Experimental priming of encephalitogenic Th1/Th17 cells requires pertussis toxin-driven IL-1β production by myeloid cells

Nature Communications

Volumn 7, Issue , 2016, Pages

  Ronchi, Francesca ^a,c   Basso, Camilla ^a   Preite, Silvia ^a   Reboldi, Andrea ^a,d   Baumjohann, Dirk ^a,e   Perlini, Luana ^a   Lanzavecchia, Antonio ^a,b   Sallusto, Federica ^a  

^a INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF BERN   (Switzerland)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; MYELOID DIFFERENTIATION FACTOR 88; PERTUSSIS TOXIN; INTERLEUKIN 1 RECEPTOR TYPE I;

ALLERGY; ANTIGEN; CELLS AND CELL COMPONENTS; DATA SET; EXPERIMENTAL STUDY; IMMUNIZATION; INFECTIOUS DISEASE; RODENT; TOXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW CELL; CD4+ T LYMPHOCYTE; CELLS; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; IMMUNIZATION; MONOCYTE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TH1 CELL; TH17 CELL; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; HELPER CELL; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; SECRETION (PROCESS);

MUS;

ANIMALS; CELL DIFFERENTIATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; INTERFERON-GAMMA; INTERLEUKIN-17; MICE, INBRED C57BL; PERTUSSIS TOXIN; RECEPTORS, INTERLEUKIN-1 TYPE I; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84969920238     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11541     Document Type: Article

References (66)

