Commensals Suppress Intestinal Epithelial Cell Retinoic Acid Synthesis to Regulate Interleukin-22 Activity and Prevent Microbial Dysbiosis

Immunity

Volumn 49, Issue 6, 2018, Pages 1103-1115.e6

  Grizotte Lake, Mayara ^a   Zhong, Guo ^b   Duncan, Kellyanne ^a   Kirkwood, Jay ^b   Iyer, Namrata ^a   Smolenski, Irina ^a   Isoherranen, Nina ^b   Vaishnava, Shipra ^a  

^a BROWN UNIVERSITY   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

antimicrobials; colonization resistance; commensal; dysbiosis; IECs; IL 22; RA signaling; Rdh7; retinoic acid; vitamin A

Indexed keywords

INTERLEUKIN 22; POLYMYXIN B; RETINOIC ACID; RETINOL DEHYDROGENASE; RETINOL DEHYDROGENASE 7; UNCLASSIFIED DRUG; VANCOMYCIN; ALCOHOL DEHYDROGENASE; CIS-RETINOL - ANDROGEN DEHYDROGENASE; INTERLEUKIN DERIVATIVE; INTERLEUKIN-22; RNA 16S;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL IMMUNITY; BACTERIAL LOAD; CLOSTRIDIA; COMMENSAL; CONTROLLED STUDY; DYSBIOSIS; FEMALE; GENE EXPRESSION; IMMUNOFLUORESCENCE; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; METABOLITE; MICROBIAL COMMUNITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; VITAMIN METABOLISM; WESTERN BLOTTING; ANIMAL; BACTERIUM; C57BL MOUSE; CLASSIFICATION; CYTOLOGY; EPITHELIUM CELL; GENETICS; INTESTINE MUCOSA; KNOCKOUT MOUSE; LYMPHOCYTE; METABOLISM; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY; SYMBIOSIS;

ALCOHOL OXIDOREDUCTASES; ANIMALS; BACTERIA; DYSBIOSIS; EPITHELIAL CELLS; HOST MICROBIAL INTERACTIONS; INTERLEUKINS; INTESTINAL MUCOSA; LYMPHOCYTES; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROBIOTA; RNA, RIBOSOMAL, 16S; SALMONELLA TYPHIMURIUM; SYMBIOSIS; TRETINOIN;

EID: 85057741316     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2018.11.018     Document Type: Article

References (78)

