Caveolin-1-mediated negative signaling plays a critical role in the induction of regulatory dendritic cells by DNA and protein coimmunization

Journal of Immunology

Volumn 189, Issue 6, 2012, Pages 2852-2859

  Li, Jinyao ^a   Geng, Shuang ^a   Xie, Xiaoping ^b   Liu, Hu ^b   Zheng, Guoxing ^c   Sun, Xiaolin ^b   Zhao, Gan ^b   Wan, Ying ^d   Wu, Yuzhang ^d   Chen, Xuan ^b   Zhong, Yiwei ^a   Wang, Bin ^a,b  

^a FUDAN UNIVERSITY   (China)

^b CHINA AGRICULTURAL UNIVERSITY   (China)

^c UNIVERSITY OF ILLINOIS   (United States)

^d THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CAVEOLIN 1; CD40 ANTIGEN; DNA VACCINE; INTERLEUKIN 10; OVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; CAVEOLA; CELL CULTURE; CONTROLLED STUDY; DENDRITIC CELL; DNA SEQUENCE; DOWN REGULATION; ENDOCYTOSIS; FEMALE; IMMUNIZATION; IN VITRO STUDY; INFLAMMATORY DISEASE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; CAVEOLAE; CAVEOLIN 1; CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; COCULTURE TECHNIQUES; DENDRITIC CELLS; DOWN-REGULATION; ENDOCYTOSIS; FEMALE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; UP-REGULATION; VACCINES, DNA;

EID: 84866146367     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102828     Document Type: Article

References (34)

