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Aryl hydrocarbon receptor protects against viridans streptococci infection by activation of immune system through IL-17RA signaling

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American Journal of BioMedicine  Volume 2, Issue 5, pages 527–541, May 2014  


Guowei Liang; David Lazenby; Jonathan D Groden; Xing Liu; Suzan N Pretlow;  Mark H Mertens

Abstract

The majority of bacterial infections during neutropenia following high-dose chemotherapy or stem cell transplantation are caused by coagulase-negative staphylococci, a large number are due to viridans streptococci. Despite considerable progress in the understanding of the AhR-mediated regulation of immune responses, the role of AhR in bacterial infections has not been clearly demonstrated. In the study presented here, we sought to determine whether the aryl hydrocarbon receptor (AhR) would protect mice from infection with viridans streptococci. AhR enhances the inflammatory response to viridans streptococci stimuli. Specifically, neutrophil numbers and levels of inflammatory cytokines are often increased in mice treated with viridans streptococci. Furthermore, AhR activation through the IL-17RA is required for protection against viridans streptococcal infection. Taken together, we concluded that AhR plays an important role in optimal innate immunoprotection against microbial infection through the down-regulation of immune response.

Keywords: Viridans streptococcal; AhR; Inflammatory cytokines; IL-17RA


References

1. Razonable RR, Litzow MR, Khaliq Y et al. Bacteremia due to viridans group Streptococci with diminished susceptibility to Levofloxacin among neutropenic patients receiving levofloxacin prophylaxis. Clin Infect Dis 2002;34:1469–1474. [PubMed]

2. Bochud PY, Calandra T, Francioli P. Bacteremia due to viridans streptococci in neutropenic patients: a review. Am J Med 1994; 97: 256–264. [PubMed

3. Dallaire F, Ouellet N, Bergeron Y, Turmel V, Gauthier MC, Simard M, Bergeron MG. Microbiological and inflammatory factors associated with the development of pneumococcal pneumonia. J Infect. Dis. 2001;184:292-300. [Abstract/FREE Full Text]

4. Dallaire F, Ouellet N, Simard M, Bergeron Y, Bergeron MG. Efficacy of recombinant human granulocyte colony-stimulating factor in a murine model of pneumococcal pneumonia: effects of lung inflammation and timing of treatment. J. Infect. Dis 2001;183:70-77. [Abstract/FREE Full Text]

5. Janeway CA, Jr, Medzhitov R. Innate immune recognition. Annu. Rev. Immunol 2002; 20:197-216. [CrossRefMedline]

6. Schluger NW, Rom WN. Early responses to infection: chemokines as mediators of inflammation. Curr. Opin. Immunol 1997; 9:504-508. [CrossRef]

7. Bals R, Hiemstra PS. Innate immunity in the lung: how epithelial cells fight against respiratory pathogens. Eur. Respir.J 2004; 23:327-333. [Full Text]

8. Kimura  A, Naka T, Nakahama T, IChinen I, Masuda K, Nohara K, et al. Aryl hydrocarbon receptor in combination with Stat1 regulates LPS-induced inflammatory responses.  JEM 2009; 206(9):2027-2035. [Full Text]

9. Wagage S, John B,  Krock BL, Hall AO, Randall LM. The Aryl Hydrocarbon Receptor Promotes IL-10 Production by NK Cells J. Immunol 2014;192:1661-1670. [Full Text]

10.  Vogel CF, Sciullo E, Li W, Wong P, Lazennec G, Matsumura F. RelB, a new partner of aryl hydrocarbon receptor-mediated transcription. Mol Endocrinol 2007;21:2941–2955.  [Medline]

11.  Fujii-Kuriyama Y, Ema M, Mimura J, Sogawa K. Ah receptor: a novel ligand-activated transcription factor. Exp. Clin. Immunogenet 1994;11:65. [Medline]

12.  Puga A, Tomlinson CR, Xia Y. Ah receptor signals cross-talk with multiple developmental pathways. Biochem. Pharmacol 2005; 69:199. [CrossRef]

13.  Apetoh L, Quintana FJ, Pot C, Joller N, Xiao S, Kumar D, Burns EJ, et al. The aryl hydrocarbon receptor interacts with c-Maf to promote the differentiation of type 1 regulatory T cells induced by IL-27. Nat Immunol 2010;11:854–861. [PubMed]

14.  Karen D. Meeks, Amy N. Sieve, Jay K. Kolls, Nico Ghilardi, Rance E. Berg. IL-23 Is Required for Protection against Systemic Infection with Listeria monocytogenes. The Journal of Immunology 2009; 183(12):8026-8034.  [Abstarct/Full-Text]

15.  Bochud PY, Calandra T, Francioli P . Bacteremia due to viridans streptococci in neutropenic patients: a review. Am J Med 1994; 97:256-64. [CrossRef]

16.  Shenep JL. Viridans-group streptococcal infections in immunocompromised hosts. Int J Antimicrob Agents 2000;14:129-35. [CrossRef]