1. Ivanov, I. I. et al. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126, 1121-1133 (2006).
2. Eberl, G. et al. An essential function for the nuclear receptor RORgamma(t) in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 5, 64-73 (2004).
3. Cua, D. J. et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421, 744-748 (2003).
4. McGeachy, M. J. et al. TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat. Immunol. 8, 1390-1397 (2007).
5. Ghoreschi, K. et al. Generation of pathogenic T(H)17 cells in the absence of TGF-b signalling. Nature 467, 967-971 (2010).
6. Lee, Y. et al. Induction and molecular signature of pathogenic TH17 cells. Nat. Immunol. 13, 991-999 (2012).
7. Ponomarev, E. D. et al. GM-CSF production by autoreactive T cells is required for the activation of microglial cells and the onset of experimental autoimmune encephalomyelitis. J. Immunol. 178, 39-48 (2007).
8. Codarri, L. et al. RORgt drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat. Immunol. 12, 560-567 (2011).
9. El-Behi, M. et al. The encephalitogenicity of T(H)17 cells is dependent on IL-1- and IL-23-induced production of the cytokine GM-CSF. Nat. Immunol. 12, 568-575 (2011).
10. Stromnes, I. M. & Goverman, J. M. Active induction of experimental allergic encephalomyelitis. Nat. Protoc. 1, 1810-1819 (2006).
11. Miller, S. D. & Karpus, W. J. Experimental autoimmune encephalomyelitis in the mouse. Curr. Protoc. Immunol. Chapter 15, Unit 15.1 (2007).
12. Kabat, E. A., Wolf, A. & Bezer, A. E. The rapid production of acute disseminated encephalomyelitis in Rhesus monkeys by injection of heterologous brain tissue with adjuvants. J. Exp. Med. 85, 117-130 (1947).
13. Levine, S., Wenk, E. J., Devlin, H. B., Pieroni, R. E. & Levine, L. Hyperacute allergic encephalomyelitis: adjuvant effect of pertussis vaccines and extracts. J. Immunol. 97, 363-368 (1966).
14. Bora, N. S., Woon, M. D., Tandhasetti, M. T., Cirrito, T. P. & Kaplan, H. J. Induction of experimental autoimmune anterior uveitis by a self-antigen: melanin complex without adjuvant. Invest. Ophthalmol. Vis. Sci. 38, 2171-2175 (1997).
15. Afanasyeva, M. et al. Experimental autoimmune myocarditis in A/J mice is an interleukin-4-dependent disease with a Th2 phenotype. Am. J. Pathol. 159, 193-203 (2001).
16. Iwanami, K. et al. Arthritogenic T cell epitope in glucose-6-phosphate isomerase-induced arthritis. Arthritis Res. Ther. 10, R130 (2008).
17. Yong, T., Meininger, G. A. & Linthicum, D. S. Enhancement of histamineinduced vascular leakage by pertussis toxin in SJL/J mice but not BALB/c mice. J. Neuroimmunol. 45, 47-52 (1993).
18. Linthicum, D. S., Munoz, J. J. & Blaskett, A. Acute experimental autoimmune encephalomyelitis in mice. I. Adjuvant action of Bordetella pertussis is due to vasoactive amine sensitization and increased vascular permeability of the central nervous system. Cell Immunol. 73, 299-310 (1982).
19. Dumas, A. et al. The inflammasome pyrin contributes to pertussis toxin-induced IL-1b synthesis, neutrophil intravascular crawling and autoimmune encephalomyelitis. PLoS Pathog. 10, e1004150 (2014).
20. Nencioni, L. et al. Characterization of genetically inactivated pertussis toxin mutants: candidates for a new vaccine against whooping cough. Infect. Immun. 58, 1308-1315 (1990).
21. Gran, B. et al. IL-12p35-deficient mice are susceptible to experimental autoimmune encephalomyelitis: evidence for redundancy in the IL-12 system in the induction of central nervous system autoimmune demyelination. J. Immunol. 169, 7104-7110 (2002).
22. Becher, B., Durell, B. G. & Noelle, R. J. Experimental autoimmune encephalitis and inflammation in the absence of interleukin-12. J. Clin. Invest. 110, 493-497 (2002).
23. Awasthi, A. & Kuchroo, V. K. Th17 cells: from precursors to players in inflammation and infection. Int. Immunol. 21, 489-498 (2009).
24. Croxford, A. L. et al. The cytokine GM-CSF drives theinflammatory signature of CCR2+ monocytes and licenses autoimmunity. Immunity 43, 502-514 (2015).
25. Medzhitov, R. et al. MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol. Cell 2, 253-258 (1998).
26. Kerfoot, S. M. et al. TLR4 contributes to disease-inducing mechanisms resulting in central nervous system autoimmune disease. J. Immunol. 173, 7070-7077 (2004).
27. Cassan, C. et al. Pertussis toxin reduces the number of splenic Foxp3+ regulatory T cells. J. Immunol. 177, 1552-1560 (2006).
28. Chen, X. et al. Pertussis toxin as an adjuvant suppresses the number and function of CD4+CD25+ T regulatory cells. Eur. J. Immunol. 36, 671-680 (2006).
29. Chen, X., Howard, O. M. Z. & Oppenheim, J. J. Pertussis toxin by inducing IL-6 promotes the generation of IL-17-producing CD4 cells. J. Immunol. 178, 6123-6129 (2007).
30. Carlson, T., Kroenke, M., Rao, P., Lane, T. E. & Segal, B. The Th17-ELR+ CXC chemokine pathway is essential for the development of central nervous system autoimmune disease. J. Exp. Med. 205, 811-823 (2008).
31. Kebir, H. et al. Human T(H)17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nature Med. 13, 1173-1175 (2007).
