TGF-β signaling in dendritic cells governs colonic homeostasis by controlling epithelial differentiation and the luminal microbiota

Journal of Immunology

Volumn 196, Issue 11, 2016, Pages 4603-4613

  Ihara, Sozaburo ^a   Hirata, Yoshihiro ^a   Serizawa, Takako ^a   Suzuki, Nobumi ^a   Sakitani, Kosuke ^a   Kinoshita, Hiroto ^a   Hayakawa, Yoku ^a   Nakagawa, Hayato ^a   Ijichi, Hideaki ^a   Tateishi, Keisuke ^a   Koike, Kazuhiko ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DEXTRAN SULFATE; JAGGED1; TRANSCRIPTION FACTOR HES 1; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW TRANSPLANTATION; COLON; COLON FLORA; COLON INJURY; CONTROLLED STUDY; DENDRITIC CELL; DYSBIOSIS; ENTEROBACTERIACEAE; FECES MICROFLORA; GOBLET CELL; HOMEOSTASIS; IMMUNE RESPONSE; INTESTINE EPITHELIUM; MALE; MOUSE; MOUSE STRAIN; MUCUS; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TISSUE DIFFERENTIATION; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CHEMICALLY INDUCED; COLITIS; CYTOLOGY; DISEASE MODEL; EPITHELIUM CELL; IMMUNOLOGY; INTESTINE FLORA; METABOLISM; MICROBIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CELL DIFFERENTIATION; COLITIS; COLON; DENDRITIC CELLS; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; GASTROINTESTINAL MICROBIOME; HOMEOSTASIS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84975125445     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1502548     Document Type: Article

References (48)

