Intestinal lamina propria dendritic cells maintain T cell homeostasis but do not affect commensalism

Journal of Experimental Medicine

Volumn 210, Issue 10, 2013, Pages 2011-2024

  Welty, Nathan E ^a   Staley, Christopher ^b   Ghilardi, Nico ^c   Sadowsky, Michael J ^b   Igyártó, Botond Z ^a   Kaplan, Daniel H ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD103 ANTIGEN; CD11B ANTIGEN; FLAGELLIN; GLYCOPROTEIN P 15095; INTERLEUKIN 17; INTERLEUKIN 22; INTERLEUKIN 23; LANGERIN;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ARTICLE; BACTEROIDETES; CD4+ T LYMPHOCYTE; CELL HOMING; CELL INTERACTION; COMMENSALISM; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FIRMICUTES; FLOW CYTOMETRY; GENOTYPE; INTESTINE INFECTION; LAMINA PROPRIA; MACROPHAGE; MICROBIAL COMMUNITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEOBACTERIA; REGULATORY T LYMPHOCYTE; SMALL INTESTINE; TH1 CELL; TH17 CELL;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD11B; DENDRITIC CELLS; DIPHTHERIA TOXIN; HOMEOSTASIS; HUMANS; IMMUNOPHENOTYPING; INTEGRIN ALPHA CHAINS; INTESTINAL MUCOSA; LECTINS, C-TYPE; MANNOSE-BINDING LECTINS; METAGENOME; MICE; MICE, TRANSGENIC; PHENOTYPE; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; TH17 CELLS;

EID: 84885447087     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20130728     Document Type: Article

References (69)

1. Atarashi, K., J. Nishimura, T. Shima, Y. Umesaki, M. Yamamoto, M. Onoue, H. Yagita, N. Ishii, R. Evans, K. Honda, and K. Takeda. 2008. ATP drives lamina propria T(H)17 cell differentiation. Nature. 455:808-812. http://dx.doi.org/10.1038/nature07240
2. Barthel, M., S. Hapfelmeier, L. Quintanilla-Martínez, M. Kremer, M. Rohde, M. Hogardt, K. Pfeffer, H. Rüssmann, and W.-D. Hardt. 2003. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect. Immun. 71:2839-2858. http://dx.doi.org/10.1128/IAI.71.5.2839-2858.2003
3. Basu, R., D.B. O'Quinn, D.J. Silberger, T.R. Schoeb, L. Fouser, W. Ouyang, R.D. Hatton, and C.T. Weaver. 2012. Th22 cells are an important source of IL-22 for host protection against enteropathogenic bacteria. Immunity. 37:1061-1075. http://dx.doi.org/10.1016/j.immuni.2012.08.024
4. Bobr, A., I. Olvera-Gomez, B.Z. Igyarto, K.M. Haley, K.A. Hogquist, and D.H. Kaplan. 2010. Acute ablation of Langerhans cells enhances skin immune responses. J. Immunol. 185:4724-4728. http://dx.doi.org/10.4049/jimmunol.1001802
5. Bogunovic, M., F. Ginhoux, J. Helft, L. Shang, D. Hashimoto, M. Greter, K. Liu, C. Jakubzick, M.A. Ingersoll, M. Leboeuf, et al. 2009. Origin of the lamina propria dendritic cell network. Immunity. 31:513-525. http://dx.doi.org/10.1016/j.immuni.2009.08.010
6. Bray, J.R., and J.T. Curtis. 1957. An ordination of the upland forest communities of southern wisconsin. Ecol. Monogr. 27:325-349. http://dx.doi.org/10.2307/1942268
7. Bursch, L.S., L. Wang, B. Igyarto, A. Kissenpfennig, B. Malissen, D.H. Kaplan, and K.A. Hogquist. 2007. Identification of a novel population of Langerin+ dendritic cells. J. Exp. Med. 204:3147-3156. http://dx.doi.org/10.1084/jem.20071966
8. Cerovic, V., S.A. Houston, C.L. Scott, A. Aumeunier, U. Yrlid, A.M. Mowat, and S.W.F. Milling. 2013. Intestinal CD103(-) dendritic cells migrate in lymph and prime effector T cells. Mucosal Immunol. 6:104-113. http://dx.doi.org/10.1038/mi.2012.53
9. Chang, S.-Y., and M.-N. Kweon. 2010. Langerin-expressing dendritic cells in gut-associated lymphoid tissues. Immunol. Rev. 234:233-246. http://dx.doi.org/10.1111/j.0105-2896.2009.00878.x
