Innate Lymphoid Cells Control Early Colonization Resistance against Intestinal Pathogens through ID2-Dependent Regulation of the Microbiota

Immunity

Volumn 42, Issue 4, 2015, Pages 731-743

  Guo, Xiaohuan ^a,b   Liang, Yong ^a,c   Zhang, Yuan ^a   Lasorella, Anna ^d   Kee, Barbara L ^a   Fu, Yang Xin ^a,c  

^a UNIVERSITY OF CHICAGO   (United States)

^b Tsinghua University   (China)

^c INSTITUTE OF BIOPHYSICS   (China)

^d NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; INHIBITOR OF DIFFERENTIATION 2; INTERLEUKIN 22; INTERLEUKIN 23; INTERLEUKIN 23 RECEPTOR; RETINOID RELATED ORPHAN RECEPTOR GAMMA; STAT3 PROTEIN; IDB2 PROTEIN, MOUSE; INTERLEUKIN DERIVATIVE; INTERLEUKIN RECEPTOR; INTERLEUKIN-22; INTERLEUKIN-23 RECEPTOR, MOUSE;

ANIMAL CELL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL INFECTION; BACTERIAL STRAIN; CELL MATURATION; CITROBACTER RODENTIUM; COLONY FORMING UNIT; CYTOKINE PRODUCTION; GNOTOBIOTICS; HOST RESISTANCE; IMMUNOSURVEILLANCE; INNATE IMMUNITY; INTESTINE FLORA; LYMPHOID CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; DEFICIENCY; ENTEROBACTERIACEAE INFECTION; GENE EXPRESSION REGULATION; GENETICS; GERMFREE ANIMAL; HOMEOSTASIS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE; MICROBIOLOGY; MICROFLORA; PATHOLOGY;

ANIMALS; CELL DIFFERENTIATION; CITROBACTER RODENTIUM; ENTEROBACTERIACEAE INFECTIONS; GENE EXPRESSION REGULATION; GERM-FREE LIFE; HOMEOSTASIS; IMMUNITY, INNATE; INHIBITOR OF DIFFERENTIATION PROTEIN 2; INTERLEUKINS; LYMPHOCYTES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROBIOTA; RECEPTORS, ARYL HYDROCARBON; RECEPTORS, INTERLEUKIN; SIGNAL TRANSDUCTION;

EID: 84928194546     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.03.012     Document Type: Article

References (49)