1. Abraham, C., and J. H. Cho. 2009. Inflammatory bowel disease. N. Engl. J. Med. 361: 2066-2078.
2. Xavier, R. J., and D. K. Podolsky. 2007. Unravelling the pathogenesis of inflammatory bowel disease. Nature 448: 427-434.
3. Jostins, L., S. Ripke, R. K. Weersma, R. H. Duerr, D. P. McGovern, K. Y. Hui, J. C. Lee, L. P. Schumm, Y. Sharma, C. A. Anderson, et al; International IBD Genetics Consortium (IIBDGC). 2012. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491: 119-124.
4. Lees, C. W., J. C. Barrett, M. Parkes, and J. Satsangi. 2011. New IBD genetics: common pathways with other diseases. Gut 60: 1739-1753.
5. Di Sabatino, A., K. M. Pickard, D. Rampton, L. Kruidenier, L. Rovedatti, N. A. Leakey, G. R. Corazza, G. Monteleone, and T. T. MacDonald. 2008. Blockade of transforming growth factor beta upregulates T-box transcription factor T-bet, and increases T helper cell type 1 cytokine and matrix metalloproteinase-3 production in the human gut mucosa. Gut 57: 605-612.
6. Monteleone, G., A. Kumberova, N. M. Croft, C. McKenzie, H. W. Steer, and T. T. MacDonald. 2001. Blocking Smad7 restores TGF-βeta1 signaling in chronic inflammatory bowel disease. J. Clin. Invest. 108: 601-609.
7. Sartor, R. B. 2008. Microbial influences in inflammatory bowel diseases. Gastroenterology 134: 577-594.
8. Garrett, W. S., C. A. Gallini, T. Yatsunenko, M. Michaud, A. DuBois, M. L. Delaney, S. Punit, M. Karlsson, L. Bry, J. N. Glickman, et al. 2010. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe 8: 292-300.
9. Qin, J., R. Li, J. Raes, M. Arumugam, K. S. Burgdorf, C. Manichanh, T. Nielsen, N. Pons, F. Levenez, T. Yamada, et al; MetaHIT Consortium. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65.
10. Goto, Y., C. Panea, G. Nakato, A. Cebula, C. Lee, M. G. Diez, T. M. Laufer, L. Ignatowicz, and I. I. Ivanov. 2014. Segmented filamentous bacteria antigens presented by intestinal dendritic cells drive mucosal Th17 cell differentiation. Immunity 40: 594-607.
11. Atarashi, K., T. Tanoue, T. Shima, A. Imaoka, T. Kuwahara, Y. Momose, G. Cheng, S. Yamasaki, T. Saito, Y. Ohba, et al. 2011. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331: 337-341.
12. Heimesaat, M. M., S. Bereswill, A. Fischer, D. Fuchs, D. Struck, J. Niebergall, H. K. Jahn, I. R. Dunay, A. Moter, D. M. Gescher, et al. 2006. Gram-negative bacteria aggravate murine small intestinal Th1-type immunopathology following oral infection with Toxoplasma gondii. J. Immunol. 177: 8785-8795.
13. Darfeuille-Michaud, A., J. Boudeau, P. Bulois, C. Neut, A. L. Glasser, N. Barnich, M. A. Bringer, A. Swidsinski, L. Beaugerie, and J. F. Colombel. 2004. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 127: 412-421.
14. Cader, M. Z., and A. Kaser. 2013. Recent advances in inflammatory bowel disease: mucosal immune cells in intestinal inflammation. Gut 62: 1653-1664.
15. + dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation. Immunity 38: 581-595.
16. Hirata, Y., L. Egea, S. M. Dann, L. Eckmann, and M. F. Kagnoff. 2010. GMCSF-facilitated dendritic cell recruitment and survival govern the intestinal mucosal response to a mouse enteric bacterial pathogen. Cell Host Microbe 7: 151-163.
17. Ramalingam, R., C. B. Larmonier, R. D. Thurston, M. T. Midura-Kiela, S. G. Zheng, F. K. Ghishan, and P. R. Kiela. 2012. Dendritic cell-specific disruption of TGF-β receptor II leads to altered regulatory T cell phenotype and spontaneous multiorgan autoimmunity. J. Immunol. 189: 3878-3893.
18. Lievens, D., K. L. Habets, A. K. Robertson, Y. Laouar, H. Winkels, T. Rademakers, L. Beckers, E. Wijnands, L. Boon, M. Mosaheb, et al. 2013. Abrogated transforming growth factor beta receptor II (TGFbRII) signalling in dendritic cells promotes immune reactivity of T cells resulting in enhanced atherosclerosis. Eur. Heart J. 34: 3717-3727.
19. Kel, J. M., M. J. Girard-Madoux, B. Reizis, and B. E. Clausen. 2010. TGF-βeta is required to maintain the pool of immature Langerhans cells in the epidermis. J. Immunol. 185: 3248-3255.
20. Chytil, A., M. A. Magnuson, C. V. Wright, and H. L. Moses. 2002. Conditional inactivation of the TGF-βeta type II receptor using Cre:Lox. Genesis 32: 73-75.
21. Caton, M. L., M. R. Smith-Raska, and B. Reizis. 2007. Notch-RBP-J signaling controls the homeostasis of CD8-dendritic cells in the spleen. J. Exp. Med. 204: 1653-1664.
22. Hayakawa, Y., Y. Hirata, H. Nakagawa, K. Sakamoto, Y. Hikiba, M. Otsuka, H. Ijichi, T. Ikenoue, K. Tateishi, M. Akanuma, et al. 2010. Apoptosis signalregulating kinase 1 regulates colitis and colitis-associated tumorigenesis by the innate immune responses. Gastroenterology 138: 1055-1067.e1051-e1054. doi: 10.1053/j.gastro.2009.11.015
23. Johansson, M. E., M. Phillipson, J. Petersson, A. Velcich, L. Holm, and G. C. Hansson. 2008. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc. Natl. Acad. Sci. USA 105: 15064-15069.
