Cerebral interleukin-15 shows upregulation and beneficial effects in experimental autoimmune encephalomyelitis

Journal of Neuroimmunology

Volumn 223, Issue 1-2, 2010, Pages 65-72

  Wu, Xiaojun ^a   Pan, Weihong ^a   He, Yi ^a   Hsuchou, Hung ^a   Kastin, Abba J ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

Autoimmune disease; Blood brain barrier; Brain; Cytokine; IL15; Immunity

Indexed keywords

INTERLEUKIN 15; INTERLEUKIN 15 RECEPTOR ALPHA; MESSENGER RNA;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EFFICACY; DRUG MECHANISM; DRUG TARGETING; FEMALE; IMMUNOHISTOCHEMISTRY; IMMUNOREGULATION; KNOCKOUT MOUSE; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SPINAL CORD; UPREGULATION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; BRAIN; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GENETIC PREDISPOSITION TO DISEASE; INTERLEUKIN-15; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; RECEPTORS, INTERLEUKIN-15; SEVERITY OF ILLNESS INDEX; SPINAL CORD; UP-REGULATION;

EID: 77953544228     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2010.04.001     Document Type: Article

References (43)

1. Araujo D.M., Lapchak P.A., Collier B., Quirion R. Localization of interleukin-2 immunoreactivity and interleukin-2 receptors in the rat brain: interaction with the cholinergic system. Brain Res. 1989, 498:257-266.
2. Banks W.A., Kastin A.J. Physiological consequences of the passage of peptides across the blood-brain barrier. Rev. Neurosci. 1993, 4:365-372.
3. Beck R.D., King M.A., Huang Z., Petitto J.M. Alterations in septohippocampal cholinergic neurons resulting from interleukin-2 gene knockout. Brain Res. 2002, 955:16-23.
4. Beck R.D., Wasserfall C., Ha G.K., Cushman J.D., Huang Z., Atkinson M.A., Petitto J.M. Changes in hippocampal IL-15, related cytokines, and neurogenesis in IL-2 deficient mice. Brain Res. 2005, 1041:223-230.
5. Ben A.M., Belhadj H.N., Moes N., Buyse S., Abdeladhim M., Louzir H., Cerf-Bensussan N. IL-15 renders conventional lymphocytes resistant to suppressive functions of regulatory T cells through activation of the phosphatidylinositol 3-kinase pathway. J. Immunol. 2009, 182:6763-6770.
6. Blanco-Jerez C., Plaza J.F., Masjuan J., Orensanz L.M., Alvarez-Cermeno J.C. Increased levels of IL-15 mRNA in relapsing-remitting multiple sclerosis attacks. J. Neuroimmunol. 2002, 128:90-94.
7. Budagian V., Bulanova E., Paus R., Bulfone-Paus S. IL-15/IL-15 receptor biology: a guided tour through an expanding universe. Cytokine Growth Factor Rev. 2006, 17:259-280.
8. Carson W.E., Giri J.G., Lindemann M.J., Linett M.L., Ahdieh M., Paxton R., Anderson D., Eisenmann J., Grabstein K., Caligiuri M.A. Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor. J. Exp. Med. 1994, 180:1395-1403.
9. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 2008, 9:46-56.
10. Gomez-Nicola D., Doncel-Perez E., Nieto-Sampedro M. Regulation by GD3 of the proinflammatory response of microglia mediated by interleukin-15. J. Neurosci. Res. 2006, 83:754-762.
11. Goshen I., Kreisel T., Ounallah-Saad H., Renbaum P., Zalzstein Y., Ben-Hur T., Levy-Lahad E., Yirmiya R. A dual role for interleukin-1 in hippocampal-dependent memory processes. Psychoneuroendocrinology 2007, 32:1106-1115.
12. Grabstein K.H., Eisenman J., Shanebeck K., Rauch C., Srinivasan S., Fung V., Beers C., Richardson J., Schoenborn M.A., Ahdieh M. Cloning of a T cell growth factor that interacts with the beta chain of the interleukin-2 receptor. Science 1994, 264:965-968.
