KDEL-retained antigen in B lymphocytes induces a proinflammatory response: A possible role for endoplasmic reticulum stress in adaptive T cell immunity

Journal of Immunology

Volumn 181, Issue 1, 2008, Pages 256-264

  Wheeler, Matthew C ^a,b   Rizzi, Marta ^a   Sasik, Roman ^a,c   Almanza, Gonzalo ^a   Hardiman, Gary ^a,c   Zanetti, Maurizio ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b Biomedical Sciences Program   (United States)

^c Biomedical Genomics Microarray   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 23P19; THAPSIGARGIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL STRESS; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENDOPLASMIC RETICULUM; INFLAMMATION; INTERFERON PRODUCTION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CELL CULTURE; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETICS; GENOME; IMMUNITY; IMMUNOLOGY; METABOLISM; PROTEIN MOTIF; PROTEIN TRANSPORT; T LYMPHOCYTE; TRANSGENE; UPREGULATION;

AMINO ACID MOTIFS; ANIMALS; ANTIGEN-PRESENTING CELLS; ANTIGENS; B-LYMPHOCYTES; CELLS, CULTURED; ENDOPLASMIC RETICULUM; GENE EXPRESSION PROFILING; GENOME; IMMUNITY; INFLAMMATION; INTERLEUKIN-23 SUBUNIT P19; MICE; MICE, INBRED C57BL; PROTEIN TRANSPORT; T-LYMPHOCYTES; TRANSCRIPTION, GENETIC; TRANSGENES; UP-REGULATION;

EID: 47949100421     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.1.256     Document Type: Article

References (55)

