Generation and transcriptional programming of intestinal dendritic cells: Essential role of retinoic acid

Mucosal Immunology

Volumn 9, Issue 1, 2016, Pages 183-193

  Zeng, R ^a,b,c   Bscheider, M ^a,b   Lahl, K ^a,b,d,e   Lee, M ^a,b   Butcher, E C ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

^c Translational Laboratory in Genetic Medicine   (Singapore)

^d TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^e LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CD135 ANTIGEN; CELL SURFACE RECEPTOR; CHEMOKINE RECEPTOR CXCR3; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; RETINOIC ACID; RETINOIC ACID RECEPTOR; TOLL LIKE RECEPTOR 3; TRANSCRIPTION FACTOR REL; ALPHA E INTEGRINS; ALPHA INTEGRIN; CD11B ANTIGEN; FLT3 LIGAND PROTEIN; LEUKOCYTE ANTIGEN; MEMBRANE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL CULTURE; CELL DIFFERENTIATION; CELL SPECIFICITY; CELL SUBPOPULATION; CLEC9A GENE; CONTROLLED STUDY; CXCR3 GENE; DENDRITIC CELL; GENE; GENE EXPRESSION; IN VITRO STUDY; MOUSE; NONHUMAN; PRE MUCOSAL DENDRITIC CELL; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION; TLR3 GENE; XCR1 GENE; ANIMAL; BAGG ALBINO MOUSE; BONE MARROW CELL; C57BL MOUSE; CELL LINEAGE; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; INTESTINE; PHENOTYPE;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD11B; BONE MARROW CELLS; CELL LINEAGE; DENDRITIC CELLS; GENE EXPRESSION REGULATION; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; INTEGRIN ALPHA CHAINS; INTESTINES; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PHENOTYPE; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRETINOIN;

EID: 84953341448     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2015.50     Document Type: Article

References (47)

