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The Course of Experimental Allergic Encephalomyelitis in Adult Rats after Administration of Interleukin-1β at Different Periods in Early Life

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Multiple sclerosis (MS) is a chronic disease of the CNS affecting people of working age, in which myelin and the cells producing it, and also neurons, become the targets for aggressive immune cells. It has been suggested that common childhood infections in later childhood increase the risk of developing MS. We report here studies of the course of experimental allergic encephalomyelitis (EAE) in rats given interleukin-1β (IL-1β) at different stages of early postnatal ontogeny. EAE was induced in rats at age three months by single subcutaneous immunizations with homologous spinal cord homogenate in complete Freund’s adjuvant. The number of sick animals was recorded daily, as were the severity and duration of disease. EAE was found to have a more severe course after administration of IL-1β in weeks 1 and 4 of life than in rats of the corresponding control groups. The harmful or protective consequences of IL-1β administration at different periods of early postnatal ontogeny are discussed, as are the role of stress reactivity and its link with the “hygiene hypothesis.”

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References

  1. I. N. Abdurasulova, Yu. L. Zhitnukhin, E. A. Tarasolva, and V. M. Klimenko, “Expression of cytokine mRNAs in the spleen and spinal cord of rats with EAE of different severities,” Med. Immunol., 6, No. 1–2, 37–46 (2004).

    Google Scholar 

  2. I. N. Abdurasulova, S. E. Serdyuk, and V. E. Gmiro, “A comparative study of the prophylactic and therapeutic action of IEM-1966 and memantine in rats with experimental allergic encephalomyelitis,” Byull. Eksperim. Biol. Med., 144, No. 8, 184–187 (2007).

    Google Scholar 

  3. O. E. Zubareva, A. P. Eliseeva, A. S. Simbirtsev, and V. M. Klimenko, “Effects of proinflammatory cytokines on the establishment of behavior in early postnatal ontogeny,” Ros. Fiziol. Zh., 91, No. 4, 374–384 (2005).

    CAS  Google Scholar 

  4. V. I. Makhin’ko and V. N. Nikitin, “Growth constants and functional periods of development in the postnatal life of white rats,” in: Molecular and Physiological Mechanisms of Age-Related Development, Naukova Dumka, Kiev (1975).

  5. M. Alter and W. Cendrowski, “Multiple sclerosis and childhood infections,” Neurology, 26, No. 3, 201–214 (1976).

    Article  CAS  PubMed  Google Scholar 

  6. S. M. Anderton and R. S. Liblau, “Regulatory T cells in the control of inflammatory demyelinating diseases of the central nervous system,” Curr. Opin. Neurol., 21, No. 3, 248–254 (2008).

    Article  CAS  PubMed  Google Scholar 

  7. D. C. Anthony, S. J. Bolton, S. Fearn, and V. H. Perry, “Age-related effects of interleukin-1 beta on polymorphonuclear neutrophil-dependent increases in blood-brain barrier permeability in rats,” Brain, 120, 435–444 (1997).

    Article  PubMed  Google Scholar 

  8. A. T. Argaw, Y. Zhang, B. J. Snyder, et al., “IL-1β regulates bloodbrain barrier permeability via reactivation of the hypoxia-angiogenesis program,” J. Immunol., 177, 5574–5584 (2006).

    Article  CAS  PubMed  Google Scholar 

  9. A. Ascherio and K. L. Munger, “Environmental risk factors for multiple sclerosis. Part I: The role of infection,” Ann. Neurol., 61, No. 4, 288–299 (2007).

    Article  PubMed  Google Scholar 

  10. S. Bachmann and J. Kesselring, “Multiple sclerosis and infectious childhood diseases,” Neuroepidemiology, 17, No. 3, 154–160 (1998).

    Article  CAS  PubMed  Google Scholar 

  11. V. Badovinac, M. Mostarica-Stojkovic, C. A. Dinarello, and S. Stosic-Grujicic, “Interleukin-1 receptor antagonist suppresses experimental autoimmune encephalomyelitis (EAE) in rats by influencing the activation and proliferation of encephalitogenic cells,” J. Neuroimmunol., 85, No. 1, 87–95 (1998).

    Article  CAS  PubMed  Google Scholar 

  12. J. M. Bakker, A. Kavelaars, P. J. Kamphuis, et al., “Neonatal dexamethasone treatment increases susceptibility to experimental autoimmune disease in adult rats,” J. Immunol., 165, No. 10, 5932–5937 (2000).