10. Chikwava, K., and R. Jaffe. 2004. Langerin (CD207) staining in normal pediatric tissues, reactive lymph nodes, and childhood histiocytic disorders. Pediatr. Dev. Pathol. 7:607-614. http://dx.doi.org/10.1007/s10024-004-3027-z
11. Chow, A., B.D. Brown, and M. Merad. 2011. Studying the mononuclear phagocyte system in the molecular age. Nat. Rev. Immunol. 11:788-798. http://dx.doi.org/10.1038/nri3087
12. Chung, H., S.J. Pamp, J.A. Hill, N.K. Surana, S.M. Edelman, E.B. Troy, N.C. Reading, E.J. Villablanca, S. Wang, J.R. Mora, et al. 2012. Gut immune maturation depends on colonization with a host-specific microbiota. Cell. 149:1578-1593. http://dx.doi.org/10.1016/j.cell.2012.04.037
13. Cole, J.R., Q. Wang, E. Cardenas, J. Fish, B. Chai, R.J. Farris, A.S. Kulam-Syed-Mohideen, D.M. McGarrell, T. Marsh, G.M. Garrity, and J.M. Tiedje. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37:D141-D145. http://dx.doi.org/10.1093/nar/gkn879
14. Coombes, J.L., and F. Powrie. 2008. Dendritic cells in intestinal immune regulation. Nat. Rev. Immunol. 8:435-446. http://dx.doi.org/10.1038/nri2335
15. + regulatory T cells via a TGF-β and retinoic acid-dependent mechanism. J. Exp. Med. 204:1757-1764. http://dx.doi.org/10.1084/jem.20070590
16. Denning, T.L., Y.-C. Wang, S.R. Patel, I.R. Williams, and B. Pulendran. 2007. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat. Immunol. 8:1086-1094. http://dx.doi.org/10.1038/ni1511
17. Denning, T.L., B.A. Norris, O. Medina-Contreras, S. Manicassamy, D. Geem, R. Madan, C.L. Karp, and B. Pulendran. 2011. Functional specializations of intestinal dendritic cell and macrophage subsets that control Th17 and regulatory T cell responses are dependent on the T cell/APC ratio, source of mouse strain, and regional localization. J. Immunol. 187:733-747. http://dx.doi.org/10.4049/jimmunol.1002701
18. Diehl, G.E., R.S. Longman, J.-X. Zhang, B. Breart, C. Galan, A. Cuesta, S.R. Schwab, and D.R. Littman. 2013. Microbiota restricts trafficking of bacteria to mesenteric lymph nodes by CX(3)CR1(hi) cells. Nature. 494:116-120. http://dx.doi.org/10.1038/nature11809
19. Dresch, C., Y. Leverrier, J. Marvel, and K. Shortman. 2012. Development of antigen cross-presentation capacity in dendritic cells. Trends Immunol. 33:381-388. http://dx.doi.org/10.1016/j.it.2012.04.009
20. + conventional dendritic cells. J. Exp. Med. 207:823-836. http://dx.doi.org/10.1084/jem.20091627
21. Elinav, E., T. Strowig, A.L. Kau, J. Henao-Mejia, C.A. Thaiss, C.J. Booth, D.R. Peaper, J. Bertin, S.C. Eisenbarth, J.I. Gordon, and R.A. Flavell. 2011. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell. 145:745-757. http://dx.doi.org/10.1016/j.cell.2011.04.022
22. Excoffier, L., P.E. Smouse, and J.M. Quattro. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics. 131:479-491.
23. Fagarasan, S., M. Muramatsu, K. Suzuki, H. Nagaoka, H. Hiai, and T. Honjo. 2002. Critical roles of activation-induced cytidine deaminase in the homeostasis of gut flora. Science. 298:1424-1427. http://dx.doi.org/10.1126/science.1077336
24. +CD8alpha+ dendritic cells in the small intestine expresses TLR3, TLR7, and TLR9 and induces Th1 response and CTL activity. J. Immunol. 186:6287-6295. http://dx.doi.org/10.4049/jimmunol.1004036
25. Garrett, W.S., G.M. Lord, S. Punit, G. Lugo-Villarino, S.K. Mazmanian, S. Ito, J.N. Glickman, and L.H. Glimcher. 2007. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell. 131:33-45. http://dx.doi.org/10.1016/j.cell.2007.08.017
26. Ghilardi, N., N. Kljavin, Q. Chen, S. Lucas, A.L. Gurney, and F.J. De Sauvage. 2004. Compromised humoral and delayed-type hypersensitivity responses in IL-23-deficient mice. J. Immunol. 172:2827-2833.
