the secreted isoform of interleukin-1 receptor antagonist in the rat brain following systemic kainic acid administration. J. Neurosci. Res. 2000, 60:266-279.
21. Eriksson C., Van Dam A.M., Lucassen P.J., Bol J.G., Winblad B., Schultzberg M. Immunohistochemical localization of interleukin-1beta, interleukin-1 receptor antagonist and interleukin-1beta converting enzyme/caspase-1 in the rat brain after peripheral administration of kainic acid. Neuroscience 1999, 93:915-930.
22. Eriksson C., Winblad B., Schultzberg M. Kainic acid induced expression of interleukin-1 receptor antagonist mRNA in the rat brain. Brain Res. Mol. Brain Res. 1998, 58:195-208.
23. Gessani S., Belardelli F. IFN-gamma expression in macrophages and its possible biological significance. Cytokine Growth Factor Rev. 1998, 9:117-123.
24. Graeber M.B., Streit W.J. Microglia: biology and pathology. Acta Neuropathol. 2010, 119:89-105.
25. Hanisch U.K. Microglia as a source and target of cytokines. Glia 2002, 40:140-155.
26. Hasegawa S., Yamaguchi M., Nagao H., Mishina M., Mori K. Enhanced cell-to-cell contacts between activated microglia and pyramidal cell dendrites following kainic acid-induced neurotoxicity in the hippocampus. J. Neuroimmunol. 2007, 186:75-85.
27. Hasegawa-Ishii, S., Takei, S., Chiba, Y., Furukawa, A., Umegaki, H., Iguchi, A., Kawamura, N., Yoshikawa, K., Hosokawa, M., Shimada, A., 2010. Morphological impairments in microglia precede age-related neuronal degeneration in senescence-accelerated mice. Neuropathology (2010 May 19, Epub ahead of print).
28. Hung J., Chansard M., Ousman S.S., Nguyen M.D., Colicos M.A. Activation of microglia by neuronal activity: results from a new in vitro paradigm based on neuronal-silicon interfacing technology. Brain Behav. Immun. 2010, 24:31-40.
29. Jeon G.S., Park S.K., Park S.W., Kim D.W., Chung C.K., Cho S.S. Glial expression of interleukin-18 and its receptor after excitotoxic damage in the mouse hippocampus. Neurochem. Res. 2008, 33:179-184.
30. Jorgensen M.B., Finsen B.R., Jensen M.B., Castellano B., Diemer N.H., Zimmer J. Microglial and astroglial reactions to ischemic and kainic acid-induced lesions of the adult rat hippocampus. Exp. Neurol. 1993, 120:70-88.
31. Jorgensen M.B., Wright D.C., Diemer N.H. Postischemic glucose metabolism is modified in the hippocampal CA1 region depleted of excitatory input or pyramidal cells. J. Cereb. Blood Flow Metab. 1990, 10:243-251.
32. Kawanokuchi J., Mizuno T., Takeuchi H., Kato H., Wang J., Mitsuma N., Suzumura A. Production of interferon-gamma by microglia. Mult. Scler. 2006, 12:558-564.
33. Kennel S.J., Lankford T.K., Foote L.J., Shinpock S.G., Stringer C. CD44 expression on murine tissues. J. Cell Sci. 1993, 104(Pt 2):373-382.
34. Kim S.Y., Choi Y.S., Choi J.S., Cha J.H., Kim O.N., Lee S.B., Chung J.W., Chun M.H., Lee M.Y. Osteopontin in kainic acid-induced microglial reactions in the rat brain. Mol. Cells 2002, 13:429-435.
35. Kirkwood T.B. Understanding the odd science of aging. Cell 2005, 120:437-447.
36. Kumagai N., Chiba Y., Hosono M., Fujii M., Kawamura N., Keino H., Yoshikawa K., Ishii S., Saitoh Y., Satoh M., Shimada A., Hosokawa M. Involvement of pro-inflammatory cytokines and microglia in an age-associated neurodegeneration model, the SAMP10 mouse. Brain Res. 2007, 1185:75-85.
37. Lin Y.H., Huang C.J., Chao J.R., Chen S.T., Lee S.F., Yen J.J., Yang-Yen H.F. Coupling of osteopontin and its cell surface receptor CD44 to the cell survival response elicited by interleukin-3 or granulocyte-macrophage colony-stimulating factor. Mol. Cell. Biol. 2000, 20:2734-2742.
38. Lynch M.A. The multifaceted profile of activated microglia. Mol. Neurobiol. 2009, 40:139-156.
39. Maetzler, W., Berg, D., Funke, C., Sandmann, F., Stunitz, H., Maetzler, C., Nitsch, C., 2010. Progressive secondary neurodegeneration and microcalcification co-occur in osteopontin-deficient mice. Am. J. Pathol. doi:. doi:10.2353/ajpath.2010.090798.
40. Majno G., Joris I. Cells, Tissues, and Disease 2004, Oxford University Press, New York.
41. McCance K.L., Huether S.E. Pathophysiology: The Biologic Basis for Disease in Adults and Children 2002, Mosby, St. Louis.