24. McCormick, D. A., L. W. Horton, and A. S. Mee. 1990. Mucin depletion in inflammatory bowel disease. J. Clin. Pathol. 43: 143-146.
25. Podolsky, D. K., and K. J. Isselbacher. 1983. Composition of human colonic mucin. Selective alteration in inflammatory bowel disease. J. Clin. Invest. 72: 142-153.
26. van Es, J. H., M. E. van Gijn, O. Riccio, M. van den Born, M. Vooijs, H. Begthel, M. Cozijnsen, S. Robine, D. J. Winton, F. Radtke, and H. Clevers. 2005. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435: 959-963.
27. Hammer, G. E., and A. Ma. 2013. Molecular control of steady-state dendritic cell maturation and immune homeostasis. Annu. Rev. Immunol. 31: 743-791.
28. Mildner, A., and S. Jung. 2014. Development and function of dendritic cell subsets. Immunity 40: 642-656.
29. Cerovic, V., S. A. Houston, C. L. Scott, A. Aumeunier, U. Yrlid, A. M. Mowat, and S. W. Milling. 2013. Intestinal CD103(-) dendritic cells migrate in lymph and prime effector T cells. Mucosal Immunol. 6: 104-113.
30. +) CD103(-) intestinal dendritic cells develop from DC-committed precursors and induce interleukin-17 production by T cells. Mucosal Immunol. 8: 327-339.
31. + T cell-induced immune colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 300: G939-G947.
32. Konkel, J. E., and W. Chen. 2011. Balancing acts: the role of TGF-β in the mucosal immune system. Trends Mol. Med. 17: 668-676.
33. Monteleone, G., M. F. Neurath, S. Ardizzone, A. Di Sabatino, M. C. Fantini, F. Castiglione, M. L. Scribano, A. Armuzzi, F. Caprioli, G. C. Sturniolo, et al. 2015. Mongersen, an oral SMAD7 antisense oligonucleotide, and Crohn's disease. N. Engl. J. Med. 372: 1104-1113.
34. Li, M. O., S. Sanjabi, and R. A. Flavell. 2006. Transforming growth factor-beta controls development, homeostasis, and tolerance of T cells by regulatory T celldependent and-independent mechanisms. Immunity 25: 455-471.
35. Marie, J. C., D. Liggitt, and A. Y. Rudensky. 2006. Cellular mechanisms of fatal early-onset autoimmunity in mice with the T cell-specific targeting of transforming growth factor-beta receptor. Immunity 25: 441-454.
36. Kim, S. C., S. L. Tonkonogy, C. A. Albright, J. Tsang, E. J. Balish, J. Braun, M. M. Huycke, and R. B. Sartor. 2005. Variable phenotypes of enterocolitis in interleukin 10-deficient mice monoassociated with two different commensal bacteria. Gastroenterology 128: 891-906.
37. Lupp, C., M. L. Robertson, M. E. Wickham, I. Sekirov, O. L. Champion, E. C. Gaynor, and B. B. Finlay. 2007. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2: 119-129.
38. Pédron, T., and P. Sansonetti. 2008. Commensals, bacterial pathogens and intestinal inflammation: an intriguing ménage à trois. Cell Host Microbe 3: 344-347.
39. Winter, S. E., M. G. Winter, M. N. Xavier, P. Thiennimitr, V. Poon, A. M. Keestra, R. C. Laughlin, G. Gomez, J. Wu, S. D. Lawhon, et al. 2013. Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science 339: 708-711.
40. Novitskiy, S. V., M. W. Pickup, A. Chytil, D. Polosukhina, P. Owens, and H. L. Moses. 2012. Deletion of TGF-β signaling in myeloid cells enhances their anti-tumorigenic properties. J. Leukoc. Biol. 92: 641-651.
41. Danese, S., and C. Fiocchi. 2011. Ulcerative colitis. N. Engl. J. Med. 365: 1713-1725.
42. Johansson, M. E., J. K. Gustafsson, J. Holmén-Larsson, K. S. Jabbar, L. Xia, H. Xu, F. K. Ghishan, F. A. Carvalho, A. T. Gewirtz, H. Sjövall, and G. C. Hansson. 2014. Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis. Gut 63: 281-291.
43. Kim, J. J., and W. I. Khan. 2013. Goblet cells and mucins: role in innate defense in enteric infections. Pathogens 2: 55-70.
44. Alkadhi, S., D. Kunde, R. Cheluvappa, S. Randall-Demllo, and R. Eri. 2014. The murine appendiceal microbiome is altered in spontaneous colitis and its pathological progression. Gut Pathog. 6: 25.
45. Miyamoto, S., and D. W. Rosenberg. 2011. Role of Notch signaling in colon homeostasis and carcinogenesis. Cancer Sci. 102: 1938-1942.
46. Sakata-Yanagimoto, M., T. Sakai, Y. Miyake, T. I. Saito, H. Maruyama, Y. Morishita, E. Nakagami-Yamaguchi, K. Kumano, H. Yagita, M. Fukayama, et al. 2011. Notch2 signaling is required for proper mast cell distribution and mucosal immunity in the intestine. Blood 117: 128-134.
47. Mathern, D. R., L. E. Laitman, Z. Hovhannisyan, D. Dunkin, S. Farsio, T. J. Malik, G. Roda, A. Chitre, A. C. Iuga, G. Yeretssian, et al. 2014. Mouse and human Notch-1 regulate mucosal immune responses. Mucosal Immunol. 7: 995-1005.
48. Gersemann, M., S. Becker, I. Kubler, M. Koslowski, G. Wang, K. R. Herrlinger, J. Griger, P. Fritz, K. Fellermann, M. Schwab, et al. 2009. Differences in goblet cell differentiation between Crohn's disease and ulcerative colitis. Differentiation 77: 84-94.