Impact of IgA isoforms on their ability to activate dendritic cells and to prime T cells.
IgA
dendritic cells
isoform
isotype
secretory
Journal
European journal of immunology
ISSN: 1521-4141
Titre abrégé: Eur J Immunol
Pays: Germany
ID NLM: 1273201
Informations de publication
Date de publication:
09 2020
09 2020
Historique:
received:
08
03
2019
revised:
20
02
2020
accepted:
07
04
2020
pubmed:
12
4
2020
medline:
13
1
2021
entrez:
12
4
2020
Statut:
ppublish
Résumé
Human IgA could be from different isotypes (IgA1/IgA2) and/or isoforms (monomeric, dimeric, or secretory). Monomeric IgA mainly IgA1 are considered as an anti-inflammatory isotype whereas dimeric/secretory IgA have clearly dual pro- and anti-inflammatory effects. Here, we show that IgA isotypes and isoforms display different binding abilities to FcαRI, Dectin-1, DC-SIGN, and CD71 on monocyte-derived dendritic cells (moDC). We describe that IgA regulate the expression of their own receptors and trigger modulation of moDC maturation. We also demonstrate that dimeric IgA2 and IgA1 induce different inflammatory responses leading to cytotoxic CD8
Identifiants
pubmed: 32277709
doi: 10.1002/eji.201948177
doi:
Substances chimiques
Immunoglobulin A
0
Protein Isoforms
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1295-1306Informations de copyright
© 2020 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.
Références
Woof, J. M. and Mestecky, J., Mucosal immunoglobulins. Immunol. Rev. 2005. 206: 64-82.
Brandtzaeg, P. and Prydz, H., Direct evidence for an integrated function of J chain and secretory component in epithelial transport of immunoglobulins. Nature 1984. 311: 71-73.
Woof, J. M. and Kerr, M. A., The function of immunoglobulin A in immunity. J. Pathol. 2006. 208: 270-282.
Zhou, M. and Ruprecht, R. M., Are anti-HIV IgAs good guys or bad guys? Retrovirology 2014. 11: 109.
Kerr, M. A., The structure and function of human IgA. Biochem. J. 1990. 271: 285-296.
Kett, K., Brandtzaeg, P., Radl, J. and Haaijman, J. J., Different subclass distribution of IgA-producing cells in human lymphoid organs and various secretory tissues. J. Immunol. 1986. 136: 3631-3635.
Lu, J., Marjon, K. D., Marnell, L. L., Wang, R., Mold, C., Du Clos, T. W. and Sun, P., Recognition and functional activation of the human IgA receptor (FcalphaRI) by C-reactive protein. Proc. Natl. Acad. Sci. U. S. A. 2011. 108: 4974-4979.
Moura, I. C., Centelles, M. N., Arcos-Fajardo, M., Malheiros, D. M., Collawn, J. F., Cooper, M. D. and Monteiro, R. C., Identification of the transferrin receptor as a novel immunoglobulin (Ig)A1 receptor and its enhanced expression on mesangial cells in IgA nephropathy. J. Exp. Med. 2001. 194: 417-425.
Rochereau, N., Drocourt, D., Perouzel, E., Pavot, V., Redelinghuys, P., Brown, G. D., Tiraby, G. et al., Dectin-1 is essential for reverse transcytosis of glycosylated SIgA-antigen complexes by intestinal M cells. PLoS Biol. 2013. 11: e1001658.
Baumann, J., Park, C. G. and Mantis, N. J., Recognition of secretory IgA by DC-SIGN: implications for immune surveillance in the intestine. Immunol. Lett. 2010. 131: 59-66.
Lycke, N. Y. and Bemark, M., The regulation of gut mucosal IgA B-cell responses: recent developments. Mucosal Immunol. 2017. 10: 1361-1374.
Heineke, M. H., van der Steen, L. P. E., Korthouwer, R. M., Hage, J. J., Langedijk, J. P. M., Benschop, J. J. et al., Peptide mimetics of immunoglobulin A (IgA) and FcalphaRI block IgA-induced human neutrophil activation and migration. Eur. J. Immunol. 2017. 47: 1835-1845.
Heineke, M. H. and van Egmond, M., Immunoglobulin A: magic bullet or Trojan horse? Eur. J. Clin. Invest. 2017. 47: 184-192.
Kubinak, J. L. and Round, J. L., Do antibodies select a healthy microbiota? Nat. Rev. Immunol. 2016. 16: 767-774.
Bunker, J. J., Erickson, S. A., Flynn, T. M., Henry, C., Koval, J. C., Meisel, M., Jabri, B. et al., Natural polyreactive IgA antibodies coat the intestinal microbiota. Science 2017. 358: eaan6619.
