Human plasma cells express granzyme B

European Journal of Immunology

Volumn 44, Issue 1, 2014, Pages 275-284

  Xu, Wei ^a,b   Narayanan, Priya ^a   Kang, Ning ^a   Clayton, Sandra ^a   Ohne, Yoichiro ^a   Shi, Peiqing ^a   Herve, Marie Cecile ^a   Balderas, Robert ^c   Picard, Capucine ^d,e   Casanova, Jean Laurent ^f   Gorvel, Jean Pierre ^g,h   Oh, Sangkon ^a   Pascual, Virginia ^a   Banchereau, Jacques ^a  

^a BAYLOR INSTITUTE FOR IMMUNOLOGY RESEARCH   (United States)

^b Roche Pharma Research and Early Development   (Switzerland)

^c BD BIOSCIENCES   (United States)

^d IMAGINE INSTITUTE   (France)

^e HÔPITAL NECKER ENFANTS MALADES   (France)

^f ROCKEFELLER UNIVERSITY   (United States)

^g CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^h INSERM   (France)

Author keywords

B cells; Granzyme B (GrzB); Plasma cells

Indexed keywords

GRANZYME B; IMMUNOGLOBULIN KAPPA CHAIN; IMMUNOGLOBULIN LAMBDA CHAIN; INTERLEUKIN 15; INTERLEUKIN 21; MESSENGER RNA; STAT3 PROTEIN; GRANZYME; INTERLEUKIN DERIVATIVE;

ARTICLE; B LYMPHOCYTE ACTIVATION; B LYMPHOCYTE DIFFERENTIATION; CELL COMPARTMENTALIZATION; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOLOGY; ENDOSOME; ENZYME SYNTHESIS; GENETIC TRANSCRIPTION; HELPER CELL; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; IN VITRO STUDY; LYSOSOME; MACROPHAGE; PLASMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA TRANSLATION; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; CELL CULTURE; CELL DIFFERENTIATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PALATINE TONSIL; TRANSCRIPTION INITIATION;

CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; GENE EXPRESSION REGULATION; GRANZYMES; HUMANS; IMMUNOGLOBULIN KAPPA-CHAINS; IMMUNOGLOBULIN LAMBDA-CHAINS; INTERLEUKIN-15; INTERLEUKINS; LYMPHOCYTE ACTIVATION; MACROPHAGES; PALATINE TONSIL; PLASMA CELLS; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, HELPER-INDUCER; TRANSCRIPTIONAL ACTIVATION;

EID: 84892463258     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343711     Document Type: Article

References (51)

