Dendritic Cell Expression of the Signaling Molecule TRAF6 Is Critical for Gut Microbiota-Dependent Immune Tolerance

Immunity

Volumn 38, Issue 6, 2013, Pages 1211-1222

  Han, Daehee ^a,e   Walsh, MatthewC ^a   Cejas, PedroJ ^a   Dang, NicholasN ^a   Kim, YoungmiF ^a   Kim, Jihyun ^a   Charrier Hisamuddin, Laetitia ^a   Chau, Lillian ^a   Zhang, Qin ^a   Bittinger, Kyle ^a   Bushman, FredericD ^a   Turka, LaurenceA ^d   Shen, Hao ^a   Reizis, Boris ^c   DeFranco, AnthonyL ^b   Wu, GaryD ^a   Choi, Yongwon ^a,e  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c New York Presbyterian Morgan Stanley Children's Hospital   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e Pohang University of Science and Technology (POSTECH)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTEGRIN; BETA INTEGRIN; GAMMA INTERFERON; INTERLEUKIN 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL COUNT; CONTROLLED STUDY; DENDRITIC CELL; EOSINOPHILIC ENTERITIS; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; INTESTINAL FIBROSIS; INTESTINE FLORA; LAMINA PROPRIA; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH2 CELL;

ANIMALS; CELLS, CULTURED; DENDRITIC CELLS; ENTERITIS; EOSINOPHILIA; EOSINOPHILS; GASTRITIS; GENE EXPRESSION REGULATION; IMMUNE TOLERANCE; INTERLEUKIN-2; INTESTINES; LYMPHOCYTE ACTIVATION; METAGENOME; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TH2 CELLS; TNF RECEPTOR-ASSOCIATED FACTOR 6;

EID: 84879605869     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.05.012     Document Type: Article

References (44)