1. Paul, W. E. 1998. Fundamental lmmunology. 4th Ed. Raven Press, New York.
2. Rudensky, A., P. Preston-Hurlburt, S. C. Hong, A. Barlow, and C. Janeway, Jr. 1991. Sequence analysis of peptides bound to MHC class II molecules. Nature 353: 622-627.
3. Chicz, R., R. Urban, W. Lane, J. Gorga, L. Stem, D. Vignali, and J. Strominger. 1992. Predominant naturally processed peptides bound to HLA-DR1 are derived from MHC-related molecules and are heterogeneous in size. Nature 358: 764-768.
4. Nuchtern, J. G., W. E. Biddison, and R. D. Klausner. 1990. Class II MHC molecules can use the endogenous pathway of antigen presentation. Nature 343: 74-76.
5. Brooks, A., S. Hartley, L. Kjer-Nielsen, J. Perera, C. C. Goodnow, A. Basten, and J. McCIuskey. 1991. Class II-restricted presentation of an endogenously derived immunodominant T-cell determinant of hen egg lysozyme. Proc. Nat!. Acad. Sci. USA 88: 3290-3294.
6. Weiss, S., and B. Bogen. 1991. MHC class II-restricted presentation of intracel-lular antigen. Cell 64: 767-776.
7. Malnati, M., M. Marti, T. LaVaute, D. Jaraquemada, W. Biddison, R. De Mars, and E. Long. 1992. Processing pathways for presentation of cytosolic antigen to MHC class II-restricted T cells. Nature 357: 702-704.
8. Adorini, L., J. C. Guery, S. Fuchs, V. Ortiz-Navarrete, G. J. Hammerling, and F. Momburg. 1993. Processing of endogenously synthesized hen egg-white lysozyme retained in the endoplasmie reticulum or in secretory form gives rise to a similar but not identical set of epitopes recognized by class II-restricted T cells. J. Immunol. 151: 3576-3586.
9. Nimmerjahn, F., S. Milosevic, U. Behrends, E. M. Jaffee, D. M. Pardoll, G. W. Bornkamm, and J. Mautner. 2003. Major histocompatibility complex class II-restricted presentation of a cytosolic antigen by autophagy. Eur. J. Immunol. 33: 1250-1259.
10. Zhou, D., P. Li, Y. Lin, J. M. Lott, A. D. Hislop, D. H. Canaday, R. R. Brutkiewicz, and J. S. Blum. 2005. Lamp-2a facilitates MHC class II presentation of cytoplasmic antigens. Immunity 22: 571-581.
11. Tewari, M. K., G. Sinnathamby, D. Rajagopal, and L. C. Eisenlohr. 2005. A cytosolic pathway for MHC class II-restricted antigen processing that is protea-some and TAP dependent. Nat. Immunol. 6: 287-294.
12. Dengjel, J., O. Schoor, R. Fischer, M. Reich, M. Kraus, M. Muller, K. Kreymborg, F. AHenberend, J. Brandenburg, H. Kalbacher, R. Brock, C. Driessen, H. G. Rammensee, and S. Stevanovic. 2005. Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc. Nail. Acad. Sci. USA 102: 7922-7927.
13. Bluestone, J. A., R. Khattri, and G. A. van Seventer. 1999. Accessory Molecules. In Fundamental Immunology, 4th Ed. W. E. Paul, ed. Raven Press, New York. 449-478.
14. Gramaglia, I., A. Jember, S. D. Pippig, A. D. Weinberg, N. Killeen, and M. Croft. 2000. The OX40 costimulatory receptor determines the development of CD4 memory by regulating primary clonal expansion. J. Immunol. 165: 3043-3050.
15. Linton, P. J., B. Bautista, E. Biederman, E. S. Bradley, J. Harbertson, R. M. Kondrack, R. C. Padrick, and L. M. Bradley. 2003. Costimulation via OX40L expressed by B cells is sufficient to determine the extent of primary CD4 cell expansion and Th2 cytokine secretion in vivo. J. Exp. Med. 197: 875-883.
16. Iwakoshi, N. N., A. H. Lee, P. Vallabhajosyula, K. L. Otipoby, K. Rajewsky, and L. H. Glimcher. 2003. Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat. Immunol. 4: 321-329.
17. Schroder, M., and R. J. Kaufman. 2005. ER stress and the unfolded protein - response. Mutat. Res. 569: 29-63.
18. Reimold, A. M., N. N. Iwakoshi, J. Manis, P. Vallabhajosyula, E. Szomolanyi-Tsuda, E. M. Gravallese, D. Friend, M. J. Grusby, F. Alt, and L. H. Glimcher. 2001. Plasma cell differentiation requires the transcription factor XBP-1. Nature 412: 300-307.
19. Filaci, G., M. Gerloni, M. Rizzi, P. Castiglioni, H. D. Chang, M. C. Wheeler, R. Fiocca, and M. Zanetli. 2004. Spontaneous transgenesis of human B lymphocytes. Gene Ther. 11: 42-51.