1. Ahern P.P., Faith J.J., Gordon J.I. Mining the human gut microbiota for effector strains that shape the immune system. Immunity 2014, 40:815-823.
2. Austin M., Mellow M., Tierney W.M. Fecal microbiota transplantation in the treatment of Clostridium difficile infections. Am. J. Med. 2014, 127:479-483.
3. Behnsen J., Jellbauer S., Wong C.P., Edwards R.A., George M.D., Ouyang W., Raffatellu M. The cytokine IL-22 promotes pathogen colonization by suppressing related commensal bacteria. Immunity 2014, 40:262-273.
4. Bergstrom K.S., Kissoon-Singh V., Gibson D.L., Ma C., Montero M., Sham H.P., Ryz N., Huang T., Velcich A., Finlay B.B., et al. Muc2 protects against lethal infectious colitis by disassociating pathogenic and commensal bacteria from the colonic mucosa. PLoS Pathog. 2010, 6:e1000902.
5. Boos M.D., Yokota Y., Eberl G., Kee B.L. Mature natural killer cell and lymphoid tissue-inducing cell development requires Id2-mediated suppression of E protein activity. J.Exp. Med. 2007, 204:1119-1130.
6. Bry L., Brenner M.B. Critical role of Tcell-dependent serum antibody, but not the gut-associated lymphoid tissue, for surviving acute mucosal infection with Citrobacter rodentium, an attaching and effacing pathogen. J.Immunol. 2004, 172:433-441.
7. Bry L., Brigl M., Brenner M.B. CD4+-T-cell effector functions and costimulatory requirements essential for surviving mucosal infection with Citrobacter rodentium. Infect. Immun. 2006, 74:673-681.
8. Buffie C.G., Pamer E.G. Microbiota-mediated colonization resistance against intestinal pathogens. Nat. Rev. Immunol. 2013, 13:790-801.
9. Cash H.L., Whitham C.V., Behrendt C.L., Hooper L.V. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 2006, 313:1126-1130.
10. Chapman S.J., Hill A.V. Human genetic susceptibility to infectious disease. Nat. Rev. Genet. 2012, 13:175-188.
11. Cherrier M., Sawa S., Eberl G. Notch, Id2, and RORγt sequentially orchestrate the fetal development of lymphoid tissue inducer cells. J.Exp. Med. 2012, 209:729-740.
12. Crim S.M., Iwamoto M., Huang J.Y., Griffin P.M., Gilliss D., Cronquist A.B., Cartter M., Tobin-D'Angelo M., Blythe D., Smith K., et al. Incidence and trends of infection with pathogens transmitted commonly through food-Foodborne Diseases Active Surveillance Network, 10U.S. sites, 2006-2013. MMWR Morb. Mortal. Wkly. Rep. 2014, 63:328-332. Centers for Disease Control and Prevention (CDC).
13. Eberl G., Littman D.R. The role of the nuclear hormone receptor RORgammat in the development of lymph nodes and Peyer's patches. Immunol. Rev. 2003, 195:81-90.
14. Eberl G., Littman D.R. Thymic origin of intestinal alphabeta Tcells revealed by fate mapping of RORgammat+ cells. Science 2004, 305:248-251.
15. Eberl G., Marmon S., Sunshine M.J., Rennert P.D., Choi Y., Littman D.R. An essential function for the nuclear receptor RORgamma(t) in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 2004, 5:64-73.
16. Ghosh S., Dai C., Brown K., Rajendiran E., Makarenko S., Baker J., Ma C., Halder S., Montero M., Ionescu V.A., et al. Colonic microbiota alters host susceptibility to infectious colitis by modulating inflammation, redox status, and ion transporter gene expression. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 301:G39-G49.
17. Guo X., Qiu J., Tu T., Yang X., Deng L., Anders R.A., Zhou L., Fu Y.X. Induction of innate lymphoid cell-derived interleukin-22 by the transcription factor STAT3 mediates protection against intestinal infection. Immunity 2014, 40:25-39.
18. Hoyler T., Klose C.S., Souabni A., Turqueti-Neves A., Pfeifer D., Rawlins E.L., Voehringer D., Busslinger M., Diefenbach A. The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity 2012, 37:634-648.
19. Ivanov I.I., Atarashi K., Manel N., Brodie E.L., Shima T., Karaoz U., Wei D., Goldfarb K.C., Santee C.A., Lynch S.V., et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009, 139:485-498.
20. Jones-Mason M.E., Zhao X., Kappes D., Lasorella A., Iavarone A., Zhuang Y. E protein transcription factors are required for the development of CD4(+) lineage Tcells. Immunity 2012, 36:348-361.
21. Kamada N., Kim Y.G., Sham H.P., Vallance B.A., Puente J.L., Martens E.C., Núñez G. Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science 2012, 336:1325-1329.
22. Kamada N., Seo S.U., Chen G.Y., Núñez G. Role of the gut microbiota in immunity and inflammatory disease. Nat. Rev. Immunol. 2013, 13:321-335.
23. Kang H.S., Chin R.K., Wang Y., Yu P., Wang J., Newell K.A., Fu Y.X. Signaling via LTbetaR on the lamina propria stromal cells of the gut is required for IgA production. Nat. Immunol. 2002, 3:576-582.
24. Kee B.L. E and ID proteins branch out. Nat. Rev. Immunol. 2009, 9:175-184.
25. Kiss E.A., Vonarbourg C., Kopfmann S., Hobeika E., Finke D., Esser C., Diefenbach A. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 2011, 334:1561-1565.
26. Lee J.S., Cella M., McDonald K.G., Garlanda C., Kennedy G.D., Nukaya M., Mantovani A., Kopan R., Bradfield C.A., Newberry R.D., Colonna M. AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat. Immunol. 2012, 13:144-151.
