1887

Abstract

Food allergies (FAs) occur due to intestinal immune dysfunction elicited by dysbiotic conditions. It was previously determined by us that species propagate in the faeces of mice with FAs and worsen allergic symptoms by inducing the allergenic cytokine IL-33. Dendritic cells can play important roles in regulation of FA responses.

species propagating in intestines of mice worsen allergic symptoms by stimulating dendritic cells to induce IL-33 expression.

The aim of the present study was to analyse whether stimulates dendritic cells to induce IL-33 expression.

IL-33 expression was evaluated in a DC2.4 mouse dendritic cell line stimulated by live or heat-inactivated JCM1658, ATP, LPS extracted from JCM1658 or other enterobacteria by real-time PCR. The ATP concentration and number of live bacteria in the culture supernatant were measured simultaneously.

Live JCM1658 induced higher levels of IL-33 expression than other enterobacteria tested, but such a response was not elicited by heat-inactivated JCM1658. LPS extracted from JCM1658 did not induce IL-33 expression and suppressed live JCM1658-induced IL-33 expression via the activation of Toll-like receptor 4 signalling. Furthermore, ATP produced by JCM1658 stimulated dendritic cells to induce IL-33 expression by stimulating the P2X receptor, and LPS attenuated extracellular ATP-induced IL-33 expression. JCM1658 was observed to proliferate more vigorously and produce more ATP than other enterobacteria.

acts as an allergenic bacterium through ATP production, stimulating dendritic cells to induce IL-33 expression, while LPS released from inactivated JCM1658 attenuates this allergenicity.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001303
2021-01-13
2024-11-12
Loading full text...

Full text loading...

/deliver/fulltext/jmm/70/3/jmm001303.html?itemId=/content/journal/jmm/10.1099/jmm.0.001303&mimeType=html&fmt=ahah

