Hepatocyte growth factor limits autoimmune neuroinflammation via glucocorticoid-induced leucine zipper expression in dendritic cells

Journal of Immunology

Volumn 193, Issue 6, 2014, Pages 2743-2752

  Benkhoucha, Mahdia ^a,b   Molnarfi, Nicolas ^a,b   Dunand Sauthier, Isabelle ^a   Merkler, Doron ^a,b,c   Schneiter, Gregory ^a,b   Bruscoli, Stefano ^d   Riccardi, Carlo ^d   Tabata, Yasuhiko ^e   Funakoshi, Hiroshi ^f   Nakamura, Toshikazu ^g   Reith, Walter ^a   Santiago Raber, Marie Laure ^a   Lalive, Patrice H ^a,b  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^d UNIVERSITY OF PERUGIA   (Italy)

^e KYOTO UNIVERSITY   (Japan)

^f ASAHIKAWA MEDICAL COLLEGE   (Japan)

^g Neurogen Inc   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GLUCOCORTICOID; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 27; LEUCINE ZIPPER PROTEIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; PROGRAMMED DEATH 1 LIGAND 1; RECOMBINANT SCATTER FACTOR; TRANSFORMING GROWTH FACTOR BETA1; CORTICOSTERONE; DSIP1 PROTEIN, MOUSE; HGF PROTEIN, MOUSE; IL10 PROTEIN, MOUSE; SCATTER FACTOR; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASIC LEUCINE ZIPPER MOTIF; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG MECHANISM; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; IMMUNOMODULATION; IMMUNOREGULATION; IN VITRO STUDY; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MOUSE; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; REGULATORY T LYMPHOCYTE; RNA INTERFERENCE; SINGLE DRUG DOSE; UPREGULATION; ADOPTIVE TRANSFER; ANIMAL; AUTOIMMUNITY; BIOSYNTHESIS; BLOOD; C57BL MOUSE; CELL CULTURE; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; INFLAMMATION; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; MULTIPLE SCLEROSIS; T LYMPHOCYTE; TRANSPLANTATION;

ADOPTIVE TRANSFER; ANIMALS; AUTOIMMUNITY; CELL PROLIFERATION; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CORTICOSTERONE; DENDRITIC CELLS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; HEPATOCYTE GROWTH FACTOR; IMMUNE TOLERANCE; INFLAMMATION; INTERLEUKIN-10; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIPLE SCLEROSIS; RNA INTERFERENCE; RNA, SMALL INTERFERING; T-LYMPHOCYTES; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84907079323     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302338     Document Type: Article

References (28)