27. + DCs. J. Exp. Med. 206:3115-3130. http://dx.doi.org/10.1084/jem.20091756
28. Guilliams, M., K. Crozat, S. Henri, S. Tamoutounour, P. Grenot, E. Devilard, B. de Bovis, L. Alexopoulou, M. Dalod, and B. Malissen. 2010. Skin-draining lymph nodes contain dermis-derived CD103(-) dendritic cells that constitutively produce retinoic acid and induce Foxp3(+) regulatory T cells. Blood. 115:1958-1968. http://dx.doi.org/10.1182/blood-2009-09-245274
29. + regulatory T cells in the lamina propria. Immunity. 34:237-246. http://dx.doi.org/10.1016/j.immuni.2011.01.016
30. Haley, K., B.Z. Igyártó, D. Ortner, A. Bobr, S. Kashem, D. Schenten, and D.H. Kaplan. 2012. Langerhans cells require MyD88-dependent signals for Candida albicans response but not for contact hypersensitivity or migration. J. Immunol. 188:4334-4339. http://dx.doi.org/10.4049/jimmunol.1102759
31. + nonlymphoid dendritic cells. Immunity. 37:60-73. http://dx.doi.org/10.1016/j.immuni.2012.04.012
32. Hildner, K., B.T. Edelson, W.E. Purtha, M. Diamond, H. Matsushita, M. Kohyama, B. Calderon, B.U. Schraml, E.R. Unanue, M.S. Diamond, et al. 2008. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science. 322:1097-1100. http://dx.doi.org/10.1126/science.1164206
33. Honda, K., and D.R. Littman. 2012. The microbiome in infectious disease and inflammation. Annu. Rev. Immunol. 30:759-795. http://dx.doi.org/10.1146/annurev-immunol-020711-074937
34. Hu, W., T.D. Troutman, R. Edukulla, and C. Pasare. 2011. Priming microenvironments dictate cytokine requirements for T helper 17 cell lineage commitment. Immunity. 35:1010-1022. http://dx.doi.org/10.1016/j.immuni.2011.10.013
35. Igyarto, B.Z., M.C. Jenison, J.C. Dudda, A. Roers, W. Müller, P.A. Koni, D.J. Campbell, M.J. Shlomchik, and D.H. Kaplan. 2009. Langerhans cells suppress contact hypersensitivity responses via cognate CD4 interaction and Langerhans cell-derived IL-10. J. Immunol. 183:5085-5093. http://dx.doi.org/10.4049/jimmunol.0901884
36. Ivanov, I.I., Rde.L. Frutos, N. Manel, K. Yoshinaga, D.B. Rifkin, R.B. Sartor, B.B. Finlay, and D.R. Littman. 2008. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe. 4:337-349. http://dx.doi.org/10.1016/j.chom.2008.09.009
37. Ivanov, I.I., K. Atarashi, N. Manel, E.L. Brodie, T. Shima, U. Karaoz, D. Wei, K.C. Goldfarb, C.A. Santee, S.V. Lynch, et al. 2009. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 139:485-498. http://dx.doi.org/10.1016/j.cell.2009.09.033
38. Iwasaki, A. 2007. Mucosal dendritic cells. Annu. Rev. Immunol. 25:381-418. http://dx.doi.org/10.1146/annurev.immunol.25.022106.141634
39. + dendritic cells display unique functional properties that are conserved between mice and humans. J. Exp. Med. 205:2139-2149. http://dx.doi.org/10.1084/jem.20080414
40. Kaplan, D.H., M.C. Jenison, S. Saeland, W.D. Shlomchik, and M.J. Shlomchik. 2005. Epidermal langerhans cell-deficient mice develop enhanced contact hypersensitivity. Immunity. 23:611-620. http://dx.doi.org/10.1016/j.immuni.2005.10.008
41. Kaplan, D.H., M.O. Li, M.C. Jenison, W.D. Shlomchik, R.A. Flavell, and M.J. Shlomchik. 2007. Autocrine/paracrine TGFβ1 is required for the development of epidermal Langerhans cells. J. Exp. Med. 204:2545-2552. http://dx.doi.org/10.1084/jem.20071401
