Top

Published in:

01-07-2018 | Review

AHR signaling in the development and function of intestinal immune cells and beyond

Authors: Luisa Cervantes-Barragan, Marco Colonna

Published in: Seminars in Immunopathology | Issue 4/2018

Abstract

The intestinal immune system is challenged daily with the task of recognizing and eliminating pathogens while simultaneously tolerating dietary and commensal antigens. All components must effectively coordinate to differentiate a continual barrage of environmental cues and mount appropriate responses dependent on the nature of the stimuli encountered. Playing a pivotal role, the aryl hydrocarbon receptor (AHR) is a chemical sensor that detects both dietary and microbial cues and is important for development, maintenance, and function of several types of intestinal immune cells, particularly innate lymphoid cells (ILCs) and T cells. In this review, we will highlight recent advances in our knowledge of the role of AHR signaling in ILCs, T cells, B cells, and dendritic cells.

Gu YZ, Hogenesch JB, Bradfield CA (2000) The PAS superfamily: sensors of environmental and developmental signals. Annu Rev Pharmacol Toxicol 40:519–561CrossRefPubMed

McIntosh BE, Hogenesch JB, Bradfield CA (2010) Mammalian Per-Arnt-Sim proteins in environmental adaptation. Annu Rev Physiol 72:625–645CrossRefPubMed

Kewley RJ, Whitelaw ML, Chapman-Smith A (2004) The mammalian basic helix-loop-helix/PAS family of transcriptional regulators. Int J Biochem Cell Biol 36:189–204CrossRefPubMed

Frericks M, Meissner M, Esser C (2007) Microarray analysis of the AHR system: tissue-specific flexibility in signal and target genes. Toxicol Appl Pharmacol 220:320–332CrossRefPubMed

Perdew GH (1988) Association of the Ah receptor with the 90-kDa heat shock protein. J Biol Chem 263:13802–13805PubMed

Carver LA, Bradfield CA (1997) Ligand-dependent interaction of the aryl hydrocarbon receptor with a novel immunophilin homolog in vivo. J Biol Chem 272:11452–11456CrossRefPubMed

Meyer BK, Pray-Grant MG, Vanden Heuvel JP, Perdew GH (1998) Hepatitis B virus X-associated protein 2 is a subunit of the unliganded aryl hydrocarbon receptor core complex and exhibits transcriptional enhancer activity. Mol Cell Biol 18:978–988CrossRefPubMedPubMedCentral

Nair SC, Toran EJ, Rimerman RA, Hjermstad S, Smithgall TE, Smith DF (1996) A pathway of multi-chaperone interactions common to diverse regulatory proteins: estrogen receptor, Fes tyrosine kinase, heat shock transcription factor Hsf1, and the aryl hydrocarbon receptor. Cell Stress Chaperones 1:237–250CrossRefPubMedPubMedCentral

McGuire J, Whitelaw ML, Pongratz I, Gustafsson JA, Poellinger L (1994) A cellular factor stimulates ligand-dependent release of hsp90 from the basic helix-loop-helix dioxin receptor. Mol Cell Biol 14:2438–2446CrossRefPubMedPubMedCentral

10.

Fukunaga BN, Probst MR, Reisz-Porszasz S, Hankinson O (1995) Identification of functional domains of the aryl hydrocarbon receptor. J Biol Chem 270:29270–29278CrossRefPubMed

11.

Schiering C, Vonk A, Das S, Stockinger B, Wincent E (2018) Cytochrome P4501-inhibiting chemicals amplify aryl hydrocarbon receptor activation and IL-22 production in T helper 17 cells. Biochem Pharmacol 151:47–58CrossRefPubMed

12.

Schiering C, Wincent E, Metidji A, Iseppon A, Li Y, Potocnik AJ, Omenetti S, Henderson CJ, Wolf CR, Nebert DW, Stockinger B (2017) Feedback control of AHR signalling regulates intestinal immunity. Nature 542:242–245CrossRefPubMedPubMedCentral

13.

Stockinger B, Di Meglio P, Gialitakis M, Duarte JH (2014) The aryl hydrocarbon receptor: multitasking in the immune system. Annu Rev Immunol 32:403–432CrossRefPubMed

14.

Mandal PK (2005) Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology. J Comp Physiol B 175:221–230CrossRefPubMed

15.

Nguyen LP, Bradfield CA (2008) The search for endogenous activators of the aryl hydrocarbon receptor. Chem Res Toxicol 21:102–116CrossRefPubMed

16.

