Divergent chemokine receptor expression and the consequence for human IgG4 B cell responses.
B cells
IgG4
chemokine receptors
rituximab
ulcerative colitis
Journal
European journal of immunology
ISSN: 1521-4141
Titre abrégé: Eur J Immunol
Pays: Germany
ID NLM: 1273201
Informations de publication
Date de publication:
08 2020
08 2020
Historique:
received:
28
10
2019
revised:
01
02
2020
accepted:
09
04
2020
pubmed:
15
4
2020
medline:
16
12
2020
entrez:
15
4
2020
Statut:
ppublish
Résumé
IgG4 antibodies are unique to humans. IgG4 is associated with tolerance during immunotherapy in allergy, but also with pathology, as in pemphigus vulgaris and IgG4-related disease. Its induction is largely restricted to nonmicrobial antigens, and requires repeated or prolonged antigenic stimulation, for reasons poorly understood. An important aspect in generating high-affinity IgG antibodies is chemokine receptor-mediated migration of B cells into appropriate niches, such as germinal centers. Here, we show that compared to IgG1 B cells, circulating IgG4 B cells express lower levels of CXCR3, CXCR4, CXCR5, CCR6, and CCR7, chemokine receptors involved in GC reactions and generation of long-lived plasma cells. This phenotype was recapitulated by in vitro priming of naive B cells with an IgG4-inducing combination of T
Identifiants
pubmed: 32289181
doi: 10.1002/eji.201948454
doi:
Substances chimiques
Immunoglobulin G
0
Receptors, Chemokine
0
Interleukin-4
207137-56-2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1113-1125Subventions
Organisme : Medical Research Council
Pays : United Kingdom
Informations de copyright
© 2020 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.
Références
Aalberse, R. C., Dieges, P. H., Knul-Bretlova, V., Vooren, P., Aalbers, M. and van Leeuwen, J., IgG4 as a blocking antibody. Clin. Rev. Allergy. 1983. 1: 289-302.
Aalberse, R. C., van der Gaag, R. and van Leeuwen, J., Serologic aspects of IgG4 antibodies. I. Prolonged immunization results in an IgG4-restricted response. J. Immunol. 1983. 130: 722-726.
Chliva, C., Aggelides, X., Makris, M., Katoulis, A., Rigopoulos, D. and Tiligada, E.. Comparable profiles of serum histamine and IgG4 levels in allergic beekeepers. Allergy. 2015. 70: 457-640.
Hofbauer, C. J., Whelan, S. F. J., Hirschler, M., Allacher, P., Horling, F. M., Lawo, J. - P., Oldenburg, J. et al., Affinity of FVIII-specific antibodies reveals major differences between neutralizing and nonneutralizing antibodies in humans. Blood. 2015. 125: 1180-1188.
van Schouwenburg, P. A., Krieckaert, C. L., Nurmohamed, M., Hart, M., Rispens, T., Aarden, L., Wouters, D. et al., IgG4 production against adalimumab during long term treatment of RA patients. J. Clin. Immunol. 2012. 32: 1000-1006.
Brito-Zerón, P., Ramos-Casals, M., Bosch, X. and Stone, J. H., The clinical spectrum of IgG4-related disease. Autoimmun. Rev. 2014. 13: 1203-1210.
Wallace, Z. S., Mattoo, H., Carruthers, M., Mahajan, V. S., Torre, E. D., Lee, H., Kulikova, M. et al., Plasmablasts as a biomarker for IgG4-related disease, independent of serum IgG4 concentrations. Ann Rheum Dis. 2015. 74: 190-195.
Akiyama, M., Suzuki, K., Yamaoka, K., Yasuoka, H., Takeshita, M., Kaneko, Y., Kondo, H. et al., Number of circulating follicular helper 2 T cells correlates with IgG4 and interleukin-4 levels and plasmablast numbers in IgG4-related disease. Arthritis Rheumatol. 2015. 67: 2476-2481.
Mahajan, V. S., Mattoo, H., Deshpande, V., Pillai, S. S. and Stone, J. H., IgG4-related disease. Annu. Rev. Pathol. 2014. 9: 315-347.
Sah, R. P. and Chari, S T. Serologic issues in IgG4-related systemic disease and autoimmune pancreatitis. Curr. Opin. Rheumatol. 2011. 23: 108-113.
Yamamoto, M., Tabeya, T., Naishiro, Y., Yajima, H., Ishigami, K., Shimizu, Y., Obara, M. et al., Value of serum IgG4 in the diagnosis of IgG4-related disease and in differentiation from rheumatic diseases and other diseases. Mod. Rheumatol. 2012. 22: 419-425.
Lighaam, L. C. and Rispens, T., The Immunobiology of Immunoglobulin G4. Semin. Liver Dis. 2016. 36: 200-215.
