B cells regulate CD4+ T cell responses to papain following B cell receptor-independent papain uptake

Journal of Immunology

Volumn 193, Issue 2, 2014, Pages 529-539

  Dwyer, Daniel F ^a   Woodruff, Matthew C ^b   Carroll, Michael C ^b   Austen, K Frank ^a   Gurish, Michael F ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD4 ANTIGEN; CELL PROTEIN; IMMUNOLOGICAL ADJUVANT; INDUCIBLE T CELL COSTIMULATOR LIGAND; INTERLEUKIN 4; PAPAIN; PROTEIN ANTIBODY; PROTEIN ICOS; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL ADHESION; CELL POLARITY; CELLULAR IMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; FOLLICULAR HELPER T CELL; HELPER CELL; IMMUNOREGULATION; INTERNALIZATION; LYMPH NODE CELL; LYMPHOCYTE DEPLETION; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; TH2 CELL;

ANIMALS; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; FLOW CYTOMETRY; IMMUNIZATION; INDUCIBLE T-CELL CO-STIMULATOR PROTEIN; INTERLEUKIN-4; LYMPH NODES; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; PAPAIN; PROTEIN BINDING; RECEPTORS, ANTIGEN, B-CELL; TH2 CELLS;

EID: 84904266454     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303247     Document Type: Article

References (44)