Denison MS, Nagy SR (2003) Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu Rev Pharmacol Toxicol 43:309–334CrossRefPubMed

17.

Bjeldanes LF, Kim JY, Grose KR, Bartholomew JC, Bradfield CA (1991) Aromatic hydrocarbon responsiveness-receptor agonists generated from indole-3-carbinol in vitro and in vivo: comparisons with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Proc Natl Acad Sci U S A 88:9543–9547CrossRefPubMedPubMedCentral

18.

Zhang S, Qin C, Safe SH (2003) Flavonoids as aryl hydrocarbon receptor agonists/antagonists: effects of structure and cell context. Environ Health Perspect 111:1877–1882CrossRefPubMedPubMedCentral

19.

Takamura T, Harama D, Fukumoto S, Nakamura Y, Shimokawa N, Ishimaru K, Ikegami S, Makino S, Kitamura M, Nakao A (2011) Lactobacillus bulgaricus OLL1181 activates the aryl hydrocarbon receptor pathway and inhibits colitis. Immunol Cell Biol 89:817–822CrossRefPubMedPubMedCentral

20.

Zelante T, Iannitti RG, Cunha C, De Luca A, Giovannini G, Pieraccini G, Zecchi R, D'Angelo C, Massi-Benedetti C, Fallarino F, Carvalho A, Puccetti P, Romani L (2013) Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 39:372–385CrossRefPubMed

21.

Cervantes-Barragan L, Chai JN, Tianero MD, Di Luccia B, Ahern PP, Merriman J, Cortez VS, Caparon MG, Donia MS, Gilfillan S, Cella M, Gordon JI, Hsieh CS, Colonna M (2017) Lactobacillus reuteri induces gut intraepithelial CD4+CD8αα+ T cells. Science 357:806–810CrossRefPubMedPubMedCentral

22.

Lamas B, Richard ML, Leducq V, Pham HP, Michel ML, Da Costa G, Bridonneau C, Jegou S, Hoffmann TW, Natividad JM, Brot L, Taleb S, Couturier-Maillard A, Nion-Larmurier I, Merabtene F, Seksik P, Bourrier A, Cosnes J, Ryffel B, Beaugerie L, Launay JM, Langella P, Xavier RJ, Sokol H (2016) CARD9 impacts colitis by altering gut microbiota metabolism of tryptophan into aryl hydrocarbon receptor ligands. Nat Med 22:598–605CrossRefPubMedPubMedCentral

23.

Sonowal R, Swimm A, Sahoo A, Luo L, Matsunaga Y, Wu Z, Bhingarde JA, Ejzak EA, Ranawade A, Qadota H, Powell DN, Capaldo CT, Flacker JM, Jones RM, Benian GM, Kalman D (2017) Indoles from commensal bacteria extend healthspan. Proc Natl Acad Sci U S A 114:E7506–E7E15CrossRefPubMedPubMedCentral

24.

Moura-Alves P, Faé K, Houthuys E, Dorhoi A, Kreuchwig A, Furkert J, Barison N, Diehl A, Munder A, Constant P, Skrahina T, Guhlich-Bornhof U, Klemm M, Koehler AB, Bandermann S, Goosmann C, Mollenkopf HJ, Hurwitz R, Brinkmann V, Fillatreau S, Daffe M, Tümmler B, Kolbe M, Oschkinat H, Krause G, Kaufmann SH (2014) AhR sensing of bacterial pigments regulates antibacterial defence. Nature 512:387–392CrossRefPubMed

25.

Gaitanis G, Magiatis P, Stathopoulou K, Bassukas ID, Alexopoulos EC, Velegraki A, Skaltsounis AL (2008) AhR ligands, malassezin, and indolo[3,2-b]carbazole are selectively produced by Malassezia furfur strains isolated from seborrheic dermatitis. J Invest Dermatol 128:1620–1625CrossRefPubMed

26.

Magiatis P, Pappas P, Gaitanis G, Mexia N, Melliou E, Galanou M, Vlachos C, Stathopoulou K, Skaltsounis AL, Marselos M, Velegraki A, Denison MS, Bassukas ID (2013) Malassezia yeasts produce a collection of exceptionally potent activators of the Ah (dioxin) receptor detected in diseased human skin. J Invest Dermatol 133:2023–2030CrossRefPubMedPubMedCentral

27.

Mezrich JD, Fechner JH, Zhang X, Johnson BP, Burlingham WJ, Bradfield CA (2010) An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells. J Immunol 185:3190–3198CrossRefPubMedPubMedCentral

28.

