Interleukin-12 (IL-12), but not IL-23, induces the expression of IL-7 in microglia and macrophages: Implications for multiple sclerosis

Immunology

Volumn 141, Issue 4, 2014, Pages 549-563

  Jana, Malabendu ^a   Mondal, Susanta ^a   Jana, Arundhati ^a   Pahan, Kalipada ^a,b  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b JESSE BROWN VA MEDICAL CENTER   (United States)

Author keywords

Interleukin 12; Interleukin 12 receptor; Interleukin 23; Interleukin 7; Microglia; Neuroinflammation

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; BETA INTERFERON; CD11B ANTIGEN; GLYCOPROTEIN GP 120; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 12; INTERLEUKIN 12 RECEPTOR BETA1; INTERLEUKIN 12 RECEPTOR BETA2; INTERLEUKIN 12P19; INTERLEUKIN 12P35; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 16; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 7; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CEREBELLUM; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE MICROSCOPY; IN VITRO STUDY; MICROGLIA; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL CORD; WILD TYPE;

INTERLEUKIN-12; INTERLEUKIN-12 RECEPTOR; INTERLEUKIN-23; INTERLEUKIN-7; MICROGLIA; NEUROINFLAMMATION;

ANIMALS; ASTROCYTES; CELLS, CULTURED; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GENES, REPORTER; HIV ENVELOPE PROTEIN GP120; HUMANS; INTERLEUKIN-12; INTERLEUKIN-12 SUBUNIT P35; INTERLEUKIN-12 SUBUNIT P40; INTERLEUKIN-23; INTERLEUKIN-7; LIPOPOLYSACCHARIDES; LUCIFERASES; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; MULTIPLE SCLEROSIS; PRIMARY CELL CULTURE; PROMOTER REGIONS, GENETIC; RECEPTORS, INTERLEUKIN-12; RECOMBINANT PROTEINS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSFECTION; UP-REGULATION;

EID: 84895794671     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12214     Document Type: Article

References (47)

