Defective IgA response to atypical intestinal commensals in IL-21 receptor deficiency reshapes immune cell homeostasis and mucosal immunity

Mucosal Immunology

Volumn 12, Issue 1, 2019, Pages 85-96

  Cho, Hyeseon ^a   Jaime, Henrique ^b   de Oliveira, Rafael Pires ^c   Kang, Byunghyun ^a   Spolski, Rosanne ^d   Vaziri, Tina ^a   Myers, Timothy G ^a   Thovarai, Vishal ^e   Shen, Zeli ^f   Fox, James G ^f   Leonard, Warren J ^d   Kelsall, Brian L ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c INSTITUTO FEDERAL DO PARANÁ   (Brazil)

^d NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^e FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^f Massachusetts Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; IMMUNOGLOBULIN A; INTERLEUKIN 21 RECEPTOR; AICDA (ACTIVATION-INDUCED CYTIDINE DEAMINASE); CYTIDINE DEAMINASE;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; BACTERIAL LOAD; CELL EXPANSION; CELLULAR IMMUNITY; CITROBACTER RODENTIUM; COMMENSAL; CYTOKINE PRODUCTION; GERMINAL CENTER; HELICOBACTER; IMMUNOGLOBULIN RESPONSE; INTERLEUKIN 21 RECEPTOR DEFICIENCY; INTESTINE FLORA; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PEYER PATCH; PHENOTYPE; PLASMA CELL; PLASMABLAST; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SMALL INTESTINE; TH17 CELL; ANIMAL; BACTERIAL PHENOMENA AND FUNCTIONS; CELL CULTURE; CELL DIFFERENTIATION; ENTEROBACTERIACEAE INFECTION; GENETICS; HOMEOSTASIS; HUMAN; HUMORAL IMMUNITY; IMMUNOLOGY; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; ATYPICAL BACTERIAL FORMS; B-LYMPHOCYTES; BACTERIAL LOAD; CELL DIFFERENTIATION; CELLS, CULTURED; CITROBACTER RODENTIUM; CYTIDINE DEAMINASE; ENTEROBACTERIACEAE INFECTIONS; HELICOBACTER; HOMEOSTASIS; HUMANS; IMMUNITY, HUMORAL; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; INTESTINAL MUCOSA; INTESTINE, SMALL; MICE; MICE, KNOCKOUT; RECEPTORS, INTERLEUKIN-21; T-LYMPHOCYTES, REGULATORY; TH17 CELLS;

EID: 85052289010     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/s41385-018-0056-x     Document Type: Article

References (62)