    Article  CAS  PubMed  Google Scholar 

  13. J. Bauer, F. Berkenbosch, A. M. Van Dam, and C. D. Dijkstra, “Demonstration of interleukin-1 beta in Lewis rat brain during experimental allergic encephalomyelitis by immunocytochemistry at the light and ultrastructural level,” J. Neuroimmunol., 48, No. 1, 13–21 (1993).

    Article  CAS  PubMed  Google Scholar 

  14. S. D. Bilbo and J. M. Schwartz, “Early-life programming of later-life brain and behavior: a critical role for the immune system,” Front. Behav. Neurosci., 3, Art. 14, 1–14, (2009).

  15. A. Brogi, M. Strazza, M. Melli, and E. Costantino-Ceccarini, “Induction of intracellular ceramide by interleukin-1 beta in oligodendrocytes,” J. Cell Biochem., 66, 532–541 (1997).

    Article  CAS  PubMed  Google Scholar 

  16. C. F. Brosnan, B. Cannella, L. Battistini, and C. S. Raine, “Cytokine localization in multiple sclerosis lesions: correlation with adhesion molecule expression and reactive nitrogen species,” Neurology, 45, No. 6, Supplement 6, S16–S21, (1995).

  17. B. A. De Jong, T. W. Huizinga, E. L. Bollen, et al., “Production of IL-1beta and IL-1Ra as risk factors for susceptibility and progression of relapse-onset multiple sclerosis,” J. Neuroimmunol., 126, 172–179 (2002).

    Article  PubMed  Google Scholar 

  18. A. de la Mano, A. Gato, M. I. Alonso, et al., “Role of interleukin-1beta in the control of neuroepithelial proliferation and differentiation of the spinal cord during development,” Cytokine, 37, No. 2, 128–137 (2007).

    Article  PubMed  Google Scholar 

  19. R. Detels, B. R. Visscher, R. W. Haile, et al., “Multiple sclerosis and age at migration,” Am. J. Epidemiol., 108, No. 5, 386–393 (1978).

    CAS  PubMed  Google Scholar 

  20. M. Dmitrijevic, O. Laban, S. von Hoersten, et al., “Neonatal sound stress and development of experimental allergic encephalomyelitis in Lewis and DA rats,” Int. J. Neurosci., 76, No. 1–2, 135–143 (1994).

    Article  Google Scholar 

  21. C. A. Dinarello, “Blocking interleukin-1β in acute and chronic autoinflammatory diseases,” J. Intern. Med., 269, No. 1, 16–28 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. D. A. Dyment, G. C. Ebers, and A. D. Sadovnick, “Genetics of multiple sclerosis,” Lancet Neurol., 3, No. 2, 104–110 (2004).

    Article  CAS  PubMed  Google Scholar 

  23. K. K. Ellestad, S. Tsutsui, F. Noorbakhsh, et al., “Early life exposure to lipopolysaccharide suppresses experimental autoimmune encephalomyelitis by promoting tolerogenic dendritic cells and regulatory T cells,” J. Immunol., 183, 298–309 (2009).

    Article  CAS  PubMed  Google Scholar 

  24. G. Favrais, Y. van de Looij, B. Fleiss, et al., “Systemic inflammation disrupts the developmental program of white matter,” Ann. Neurol., 70, 550–565 (2011).

    Article  CAS  PubMed  Google Scholar 

  25. H. Furukawa, A. del Rey, G. Monge-Arditti, and H. O. Besedovsky, “Interleukin-1β but not stress stimulates glucocorticoid output during early postnatal life in mice,” Ann. N.Y. Acad. Sci., 840, 117–122 (1998).

    Article  CAS  PubMed  Google Scholar 

  26. M. A. Galic, S. J. Spencer, A. Mouihate, and Q. J. Pittman, “Postnatal programming of the innate immune response,” Integrat. Comp. Biol., 49, No. 3, 237–245 (2009).

    Article  CAS  Google Scholar 

  27. D. Giulian, D. G. Young, J. Woodward, et al., “Interleukin-1 is an astroglial growth factor in developing nervous system,” J. Neurosci., 8, 709–714 (1988).

    CAS  PubMed  Google Scholar 

  28. R. Gold, C. Linington, and H. Lassmann, “Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research,” Brain, 129, 1953–1971 (2006).

