Notch2-dependent classical dendritic cells orchestrate intestinal immunity to attaching-and-effacing bacterial pathogens

Nature Immunology

Volumn 14, Issue 9, 2013, Pages 937-948

  Satpathy, Ansuman T ^a   Briseño, Carlos G ^a   Lee, Jacob S ^a   Ng, Dennis ^b   Manieri, Nicholas A ^a   Kc, Wumesh ^a   Wu, Xiaodi ^a   Thomas, Stephanie R ^a   Lee, Wan Ling ^a   Turkoz, Mustafa ^a   McDonald, Keely G ^a   Meredith, Matthew M ^c   Song, Christina ^a   Guidos, Cynthia J ^b,d   Newberry, Rodney D ^a   Ouyang, Wenjun ^e   Murphy, Theresa L ^a   Stappenbeck, Thaddeus S ^a   Gommerman, Jennifer L ^b   Nussenzweig, Michel C ^c   Colonna, Marco ^a   Kopan, Raphael ^a   Murphy, Kenneth M ^a   more..

^a WASHINGTON UNIVERSITY   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c ROCKEFELLER UNIVERSITY   (United States)

^d HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^e GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD103 ANTIGEN; CD11B ANTIGEN; INTERLEUKIN 22; INTERLEUKIN 23; NOTCH2 RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BATF3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL POPULATION; CELL SURVIVAL; CITROBACTER RODENTIUM; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; GENETIC PROCEDURES; HOST RESISTANCE; INNATE IMMUNITY; LYMPHOID CELL; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD11B; CELL DIFFERENTIATION; CITROBACTER RODENTIUM; DENDRITIC CELLS; ENTEROBACTERIACEAE INFECTIONS; HOST-PATHOGEN INTERACTIONS; INTERLEUKIN-23; INTESTINAL MUCOSA; LECTINS, C-TYPE; LYMPHOTOXIN BETA RECEPTOR; MICE; MICE, TRANSGENIC; RECEPTOR, NOTCH2; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; SPLEEN; TRANSCRIPTION FACTORS; WOUND HEALING;

EID: 84883172356     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2679     Document Type: Article

References (63)