1. Abt, M.C., Osborne, L.C., Monticelli, L.A., Doering, T.A., Alenghat, T., Sonnenberg, G.F., Paley, M.A., Antenus, M., Williams, K.L., Erikson, J., et al. Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity 37 (2012), 158–170.
2. Atarashi, K., Tanoue, T., Shima, T., Imaoka, A., Kuwahara, T., Momose, Y., Cheng, G., Yamasaki, S., Saito, T., Ohba, Y., et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331 (2011), 337–341.
3. Bai, A., Lu, N., Guo, Y., Liu, Z., Chen, J., Peng, Z., All-trans retinoic acid down-regulates inflammatory responses by shifting the Treg/Th17 profile in human ulcerative and murine colitis. J. Leukoc. Biol. 86 (2009), 959–969.
4. Barthel, M., Hapfelmeier, S., Quintanilla-Martínez, L., Kremer, M., Rohde, M., Hogardt, M., Pfeffer, K., Rüssmann, H., Hardt, W.-D., Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect. Immun. 71 (2003), 2839–2858.
5. Behnsen, J., Jellbauer, S., Wong, C.P., Edwards, R.A., George, M.D., Ouyang, W., Raffatellu, M., The cytokine IL-22 promotes pathogen colonization by suppressing related commensal bacteria. Immunity 40 (2014), 262–273.
6. Belzer, C., Liu, Q., Carroll, M.C., Bry, L., The role of specific iGG and complement in combating a primary mucosal infection of the gut epithelium. Eur. J. Microbiol. Immunol. (Bp.) 1 (2011), 311–318.
7. Bhattacharya, N., Yuan, R., Prestwood, T.R., Penny, H.L., DiMaio, M.A., Reticker-Flynn, N.E., Krois, C.R., Kenkel, J.A., Pham, T.D., Carmi, Y., et al. Normalizing microbiota-induced retinoic acid deficiency stimulates protective CD8(+) T cell-mediated immunity in colorectal cancer. Immunity 45 (2016), 641–655.
8. Callahan, B., Proctor, D., Relman, D., Fukuyama, J., Holmes, S., Reproducible Research Workflow in R for the Analysis of Personalized Human Microbiome Data. Pac. Symp. Biocomput. 21 (2016), 183–194.
9. Cash, H.L., Whitham, C.V., Behrendt, C.L., Hooper, L.V., Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313 (2006), 1126–1130.
10. Chelstowska, S., Widjaja-Adhi, M.A., Silvaroli, J.A., Golczak, M., Molecular basis for vitamin A uptake and storage in vertebrates. Nutrients, 8, 2016, 8.
11. Costa, M.M., Saraceni, P.R., Forn-Cuní G., Dios, S., Romero, A., Figueras, A., Novoa, B., IL-22 is a key player in the regulation of inflammation in fish and involves innate immune cells and PI3K signaling. Dev. Comp. Immunol. 41 (2013), 746–755.
12. Cullen, T.W., Schofield, W.B., Barry, N.A., Putnam, E.E., Rundell, E.A., Trent, M.S., Degnan, P.H., Booth, C.J., Yu, H., Goodman, A.L., Gut microbiota. Antimicrobial peptide resistance mediates resilience of prominent gut commensals during inflammation. Science 347 (2015), 170–175.
13. D'Ambrosio, D.N., Clugston, R.D., Blaner, W.S., Vitamin A metabolism: an update. Nutrients 3 (2011), 63–103.
14. DePaolo, R.W., Abadie, V., Tang, F., Fehlner-Peach, H., Hall, J.A., Wang, W., Marietta, E.V., Kasarda, D.D., Waldmann, T.A., Murray, J.A., et al. Co-adjuvant effects of retinoic acid and IL-15 induce inflammatory immunity to dietary antigens. Nature 471 (2011), 220–224.
15. Duerkop, B.A., Vaishnava, S., Hooper, L.V., Immune responses to the microbiota at the intestinal mucosal surface. Immunity 31 (2009), 368–376.
16. Eidenschenk, C., Rutz, S., Liesenfeld, O., Ouyang, W., Role of IL-22 in microbial host defense. Curr. Top. Microbiol. Immunol. 380 (2014), 213–236.
17. Erkelens, M.N., Mebius, R.E., Retinoic acid and immune homeostasis: a balancing act. Trends Immunol. 38 (2017), 168–180.
18. Fahlgren, A., Hammarström, S., Danielsson, A., Hammarström, M.L., Increased expression of antimicrobial peptides and lysozyme in colonic epithelial cells of patients with ulcerative colitis. Clin. Exp. Immunol. 131 (2003), 90–101.
19. Fengming, Y., Jianbing, W., Biomarkers of inflammatory bowel disease. Dis. Markers, 2014, 2014, 710915.
20. Fransén, K., Franzén, P., Magnuson, A., Elmabsout, A.A., Nyhlin, N., Wickbom, A., Curman, B., Törkvist, L., D'Amato, M., Bohr, J., et al. Polymorphism in the retinoic acid metabolizing enzyme CYP26B1 and the development of Crohn's disease. PLoS ONE, 8, 2013, e72739.