    Article  PubMed  Google Scholar 

  29. H. Hagberg, E. Bona, E. Gilland, and M. Puka-Sundvall, “Hypoxiaischemia model in the 7 day old rat: possibilities and shortcomings,” Acta Pediatr., 422, Supplement, 85–88 (1997).

  30. S. L. Hauder, T. H. Doolittle, R. Lincoln, et al., “Cytokine accumulations in CSF of multiple sclerosis patients: frequent detection of interleukin-1 and tumor necrosis factor but not interleukin-6,” Neurology, 40, 1735–1739 (1990).

    Article  Google Scholar 

  31. A. G. Kermode, P. S. Tofts, A. J. Thompson, et al., “Heterogeneity of blood-brain barrier changes in multiple sclerosis: an MRI study with gadolinium-DTPA enhancement,” Neurology, 40, No. 2, 229–235 (1990).

    Article  CAS  PubMed  Google Scholar 

  32. B. Krone, E. Oeffner, and J. M. Grange, “Is the risk of multiple sclerosis related to the ‘biography’ of the immune system?” J. Neurol., 256, 1052–1060 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  33. O. Laban, B. M. Markovic, M. Dmitrijevic, and B. D. Jankovic, “Maternal deprivation and early weaning modulate experimental allergic encephalomyelitis in the rat,” Brain Behav. Immun., 9, No. 1, 9–19 (1995).

    Article  CAS  PubMed  Google Scholar 

  34. X. L. Li, J. Lv, N. N. Xi, et al., “Neonatal endotoxin exposure suppresses experimental autoimmune encephalomyelitis through regulating the immune cells responsivity in the central nervous system of adult rats,” Biochem. Biophys. Res. Commun., 398, No. 2, 302–208 (2010).

    Article  CAS  PubMed  Google Scholar 

  35. C. L. Mann, M. B. Davies, V. L. Stevenson, et al., “Interleukin 1 genotypes in multiple sclerosis and relationship to disease severity,” J. Neuroimmunol., 129, 197–204 (2002).

    Article  CAS  PubMed  Google Scholar 

  36. D. Martin and S. L. Near, “Protective effect of the interleukin-1 receptor antagonist (IL-1ra) on experimental allergic encephalomyelitis in rats,” J. Neuroimmunol., 61, 241–245 (1995).

    Article  CAS  PubMed  Google Scholar 

  37. J. L. Mason, K. Suzuki, D. D. Chaplin, and G. K. Matsushima, “Interleukin-1beta promotes repair of the CNS,” J. Neurosci., 21, 7046–7052 (2001).

    CAS  PubMed  Google Scholar 

  38. T. Matsuki, S. Nakae, K. Sudo, et al., “Abnormal T cell activation caused by the imbalance of the IL-1/IL-1R antagonist system is responsible for the development of experimental autoimmune encephalomyelitis,” Int. Immunol., 18, No. 2, 399–340 (2006).

    Article  CAS  PubMed  Google Scholar 

  39. E. E. McCandless, M. Budde, J. R. Lees, et al., “IL-1R signaling within the central nervous system regulates CXCL12 expression at the blood-brain barrier and disease severity during experimental autoimmune encephalomyelitis,” J. Immunol., 183, No. 1, 613–620 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. J. E. Merrill and N. J. Scolding, “Mechanisms of damage to myelin and oligodendrocytes and their relevance to disease,” Neuropathol. Appl. Neurobiol., 25, 435–458 (1999).

    Article  CAS  PubMed  Google Scholar 

  41. D. Michelson, L. Stone, E. Galliven, et al., “Multiple sclerosis is associated with alterations in hypothalamic-pituitary-adrenal axis function,” J. Clin. Endocrinol. Metab., 79, No. 3, 848–853 (1994).

    CAS  PubMed  Google Scholar 

  42. H. Okada, C. Kuhn, H. Feillet, and J.-F. Bach, “The ‘hygiene hypothesis’ for autoimmune and allergic diseases: an update,” Clin. Exp. Immunol., 160, 1–9 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. M. Oprica, E. Hjorth, S. Spulber, et al., “Studies on brain volume, Alzheimer-related proteins and cytokines in mice with chronic overexpression of IL-1 receptor antagonist,” J. Cell Mol. Med., 11, No. 4, 810–825 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. J. W. Peterson and B. D. Trapp, “Neuropathobiology of multiple sclerosis,” Neurol. Clin., 23, No. 1, 107–129 (2005).

