A soluble form of IL-27Rα is a natural IL-27 antagonist

Journal of Immunology

Volumn 192, Issue 11, 2014, Pages 5382-5389

  Dietrich, Céline ^a   Candon, Sophie ^a,b   Ruemmele, Frank M ^c   Devergne, Odile ^a  

^a CNRS   (France)

^b INSERM   (France)

^c HÔPITAL NECKER ENFANTS MALADES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ILOMASTAT; INTERLEUKIN 27; INTERLEUKIN RECEPTOR; METALLOPROTEINASE; RECOMBINANT PROTEIN; SOLUBLE INTERLEUKIN 27 RECEPTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME INHIBITOR; UNCLASSIFIED DRUG;

ARTICLE; BIOCHEMISTRY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CROHN DISEASE; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; IMMUNOMODULATION; IMMUNOREGULATION; IN VITRO STUDY; INNATE IMMUNITY; INTRACELLULAR SIGNALING; MAJOR CLINICAL STUDY; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN GLYCOSYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN SYNTHESIS INHIBITION; T LYMPHOCYTE ACTIVATION;

ADULT; ANIMALS; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; COS CELLS; CROHN DISEASE; FEMALE; HUMANS; INTERLEUKINS; LYMPHOCYTE ACTIVATION; LYMPHOCYTES; MALE; RECEPTORS, INTERLEUKIN; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS;

EID: 84901264863     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303435     Document Type: Article

References (41)