References

  1. Berin MC, Sampson HA. Food allergy: an enigmatic epidemic. Trends Immunol 2013; 34:390–397 [View Article][PubMed]
    [Google Scholar]
  2. Prioult G, Nagler-Anderson C. Mucosal immunity and allergic responses: lack of regulation and/or lack of microbial stimulation?. Immunol Rev 2005; 206:204–218 [View Article][PubMed]
    [Google Scholar]
  3. Plunkett CH, Nagler CR. The influence of the microbiome on allergic sensitization to food. J Immunol 2017; 198:581–589 [View Article][PubMed]
    [Google Scholar]
  4. Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science 2012; 336:1268–1273 [View Article][PubMed]
    [Google Scholar]
  5. Aguilera AC, Dagher IA, Kloepfer KM. Role of the microbiome in allergic disease development. Curr Allergy Asthma Rep 2020; 20:44 [View Article][PubMed]
    [Google Scholar]
  6. Matsui S, Kataoka H, Tanaka J-I, Kikuchi M, Fukamachi H et al. Dysregulation of intestinal microbiota elicited by food allergy induces IgA-mediated oral dysbiosis. Infect Immun 2019; 88:e00741–19 [View Article][PubMed]
    [Google Scholar]
  7. Altmann G, Sechter I, Cahan D, Gerichter CB. Citrobacter diversus isolated from clinical material. J Clin Microbiol 1976; 3:390–392[PubMed]
    [Google Scholar]
  8. Cayrol C, Girard J-P. Il-33: an alarmin cytokine with crucial roles in innate immunity, inflammation and allergy. Curr Opin Immunol 2014; 31:31–37 [View Article][PubMed]
    [Google Scholar]
  9. Cayrol C, Girard J-P. Interleukin-33 (IL-33): a nuclear cytokine from the IL-1 family. Immunol Rev 2018; 281:154–168 [View Article][PubMed]
    [Google Scholar]
  10. Muto T, Fukuoka A, Kabashima K, Ziegler SF, Nakanishi K et al. The role of basophils and proallergic cytokines, TSLP and IL-33, in cutaneously sensitized food allergy. Int Immunol 2014; 26:539–549 [View Article][PubMed]
    [Google Scholar]
  11. Polumuri SK, Jayakar GG, Shirey KA, Roberts ZJ, Perkins DJ et al. Transcriptional regulation of murine IL-33 by TLR and non-TLR agonists. J Immunol 2012; 189:50–60 [View Article][PubMed]
    [Google Scholar]
  12. Talabot-Ayer D, Calo N, Vigne S, Lamacchia C, Gabay C et al. The mouse interleukin (Il)33 gene is expressed in a cell type- and stimulus-dependent manner from two alternative promoters. J Leukoc Biol 2012; 91:119–125 [View Article][PubMed]
    [Google Scholar]
  13. Su Z, Lin J, Lu F, Zhang X, Zhang L et al. Potential autocrine regulation of interleukin-33/ST2 signaling of dendritic cells in allergic inflammation. Mucosal Immunol 2013; 6:921–930 [View Article][PubMed]
    [Google Scholar]
  14. Renz H, Allen KJ, Sicherer SH, Sampson HA, Lack G et al. Food allergy. Nat Rev Dis Primers 2018; 4:17098 [View Article][PubMed]
    [Google Scholar]
  15. Persson EK, Uronen-Hansson H, Semmrich M, Rivollier A, Hagerbrand K et al. IRF4 transcription-factor-dependent CD103(+)CD11b(+) dendritic cells drive mucosal T helper 17 cell differentiation. Immunity 2013; 38:958–969 [View Article][PubMed]
    [Google Scholar]
  16. Sun CM, Hall JA, Blank RB, Bouladoux N, Oukka M et al. Small intestine lamina propria dendritic cells promote de novo generation of FOXP3 T reg cells via retinoic acid. J Exp Med 2007; 204:1775–1785 [View Article][PubMed]
    [Google Scholar]
  17. Johansson-Lindbom B, Svensson M, Pabst O, Palmqvist C, Marquez G et al. Functional specialization of gut CD103+ dendritic cells in the regulation of tissue-selective T cell homing. J Exp Med 2005; 202:1063–1073 [View Article][PubMed]
    [Google Scholar]
  18. Kawamoto T, Ii M, Kitazaki T, Iizawa Y, Kimura H. Tak-242 selectively suppresses Toll-like receptor 4-signaling mediated by the intracellular domain. Eur J Pharmacol 2008; 584:40–48 [View Article][PubMed]
    [Google Scholar]
  19. Donnelly-Roberts DL, Jarvis MF. Discovery of P2X7 receptor-selective antagonists offers new insights into P2X7 receptor function and indicates a role in chronic pain states. Br J Pharmacol 2007; 151:571–579 [View Article][PubMed]
    [Google Scholar]
  20. Inomata M, Horie T, Into T. OmpA-like proteins of Porphyromonas gingivalis contribute to serum resistance and prevent Toll-like receptor 4-mediated host cell activation. PLoS One 2018; 13:e0202791 [View Article][PubMed]
    [Google Scholar]