42. Kaser, A., O. Ludwiczek, S. Holzmann, A.R. Moschen, G. Weiss, B. Enrich, I. Graziadei, S. Dunzendorfer, C.J. Wiedermann, E. Mürzl, et al. 2004. Increased expression of CCL20 in human inflammatory bowel disease. J. Clin. Immunol. 24:74-85. http://dx.doi.org/10.1023/B:JOCI.0000018066.46279.6b
43. Khan, M.A., S. Bouzari, C. Ma, C.M. Rosenberger, K.S.B. Bergstrom, D.L. Gibson, T.S. Steiner, and B.A. Vallance. 2008. Flagellindependent and -independent inflammatory responses following infection by enteropathogenic Escherichia coli and Citrobacter rodentium. Infect. Immun. 76:1410-1422. http://dx.doi.org/10.1128/IAI.01141-07
44. Kinnebrew, M.A., C. Ubeda, L.A. Zenewicz, N. Smith, R.A. Flavell, and E.G. Pamer. 2010. Bacterial flagellin stimulates Toll-like receptor 5-dependent defense against vancomycin-resistant Enterococcus infection. J. Infect. Dis. 201:534-543. http://dx.doi.org/10.1086/650203
45. Kinnebrew, M.A., C.G. Buffie, G.E. Diehl, L.A. Zenewicz, I. Leiner, T.M. Hohl, R.A. Flavell, D.R. Littman, and E.G. Pamer. 2012. Interleukin 23 production by intestinal CD103(+)CD11b(+) dendritic cells in response to bacterial flagellin enhances mucosal innate immune defense. Immunity. 36:276-287. http://dx.doi.org/10.1016/j.immuni.2011.12.011
46. Kissenpfennig, A., S. Henri, B. Dubois, C. Laplace-Builhé, P. Perrin, N. Romani, C.H. Tripp, P. Douillard, L. Leserman, D. Kaiserlian, et al. 2005. Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity. 22:643-654. http://dx.doi.org/10.1016/j.immuni.2005.04.004
47. Korn, T., E. Bettelli, M. Oukka, and V.K. Kuchroo. 2009. IL-17 and Th17 Cells. Annu. Rev. Immunol. 27:485-517. http://dx.doi.org/10.1146/annurev.immunol.021908.132710
48. Lewis, K.L., M.L. Caton, M. Bogunovic, M. Greter, L.T. Grajkowska, D. Ng, A. Klinakis, I.F. Charo, S. Jung, J.L. Gommerman, et al. 2011. Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity. 35:780-791. http://dx.doi.org/10.1016/j.immuni.2011.08.013
49. Lochner, M., M. Bérard, S. Sawa, S. Hauer, V. Gaboriau-Routhiau, T.D. Fernandez, J. Snel, P. Bousso, N. Cerf-Bensussan, and G. Eberl. 2011. Restricted microbiota and absence of cognate TCR antigen leads to an unbalanced generation of Th17 cells. J. Immunol. 186:1531-1537. http://dx.doi.org/10.4049/jimmunol.1001723
50. Lozupone, C., and R. Knight. 2005. UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71:8228-8235. http://dx.doi.org/10.1128/AEM.71.12.8228-8235.2005
51. Mangan, P.R., L.E. Harrington, D.B. O'Quinn, W.S. Helms, D.C. Bullard, C.O. Elson, R.D. Hatton, S.M. Wahl, T.R. Schoeb, and C.T. Weaver. 2006. Transforming growth factor-β induces development of the T(H)17 lineage. Nature. 441:231-234. http://dx.doi.org/10.1038/nature04754
52. Miller, J.C., B.D. Brown, T. Shay, E.L. Gautier, V. Jojic, A. Cohain, G. Pandey, M. Leboeuf, K.G. Elpek, J. Helft, et al; Immunological Genome Consortium. 2012. Deciphering the transcriptional network of the dendritic cell lineage. Nat. Immunol. 13:888-899. http://dx.doi.org/10.1038/ni.2370
53. Moon, J.J., H.H. Chu, M. Pepper, S.J. McSorley, S.C. Jameson, R.M. Kedl, and M.K. Jenkins. 2007. Naive CD4(+) T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity. 27:203-213. http://dx.doi.org/10.1016/j.immuni.2007.07.007
54. Nelson, R.W., J.B. McLachlan, J.R. Kurtz, and M.K. Jenkins. 2013. CD4+ T cell persistence and function after infection are maintained by lowlevel peptide:MHC class II presentation. J. Immunol. 190:2828-2834. http://dx.doi.org/10.4049/jimmunol.1202183