1. Devergne, O., M. Hummel, H. Koeppen, M. M. Le Beau, E. C. Nathanson, E. Kieff, and M. Birkenbach. 1996. A novel interleukin-12 p40-related protein induced by latent Epstein-Barr virus infection in B lymphocytes. J. Virol. 70: 1143-1153.
2. Pflanz, S., J. C. Timans, J. Cheung, R. Rosales, H. Kanzler, J. Gilbert, L. Hibbert, T. Churakova, M. Travis, E. Vaisberg, et al. 2002. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(+) T cells. Immunity 16: 779-790.
3. Devergne, O., A. Coulomb-L'Herminé, F. Capel, M. Moussa, and F. Capron. 2001. Expression of Epstein-Barr virus-induced gene 3, an interleukin-12 p40- related molecule, throughout human pregnancy: involvement of syncytiotrophoblasts and extravillous trophoblasts. Am. J. Pathol. 159: 1763-1776.
4. Coulomb-L'Herminé, A., F. Larousserie, S. Pflanz, E. Bardel, R. A. Kastelein, and O. Devergne. 2007. Expression of interleukin-27 by human trophoblast cells. Placenta 28: 1133-1140.
5. Hunter, C. A., and R. Kastelein. 2012. Interleukin-27: balancing protective and pathological immunity. Immunity 37: 960-969.
6. Hall, A. O., J. S. Silver, and C. A. Hunter. 2012. The immunobiology of IL-27. Adv. Immunol. 115: 1-44.
7. Pflanz, S., L. Hibbert, J. Mattson, R. Rosales, E. Vaisberg, J. F. Bazan, J. H. Phillips, T. K. McClanahan, R. de Waal Malefyt, and R. A. Kastelein. 2004. WSX-1 and glycoprotein 130 constitute a signal-transducing receptor for IL-27. J. Immunol. 172: 2225-2231.
8. Shimozato, O., A. Sato, K. Kawamura, M. Chiyo, G. Ma, Q. Li, and M. Tagawa. 2009. The secreted form of p28 subunit of interleukin (IL)-27 inhibits biological functions of IL-27 and suppresses anti-allogeneic immune responses. Immunology 128:e816-e825.
9. Stumhofer, J. S., E. D. Tait, W. J. Quinn, III, N. Hosken, B. Spudy, R. Goenka, C. A. Fielding, A. C. O'Hara, Y. Chen, M. L. Jones, et al. 2010. A role for IL- 27p28 as an antagonist of gp130-mediated signaling. Nat. Immunol. 11: 1119- 1126.
10. Garbers, C., B. Spudy, S. Aparicio-Siegmund, G. H. Waetzig, J. Sommer, C. Hölscher, S. Rose-John, J. Grötzinger, I. Lorenzen, and J. Scheller. 2013. An interleukin-6 receptor-dependent molecular switch mediates signal transduction of the IL-27 cytokine subunit p28 (IL-30) via a gp130 protein receptor homodimer. J. Biol. Chem. 288: 4346-4354.
11. Levine, S. J. 2008. Molecular mechanisms of soluble cytokine receptor generation. J. Biol. Chem. 283: 14177-14181.
12. Bergamaschi, C., M. Rosati, R. Jalah, A. Valentin, V. Kulkarni, C. Alicea, G. M. Zhang, V. Patel, B. K. Felber, and G. N. Pavlakis. 2008. Intracellular interaction of interleukin-15 with its receptor alpha during production leads to mutual stabilization and increased bioactivity. J. Biol. Chem. 283: 4189-4199.
13. Lundström, W., S. Highfill, S. T. Walsh, S. Beq, E. Morse, I. Kockum, L. Alfredsson, T. Olsson, J. Hillert, and C. L. Mackall. 2013. Soluble IL7Ra potentiates IL-7 bioactivity and promotes autoimmunity. Proc. Natl. Acad. Sci. USA 110: E1761-E1770.
14. Jostock, T., J. Mullberg, S. Özbek, R. Atreya, G. Blinn, N. Voltz, M. Fischer, M. F. Neurath, and S. Rose-John. 2001. Soluble gp130 is the natural inhibitor of soluble interleukin-6 receptor transsignaling responses. Eur. J. Biochem. 268: 160-167.
15. Scheller, J., B. Schuster, C. Hölscher, T. Yoshimoto, and S. Rose-John. 2005. No inhibition of IL-27 signaling by soluble gp130. Biochem. Biophys. Res. Commun. 326: 724-728.
16. Hashimoto, Y., M. Kurita, and M. Matsuoka. 2009. Identification of soluble WSX-1 not as a dominant-negative but as an alternative functional subunit of a receptor for an anti-Alzheimer's disease rescue factor Humanin. Biochem. Biophys. Res. Commun. 389: 95-99.
17. Hashimoto, Y., M. Kurita, S. Aiso, I. Nishimoto, and M. Matsuoka. 2009. Humanin inhibits neuronal cell death by interacting with a cytokine receptor complex or complexes involving CNTF receptor a/WSX-1/gp130. Mol. Biol. Cell 20: 2864-2873.
18. Charlot-Rabiega, P., E. Bardel, C. Dietrich, R. Kastelein, and O. Devergne. 2011. Signaling events involved in interleukin 27 (IL-27)-induced proliferation of human naive CD4+ T cells and B cells. J. Biol. Chem. 286: 27350-27362.
19. Larousserie, F., P. Charlot, E. Bardel, J. Froger, R. A. Kastelein, and O. Devergne. 2006. Differential effects of IL-27 on human B cell subsets. J. Immunol. 176: 5890-5897.
20. Nagai, T., O. Devergne, T. F. Mueller, D. L. Perkins, J. M. van Seventer, and G. A. van Seventer. 2003. Timing of IFN-b exposure during human dendritic cell maturation and naive Th cell stimulation has contrasting effects on Th1 subset generation: a role for IFN-b-mediated regulation of IL-12 family cytokines and IL-18 in naive Th cell differentiation. J. Immunol. 171: 5233-5243.
21. Bergamaschi, C., J. Bear, M. Rosati, R. K. Beach, C. Alicea, R. Sowder, E. Chertova, S. A. Rosenberg, B. K. Felber, and G. N. Pavlakis. 2012. Circulating IL-15 exists as heterodimeric complex with soluble IL-15Ra in human and mouse serum. Blood 120: e1-e8.