Seok SH, Ma ZX, Feltenberger JB, Chen H, Scarlett C, Lin Z, Satyshur KA, Cortopassi M, Jefcoate CR, Ge Y, Tang W, Bradfield CA, Xing Y (2018) Trace derivatives of kynurenine potently activate the aryl hydrocarbon receptor (AHR). J Biol Chem 293(6):1994–2005CrossRefPubMed

29.

Rannug U, Rannug A, Sjöberg U, Li H, Westerholm R, Bergman J (1995) Structure elucidation of two tryptophan-derived, high affinity Ah receptor ligands. Chem Biol 2:841–845CrossRefPubMed

30.

Smirnova A, Wincent E, Vikström Bergander L, Alsberg T, Bergman J, Rannug A, Rannug U (2016) Evidence for new light-independent pathways for generation of the endogenous aryl hydrocarbon receptor agonist FICZ. Chem Res Toxicol 29:75–86CrossRefPubMed

31.

Diefenbach A, Colonna M, Koyasu S (2014) Development, differentiation, and diversity of innate lymphoid cells. Immunity 41:354–365CrossRefPubMedPubMedCentral

32.

Diefenbach A, Colonna M, Romagnani C (2017) The ILC world revisited. Immunity 46:327–332CrossRefPubMed

33.

Cortez VS, Robinette ML, Colonna M (2015) Innate lymphoid cells: new insights into function and development. Curr Opin Immunol 32:71–77CrossRefPubMedPubMedCentral

34.

Ebihara T, Song C, Ryu SH, Plougastel-Douglas B, Yang L, Levanon D, Groner Y, Bern MD, Stappenbeck TS, Colonna M, Egawa T, Yokoyama WM (2015) Runx3 specifies lineage commitment of innate lymphoid cells. Nat Immunol 16:1124–1133CrossRefPubMedPubMedCentral

35.

Li S, Heller JJ, Bostick JW, Lee A, Schjerven H, Kastner P, Chan S, Chen ZE, Zhou L (2016) Ikaros inhibits group 3 innate lymphoid cell development and function by suppressing the aryl hydrocarbon receptor pathway. Immunity 45:185–197CrossRefPubMedPubMedCentral

36.

Lee JS, Cella M, McDonald KG, Garlanda C, Kennedy GD, Nukaya M, Mantovani A, Kopan R, Bradfield CA, Newberry RD, Colonna M (2011) AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat Immunol 13:144–151CrossRefPubMedPubMedCentral

37.

Kiss EA, Vonarbourg C, Kopfmann S, Hobeika E, Finke D, Esser C, Diefenbach A (2011) Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 334:1561–1565CrossRefPubMed

38.

Hughes T, Briercheck EL, Freud AG, Trotta R, McClory S, Scoville SD, Keller K, Deng Y, Cole J, Harrison N, Mao C, Zhang J, Benson DM, Yu J, Caligiuri MA (2014) The transcription factor AHR prevents the differentiation of a stage 3 innate lymphoid cell subset to natural killer cells. Cell Rep 8:150–162CrossRefPubMedPubMedCentral

39.

Shin JH, Zhang L, Murillo-Sauca O, Kim J, Kohrt HE, Bui JD, Sunwoo JB (2013) Modulation of natural killer cell antitumor activity by the aryl hydrocarbon receptor. Proc Natl Acad Sci U S A 110:12391–12396CrossRefPubMedPubMedCentral

40.

Wagage S, John B, Krock BL, Hall AO, Randall LM, Karp CL, Simon MC, Hunter CA (2014) The aryl hydrocarbon receptor promotes IL-10 production by NK cells. J Immunol 192:1661–1670CrossRefPubMedPubMedCentral

41.

Qiu J, Heller JJ, Guo X, Chen ZM, Fish K, Fu YX, Zhou L (2012) The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity 36:92–104CrossRefPubMed

42.

Qiu J, Guo X, Chen ZM, He L, Sonnenberg GF, Artis D, Fu YX, Zhou L (2013) Group 3 innate lymphoid cells inhibit T-cell-mediated intestinal inflammation through aryl hydrocarbon receptor signaling and regulation of microflora. Immunity 39:386–399CrossRefPubMed

43.