1. Grobe, K., W. M. Becker, M. Schlaak, and A. Petersen. 1999. Grass group I allergens (beta-expansins) are novel, papain-related proteinases. Eur. J. Biochem. 263: 33-40. (Pubitemid 29313835)
2. Chua, K. Y., G. A. Stewart, W. R. Thomas, R. J. Simpson, R. J. Dilworth, T. M. Plozza, and K. J. Turner. 1988. Sequence analysis of cDNA coding for a major house dust mite allergen, Der p 1. Homology with cysteine proteases. J. Exp. Med. 167: 175-182. (Pubitemid 18093701)
3. Gough, L., H. F. Sewell, and F. Shakib. 2001. The proteolytic activity of the major dust mite allergen Der p 1 enhances the IgE antibody response to a bystander antigen. Clin. Exp. Allergy 31: 1594-1598. (Pubitemid 32939467)
4. Finkelman, F. D., K. B. Madden, A. W. Cheever, I. M. Katona, S. C. Morris, M. K. Gately, B. R. Hubbard, W. C. Gause, and J. F. Urban, Jr. 1994. Effects of interleukin 12 on immune responses and host protection in mice infected with intestinal nematode parasites. J. Exp. Med. 179: 1563-1572. (Pubitemid 24129573)
5. McKerrow, J. H., C. Caffrey, B. Kelly, P. Loke, and M. Sajid. 2006. Proteases in parasitic diseases. Annu. Rev. Pathol. 1: 497-536.
6. Robinson, M. W., J. P. Dalton, and S. Donnelly. 2008. Helminth pathogen cathepsin proteases: it's a family affair. Trends Biochem. Sci. 33: 601-608.
7. Simpson, R. J., E. C. Nice, R. L. Moritz, and G. A. Stewart. 1989. Structural studies on the allergen Der p1 from the house dust mite Dermatophagoides pteronyssinus: similarity with cysteine proteinases. Protein Seq. Data Anal. 2: 17-21.
8. Sokol, C. L., G. M. Barton, A. G. Farr, and R. Medzhitov. 2008. A mechanism for the initiation of allergen-induced T helper type 2 responses. Nat. Immunol. 9: 310-318. (Pubitemid 351267328)
9. Sokol, C. L., N. Q. Chu, S. Yu, S. A. Nish, T. M. Laufer, and R. Medzhitov. 2009. Basophils function as antigen-presenting cells for an allergen-induced T helper type 2 response. Nat. Immunol. 10: 713-720.
10. + dermal dendritic cells drive T helper 2 cell-mediated immunity. Immunity 39: 733-743.
11. Tang, H., W. Cao, S. P. Kasturi, R. Ravindran, H. I. Nakaya, K. Kundu, N. Murthy, T. B. Kepler, B. Malissen, and B. Pulendran. 2010. The T helper type 2 response to cysteine proteases requires dendritic cell-basophil cooperation via ROS-mediated signaling. Nat. Immunol. 11: 608-617.
12. Ohnmacht, C., C. Schwartz, M. Panzer, I. Schiedewitz, R. Naumann, and D. Voehringer. 2010. Basophils orchestrate chronic allergic dermatitis and protective immunity against helminths. Immunity 33: 364-374.
13. Gao, Y., S. A. Nish, R. Jiang, L. Hou, P. Licona-Limón, J. S. Weinstein, H. Zhao, and R. Medzhitov. 2013. Control of T helper 2 responses by transcription factor IRF4-dependent dendritic cells. Immunity 39: 722-732.
14. Perrigoue, J. G., S. A. Saenz, M. C. Siracusa, E. J. Allenspach, B. C. Taylor, P. R. Giacomin, M. G. Nair, Y. Du, C. Zaph, N. van Rooijen, et al. 2009. MHC class II-dependent basophil-CD4+ T cell interactions promote T(H)2 cytokinedependent immunity. Nat. Immunol. 10: 697-705.
15. Yoshimoto, T., K. Yasuda, H. Tanaka, M. Nakahira, Y. Imai, Y. Fujimori, and K. Nakanishi. 2009. Basophils contribute to T(H)2-IgE responses in vivo via IL- 4 production and presentation of peptide-MHC class II complexes to CD4+ T cells. Nat. Immunol. 10: 706-712.
16. Kitamura, D., J. Roes, R. Kühn, and K. Rajewsky. 1991. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 350: 423-426. (Pubitemid 21912244)
17. Gommerman, J. L., D. Y. Oh, X. Zhou, T. F. Tedder, M. Maurer, S. J. Galli, and M. C. Carroll. 2000. A role for CD21/CD35 and CD19 in responses to acute septic peritonitis: a potential mechanism for mast cell activation. J. Immunol. 165: 6915-6921. (Pubitemid 32001162)
18. Silveira, P. A., J. Dombrowsky, E. Johnson, H. D. Chapman, D. Nemazee, and D. V. Serreze. 2004. B cell selection defects underlie the development of diabetogenic APCs in nonobese diabetic mice. J. Immunol. 172: 5086-5094. (Pubitemid 38456437)
19. Phan, T. G., I. Grigorova, T. Okada, and J. G. Cyster. 2007. Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat. Immunol. 8: 992-1000. (Pubitemid 47300014)
20. Mu, F. T., J. M. Callaghan, O. Steele-Mortimer, H. Stenmark, R. G. Parton, P. L. Campbell, J. McCluskey, J. P. Yeo, E. P. Tock, and B. H. Toh. 1995. EEA1, an early endosome-associated protein. EEA1 is a conserved alpha-helical peripheral membrane protein flanked by cysteine "fingers" and contains a calmodulin- binding IQ motif. J. Biol. Chem. 270: 13503-13511.
21. Palm, N. W., R. K. Rosenstein, S. Yu, D. D. Schenten, E. Florsheim, and R. Medzhitov. 2013. Bee venom phospholipase A2 induces a primary type 2 response that is dependent on the receptor ST2 and confers protective immunity. Immunity 39: 976-985.
22. Haynes, N. M., C. D. Allen, R. Lesley, K. M. Ansel, N. Killeen, and J. G. Cyster. 2007. Role of CXCR5 and CCR7 in follicular Th cell positioning and appearance of a programmed cell death gene-1high germinal center-associated subpopulation. J. Immunol. 179: 5099-5108.