32. Huppert, J. et al. Cellular mechanisms of IL-17-induced blood-brain barrier disruption. FASEB J. 24, 1023-1034 (2010).
33. Kawanokuchi, J. et al. Production and functions of IL-17 in microglia. J. Neuroimmunol. 194, 54-61 (2008).
34. Petermann, F. & Korn, T. Cytokines and effector T cell subsets causing autoimmune CNS disease. FEBS Lett. 585, 3747-3757 (2011).
35. Ladant, D. & Ullmann, A. Bordatella pertussis adenylate cyclase: a toxin with multiple talents. Trends Microbiol. 7, 172-176 (1999).
36. Wakatsuki, A., Borrow, P., Rigley, K. & Beverley, P. C. L. Cell-surface bound pertussis toxin induces polyclonal T cell responses with high levels of interferon-gamma in the absence of interleukin-12. Eur. J. Immunol. 33, 1859-1868 (2003).
37. Peters, A., Lee, Y. & Kuchroo, V. K. The many faces of Th17 cells. Curr. Opin. Immunol. 23, 702-706 (2011).
38. McGeachy, M. J. et al. The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat. Immunol. 10, 314-324 (2009).
39. Fife, B. T., Huffnagle, G. B., Kuziel, W. A. & Karpus, W. J. CC chemokine receptor 2 is critical for induction of experimental autoimmune encephalomyelitis. J. Exp. Med. 192, 899-905 (2000).
40. Izikson, L., Klein, R. S., Charo, I. F., Weiner, H. L. & Luster, A. D. Resistance to experimental autoimmune encephalomyelitis in mice lacking the CC chemokine receptor (CCR)2. J. Exp. Med. 192, 1075-1080 (2000).
41. Huang, D. R., Wang, J., Kivisakk, P., Rollins, B. J. & Ransohoff, R. M. Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J. Exp. Med. 193, 713-726 (2001).
42. Acosta-Rodriguez, E. V., Napolitani, G., Lanzavecchia, A. & Sallusto, F. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 8, 942-949 (2007).
43. Guarda, G. et al. Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 34, 213-223 (2011).
44. Schenten, D. et al. Signaling through the adaptor molecule MyD88 in CD4(+) T cells is required to overcome suppression by regulatory T cells. Immunity 40, 78-90 (2014).
45. Sutton, C., Brereton, C., Keogh, B., Mills, K. H. G. & Lavelle, E. C. A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis. J. Exp. Med. 203, 1685-1691 (2006).
46. Zielinski, C. E. et al. Pathogen-induced human TH17 cells produce IFN-g or IL-10 and are regulated by IL-1b. Nature 484, 514-518 (2012).
47. Horai, R. et al. Production of mice deficient in genes for interleukin (IL)-1alpha, IL-1beta, IL-1alpha/beta, and IL-1 receptor antagonist shows that IL-1beta is crucial in turpentine-induced fever development and glucocorticoid secretion. J. Exp. Med. 187, 1463-1475 (1998).
48. Mariathasan, S. et al. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430, 213-218 (2004).
49. Cua, D. J. et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421, 744-748 (2003).
50. Adachi, O. et al. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9, 143-150 (1998).
51. Hoshino, K. et al. Cutting edge. Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol. 162, 3749-3752 (1999).
52. Hemmi, H. et al. A Toll-like receptor recognizes bacterial DNA. Nature 408, 740-745 (2000).
53. Takeuchi, O. et al. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 11, 443-451 (1999).
54. Labow, M. et al. Absence of IL-1 signaling and reduced inflammatory response in IL-1 type I receptor-deficient mice. J. Immunol. 159, 2452-2461 (1997).
55. Boring, L. et al. Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J. Clin. Invest. 100, 2552-2561 (1997).
56. Neighbors, M. et al. Breakpoints in immunoregulation required for Th1 cells to induce diabetes. Eur. J. Immunol. 36, 2315-2323 (2006).
57. Barnden, M. J., Allison, J., Heath, W. R. & Carbone, F. R. Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and beta-chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 76, 34-40 (1998).
58. Hogquist, K. A. et al. T cell receptor antagonist peptides induce positive selection. Cell 76, 17-27 (1994).
59. Bettelli, E. et al. Myelin oligodendrocyte glycoprotein-specific T cell receptor transgenic mice develop spontaneous autoimmune optic neuritis. J. Exp. Med. 197, 1073-1081 (2003).
60. Van Rooijen, N. & Sanders, A. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J. Immunol. Methods 174, 83-93 (1994).
61. Lutz, M. B. et al. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223, 77-92 (1999).
62. Zal, T., Volkmann, A. & Stockinger, B. Mechanisms of tolerance induction in major histocompatibility complex class II-restricted T cells specific for a blood-borne self-antigen. J. Exp. Med. 180, 2089-2099 (1994).
63. Martín-Fontecha, A. et al. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat. Immunol. 5, 1260-1265 (2004).
64. + inflammatory monocytes during Mycobacterium tuberculosis-specific T cell priming. Elife 2, e01086 (2013).
65. Seder, R. A., Darrah, P. A. & Roederer, M. T-cell quality in memory and protection: implications for vaccine design. Nat. Rev. Immunol. 8, 247-258 (2008).
66. Reboldi, A. et al. C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat. Immunol. 10, 514-523 (2009).