13. Hanisch U.K., Quirion R. Interleukin-2 as a neuroregulatory cytokine. Brain Res. Brain Res. Rev. 1995, 21:246-284.
14. Hart B.A., Bauer J., Muller H.J., Melchers B., Nicolay K., Brok H., Bontrop R.E., Lassmann H., Massacesi L. Histopathological characterization of magnetic resonance imaging-detectable brain white matter lesions in a primate model of multiple sclerosis: a correlative study in the experimental autoimmune encephalomyelitis model in common marmosets (Callithrix jacchus). Am. J. Pathol. 1998, 153:649-663.
15. He Y., Wu X., Khan R.S., Kastin A.J., Cornélissen G.G., Hsuchou H., Robert B., Halberg F., Pan W. IL15 receptor deletion results in circadian changes of locomotor and metabolic activity. J. Mol. Neurosci. 2010, PMID: 20012227.
16. He Y., Hsuchou H., Wu X., Kastin A.J., Khan R.S., Pistell P.J., Wang W.-H., Feng J., Li Z., Guo X., Pan W. Interleukin-15 receptor is essential to facilitate GABA transmission and hippocampal dependent memory. J. Neurosci. 2010, 30:4725-4734.
17. Hsuchou H., He Y., Kastin A.J., Tu H., Markadakis E.N., Rogers R.C., Fossier P.B., Pan W. Obesity induces functional astrocytic leptin receptors in hypothalamus. Brain 2009, 132:889-902.
18. Hsuchou H., Pan W., Wu X., Kastin A.J. Cessation of blood-to-brain influx of interleukin-15 during development of EAE. J. Cereb. Blood Flow Metab. 2009, 29:1568-1578.
19. Huang Z., Ha G.K., Petitto J.M. IL-15 and IL-15R alpha gene deletion: effects on T lymphocyte trafficking and the microglial and neuronal responses to facial nerve axotomy. Neurosci. Lett. 2007, 417:160-164.
20. Kivisakk P., Matusevicius D., He B., Soderstrom M., Fredrikson S., Link H. IL-15 mRNA expression is up-regulated in blood and cerebrospinal fluid mononuclear cells in multiple sclerosis (MS). Clin. Exp. Immunol. 1998, 111:193-197.
21. Kohm A.P., Carpentier P.A., Anger H.A., Miller S.D. Cutting edge: CD4+CD25+ regulatory T cells suppress antigen-specific autoreactive immune responses and central nervous system inflammation during active experimental autoimmune encephalomyelitis. J. Immunol. 2002, 169:4712-4716.
22. Lee Y.B., Satoh J., Walker D.G., Kim S.U. Interleukin-15 gene expression in human astrocytes and microglia in culture. NeuroReport 1996, 7:1062-1066.
23. Losy J., Niezgoda A., Zaremba J. IL-15 is elevated in sera of patients with relapsing-remitting multiple sclerosis. Folia Neuropathol. 2002, 40:151-153.
24. Merrill J.E., Mohlstrom C., Uittenbogaart C., Kermaniarab V., Ellison G.W., Myers L.W. Response to and production of interleukin 2 by peripheral blood and cerebrospinal fluid lymphocytes of patients with multiple sclerosis. J. Immunol. 1984, 133:1931-1937.
25. Pan W., Banks W.A., Kennedy M.K., Gutierrez E.G., Kastin A.J. Differential permeability of the BBB in acute EAE: enhanced transport of TNF-α. Am. J. Physiol. 1996, 271:E636-E642.
26. Pan W., Hsuchou H., He Y., Sakharkar A., Cain C., Yu C., Kastin A.J. Astrocyte leptin receptor (ObR) and leptin transport in adult-onset obese mice. Endocrinology 2008, 149:2798-2806.
27. Pan W., Hsuchou H., Yu C., Kastin A.J. Permeation of blood-borne IL15 across the blood-brain barrier and the effect of LPS. J Neurochem 2008, 106:313-319.
28. Pan W., Yu C., Hsuhou H., Khan R.S., Kastin A.J. Cerebral microvascular IL15 is a novel mediator of TNF action. J. Neurochem. 2009, 111:819-827.