42. Meller R., Stevens S.L., Minami M., Cameron J.A., King S., Rosenzweig H., Doyle K., Lessov N.S., Simon R.P., Stenzel-Poore M.P. Neuroprotection by osteopontin in stroke. J. Cereb. Blood Flow Metab. 2005, 25:217-225.
43. Moriguchi S., Mizoguchi Y., Tomimatsu Y., Hayashi Y., Kadowaki T., Kagamiishi Y., Katsube N., Yamamoto K., Inoue K., Watanabe S., Nabekura J., Nakanishi H. Potentiation of NMDA receptor-mediated synaptic responses by microglia. Brain Res. Mol. Brain Res. 2003, 119:160-169.
44. Munder M., Mallo M., Eichmann K., Modolell M. Murine macrophages secrete interferon gamma upon combined stimulation with interleukin (IL)-12 and IL-18: a novel pathway of autocrine macrophage activation. J. Exp. Med. 1998, 187:2103-2108.
45. Nadler J.V., Perry B.W., Gentry C., Cotman C.W. Loss and reacquisition of hippocampal synapses after selective destruction of CA3-CA4 afferents with kainic acid. Brain Res. 1980, 191:387-403.
46. Nagineni C.N., Kommineni V.K., William A., Hooks J.J., Detrick B. IL-11 expression in retinal and corneal cells is regulated by interferon-gamma. Biochem. Biophys. Res. Commun. 2010, 391:287-292.
47. Nakamura K., Okamura H., Wada M., Nagata K., Tamura T. Endotoxin-induced serum factor that stimulates gamma interferon production. Infect. Immun. 1989, 57:590-595.
48. Neumann J., Gunzer M., Gutzeit H.O., Ullrich O., Reymann K.G., Dinkel K. Microglia provide neuroprotection after ischemia. FASEB J. 2006, 20:714-716.
49. Okamura H., Tsutsi H., Komatsu T., Yutsudo M., Hakura A., Tanimoto T., Torigoe K., Okura T., Nukada Y., Hattori K., Akita K., Namba M., Tanabe F., Konishi K., Fukuda S., Kurimoto M. Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature 1995, 378:88-91.
50. Oprica M., Eriksson C., Schultzberg M. Inflammatory mechanisms associated with brain damage induced by kainic acid with special reference to the interleukin-1 system. J. Cell. Mol. Med. 2003, 7:127-140.
51. Ottonello L., Montecucco F., Bertolotto M., Arduino N., Mancini M., Corcione A., Pistoia V., Dallegri F. CCL3 (MIP-1alpha) induces in vitro migration of GM-CSF-primed human neutrophils via CCR5-dependent activation of ERK 1/2. Cell. Signal. 2005, 17:355-363.
52. Prinz M., Hanisch U.K. Murine microglial cells produce and respond to interleukin-18. J. Neurochem. 1999, 72:2215-2218.
53. Raices R.M., Kannan Y., Sarkar A., Bellamkonda-Athmaram V., Wewers M.D. A synergistic role for IL-1beta and TNFalpha in monocyte-derived IFNgamma inducing activity. Cytokine 2008, 44:234-241.
54. Ransohoff R.M., Hamilton T.A., Tani M., Stoler M.H., Shick H.E., Major J.A., Estes M.L., Thomas D.M., Tuohy V.K. Astrocyte expression of mRNA encoding cytokines IP-10 and JE/MCP-1 in experimental autoimmune encephalomyelitis. FASEB J. 1993, 7:592-600.
55. Rappert A., Bechmann I., Pivneva T., Mahlo J., Biber K., Nolte C., Kovac A.D., Gerard C., Boddeke H.W., Nitsch R., Kettenmann H. CXCR3-dependent microglial recruitment is essential for dendrite loss after brain lesion. J. Neurosci. 2004, 24:8500-8509.
56. Reddy J., Chastagner P., Fiette L., Liu X., Theze J. IL-2-induced tumor necrosis factor (TNF)-beta expression: further analysis in the IL-2 knockout model, and comparison with TNF-alpha, lymphotoxin-beta, TNFR1 and TNFR2 modulation. Int. Immunol. 2001, 13:135-147.
57. Ries A., Goldberg J.L., Grimpe B. A novel biological function for CD44 in axon growth of retinal ganglion cells identified by a bioinformatics approach. J. Neurochem. 2007, 103:1491-1505.
58. Scemes E., Giaume C. Astrocyte calcium waves: what they are and what they do. Glia 2006, 54:716-725.
59. Schroeter M., Zickler P., Denhardt D.T., Hartung H.P., Jander S. Increased thalamic neurodegeneration following ischaemic cortical stroke in osteopontin-deficient mice. Brain 2006, 129:1426-1437.
60. Seilhean D., Girolami U.D., Gray F. Basic pathology of the central nervous system. Escourolle & Poirier Mnual of Basic Neuropathology 2004, 1-20. Butterworth-Heinemann, Philadelphia. F. Gray, U.D. Girolami, J. Poirier (Eds.).