  21. Shimokawa C, Kanaya T, Hachisuka M, Ishiwata K, Hisaeda H et al. Mast cells are crucial for induction of group 2 innate lymphoid cells and clearance of helminth infections. Immunity 2017; 46:e864863–874 [View Article][PubMed]
    [Google Scholar]
  22. Pepperell C, Kus JV, Gardam MA, Humar A, Burrows LL. Low-Virulence Citrobacter species encode resistance to multiple antimicrobials. Antimicrob Agents Chemother 2002; 46:3555–3560 [View Article][PubMed]
    [Google Scholar]
  23. Janda JM, Abbott SL, Cheung WK, Hanson DF. Biochemical identification of citrobacteria in the clinical laboratory. J Clin Microbiol 1994; 32:1850–1854 [View Article][PubMed]
    [Google Scholar]
  24. Rodrigues J, Rocha D, Santos F, João A. Neonatal Citrobacter koseri meningitis: report of four cases. Case Rep Pediatr 2014; 2014:195204 [View Article][PubMed]
    [Google Scholar]
  25. Vaz Marecos C, Ferreira M, Ferreira MM, Barroso MR. Sepsis, meningitis and cerebral abscesses caused by Citrobacter koseri. BMJ Case Rep 2012; 2012:bcr1020114941 [View Article][PubMed]
    [Google Scholar]
  26. Pennington K, Van Zyl M, Escalante P. Citrobacter koseri pneumonia as initial presentation of underlying pulmonary adenocarcinoma. Clin Med Insights Case Rep 2016; 9:87–89 [View Article][PubMed]
    [Google Scholar]
  27. Underwood S, Avison MB. Citrobacter koseri and Citrobacter amalonaticus isolates carry highly divergent beta-lactamase genes despite having high levels of biochemical similarity and 16S rRNA sequence homology. J Antimicrob Chemother 2004; 53:1076–1080 [View Article][PubMed]
    [Google Scholar]
  28. Petrella S, Renard M, Ziental-Gelus N, Clermont D, Jarlier V et al. Characterization of the chromosomal class A beta-lactamase CKO from Citrobacter koseri. FEMS Microbiol Lett 2006; 254:285–292 [View Article][PubMed]
    [Google Scholar]
  29. Plantinga M, Guilliams M, Vanheerswynghels M, Deswarte K, Branco-Madeira F et al. Conventional and monocyte-derived CD11b(+) dendritic cells initiate and maintain T helper 2 cell-mediated immunity to house dust mite allergen. Immunity 2013; 38:322–335 [View Article][PubMed]
    [Google Scholar]
  30. Kouzaki H, Iijima K, Kobayashi T, O'Grady SM, Kita H. The danger signal, extracellular ATP, is a sensor for an airborne allergen and triggers IL-33 release and innate Th2-type responses. J Immunol 2011; 186:4375–4387 [View Article][PubMed]
    [Google Scholar]
  31. Saez PJ, Vargas P, Shoji KF, Harcha PA, Lennon-Dumenil AM et al. ATP promotes the fast migration of dendritic cells through the activity of pannexin 1 channels and P2X7 receptors. Sci Signal 2017; 10:eaah7107 [View Article][PubMed]
    [Google Scholar]
  32. la Sala A, Ferrari D, Corinti S, Cavani A, Di Virgilio F et al. Extracellular ATP induces a distorted maturation of dendritic cells and inhibits their capacity to initiate Th1 responses. J Immunol 2001; 166:1611–1617 [View Article][PubMed]
    [Google Scholar]
  33. la Sala A, Sebastiani S, Ferrari D, Di Virgilio F, Idzko M et al. Dendritic cells exposed to extracellular adenosine triphosphate acquire the migratory properties of mature cells and show a reduced capacity to attract type 1 T lymphocytes. Blood 2002; 99:1715–1722 [View Article][PubMed]
    [Google Scholar]
  34. Atarashi K, Nishimura J, Shima T, Umesaki Y, Yamamoto M et al. ATP drives lamina propria T(H)17 cell differentiation. Nature 2008; 455:808–812 [View Article][PubMed]
    [Google Scholar]
  35. Englezou PC, Rothwell SW, Ainscough JS, Brough D, Landsiedel R et al. P2X7R activation drives distinct IL-1 responses in dendritic cells compared to macrophages. Cytokine 2015; 74:293–304 [View Article][PubMed]
    [Google Scholar]
  36. Lin TH, Cheng CC, Su H-H, Huang N-C, Chen J-J et al. Lipopolysaccharide attenuates induction of proallergic cytokines, thymic stromal lymphopoietin, and interleukin 33 in respiratory epithelial cells stimulated with PolyI:C and human parechovirus. Front Immunol 2016; 7:440 [View Article][PubMed]
    [Google Scholar]
  37. Tada H, Suzuki R, Nemoto E, Shimauchi H, Matsushita K et al. Increases in IL-33 production by fimbriae and lipopeptide from Porphyromonas gingivalis in mouse bone marrow-derived dendritic cells via Toll-like receptor 2. Biomed Res 2017; 38:189–195 [View Article][PubMed]
    [Google Scholar]
/content/journal/jmm/10.1099/jmm.0.001303
Loading
/content/journal/jmm/10.1099/jmm.0.001303
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error