Wagage S, Harms Pritchard G, Dawson L, Buza EL, Sonnenberg GF, Hunter CA (2015) The group 3 innate lymphoid cell defect in aryl hydrocarbon receptor deficient mice is associated with T cell hyperactivation during intestinal infection. PLoS One 10:e0128335CrossRefPubMedPubMedCentral

44.

Funatake CJ, Marshall NB, Steppan LB, Mourich DV, Kerkvliet NI (2005) Cutting edge: activation of the aryl hydrocarbon receptor by 2,3,7,8-tetrachlorodibenzo-p-dioxin generates a population of CD4+ CD25+ cells with characteristics of regulatory T cells. J Immunol 175:4184–4188CrossRefPubMed

45.

Apetoh L, Quintana FJ, Pot C, Joller N, Xiao S, Kumar D, Burns EJ, Sherr DH, Weiner HL, Kuchroo VK (2010) The aryl hydrocarbon receptor interacts with c-Maf to promote the differentiation of type 1 regulatory T cells induced by IL-27. Nat Immunol 11:854–861CrossRefPubMedPubMedCentral

46.

Mascanfroni ID, Takenaka MC, Yeste A, Patel B, Wu Y, Kenison JE, Siddiqui S, Basso AS, Otterbein LE, Pardoll DM, Pan F, Priel A, Clish CB, Robson SC, Quintana FJ (2015) Metabolic control of type 1 regulatory T cell differentiation by AHR and HIF1-α. Nat Med 21:638–646CrossRefPubMedPubMedCentral

47.

Ehrlich AK, Pennington JM, Tilton S, Wang X, Marshall NB, Rohlman D, Funatake C, Punj S, O'Donnell E, Yu Z, Kolluri SK, Kerkvliet NI (2017) AhR activation increases IL-2 production by alloreactive CD4+ T cells initiating the differentiation of mucosal-homing Tim3+ Lag3+ Tr1 cells. Eur J Immunol 47:1989–2001CrossRefPubMed

48.

Veldhoen M, Hirota K, Westendorf AM, Buer J, Dumoutier L, Renauld JC, Stockinger B (2008) The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 453:106–109CrossRefPubMed

49.

Quintana FJ, Basso AS, Iglesias AH, Korn T, Farez MF, Bettelli E, Caccamo M, Oukka M, Weiner HL (2008) Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature 453:65–71CrossRefPubMed

50.

Veldhoen M, Hirota K, Christensen J, O'Garra A, Stockinger B (2009) Natural agonists for aryl hydrocarbon receptor in culture medium are essential for optimal differentiation of Th17 T cells. J Exp Med 206:43–49CrossRefPubMedPubMedCentral

51.

Kimura A, Naka T, Nakahama T, Chinen I, Masuda K, Nohara K, Fujii-Kuriyama Y, Kishimoto T (2009) Aryl hydrocarbon receptor in combination with Stat1 regulates LPS-induced inflammatory responses. J Exp Med 206:2027–2035CrossRefPubMedPubMedCentral

52.

Rutz S, Noubade R, Eidenschenk C, Ota N, Zeng W, Zheng Y, Hackney J, Ding J, Singh H, Ouyang W (2011) Transcription factor c-Maf mediates the TGF-β-dependent suppression of IL-22 production in T(H)17 cells. Nat Immunol 12:1238–1245CrossRefPubMed

53.

Ehrlich AK, Pennington JM, Bisson WH, Kolluri SK, Kerkvliet NI (2018) TCDD, FICZ, and other high affinity AhR ligands dose-dependently determine the fate of CD4+ T cell differentiation. Toxicol Sci 161(2):310–320CrossRefPubMed

54.

Li Y, Innocentin S, Withers DR, Roberts NA, Gallagher AR, Grigorieva EF, Wilhelm C, Veldhoen M (2011) Exogenous stimuli maintain intraepithelial lymphocytes via aryl hydrocarbon receptor activation. Cell 147:629–640CrossRefPubMed

55.

Konkel JE, Maruyama T, Carpenter AC, Xiong Y, Zamarron BF, Hall BE, Kulkarni AB, Zhang P, Bosselut R, Chen W (2011) Control of the development of CD8αα+ intestinal intraepithelial lymphocytes by TGF-β. Nat Immunol 12:312–319CrossRefPubMedPubMedCentral

56.

