IL-22 receptor signaling in Paneth cells is critical for their maturation, microbiota colonization, Th17-related immune responses, and anti-Salmonella immunity.
Animals
Cell Differentiation
Immunity, Mucosal
Interleukins
/ genetics
Lymphocyte Activation
Mice
Mice, Inbred C57BL
Mice, Knockout
Microbiota
/ physiology
Paneth Cells
/ metabolism
Receptors, Interleukin
/ genetics
Salmonella typhi
/ physiology
Signal Transduction
Th17 Cells
/ immunology
Typhoid Fever
/ immunology
Interleukin-22
Journal
Mucosal immunology
ISSN: 1935-3456
Titre abrégé: Mucosal Immunol
Pays: United States
ID NLM: 101299742
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
03
10
2019
accepted:
10
09
2020
revised:
11
08
2020
pubmed:
17
10
2020
medline:
30
11
2021
entrez:
16
10
2020
Statut:
ppublish
Résumé
Interleukin-22 (IL-22) signaling in the intestines is critical for promoting tissue-protective functions. However, since a diverse array of cell types (absorptive and secretory epithelium as well as stem cells) express IL-22Ra1, a receptor for IL-22, it has been difficult to determine what cell type(s) specifically respond to IL-22 to mediate intestinal mucosal host defense. Here, we report that IL-22 signaling in the small intestine is positively correlated with Paneth cell differentiation programs. Our Il22Ra1
Identifiants
pubmed: 33060802
doi: 10.1038/s41385-020-00348-5
pii: S1933-0219(22)00139-8
pmc: PMC7946635
mid: NIHMS1632369
doi:
Substances chimiques
Interleukins
0
Receptors, Interleukin
0
interleukin-22 receptor
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
389-401Subventions
Organisme : NIAID NIH HHS
ID : R01 AI101221
Pays : United States
Organisme : NIAID NIH HHS
ID : T32 AI007539
Pays : United States
Organisme : NIAID NIH HHS
ID : R21 AI128372
Pays : United States
Organisme : NIAID NIH HHS
ID : R21 AI149257
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI153280
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK121798
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK088199
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA045508
Pays : United States
Organisme : NIAID NIH HHS
ID : R21 AI146696
Pays : United States
Références
Zheng, Y. et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14, 282–289 (2008).
pubmed: 18264109
Zenewicz, L. A. et al. Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease. Immunity 29, 947–957 (2008).
pubmed: 19100701
pmcid: 3269819
Shih, V. F. S. et al. Homeostatic IL-23 receptor signaling limits Th17 response through IL-22-mediated containment of commensal microbiota. Proc. Natl Acad. Sci. USA 111, 13942–13947 (2014).
pubmed: 25201978
Sugimoto, K. et al. IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis. J. Clin. Invest. 118, 534–544 (2008).
pubmed: 18172556
pmcid: 2157567
Zindl, C. L. et al. IL-22-producing neutrophils contribute to antimicrobial defense and restitution of colonic epithelial integrity during colitis. Proc. Natl Acad. Sci. USA 110, 12768–12773 (2013).
pubmed: 23781104
Monteleone, I. et al. Aryl hydrocarbon receptor-induced signals up-regulate IL-22 production and inhibit inflammation in the gastrointestinal tract. Gastroenterology 141, 237–248 (2011). 248.e231.
pubmed: 21600206
Pham, T. A. et al. Epithelial IL-22RA1-mediated fucosylation promotes intestinal colonization resistance to an opportunistic pathogen. Cell Host Microbe 16, 504–516 (2014).
pubmed: 25263220
pmcid: 4190086
Kryczek, I. et al. IL-22(+)CD4(+) T cells promote colorectal cancer stemness via STAT3 transcription factor activation and induction of the methyltransferase DOT1L. Immunity 40, 772–784 (2014).
pubmed: 4032366
pmcid: 4032366
Ji, Y. et al. IL-22 promotes the migration and invasion of gastric cancer cells via IL-22R1/AKT/MMP-9 signaling. Int J. Clin. Exp. Pathol. 7, 3694–3703 (2014).