1. Batista, F. D. and Harwood, N. E., The who, how and where of antigen presentation to B cells. Nat. Rev. Immunol. 2009. 9: 15-27.
2. Suzuki, K., Grigorova, I., Phan, T. G., Kelly, L. M. and Cyster, J. G., Visualizing B cell capture of cognate antigen from follicular dendritic cells. J. Exp. Med. 2009. 206: 1485-1493.
3. Dubois, B., Bridon, J. M., Fayette, J., Barthelemy, C., Banchereau, J., Caux, C. and Briere, F., Dendritic cells directly modulate B cell growth and differentiation. J. Leukoc. Biol. 1999. 66: 224-230.
4. Litinskiy, M. B., Nardelli, B., Hilbert, D. M., He, B., Schaffer, A., Casali, P. and Cerutti, A., DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat. Immunol. 2002. 3: 822-829.
5. Qi, H., Egen, J. G., Huang, A. Y. and Germain, R. N., Extrafollicular activation of lymph node B cells by antigen-bearing dendritic cells. Science 2006. 312: 1672-1676.
6. Wykes, M., Pombo, A., Jenkins, C. and MacPherson, G. G., Dendritic cells interact directly with naive B lymphocytes to transfer antigen and initiate class switching in a primary T-dependent response. J. Immunol. 1998. 161: 1313-1319.
7. Carrasco, Y. R. and Batista, F. D., B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity 2007. 27: 160-171.
8. Junt, T., Moseman, E. A., Iannacone, M., Massberg, S., Lang, P. A., Boes, M., Fink, K. et al., Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 2007. 450: 110-114.
9. Phan, T. G., Grigorova, I., Okada, T. and Cyster, J. G., Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat. Immunol. 2007. 8: 992-1000.
10. Xu, W., Joo, H., Clayton, S., Dullaers, M., Herve, M. C., Blankenship, D., De La Morena, M. T. et al., Macrophages induce differentiation of plasma cells through CXCL10/IP-10. J. Exp. Med. 2012. 209: 1813-1823.
11. Lanzavecchia, A., Antigen-specific interaction between T and B cells. Nature 1985. 314: 537-539.
12. Garside, P., Ingulli, E., Merica, R. R., Johnson, J. G., Noelle, R. J. and Jenkins, M. K., Visualization of specific B and T lymphocyte interactions in the lymph node. Science 1998. 281: 96-99.
13. Okada, T., Miller, M. J., Parker, I., Krummel, M. F., Neighbors, M., Hartley, S. B., O'Garra, A. et al., Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells. PLoS Biol. 2005. 3: e150.
14. Allen, C. D., Okada, T., Tang, H. L. and Cyster, J. G., Imaging of germinal center selection events during affinity maturation. Science 2007. 315: 528-531.
15. Hauser, A. E., Junt, T., Mempel, T. R., Sneddon, M. W., Kleinstein, S. H., Henrickson, S. E., von Andrian, U. H. et al., Definition of germinal-center B cell migration in vivo reveals predominant intrazonal circulation patterns. Immunity 2007. 26: 655-667.
16. Schwickert, T. A., Lindquist, R. L., Shakhar, G., Livshits, G., Skokos, D., Kosco-Vilbois, M. H., Dustin, M. L. et al., In vivo imaging of germinal centres reveals a dynamic open structure. Nature 2007. 446: 83-87.
17. Junt, T., Scandella, E. and Ludewig, B., Form follows function: lymphoid tissue microarchitecture in antimicrobial immune defence. Nat. Rev. Immunol. 2008. 8: 764-775.
18. Shapiro-Shelef, M. and Calame, K., Regulation of plasma-cell development. Nat. Rev. Immunol. 2005. 5: 230-242.
19. Radbruch, A., Muehlinghaus, G., Luger, E. O., Inamine, A., Smith, K. G., Dorner, T. and Hiepe, F., Competence and competition: the challenge of becoming a long-lived plasma cell. Nat. Rev. Immunol. 2006. 6: 741-750.
20. Kunkel, E. J. and Butcher, E. C., Plasma-cell homing. Nat. Rev. Immunol. 2003. 3: 822-829.
21. Hiepe, F., Dorner, T., Hauser, A. E., Hoyer, B. F., Mei, H. and Radbruch, A., Long-lived autoreactive plasma cells drive persistent autoimmune inflammation. Nat. Rev. Rheumatol. 2011. 7: 170-178.
22. Rousset, F., Garcia, E., Defrance, T., Peronne, C., Vezzio, N., Hsu, D. H., Kastelein, R. et al., Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc. Natl. Acad. Sci. USA 1992. 89: 1890-1893.
23. Fairfax, K. A., Kallies, A., Nutt, S. L. and Tarlinton, D. M., Plasma cell development: from B-cell subsets to long-term survival niches. Semin. Immunol. 2008. 20: 49-58.
24. Jego, G., Palucka, A. K., Blanck, J. P., Chalouni, C., Pascual, V. and Banchereau, J., Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity 2003. 19: 225-234.
25. Oracki, S. A., Walker, J. A., Hibbs, M. L., Corcoran, L. M. and Tarlinton, D. M., Plasma cell development and survival. Immunol. Rev. 2010. 237: 140-159.
26. Bentebibel, S. E., Schmitt, N., Banchereau, J. and Ueno, H., Human tonsil B-cell lymphoma 6 (BCL6)-expressing CD4+ T-cell subset specialized for B-cell help outside germinal centers. Proc. Natl. Acad. Sci. USA 2011. 108: E488-E497.
27. Ma, C. S., Deenick, E. K., Batten, M. and Tangye, S. G., The origins, function, and regulation of T follicular helper cells. J. Exp. Med. 2012. 209: 1241-1253.
28. Yoshimori, T., Yamamoto, A., Moriyama, Y., Futai, M. and Tashiro, Y., Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J. Biol. Chem. 1991. 266: 17707-17712.