Meiler, F., Zumkehr, J., Klunker, S., Rückert, B., Akdis, C. A. and Akdis, M., In vivo switch to IL-10-secreting T regulatory cells in high dose allergen exposure. J. Exp. Med. 2008. 205: 2887-2898.
Zen, Y., Fujii, T., Harada, K., Kawano, M., Yamada, K., Takahira, M. and Nakanuma, Y., Th2 and regulatory immune reactions are increased in immunoglobin G4-related sclerosing pancreatitis and cholangitis. Hepatology. 2007. 45: 1538-1546.
Carbone, G., Wilson, A., Diehl, S. A., Bunn, J., Cooper, S. M. and Rincon, M., Interleukin-6 receptor blockade selectively reduces IL-21 production by CD4 T cells and IgG4 autoantibodies in rheumatoid arthritis. Int. J. Biol. Sci. 2013. 9: 279-288.
Cargill, T., Makuch, M., Sadler, R., Lighaam, L. C., Peters, R., van Ham, M., Klenerman, P. et al., Activated T-Follicular Helper 2 Cells Are Associated With Disease Activity in IgG4-Related Sclerosing Cholangitis and Pancreatitis. Clin. Transl. Gastroenterol. 2019. 10: e00020.
Maehara, T., Mattoo, H., Mahajan, V. S., Murphy, S. J., Yuen, G. J., Ishiguro, N., Ohta, M. et al., The expansion in lymphoid organs of IL-4 + BATF + T follicular helper cells is linked to IgG4 class switching in vivo. Life Sci. Alliance. 2018. 1: e201800050.
Khosroshahi, A., Bloch, D. B., Deshpande, V. and Stone, J. H., Rituximab therapy leads to rapid decline of serum IgG4 levels and prompt clinical improvement in IgG4-related systemic disease. Arthritis Rheum. 2010. 62: 1755-1762.
Carruthers, M. N., Topazian, M. D., Khosroshahi, A., Witzig, T. E., Wallace, Z. S., Hart, P. A., Deshpande, V. et al., Rituximab for IgG4-related disease: a prospective, open-label trial. Ann. Rheum. Dis. 2015. 74: 1171-1177.
Lighaam, L. C., Vermeulen, E., den Bleker, T., Meijlink, K. J., Aalberse, R. C., Barnes, E., Culver, E. L. et al., Phenotypic differences between IgG4+ and IgG1+ B cells point to distinct regulation of the IgG4 response. J. Allergy Clin. Immunol. 2014. 133: 267-270.e6.
Heeringa, J. J., Karim, A. F., van Laar, J. A. M., Verdijk, R. M., Paridaens, D., van Hagen, P. M. and van Zelm, M. C., Expansion of blood IgG4+ B, TH2, and regulatory T cells in patients with IgG4-related disease. J. Allergy Clin. Immunol. 2018. 141: 1831-1843.e10.
Avery, D. T., Bryant, V. L., Ma, C. S., de Waal Malefyt, R. and Tangye, S. G., IL-21-induced isotype switching to IgG and IgA by human naive B cells is differentially regulated by IL-4. J. Immunol. 2008. 181: 1767-1779.
Kallies, A., Hasbold, J., Tarlinton, D. M., Dietrich, W., Corcoran, L. M., Hodgkin, P. D. and Nutt, S. L., Plasma cell ontogeny defined by quantitative changes in blimp-1 expression. J. Exp. Med. 2004. 200: 967-977.
Nutt, S. L., Metcalf, D., D'Amico, A., Polli, M. and Wu, L., Dynamic regulation of PU.1 expression in multipotent hematopoietic progenitors. J. Exp. Med. 2005. 201: 221-231.
Weisel, F. J., Zuccarino-Catania, G. V., Chikina, M. and Shlomchik, M. J., A Temporal Switch in the Germinal Center Determines Differential Output of Memory B and Plasma Cells. Immunity. 2016. 44: 116-130.
Cyster, J. G., Chemokines, Sphingosine-1-Phosphate, and Cell Migration in Secondary Lymphoid Organs. Annu. Rev. Immunol. 2005. 23: 127-159.
Park, C., Hwang, I. Y., Sinha, R. K., Kamenyeva, O., Davis, M. D. and Kehrl, J. H., Lymph node B lymphocyte trafficking is constrained by anatomy and highly dependent upon chemoattractant desensitization. Blood. 2012. 119: 978-989.
Hiepe, F., Dörner, 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.
Legler, D. F., Loetscher, M., Roos, R. S., Clark-Lewis, I., Baggiolini, M. and Moser, B., B cell-attracting chemokine 1, a human CXC chemokine expressed in lymphoid tissues, selectively attracts B lymphocytes via BLR1/CXCR5. J. Exp. Med. 1998. 187: 655-660.