55. Perona-Wright, G., K. Mohrs, and M. Mohrs. 2010. Sustained signaling by canonical helper T cell cytokines throughout the reactive lymph node. Nat. Immunol. 11:520-526. http://dx.doi.org/10.1038/ni.1866
56. Persson, E.K., H. Uronen-Hansson, M. Semmrich, A. Rivollier, K. Hägerbrand, J. Marsal, S. Gudjonsson, U. Håkansson, B. Reizis, K. Kotarsky, and W.W. Agace. 2013. IRF4 transcription-factor-dependent CD103(+)CD11b(+) dendritic cells drive mucosal T helper 17 cell differentiation. Immunity. 38:958-969. http://dx.doi.org/10.1016/j.immuni.2013.03.009
57. + dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity. 38:970-983. http://dx.doi.org/10.1016/j.immuni.2013.04.011
58. Schloss, P.D., S.L. Westcott, T. Ryabin, J.R. Hall, M. Hartmann, E.B. Hollister, R.A. Lesniewski, B.B. Oakley, D.H. Parks, C.J. Robinson, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541. http://dx.doi.org/10.1128/AEM.01541-09
59. +, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J. Exp. Med. 206:3101-3114. http://dx.doi.org/10.1084/jem.20091925
60. + dendritic cells in both tolerogenic and immunogenic T-cell responses. Mucosal Immunol. 5:150-160.
61. Shaw, M.H., N. Kamada, Y.G. Kim, and G. Núñez. 2012. Microbiotainduced IL-1β, but not IL-6, is critical for the development of steady-state TH17 cells in the intestine. J. Exp. Med. 209:251-258. http://dx.doi.org/10.1084/jem.20111703
62. Sogin, M.L., H.G. Morrison, J.A. Huber, D. Mark Welch, S.M. Huse, P.R. Neal, J.M. Arrieta, and G.J. Herndl. 2006. Microbial diversity in the deep sea and the underexplored "rare biosphere". Proc. Natl. Acad. Sci. USA. 103:12115-12120. http://dx.doi.org/10.1073/pnas.0605127103
63. Sun, C.-M., J.A. Hall, R.B. Blank, N. Bouladoux, M. Oukka, J.R. Mora, and Y. Belkaid. 2007. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204:1775-1785. http://dx.doi.org/10.1084/jem.20070602
64. Ubeda, C., L. Lipuma, A. Gobourne, A. Viale, I. Leiner, M. Equinda, R. Khanin, and E.G. Pamer. 2012. Familial transmission rather than defective innate immunity shapes the distinct intestinal microbiota of TLR-deficient mice. J. Exp. Med. 209:1445-1456. http://dx.doi.org/10.1084/jem.20120504
65. Uematsu, S., K. Fujimoto, M.H. Jang, B.-G. Yang, Y.-J. Jung, M. Nishiyama, S. Sato, T. Tsujimura, M. Yamamoto, Y. Yokota, et al. 2008. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat. Immunol. 9:769-776. http://dx.doi.org/10.1038/ni.1622
66. Van Maele, L., C. Carnoy, D. Cayet, P. Songhet, L. Dumoutier, I. Ferrero, L. Janot, F. Erard, J. Bertout, H. Leger, et al. 2010. TLR5 signaling stimulates the innate production of IL-17 and IL-22 by CD3(neg)CD127+ immune cells in spleen and mucosa. J. Immunol. 185:1177-1185. http://dx.doi.org/10.4049/jimmunol.1000115
67. Varol, C., A. Vallon-Eberhard, E. Elinav, T. Aychek, Y. Shapira, H. Luche, H.J. Fehling, W.-D. Hardt, G. Shakhar, and S. Jung. 2009. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity. 31:502-512. http://dx.doi.org/10.1016/j.immuni.2009.06.025
68. Wirtz, S., C. Neufert, B. Weigmann, and M.F. Neurath. 2007. Chemically induced mouse models of intestinal inflammation. Nat. Protoc. 2:541-546. http://dx.doi.org/10.1038/nprot.2007.41
69. Zheng, Y., P.A. Valdez, D.M. Danilenko, Y. Hu, S.M. Sa, Q. Gong, A.R. Abbas, Z. Modrusan, N. Ghilardi, F.J. de Sauvage, and W. Ouyang. 2008. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14:282-289. http://dx.doi.org/10.1038/nm1720