1. Agace W.W., Persson E.K. How vitamin A metabolizing dendritic cells are generated in the gut mucosa. Trends Immunol. 2012, 33:42-48.
2. Atarashi K., Nishimura J., Shima T., Umesaki Y., Yamamoto M., Onoue M., Yagita H., Ishii N., Evans R., Honda K., Takeda K. ATP drives lamina propria T(H)17 cell differentiation. Nature 2008, 455:808-812.
3. Atarashi K., Tanoue T., Shima T., Imaoka A., Kuwahara T., Momose Y., Cheng G., Yamasaki S., Saito T., Ohba Y., et al. Induction of colonic regulatory Tcells by indigenous Clostridium species. Science 2011, 331:337-341.
4. Blanchard C., Rothenberg M.E. Biology of the eosinophil. Adv. Immunol. 2009, 101:81-121.
5. Brand S. Crohn's disease: Th1, Th17 or both? The change of a paradigm: new immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn's disease. Gut 2009, 58:1152-1167.
6. Burchill M.A., Goetz C.A., Prlic M., O'Neil J.J., Harmon I.R., Bensinger S.J., Turka L.A., Brennan P., Jameson S.C., Farrar M.A. Distinct effects of STAT5 activation on CD4+ and CD8+ Tcell homeostasis: development of CD4+CD25+ regulatory Tcells versus CD8+ memory Tcells. J.Immunol. 2003, 171:5853-5864.
7. Caton M.L., Smith-Raska M.R., Reizis B. Notch-RBP-J signaling controls the homeostasis of CD8- dendritic cells in the spleen. J.Exp. Med. 2007, 204:1653-1664.
8. Chang S.H., Dong C. Signaling of interleukin-17 family cytokines in immunity and inflammation. Cell. Signal. 2011, 23:1069-1075.
9. Chiffoleau E., Kobayashi T., Walsh M.C., King C.G., Walsh P.T., Hancock W.W., Choi Y., Turka L.A. TNF receptor-associated factor 6 deficiency during hemopoiesis induces Th2-polarized inflammatory disease. J.Immunol. 2003, 171:5751-5759.
10. Deng L., Wang C., Spencer E., Yang L., Braun A., You J., Slaughter C., Pickart C., Chen Z.J. Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 2000, 103:351-361.
11. Fontenot J.D., Rasmussen J.P., Gavin M.A., Rudensky A.Y. A function for interleukin 2 in Foxp3-expressing regulatory Tcells. Nat. Immunol. 2005, 6:1142-1151.
12. Fritz T., Niederreiter L., Adolph T., Blumberg R.S., Kaser A. Crohn's disease: NOD2, autophagy and ER stress converge. Gut 2011, 60:1580-1588.
13. Granucci F., Vizzardelli C., Pavelka N., Feau S., Persico M., Virzi E., Rescigno M., Moro G., Ricciardi-Castagnoli P. Inducible IL-2 production by dendritic cells revealed by global gene expression analysis. Nat. Immunol. 2001, 2:882-888.
14. Hammer G.E., Turer E.E., Taylor K.E., Fang C.J., Advincula R., Oshima S., Barrera J., Huang E.J., Hou B., Malynn B.A., et al. Expression of A20 by dendritic cells preserves immune homeostasis and prevents colitis and spondyloarthritis. Nat. Immunol. 2011, 12:1184-1193.
15. Hou B., Reizis B., DeFranco A.L. Toll-like receptors activate innate and adaptive immunity by using dendritic cell-intrinsic and -extrinsic mechanisms. Immunity 2008, 29:272-282.
16. Idzko M., Hammad H., van Nimwegen M., Kool M., Willart M.A., Muskens F., Hoogsteden H.C., Luttmann W., Ferrari D., Di Virgilio F., et al. Extracellular ATP triggers and maintains asthmatic airway inflammation by activating dendritic cells. Nat. Med. 2007, 13:913-919.
17. Inoue J., Gohda J., Akiyama T. Characteristics and biological functions of TRAF6. Adv. Exp. Med. Biol. 2007, 597:72-79.
18. Kel J.M., Girard-Madoux M.J., Reizis B., Clausen B.E. TGF-beta is required to maintain the pool of immature Langerhans cells in the epidermis. J.Immunol. 2010, 185:3248-3255.
19. King C.G., Kobayashi T., Cejas P.J., Kim T., Yoon K., Kim G.K., Chiffoleau E., Hickman S.P., Walsh P.T., Turka L.A., Choi Y. TRAF6 is a Tcell-intrinsic negative regulator required for the maintenance of immune homeostasis. Nat. Med. 2006, 12:1088-1092.
20. Kobayashi T., Walsh P.T., Walsh M.C., Speirs K.M., Chiffoleau E., King C.G., Hancock W.W., Caamano J.H., Hunter C.A., Scott P., et al. TRAF6 is a critical factor for dendritic cell maturation and development. Immunity 2003, 19:353-363.
21. Kool M., van Loo G., Waelput W., De Prijck S., Muskens F., Sze M., van Praet J., Branco-Madeira F., Janssens S., Reizis B., et al. The ubiquitin-editing protein A20 prevents dendritic cell activation, recognition of apoptotic cells, and systemic autoimmunity. Immunity 2011, 35:82-96.
22. Kulhankova K., Rouse T., Nasr M.E., Field E.H. Dendritic cells control CD4+CD25+ Treg cell suppressor function invitro through juxtacrine delivery of IL-2. PLoS ONE 2012, 7:e43609.
23. Landström M. The TAK1-TRAF6 signalling pathway. Int. J. Biochem. Cell Biol. 2010, 42:585-589.
24. Lucendo A.J. Eosinophilic diseases of the gastrointestinal tract. Scand. J. Gastroenterol. 2010, 45:1013-1021.
25. Malek T.R., Castro I. Interleukin-2 receptor signaling: at the interface between tolerance and immunity. Immunity 2010, 33:153-165.
26. Maloy K.J., Powrie F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 2011, 474:298-306.
27. Manicassamy S., Pulendran B. Dendritic cell control of tolerogenic responses. Immunol. Rev. 2011, 241:206-227.
28. Masterson J.C., Furuta G.T., Lee J.J. Update on clinical and immunological features of eosinophilic gastrointestinal diseases. Curr. Opin. Gastroenterol. 2011, 27:515-522.
29. McKarns S.C., Schwartz R.H. Biphasic regulation of Il2 transcription in CD4+ Tcells: roles for TNF-alpha receptor signaling and chromatin structure. J.Immunol. 2008, 181:1272-1281.
30. Naramura M., Hu R.J., Gu H. Mice with a fluorescent marker for interleukin 2 gene activation. Immunity 1998, 9:209-216.
31. Pulendran B., Tang H., Manicassamy S. Programming dendritic cells to induce T(H)2 and tolerogenic responses. Nat. Immunol. 2010, 11:647-655.
32. Rescigno M. Intestinal dendritic cells. Adv. Immunol. 2010, 107:109-138.
33. Rescigno M. Dendritic cells in oral tolerance in the gut. Cell. Microbiol. 2011, 13:1312-1318.
34. Santaolalla R., Fukata M., Abreu M.T. Innate immunity in the small intestine. Curr. Opin. Gastroenterol. 2011, 27:125-131.
35. Sgouroudis E., Kornete M., Piccirillo C.A. IL-2 production by dendritic cells promotes Foxp3(+) regulatory T-cell expansion in autoimmune-resistant NOD congenic mice. Autoimmunity 2011, 44:406-414.
36. Shembade N., Ma A., Harhaj E.W. Inhibition of NF-kappaB signaling by A20 through disruption of ubiquitin enzyme complexes. Science 2010, 327:1135-1139.
37. Sorrentino A., Thakur N., Grimsby S., Marcusson A., von Bulow V., Schuster N., Zhang S., Heldin C.H., Landström M. The type I TGF-beta receptor engages TRAF6 to activate TAK1 in a receptor kinase-independent manner. Nat. Cell Biol. 2008, 10:1199-1207.
38. Steinman R.M. Decisions about dendritic cells: past, present, and future. Annu. Rev. Immunol. 2012, 30:1-22.
39. Swiatczak B., Rescigno M. How the interplay between antigen presenting cells and microbiota tunes host immune responses in the gut. Semin. Immunol. 2012, 24:43-49.
40. Takeda K., Akira S. TLR signaling pathways. Semin. Immunol. 2004, 16:3-9.
41. Travis M.A., Reizis B., Melton A.C., Masteller E., Tang Q., Proctor J.M., Wang Y., Bernstein X., Huang X., Reichardt L.F., et al. Loss of integrin alpha(v)beta8 on dendritic cells causes autoimmunity and colitis in mice. Nature 2007, 449:361-365.
42. Walsh M.C., Kim N., Kadono Y., Rho J., Lee S.Y., Lorenzo J., Choi Y. Osteoimmunology: interplay between the immune system and bone metabolism. Annu. Rev. Immunol. 2006, 24:33-63.
43. Wang F.L., Qin W.J., Wen W.H., Tian F., Song B., Zhang Q., Lee C., Zhong W.D., Guo Y.L., Wang H. TGF-beta insensitive dendritic cells: an efficient vaccine for murine prostate cancer. Cancer Immunol. Immunother. 2007, 56:1785-1793.
44. Webster K.E., Walters S., Kohler R.E., Mrkvan T., Boyman O., Surh C.D., Grey S.T., Sprent J. Invivo expansion of T reg cells with IL-2-mAb complexes: induction of resistance to EAE and long-term acceptance of isletallografts without immunosuppression. J.Exp. Med. 2009, 206:751-760.