Förster, R., Mattis, A. E., Kremmer, E., Wolf, E., Brem, G. and Lipp, M., A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen. Cell. 1996. 87: 1037-1047.
Förster, R., Schubel, A., Breitfeld, D., Kremmer, E., Renner-Müller, I., Wolf, E. and Lipp, M., CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell. 1999. 99: 23-33.
Victora, G. D., Dominguez-sola, D., Holmes, A. B., Deroubaix, S., Dalla-favera, R. and Nussenzweig, M. C., Identification of human germinal center light and dark zone cells and their relationship to human B-cell lymphomas. Immunobiology. 2012. 120: 2240-2248.
Allen, C. D. C., Ansel, K. M., Low, C., Lesley, R., Tamamura, H., Fujii, N. and Cyster, J. G., Germinal center dark and light zone organization is mediated by CXCR4 and CXCR5. Nat. Immunol. 2004. 5: 943-952.
Cassese, G., Arce, S., Hauser, A. E., Lehnert, K., Moewes, B., Mostarac, M., Muehlinghaus, G. et al., Plasma cell survival is mediated by synergistic effects of cytokines and adhesion-dependent signals. J. Immunol. 2003. 171: 1684-1690.
Tarlinton, D., Radbruch, A., Hiepe, F. and Dörner, T., Plasma cell differentiation and survival. Curr. Opin. Immunol. 2008. 20: 162-169.
Humpert, M. L., Pinto, D., Jarrossay, D. and Thelen, M., CXCR7 influences the migration of B cells during maturation. Eur. J. Immunol. 2014. 44: 694-705.
Noelle, R., O ’connell, S., Hess, H., Lord, G. M., Menezes, M., Benson, V. S., Raman, C. et al., CCR6-Dependent Positioning of Memory B Cells Is Essential for Their Ability To Mount a Recall Response to Antigen. J Immunol Mater. Suppl. J. Immunol. 2016. 194: 505513.
Lacotte, S., Decossas, M., Le Coz, C., Brun, S., Muller, S. and Dumortier, H., Early Differentiated CD138highMHCII+IgG+ Plasma Cells Express CXCR3 and Localize into Inflamed Kidneys of Lupus Mice. PLoS One. 2013. 8: 1-14.
Muehlinghaus, G., Cigliano, L., Huehn, S., Peddinghaus, A., Leyendeckers, H., Hauser, A. E., Hiepe, F. et al., Regulation of CXCR3 and CXCR4 expression during terminal differentiation of memory B cells into plasma cells. Blood. 2005. 105: 3965-3971.
Armas-González, E., Domínguez-Luis, M. J., Díaz-Martín, A., Arce-Franco, M., Castro-Hernández, J., Danelon, G., Hernández-Hernández, V. et al., Role of CXCL13 and CCL20 in the recruitment of B cells to inflammatory foci in chronic arthritis. Arthritis Res. Ther. 2018. 20: 1-12.
Achtman, A. H., Höpken, U. E., Bernert, C. and Lipp, M., CCR7-deficient mice develop atypically persistent germinal centers in response to thymus-independent type 2 antigens. J. Leukoc. Biol. 2009. 85: 409-417.
Junt, T., Fink, K., Förster, R., Senn, B., Lipp, M., Muramatsu, M., Zinkernagel, R. M. et al., CXCR5-dependent seeding of follicular niches by B and Th cells augments antiviral B cell responses. J. Immunol. 2005. 175: 7109-7116.
Moser, K., Kalies, K., Szyska, M., Humrich, J. Y., Amann, K. and Manz, R. A., CXCR3 promotes the production of IgG1 autoantibodies but is not essential for the development of lupus nephritis in NZB/NZW mice. Arthritis Rheum. 2012. 64: 1237-1246.
Nie, Y., Waite, J., Brewer, F., Sunshine, M. -. J., Littman, D. R. and Zou, Y. -. R., The role of CXCR4 in maintaining peripheral B cell compartments and humoral immunity. J. Exp. Med. 2004. 200: 1145-1156.
Velaga, S., Herbrand, H., Friedrichsen, M., Jiong, T., Dorsch, M., Hoffmann, M. W., Förster, R. et al., Chemokine receptor CXCR5 supports solitary intestinal lymphoid tissue formation, B cell homing, and induction of intestinal IgA responses. J. Immunol. 2009. 182: 2610-2619.
Bryant, V. L., Ma, C. S., Avery, D. T., Li, Y., Good, K. L., Corcoran, L. M., de Waal Malefyt, R. et al., Cytokine-mediated regulation of human B cell differentiation into Ig-secreting cells: predominant role of IL-21 produced by CXCR5+ T follicular helper cells. J. Immunol. 2007. 179: 8180-8190.
