Comparative transcriptional and functional profiling defines conserved programs of intestinal DC differentiation in humans and mice

Nature Immunology

Volumn 15, Issue 1, 2014, Pages 98-108

  Watchmaker, Payal B ^a,b   Lahl, Katharina ^a,b   Lee, Mike ^a,b   Baumjohann, Dirk ^c   Morton, John ^a   Kim, Sun Jung ^d   Zeng, Ruizhu ^a,b   Dent, Alexander ^e   Ansel, K Mark ^c   Diamond, Betty ^d   Hadeiba, Husein ^b,f   Butcher, Eugene C ^a,b,f  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^e INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f Palo Alto Institute for Research and Education   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; CD103 ANTIGEN; CD11B ANTIGEN; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CCR9; CHEMOKINE RECEPTOR CX3CR1; PROTEIN BCL 6; TOLL LIKE RECEPTOR 5; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL DIFFERENTIATION; CELL SUSPENSION; CELLULAR IMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; HELPER CELL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INTESTINE CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

EID: 84890987173     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2768     Document Type: Article

References (53)

1. Varol, C. et al. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 31, 502-512 (2009).
2. Bogunovic, M. et al. Origin of the lamina propria dendritic cell network. Immunity 31, 513-525 (2009).
3. Miller, J.C. et al. Deciphering the transcriptional network of the dendritic cell lineage. Nat. Immunol. 13, 888-899 (2012).
4. Helft, J., Ginhoux, F., Bogunovic, M. & Merad, M. Origin and functional heterogeneity of non-lymphoid tissue dendritic cells in mice. Immunol. Rev. 234, 55-75 (2010).
5. Uematsu, S. et al. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat. Immunol. 9, 769-776 (2008). (Pubitemid 351859160)
6. Kinnebrew, M.A. et al. Interleukin 23 production by intestinal CD103+CD11b+ dendritic cells in response to bacterial flagellin enhances mucosal innate immune defense. Immunity 36, 276-287 (2012).
7. Coombes, J.L. et al. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-β and retinoic acid-dependent mechanism. J. Exp. Med. 204, 1757-1764 (2007). (Pubitemid 47236314)
8. Manicassamy, S. & Pulendran, B. Dendritic cell control of tolerogenic responses. Immunol. Rev. 241, 206-227 (2011).
9. Persson, E.K. et al. IRF4 Transcription-factor-dependent CD103CD11b dendritic cells drive mucosal T helper 17 cell differentiation. Immunity 38, 958-969 (2013).
10. Lewis, K.L. et al. Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity 35, 780-791 (2011).
11. Poulin, L.F. et al. DNGR-1 is a specific and universal marker of mouse and human Batf3-dependent dendritic cells in lymphoid and nonlymphoid tissues. Blood 119, 6052-6062 (2012).
12. Haniffa, M. et al. Human tissues contain CD141hi cross-presenting dendritic cells with functional homology to mouse CD103+ nonlymphoid dendritic cells. Immunity 37, 60-73 (2012).
13. Villadangos, J.A. & Shortman, K. Found in translation: the human equivalent of mouse CD8+ dendritic cells. J. Exp. Med. 207, 1131-1134 (2010).
14. Schlitzer, A. et al. IRF4 rranscription factor-dependent CD11b dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity 38, 970-983 (2013).
15. Jaensson, E. et al. Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans. J. Exp. Med. 205, 2139-2149 (2008).
16. Mittag, D. et al. Human dendritic cell subsets from spleen and blood are similar in phenotype and function but modified by donor health status. J. Immunol. 186, 6207-6217 (2011).
17. Tamoutounour, S. et al. CD64 distinguishes macrophages from dendritic cells in the gut and reveals the Th1-inducing role of mesenteric lymph node macrophages during colitis. Eur. J. Immunol. 42, 3150-3166 (2012).
18. Denning, T.L. et al. 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 (2011).
19. Baumgart, D.C. et al. Patients with active inflammatory bowel disease lack immature peripheral blood plasmacytoid and myeloid dendritic cells. Gut 54, 228-236 (2005). (Pubitemid 40139239)
20. Hadeiba, H. et al. CCR9 expression defines tolerogenic plasmacytoid dendritic cells able to suppress acute graft-versus-host disease. Nat. Immunol. 9, 1253-1260 (2008).
21. Cerovic, V. et al. Intestinal CD103- dendritic cells migrate in lymph and prime effector T cells. Mucosal Immunol. 6, 104-113 (2013).
22. Ito, T., Carson, W.F.t., Cavassani, K.A., Connett, J.M. & Kunkel, S.L. CCR6 as a mediator of immunity in the lung and gut. Exp. Cell Res. 317, 613-619 (2011).
23. Jang, M.H. et al. CCR7 is critically important for migration of dendritic cells in intestinal lamina propria to mesenteric lymph nodes. J. Immunol. 176, 803-810 (2006). (Pubitemid 43099676)