22. Sprecher, C. A., F. J. Grant, J. W. Baumgartner, S. R. Presnell, S. K. Schrader, T. Yamagiwa, T. E. Whitmore, P. J. O'Hara, and D. F. Foster. 1998. Cloning and characterization of a novel class I cytokine receptor. Biochem. Biophys. Res. Commun. 246: 82-90.
23. Chen, Q., N. Ghilardi, H. Wang, T. Baker, M.-H. Xie, A. Gurney, I. S. Grewal, and F. J. de Sauvage. 2000. Development of Th1-type immune responses requires the type I cytokine receptor TCCR. Nature 407: 916-920.
24. Hayashida, K., A. H. Bartlett, Y. Chen, and P. W. Park. 2010. Molecular and cellular mechanisms of ectodomain shedding. Anat. Rec. 293: 925-937.
25. Wirtz, S., I. Tubbe, P. R. Galle, H. J. Schild, M. Birkenbach, R. S. Blumberg, and M. F. Neurath. 2006. Protection from lethal septic peritonitis by neutralizing the biological function of interleukin 27. J. Exp. Med. 203: 1875-1881.
26. Larousserie, F., S. Pflanz, A. Coulomb-L'Herminé, N. Brousse, R. Kastelein, and O. Devergne. 2004. Expression of IL-27 in human Th1-associated granulomatous diseases. J. Pathol. 202: 164-171.
27. Li, C. S., Q. Zhang, K. J. Lee, S. W. Cho, K. M. Lee, K. B. Hahm, S. C. Choi, K. J. Yun, H. T. Chung, and S. C. Chae. 2009. Interleukin-27 polymorphisms are associated with inflammatory bowel diseases in a Korean population. J. Gastroenterol. Hepatol. 24: 1692-1696.
28. Nimmo, E. R., J. G. Prendergast, M. C. Aldhous, N. A. Kennedy, P. Henderson, H. E. Drummond, B. H. Ramsahoye, D. C. Wilson, C. A. Semple, and J. Satsangi. 2012. Genome-wide methylation profiling in Crohn's disease identifies altered epigenetic regulation of key host defense mechanisms including the Th17 pathway. Inflamm. Bowel Dis. 18: 889-899.
29. NIDDK IBD Genetics ConsortiumBelgian-French IBD ConsortiumWellcome Trust CaseControl Consortium. 2009. Common variants at five new loci associated with early-onset inflammatory bowel disease. Nat. Genet. 41: 1335-1340.
30. Shibata, S., Y. Tada, N. Kanda, K. Nashiro, M. Kamata, M. Karakawa, T. Miyagaki, H. Kai, H. Saeki, Y. Shirakata, et al. 2010. Possible roles of IL-27 in the pathogenesis of psoriasis. J. Invest. Dermatol. 130: 1034-1039.
31. Shibata, S., Y. Tada, Y. Asano, K. Yanaba, M. Sugaya, T. Kadono, N. Kanda, S. Watanabe, and S. Sato. 2013. IL-27 activates Th1-mediated responses in imiquimod-induced psoriasis-like skin lesions. J. Invest. Dermatol. 133: 479-488.
32. Miyazaki, Y., H. Inoue, M. Matsumura, K. Matsumoto, T. Nakano, M. Tsuda, S. Hamano, A. Yoshimura, and H. Yoshida. 2005. Exacerbation of experimental allergic asthma by augmented Th2 responses in WSX-1-deficient mice. J. Immunol. 175: 2401-2407.
33. Chae, S. C., C. S. Li, K. M. Kim, J. Y. Yang, Q. Zhang, Y. C. Lee, Y. S. Yang, and H. T. Chung. 2007. Identification of polymorphisms in human interleukin-27 and their association with asthma in a Korean population. J. Hum. Genet. 52: 355-361.
34. Schmidt, C., T. Giese, B. Ludwig, I. Mueller-Molaian, T. Marth, S. Zeuzem, S. C. Meuer, and A. Stallmach. 2005. Expression of interleukin-12- related cytokine transcripts in inflammatory bowel disease: elevated interleukin-23p19 and interleukin-27p28 in Crohn's disease but not in ulcerative colitis. Inflamm. Bowel Dis. 11: 16-23.
35. Ansari, N. A., R. Kumar, S. Gautam, S. Nylén, O. P. Singh, S. Sundar, and D. Sacks. 2011. IL-27 and IL-21 are associated with T cell IL-10 responses in human visceral leishmaniasis. J. Immunol. 186: 3977-3985.
36. Tanida, S., H. Yoshitomi, M. Ishikawa, T. Kasahara, K. Murata, H. Shibuya, H. Ito, and T. Nakamura. 2011. IL-27-producing CD14(+) cells infiltrate inflamed joints of rheumatoid arthritis and regulate inflammation and chemotactic migration. Cytokine 55: 237-244.
37. Gonin, J., A. Carlotti, C. Dietrich, A. Audebourg, B. Radenen-Bussière, A. Caignard, M. F. Avril, M. C. Vacher-Lavenu, F. Larousserie, and O. Devergne. 2013. Expression of IL-27 by tumor cells in invasive cutaneous and metastatic melanomas. [Published erratum appears in 2013 PLoS One 8:11.] . PLoS One 8: e75694.
38. Honda, K., K. Nakamura, N. Matsui, M. Takahashi, Y. Kitamura, T. Mizutani, N. Harada, H. Nawata, S. Hamano, and H. Yoshida. 2005. T helper 1-inducing property of IL-27/WSX-1 signaling is required for the induction of experimental colitis. Inflamm. Bowel Dis. 11: 1044-1052.
39. Troy, A. E., C. Zaph, Y. Du, B. C. Taylor, K. J. Guild, C. A. Hunter, C. J. Saris, and D. Artis. 2009. IL-27 regulates homeostasis of the intestinal CD4+ effector T cell pool and limits intestinal inflammation in a murine model of colitis. J. Immunol. 183: 2037-2044.
40. Sasaoka, T., M. Ito, J. Yamashita, K. Nakajima, I. Tanaka, M. Narita, Y. Hara, K. Hada, M. Takahashi, Y. Ohno, et al. 2011. Treatment with IL-27 attenuates experimental colitis through the suppression of the development of IL-17-producing T helper cells. Am. J. Physiol. Gastrointest. Liver Physiol. 300: G568-G576.
41. Hanson, M. L., J. A. Hixon,W. Li, B. K. Felber,M. R. Anver, C. A. Stewart, B. M. Janelsins, S. K. Datta, W. Shen, M. H. McLean, and S. K. Durum. 2014. Oral delivery of IL-27 recombinant bacteria attenuates immune colitis in mice. Gastroenterology 146: 210-221.e13. doi: 10.1053/j.gastro. 2013.09.060.