17.  Bracale MM, Wonderge RB, Zhou M, Hazen EG. Endotoxemia-suppress cardiac function through dysregulation of mitochondrial biogenesis in mice model. American journal of BioMedicine 2014; 2(2): 23–336. [Abstarct/Full-Text]

18.  Kimura A, Naka T, Nohara K, Fujii-Kuriyama Y, Kishimoto T. Aryl hydrocarbon receptor regulates Stat1 activation and participates in the development of Th17 cells. Proc. Natl Acad.Sci.USA 2009;105:9721. [Abstract/FREE Full Text]

19.  Kimura A, Naka T, Nakahama T, et al. Aryl hydrocarbon receptor in combination with Stat1 regulates LPS-induced inflammatory responses. J. Exp. Med. 2008;206:2027. [Abstract/FREE Full Text]

20.  Lawrence BP, Roberts AD, Neumiller JJ, Cundiff JA, Woodland DL. Aryl hydrocarbon receptor activation impairs the priming but not the recall of influenza virus-specific CD8+T cells in the lung. J Immunol 2006;177:5819–5828. [PubMed]

21. Teske S, Bohn AA, Regal JF, Neumiller JJ, Lawrence BP. Exploring mechanisms that underlie aryl hydrocarbon receptor-mediated increases in pulmonary neutrophilia and diminished host resistance to influenza A virus. Am J Physiol Lung Cell Mol Physiol 2005;289:111–124. [PubMed]

22. Walisser JA, Glover E, Pande K, Liss AL, Bradfield CA. Aryl hydrocarbon receptor-dependent liver development and hepatotoxicity are mediated by different cell types. Proc Natl Acad Sci USA 2005;102:17858–17863. [PubMed]

23.  Puga A, Barnes SJ, Dalton TP, Chang C, Knudsen ES, Maier MA. Aromatic hydrocarbon receptor interaction with the retinoblastoma protein potentiates repression of E2F-dependent transcription and cell cycle arrest. J Biol Chem 2000;275:2943–2950. [PubMed]

24.  Zenewicz LA, Yancopoulos GD,Valenzuela DM, Murphy AJ, Karow M, Flavell RA. Interleukin-22 but not interleukin-17 provides protection to hepatocytes during acute liver inflammation. Immunity 2007;27: 647-659. [CrossRef]

25.  Kimura A, Naka T, Nakahama T, Chinen I, Masuda K, Nohara K, et al. Aryl hydrocarbon receptor in combination with Stat1 regulates LPS-induced inflammatory responses. J Exp Med 2009; 206:2027–2035. [PubMed]

26.  Puga A, Tomlinson CR, Xia Y. Ah receptor signals cross-talk with multiple developmental pathways. Biochem. Pharmacol 2005; 69:199.  [CrossRef]

27.  Kimura A, Naka T, Nohara K, Fujii-Kuriyama Y, Kishimoto T. Aryl hydrocarbon receptor regulates Stat1 activation and participates in the development of Th17 cells. Proc. Natl Acad. Sci. USA 2005;105:9721. [Abstract/FREE Full Text]

28.  Veldhoen M, Hirota K, Westendorf AM, et al. The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 2008; 453:106.  [CrossRef]

29.  Joseph SB, Bradley MN, Castrillo A, et al. LXR-dependent gene expression is important for macrophage survival and the innate immune response. Cell 2004;119:299.  [CrossRef]

30.  Esser C, Rannug A, Stockinger B. The aryl hydrocarbon receptor in immunity. Trends Immunol 2009; 30:447.  [CrossRef]

31. Vorderstrasse BA, Lawrence BP. Protection against lethal challenge with Streptococcus pneumoniae is conferred by aryl hydrocarbon receptor activation but is not associated with an enhanced inflammatory response. Infect. Immun 2006;74:5679. [Abstract/FREE Full Text]

32.  Hauben E, et al. Activation of the aryl hydrocarbon receptor promotes allograft-specific tolerance through direct and dendritic cell-mediated effects on regulatory T cells. Blood 2008;112:1214–1222.  [PubMed]

33.  Kimura A, Naka T, Nohara K, Fujii-Kuriyama Y, Kishimoto T. Aryl hydrocarbon receptor regulates Stat1 activation and participates in the development of Th17 cells. Proc Natl Acad Sci USA 2008;105:9721–9726.  [PubMed]

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

35.  Zhang L, et al. Suppression of experimental autoimmune uveoretinitis by inducing differentiation of regulatory T cells via activation of aryl hydrocarbon receptor. Invest Ophthalmol Vis Sci 2010;51:2109–2117. [PubMed]

36.  Veldhoen M, et al. The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 2008;453:106–109. [PubMed]

37.  Kerkvliet NI, et al. Activation of aryl hydrocarbon receptor by TCDD prevents diabetes in NOD mice and increases Foxp3+ T cells in pancreatic lymph nodes. Immunotherapy 2009;1:539–547.  [PubMed]

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