Chemically induced neuronal damage and gliosis: Enhanced expression of the proinflammatory chemokine, monocyte chemoattractant protein (MCP)-1, without a corresponding increase in proinflammatory cytokines

Neuroscience

Volumn 115, Issue 1, 2002, Pages 307-320

  Little, A R ^a   Benkovic, S A ^a   Miller, D B ^a   O'Callaghan, J P ^a  

^a NATIONAL INSTITUTE FOR OCCUPATIONAL SAFETY AND HEALTH   (United States)

Author keywords

Glial fibrillary acidic protein; Gliosis; Inflammation; Interleukin 1 ; Monocyte chemoattractant protein 1; Tumor necrosis factor

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; TRIMETHYLTIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BLOOD BRAIN BARRIER; BRAIN NERVE CELL; CONTROLLED STUDY; GLIOSIS; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; INFLAMMATION; LIVER; MALE; NERVE CELL LESION; NEUROPATHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; RAT;

ANIMALS; CELL DEATH; CHEMOKINE CCL2; CHEMOKINES; CYTOKINES; GLIOSIS; HIPPOCAMPUS; INFLAMMATION; MALE; NEURONS; RATS; RATS, LONG-EVANS; RNA, MESSENGER; TRIMETHYLTIN COMPOUNDS;

EID: 0037110606     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(02)00359-7     Document Type: Article

References (75)