1. Alpdogan O, van den Brink MR. IL-7 and IL-15: therapeutic cytokines for immunodeficiency. Trends Immunol 2005; 26:56-64.
2. Schluns KS, Kieper WC, Jameson SC, Lefrancois L. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat Immunol 2000; 1:426-32.
3. Ma A, Koka R, Burkett P. Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu Rev Immunol 2006; 24:657-79.
4. Mazzucchelli R, Durum SK. Interleukin-7 receptor expression: intelligent design. Nat Rev Immunol 2007; 7:144-54.
5. van Roon JA, Glaudemans KA, Bijlsma JW, Lafeber FP. Interleukin 7 stimulates tumour necrosis factor α and Th1 cytokine production in joints of patients with rheumatoid arthritis. Ann Rheum Dis 2003; 62:113-9.
6. Ariizumi K, Meng Y, Bergstresser PR, Takashima A. IFN-γ-dependent IL-7 gene regulation in keratinocytes. J Immunol 1995; 154:6031-9.
7. Tang J, Nuccie BL, Ritterman I, Liesveld JL, Abboud CN, Ryan DH. TGF-β down-regulates stromal IL-7 secretion and inhibits proliferation of human B cell precursors. J Immunol 1997; 159:117-25.
8. Sawa Y, Arima Y, Ogura H et al. Hepatic interleukin-7 expression regulates T cell responses. Immunity 2009; 30:447-57.
9. Sawa S, Kamimura D, Jin GH et al. Autoimmune arthritis associated with mutated interleukin (IL)-6 receptor gp130 is driven by STAT3/IL-7-dependent homeostatic proliferation of CD4+ T cells. J Exp Med 2006; 203:1459-70.
10. Chou YK, Bourdette DN, Barnes D et al. IL-7 enhances Ag-specific human T cell response by increasing expression of IL-2R α and γ chains. J Neuroimmunol 1999; 96:101-11.
11. Bebo BF Jr, Schuster JC, Adlard K, Vandenbark AA, Offner H. Interleukin 7 is a potent co-stimulator of myelin specific T cells that enhances the adoptive transfer of experimental autoimmune encephalomyelitis. Cytokine 2000; 12:324-31.
12. Traggiai E, Biagioli T, Rosati E, Ballerini C, Mazzanti B, Ben Nun A, Massacesi L, Vergelli M. IL-7-enhanced T-cell response to myelin proteins in multiple sclerosis. J Neuroimmunol 2001; 121:111-9.
13. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, Weaver CT. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005; 6:1123-32.
14. Liu X, Leung S, Wang C et al. Crucial role of interleukin-7 in T helper type 17 survival and expansion in autoimmune disease. Nat Med 2010; 16:191-7.
15. El-behi M, Rostami A, Ciric B. Current views on the roles of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. J Neuroimmune Pharmacol 2010; 5:189-97.
16. Lassmann H, Ransohoff RM. The CD4-Th1 model for multiple sclerosis: a critical [correction of crucial] re-appraisal. Trends Immunol 2004; 25:132-7.
17. Kreft KL, Verbraak E, Wierenga-Wolf AF, van Meurs M, Oostra BA, Laman JD, Hintzen RQ. The IL-7Ralpha pathway is quantitatively and functionally altered in CD8 T cells in multiple sclerosis. J Immunol 2012; 188:1874-83.
18. Kremlev SG, Gaurnier-Hausser AL, Del Valle L, Perez-Liz G, Dimitrov S, Tuszynski G. Angiocidin promotes pro-inflammatory cytokine production and antigen presentation in multiple sclerosis. J Neuroimmunol 2008; 194:132-42.
19. Malmestrom C, Lycke J, Haghighi S, Andersen O, Carlsson L, Wadenvik H, Olsson B. Relapses in multiple sclerosis are associated with increased CD8+ T-cell mediated cytotoxicity in CSF. J Neuroimmunol 2008; 196:159-65.
20. Hsieh CS, Macatonia SE, Tripp CS, Wolf SF, O'Garra A, Murphy KM. Development of TH1 CD4+ T cells through IL-12 produced by Listeria-induced macrophages. Science 1993; 260:547-9.
21. Constantinescu CS, Goodman DB, Hilliard B, Wysocka M, Cohen JA. Murine macrophages stimulated with central and peripheral nervous system myelin or purified myelin proteins release inflammatory products. Neurosci Lett 2000; 287:171-4.
22. Zipris D, Greiner DL, Malkani S, Whalen B, Mordes JP, Rossini AA. Cytokine gene expression in islets and thyroids of BB rats. IFN-gamma and IL-12p40 mRNA increase with age in both diabetic and insulin-treated nondiabetic BB rats. J Immunol 1996; 156:1315-21.
23. Gately MK, Renzetti LM, Magram J, Stern AS, Adorini L, Gubler U, Presky DH. The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses. Annu Rev Immunol 1998; 16:495-521.
24. Kobayashi M, Kweon MN, Kuwata H, Schreiber RD, Kiyono H, Takeda K, Akira S. Toll-like receptor-dependent production of IL-12p40 causes chronic enterocolitis in myeloid cell-specific Stat3-deficient mice. J Clin Investig 2003; 111:1297-308.
25. Jana M, Dasgupta S, Saha RN, Liu X, Pahan K. Induction of tumor necrosis factor-alpha (TNF-alpha) by interleukin-12 p40 monomer and homodimer in microglia and macrophages. J Neurochem 2003; 86:519-28.