Deenick, E. K., Avery, D. T., Chan, A., Berglund, L. J., Ives, M. L., Moens, L., Stoddard, J. L. et al., Naive and memory human B cells have distinct requirements for STAT3 activation to differentiate into antibody-secreting plasma cells. J. Exp. Med. 2013. 210: 2739-2753.
Xie, J. H., Nomura, N., Lu, M., Chen, S. -. L., Koch, G. E., Weng, Y., Rosa, R. et al., Antibody-mediated blockade of the CXCR3 chemokine receptor results in diminished recruitment of T helper 1 cells into sites of inflammation. J. Leukoc. Biol. 2003. 73: 771-780.
Huijbers, M. G., Querol, L. A., Niks, E. H., Plomp, J. J., van der Maarel, S. M., Graus, F., Dalmau, J. et al., The expanding field of IgG4-mediated neurological autoimmune disorders. Eur. J. Neurol. 2015. 22: 1151-1161.
Karagiannis, P., Gilbert, A. E., Josephs, D. H., Ali, N., Dodev, T., Saul, L., Correa, I. et al., IgG4 subclass antibodies impair antitumor immunity in melanoma. J. Clin. Invest. 2013. 123: 1457-1474.
Karagiannis, P., Villanova, F., Josephs, D. H., Correa, I., Van Hemelrijck, M., Hobbs, C., Saul, L. et al., Elevated IgG4 in patient circulation is associated with the risk of disease progression in melanoma. Oncoimmunology. 2015. 4.https://doi.org/10.1080/2162402X.2015.1032492.
Okada, T., Ngo, V. N., Ekland, E. H., Förster, R., Lipp, M., Littman, D. R. and Cyster, J. G., Chemokine requirements for B cell entry to lymph nodes and Peyer's patches. J. Exp. Med. 2002. 196: 65-75.
De Silva, N. S. and Klein, U., Dynamics of B cells in germinal centres. Nat. Rev. Immunol. 2015. 15: 137-148.
Suan, D., Sundling, C. and Brink, R., Plasma cell and memory B cell differentiation from the germinal center. Curr. Opin. Immunol. 2017. 45: 97-102.
Suan, D., Kräutler, N. J., Maag JL, V., Butt, D., Bourne, K., Hermes, J. R., Avery, D. T. et al., CCR6 Defines Memory B Cell Precursors in Mouse and Human Germinal Centers, Revealing Light-Zone Location and Predominant Low Antigen Affinity. Immunity. 2017. 47: 1142-1153.e4.
Victora, G. D. and Nussenzweig, M. C., Germinal centers. Annu. Rev. Immunol. 2012. 30: 429-457.
Tuijnenburg, P., aan de Kerk, D. J., Jansen, M. H., Morris, B., Lieftink, C., Beijersbergen, R. L., van Leeuwen, E. M. M. et al., High-throughput compound screen reveals mTOR inhibitors as potential therapeutics to reduce (auto)antibody production by human plasma cells. Eur. J. Immunol. 2019: 73-85.
Urashima, M., Chauhan, D., Uchiyama, H., Freeman, G. J. and Anderson, K. C., CD40 ligand triggered interleukin-6 secretion in multiple myeloma. Blood. 1995. 85: 1903-1912.
de Back, D. Z., Red blood cells, far more than oxygen transporters alone. 2019.
Nagelkerke, S. Q., Aan De Kerk, D. J., Jansen, M. H., Van Den Berg, T. K. and Kuijpers, T. W., Failure to detect functional neutrophil B Helper cells in the human spleen. PLoS One. 2014. 9: 1-6.
Teng, Y. K. O., Levarht, E. W. N., Hashemi, M., Bajema, I. M., Toes, R. E. M., Huizinga, T. W. J. and van Laar, J. M., Immunohistochemical analysis as a means to predict responsiveness to rituximab treatment. Arthritis Rheum. 2007. 56: 3909-3918.
Thurlings, R. M., Vos, K., Wijbrandts, C. A., Zwinderman, A. H., Gerlag, D. M. and Tak, P. P., Synovial tissue response to rituximab: mechanism of action and identification of biomarkers of response. Ann. Rheum. Dis. 2008. 67: 917-925.
Chari, S. T., Diagnosis of autoimmune pancreatitis using its five cardinal features: introducing the Mayo Clinic's HISORt criteria. J. Gastroenterol. 2007. 42(Suppl 1): 39-41.
Okazaki, K. and Umehara, H., Are Classification Criteria for IgG4-RD Now Possible? The Concept of IgG4-Related Disease and Proposal of Comprehensive Diagnostic Criteria in Japan. Int. J. Rheumatol. 2012. 2012: 357071.
Cossarizza, A., Chang, H. D., Radbruch, A., Acs, A., Adam, A., Adam-Klages, S., Agace, W. et al., Guidelines for the use of flow cytometry and cell sorting in immunological studies (second edition). Eur. J. Immunol. 2019. 49: 1457-1973.