1. Cools, N., P. Ponsaerts, V. F. I. Van Tendeloo, and Z. N. Berneman. 2007. Balancing between immunity and tolerance: an interplay between dendritic cells, regulatory T cells, and effector T cells. J. Leukoc. Biol. 82: 1365-1374. (Pubitemid 350276946)
2. + T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J. Exp. Med. 192: 1213-1222.
3. Levings, M. K., S. Gregori, E. Tresoldi, S. Cazzaniga, C. Bonini, and M. G. Roncarolo. 2005. Differentiation of Tr1 cells by immature dendritic cells requires IL-10 but not CD25+CD4+ Tr cells. Blood 105: 1162-1169. (Pubitemid 40170889)
4. D'Ambrosio, A., M. Colucci, O. Pugliese, F. Quintieri, and M. Boirivant. 2008. Cholera toxin B subunit promotes the induction of regulatory T cells by preventing human dendritic cell maturation. J. Leukoc. Biol. 84: 661-668.
5. Lavelle, E. C., E. McNeela, M. E. Armstrong, O. Leavy, S. C. Higgins and K. H. G. Mills. 2003. Cholera toxin promotes the induction of regulatory T cells specific for bystander antigens by modulating dendritic cell activation. J. Immunol. 171: 2384-2392. (Pubitemid 37025545)
6. + regulatory T cells. Proc. Natl. Acad. Sci. USA 104: 2821-2826.
7. +regulatory T cell expansion resulting in suppression of autoimmune thyroiditis. Int. Immunol. 21: 269-282.
8. Jin,H.,Y. Kang,L.Zhao, C. Xiao,Y.Hu, R. She, Y. Yu,X.Du,G.Zhao,T.Ng, et al. 2008. Induction of adaptive T regulatory cells that suppress the allergic response by coimmunization of DNA and protein vaccines. J. Immunol. 180: 5360-5372.
9. Jin, H., Y. Kang, G. Zheng, Q. Xie, C. Xiao, X. Zhang, Y. Yu, K. Zhu, G. Zhao, F. Zhang, et al. 2005. Induction of active immune suppression by co-immunization with DNA- and protein-based vaccines. Virology 337: 183-191. (Pubitemid 40725451)
10. Kang, Y., H. Jin, G. Zheng, X. Du, C. Xiao, X. Zhang, S. Geng, X. Li, J. Wang, A. Chen, and B. Wang. 2007. Co-inoculation of DNA and protein vaccines induces antigen-specific T cell suppression. Biochem. Biophys. Res. Commun. 353: 1034-1039. (Pubitemid 46080401)
11. Li, J., H. Jin, F. Zhang, X. Du, G. Zhao, Y. Yu, and B. Wang. 2008. Treatment of autoimmune ovarian disease by co-administration with mouse zona pellucida protein 3 and DNA vaccine through induction of adaptive regulatory T cells. J. Gene Med. 10: 810-820. (Pubitemid 352003924)
12. Jin, H., C. Xiao, S. Geng, Y. Hu, R. She, Y. Yu, Y. Kang, and B. Wang. 2008. Protein/DNA vaccine-induced antigen-specific Treg confer protection against asthma. Eur. J. Immunol. 38: 2451-2463.
13. Li, J., H. Jin, A. Zhang, Y. Li, B. Wang, and F. Zhang. 2007. Enhanced contraceptive response by co-immunization of DNA and protein vaccines encoding the mouse zona pellucida 3 with minimal oophoritis in mouse ovary. J. Gene Med. 9: 1095-1103. (Pubitemid 350286415)
14. Wesemann, D. R., H. Qin, N. Kokorina, and E. N. Benveniste. 2004. TRADD interacts with STAT1-α and influences interferon-γ signaling. Nat. Immunol. 5: 199-207. (Pubitemid 38208362)
15. Oh, S.-W., C. I. Pae, D.-K. Lee, F. Jones, G. K. S. Chiang, H.-O. Kim, S.-H. Moon, B. Cao, C. Ogbu, K.-W. Jeong, et al. 2002. Tryptase inhibition blocks airway inflammation in a mouse asthma model. J. Immunol. 168: 1992-2000. (Pubitemid 34135803)
16. Carson, R. T., and D. A. Vignali. 1999. Simultaneous quantitation of 15 cytokines using a multiplexed flow cytometric assay. J. Immunol. Methods 227: 41-52. (Pubitemid 29408703)
17. Härtel, C., N. Adam, T. Strunk, P. Temming, M. Müller- Steinhardt, and C. Schultz. 2005. Cytokine responses correlate differentially with age in infancy and early childhood. Clin. Exp. Immunol. 142: 446-453. (Pubitemid 41719840)
18. Lamaze, C., and S. L. Schmid. 1995. The emergence of clathrin-independent pinocytic pathways. Curr. Opin. Cell Biol. 7: 573-580.
19. Bradley, J. R., D. R. Johnson, and J. S. Pober. 1993. Four different classes of inhibitors of receptor-mediated endocytosis decrease tumor necrosis factor-induced gene expression in human endothelial cells. J. Immunol. 150: 5544-5555. (Pubitemid 23180669)
20. Nandi, P. K., P. P. Van Jaarsveld, R. E. Lippoldt, and H. Edelhoch. 1981. Effect of basic compounds on the polymerization of clathrin. Biochemistry 20: 6706-6710.
21. Rothberg, K. G., J. E. Heuser, W. C. Donzell, Y. S. Ying, J. R. Glenney, and R. G. Anderson. 1992. Caveolin, a protein component of caveolae membrane coats. Cell 68: 673-682.
22. Sallusto, F., M. Cella, C. Danieli, and A. Lanzavecchia. 1995. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J. Exp. Med. 182: 389-400.
23. Nguyen, V. T., and E. N. Benveniste. 2002. Critical role of tumor necrosis factor-α and NF-κB in interferon-γ-induced CD40 expression in microglia/macrophages. J. Biol. Chem. 277: 13796-13803. (Pubitemid 34967983)
24. Qin, H., C. A. Wilson, S. J. Lee, X. Zhao, and E. N. Benveniste. 2005. LPS induces CD40 gene expression through the activation of NF-κB and STAT-1α in macrophages and microglia. Blood 106: 3114-3122. (Pubitemid 41565908)
25. Ohnuma, K., T. Yamochi, M. Uchiyama, K. Nishibashi, S. Iwata, O. Hosono, H. Kawasaki, H. Tanaka, N. H. Dang, and C. Morimoto. 2005. CD26 mediates dissociation of Tollip and IRAK-1 from caveolin-1 and induces upregulation of CD86 on antigen-presenting cells. Mol. Cell. Biol. 25: 7743-7757. (Pubitemid 41170135)
26. Lang, T., and A. Mansell. 2007. The negative regulation of Toll-like receptor and associated pathways. Immunol. Cell Biol. 85: 425-434. (Pubitemid 47367504)
27. Heeg, K., and A. Dalpke. 2003. TLR-induced negative regulatory circuits: role of suppressor of cytokine signaling (SOCS) proteins in innate immunity. Vaccine 21(Suppl. 2): S61-S67. (Pubitemid 36608882)
28. Yoshimura, A., T. Naka, and M. Kubo. 2007. SOCS proteins, cytokine signalling and immune regulation. Nat. Rev. Immunol. 7: 454-465. (Pubitemid 46834848)
29. Rhim, S. H., S. E. Millar, F. Robey, A. M. Luo, Y. H. Lou, T. Yule, P. Allen, J. Dean, and K. S. Tung. 1992. Autoimmune disease of the ovary induced by a ZP3 peptide from the mouse zona pellucida. J. Clin. Invest. 89: 28-35.
30. Engelman, J. A., C. Chu, A. Lin, H. Jo, T. Ikezu, T. Okamoto, D. S. Kohtz, and M. P. Lisanti. 1998. Caveolin-mediated regulation of signaling along the p42/44 MAP kinase cascade in vivo: a role for the caveolin-scaffolding domain. FEBS Lett. 428: 205-211. (Pubitemid 28319685)
31. Couet, J., S. Li, T. Okamoto, T. Ikezu, and M. P. Lisanti. 1997. Identification of peptide and protein ligands for the caveolin-scaffolding domain: implications for the interaction of caveolin with caveolae-associated proteins. J. Biol. Chem. 272: 6525-6533. (Pubitemid 27118133)
32. Ohnuma, K., T. Yamochi, M. Uchiyama, K. Nishibashi, N. Yoshikawa, N. Shimizu, S. Iwata, H. Tanaka, N. H. Dang, and C. Morimoto. 2004. CD26 upregulates expression of CD86 on antigen-presenting cells by means of caveolin-1. Proc. Natl. Acad. Sci. USA 101: 14186-14191. (Pubitemid 39305051)
33. Burns, K., J. Clatworthy, L. Martin, F. Martinon, C. Plumpton, B. Maschera, A. Lewis, K. Ray, J. Tschopp, and F. Volpe. 2000. Tollip, a new component of the IL-1RI pathway, links IRAK to the IL-1 receptor. Nat. Cell Biol. 2: 346-351.
34. Zhang, G., and S. Ghosh. 2002. Negative regulation of Toll-like receptor-mediated signaling by Tollip. J. Biol. Chem. 277: 7059-7065. (Pubitemid 34953094)