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Alternation of interleukin-1α production and interleukin-1α binding sites in mouse brain during rabies infection

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Summary

We have evaluated the effect of rabies virus infection on interleukin-1α(IL-1α) production and its receptors in mouse brain. Study of virus dissemination in the central nervous system (CNS) showed a massive infection of main brain structures from day 4 post infection (p.i.) up to the agony stage on day 6 p.i. At the same time, IL-1α concentrations increased in cortical and hippocampal homogenates, whereas no change was detected in serum. In non-infected mice, IL-1α binding sites were observed in the dentate gyrus, the cortex, the choroid plexus, the meninges and the anterior pituitary. During rabies virus infection, a striking decrease in IL-1α binding sites was observed on day 4 p.i. with a complete disappearance on day 6 p.i., except in the pituitary gland where they remained at control level. In conclusion, concomitantly with the early rabid pathological signs, brain IL-1α production and IL-1α binding sites are specifically and significantly altered by brain viral proliferation. These results indicate that IL-1α could be involved in the brain response to viral infection as a mediator and could participate in the genesis of the rabies pathogeny.

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References

  1. Smith JS, McClelland CL, Reid FL, Baer GM (1982) Dual role of the immune response in street rabies infection of mice. Infect Immun 35: 213–221

    PubMed  Google Scholar 

  2. Johnson RT (1965) Experimental rabies. J Neuropathol Exp Neurol 24: 662–674

    PubMed  Google Scholar 

  3. Matsumoto S (1975) Electron microscopy of central nervous system. In: Baer GM (ed) The natural history of rabies. Academic Press, New York, pp 217–235

    Google Scholar 

  4. Tsiang H (1982) Neuronal impairment in rabies-infected rat brain. J Gen Virol 61: 277–281

    PubMed  Google Scholar 

  5. Tsiang H (1993) Pathophysiology of rabies virus infection of the nervous system. In: Maramorosch K, Murphy FA, Shatkin AJ (eds) Advance in virus research, vol 42. Academic Press, New York, pp 375–412

    Google Scholar 

  6. Charlton KM (1988) The pathogenesis of rabies. In: Campbell JB, Charlton KM (eds) Rabies. Kluwer, Boston, pp 101–150

    Google Scholar 

  7. Torres-Anjel MJ, Volz D, Torres MJR, Turk M, Tshikuka JG (1988) Failure to thrive, wasting syndrome, and immunodeficiency in rabies: a hypophyseal/hypothalamic/thymic axis effect of rabies virus. Rev Infect Dis 10: S710–725

    PubMed  Google Scholar 

  8. Hirai K, Kawano H, Mifune K, Fuji H, Nishizono A, Shichijo A, Mannen K (1992) Suppression of cell-mediated immunity by street rabies virus infection. Microbiol Immun 36: 1277–1290

    Google Scholar 

  9. Marcovistz R, Galabru J, Tsiang H, Hovanessian AG (1986) Neutralization of interferon produced early during rabies virus infection in mice. J Gen Virol 67: 387–390

    PubMed  Google Scholar 

  10. Plata-Salaman CR (1991) Immunoregulators in the nervous system. Neurosci Behav Rev 15: 185–215

    Google Scholar 

  11. Rothwell NJ, Hopkins SJ (1995) Cytokines and the nervous system II: actions and mechanisms of action. Trends Neurosci 18: 130–136

    PubMed  Google Scholar 

  12. Schöbitz B, de Kloet RE, Holsboer F (1994) Gene expression and function of interleukin 1, interleukin 6 and tumor necrosis factor in the brain. Prog Neurobiol 144: 397–432

    Google Scholar 

  13. Berkenbosch F, Van Oers J, Del Rey A, Tilders F, Besedovsky H (1987) Corticotropin-releasing factor-producing neurons in the rat activated by interleukin-1. Science 238: 524–526

    PubMed  Google Scholar 

  14. Salposky R, River C, Yamamoto G, Plotsky P, Vale W (1987) Interleukin-1 stimulates the secretion of hypothalamic corticotropin-releasing-factor. Science 238: 522–524