pubmed: 25120745
pmcid: 4128980
Huber, S. et al. IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine. Nature 491, 259–263 (2012).
pubmed: 3493690
pmcid: 3493690
Jinnohara, T. et al. IL-22BP dictates characteristics of Peyer’s patch follicle-associated epithelium for antigen uptake. J. Exp. Med. 214, 1607–1618 (2017).
pubmed: 28512157
pmcid: 5460992
Lindemans, C. A. et al. Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature 528, 560–564 (2015).
pubmed: 26649819
pmcid: 4720437
Salzman, N. H. et al. Enteric defensins are essential regulators of intestinal microbial ecology. Nat. Immunol. 11, 76–82 (2010).
pubmed: 19855381
Liu, T. C. et al. Paneth cell defects in Crohn’s disease patients promote dysbiosis. JCI Insight 1, e86907 (2016).
pubmed: 27699268
pmcid: 5033844
Vaishnava, S., Behrendt, C. L., Ismail, A. S., Eckmann, L. & Hooper, L. V. Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc. Natl Acad. Sci. USA 105, 20858–20863 (2008).
pubmed: 19075245
Fujino, S. et al. Increased expression of interleukin 17 in inflammatory bowel disease. Gut 52, 65–70 (2003).
pubmed: 12477762
pmcid: 1773503
Fellermann, K., Wehkamp, J., Herrlinger, K. R. & Stange, E. F. Crohn’s disease: a defensin deficiency syndrome? Eur. J. Gastroenterol. Hepatol. 15, 627–634 (2003).
pubmed: 12840673
Gronke, K. et al. Interleukin-22 protects intestinal stem cells against genotoxic stress. Nature 566, 249–253 (2019).
pubmed: 30700914
pmcid: 6420091
Zwarycz, B. et al. IL22 inhibits epithelial stem cell expansion in an ileal organoid model. Cell Mol. Gastroenterol. Hepatol. 7, 1–17 (2019).
pubmed: 30364840
Fevr, T., Robine, S., Louvard, D. & Huelsken, J. Wnt/beta-catenin is essential for intestinal homeostasis and maintenance of intestinal stem cells. Mol. Cell Biol. 27, 7551–7559 (2007).
pubmed: 17785439
pmcid: 2169070
van Es, J. H. et al. A critical role for the Wnt effector Tcf4 in adult intestinal homeostatic self-renewal. Mol. Cell Biol. 32, 1918–1927 (2012).
pubmed: 22393260
pmcid: 3347420
Sato, T. et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469, 415–418 (2011).
pubmed: 21113151
Behnsen, J. et al. The cytokine IL-22 promotes pathogen colonization by suppressing related commensal bacteria. Immunity 40, 262–273 (2014).
pubmed: 24508234
pmcid: 3964146
Goto, Y. et al. Innate lymphoid cells regulate intestinal epithelial cell glycosylation. Science 345, 1254009 (2014).
pubmed: 25214634
pmcid: 4774895
Bel, S. et al. Paneth cells secrete lysozyme via secretory autophagy during bacterial infection of the intestine. Science 357, 1047–1051 (2017).
pubmed: 28751470
pmcid: 5702267
Salzman, N. H., Ghosh, D., Huttner, K. M., Paterson, Y. & Bevins, C. L. Protection against enteric salmonellosis in transgenic mice expressing a human intestinal defensin. Nature 422, 522–526 (2003).
pubmed: 12660734
Salzman, N. H. Paneth cell defensins and the regulation of the microbiome: Détente at mucosal surfaces. Gut Microbes 1, 401–406 (2010).
pubmed: 21468224
pmcid: 3056107
Sano, T. et al. An IL-23R/IL-22 circuit regulates epithelial serum amyloid A to promote local effector Th17 responses. Cell 164, 324 (2016).
pubmed: 28915371
Kumar, P. et al. Intestinal interleukin-17 receptor signaling mediates reciprocal control of the gut microbiota and autoimmune inflammation. Immunity 44, 659–671 (2016).