29. Krutzik, P. O. and Nolan, G. P., Fluorescent cell barcoding in flow cytometry allows high-throughput drug screening and signaling profiling. Nat. Methods 2006. 3: 361-368.
30. Rochman, Y., Spolski, R. and Leonard, W. J., New insights into the regulation of T cells by gamma(c) family cytokines. Nat. Rev. Immunol. 2009. 9: 480-490.
31. Casanova, J. L., Holland, S. M. and Notarangelo, L. D., Inborn errors of human JAKs and STATs. Immunity 2012. 36: 515-528.
32. Chandesris, M. O., Melki, I., Natividad, A., Puel, A., Fieschi, C., Yun, L., Thumerelle, C. et al., Autosomal dominant STAT3 deficiency and hyper-IgE syndrome: molecular, cellular, and clinical features from a French national survey. Medicine 2012. 91: e1-e19.
33. Hagn, M., Schwesinger, E., Ebel, V., Sontheimer, K., Maier, J., Beyer, T., Syrovets, T. et al., Human B cells secrete granzyme B when recognizing viral antigens in the context of the acute phase cytokine IL-21. J. Immunol. 2009. 183: 1838-1845.
34. Hagn, M., Ebel, V., Sontheimer, K., Schwesinger, E., Lunov, O., Beyer, T., Fabricius, D. et al., CD5+ B cells from individuals with systemic lupus erythematosus express granzyme B. Eur. J. Immunol. 2010. 40: 2060-2069.
35. Hagn, M., Sontheimer, K., Dahlke, K., Brueggemann, S., Kaltenmeier, C., Beyer, T., Hofmann, S. et al., Human B cells differentiate into granzyme B-secreting cytotoxic B lymphocytes upon incomplete T-cell help. Immunol. Cell Biol. 2012. 90: 457-467.
36. Hahne, M., Renno, T., Schroeter, M., Irmler, M., French, L., Bornard, T., MacDonald, H. R. et al., Activated B cells express functional Fas ligand. Eur. J. Immunol. 1996. 26: 721-724.
37. Boivin, W. A., Cooper, D. M., Hiebert, P. R. and Granville, D. J., Intracellular versus extracellular granzyme B in immunity and disease: challenging the dogma. Lab. Invest. 2009. 89: 1195-1220.
38. Heusel, J. W., Wesselschmidt, R. L., Shresta, S., Russell, J. H. and Ley, T. J., Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells. Cell 1994. 76: 977-987.
39. Hagn, M., Belz, G. T., Kallies, A., Sutton, V. R., Thia, K. Y., Tarlinton, D. M., Hawkins, E. D. et al., Activated mouse B cells lack expression of granzyme B. J. Immunol. 2012. 188: 3886-3892.
40. Lindner, S., Dahlke, K., Sontheimer, K., Hagn, M., Kaltenmeier, C., Barth, T. F., Beyer, T. et al., Interleukin 21-induced granzyme B-expressing B cells infiltrate tumors and regulate T cells. Cancer Res. 2013. 73: 2468-2479.
41. Armitage, R. J., Macduff, B. M., Eisenman, J., Paxton, R. and Grabstein, K. H., IL-15 has stimulatory activity for the induction of B cell proliferation and differentiation. J. Immunol. 1995. 154: 483-490.
42. Ozaki, K., Spolski, R., Feng, C. G., Qi, C. F., Cheng, J., Sher, A., Morse, H. C., 3rd et al., A critical role for IL-21 in regulating immunoglobulin production. Science 2002. 298: 1630-1634.
43. Ozaki, K., Spolski, R., Ettinger, R., Kim, H. P., Wang, G., Qi, C. F., Hwu, P. et al., Regulation of B cell differentiation and plasma cell generation by IL-21, a novel inducer of Blimp-1 and Bcl-6. J. Immunol. 2004. 173: 5361-5371.
44. Ettinger, R., Sims, G. P., Fairhurst, A. M., Robbins, R., da Silva, Y. S., Spolski, R., Leonard, W. J. et al., IL-21 induces differentiation of human naive and memory B cells into antibody-secreting plasma cells. J. Immunol. 2005. 175: 7867-7879.
45. Fehniger, T. A., Cai, S. F., Cao, X., Bredemeyer, A. J., Presti, R. M., French, A. R. and Ley, T. J., Acquisition of murine NK cell cytotoxicity requires the translation of a pre-existing pool of granzyme B and perforin mRNAs. Immunity 2007. 26: 798-811.
46. Gonzalez-Alvaro, I., Ortiz, A. M., Garcia-Vicuna, R., Balsa, A., Pascual-Salcedo, D. and Laffon, A., Increased serum levels of interleukin-15 in rheumatoid arthritis with long-term disease. Clin. Exp. Rheumatol. 2003. 21: 639-642.
47. Aringer, M., Stummvoll, G. H., Steiner, G., Koller, M., Steiner, C. W., Hofler, E., Hiesberger, H. et al., Serum interleukin-15 is elevated in systemic lupus erythematosus. Rheumatology 2001. 40: 876-881.
48. Nakou, M., Papadimitraki, E. D., Fanouriakis, A., Bertsias, G. K., Choulaki, C., Goulidaki, N., Sidiropoulos, P. et al., Interleukin-21 is increased in active systemic lupus erythematosus patients and contributes to generation of plasma B cells. Clin. Exp. Rheumatol. 2013. 31: 172-179.
49. Rasmussen, T. K., Andersen, T., Hvid, M., Hetland, M. L., Horslev-Petersen, K., Stengaard-Pedersen, K., Holm, C. K. et al., Increased interleukin 21 (IL-21) and IL-23 are associated with increased disease activity and with radiographic status in patients with early rheumatoid arthritis. J. Rheumatol. 2010. 37: 2014-2020.
50. Avery, D. T., Deenick, E. K., Ma, C. S., Suryani, S., Simpson, N., Chew, G. Y., Chan, T. D. et al., B cell-intrinsic signaling through IL-21 receptor and STAT3 is required for establishing long-lived antibody responses in humans. J. Exp. Med. 2010. 207: 155-171.
51. Xu, W., Roos, A., Schlagwein, N., Woltman, A. M., Daha, M. R. and van Kooten, C., IL-10-producing macrophages preferentially clear early apoptotic cells. Blood 2006. 107: 4930-4937.