23. León, B., A. Ballesteros-Tato, J. L. Browning, R. Dunn, T. D. Randall, and F. E. Lund. 2012. Regulation of T(H)2 development by CXCR5+ dendritic cells and lymphotoxin-expressing B cells. Nat. Immunol. 13: 681-690.
24. Choi, Y. S., R. Kageyama, D. Eto, T. C. Escobar, R. J. Johnston, L. Monticelli, C. Lao, and S. Crotty. 2011. ICOS receptor instructs T follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6. Immunity 34: 932-946.
25. McAdam, A. J., T. T. Chang, A. E. Lumelsky, E. A. Greenfield, V. A. Boussiotis, J. S. Duke-Cohan, T. Chernova, N. Malenkovich, C. Jabs, V. K. Kuchroo, et al. 2000. Mouse inducible costimulatory molecule (ICOS) expression is enhanced by CD28 costimulation and regulates differentiation of CD4+ T cells. J. Immunol. 165: 5035-5040.
26. Logue, E. C., S. Bakkour, M. M. Murphy, H. Nolla, and W. C. Sha. 2006. ICOS-induced B7h shedding on B cells is inhibited by TLR7/8 and TLR9. J. Immunol. 177: 2356-2364. (Pubitemid 44200996)
27. Nurieva, R. I., Y. Chung, D. Hwang, X. O. Yang, H. S. Kang, L. Ma, Y. H. Wang, S. S. Watowich, A. M. Jetten, Q. Tian, and C. Dong. 2008. Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 29: 138-149.
28. Pulendran, B., and D. Artis. 2012. New paradigms in type 2 immunity. Science 337: 431-435.
29. Liang, G., T. Barker, Z. Xie, N. Charles, J. Rivera, and K. M. Druey. 2012. Naive T cells sense the cysteine protease allergen papain through protease-activated receptor 2 and propel TH2 immunity. J. Allergy Clin. Immunol. 129: 1377-1386.e13.
30. Busso, N., M. Frasnelli, R. Feifel, B. Cenni, M. Steinhoff, J. Hamilton, and A. So. 2007. Evaluation of protease-activated receptor 2 in murine models of arthritis. Arthritis Rheum. 56: 101-107. (Pubitemid 46106182)
31. Porter, R. R. 1950. The formation of a specific inhibitor by hydrolysis of rabbit antiovalbumin. Biochem. J. 46: 479-484.
32. Schulz, O., B. J. Sutton, R. L. Beavil, J. Shi, H. F. Sewell, H. J. Gould, P. Laing, and F. Shakib. 1997. Cleavage of the low-affinity receptor for human IgE (CD23) by a mite cysteine protease: nature of the cleaved fragment in relation to the structure and function of CD23. Eur. J. Immunol. 27: 584-588. (Pubitemid 27110568)
33. Liang, H. E., R. L. Reinhardt, J. K. Bando, B. M. Sullivan, I. C. Ho, and R. M. Locksley. 2011. Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity. Nat. Immunol. 13: 58-66.
34. King, I. L., and M. Mohrs. 2009. IL-4-producing CD4+ T cells in reactive lymph nodes during helminth infection are T follicular helper cells. J. Exp. Med. 206: 1001-1007.
35. Marshall-Clarke, S., L. Tasker, M. P. Heaton, and R. M. Parkhouse. 2003. A differential requirement for phosphoinositide 3-kinase reveals two pathways for inducible upregulation of major histocompatibility complex class II molecules and CD86 expression by murine B lymphocytes. Immunology 109: 102-108. (Pubitemid 36577980)
36. Nutt, S. L., and D. M. Tarlinton. 2011. Germinal center B and follicular helper T cells: siblings, cousins or just good friends? Nat. Immunol. 12: 472-477.
37. Brown, J. A., R. G. Titus, N. Nabavi, and L. H. Glimcher. 1996. Blockade of CD86 ameliorates Leishmania major infection by down-regulating the Th2 response. J. Infect. Dis. 174: 1303-1308. (Pubitemid 26393910)
38. Dong, C., A. E. Juedes, U. A. Temann, S. Shresta, J. P. Allison, N. H. Ruddle, and R. A. Flavell. 2001. ICOS co-stimulatory receptor is essential for T-cell activation and function. Nature 409: 97-101. (Pubitemid 32098632)
39. Shilling, R. A., B. S. Clay, A. G. Tesciuba, E. L. Berry, T. Lu, T. V. Moore, H. S. Bandukwala, J. Tong, J. V. Weinstock, R. A. Flavell, et al. 2009. CD28 and ICOS play complementary non-overlapping roles in the development of Th2 immunity in vivo. Cell. Immunol. 259: 177-184.
40. Tafuri, A., A. Shahinian, F. Bladt, S. K. Yoshinaga, M. Jordana, A. Wakeham, L. M. Boucher, D. Bouchard, V. S. Chan, G. Duncan, et al. 2001. ICOS is essential for effective T-helper-cell responses. Nature 409: 105-109. (Pubitemid 32098634)
41. Watanabe, M., S. Watanabe, Y. Hara, Y. Harada, M. Kubo, K. Tanabe, H. Toma, and R. Abe. 2005. ICOS-mediated costimulation on Th2 differentiation is achieved by the enhancement of IL-4 receptor-mediated signaling. J. Immunol. 174: 1989-1996.
42. Tesciuba, A. G., S. Subudhi, R. P. Rother, S. J. Faas, A. M. Frantz, D. Elliot, J. Weinstock, L. A. Matis, J. A. Bluestone, and A. I. Sperling. 2001. Inducible costimulator regulates Th2-mediated inflammation, but not Th2 differentiation, in a model of allergic airway disease. J. Immunol. 167: 1996-2003. (Pubitemid 32747506)
43. Hernandez, H. J., Y. Wang, and M. J. Stadecker. 1997. In infection with Schistosoma mansoni, B cells are required for T helper type 2 cell responses but not for granuloma formation. J. Immunol. 158: 4832-4837. (Pubitemid 127483804)
44. Liu, Q., Z. Liu, C. T. Rozo, H. A. Hamed, F. Alem, J. F. Urban, Jr., and W. C. Gause. 2007. The role of B cells in the development of CD4 effector T cells during a polarized Th2 immune response. J. Immunol. 179: 3821-3830.