29. Pashenkov M., Mustafa M., Kivisakk P., Link H. Levels of interleukin-15-expressing blood mononuclear cells are elevated in multiple sclerosis. Scand. J. Immunol. 1999, 50:302-308.
30. Petitto J.M., Huang Z. Cloning the full-length IL-2/15 receptor-beta cDNA sequence from mouse brain: evidence of enrichment in hippocampal formation neurons. Regul. Pept. 2001, 98:77-87.
31. Petitto J.M., Huang Z., Raizada M.K., Rinker C.M., McCarthy D.B. Molecular cloning of the cDNA coding sequence of IL-2 receptor-gamma (gammac) from human and murine forebrain: expression in the hippocampus in situ and by brain cells in vitro. Brain Res. Mol. Brain Res. 1998, 53:152-162.
32. Petitto J.M., McNamara R.K., Gendreau P.L., Huang Z., Jackson A.J. Impaired learning and memory and altered hippocampal neurodevelopment resulting from interleukin-2 gene deletion. J. Neurosci. Res. 1999, 56:441-446.
33. Petitto J.M., Streit W.J., Huang Z., Butfiloski E., Schiffenbauer J. Interleukin-2 gene deletion produces a robust reduction in susceptibility to experimental autoimmune encephalomyelitis in C57BL/6 mice. Neurosci. Lett. 2000, 285:66-70.
34. Pollak Y., Orion E., Goshen I., Ovadia H., Yirmiya R. Experimental autoimmune encephalomyelitis-associated behavioral syndrome as a model of 'depression due to multiple sclerosis'. Brain Behav. Immun. 2002, 16:533-543.
35. Rentzos M., Cambouri C., Rombos A., Nikolaou C., Anagnostouli M., Tsoutsou A., Dimitrakopoulos A., Triantafyllou N., Vassilopoulos D. IL-15 is elevated in serum and cerebrospinal fluid of patients with multiple sclerosis. J. Neurol. Sci. 2006, 241:25-29.
36. Rentzos M., Paraskevas G.P., Kapaki E., Nikolaou C., Zoga M., Tsoutsou A., Rombos A., Vassilopoulos D. Circulating interleukin-15 in dementia disorders. J. Neuropsychiatry Clin. Neurosci. 2007, 19:318-325.
37. 't Hart B.A., Amor S. The use of animal models to investigate the pathogenesis of neuroinflammatory disorders of the central nervous system. Curr. Opin. Neurol. 2003, 16:375-383.
38. Viglietta V., Baecher-Allan C., Weiner H.L., Hafler D.A. Loss of functional suppression by CD4+CD25+ regulatory T cells in patients with multiple sclerosis. J. Exp. Med. 2004, 199:971-979.
39. Villadsen L.S., Schuurman J., Beurskens F., Dam T.N., Dagnaes-Hansen F., Skov L., Rygaard J., Voorhorst-Ogink M.M., Gerritsen A.F., van Dijk M.A., Parren P.W., Baadsgaard O., van de Winkel J.G. Resolution of psoriasis upon blockade of IL-15 biological activity in a xenograft mouse model. J. Clin. Invest 2003, 112:1571-1580.
40. Waldmann T.A. Targeting the interleukin-15/interleukin-15 receptor system in inflammatory autoimmune diseases. Arthritis Res. Ther. 2004, 6:174-177.
41. Wang J., Takeuchi H., Sonobe Y., Jin S., Mizuno T., Miyakawa S., Fujiwara M., Nakamura Y., Kato T., Muramatsu H., Muramatsu T., Suzumura A. Inhibition of midkine alleviates experimental autoimmune encephalomyelitis through the expansion of regulatory T cell population. Proc. Natl. Acad. Sci. U. S. A 2008, 105:3915-3920.
42. Winocur G., Greenwood C.E., Piroli G.G., Grillo C.A., Reznikov L.R., Reagan L.P., McEwen B.S. Memory impairment in obese Zucker rats: an investigation of cognitive function in an animal model of insulin resistance and obesity. Behav. Neurosci. 2005, 119:1389-1395.
43. Zozulya A.L., Ortler S., Lee J., Weidenfeller C., Sandor M., Wiendl H., Fabry Z. Intracerebral dendritic cells critically modulate encephalitogenic versus regulatory immune responses in the CNS. J. Neurosci. 2009, 29:140-152.