21. Geboes, L., Dumoutier, L., Kelchtermans, H., Schurgers, E., Mitera, T., Renauld, J.C., Matthys, P., Proinflammatory role of the Th17 cytokine interleukin-22 in collagen-induced arthritis in C57BL/6 mice. Arthritis Rheum. 60 (2009), 390–395.
22. Goverse, G., Labao-Almeida, C., Ferreira, M., Molenaar, R., Wahlen, S., Konijn, T., Koning, J., Veiga-Fernandes, H., Mebius, R.E., Vitamin A controls the presence of RORγ+ innate lymphoid cells and lymphoid tissue in the small intestine. J. Immunol. 196 (2016), 5148–5155.
23. Hall, J.A., Cannons, J.L., Grainger, J.R., Dos Santos, L.M., Hand, T.W., Naik, S., Wohlfert, E.A., Chou, D.B., Oldenhove, G., Robinson, M., et al. Essential role for retinoic acid in the promotion of CD4(+) T cell effector responses via retinoic acid receptor alpha. Immunity 34 (2011), 435–447.
24. Hill, J.A., Hall, J.A., Sun, C.M., Cai, Q., Ghyselinck, N., Chambon, P., Belkaid, Y., Mathis, D., Benoist, C., Retinoic acid enhances Foxp3 induction indirectly by relieving inhibition from CD4+CD44hi Cells. Immunity 29 (2008), 758–770.
25. Ho, S., Pothoulakis, C., Koon, H.W., Antimicrobial peptides and colitis. Curr. Pharm. Des. 19 (2013), 40–47.
26. Hong, K., Zhang, Y., Guo, Y., Xie, J., Wang, J., He, X., Lu, N., Bai, A., All-trans retinoic acid attenuates experimental colitis through inhibition of NF-κB signaling. Immunol. Lett. 162:1 Pt A (2014), 34–40.
27. Huber, S., Gagliani, N., Zenewicz, L.A., Huber, F.J., Bosurgi, L., Hu, B., Hedl, M., Zhang, W., O'Connor, W. Jr., Murphy, A.J., et al. IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine. Nature 491 (2012), 259–263.
28. Hurst, R.J., Else, K.J., The retinoic acid-producing capacity of gut dendritic cells and macrophages is reduced during persistent T. muris infection. Parasite Immunol. 35 (2013), 229–233.
29. Ivanov, I.I., McKenzie, B.S., Zhou, L., Tadokoro, C.E., Lepelley, A., Lafaille, J.J., Cua, D.J., Littman, D.R., The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126 (2006), 1121–1133.
30. Iwata, M., Hirakiyama, A., Eshima, Y., Kagechika, H., Kato, C., Song, S.Y., Retinoic acid imprints gut-homing specificity on T cells. Immunity 21 (2004), 527–538.
31. Jaensson, E., Uronen-Hansson, H., Pabst, O., Eksteen, B., Tian, J., Coombes, J.L., Berg, P.L., Davidsson, T., Powrie, F., Johansson-Lindbom, B., Agace, W.W., Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans. J. Exp. Med. 205 (2008), 2139–2149.
32. Jaensson-Gyllenbäck, E., Kotarsky, K., Zapata, F., Persson, E.K., Gundersen, T.E., Blomhoff, R., Agace, W.W., Bile retinoids imprint intestinal CD103+ dendritic cells with the ability to generate gut-tropic T cells. Mucosal Immunol. 4 (2011), 438–447.
33. Jason, J., Archibald, L.K., Nwanyanwu, O.C., Sowell, A.L., Buchanan, I., Larned, J., Bell, M., Kazembe, P.N., Dobbie, H., Jarvis, W.R., Vitamin A levels and immunity in humans. Clin. Diagn. Lab. Immunol. 9 (2002), 616–621.
34. Kane, M.A., Napoli, J.L., Quantification of endogenous retinoids. Methods Mol. Biol. 652 (2010), 1–54.
35. Kawaguchi, R., Yu, J., Honda, J., Hu, J., Whitelegge, J., Ping, P., Wiita, P., Bok, D., Sun, H., A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A. Science 315 (2007), 820–825.
36. Kinnebrew, M.A., Ubeda, C., Zenewicz, L.A., Smith, N., Flavell, R.A., Pamer, E.G., Bacterial flagellin stimulates Toll-like receptor 5-dependent defense against vancomycin-resistant Enterococcus infection. J. Infect. Dis. 201 (2010), 534–543.
37. Koh, A., De Vadder, F., Kovatcheva-Datchary, P., Bäckhed, F., From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 165 (2016), 1332–1345.
38. Krautkramer, K.A., Kreznar, J.H., Romano, K.A., Vivas, E.I., Barrett-Wilt, G.A., Rabaglia, M.E., Keller, M.P., Attie, A.D., Rey, F.E., Denu, J.M., Diet-microbiota interactions mediate global epigenetic programming in multiple host tissues. Mol. Cell 64 (2016), 982–992.
39. Lampen, A., Meyer, S., Arnhold, T., Nau, H., Metabolism of vitamin A and its active metabolite all-trans-retinoic acid in small intestinal enterocytes. J. Pharmacol. Exp. Ther. 295 (2000), 979–985.