    PubMed  Google Scholar 

  15. Suda T, Tozawa F, Ushiyama, Sumitomo T, Yamada M, Demura H (1990) Interleukin-1 stimulates corticotropin-releasing factor gene expression in rat hypothalamus. Endocrinology 126: 1223–1228

    PubMed  Google Scholar 

  16. Naito Y, Fukata J, Tominaga T, Masui Y, Hirai Y, Murakami N, Tamai S, Mori K, Imura H (1989) Adrenocorticotropic hormone-releasing activities of interleukins in a homologous in vivo system. Biochem Biophys Res Commun 164: 1262–1267

    PubMed  Google Scholar 

  17. Fukuta J, Usiu T, Naitoh Y, Nakai Y, Imura H (1989) Effects of recombinant human interleukin-1α,1β,2 and 6 on ACTH synthesis and release in the mouse pituitary tumor cell line AtT-20. J Endocrinol 122: 33–39

    PubMed  Google Scholar 

  18. Besedovsky H, Del Rey A, Sorkin E, Dinarello CA (1986) Immunoregulatory feedback between interleukin-1 and glucocorticoid hormones. Science 233: 652–654

    PubMed  Google Scholar 

  19. Lee SW, Tsou AP, Chan H, Thomas J, Petrie K, Eugui EM, Allison AC (1988) Glucocorticoids selectively inhibit the transcription of interleukin-1 beta gene and decrease the stability of interleukin-1 beta mRNA. Proc Natl Acad Sci USA 85: 1204–1208

    PubMed  Google Scholar 

  20. Rivier C, Vale W, Brown M (1989) In the rat interleukin-1 α and β stimulate ACTH and catecholamine release. Endocrinology 125: 3096–3102

    PubMed  Google Scholar 

  21. Baybutt HN, Holsboer F (1990) Inhibition of macrophage differentiation and function by cortisol. Endocrinology 127: 476–480

    PubMed  Google Scholar 

  22. Jain R, Zwicker D, Hollander CS, Brand H, Saperstein A, Hutchinson B, Brown C, Audhya T (1991) Corticotropin-releasing factor modulates the immune response to stress in the rat. Endocrinology 128: 1329–1336

    PubMed  Google Scholar 

  23. Haour F, Ban E, Milon G, Baran D, Fillion G (1990) Brain interleukin 1 receptors: characterization and modulation after lipopolysaccharide injection. Prog NeuroEndocrinImmunol 3: 196–204

    Google Scholar 

  24. Ban E, Milon G, Prudhomme N, Fillion G, Haour F (1991) Receptors for interleukin-1 (α and β) in mouse brain: mapping and neuronal localization in hippocampus. Neuroscience 43: 21–30

    PubMed  Google Scholar 

  25. Takao T, Tracey DE, Mitchell WM, De Souza EB (1991) Interleukin 1 receptors in mouse brain: characterization and neuronal localization. Endocrinology 127: 3070–3078

    Google Scholar 

  26. Kaplan MM, Koprowski H (1973) In: Kaplan MM, Koprowski H (eds) Laboratory techniques in rabies. WHO Monograph series no. 23. WHO, Geneva, pp 85–93

    Google Scholar 

  27. Lehmann A (1974) Atlas stereotaxique du cerveau de la souris. Le Centre National de la Recherche Scientifique, Paris

    Google Scholar 

  28. Atanasiu P, Perrin P, Favre S, Chevalier G, Tsiang H (1974) Immunofluorescence and immunoperoxydase in the diagnosis of rabies. In: Kurstak E, Morrisset R (eds) Viral immunodiagnosis. Academic Press, London, pp 141–155

    Google Scholar 

  29. Johnson RT (1971) The pathogenesis of experimental rabies. In: Nagano Y, Davenport FM (eds) Rabies. University of Tokyo Press, Tokyo, pp 59–75

    Google Scholar 

  30. Quan N, Sundar SK, Weiss JM (1994) Induction of interleukin-1 in various brain regions after peripheral and central injections of lipopolysaccharide. J Neuroimmunol 49: 125–134