1. McFarland, H. F., and R. Martin. 2007. Multiple sclerosis: a complicated picture of autoimmunity. Nat. Immunol. 8: 913-919
2. Bailey, S. L., B. Schreiner, E. J. McMahon, and S. D. Miller. 2007. CNS myeloid DCs presenting endogenous myelin peptides ? preferentially' polarize CD4+ T(H)-17 cells in relapsing EAE. Nat. Immunol. 8: 172-180
3. Li, H., G. X. Zhang, Y. Chen, H. Xu, D. C. Fitzgerald, Z. Zhao, and A. Rostami. 2008. CD11c+CD11 b+ dendritic cells play an important role in intravenous tolerance and the suppression of experimental autoimmune encephalomyelitis. J. Immunol. 181: 2483-2493
4. Pulendran, B., H. Tang, and S. Manicassamy. 2010. Programming dendritic cells to induce T(H)2 and tolerogenic responses. Nat. Immunol. 11: 647-655
5. Nakamura, T., T. Nishizawa, M. Hagiya, T. Seki, M. Shimonishi, A. Sugimura, K. Tashiro, and S. Shimizu. 1989. Molecular cloning and expression of human hepatocyte growth factor. Nature 342: 440-443
6. Beilmann, M., G. F. Vande Woude, H. P. Dienes, and P. Schirmacher. 2000. Hepatocyte growth factor-stimulated invasiveness of monocytes. Blood 95: 3964-3969
7. Okunishi, K., M. Dohi, K. Nakagome, R. Tanaka, S. Mizuno, K. Matsumoto, J. Miyazaki, T. Nakamura, and K. Yamamoto. 2005. A novel role of hepatocyte growth factor as an immune regulator through suppressing dendritic cell function. J. Immunol. 175: 4745-4753
8. Futamatsu, H., J. Suzuki, S. Mizuno, N. Koga, S. Adachi, H. Kosuge, Y. Maejima, K. Hirao, T. Nakamura, and M. Isobe. 2005. Hepatocyte growth factor ameliorates the progress ion of experimental autoimmune myocarditis: a potential role for induction of T helper 2 cytokines. Circ. Res. 96: 823-830
9. Kuroiwa, T., T. Iwasaki, T. Imado, M. Sekiguchi, J. Fujimoto, and H. Sano. 2006. Hepatocyte growth factor prevents lupus nephritis in a murine lupus model of chronic graft-versus-host disease. Arthritis Res. Ther. 8: R123
10. Okunishi, K., M. Dohi, K. Fujio, K. Nakagome, Y. Tabata, T. Okasora, M. Seki, M. Shibuya, M. Imamura, H. Harada, et al. 2007. Hepatocyte growth factor significantly suppresses collagen-induced arthritis in mice. J. Immunol. 179: 5504-5513
11. Benkhoucha, M., M. L. Santiago-Raber, G. Schneiter, M. Chofflon, H. Funakoshi, T. Nakamura, and P. H. Lalive. 2010. Hepatocyte growth factor inhibits CNS autoimmunity by inducing tolerogenic dendritic cells an d CD25+ Foxp3+ regulatory T cells. Proc. Natl. Acad. Sci. USA 107: 6424-6429
12. Rutella, S., G. Bonanno, A. Procoli, A. Mariotti, D. G. de Ritis, A. Curti, S. Danese, G. Pessina, S. Pando lfi, F. Natoni, et al. 2006. Hepatocyte growth factor favors monocyte differentiation into regulatory interleukin (IL)-10++IL-12low/neg accessory cells with dendritic-cell features. Blood 108: 218-227
13. Maina, F., and R. Klein. 1999. Hepatocyte growth factor, a versatile signal for developing neurons. Nat. Neurosci. 2: 213-217
14. Lalive, P. H., R. Paglinawan, G. Biollaz, E. A. Kappos, D. P. Leone, U. Malipiero, J. B. Relvas, M. Moransard, T. Suter, and A. Fontana. 2005. TGFbeta-treated microglia induce oligodendrocyte precursor cell chemotaxis through the HGF-c-Met pathway. Eur. J. Immunol. 35: 727-737
15. Kitamura, K., A. Iwanami, M. Nakamura, J. Yamane, K. Watanabe, Y. Suzuki, D. Miyazawa, S. Shibata, H. Funakoshi, S. Miyatake, et al. 2007. Hepatocyte growth factor promo tes endogenous repair and functional recovery after spinal cord injury. J. Neurosci. Res. 85: 2332-2342
16. Bai, L., D. P. Lennon, A. I. Caplan, A. DeChant, J. Hecker, J. Kranso, A. Zaremba, and R. H. Miller. 2012. Hepatocyte growth factor mediates mesenchymal stem cell-induced recovery in multiple sclerosis models. Nat. Neurosci. 15: 862-870
17. Molnarfi, N., M. Benkhoucha, K. Bjarnadóttir, C. Juillard, and P. H. Lalive. 2012. Interferon-b induces hepatocyte growth factor in monocytes of multiple sclerosis patients. PLoS ONE 7: e49882
18. M€ uller, A. M., E. Jun, H. Conlon, and S. A. Sadiq. 2012. Cerebrospinal hepatocyte growth factor levels correlate negatively with disease activity in multiple sclerosis. J. Neuroimmunol. 251: 80-86
19. Ayroldi, E., and C. Riccardi. 2009. G lucocorticoid-induced leucine zipper (GILZ): a new important mediator of glucocorticoid action. FASEB J. 23: 3649-3658
20. Bruscoli, S., E. Velardi, M. Di Sante, O. Bereshchenko, A. Venanzi, M. Coppo, V. Berno, M. G. Mameli, R. Colella, A. Cavaliere, and C. Riccardi. 2012. Long glucocorticoid-induced leucine zipp er (L-GILZ) protein interacts with ras protein pathway and contributes to spermatogenesis control. J. Biol. Chem. 287: 1242-1251.
21. Ozeki M.,T. Ishii,Y. Hirano,Y. Tabata, 2001, Controlled release of hepatocyte growth factor from gelatin hydrogels based on hydrogel degradation, J. Drug Target, 9, 461-471.
22. Hamdi, H., V. Godot, M. C. Maillot, M. V. Prejean, N. Cohen, R. Krzysiek, F. M. Lemoine, W. Zou, and D. Emilie. 2007. Induction of antigen-specific regulatory T lymphocytes by human dendritic cells expressing the glucocorticoid-induced leucine zipper. Blood 110: 211-219
23. Grewal, I. S., H. G. Foellmer, K. D. Grewal, J. Xu, F. Hardardottir, J. L. Baron, C. A. Janeway, Jr., and R. A. Flavell. 1996. Requirement for CD40 ligand in costimulation ind uction, T cell activation, and experimental allergic encephalomyelitis. Science 273: 1864-1867
24. Yogev, N., F. Frommer, D. Lukas, K. Kautz-Neu, K. Karram, D. Ielo, E. von Stebut, H. C. Probs t, M. van den Broek, D. Riethmacher, et al. 2012. Dendritic cells ameliorate autoimmunity in the CNS by controlling the homeostasis of PD-1 receptor(+) regulatory T cells. Immunity 37: 264-275
25. C ohen, N., E. Mouly, H. Hamdi, M. C. Maillot, M. Pallardy, V. Godot, F. Capel, A. Balian, S. Naveau, P. Galanaud, et al. 2006. GILZ expression in human dendritic cells redirects their maturation and prevents antigen-specific T lymphocyte response. Blood 107: 2037-2044
26. Singhal, E., P. Kumar, and P. Sen. 2011. A novel role for Bruton's tyrosine kinase in hepatocyte growth factor-mediated immunoregulation of dendritic cells. J. Biol. Chem. 286: 32054-32063
27. Berrebi, D., S. Bruscoli, N. Cohen, A. Foussat, G. Migliorati, L. Bouchet-Delbos, M. C. Maillot, A. Portier, J. Couderc, P. Gala naud, et al. 2003. Synthesis of glucocorticoid-induced leucine zipper (GILZ) by macrophages: an antiinflammatory and immunosuppressive mechanism shared by glucocorticoids and IL-10. Blood 101: 729-738
28. Goverman, J. 2009. Autoimmune T cell responses in the central nervous system. Nat. Rev. Immunol. 9: 393-407