Mucida D, Husain MM, Muroi S, van Wijk F, Shinnakasu R, Naoe Y, Reis BS, Huang Y, Lambolez F, Docherty M, Attinger A, Shui JW, Kim G, Lena CJ, Sakaguchi S, Miyamoto C, Wang P, Atarashi K, Park Y, Nakayama T, Honda K, Ellmeier W, Kronenberg M, Taniuchi I, Cheroutre H (2013) Transcriptional reprogramming of mature CD4⁺ helper T cells generates distinct MHC class II-restricted cytotoxic T lymphocytes. Nat Immunol 14:281–289CrossRefPubMedPubMedCentral

57.

Reis BS, Rogoz A, Costa-Pinto FA, Taniuchi I, Mucida D (2013) Mutual expression of the transcription factors Runx3 and ThPOK regulates intestinal CD4⁺ T cell immunity. Nat Immunol 14:271–280CrossRefPubMedPubMedCentral

58.

Hauben E, Gregori S, Draghici E, Migliavacca B, Olivieri S, Woisetschläger M, Roncarolo MG (2008) Activation of the aryl hydrocarbon receptor promotes allograft-specific tolerance through direct and dendritic cell-mediated effects on regulatory T cells. Blood 112:1214–1222CrossRefPubMed

59.

Lawrence BP, Denison MS, Novak H, Vorderstrasse BA, Harrer N, Neruda W, Reichel C, Woisetschläger M (2008) Activation of the aryl hydrocarbon receptor is essential for mediating the anti-inflammatory effects of a novel low-molecular-weight compound. Blood 112:1158–1165CrossRefPubMedPubMedCentral

60.

Jurado-Manzano BB, Zavala-Reyes D, Turrubiartes-Martínez EA, Portales-Pérez DP, González-Amaro R, Layseca-Espinosa E (2017) FICZ generates human tDCs that induce CD4+ CD25high Foxp3+ Treg-like cell differentiation. Immunol Lett 190:84–92CrossRefPubMed

61.

Kado S, Chang WLW, Chi AN, Wolny M, Shepherd DM, Vogel CFA (2017) Aryl hydrocarbon receptor signaling modifies Toll-like receptor-regulated responses in human dendritic cells. Arch Toxicol 91:2209–2221CrossRefPubMed

62.

Platzer B, Richter S, Kneidinger D, Waltenberger D, Woisetschläger M, Strobl H (2009) Aryl hydrocarbon receptor activation inhibits in vitro differentiation of human monocytes and Langerhans dendritic cells. J Immunol 183:66–74CrossRefPubMed

63.

Boitano AE, Wang J, Romeo R, Bouchez LC, Parker AE, Sutton SE, Walker JR, Flaveny CA, Perdew GH, Denison MS, Schultz PG, Cooke MP (2010) Aryl hydrocarbon receptor antagonists promote the expansion of human hematopoietic stem cells. Science 329:1345–1348CrossRefPubMedPubMedCentral

64.

Thordardottir S, Hangalapura BN, Hutten T, Cossu M, Spanholtz J, Schaap N, Radstake TR, van der Voort R, Dolstra H (2014) The aryl hydrocarbon receptor antagonist StemRegenin 1 promotes human plasmacytoid and myeloid dendritic cell development from CD34+ hematopoietic progenitor cells. Stem Cells Dev 23:955–967CrossRefPubMed

65.

Goudot C, Coillard A, Villani AC, Gueguen P, Cros A, Sarkizova S, Tang-Huau TL, Bohec M, Baulande S, Hacohen N, Amigorena S, Segura E (2017) Aryl hydrocarbon receptor controls monocyte differentiation into dendritic cells versus macrophages. Immunity 47:582–96.e6

66.

Jux B, Kadow S, Esser C (2009) Langerhans cell maturation and contact hypersensitivity are impaired in aryl hydrocarbon receptor-null mice. J Immunol 182:6709–6717CrossRefPubMed

67.

Liu H, Ramachandran I, Gabrilovich DI (2014) Regulation of plasmacytoid dendritic cell development in mice by aryl hydrocarbon receptor. Immunol Cell Biol 92:200–203CrossRefPubMed

68.

Quintana FJ, Murugaiyan G, Farez MF, Mitsdoerffer M, Tukpah AM, Burns EJ, Weiner HL (2010) An endogenous aryl hydrocarbon receptor ligand acts on dendritic cells and T cells to suppress experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 107:20768–20773CrossRefPubMedPubMedCentral

69.

Vogel CF, Goth SR, Dong B, Pessah IN, Matsumura F (2008) Aryl hydrocarbon receptor signaling mediates expression of indoleamine 2,3-dioxygenase. Biochem Biophys Res Commun 375:331–335CrossRefPubMedPubMedCentral

70.