1. Balaban C.D., O'Callaghan J.P., Billingsley M.L. Trimethyltin-induced neuronal damage in the rat brain: comparative studies using silver degeneration stains, immunocytochemistry and immunoassay for neuronotypic and gliotypic proteins. Neuroscience. 26:1988;337-361.
2. Balasingam V., Tejada-Berges T., Wright E., Bouckova R., Yong V.W. Reactive astrogliosis in the neonatal mouse brain and its modulation by cytokines. J. Neurosci. 14:1994;846-856.
3. Berman J.W., Guida M.P., Warren J., Amat J., Brosnan C.F. Localization of monocyte chemoattractant peptide-1 expression in the central nervous system in experimental autoimmune encephalomyelitis and trauma in the rat. J. Immunol. 156:1996;3017-3023.
4. Brock T.O., O'Callaghan J.P. Quantitative changes in the synaptic vesicle proteins synapsin I and p38 and the astrocyte-specific protein glial fibrillary acidic protein are associated with chemical-induced injury to the rat central nervous system. J. Neurosci. 7:1987;931-942.
5. Buttini M., Limonta S., Boddeke H.W. Peripheral administration of lipopolysaccharide induces activation of microglial cells in rat brain. Neurochem. Int. 29:1996;25-35.
6. Buttini M., Mir A., Appel K., Wiederhold K.H., Limonta S., Gebicke-Haerter P.J., Boddeke H.W. Lipopolysaccharide induces expression of tumour necrosis factor alpha in rat brain: inhibition by methylprednisolone and by rolipram. Br. J. Pharmacol. 122:1997;1483-1489.
7. de Olmos J.S., Beltramino C.A., de Olmos de Lorenzo S. Use of an amino-cupric-silver technique for the detection of early and semiacute neuronal degeneration caused by neurotoxicants, hypoxia, and physical trauma. Neurotoxicol. Teratol. 16:1994;545-561.
8. Dickson D.W., Lee S.C., Mattiace L.A., Yen S.H., Brosnan C. Microglia and cytokines in neurological disease, with special reference to AIDS and Alzheimer's disease. Glia. 7:1993;75-83.
9. Eng L.F., Ghirnikar R.S., Lee Y.L. Inflammation in EAE: role of chemokine/cytokine expression by resident and infiltrating cells. Neurochem. Res. 21:1996;511-525.
10. Feuerstein G.Z., Wang X., Barone F.C. Inflammatory gene expression in cerebral ischemia and trauma. Potential new therapeutic targets. Ann. N.Y. Acad. Sci. 825:1997;179-193.
11. Foss D.L., Baarsch M.J., Murtaugh M.P. Regulation of hypoxanthine phosphoribosyltransferase, glyceraldehyde-3-phosphate dehydrogenase and beta-actin mRNA expression in porcine immune cells and tissues. Animal Biotechnol. 9:1998;67-78.
12. Galasso J.M., Miller M.J., Cowell R.M., Harrison J.K., Warren J.S., Silverstein F.S. Acute excitotoxic injury induces expression of monocyte chemoattractant protein-1 and its receptor, CCR2, in neonatal rat brain. Exp. Neurol. 165:2000;295-305.
13. Garlind A., Brauner A., Hojeberg B., Basun H., Schultzberg M. Soluble interleukin-1 receptor type II levels are elevated in cerebrospinal fluid in Alzheimer's disease patients. Brain Res. 826:1999;112-116.
14. Ghirnikar R.S., Lee Y.L., Li J.D., Eng L.F. Chemokine inhibition in rat stab wound brain injury using antisense oligodeoxynucleotides. Neurosci. Lett. 247:1998;21-24.
15. Giulian D., Li J., Leara B., Keenen C. Phagocytic microglia release cytokines and cytotoxins that regulate the survival of astrocytes and neurons in culture. Neurochem. Int. 25:1994;227-233.
16. Giulian D., Vaca K., Corpuz M. Brain glia release factors with opposing actions upon neuronal survival. J. Neurosci. 13:1993;29-37.
17. Giulian D., Woodward J., Young D.G., Krebs J.F., Lachman L.B. Interleukin-1 injected into mammalian brain stimulates astrogliosis and neovascularization. J. Neurosci. 8:1988;2485-2490.
18. Glabinski A.R., Balasingam V., Tani M., Kunkel S.L., Strieter R.M., Yong V.W., Ransohoff R.M. Chemokine monocyte chemoattractant protein-1 is expressed by astrocytes after mechanical injury to the brain. J. Immunol. 156:1996;4363-4368.
19. Glabinski A.R., Krakowski M., Han Y., Owens T., Ransohoff R.M. Chemokine expression in GKO mice (lacking interferon-gamma) with experimental autoimmune encephalomyelitis. J. Neurovirol. 5:1999;95-101.
20. Glabinski A.R., Ransohoff R.M. Chemokines and chemokine receptors in CNS pathology. J. Neurovirol. 5:1999;3-12.
21. Glabinski A.R., Tani M., Strieter R.M., Tuohy V.K., Ransohoff R.M. Synchronous synthesis of alpha- and beta-chemokines by cells of diverse lineage in the central nervous system of mice with relapses of chronic experimental autoimmune encephalomyelitis. Am. J. Pathol. 150:1997;617-630.
22. Goujon E., Parnet P., Laye S., Combe C., Dantzer R. Adrenalectomy enhances pro-inflammatory cytokines gene expression, in the spleen, pituitary and brain of mice in response to lipopolysaccharide. Mol. Brain Res. 36:1996;53-62.
23. Gourmala N.G., Buttini M., Limonta S., Sauter A., Boddeke H.W. Differential and time-dependent expression of monocyte chemoattractant protein-1 mRNA by astrocytes and macrophages in rat brain: effects of ischemia and peripheral lipopolysaccharide administration. J. Neuroimmunol. 74:1997;35-44.