40. Larange, A., Cheroutre, H., Retinoic acid and retinoic acid receptors as pleiotropic modulators of the immune system. Annu. Rev. Immunol. 34 (2016), 369–394.
41. Lozupone, C., Knight, R., UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71 (2005), 8228–8235.
42. Magnusson, M.K., Brynjólfsson, S.F., Dige, A., Uronen-Hansson, H., Börjesson, L.G., Bengtsson, J.L., Gudjonsson, S., Öhman, L., Agnholt, J., Sjövall, H., et al. Macrophage and dendritic cell subsets in IBD: ALDH+ cells are reduced in colon tissue of patients with ulcerative colitis regardless of inflammation. Mucosal Immunol. 9 (2016), 171–182.
43. McDonald, K.G., Leach, M.R., Brooke, K.W., Wang, C., Wheeler, L.W., Hanly, E.K., Rowley, C.W., Levin, M.S., Wagner, M., Li, E., Newberry, R.D., Epithelial expression of the cytosolic retinoid chaperone cellular retinol binding protein II is essential for in vivo imprinting of local gut dendritic cells by lumenal retinoids. Am. J. Pathol. 180 (2012), 984–997.
44. McMurdie, P.J., Holmes, S., phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE, 8, 2013, e61217.
45. Mielke, L.A., Jones, S.A., Raverdeau, M., Higgs, R., Stefanska, A., Groom, J.R., Misiak, A., Dungan, L.S., Sutton, C.E., Streubel, G., et al. Retinoic acid expression associates with enhanced IL-22 production by γδ T cells and innate lymphoid cells and attenuation of intestinal inflammation. J. Exp. Med. 210 (2013), 1117–1124.
46. Miki, T., Goto, R., Fujimoto, M., Okada, N., Hardt, W.D., The bactericidal lectin RegIIIβ prolongs gut colonization and enteropathy in the streptomycin mouse model for Salmonella diarrhea. Cell Host Microbe 21 (2017), 195–207.
47. Monteleone, I., Rizzo, A., Sarra, M., Sica, G., Sileri, P., Biancone, L., MacDonald, T.T., Pallone, F., Monteleone, G., Aryl hydrocarbon receptor-induced signals up-regulate IL-22 production and inhibit inflammation in the gastrointestinal tract. Gastroenterology 141 (2011), 237–248, 248.e1.
48. Mora, J.R., Iwata, M., Eksteen, B., Song, S.Y., Junt, T., Senman, B., Otipoby, K.L., Yokota, A., Takeuchi, H., Ricciardi-Castagnoli, P., et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 314 (2006), 1157–1160.
49. Mucida, D., Park, Y., Kim, G., Turovskaya, O., Scott, I., Kronenberg, M., Cheroutre, H., Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317 (2007), 256–260.
50. Mullin, G.E., Vitamin A and immunity. Nutr. Clin. Pract. 26 (2011), 495–496.
51. Nicholson, J.K., Holmes, E., Kinross, J., Burcelin, R., Gibson, G., Jia, W., Pettersson, S., Host-gut microbiota metabolic interactions. Science 336 (2012), 1262–1267.
52. Nolting, J., Daniel, C., Reuter, S., Stuelten, C., Li, P., Sucov, H., Kim, B.G., Letterio, J.J., Kretschmer, K., Kim, H.J., von Boehmer, H., Retinoic acid can enhance conversion of naive into regulatory T cells independently of secreted cytokines. J. Exp. Med. 206 (2009), 2131–2139.
53. Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, P., Henry, M., Stevens, H., et al. (2018). vegan: Community Ecology Package. R package version 2.5-3. http://CRAN.R-project.org/package=vegan.
54. Peterson, L.W., Artis, D., Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat. Rev. Immunol. 14 (2014), 141–153.
55. Pino-Lagos, K., Guo, Y., Brown, C., Alexander, M.P., Elgueta, R., Bennett, K.A., De Vries, V., Nowak, E., Blomhoff, R., Sockanathan, S., et al. A retinoic acid-dependent checkpoint in the development of CD4+ T cell-mediated immunity. J. Exp. Med. 208 (2011), 1767–1775.
56. Qiu, J., Heller, J.J., Guo, X., Chen, Z.M., Fish, K., Fu, Y.X., Zhou, L., The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity 36 (2012), 92–104.
57. Rankin, L.C., Girard-Madoux, M.J., Seillet, C., Mielke, L.A., Kerdiles, Y., Fenis, A., Wieduwild, E., Putoczki, T., Mondot, S., Lantz, O., et al. Complementarity and redundancy of IL-22-producing innate lymphoid cells. Nat. Immunol. 17 (2016), 179–186.