26. Pahan K, Sheikh FG, Liu X, Hilger S, McKinney M, Petro TM. Induction of nitric-oxide synthase and activation of NF-kappaB by interleukin-12 p40 in microglial cells. J Biol Chem 2001; 276:7899-905.
27. Jana M, Pahan K. IL-12 p40 homodimer, but not IL-12 p70, induces the expression of IL-16 in microglia and macrophages. Mol Immunol 2009; 46:773-83.
28. Jana M, Pahan K. Induction of lymphotoxin-alpha by interleukin-12 p40 homodimer, the so-called biologically inactive molecule, but not IL-12 p70. Immunology 2009; 127:312-25.
29. Giulian D, Baker TJ. Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci 1986; 6:2163-78.
30. Jana M, Dasgupta S, Pal U, Pahan K. IL-12 p40 homodimer, the so-called biologically inactive molecule, induces nitric oxide synthase in microglia via IL-12R beta 1. Glia 2009; 57:1553-65.
31. Jana M, Jana A, Pal U, Pahan K. A simplified method for isolating highly purified neurons, oligodendrocytes, astrocytes, and microglia from the same human fetal brain tissue. Neurochem Res 2007; 32:2015-22.
32. Jana M, Jana A, Liu X, Ghosh S, Pahan K. Involvement of phosphatidylinositol 3-kinase-mediated up-regulation of I kappa B alpha in anti-inflammatory effect of gemfibrozil in microglia. J Immunol 2007; 179:4142-52.
33. Jana M, Anderson JA, Saha RN, Liu X, Pahan K. Regulation of inducible nitric oxide synthase in proinflammatory cytokine-stimulated human primary astrocytes. Free Radic Biol Med 2005; 38:655-64.
34. Dasgupta S, Jana M, Zhou Y, Fung YK, Ghosh S, Pahan K. Antineuroinflammatory effect of NF-kappaB essential modifier-binding domain peptides in the adoptive transfer model of experimental allergic encephalomyelitis. J Immunol 2004; 173:1344-54.
35. Jana M, Pahan K. Redox regulation of cytokine-mediated inhibition of myelin gene expression in human primary oligodendrocytes. Free Radic Biol Med 2005; 39:823-31.
36. Jana M, Liu X, Koka S, Ghosh S, Petro TM, Pahan K. Ligation of CD40 stimulates the induction of nitric-oxide synthase in microglial cells. J Biol Chem 2001; 276:44527-33.
37. Liu X, Jana M, Dasgupta S, Koka S, He J, Wood C, Pahan K. Human immunodeficiency virus type 1 (HIV-1) tat induces nitric-oxide synthase in human astroglia. J Biol Chem 2002; 277:39312-9.
38. Weber MS, Benkhoucha M, Lehmann-Horn K et al. Repetitive pertussis toxin promotes development of regulatory T cells and prevents central nervous system autoimmune disease. PLoS One 2010; 5:e16009.
39. Dasgupta S, Roy A, Jana M, Hartley DM, Pahan K. Gemfibrozil ameliorates relapsing-remitting experimental autoimmune encephalomyelitis independent of peroxisome proliferator-activated receptor-alpha. Mol Pharmacol 2007; 72:934-46.
40. Cua DJ, Sherlock J, Chen Y et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003; 421:744-8.
41. Watanabe M, Ueno Y, Yajima T et al. Interleukin 7 transgenic mice develop chronic colitis with decreased interleukin 7 protein accumulation in the colonic mucosa. J Exp Med 1998; 187:389-402.
42. Aragane Y, Schwarz A, Luger TA, Ariizumi K, Takashima A, Schwarz T. Ultraviolet light suppresses IFN-gamma-induced IL-7 gene expression in murine keratinocytes by interfering with IFN regulatory factors. J Immunol 1997; 158:5393-9.
43. Oshima S, Nakamura T, Namiki S et al. Interferon regulatory factor 1 (IRF-1) and IRF-2 distinctively up-regulate gene expression and production of interleukin-7 in human intestinal epithelial cells. Mol Cell Biol 2004; 24:6298-310.
44. Cooper AM, Khader SA. IL-12p40: an inherently agonistic cytokine. Trends Immunol 2007; 28:33-8.
45. Tortorella C, Stella I, Piazzolla G, Cappiello V, Simone O, Pisconti A, Antonaci S. Impaired interleukin-12-dependent T-cell functions during aging: role of signal transducer and activator of transcription 4 (STAT4) and suppressor of cytokine signaling 3 (SOCS3). J Gerontol A Biol Sci Med Sci 2006; 61:125-35.
46. Martin J, LaBranche CC, Gonzalez-Scarano F. Differential CD4/CCR5 utilization, gp120 conformation, and neutralization sensitivity between envelopes from a microglia-adapted human immunodeficiency virus type 1 and its parental isolate. J Virol 2001; 75:3568-80.
47. Minagar A, Shapshak P, Fujimura R, Ownby R, Heyes M, Eisdorfer C. The role of macrophage/microglia and astrocytes in the pathogenesis of three neurologic disorders: HIV-associated dementia, Alzheimer disease, and multiple sclerosis. J Neurol Sci 2002; 202:13-23.