1. Spolski, R. & Leonard, W. J. Interleukin-21: a double-edged sword with therapeutic potential. Nat. Rev. Drug Discov. 13, 379–395 (2014).
2. Caruso, R. et al. A functional role for interleukin-21 in promoting the synthesis of the T-cell chemoattractant, MIP-3alpha, by gut epithelial cells. Gastroenterology 132, 166–175 (2007).
3. Tangye, S. G. Advances in IL-21 biology - enhancing our understanding of human disease. Curr. Opin. Immunol. 34, 107–115 (2015).
4. Kotlarz, D. et al. Loss-of-function mutations in the IL-21 receptor gene cause a primary immunodeficiency syndrome. J. Exp. Med. 210, 433–443 (2013).
5. Linterman, M. A. et al. IL-21 acts directly on B cells to regulate Bcl-6 expression and germinal center responses. J. Exp. Med. 207, 353–363 (2010).
6. Ozaki, K. et al. A critical role for IL-21 in regulating immunoglobulin production. Science 298, 1630–1634 (2002).
7. Zotos, D. et al. IL-21 regulates germinal center B cell differentiation and proliferation through a B cell-intrinsic mechanism. J. Exp. Med. 207, 365–378 (2010).
8. Nurieva, R. I. et al. 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 (2008).
9. Vogelzang, A. et al. A fundamental role for interleukin-21 in the generation of T follicular helper cells. Immunity 29, 127–137 (2008).
10. Ivanov, I. I., Zhou, L. & Littman, D. R. Transcriptional regulation of Th17 cell differentiation. Semin Immunol. 19, 409–417 (2007).
11. Attridge, K. et al. IL-21 inhibits T cell IL-2 production and impairs Treg homeostasis. Blood 119, 4656–4664 (2012).
12. Jandl, C. et al. IL-21 restricts T follicular regulatory T cell proliferation through Bcl-6 mediated inhibition of responsiveness to IL-2. Nat. Commun. 8, 14647 (2017).
13. Festen, E. A. et al. Genetic variants in the region harbouring IL2/IL21 associated with ulcerative colitis. Gut 58, 799–804 (2009).
14. Stolfi, C. et al. Involvement of interleukin-21 in the regulation of colitis-associated colon cancer. J. Exp. Med. 208, 2279–2290 (2011).
15. Zorzi, F. et al. Distinct profiles of effector cytokines mark the different phases of Crohn’s disease. PLoS ONE 8, e54562 (2013).
16. Fina, D. et al. Regulation of gut inflammation and th17 cell response by interleukin-21. Gastroenterology 134, 1038–1048 (2008).
17. Salzer, E. et al. Early-onset inflammatory bowel disease and common variable immunodeficiency-like disease caused by IL-21 deficiency. J. Allergy Clin. Immunol. 133, 1651–1659.e12 (2014).
18. Wang, Y. et al. IL-21/IL-21R signaling suppresses intestinal inflammation induced by DSS through regulation of Th responses in lamina propria in mice. Sci. Rep. 6, 31881 (2016).
19. Wan, C. K. et al. The cytokines IL-21 and GM-CSF have opposing regulatory roles in the apoptosis of conventional dendritic cells. Immunity 38, 514–527 (2013).
20. Cao, A. T. et al. Interleukin (IL)-21 promotes intestinal IgA response to microbiota. Mucosal. Immunol. 8, 1072–1082 (2015).
21. Chai, J. N. et al. Helicobacter species are potent drivers of colonic T cell responses in homeostasis and inflammation. Sci. Immunol. 2, eaal5068 (2017).
22. Sano, T. et al. An IL-23R/IL-22 circuit regulates epithelial serum amyloid A to promote local effector Th17 responses. Cell 163, 381–393 (2015).
23. Xu, M. et al. c-MAF-dependent regulatory T cells mediate immunological tolerance to a gut pathobiont. Nature 554, 373–377 (2018).
24. Wang, L. et al. Key role for IL-21 in experimental autoimmune uveitis. Proc. Natl Acad. Sci. USA 108, 9542–9547 (2011).
25. Ballesteros-Tato, A. et al. T follicular helper cell plasticity shapes pathogenic T helper 2 cell-mediated immunity to inhaled house dust mite. Immunity 44, 259–273 (2016).
26. Ivanov, I. I. et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139, 485–498 (2009).
27. Liu, S. M. & King, C. IL-21-producing Th cells in immunity and autoimmunity. J. Immunol. 191, 3501–3506 (2013).
28. Jones, L. et al. A subpopulation of high IL-21-producing CD4(+) T cells in Peyer’s Patches is induced by the microbiota and regulates germinal centers. Sci. Rep. 6, 30784 (2016).
29. Pabst, O. New concepts in the generation and functions of IgA. Nat. Rev. Immunol. 12, 821–832 (2012).
30. Lecuyer, E. et al. Segmented filamentous bacterium uses secondary and tertiary lymphoid tissues to induce gut IgA and specific T helper 17 cell responses. Immunity 40, 608–620 (2014).