    PubMed  Google Scholar 

  31. Takao T, Culp SC, De Souza EB (1993) Reciprocal modulation of interleukin-1β(IL-1β) and IL-1 receptors by lipopolysaccharide (endotoxin) treatment in the mouse brain-endocrine-immune axis. Endocrinology 132: 1497–1504

    PubMed  Google Scholar 

  32. Ban E, Haour F, Lenstra R (1992) Brain interleukin-1 gene expression induced by peripheral lipopolysaccharide administration. Cytokine 4: 48–54

    PubMed  Google Scholar 

  33. Gabellec M-M, Griffais R, Fillion G, Haour F (1995) Expression of interleukin-1α, interleukin-1β and interleukin-1 ra mRNA in mouse brain: regulation by bacterial lipopolysaccharide (LPS) treatment. Mol Brain Res 31: 122–130

    PubMed  Google Scholar 

  34. Bouzamondo E, Ladogana A, Tsiang H (1993) Alteration of potassium-evoked 5-hydroxytryptamine release from virus-infected rat cortical synaptosomes. Neuroreport 4: 555–558

    PubMed  Google Scholar 

  35. Ladogana A, Bouzamondo E, Pocchiari M, Tsiang H (1994) Modification of tritiated γ-amino-n-butyric acid transport in rabies virus-infected primary cortical cultures. J Gen Virol 75: 623–627

    PubMed  Google Scholar 

  36. Koschel K, Halbach M (1979) Rabies virus infection selectively impairs membrane receptor functions in neuronal model cells. J Gen Virol 42: 627–632

    PubMed  Google Scholar 

  37. Koschel K, Münzel M (1984) Inhibition of opiate receptor-mediated signal transmission by rabies virus in persistently infected NG-108-15 mouse neuroblastoma-rat glioma hybrid cells. Proc Natl Acad Sci USA 81: 950–954

    PubMed  Google Scholar 

  38. Münzel P, Koschel K (1981) Rabies virus decreases agonist binding to opiate receptors of mouse neuroblastoma-rat glioma hybrid cells 108-cc-15. Biochem Biophys Res Commun 101: 1241–1250

    PubMed  Google Scholar 

  39. Ceccaldi P-E, Fillion M-P, Ermine A, Tsiang H, Fillion G (1993) Rabies virus selectively alters 5-HT1 receptors subtypes in rat brain. Eur J Pharmacol 245: 129–138

    PubMed  Google Scholar 

  40. Gourmelon P, Briet D, Court L, Tsiang H (1986) Electrophysiological and sleep alterations in experimental rabies. Brain Res 398: 128–140

    PubMed  Google Scholar 

  41. Gourmelon P, Briet D, Clarençon D, Court L, Tsiang H (1991) Sleep alterations in experimental street rabies virus infection occur in the absence of major EEG abnormalities. Brain Res 554: 159–165

    PubMed  Google Scholar 

  42. Katsuki H, Nakai S, Hirai Y, Akaji K, Kiso Y, Satoh M (1990) Interleukin-1β inhibits long-term potentiation in the CA3 region of mouse hippocampal slices. Eur J Pharmacol 811: 323–326

    Google Scholar 

  43. Zeise ML, Madamba S, Siggins GR (1992) Interleukin-1β increases synaptic inhibition in rat hippocampal pyramidal neurons in vitro. Regul Pept 39: 1–7

    PubMed  Google Scholar 

  44. Plata-Salaman CR, Ffrench-Mullen JMH (1992) Interleukin-1β depresses calcium currents in CA1 hippocampal neurons pathophysiological concentrations. Brain Res Bull 29: 221–223

    PubMed  Google Scholar 

  45. Rada P, Mark GP, Vitek MP, Mangano RM, Blume AJ, Beer B, Hoebel BG (1991) Interleukin-1β decreases acetylcholine measured by microdialysis in the hippocampus of freely moving rats. Brain Res 550: 287–290

    PubMed  Google Scholar 

  46. Lapchack PA, Araujo DM, Hefti F (1993) Systemic interleukin-1β decreases brain-derived neurotrophic factor messenger RNA expression in the rat hippocampal formation. Neuroscience 53: 297–301

