NIK signaling axis regulates dendritic cell function in intestinal immunity and homeostasis

Nature Immunology

Volumn 19, Issue 11, 2018, Pages 1224-1235

  Jie, Zuliang ^a   Yang, Jin Young ^a   Gu, Meidi ^a   Wang, Hui ^a,b   Xie, Xiaoping ^a   Li, Yanchuan ^a   Liu, Ting ^a,c   Zhu, Lele ^a   Shi, Jianhong ^a,d   Zhang, Lingyun ^a,e   Zhou, Xiaofei ^a   Joo, Donghyun ^a   Brightbill, Hans D ^f   Cong, Yingzi ^g   Lin, Daniel ^a   Cheng, Xuhong ^a   Sun, Shao Cong ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b XUZHOU MEDICAL UNIVERSITY   (China)

^c SICHUAN UNIVERSITY   (China)

^d HEBEI UNIVERSITY   (China)

^e THE FIRST AFFILIATED HOSPITAL OF ZHENGZHOU UNIVERSITY   (China)

^f GENENTECH INC   (United States)

^g University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; INTERLEUKIN 23; SECRETORY COMPONENT; SECRETORY IMMUNOGLOBULIN; NF-KAPPA B KINASE; PROTEIN SERINE THREONINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUNCTION; CITROBACTER RODENTIUM; CONTROLLED STUDY; DENDRITIC CELL; HOMEOSTASIS; HOST RESISTANCE; INFLAMMATION; INTESTINE; INTESTINE EPITHELIUM CELL; LYMPHOID CELL; MICROFLORA; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; TH17 CELL; ANIMAL; C57BL MOUSE; COLITIS; IMMUNOLOGY; INNATE IMMUNITY; INTESTINE MUCOSA; KNOCKOUT MOUSE; SIGNAL TRANSDUCTION;

ANIMALS; COLITIS; DENDRITIC CELLS; HOMEOSTASIS; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EID: 85053790780     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/s41590-018-0206-z     Document Type: Article

References (54)