27. Lozupone C.A., Stombaugh J.I., Gordon J.I., Jansson J.K., Knight R. Diversity, stability and resilience of the human gut microbiota. Nature 2012, 489:220-230.
28. Niola F., Zhao X., Singh D., Castano A., Sullivan R., Lauria M., Nam H.S., Zhuang Y., Benezra R., Di Bernardo D., et al. Id proteins synchronize stemness and anchorage to the niche of neural stem cells. Nat. Cell Biol. 2012, 14:477-487.
29. Ochoa T.J., Barletta F., Contreras C., Mercado E. New insights into the epidemiology of enteropathogenic Escherichia coli infection. Trans. R. Soc. Trop. Med. Hyg. 2008, 102:852-856.
30. Pickert G., Neufert C., Leppkes M., Zheng Y., Wittkopf N., Warntjen M., Lehr H.A., Hirth S., Weigmann B., Wirtz S., et al. STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J.Exp. Med. 2009, 206:1465-1472.
31. Qiu J., Heller J.J., Guo X., Chen Z.M., Fish K., Fu Y.X., Zhou L. The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity 2012, 36:92-104.
32. Qiu J., Guo X., Chen Z.M., He L., Sonnenberg G.F., Artis D., Fu Y.X., Zhou L. Group 3 innate lymphoid cells inhibit T-cell-mediated intestinal inflammation through aryl hydrocarbon receptor signaling and regulation of microflora. Immunity 2013, 39:386-399.
33. Rankin L.C., Groom J.R., Chopin M., Herold M.J., Walker J.A., Mielke L.A., McKenzie A.N., Carotta S., Nutt S.L., Belz G.T. The transcription factor T-bet is essential for the development of NKp46+ innate lymphocytes via the Notch pathway. Nat. Immunol. 2013, 14:389-395.
34. Rawlins E.L., Clark C.P., Xue Y., Hogan B.L. The Id2+ distal tip lung epithelium contains individual multipotent embryonic progenitor cells. Development 2009, 136:3741-3745.
35. Schmutz S., Bosco N., Chappaz S., Boyman O., Acha-Orbea H., Ceredig R., Rolink A.G., Finke D. Cutting edge: IL-7 regulates the peripheral pool of adult ROR gamma+ lymphoid tissue inducer cells. J.Immunol. 2009, 183:2217-2221.
36. Serafini N., Klein Wolterink R.G., Satoh-Takayama N., Xu W., Vosshenrich C.A., Hendriks R.W., Di Santo J.P. Gata3 drives development of RORγt+ group 3 innate lymphoid cells. J.Exp. Med. 2014, 211:199-208.
37. Spahn T.W., Maaser C., Eckmann L., Heidemann J., Lügering A., Newberry R., Domschke W., Herbst H., Kucharzik T. The lymphotoxin-beta receptor is critical for control of murine Citrobacter rodentium-induced colitis. Gastroenterology 2004, 127:1463-1473.
38. Spits H., Artis D., Colonna M., Diefenbach A., Di Santo J.P., Eberl G., Koyasu S., Locksley R.M., McKenzie A.N., Mebius R.E., et al. Innate lymphoid cells-a proposal for uniform nomenclature. Nat. Rev. Immunol. 2013, 13:145-149.
39. Tumanov A.V., Koroleva E.P., Guo X., Wang Y., Kruglov A., Nedospasov S., Fu Y.X. Lymphotoxin controls the IL-22 protection pathway in gut innate lymphoid cells during mucosal pathogen challenge. Cell Host Microbe 2011, 10:44-53.
40. Upadhyay V., Poroyko V., Kim T.J., Devkota S., Fu S., Liu D., Tumanov A.V., Koroleva E.P., Deng L., Nagler C., et al. Lymphotoxin regulates commensal responses to enable diet-induced obesity. Nat. Immunol. 2012, 13:947-953.
41. Vallance B.A., Deng W., Jacobson K., Finlay B.B. Host susceptibility to the attaching and effacing bacterial pathogen Citrobacter rodentium. Infect. Immun. 2003, 71:3443-3453.
42. van der Waaij D., Berghuis-de Vries J.M., Lekkerkerk Lekkerkerk-v Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J.Hyg. (Lond.) 1971, 69:405-411.
43. Vonarbourg C., Mortha A., Bui V.L., Hernandez P.P., Kiss E.A., Hoyler T., Flach M., Bengsch B., Thimme R., Hölscher C., et al. Regulated expression of nuclear receptor RORγt confers distinct functional fates to NK cell receptor-expressing RORγt(+) innate lymphocytes. Immunity 2010, 33:736-751.
44. Wang Y., Koroleva E.P., Kruglov A.A., Kuprash D.V., Nedospasov S.A., Fu Y.X., Tumanov A.V. Lymphotoxin beta receptor signaling in intestinal epithelial cells orchestrates innate immune responses against mucosal bacterial infection. Immunity 2010, 32:403-413.
45. Wlodarska M., Willing B., Keeney K.M., Menendez A., Bergstrom K.S., Gill N., Russell S.L., Vallance B.A., Finlay B.B. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect. Immun. 2011, 79:1536-1545.
46. Wlodarska M., Thaiss C.A., Nowarski R., Henao-Mejia J., Zhang J.P., Brown E.M., Frankel G., Levy M., Katz M.N., Philbrick W.M., et al. NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion. Cell 2014, 156:1045-1059.
47. Zelante T., Iannitti R.G., Cunha C., De Luca A., Giovannini G., Pieraccini G., Zecchi R., D'Angelo C., Massi-Benedetti C., Fallarino F., et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptorand balance mucosal reactivity via interleukin-22. Immunity 2013, 39:372-385.
48. Zhang F., Fuss I.J., Yang Z., Strober W. Transcription of RORγt in developing Th17 cells is regulated by E-proteins. Mucosal Immunol. 2014, 7:521-532.
49. Zheng Y., Valdez P.A., Danilenko D.M., Hu Y., Sa S.M., Gong Q., Abbas A.R., Modrusan Z., Ghilardi N., de Sauvage F.J., Ouyang W. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 2008, 14:282-289.