24. Takeuchi, A. et al. CRTAM confers late-stage activation of CD8+ T cells to regulate retention within lymph node. J. Immunol. 183, 4220-4228 (2009).
25. Kobayashi, K.S. & van den Elsen, P.J. NLRC5: a key regulator of MHC class I-dependent immune responses. Nat. Rev. Immunol. 12, 813-820 (2012).
26. Bouloc, A., Bagot, M., Delaire, S., Bensussan, A. & Boumsell, L. Triggering CD101 molecule on human cutaneous dendritic cells inhibits T cell proliferation via IL-10 production. Eur. J. Immunol. 30, 3132-3139 (2000).
27. Huber, S. et al. IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine. Nature 491, 259-263 (2012).
28. Sonnenberg, G.F., Fouser, L.A. & Artis, D. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat. Immunol. 12, 383-390 (2011).
29. Bakri, Y. et al. Balance of MafB and PU.1 specifies alternative macrophage or dendritic cell fate. Blood 105, 2707-2716 (2005). (Pubitemid 40446260)
30. Liu, W. et al. CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J. Exp. Med. 203, 1701-1711 (2006). (Pubitemid 44036276)
31. Mora, J.R. Homing imprinting and immunomodulation in the gut: role of dendritic cells and retinoids. Inflamm. Bowel Dis. 14, 275-289 (2008). (Pubitemid 351288051)
32. Ivanov, I.I. et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139, 485-498 (2009).
33. Atarashi, K. et al. ATP drives lamina propria TH17 cell differentiation. Nature 455, 808-812 (2008).
34. Rivollier, A., He, J., Kole, A., Valatas, V. & Kelsall, B.L. Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J. Exp. Med. 209, 139-155 (2012).
35. Dent, A.L., Shaffer, A.L., Yu, X., Allman, D. & Staudt, L.M. Control of inflammation, cytokine expression, and germinal center formation by BCL-6. Science 276, 589-592 (1997). (Pubitemid 27193682)
36. Johnston, R.J. et al. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science 325, 1006-1010 (2009).
37. Crotty, S., Johnston, R.J. & Schoenberger, S.P. Effectors and memories: Bcl-6 and Blimp-1 in T and B lymphocyte differentiation. Nat. Immunol. 11, 114-120 (2010).
38. Miller, J.C. et al. Deciphering the transcriptional network of the dendritic cell lineage. Nat. Immunol. 13, 888-899 (2012).
39. Kim, S.J., Zou, Y.R., Goldstein, J., Reizis, B. & Diamond, B. Tolerogenic function of Blimp-1 in dendritic cells. J. Exp. Med. 208, 2193-2199 (2011).
40. Sancho, D. et al. Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature 458, 899-903 (2009).
41. Dorner, B.G. et al. Selective expression of the chemokine receptor XCR1 on cross-presenting dendritic cells determines cooperation with CD8+ T cells. Immunity 31, 823-833 (2009).
42. Galibert, L. et al. Nectin-like protein 2 defines a subset of T-cell zone dendritic cells and is a ligand for class-I-restricted T-cell-associated molecule. J. Biol. Chem. 280, 21955-21964 (2005). (Pubitemid 40827848)
43. Yeh, J.H., Sidhu, S.S. & Chan, A.C. Regulation of a late phase of T cell polarity and effector functions by Crtam. Cell 132, 846-859 (2008). (Pubitemid 351312800)
44. Sigmundsdottir, H. & Butcher, E.C. Environmental cues, dendritic cells and the programming of tissue-selective lymphocyte trafficking. Nat. Immunol. 9, 981-987 (2008).
45. Fujikado, N. et al. Dcir deficiency causes development of autoimmune diseases in mice due to excess expansion of dendritic cells. Nat. Med. 14, 176-180 (2008). (Pubitemid 351214549)
46. Smythies, L.E. et al. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J. Clin. Invest. 115, 66-75 (2005). (Pubitemid 40385506)
47. Ohtsuka, H. et al. Bcl6 is required for the development of mouse CD4+ and CD8α+ dendritic cells. J. Immunol. 186, 255-263 (2011).
48. Milling, S., Yrlid, U., Cerovic, V. & MacPherson, G. Subsets of migrating intestinal dendritic cells. Immunol. Rev. 234, 259-267 (2010).
49. Bull, D.M. & Bookman, M.A. Isolation and functional characterization of human intestinal mucosal lymphoid cells. J. Clin. Invest. 59, 966-974 (1977). (Pubitemid 8096349)
50. Zeng, R. et al. Retinoic acid regulates the development of a gut-homing precursor for intestinal dendritic cells. Mucosal Immunol. 6, 847-856 (2013).
51. Kitano, M. et al. Bcl6 protein expression shapes pre-germinal center B cell dynamics and follicular helper T cell heterogeneity. Immunity 34, 961-972 (2011).
52. Rutishauser, R.L. et al. Transcriptional repressor Blimp-1 promotes CD8+ T cell terminal differentiation and represses the acquisition of central memory T cell properties. Immunity 31, 296-308 (2009).
53. Suzuki, R. & Shimodaira, H. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22, 1540-1542 (2006). (Pubitemid 43985330)