Nguyen NT, Kimura A, Nakahama T, Chinen I, Masuda K, Nohara K, Fujii-Kuriyama Y, Kishimoto T (2010) Aryl hydrocarbon receptor negatively regulates dendritic cell immunogenicity via a kynurenine-dependent mechanism. Proc Natl Acad Sci U S A 107:19961–19966CrossRefPubMedPubMedCentral

71.

Bessede A, Gargaro M, Pallotta MT, Matino D, Servillo G, Brunacci C, Bicciato S, Mazza EM, Macchiarulo A, Vacca C, Iannitti R, Tissi L, Volpi C, Belladonna ML, Orabona C, Bianchi R, Lanz TV, Platten M, Della Fazia MA, Piobbico D, Zelante T, Funakoshi H, Nakamura T, Gilot D, Denison MS, Guillemin GJ, DuHadaway JB, Prendergast GC, Metz R, Geffard M, Boon L, Pirro M, Iorio A, Veyret B, Romani L, Grohmann U, Fallarino F, Puccetti P (2014) Aryl hydrocarbon receptor control of a disease tolerance defence pathway. Nature 511:184–190CrossRefPubMedPubMedCentral

72.

Sulentic CE, Kaminski NE (2011) The long winding road toward understanding the molecular mechanisms for B-cell suppression by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Sci 120(Suppl 1):S171–S191CrossRefPubMed

73.

Allan LL, Sherr DH (2005) Constitutive activation and environmental chemical induction of the aryl hydrocarbon receptor/transcription factor in activated human B lymphocytes. Mol Pharmacol 67:1740–1750CrossRefPubMed

74.

Tanaka G, Kanaji S, Hirano A, Arima K, Shinagawa A, Goda C, Yasunaga S, Ikizawa K, Yanagihara Y, Kubo M, Kuriyama-Fujii Y, Sugita Y, Inokuchi A, Izuhara K (2005) Induction and activation of the aryl hydrocarbon receptor by IL-4 in B cells. Int Immunol 17:797–805CrossRefPubMed

75.

Villa M, Gialitakis M, Tolaini M, Ahlfors H, Henderson CJ, Wolf CR, Brink R, Stockinger B (2017) Aryl hydrocarbon receptor is required for optimal B-cell proliferation. EMBO J 36:116–128CrossRefPubMed

76.

Inoue H, Mishima K, Yamamoto-Yoshida S, Ushikoshi-Nakayama R, Nakagawa Y, Yamamoto K, Ryo K, Ide F, Saito I (2012) Aryl hydrocarbon receptor-mediated induction of EBV reactivation as a risk factor for Sjögren’s syndrome. J Immunol 188:4654–4662CrossRefPubMed

77.

Yoshida T, Katsuya K, Oka T, Koizumi S, Wakita D, Kitamura H, Nishimura T (2012) Effects of AhR ligands on the production of immunoglobulins in purified mouse B cells. Biomed Res 33:67–74CrossRefPubMed

78.

Phadnis-Moghe AS, Li J, Crawford RB, Kaminski NE (2016) SHP-1 is directly activated by the aryl hydrocarbon receptor and regulates BCL-6 in the presence of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicol Appl Pharmacol 310:41–50CrossRefPubMedPubMedCentral

79.

Kovalova N, Manzan M, Crawford R, Kaminski N (2016) Role of aryl hydrocarbon receptor polymorphisms on TCDD-mediated CYP1B1 induction and IgM suppression by human B cells. Toxicol Appl Pharmacol 309:15–23CrossRefPubMedPubMedCentral

Title: AHR signaling in the development and function of intestinal immune cells and beyond
Authors: Luisa Cervantes-Barragan
Marco Colonna
Publication date: 01-07-2018
Publisher: Springer Berlin Heidelberg
Published in: Seminars in Immunopathology / Issue 4/2018
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI: https://doi.org/10.1007/s00281-018-0694-9

ACC 2024 Congress Coverage

Heart Failure Video

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

AHR signaling in the development and function of intestinal immune cells and beyond

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2018

Orchestration of intestinal homeostasis and tolerance by group 3 innate lymphoid cells

Innate lymphoid cells—key immune integrators of overall body homeostasis

ILC2s in infectious diseases and organ-specific fibrosis

Innate lymphoid cells: key players in tissue-specific immunity

Activating and inhibitory receptors expressed on innate lymphoid cells

Memory responses of innate lymphocytes and parallels with T cells

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page