24. Hanisch U.K., Quirion R. Interleukin-2 as a neuroregulatory cytokine. Brain Res. Rev. 21:1995;246-284.
25. Hausmann E.H., Berman N.E., Wang Y.Y., Meara J.B., Wood G.W., Klein R.M. Selective chemokine mRNA expression following brain injury. Brain Res. 788:1998;49-59.
26. Hauss-Wegrzyniak B., Dobrzanski P., Stoehr J.D., Wenk G.L. Chronic neuroinflammation in rats reproduces components of the neurobiology of Alzheimer's disease. Brain Res. 780:1998;294-303.
27. Himi T., Yoshioka I., Kataura A. Production and gene expression of IL-8-like cytokine GRO/CINC-1 in rat nasal mucosa. Acta Otolaryngol. 117:1997;123-127.
28. Jankowsky J.L., Patterson P.H. The role of cytokines and growth factors in seizures and their sequelae. Prog. Neurobiol. 63:2001;125-149.
29. Kim J.S., Gautam S.C., Chopp M., Zaloga C., Jones M.L., Ward P.A., Welch K.M. Expression of monocyte chemoattractant protein-1 and macrophage inflammatory protein-1 after focal cerebral ischemia in the rat. J. Neuroimmunol. 56:1995;127-134.
30. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19:1996;312-318.
31. Lemke R., Hartlage-Rubsamen M., Schliebs R. Differential injury-dependent glial expression of interleukins-1 alpha, beta, and interleukin-6 in rat brain. Glia. 27:1999;75-87.
32. Li H., Shi F.D., Bai X., Huang Y., Diab A., He B., Link H. Cytokine and chemokine mRNA expressing cells in muscle tissues of experimental autoimmune myasthenia gravis. J. Neurol. Sci. 161:1998;40-46.
33. Licastro F., Pedrini S., Caputo L., Annoni G., Davis L.J., Ferri C., Casadei V., Grimaldi L.M. Increased plasma levels of interleukin-1, interleukin-6 and alpha-1-antichymotrypsin in patients with Alzheimer's disease: peripheral inflammation or signals from the brain? J. Neuroimmunol. 103:2000;97-102.
34. Little, A.R., Jr., O'Callaghan, J.P., 2002. The astrocyte response to neural injury: A review and reconsideration of key features. In: Lester, D.S., Slikker, W. (Eds.), Site-Specific Neurotoxicity. Taylor and Francis, London, pp. 233-265.
35. Little A.R., O'Callaghan J.P. Astrogliosis in the adult and developing CNS: Is there a role for proinflammatory cytokines? Neurotoxicology. 22:2001;607-618.
36. Loddick S.A., Turnbull A.V., Rothwell N.J. Cerebral interleukin-6 is neuroprotective during permanent focal cerebral ischemia in the rat. J. Cereb. Blood Flow Metabol. 18:1998;176-179.
37. Loscher C.E., Donnelly S., Lynch M.A., Mills K.H. Induction of inflammatory cytokines in the brain following respiratory infection with Bordetella pertussis. J. Neuroimmunol. 102:2001;172-181.
38. Lubec G., Labudova O., Cairns N., Fountoulakis M. Increased glyceraldehyde 3-phosphate dehydrogenase levels in the brain of patients with Down's syndrome. Neurosci. Lett. 260:1999;141-145.
39. Maier W.E., Brown H.W., Tilson H.A., Luster M.I., Harry G.J. Trimethyltin increases interleukin (IL)-1 alpha, IL-6 and tumor necrosis factor alpha mRNA levels in rat hippocampus. J. Neuroimmunol. 59:1995;65-75.
40. Mattson M.P., Barger S.W., Furukawa K., Bruce A.J., Wyss-Coray T., Mark R.J., Mucke L. Cellular signaling roles of TGF beta, TNF alpha and beta APP in brain injury responses and Alzheimer's disease. Brain Res. Rev. 23:1997;47-61.
41. McCann M.J., O'Callaghan J.P., Martin P.M., Bertram T., Streit W.J. Differential activation of microglia and astrocytes following trimethyl tin-induced neurodegeneration. Neuroscience. 72:1996;273-281.
42. McGeer P.L., McGeer E.G. The inflammatory response system of brain: implications for therapy of Alzheimer and other neurodegenerative diseases. Brain Res. Rev. 21:1995;195-218.
43. McGeer P.L., Rogers J., McGeer E.G. Neuroimmune mechanisms in Alzheimer disease pathogenesis. Alzheimer Dis. Assoc. Disord. 8:1994;149-158.
44. McManus C., Berman J.W., Brett F.M., Staunton H., Farrell M., Brosnan C.F. MCP-1, MCP-2 and MCP-3 expression in multiple sclerosis lesions: an immunohistochemical and in situ hybridization study. J. Neuroimmunol. 86:1998;20-29.
45. McTigue D.M., Tani M., Krivacic K., Chernosky A., Kelner G.S., Maciejewski D., Maki R., Ransohoff R.M., Stokes B.T. Selective chemokine mRNA accumulation in the rat spinal cord after contusion injury. J. Neurosci. Res. 53:1998;368-376.
46. Merrill J.E., Benveniste E.N. Cytokines in inflammatory brain lesions: helpful and harmful. Trends Neurosci. 19:1996;331-338.
47. Muessel M., Klein R.M., Berman N.E. Expression and localization of monocyte chemoattractant protein-1 during retrograde degeneration. Soc. Neurosci. Abstr. 25:1999;1275.
48. Muessel M.J., Berman N.E., Klein R.M. Early and specific expression of monocyte chemoattractant protein-1 in the thalamus induced by cortical injury. Brain Res. 870:2000;211-221.
49. Nagatsu T., Mogi M., Ichinose H., Togari A. Cytokines in Parkinson's disease. J. Neural Trans. Suppl. 58:(Suppl.):2000;143-151.