    PubMed  Google Scholar 

  47. Linthorst ACE, Flachskamm C, Holsboer F, Reul JMHM (1994) Local administration of recombinant human interleukin-1β in the rat hippocampus increases serotoninergic neurotransmission, hypothalamic-pituitary-adrenocortical axis activity, and body temperature. Endocrinology 135: 520–532

    PubMed  Google Scholar 

  48. Sundar SK, Becker KJ, Cierpial MA, Carpenter MD, Rankin LA, Fleener SL, Ritchie JC, Simson PE, Weiss JM (1989) Interacerebroventricular infusion of interleukin 1 rapidly decreases peripheral cellular immune response. Proc Natl Acad Sci USA 86: 6398–6402

    PubMed  Google Scholar 

  49. Sundar SK, Cierpal MA, Kamaraju LS, Long S, Hsieh S-I, Lorenz C, Aaron M, Ritchie JC, Weiss JM (1991) Human immunodeficiency virus glycoprotein (gp 120) infused into rat brain induces interleukin 1 to elevate pituitary-adrenal activity and decrease peripheral cellular responses. Proc Natl Acad Sci USA 88: 11246–11250

    PubMed  Google Scholar 

  50. Brown R, Li Z, Vriend CY, Nirula R, Janz L, Falk J, Nance DM, Dyck DG, Greenberg AH (1991) Suppression of splenic macrophage interleukin-1 secretion following intracerebroventricular injection of interleukin-1β: evidence for pituitary-adrenal and sympathetic control. Cell Immunol 132: 84–93

    PubMed  Google Scholar 

  51. Sundar SK, Cierpal MA, Kilts C, Ritchie JC, Weiss JM (1990) Brain IL-1-induced immunosuppression occurs though activation of both pituitary-adrenal axis and sympathetic nervous system by corticotropin-releasing factor. J Neurosci 10: 3701–3706

    PubMed  Google Scholar 

  52. Saperstein A, Brand H, Audhya T, Nabriski D, Hutchinson B, Rosenzweig S, Hollander CS (1992) Interleukin 1β mediates stress-induced immunosuppression via corticotropin-releasing-factor. Endocrinology 130: 152–158

    PubMed  Google Scholar 

  53. Wiktor TJ, Doherty PC, Koprowski H (1977) Suppression of cell-mediated immunity by street rabies virus. J Exp Med 145: 1617–1622

    PubMed  Google Scholar 

  54. Tsiang H, Lagrange PH (1980) In vivo detection of specific cell-mediated immunity in street rabies virus infection in mice. J Gen Virol 47: 183–191

    PubMed  Google Scholar 

  55. Wiktor TJ, McFarlan RI, Koprowski H (1985) Rabies virus pathogenicity. In: Kuwert E, Merieux C, Koprowski H, Bogel K (eds) Rabies in the tropics. Curr Top Microbiol Immunol 5: 21–29

    Google Scholar 

  56. Schneider-Schaulies J, Schneider-Schaulies S, Ter Meulen V (1993) Differential induction of cytokines by primary and persistent measles virus infection in human glial cells. Virology 195: 219–228

    PubMed  Google Scholar 

  57. Stanley LC, Mrak RE, Woody RC, Perrot LJ, Zhang S, Marshak DR, Nelson SJ, Griffin WS (1994) Glial cytokines as neuropathogenic factors in HIV infection: pathogenic similarities to Alzheimer's disease. J Neuropathol Exp Neurol 53: 231–238

    PubMed  Google Scholar 

  58. Merrill JE, Chen ISY (1991) HIV-1, macrophages, glial cells, and cytokines in AIDS nervous system disease. FASEB J 5: 2391–2397

    PubMed  Google Scholar 

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Marquette, C., Ceccaldi, P.E., Ban, E. et al. Alternation of interleukin-1α production and interleukin-1α binding sites in mouse brain during rabies infection. Archives of Virology 141, 573–585 (1996). https://doi.org/10.1007/BF01718318

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  • DOI: https://doi.org/10.1007/BF01718318

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