pubmed: 26982366
pmcid: 4794750
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 (2011).
pubmed: 22101730
pmcid: 3468413
Liu, X., Lu, R., Wu, S. & Sun, J. Salmonella regulation of intestinal stem cells through the Wnt/beta-catenin pathway. FEBS Lett. 584, 911–916 (2010).
pubmed: 20083111
pmcid: 2829849
Durand, A. et al. Functional intestinal stem cells after Paneth cell ablation induced by the loss of transcription factor Math1 (Atoh1). Proc. Natl Acad. Sci. USA 109, 8965–8970 (2012).
pubmed: 22586121
Bry, L. et al. Paneth cell differentiation in the developing intestine of normal and transgenic mice. Proc. Natl Acad. Sci. USA 91, 10335–10339 (1994).
pubmed: 7937951
Mao, K. et al. Innate and adaptive lymphocytes sequentially shape the gut microbiota and lipid metabolism. Nature 554, 255–259 (2018).
pubmed: 29364878
Zha, J.-M. et al. Interleukin 22 expands transit-amplifying cells while depleting Lgr5+ stem cells via inhibition of Wnt and notch signaling. Cell. Mol. Gastroenterol. Hepatol. 7, 255–274 (2019).
pubmed: 30686779
Greicius, G. et al. PDGFRalpha(+) pericryptal stromal cells are the critical source of Wnts and RSPO3 for murine intestinal stem cells in vivo. Proc. Natl Acad. Sci. USA 115, E3173–E3181 (2018).
pubmed: 29559533
Fukui, H. et al. IL-22 produced by cancer-associated fibroblasts promotes gastric cancer cell invasion via STAT3 and ERK signaling. Br. J. Cancer 111, 763–771 (2014).
pubmed: 24937671
pmcid: 4134496
Cantwell, M. T. et al. STAT3 suppresses Wnt/beta-catenin signaling during the induction phase of primary Myf5+ brown adipogenesis. Cytokine 111, 434–444 (2018).
pubmed: 29934048
pmcid: 6289720
Chen, M. W. et al. The STAT3-miRNA-92-Wnt signaling pathway regulates spheroid formation and malignant progression in ovarian cancer. Cancer Res. 77, 1955–1967 (2017).
pubmed: 28209618
Fragoso, M. A. et al. The Wnt/beta-catenin pathway cross-talks with STAT3 signaling to regulate survival of retinal pigment epithelium cells. PLoS ONE 7, e46892 (2012).
pubmed: 23056515
pmcid: 3464242
Kim, T. H., Escudero, S. & Shivdasani, R. A. Intact function of Lgr5 receptor-expressing intestinal stem cells in the absence of Paneth cells. Proc. Natl Acad. Sci. USA 109, 3932–3937 (2012).
pubmed: 22355124
Pearce, S. C. et al. Marked differences in tight junction composition and macromolecular permeability among different intestinal cell types. BMC Biol. 16, 19 (2018).
pubmed: 29391007
pmcid: 5793346
Vaishnava, S. et al. The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science 334, 255–258 (2011).
pubmed: 21998396
pmcid: 3321924
Yu, S. et al. Paneth cell multipotency induced by notch activation following injury. Cell Stem Cell 23, 46–59.e45 (2018).
pubmed: 29887318
pmcid: 6035085
Zheng, M. et al. Therapeutic role of interleukin 22 in experimental intra-abdominal klebsiella pneumoniae infection in mice. Infect. Immun. 84, 782–789 (2016).
pubmed: 26729763
pmcid: 4771339
Croswell, A., Amir, E., Teggatz, P., Barman, M. & Salzman, N. H. Prolonged impact of antibiotics on intestinal microbial ecology and susceptibility to enteric salmonella infection. Infect. Immun. 77, 2741–2753 (2009).
pubmed: 19380465
pmcid: 2708550
Shah, R. et al. Composition and function of the pediatric colonic mucosal microbiome in untreated patients with ulcerative colitis. Gut Microbes 7, 384–396 (2016).
pubmed: 27217061
pmcid: 5046168