1. Mangan, P.R. et al. Transforming growth factor-? induces development of the TH17 lineage. Nature 441, 231-234 (2006).
2. Zheng, Y. et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14, 282-289 (2008).
3. Spits, H. & Di Santo, J.P. The expanding family of innate lymphoid cells: regulators and effectors of immunity and tissue remodeling. Nat. Immunol. 12, 21-27 (2011).
4. Colonna, M. Interleukin-22-producing natural killer cells and lymphoid tissue inducer-like cells in mucosal immunity. Immunity 31, 15-23 (2009).
5. Sonnenberg, G.F. et al. CD4+ lymphoid tissue-inducer cells promote innate immunity in the gut. Immunity 34, 122-134 (2011).
6. Zheng, Y. et al. Interleukin-22, a TH17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 445, 648-651 (2007).
7. Mundy, R. et al. Citrobacter rodentium of mice and man. Cell. Microbiol. 7, 1697-1706 (2005).
8. Cella, M. et al. A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 457, 722-725 (2009).
9. Eberl, G. et al. An essential function for the nuclear receptor ROR?(t) in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 5, 64-73 (2004).
10. Sanos, S.L. et al. RORgammat and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nat. Immunol. 10, 83-91 (2009).
11. Tumanov, A.V. et al. Lymphotoxin controls the IL-22 protection pathway in gut innate lymphoid cells during mucosal pathogen challenge. Cell Host Microbe 10, 44-53 (2011).
12. Manta, C. et al. CX3CR1+ macrophages support IL-22 production by innate lymphoid cells during infection with Citrobacter rodentium. Mucosal Immunol. 6, 177-188 (2012).
13. 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).
14. Bennett, C.L. & Clausen, B.E. DC ablation in mice: promises, pitfalls, and challenges. Trends Immunol. 28, 525-531 (2007).
15. Meredith, M.M. et al. Expression of the zinc finger transcription factor zDC (Zbtb46, Btbd4) defines the classical dendritic cell lineage. J. Exp. Med. 209, 1153-1165 (2012).
16. Satpathy, A.T. et al. Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J. Exp. Med. 209, 1135-1152 (2012).
17. Hildner, K. et al. Batf3 deficiency reveals a critical role for CD8?+ dendritic cells in cytotoxic T cell immunity. Science 322, 1097-1100 (2008).
18. Lewis, K.L. et al. Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity 35, 780-791 (2011).
19. Swiecki, M. et al. Plasmacytoid dendritic cell ablation impacts early interferon responses and antiviral NK and CD8+ T cell accrual. Immunity 33, 955-966 (2010).
20. Hashimoto, D., Miller, J. & Merad, M. Dendritic cell and macrophage heterogeneity in vivo. Immunity 35, 323-335 (2011).
21. Torti, N. et al. Batf3 transcription factor-dependent DC subsets in murine CMV infection: differential impact on T-cell priming and memory inflation. Eur. J. Immunol. 41, 2612-2618 (2011).
22. Mashayekhi, M. et al. CD8a+ dendritic cells are the critical source of interleukin-12 that controls acute infection by Toxoplasma gondii tachyzoites. Immunity 35, 249-259 (2011).
23. Cervantes-Barragan, L. et al. Plasmacytoid dendritic cells control T-cell response to chronic viral infection. Proc. Natl. Acad. Sci. USA 109, 3012-3017 (2012).
24. Bogunovic, M. et al. Origin of the lamina propria dendritic cell network. Immunity 31, 513-525 (2009).
25. Varol, C. et al. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 31, 502-512 (2009).
26. Ohl, L. et al. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 21, 279-288 (2004).
27. Jakubzick, C. et al. Lymph-migrating, tissue-derived dendritic cells are minor constituents within steady-state lymph nodes. J. Exp. Med. 205, 2839-2850 (2008).
28. Randolph, G.J., Ochando, J. & Partida-Sanchez, S. Migration of dendritic cell subsets and their precursors. Annu. Rev. Immunol. 26, 293-316 (2008).
29. McKenna, H.J. et al. Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood 95, 3489-3497 (2000).
30. Boring, L. et al. Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J. Clin. Invest. 100, 2552-2561 (1997).
31. Zigmond, E. et al. Ly6C hi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity 37, 1076-1090 (2012).
32. Dudziak, D. et al. Differential antigen processing by dendritic cell subsets in vivo. Science 315, 107-111 (2007).
33. Radtke, F., Fasnacht, N. & MacDonald, H.R. Notch signaling in the immune system. Immunity 32, 14-27 (2010).
34. Edelson, B.T. et al. Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8?+ conventional dendritic cells. J. Exp. Med. 207, 823-836 (2010).
35. McDonald, K.G. et al. Dendritic cells produce CXCL13 and participate in the development of murine small intestine lymphoid tissues. Am. J. Pathol. 176, 2367-2377 (2010).
36. 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. 204, 1653-1664 (2007).
37. Waskow, C. et al. The receptor tyrosine kinase Flt3 is required for dendritic cell development in peripheral lymphoid tissues. Nat. Immunol. 9, 676-683 (2008).
38. Kabashima, K. et al. Intrinsic lymphotoxin-? receptor requirement for homeostasis of lymphoid tissue dendritic cells. Immunity 22, 439-450 (2005).
39. Summers deLuca, L. & Gommerman, J.L. Fine-tuning of dendritic cell biology by the TNF superfamily. Nat. Rev. Immunol. 12, 339-351 (2012).
40. Fütterer, A. et al. The lymphotoxin ? receptor controls organogenesis and affinity maturation in peripheral lymphoid tissues. Immunity 9, 59-70 (1998).
41. Tussiwand, R. et al. Compensatory dendritic cell development mediated by BATF-IRF interactions. Nature 490, 502-507 (2012).
42. Bajaña, S. et al. IRF4 promotes cutaneous dendritic cell migration to lymph nodes during homeostasis and inflammation. J. Immunol. 189, 3368-3377 (2012).
43. Klein, U. et al. Transcription factor IRF4 controls plasma cell differentiation and class-switch recombination. Nat. Immunol. 7, 773-782 (2006).
44. Manieri, N.A. et al. Igf2bp1 is required for full induction of Ptgs2 mRNA in colonic mesenchymal stem cells in mice. Gastroenterology 143, 110-121 (2012).
45. Brown, S.L. et al. Myd88-dependent positioning of Ptgs2-expressing stromal cells maintains colonic epithelial proliferation during injury. J. Clin. Invest. 117, 258-269 (2007).
46. Satpathy, A.T. et al. Re(de)fining the dendritic cell lineage. Nat. Immunol. 13, 1145-1154 (2012).
47. Possot, C. et al. Notch signaling is necessary for adult, but not fetal, development of ROR?t+ innate lymphoid cells. Nat. Immunol. 12, 949-958 (2011).
48. Lee, J.S. et al. AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat. Immunol. 13, 144-151 (2012).
49. Ota, N. et al. IL-22 bridges the lymphotoxin pathway with the maintenance of colonic lymphoid structures during infection with Citrobacter rodentium. Nat. Immunol. 12, 941-948 (2011).
50. Wang, Y. et al. Lymphotoxin beta receptor signaling in intestinal epithelial cells orchestrates innate immune responses against mucosal bacterial infection. Immunity 32, 403-413 (2010).
51. Kim, Y.G. et al. The Nod2 sensor promotes intestinal pathogen eradication via the chemokine CCL2-dependent recruitment of inflammatory monocytes. Immunity 34, 769-780 (2011).
52. Rivollier, A. et al. 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).
53. Basu, R. et al. Th22 cells are an important source of IL-22 for host protection against enteropathogenic bacteria. Immunity 37, 1061-1075 (2012).
54. Steinman, R.M. Decisions about dendritic cells: past, present, and future. Annu. Rev. Immunol. 30, 1-22 (2011).
55. Heng, T.S. & Painter, M.W. The Immunological Genome Project: networks of gene expression in immune cells. Nat. Immunol. 9, 1091-1094 (2008)
56. Han, H. et al. Inducible gene knockout of transcription factor recombination signal binding protein-J reveals its essential role in T versus B lineage decision. Int. Immunol. 14, 637-645 (2002).
57. Yu, H. et al. APP processing and synaptic plasticity in presenilin-1 conditional knockout mice. Neuron 31, 713-726 (2001).
58. Yin, L. et al. Defective lymphotoxin-beta receptor-induced NF-kappaB transcriptional activity in NIK-deficient mice. Science 291, 2162-2165 (2001).
59. Keskintepe, L. et al. Derivation and comparison of C57BL/6 embryonic stem cells to a widely used 129 embryonic stem cell line. Transgenic Res. 16, 751-758 (2007).
60. Schwenk, F., Baron, U. & Rajewsky, K. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res. 23, 5080-5081 (1995).
61. Robben, P.M. et al. Production of IL-12 by macrophages infected with Toxoplasma gondii depends on the parasite genotype. J. Immunol. 172, 3686-3694 (2004).
62. Akashi, K. et al. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404, 193-197 (2000).
63. Onai, N. et al. Identification of clonogenic common Flt3+M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat. Immunol. 8, 1207-1216 (2007).