    Article  PubMed  Google Scholar 

  45. M. Pugliatti, T. Riise, M. A. Sotgiu, et al., “Evidence of early childhood as the susceptibility period in multiple sclerosis: space-time cluster analysis in a Sardinian population,” Am. J. Epidemiol., 164, 326–333 (2006).

    Article  PubMed  Google Scholar 

  46. M. Reale, F.de Angelis, M. di Nicola, et al., “Relation between pro-inflammatory cytokines and acetylcholine levels in relapsing-remitting multiple sclerosis patients,” Int. J. Mol. Sci., 13, No. 10, 12,656–12,664 (2012).

    Article  CAS  Google Scholar 

  47. D. Rice and S. Barone, “Critical periods of vulnerability for the developing nervous system: Evidence from humans and animal models,” Environ. Health Perspect., 108, Supplement 3, 511–533 (2000).

    Article  PubMed  PubMed Central  Google Scholar 

  48. S. S. Shaftel, T. J. Carlson, J. A. Olschowska, et al., “Chronic Interleukin-1β expression in mouse brain leads to leukocyte infiltration and neutrophil-independent blood-brain barrier permeability without overt neurodegeneration,” J. Neurosci., 27, No. 35, 9301–9309 (2007).

    Article  CAS  PubMed  Google Scholar 

  49. N. Shanks, R. J. Windle, P. A. Perks, et al., “Early-life exposure to endotoxin alters hypothalamic-pituitary-adrenal function and predisposition to inflammation,” Proc. Natl. Acad. Sci. USA, 97, 5645–5650 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. S. J. Spencer, S. Martin, A. Mouihate, and Q. J. Pittman, “Early life immune challenge: defi ning a critical window for effects on adult responses to immune challenge,” Neuropsychopharmacology, 31, 1910–1918 (2006).

    Article  CAS  PubMed  Google Scholar 

  51. E. M. Sternberg, J. M. Hilol, G. P. Chrousos, et al., “Inflammatory mediator-induced hypothalamic–pituitary–adrenal axis activation is defective in streptococcal cell wall arthritis-susceptible Lewis rats,” Proc. Natl. Acad. Sci. USA, 86, 2374–2378 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. C. Sutton, C. Brereton, B. Keogh, et al., “A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis,” J. Exp. Med., 203, No. 7, 1685–1691 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. J. A. Symons, R. V. Bundick, A. J. Suckling, and M. G. Rumsby, “Cerebrospinal fluid interleukin 1 like activity during chronic relapsing experimental allergic encephalomyelitis,” Clin. Exp. Immunol., 68, No. 3, 648–654 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. J. L. Takahashi, F. Giuliani, C. Power, et al., “Interleukin-lbeta promotes oligodendrocyte death through glutamate excitotoxicity,” Ann. Neurol., 53, No. 5, 588–595 (2003).

    Article  CAS  PubMed  Google Scholar 

  55. M. A. Teunis, C. J. Heijnen, F. Sluyter, et al., “Maternal deprivation of rat pups increases clinical symptoms of experimental autoimmune encephalomyelitis at adult age,” J. Neuroimmunol., 133, No. 1–2, 30–38 (2002).

    Article  CAS  PubMed  Google Scholar 

  56. J. M. Vela, E. Molina-Holgado, A. Arevalo-Martin, et al., “Inter leukin-1 regulates proliferation and differentiation of oligoden drocyte progenitor cells,” Mol. Cell. Neurosci., 20, 489–502 (2002).

    Article  CAS  PubMed  Google Scholar 

  57. Z. W. Wang, P. Wang, F. H. Lin, et al., “Early-life exposure to lipopolysaccharide reduces the severity of experimental autoimmune encephalomyelitis in adulthood and correlated with increased urine corticosterone and apoptotic CD4+ T cells,” Neuroscience, 193, 283–290 (2011).

    Article  CAS  PubMed  Google Scholar 

  58. R. C. Wiggins, “Myelination: a critical stage in development,” Neurotoxicol., 7, No. 2, 103–120 (1986).

    CAS  Google Scholar 

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Correspondence to I. N. Abdurasulova.

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Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 101, No. 4, pp. 386–399, April, 2015.

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Abdurasulova, I.N., Zubareva, O.E., Zhitnukhin, Y.L. et al. The Course of Experimental Allergic Encephalomyelitis in Adult Rats after Administration of Interleukin-1β at Different Periods in Early Life. Neurosci Behav Physi 46, 794–802 (2016). https://doi.org/10.1007/s11055-016-0313-y

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