1. Gottschalk C., et al. Batf3-dependent dendritic cells in the renal lymph node induce tolerance against circulating antigens. J. Am. Soc. Nephrol. 24, 543-549 (2013
2. Crozat K., et al. Cutting edge: expression of XCR1 defines mouse lymphoid-Tissue resident and migratory dendritic cells of the CD8alpha+ type. J. Immunol. 187, 4411-4415 (2011
3. Bachem A., et al. Expression of XCR1 characterizes the Batf3-dependent lineage of dendritic cells capable of antigen cross-presentation. Front. Immunol. 3, 214 (2012
4. Zhang J.G., et al. The dendritic cell receptor Clec9A binds damaged cells via exposed actin filaments. Immunity 36, 646-657 (2012
5. Zelenay S., et al. The dendritic cell receptor DNGR-1 controls endocytic handling of necrotic cell antigens to favor cross-priming of CTLs in virusinfected mice. J. Clin. Invest. 122, 1615-1627 (2012
6. Sancho D., et al. Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature 458, 899-903 (2009
7. 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
8. Iborra, S., Izquierdo, H.M., Martinez-Lopez, M., Blanco-Menendez, N., Reis e Sousa, C., & Sancho, D. The DC receptor DNGR-1 mediates crosspriming of CTLs during vaccinia virus infection in mice. J. Clin. Invest. 122, 1628-1643 (2012
9. Caminschi I., et al. Antibody responses initiated by Clec9A-bearing dendritic cells in normal and Batf3(-/-) mice. Mol. Immunol. 50, 9-17 (2012
10. Liu K., et al. In vivo analysis of dendritic cell development and homeostasis. Science 324, 392-397 (2009
11. Zeng R., et al. Retinoic acid regulates the development of a gut-homing precursor for intestinal dendritic cells. Mucosal. Immunol. 6, 847-856 (2013
12. Jaensson-Gyllenback E., et al. Bile retinoids imprint intestinal CD103+ dendritic cells with the ability to generate gut-Tropic T cells. Mucosal. Immunol. 4, 438-447 (2011
13. Hall, J.A., Grainger, J.R., Spencer, S.P., & Belkaid, Y. The role of retinoic acid in tolerance and immunity. Immunity 35, 13-22 (2011
14. Mora J.R., et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 314, 1157-1160 (2006
15. Sun C.M., et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204, 1775-1785 (2007
16. Hill J.A., et al. Retinoic acid enhances Foxp3 induction indirectly by relieving inhibition from CD4+CD44hi Cells. Immunity 29, 758-770 (2008
17. Iwata, M., Hirakiyama, A., Eshima, Y., Kagechika, H., Kato, C., & Song, S.Y. Retinoic acid imprints gut-homing specificity on T cells. Immunity 21, 527-538 (2004
18. Beijer, M.R., Molenaar, R., Goverse, G., Mebius, R.E., Kraal, G., & den Haan, J.M. A crucial role for retinoic acid in the development of Notchdependent murine splenic CD8-CD4-And CD4+ dendritic cells. Eur. J. Immunol. 2013)43, 1608-1616 (2013
19. Klebanoff C.A., et al. Retinoic acid controls the homeostasis of pre-cDCderived splenic and intestinal dendritic cells. J. Exp. Med. 210, 1961-1976 (2013
20. Molenaar R., et al. Expression of retinaldehyde dehydrogenase enzymes in mucosal dendritic cells and gut-draining lymph node stromal cells is controlled by dietary vitamin A. J. Immunol. 186, 1934-1942 (2011
21. Yokota A., et al. GM-CSF and IL-4 synergistically trigger dendritic cells to acquire retinoic acid-producing capacity. Int. Immunol. 21, 361-377 (2009
22. Iliev, I.D., Mileti, E., Matteoli, G., Chieppa, M., & Rescigno, M. Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal. Immunol. 2, 340-350 (2009
23. Chang S.Y., et al. Lack of retinoic acid leads to increased langerinexpressing dendritic cells in gut-Associated lymphoid tissues. Gastroenterology 138, 1468-1478 (2010). 1478 e1461-1466
24. Hashimoto, D., Miller, J., & Merad, M. Dendritic cell and macrophage heterogeneity in vivo. Immunity 35, 323-335 (2011
25. Villablanca E.J., et al. MyD88 and retinoic acid signaling pathways interact to modulate gastrointestinal activities of dendritic cells. Gastroenterology 141, 176-185 (2011
26. Mowat, A.M., & Agace, W.W. Regional specialization within the intestinal immune system. Nat. Rev. Immunol. 14, 667-685 (2014
27. Denning, T.L., et al. Functional specializations of intestinal dendritic cell and macrophage subsets that control Th17 and regulatory Tcell responses are dependent on the T cell/APC ratio, source of mouse strain, and regional localization. J. Immunol. 187, 733-747 (2011
28. 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
29. Rajaii, F., Bitzer, Z.T., Xu, Q., & Sockanathan, S. Expression of the dominant negative retinoid receptor, RAR403, alters telencephalic progenitor proliferation, survival, and cell fate specification. Dev. Biol. 316, 371-382 (2008
30. Murphy, K.M. Comment on 'Activation of beta-catenin in dendritic cells regulates immunity versus tolerance in the intestine'. Science 333, 405 (2011
31. Inaba K., et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176, 1693-1702 (1992
32. Mayer C.T., et al. Selective and efficient generation of functional Batf3-dependent CD103+ dendritic cells from mouse bone marrow. Blood 124, 3081-3091 (2014
33. Naik S.H., et al. Cutting edge: generation of splenic CD8+ and CD8-dendritic cell equivalents in Fms-like tyrosine kinase 3 ligand bone marrow cultures. J. Immunol. 174, 6592-6597 (2005
34. Bogunovic M., et al. Origin of the lamina propria dendritic cell network. Immunity 31, 513-525 (2009
35. Heng, T.S., & Painter, M.W. The Immunological Genome Project: networks of gene expression in immune cells. Nat. Immunol. 9, 1091-1094 (2008
36. 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
37. Watchmaker P.B., et al. Comparative transcriptional and functional profiling defines conserved programs of intestinal DC differentiation in humans and mice. Nat. Immunol. 15, 98-108 (2014
38. Chen E.Y., et al. Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics 14, 128 (2013
39. Soares, L.R., Tsavaler, L., Rivas, A., & Engleman, E.G. V7 (CD101) ligation inhibits TCR/CD3-induced IL-2 production by blocking Ca2+ flux and nuclear factor of activated T cell nuclear translocation. J. Immunol. 161, 209-217 (1998
40. 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
41. Bouchon, A., Facchetti, F., Weigand, M.A., & Colonna, M. TREM-1 amplifies inflammation and is a crucial mediator of septic shock. Nature 410, 1103-1107 (2001
42. Enomoto Y., et al. Characterization of leukocyte mono-immunoglobulinlike receptor 7 (LMIR7)/CLM-3 as an activating receptor: its similarities to and differences from LMIR4/CLM-5. J. Biol. Chem. 285, 35274-35283 (2010
43. Weber M.A., et al. Endogenous leukemia inhibitory factor attenuates endotoxin response. Lab. Invest. 85, 276-284 (2005
44. Caton, M.L., Smith-Raska, M.R., & Reizis, B. Notch-RBP-J signaling controls the homeostasis ofCD8-dendritic cells in the spleen. J. Exp. Med. 204, 1653-1664 (2007
45. Edelson B.T., et al. Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. J. Exp. Med. 207, 823-836 (2010
46. Persson E.K., et al. IRF4 transcription-factor-dependent CD103(+) CD11b(+) dendritic cells drive mucosal T helper 17 cell differentiation. Immunity 38, 958-969 (2013
47. Schlitzer A., et al. IRF4 transcription factor-dependent CD11b+ dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity 38, 970-983 (2013