Macpherson, A. J., Yilmaz, B., Limenitakis, J. P. and Ganal-Vonarburg, S. C., IgA function in relation to the intestinal microbiota. Annu. Rev. Immunol. 2018. 36: 359-381.
Mkaddem, S. B., Christou, I., Rossato, E., Berthelot, L., Lehuen, A. and Monteiro, R. C., IgA, IgA receptors, and their anti-inflammatory properties. Curr. Top. Microbiol. Immunol. 2014. 382: 221-235.
Hansen, I. S., Krabbendam, L., Bernink, J. H., Loayza-Puch, F., Hoepel, W., van Burgsteden, J. A., Kuijper, E. C. et al., FcalphaRI co-stimulation converts human intestinal CD103(+) dendritic cells into pro-inflammatory cells through glycolytic reprogramming. Nat. Commun. 2018. 9: 863.
Chang, C. C., Wright, A. and Punnonen, J., Monocyte-derived CD1a+ and CD1a- dendritic cell subsets differ in their cytokine production profiles, susceptibilities to transfection, and capacities to direct Th cell differentiation. J. Immunol. 2000. 165: 3584-3591.
Gogolak, P., Rethi, B., Szatmari, I., Lanyi, A., Dezso, B., Nagy, L. and Rajnavolgyi, E., Differentiation of CD1a- and CD1a+ monocyte-derived dendritic cells is biased by lipid environment and PPARgamma. Blood 2007. 109: 643-652.
Pasquier, B., Lepelletier, Y., Baude, C., Hermine, O. and Monteiro, R. C., Differential expression and function of IgA receptors (CD89 and CD71) during maturation of dendritic cells. J. Leukoc. Biol. 2004. 76: 1134-1141.
Lissina, A., Briceno, O., Afonso, G., Larsen, M., Gostick, E., Price, D. A., Mallone, R. et al., Priming of qualitatively superior human effector CD8+ T cells using TLR8 Ligand combined with FLT3 ligand. J. Immunol. 2016. 196: 256-263.
Cernadas, M., Lu, J., Watts, G. and Brenner, M. B., CD1a expression defines an interleukin-12 producing population of human dendritic cells. Clin. Exp. Immunol. 2009. 155: 523-533.
Monteiro, R. C. and Van De Winkel, J. G., IgA Fc receptors. Annu. Rev. Immunol. 2003. 21: 177-204.
Geijtenbeek, T. B., Torensma, R., van Vliet, S. J., van Duijnhoven, G. C., Adema, G. J., van Kooyk, Y. and Figdor, C. G., Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 2000. 100: 575-585.
Heystek, H. C., Moulon, C., Woltman, A. M., Garonne, P. and van Kooten, C., Human immature dendritic cells efficiently bind and take up secretory IgA without the induction of maturation. J. Immunol. 2002. 168: 102-107.
Fabiano, R. C., Pinheiro, S. V. and Simoes, E. S. A. C., Immunoglobulin A nephropathy: a pathophysiology view. Inflamm. Res. 2016. 65: 757-770.
Pasquier, B., Launay, P., Kanamaru, Y., Moura, I. C., Pfirsch, S., Ruffie, C., Henin, D. et al., Identification of FcalphaRI as an inhibitory receptor that controls inflammation: dual role of FcRgamma ITAM. Immunity 2005. 22: 31-42.
Wehrli, M., Cortinas-Elizondo, F., Hlushchuk, R., Daudel, F., Villiger, P. M., Miescher, S., Zuercher, A. W. et al., Human IgA Fc receptor FcalphaRI (CD89) triggers different forms of neutrophil death depending on the inflammatory microenvironment. J. Immunol. 2014. 193: 5649-5659.
Saha, C., Das, M., Patil, V., Stephen-Victor, E., Sharma, M., Wymann, S., Jordi, M. et al., Monomeric immunoglobulin A from plasma inhibits human Th17 responses in vitro independent of FcalphaRI and DC-SIGN. Front. Immunol. 2017. 8: 275.
Cruikshank, W. W., Kornfeld, H. and Center, D. M., Interleukin-16. J Leukoc Biol 2000. 67: 757-766.
Sadasivan, B., Lehner, P. J., Ortmann, B., Spies, T. and Cresswell, P., Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Immunity 1996. 5: 103-114.
Diana, J., Moura, I. C., Vaugier, C., Gestin, A., Tissandie, E., Beaudoin, L., Corthesy, B. et al., Secretory IgA induces tolerogenic dendritic cells through SIGNR1 dampening autoimmunity in mice. J. Immunol. 2013. 191: 2335-2343.