50. Norton W.T., Brosnan C.F., Cammer W., Goldmuntz E.A. Mechanisms and suppression of inflammatory demyelination. Acta Neurobiol. Exp. 50:1990;225-235.
51. O'Callaghan J.P. Quantification of glial fibrillary acidic protein: comparison of slot-immunobinding assays with a novel sandwich ELISA. Neurotoxicol. Teratol. 13:1991;275-281.
52. O'Callaghan, J.P., 2001. Measurement of glial fibrillary acidic protein. In: Costa, L.G. (Ed.), Current Protocols in Toxicology. John Wiley and Sons, New York, in press.
53. O'Callaghan J.P., Jensen K.F., Miller D.B. Quantitative aspects of drug and toxicant-induced astrogliosis. Neurochem. Int. 26:1995;115-124.
54. Panenka W., Jijon H., Herx L.M., Armstrong J.N., Feighan D., Wei T., Yong V.W., Ransohoff R.M., MacVicar B.A. P2X7-like receptor activation in astrocytes increases chemokine monocyte chemoattractant protein-1 expression via mitogen-activated protein kinase. J. Neurosci. 21:2001;7135-7142.
55. Perry V.H., Andersson P.B. The inflammatory response in the CNS. Neuropathol. Appl. Neurobiol. 18:1992;454-459.
56. Plata-Salaman C.R., Ilyin S.E., Turrin N.P., Gayle D., Flynn M.C., Romanovitch A.E., Kelly M.E., Bureau Y., Anisman H., McIntyre D.C. Kindling modulates the IL-1beta system, TNF-alpha, TGF-beta1, and neuropeptide mRNAs in specific brain regions. Mol. Brain Res. 75:2000;248-258.
57. Raivich G., Bohatschek M., Kloss C.U., Werner A., Jones L.L., Kreutzberg G.W. Neuroglial activation repertoire in the injured brain: Graded response, molecular mechanisms and cues to physiological function. Brain Res. Rev. 30:1999;77-105.
58. Ransohoff R.M., Glabinski A., Tani M. Chemokines in immune-mediated inflammation of the central nervous system. Cytokine Growth Factor Rev. 7:1996;35-46.
59. 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. 7:1993;592-600.
60. Ridet J.L., Malhotra S.K., Privat A., Gage F.H. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci. 20:1997;570-577.
61. Rostworowski M., Balasingam V., Chabot S., Owens T., Yong V.W. Astrogliosis in the neonatal and adult murine brain post-trauma: elevation of inflammatory cytokines and the lack of requirement for endogenous interferon-gamma. J. Neurosci. 17:1997;3664-3674.
62. Rothwell N.J., Loddick S.A., Stroemer P. Interleukins and cerebral ischaemia. Int. Rev. Neurobiol. 40:1997;281-298.
63. Rothwell N.J., Luheshi G.N. Interleukin 1 in the brain: biology, pathology and therapeutic target. Trends Neurosci. 23:2000;618-625.
64. Schoneboom B.A., Catlin K.M., Marty A.M., Grieder F.B. Inflammation is a component of neurodegeneration in response to Venezuelan equine encephalitis virus infection in mice. J. Neuroimmunol. 109:2000;132-146.
65. Schwaiger F.-W., Flugel A., Hager G., Horvat A., Spitzer C., Graeber M.B., Kreutzberg G.W. Neuronal expression of MCP-1 following a remote lesion of the CNS. Soc. Neurosci. Abstr. 25:1999;1275.
66. Sharafeldin A., Eltayeb R., Pashenkov M., Bakhiet M. Chemokines are produced in the brain early during the course of experimental African trypanosomiasis. J. Neuroimmunol. 103:2000;165-170.
67. Simpson J.E., Newcombe J., Cuzner M.L., Woodroofe M.N. Expression of monocyte chemoattractant protein-1 and other beta-chemokines by resident glia and inflammatory cells in multiple sclerosis lesions. J. Neuroimmunol. 84:1998;238-249.
68. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., Fujimoto E.K., Goeke N.M., Olson B.J., Klenk D.C. Measurement of protein using bicinchononic acid. Anal. Biochem. 150:1985;76-85.
69. Streit W.J., Semple-Rowland S.L., Hurley S.D., Miller R.C., Popovich P.G., Stokes B.T. Cytokine mRNA profiles in contused spinal cord and axotomized facial nucleus suggest a beneficial role for inflammation and gliosis. Exp. Neurol. 152:1998;74-87.
70. Streit W.J., Walter S.A., Pennell N.A. Reactive microgliosis. Prog. Neurobiol. 57:1999;563-581.
71. Sullivan P.G., Bruce-Keller A.J., Rabchevsky A.G., Christakos S., Clair D.K., Mattson M.P., Scheff S.W. Exacerbation of damage and altered NF-kappaB activation in mice lacking tumor necrosis factor receptors after traumatic brain injury. J. Neurosci. 19:1999;6248-6256.
72. Turnbull A.V., Pitossi F.J., Lebrun J.J., Lee S., Meltzer J.C., Nance D.M., del Rey A., Besedovsky H.O., Rivier C. Inhibition of tumor necrosis factor-alpha action within the CNS markedly reduces the plasma adrenocorticotropin response to peripheral local inflammation in rats. J. Neurosci. 17:1997;3262-3273.
73. Van Coillie E., Van Damme J., Opdenakker G. The MCP/eotaxin subfamily of CC chemokines. Cytokine Growth Factor Rev. 10:1999;61-86.
74. Vogt, B.A., 1968. Vogt's method for nerve cell products. In: Luna, L.G. (Ed.), Manual of Histologic Staining Methods of the Armed Forces Institute of Pathology, 3rd edn. McGraw-Hill, New York, p. 206.
75. Yu A.C., Lau L.T. Expression of interleukin-1 alpha, tumor necrosis factor alpha and interleukin-6 genes in astrocytes under ischemic injury. Neurochem. Int. 36:2000;369-377.