1. Gutzeit, C., Magri, G. & Cerutti, A. Intestinal IgA production and its role in host–microbe interaction. Immunol. Rev. 260, 76–85 (2014).
2. Brandtzaeg, P. Secretory IgA: designed for anti-microbial defense. Front. Immunol. 4, 222 (2013).
3. Palm, N. W. et al. Immunoglobulin A coating identifies colitogenic bacteria in inflammatory bowel disease. Cell 158, 1000–1010 (2014).
4. Coombes, J. L. & Powrie, F. Dendritic cells in intestinal immune regulation. Nat. Rev. Immunol. 8, 435–446 (2008).
5. Briseno, C. G., Murphy, T. L. & Murphy, K. M. Complementary diversification of dendritic cells and innate lymphoid cells. Curr. Opin. Immunol. 29, 69–78 (2014).
6. Walker, J. A., Barlow, J. L. & McKenzie, A. N. Innate lymphoid cells—How did we miss them? Nat. Rev. Immunol. 13, 75–87 (2013).
7. Buela, K. A., Omenetti, S. & Pizarro, T. T. Cross-talk between type 3 innate lymphoid cells and the gut microbiota in inflammatory bowel disease. Curr. Opin. Gastroenterol. 31, 449–455 (2015).
8. Cerutti, A. The regulation of IgA class switching. Nat. Rev. Immunol. 8, 421–434 (2008).
9. Massacand, J. C. et al. Intestinal bacteria condition dendritic cells to promote IgA production. PLoS One 3, e2588 (2008).
10. Ruane, D. et al. Microbiota regulate the ability of lung dendritic cells to induce IgA class-switch recombination and generate protective gastrointestinal immune responses. J. Exp. Med. 213, 53–73 (2016).
11. + T-cell subsets. Immunol. Rev. 252, 41–51 (2013).
12. Sun, S. C. The non-canonical NF-κB pathway in immunity and inflammation. Nat. Rev. Immunol. 17, 545–558 (2017).
13. Sun, S. C. The noncanonical NF-κB pathway. Immunol. Rev. 246, 125–140 (2012).
14. Senftleben, U. et al. Activation of IKKa of a second, evolutionary conserved, NF-kB signaling pathway. Science 293, 1495–1499 (2001).
15. Xiao, G., Harhaj, E. W. & Sun, S. C. NF-κB-inducing kinase regulates the processing of NF-κB2 p100. Mol. Cell 7, 401–409 (2001).
16. Liao, G., Zhang, M., Harhaj, E. W. & Sun, S. C. Regulation of the NF-κB-inducing kinase by tumor necrosis factor receptor-associated factor 3-induced degradation. J. Biol. Chem. 279, 26243–26250 (2004).
17. + T cells. Proc. Natl Acad. Sci. USA 112, 14664–14669 (2015).
18. Vedantam, G. & Viswanathan, V. K. Unlocking the gates to inflammatory bowel disease: the role of Enterococcus faecalis gelatinase. Gastroenterology 141, 795–798 (2011).
19. Zhou, Y. et al. Increased Enterococcus faecalis infection is associated with clinically active Crohn disease. Medicine (Baltimore) 95, e5019 (2016).
20. Jett, B. D., Huycke, M. M. & Gilmore, M. S. Virulence of enterococci. Clin. Microbiol. Rev. 7, 462–478 (1994).
21. Thompson, C. L., Vier, R., Mikaelyan, A., Wienemann, T. & Brune, A. ‘Candidatus Arthromitus’ revised: segmented filamentous bacteria in arthropod guts are members of Lachnospiraceae. Environ. Microbiol. 14, 1454–1465 (2012).
22. Ericsson, A. C., Hagan, C. E., Davis, D. J. & Franklin, C. L. Segmented filamentous bacteria: commensal microbes with potential effects on research. Comp. Med. 64, 90–98 (2014).
23. Talham, G. L., Jiang, H. Q., Bos, N. A. & Cebra, J. J. Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system. Infect. Immun. 67, 1992–2000 (1999).
24. Jaffar, Z., Ferrini, M. E., Herritt, L. A. & Roberts, K. Cutting edge: lung mucosal Th17-mediated responses induce polymeric Ig receptor expression by the airway epithelium and elevate secretory IgA levels. J. Immunol. 182, 4507–4511 (2009).
25. Cao, A. T., Yao, S., Gong, B., Elson, C. O. & Cong, Y. Th17 cells upregulate polymeric Ig receptor and intestinal IgA and contribute to intestinal homeostasis. J. Immunol. 189, 4666–4673 (2012).
26. Zheng, Y. et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14, 282–289 (2008).
27. Pham, T. A. et al. Epithelial IL-22RA1-mediated fucosylation promotes intestinal colonization resistance to an opportunistic pathogen. Cell. Host. Microbe. 16, 504–516 (2014).
28. Eberl, G. RORgammat, a multitask nuclear receptor at mucosal surfaces. Mucosal Immunol. 10, 27–34 (2017).
29. Hue, S. et al. Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J. Exp. Med. 203, 2473–2483 (2006).
30. Kullberg, M. C. et al. IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis. J. Exp. Med. 203, 2485–2494 (2006).
31. Yen, D. et al. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J. Clinic. Invest. 116, 1310–1316 (2006).
32. Maloy, K. J. & Kullberg, M. C. IL-23 and Th17 cytokines in intestinal homeostasis. Mucosal Immunol. 1, 339–349 (2008).
33. Shih, V. F. et al. Control of RelB during dendritic cell activation integrates canonical and noncanonical NF-κB pathways. Nat. Immunol. 13, 1162–1170 (2012).
34. Yu, J. et al. T cell–intrinsic function of the noncanonical NF-κB pathway in the regulation of GM-CSF expression and experimental autoimmune encephalomyelitis pathogenesis. J. Immunol. 193, 422–430 (2014).
35. Liang, C., Zhang, M. & Sun, S. C. β-TrCP binding and processing of NF-κB2/p100 involve its phosphorylation at serines 866 and 870. Cell. Signal. 18, 1309–1317 (2006).
36. Tucker, E. et al. A novel mutation in the Nfkb2 gene generates an NF-κB2 ‘super repressor’. J. Immunol. 179, 7514–7522 (2007).
37. Li, X., Yang, Y. & Ashwell, J. D. TNF-RII and c-IAP1 mediate ubiquitination and degradation of TRAF2. Nature 416, 345–347 (2002).
38. H 17 lineage. Nature 441, 231–234 (2006).
39. Basu, R. et al. Th22 cells are an important source of IL-22 for host protection against enteropathogenic bacteria. Immunity 37, 1061–1075 (2012).
40. Catana, C. S. et al. Contribution of the IL-17/IL-23 axis to the pathogenesis of inflammatory bowel disease. World J. Gastroenterol. 21, 5823–5830 (2015).
41. Neurath, M. F. Current and emerging therapeutic targets for IBD. Nat. Rev. Gastroenterol. Hepatol. 14, 269–278 (2017).
42. Kühn, R., Löhler, J., Rennick, D., Rajewsky, K. & Müller, W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75, 263–274 (1993).
43. Specht, S., Arriens, S. & Hoerauf, A. Induction of chronic colitis in IL-10 deficient mice requires IL-4. Microbes Infect. 8, 694–703 (2006).
44. −/− mice: insufficient counter regulation of a Th1 response. Int. Rev. Immunol. 19, 91–121 (2000).
45. Gomes-Santos, A. C. et al. New insights into the immunological changes in IL-10-deficient mice during the course of spontaneous inflammation in the gut mucosa. Clin. Dev. Immunol. 2012, 560817 (2012).
46. Suzuki, K. et al. Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc. Natl Acad. Sci. USA 101, 1981–1986 (2004).
47. Tumanov, A. V. et al. Lymphotoxin controls the IL-22 protection pathway in gut innate lymphoid cells during mucosal pathogen challenge. Cell. Host. Microbe. 10, 44–53 (2011).
48. Brightbill, H. D. et al. Conditional deletion of NF-κB-inducing kinase (NIK) in adult mice disrupts mature B cell survival and activation. J. Immunol. 195, 953–964 (2015).
49. Jin, J. et al. Epigenetic regulation of the expression of Il12 and Il23 and autoimmune inflammation by the deubiquitinase Trabid. Nat. Immunol. 17, 259–268 (2016).
50. Ajami, N. J., Cope, J. L., Wong, M. C., Petrosino, J. F. & Chesnel, L. Impact of oral fidaxomicin administration on the intestinal microbiota and susceptibility to Clostridium difficile colonization in mice. Antimicrob. Agents Chemother. 62, e02112-17 (2018).
51. Caporaso, J. G. et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621–1624 (2012).
52. Hu, H. et al. OTUD7B controls non-canonical NF-κB activation through deubiquitination of TRAF3. Nature 494, 371–374 (2013).
53. Qiu, J. et al. The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity 36, 92–104 (2012).
54. Nelson, J. D., Denisenko, O. & Bomsztyk, K. Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat. Protoc. 1, 179–185 (2006).