Kassiotis, G. and Kollias, G., Uncoupling the proinflammatory from the immunosuppressive properties of tumor necrosis factor (TNF) at the p55 TNF receptor level: implications for pathogenesis and therapy of autoimmune demyelination. J. Exp. Med. 2001. 193: 427-434.
Scheller, J., Chalaris, A., Schmidt-Arras, D. and Rose-John, S., The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim. Biophys. Acta 2011. 1813: 878-888.
Gillessen, S., Carvajal, D., Ling, P., Podlaski, F. J., Stremlo, D. L., Familletti, P. C., Gubler, U. et al., Mouse interleukin-12 (IL-12) p40 homodimer: a potent IL-12 antagonist. Eur. J. Immunol. 1995. 25: 200-206.
Teng, M. W., Bowman, E. P., McElwee, J. J., Smyth, M. J., Casanova, J. L., Cooper, A. M. and Cua, D. J., IL-12 and IL-23 cytokines: from discovery to targeted therapies for immune-mediated inflammatory diseases. Nat. Med. 2015. 21: 719-729.
Cooper, A. M. and Khader, S. A., IL-12p40: an inherently agonistic cytokine. Trends Immunol. 2007. 28: 33-38.
Pabst, O., New concepts in the generation and functions of IgA. Nat. Rev. Immunol. 2012. 12: 821-832.
Pfeifle, R., Rothe, T., Ipseiz, N., Scherer, H. U., Culemann, S., Harre, U., Ackermann, J. A. et al., Regulation of autoantibody activity by the IL-23-TH17 axis determines the onset of autoimmune disease. Nat. Immunol. 2017. 18: 104-113.
Milpied, P. J. and McHeyzer-Williams, M. G., High-affinity IgA needs TH17 cell functional plasticity. Nat. Immunol. 2013. 14: 313-315.
Corthesy, B., Role of secretory immunoglobulin A and secretory component in the protection of mucosal surfaces. Future Microbiol. 2010. 5: 817-829.
Crottet, P. and Corthesy, B., Secretory component delays the conversion of secretory IgA into antigen-binding competent F(ab')2: a possible implication for mucosal defense. J. Immunol. 1998. 161: 5445-5453.
Farache, J., Koren, I., Milo, I., Gurevich, I., Kim, K. W., Zigmond, E., Furtado, G. C. et al., Luminal bacteria recruit CD103+ dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation. Immunity 2013. 38: 581-595.
Niess, J. H., Brand, S., Gu, X., Landsman, L., Jung, S., McCormick, B. A., Vyas, J. M. et al., CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 2005. 307: 254-258.
Cheroutre, H., Lambolez, F. and Mucida, D., The light and dark sides of intestinal intraepithelial lymphocytes. Nat. Rev. Immunol. 2011. 11: 445-456.
Bennett, M. S., Trivedi, S., Iyer, A. S., Hale, J. S. and Leung, D. T., Human mucosal-associated invariant T (MAIT) cells possess capacity for B cell help. J. Leukoc. Biol. 2017. 102: 1261-1269.
Ludvigsson, J. F., Neovius, M. and Hammarstrom, L., Association between IgA deficiency & other autoimmune conditions: a population-based matched cohort study. J. Clin. Immunol. 2014. 34: 444-451.
Rochereau, N., Pavot, V., Verrier, B., Jospin, F., Ensinas, A., Genin, C., Corthesy, B. et al., Delivery of antigen to nasal-associated lymphoid tissue microfold cells through secretory IgA targeting local dendritic cells confers protective immunity. J. Allergy Clin. Immunol. 2016.137: 214-222 e212.
Rochereau, N., Pavot, V., Verrier, B., Ensinas, A., Genin, C., Corthesy, B. and Paul, S., Secretory IgA as a vaccine carrier for delivery of HIV antigen to M cells. Eur. J. Immunol. 2015. 45: 773-779.
Cossarizza, A., Chang, H. D., Radbruch, A., Acs, A., Adam, D., Adam-Klages, S., Agace, W. 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.
Crottet, P. and Corthesy, B., Mapping the interaction between murine IgA and murine secretory component carrying epitope substitutions reveals a role of domains II and III in covalent binding to IgA. J. Biol. Chem. 1999. 274: 31456-31462.
Crottet, P., Peitsch, M. C., Servis, C. and Corthesy, B., Covalent homodimers of murine secretory component induced by epitope substitution unravel the capacity of the polymeric Ig receptor to dimerize noncovalently in the absence of IgA ligand. J. Biol. Chem. 1999. 274: 31445-31455.