20. Gerloni, M., M. Rizzi, P. Castiglioni, and M. Zanetti. 2004. T cell immunity using transgenic B lymphocytes. Proc. Nail. Acad. Sci. USA 101: 3892-3897.
21. Zanetti, M. 1992. Antigenized antibodies. Nature 355: 466-477.
22. Sollazzo, M., D. Castiglia, R. Billetta, A. Tramontano, and M. Zanetti. 1990. Structural definition by antibody engineering of an idiotypic determinant. Protein Eng. 3: 531-539.
23. Sollazzo, M., R. Billetta, and M. Zanetti. 1990. Expression of an exogenous peptide epitope genetically engineered in the variable domain of an immuno-globulin: implications for antibody and peptide folding. Protein Eng. 4: 215-220.
24. Xiong, S., M. Gerloni, and M. Zanetti. 1997. Engineering vaccines with heter-ologous B and T cell epitopes using immunoglobulin genes. Nat. Biotechnol. 15: 882-886.
25. Eberwine, J., H. Yeh, K. Miyashiro, Y. Cao, S. Nair, R. Finnell, M. Zettel, and P. Coleman. 1992. Analysis of gene expression in single live neurons. Proc. Nail. Acad. Sci. USA 89: 3010-3014.
26. Fan, J. B., J. M. Yeakley, M. Bibikova, E. Chudin, E. Wickham, J. Chen, D. Doucet, P. Rigault, B. Zhang, R. Shen, C. McBride, H. R. Li, X. D. Fu, A. Oliphant, D. L. Barker, and M. S. Chee. 2004. A versatile assay for high-throughput gene expression profiling on universal array matrices. Genome Res. 14: 878-885.
27. Galinsky, V. L. 2003. Automatic registration of microarray images. II. Hexagonal grid. Bioinformatics 19: 1832-1836.
28. Persic, L., M. Righi, A. Roberts, H. R. Hoogenboom, A. Cattaneo, and A. Bradbury. 1997. Targeting vectors for intracellular immunization. Gene 187: 1-8.
29. Rudensky, A., S. Rath, P. Preston-Hurlburt, D. Murphy, and C. Janeway, Jr. 1991. On the complexity of self. Nature 353: 660-662.
30. Krieg, A. M., A. K. Yi, S. Matson, T. J. Waldschmidt, G. A. Bishop, R. Teasdale, G. A. Koretzky, and D. M. Klinman. 1995. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374: 546-549.
31. Cortez-Gozalez, X., I. Pellicciotta, M. Gerloni, M. C. Wheeler, P. Castiglioni, P. Lenert, and M. Zanetti. 2006. TLR9 independent activation of B lymphocytes by bacterial DNA. DNA Cell Biology 27: 253-261.
32. Heit, A., T. Maurer, H. Hochrein, S. Bauer, K. M. Huster, D. H. Busch, and H. Wagner. 2003. Cutting edge: toll-like receptor 9 expression is not required for CpG DNA-aided cross-presentation of DNA-conjugated antigens but essential for cross-priming of CD8 T cells. J. Immunol. 170: 2802-2805.
33. Garside, P., E. Ingulli, R. R. Merica, J. G. Johnson, R. J. Noelle, and M. K. Jenkins. 1998. Visualization of specific B and T lymphocyte interactions in the lymph node. Science 281: 96-99.
34. Dorner, A. J., L. C. Wasley, P. Raney, S. Haugejorden, M. Green, and R. J. Kaufman. 1990. The stress response in Chinese hamster ovary cells: regulation of ERp72 and protein disulfide isomerase expression and secretion. J. Biol. Chem. 265: 22029-22034.
35. Klein, U., S. Casola, G. Cattoretti, Q. Shen, M. Lia, T. Mo, T. Ludwig, K. Rajewsky, and R. Dalla-Favera. 2006. Transcription factor IRF4 controls plasma cell differentiation and class-switch recombination. Nat. Immunol. 7: 773-782.
36. Oppmann, B., R. Lesley, B. Blom, J. C. Timans, Y. Xu, B. Hunte, F. Vega, N. Yu, J. Wang, K. Singh, et al. 2000. Novel pl9 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13: 715-725.
37. Yamamoto, K., H. Hamada, H. Shinkai, Y. Kohno, H. Koseki, and T. Aoe. 2003. The KDEL receptor modulates the endoplasmic reticulum stress response through mitogen-activated protein kinase signaling cascades. J. Biol. Chem. 278: 34525-34532.
38. Gass, J. N., N. M. Gifford, and J. W. Brewer. 2002. Activation of an unfolded protein response during differentiation of antibody-secreting B cells. J. Biol. Chem. 277: 49047-49054.