31. Seo, G. Y., Youn, J. & Kim, P. H. IL-21 ensures TGF-beta 1-induced IgA isotype expression in mouse Peyer’s patches. J. Leukoc. Biol. 85, 744–750 (2009).
32. Suzuki, K. et al. Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc. Natl Acad. Sci. USA 101, 1981–1986 (2004).
33. Longman, R. S. et al. CX(3)CR1(+) mononuclear phagocytes support colitis-associated innate lymphoid cell production of IL-22. J. Exp. Med. 211, 1571–1583 (2014).
34. Kumar, P. et al. Intestinal interleukin-17 receptor signaling mediates reciprocal control of the gut microbiota and autoimmune inflammation. Immunity 44, 659–671 (2016).
35. Tanoue, T., Atarashi, K. & Honda, K. Development and maintenance of intestinal regulatory T cells. Nat. Rev. Immunol. 16, 295–309 (2016).
36. Kullberg, M. C. et al. Bacteria-triggered CD4(+) T regulatory cells suppress Helicobacter hepaticus-induced colitis. J. Exp. Med. 196, 505–515 (2002).
37. Schiering, C. et al. The alarmin IL-33 promotes regulatory T-cell function in the intestine. Nature 513, 564–568 (2014).
38. Palm, N. W. et al. Immunoglobulin A coating identifies colitogenic bacteria in inflammatory bowel disease. Cell 158, 1000–1010 (2014).
39. Bunker, J. J. et al. Innate and adaptive humoral responses coat distinct commensal bacteria with immunoglobulin A. Immunity 43, 541–553 (2015).
40. Hadis, U. et al. Intestinal tolerance requires gut homing and expansion of FoxP3 + regulatory T cells in the lamina propria. Immunity 34, 237–246 (2011).
41. Konkel, J. E. et al. Transforming growth factor-beta signaling in regulatory T cells controls T helper-17 cells and tissue-specific immune responses. Immunity 46, 660–674 (2017).
42. Silberger, D. J., Zindl, C. L. & Weaver, C. T. Citrobacter rodentium: a model enteropathogen for understanding the interplay of innate and adaptive components of type 3 immunity. Mucosal Immunol. 10, 1108–1117 (2017).
43. Basu, R. et al. Th22 cells are an important source of IL-22 for host protection against enteropathogenic bacteria. Immunity 37, 1061–1075 (2012).
44. Aychek, T. et al. IL-23-mediated mononuclear phagocyte crosstalk protects mice from Citrobacter rodentium-induced colon immunopathology. Nat. Commun. 6, 6525 (2015).
45. Seo, S. U. et al. Intestinal macrophages arising from CCR2(+) monocytes control pathogen infection by activating innate lymphoid cells. Nat. Commun. 6, 8010 (2015).
46. Lee, Y. et al. IL-21R signaling is critical for induction of spontaneous experimental autoimmune encephalomyelitis. J. Clin. Invest. 125, 4011–4020 (2015).
47. − cell responses: recent developments. Mucosal Immunol. 10, 1361–1374 (2017).
48. Bunker, J. J. et al. Natural polyreactive IgA antibodies coat the intestinal microbiota. Science 358, eaan6619 (2017).
49. Masahata, K. et al. Generation of colonic IgA-secreting cells in the caecal patch. Nat. Commun. 5, 3704 (2014).
50. Morrison, P. J. et al. Th17-cell plasticity in Helicobacter hepaticus-induced intestinal inflammation. Mucosal Immunol. 6, 1143–1156 (2013).
51. Atarashi K et al. Science. 331, 337–341 (2011).
52. Schmitz, I. et al. IL-21 restricts virus-driven Treg cell expansion in chronic LCMV infection. PLoS Pathog. 9, e1003362 (2013).
53. Yang, Y. et al. Focused specificity of intestinal TH17 cells towards commensal bacterial antigens. Nature 510, 152–156 (2014).
54. Petursdottir, D. H. et al. Early-life human microbiota associated with childhood allergy promotes the T helper 17 axis in mice. Front Immunol. 8, 1699 (2017).
55. Kole, A. et al. Type I IFNs regulate effector and regulatory T cell accumulation and anti-inflammatory cytokine production during T cell-mediated colitis. J. Immunol. 191, 2771–2779 (2013).
56. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).
57. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011).
58. Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).
59. Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol 73, 5261–5267 (2007).
60. Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).
61. Lozupone, C. & Knight, R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228–8235 (2005).
62. Vazquez-Baeza, Y., Pirrung, M., Gonzalez, A. & Knight, R. EMPeror: a tool for visualizing high-throughput microbial community data. Gigascience 2, 16 (2013).