61. Shimada A. Age-dependent cerebral atrophy and cognitive dysfunction in SAMP10 mice. Neurobiol. Aging 1999, 20:125-136.
62. Shimada A., Hosokawa M., Ohta A., Akiguchi I., Takeda T. Localization of atrophy-prone areas in the aging mouse brain: comparison between the brain atrophy model SAM-P/10 and the normal control SAM-R/1. Neuroscience 1994, 59:859-869.
63. Shimada A., Keino H., Kawamura N., Chiba Y., Hosokawa M. Limbic structures are prone to age-related impairments in proteasome activity and neuronal ubiquitinated inclusions in SAMP10 mouse: a model of cerebral degeneration. Neuropathol. Appl. Neurobiol. 2008, 34:33-51.
64. Shimada A., Keino H., Satoh M., Kishikawa M., Hosokawa M. Age-related loss of synapses in the frontal cortex of SAMP10 mouse: a model of cerebral degeneration. Synapse 2003, 48:198-204.
65. Shimada A., Keino H., Satoh M., Kishikawa M., Seriu N., Hosokawa M. Age-related progressive neuronal DNA damage associated with cerebral degeneration in a mouse model of accelerated senescence. J. Gerontol. A Biol. Sci. Med. Sci. 2002, 57:B415-421.
66. Shimada A., Ohta A., Akiguchi I., Takeda T. Inbred SAM-P/10 as a mouse model of spontaneous, inherited brain atrophy. J. Neuropathol. Exp. Neurol. 1992, 51:440-450.
67. Shimada A., Ohta A., Akiguchi I., Takeda T. Age-related deterioration in conditional avoidance task in the SAM-P/10 mouse, an animal model of spontaneous brain atrophy. Brain Res. 1993, 608:266-272.
68. Shimada A., Tsuzuki M., Keino H., Satoh M., Chiba Y., Saitoh Y., Hosokawa M. Apical vulnerability to dendritic retraction in prefrontal neurones of ageing SAMP10 mouse: a model of cerebral degeneration. Neuropathol. Appl. Neurobiol. 2006, 32:1-14.
69. Sparkman N.L., Johnson R.W. Neuroinflammation associated with aging sensitizes the brain to the effects of infection or stress. Neuroimmunomodulation 2008, 15:323-330.
70. Sprott R.L., Austad S.N. Historical development of animal models of aging. Handbook of Models for Human Aging 2006, 1-8. Elsevier Academic Press. P.M. Conn (Ed.).
71. Streit W.J. Microglia and macrophages in the developing CNS. Neurotoxicology 2001, 22:619-624.
72. Takeda T., Hosokawa M., Higuchi K. Senescence-accelerated mouse (SAM): a novel murine model of accelerated senescence. J. Am. Geriatr. Soc. 1991, 39:911-919.
73. Takeda T., Hosokawa M., Takeshita S., Irino M., Higuchi K., Matsushita T., Tomita Y., Yasuhira K., Hamamoto H., Shimizu K., Ishii M., Yamamuro T. A new murine model of accelerated senescence. Mech. Ageing Dev. 1981, 17:183-194.
74. Tambuyzer B.R., Ponsaerts P., Nouwen E.J. Microglia: gatekeepers of central nervous system immunology. J. Leukoc. Biol. 2009, 85:352-370.
75. Tauck D.L., Nadler J.V. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J. Neurosci. 1985, 5:1016-1022.
76. Wang H.K., Park U.J., Kim S.Y., Lee J.H., Kim S.U., Gwag B.J., Lee Y.B. Free radical production in CA1 neurons induces MIP-1alpha expression, microglia recruitment, and delayed neuronal death after transient forebrain ischemia. J. Neurosci. 2008, 28:1721-1727.
77. Wang X., Louden C., Yue T.L., Ellison J.A., Barone F.C., Solleveld H.A., Feuerstein G.Z. Delayed expression of osteopontin after focal stroke in the rat. J. Neurosci. 1998, 18:2075-2083.
78. Wang X., Suzuki Y. Microglia produce IFN-gamma independently from T cells during acute toxoplasmosis in the brain. J. Interferon Cytokine Res. 2007, 27:599-605.
79. Wang Y., Zhou C.F. Involvement of interferon-gamma and its receptor in the activation of astrocytes in the mouse hippocampus following entorhinal deafferentation. Glia 2005, 50:56-65.
80. Weiss T.W., Samson A.L., Niego B., Daniel P.B., Medcalf R.L. Oncostatin M is a neuroprotective cytokine that inhibits excitotoxic injury in vitro and in vivo. FASEB J. 2006, 20:2369-2371.
81. Ye J.H., Zalcman S.S., Tao L. Kainate-activated currents in the ventral tegmental area of neonatal rats are modulated by interleukin-2. Brain Res. 2005, 1049:227-233.
82. Zhao W., Wang L., Zhang L., Yuan C., Kuo P.C., Gao C. Differential expression of intracellular and secreted osteopontin isoforms by murine macrophages in response to toll-like receptor agonists. J. Biol. Chem. 2010, 285:20452-20461.