39. van Anken, E., E. P. Romijn, C. Maggioni, A. Mezghrani, R. Sitia, I. Braakman, and A. J. Heck. 2003. Sequential waves of functionally related proteins are expressed when B cells prepare for antibody secretion. Immunity 18: 243-253.
40. Skalet, A. H., J. A. Isler, L. B. King, H. P. Harding, D. Ron, and J. G. Monroe. 2005. Rapid B cell receptor-induced unfolded protein response in nonsecretory B cells correlates with pro versus antiapoptotic cell fate. J. Biol. Chem. 280: 39762-39771.
41. Zanetti, M., P. Castiglioni, M. Rizzi, M. Wheeler, and M. Gerloni. 2004. B lymphocytes as APC based genetic vaccines. Immunol. Rev. 199: 264-278.
42. Hung, J. H., I. J. Su, H. Y. Lei, H. C. Wang, W. C. Lin, W. T. Chang, W. Huang, W. C. Chang, Y. S. Chang, C. C. Chen, and M. D. Lai. 2004. Endoplasmic reticulum stress stimulates the expression of cyclooxygenase-2 through activation of NF-κB and pp38 mitogen-activated protein kinase. J. Biol. Chem. 279: 46384-46392.
43. Majors, A. K., R. C. Austin, C. A. de la Motte, R. E. Pyeritz, V. C. Hascall, S. P. Kessler, G. Sen, and S. A. Strong. 2003. Endoplasmic reticulum stress induces hyaluronan deposition and leukocyte adhesion. J. Biol. Chem. 278: 47223-47231.
44. Bertolotti, A., X. Wang, I. Novoa, R. Jungreis, K. Schlessinger, J. H. Cho, A. B. West, and D. Ron. 2001. Increased sensitivity to dextran sodium sulfate colitis in IRElβ-deficient mice. J. Clin. Invest. 107: 585-593.
45. Salek-Ardakani, S., J. Song, B. S. Halteman, A. G. Jember, H. Akiba, H. Yagita, and M. Croft. 2003. OX40 (CD134) controls memory T helper 2 cells that drive lung inflammation. J. Exp. Med. 198: 315-324.
46. Dawicki, W., E. M. Bertram, A. H. Sharpe, and T. H. Watts. 2004. 4-1BB and OX40 act independently to facilitate robust CD8 and CD4 recall responses. J. Immunol. 173:5944-5951.
47. Zanetti, M., and G. Franchini. 2006. T cell memory and protective immunity by vaccination: is more better? Trends Immunol. 27: 511-517.
48. Xue, X., J. H. Piao, A. Nakajima, S. Sakon-Komazawa, Y. Kojima, K. Mori, H. Yagita, K. Okumura, H. Harding, and H. Nakano. 2005. Tumor necrosis factor a (TNF-α) induces the unfolded protein response (UPR) in a reactive oxygen species (ROS)-dependent fashion, and the UPR counteracts ROS accumulation by TNF-α. J. Biol. Chem. 280: 33917-33925.
49. Shkoda, A., P. A. Ruiz, H. Daniel, S. C. Kim, G. Rogler, R. B. Sartor, and D. Haller. 2007. Interleukin-10 blocked endoplasmic reticulum stress in intestinal epithelial cells: impact on chronic inflammation. Gastroenterology 132: 190-207.
50. Ruiz, P. A., A. Shkoda, S. C. Kim, R. B. Sartor, and D. Haller. 2006. IL-10 gene-deficient mice lack TGF-β Smad-mediated TLR2 degradation and fail to inhibit proi-nflammatory gene expression in intestinal epithelial cells under conditions of chronic inflammation. Ann. NY Acad. Sci. 1072: 389-394.
51. Ciccaglione, A. R., A. Costantino, E. Tritarelli, C. Marcantonio, M. Equestre, N. Marziliano, and M. Rapicetta. 2005. Activation of endoplasmic reticulum stress response by hepatitis C virus proteins. Arch. Virol. 150: 1339-1356.
52. Lee, A. S. 2001. The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem. Sci. 26: 504-510.
53. Hue, S., P. Ahem, S. Buonocore, M. C. Kullberg, D. J. Cua, B. S. McKenzie, F. Powrie, and K. J. Maloy. 2006. Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J. Exp. Med. 203: 2473-2483.
54. Wozniak, T. M., A. A. Ryan, and W. J. Britton. 2006. Interleukin-23 restores immunity to Mycobacterium tuberculosis infection in IL-12p40-deficient mice and is not required for the development of IL-17-secreting T cell responses. J. Immunol. 177: 8684-8692.
55. Wiekowski. M. T., M. W. Leach, E. W. Evans, L. Sullivan, S. C. Chen, G. Vassileva, J. F. Bazan, D. M. Gorman, R. A. Kastelein, S. Narula, and S. A. Lira. 2001. Ubiquitous transgenic expression of the IL-23 subunit pl9 induces multiorgan inflammation, runting, infertility, and premature death. J. Immunol. 166: 7563-7570.