58. Rivera-Chávez, F., Zhang, L.F., Faber, F., Lopez, C.A., Byndloss, M.X., Olsan, E.E., Xu, G., Velazquez, E.M., Lebrilla, C.B., Winter, S.E., Bäumler, A.J., Depletion of butyrate-producing Clostridia from the gut microbiota drives an aerobic luminal expansion of Salmonella. Cell Host Microbe 19 (2016), 443–454.
59. Ross, A.C., Vitamin A and retinoic acid in T cell-related immunity. Am. J. Clin. Nutr. 96 (2012), 1166S–1172S.
60. Rubino, S.J., Geddes, K., Girardin, S.E., Innate IL-17 and IL-22 responses to enteric bacterial pathogens. Trends Immunol. 33 (2012), 112–118.
61. Sawa, S., Lochner, M., Satoh-Takayama, N., Dulauroy, S., Bérard, M., Kleinschek, M., Cua, D., Di Santo, J.P., Eberl, G., RORγt+ innate lymphoid cells regulate intestinal homeostasis by integrating negative signals from the symbiotic microbiota. Nat. Immunol. 12 (2011), 320–326.
62. Sirisinha, S., The pleiotropic role of vitamin A in regulating mucosal immunity. Asian Pac. J. Allergy Immunol. 33 (2015), 71–89.
63. Sonnenberg, G.F., Nair, M.G., Kirn, T.J., Zaph, C., Fouser, L.A., Artis, D., Pathological versus protective functions of IL-22 in airway inflammation are regulated by IL-17A. J. Exp. Med. 207 (2010), 1293–1305.
64. 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 (2011), 383–390.
65. Su, J., Chai, X., Kahn, B., Napoli, J.L., cDNA cloning, tissue distribution, and substrate characteristics of a cis-Retinol/3alpha-hydroxysterol short-chain dehydrogenase isozyme. J. Biol. Chem. 273 (1998), 17910–17916.
66. Tomita, K., Sato, M., Kajiwara, K., Tanaka, M., Tamiya, G., Makino, S., Tomizawa, M., Mizutani, A., Kuwano, Y., Shiina, T., et al. Gene structure and promoter for Crad2 encoding mouse cis-retinol/3alpha-hydroxysterol short-chain dehydrogenase isozyme. Gene 251 (2000), 175–186.
67. 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 (2008), 20858–20863.
68. Vaishnava, S., Yamamoto, M., Severson, K.M., Ruhn, K.A., Yu, X., Koren, O., Ley, R., Wakeland, E.K., Hooper, L.V., The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science 334 (2011), 255–258.
69. van de Pavert, S.A., Mebius, R.E., New insights into the development of lymphoid tissues. Nat. Rev. Immunol. 10 (2010), 664–674.
70. van de Pavert, S.A., Ferreira, M., Domingues, R.G., Ribeiro, H., Molenaar, R., Moreira-Santos, L., Almeida, F.F., Ibiza, S., Barbosa, I., Goverse, G., et al. Maternal retinoids control type 3 innate lymphoid cells and set the offspring immunity. Nature 508 (2014), 123–127.
71. Velazquez, E.M., Rivera-Chávez, F., Bäumler, A.J., Spore preparation protocol for enrichment of Clostridia from murine intestine. Biol. Protocol, 7, 2017, e2296.
72. Vicente-Suarez, I., Larange, A., Reardon, C., Matho, M., Feau, S., Chodaczek, G., Park, Y., Obata, Y., Gold, R., Wang-Zhu, Y., et al. Unique lamina propria stromal cells imprint the functional phenotype of mucosal dendritic cells. Mucosal Immunol. 8 (2015), 141–151.
73. Voss, E., Wehkamp, J., Wehkamp, K., Stange, E.F., Schröder, J.M., Harder, J., NOD2/CARD15 mediates induction of the antimicrobial peptide human beta-defensin-2. J. Biol. Chem. 281 (2006), 2005–2011.
74. Vrieze, A., Out, C., Fuentes, S., Jonker, L., Reuling, I., Kootte, R.S., van Nood, E., Holleman, F., Knaapen, M., Romijn, J.A., et al. Impact of oral vancomycin on gut microbiota, bile acid metabolism, and insulin sensitivity. J. Hepatol. 60 (2014), 824–831.
75. Winter, S.E., Lopez, C.A., Bäumler, A.J., The dynamics of gut-associated microbial communities during inflammation. EMBO Rep. 14 (2013), 319–327.
76. Xiao, L., Feng, Q., Liang, S., Sonne, S.B., Xia, Z., Qiu, X., Li, X., Long, H., Zhang, J., Zhang, D., et al. A catalog of the mouse gut metagenome. Nat. Biotechnol. 33 (2015), 1103–1108.
77. Zheng, Y., Danilenko, D.M., Valdez, P., Kasman, I., Eastham-Anderson, J., Wu, J., Ouyang, W., Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 445 (2007), 648–651.
78. Zheng, Y., Valdez, P.A., Danilenko, D.M., Hu, Y., Sa, S.M., Gong, Q., Abbas, A.R., Modrusan, Z., Ghilardi, N., de Sauvage, F.J., Ouyang, W., Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14 (2008), 282–289.