Association of Staphylococcus aureus colonization with food allergy occurs independently of eczema severity

Tsilochristou, Olympia; Toit, George Du; Sayre, Peter H.; Roberts, Graham; Lawson, Kaitie; Sever, Michelle L.; Bahnson, Henry T.; Radulović, Suzana; Basting, Monica; Plaut, Marshall; Lack, Gideon; Chan, Susan; Fox, Adam; Fisher, Harriet; Abraham, Mable; Adam, Muhsinah; Coverdale, Louise; Duncan, Claire; Nixon, Amy; O'Dwyer-Leeson, Una; Offord, Victoria; Sheridan, Aine; Watson, Fiona; Witham, Natalie; Cockerell, Kathryn; Harland, Gail; Miller, Tiffany; Stedman, Charlotte; Clarke, C. W.; Cleaver, Richard; Deutsch, Gemma; Parr, Alicia; Bécares, Natalia; Crossley, Matthew; Francisco, Natalia do Couto; Richards, Kerry; Pietraszewicz, Ewa; Stephens, Alick; Sudra, Asha; Wester, Rianne; Wilson, Alastair; Wu, Celine; Heath, Jenna; Hersee, Kathryn; Patkunam, Devi; Asare, Adam; Chani, Eduard; Evind, Judith; Lim, Noha; Plough, Audrey; Whitehouse, Don; Lorenzo, Margarita Gomez; Panza, Joy Laurienzo; Lussier, Stephanie; Hu, Jack W.; Mason, Travis

doi:10.1016/j.jaci.2019.04.025

“…There is increasing interest in compositional and predicted functional differences in respiratory mucus microbiomes of allergic diseases. The importance of the respiratory microbiome, especially with respect to Th2 cytokine-regulated immune responses, has been increasingly recognized [24][25][26][27][28]. Understanding compositional changes in the microbiome and identifying dominant microbial species in respiratory mucus might be essential for developing new therapeutic approaches for allergic respiratory diseases.…”

Section: Discussionmentioning

confidence: 99%

Symbiotic microbiome Staphylococcus aureus from human nasal mucus modulates IL-33-mediated type 2 immune responses in allergic nasal mucosa

Jeon

¹

,

Gil

²

,

Won

³

et al. 2020

Preprint

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Background: The host-microbial commensalism can shape the innate immune responses in respiratory mucosa and nasal microbiome also modulates front-line immune mechanism in the nasal mucosa. Inhaled allergens encounter the host immune system first in the nasal mucosa, and microbial characteristics of nasal mucus directly impact the mechanisms of initial allergic responses in nasal epithelium. However, the roles of the nasal microbiome in allergic nasal mucosa remain uncertain. We sought to determine the distribution of nasal microbiomes in allergic nasal mucosa and elucidate the interplay between nasal microbiome Staphylococcus species and Th2 cytokines in allergic rhinitis (AR) models.Results: Staphylococcus aureus (AR-SA) and S. epidermidis (AR-SE) were isolated from the nasal mucosa of patients with AR. The influence of nasal microbiome Staphylococcus species on allergic nasal mucosa was also tested with in vitro and in vivo AR models. Pyrosequencing data showed that colonization by S. epidermidis and S. aureus was more dominant in nasal mucus of AR subjects. The mRNA and protein levels of IL-33 and TSLP were significantly higher in AR nasal epithelial (ARNE) cells which were cultured from nasal mucosa of AR subjects, and exposure of ARNE cells to AR-SA reduced IL-33 mRNA and secreted protein levels. Particularly, ovalbumin-driven AR mice inoculated with AR-SA by intranasal delivery exhibited significantly reduced IL-33 in their nasal mucosa. In the context of these results, allergic symptoms and Th2 cytokine levels were significantly downregulated after intranasal inoculation of AR-SA in vivo AR mice. Conclusion: Colonization by Staphylococcus species was more dominant in allergic nasal mucosa, and nasal commensal S. aureus from subjects with AR mediates anti-allergic effects by modulating IL-33-dependent Th2 inflammation. The results demonstrate the role of host-bacterial commensalism in shaping human allergic inflammation.

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“…Both S. epidermidis and S. aureus are well-known human pathogens that may cause serious opportunistic infections of the respiratory tract. However, Staphylococcus species are commonly detected in the normal microflora of the skin, intestine, and upper airway and many studies implicate the role of Staphylococcus species as symbiotic commensal organisms that are also involved in allergic diseases [31][32][33]. Patients with allergic eczema are more likely to have skin colonized with S. aureus than healthy control subjects, and disease severity is associated with S. aureus colonization.…”

Section: Discussionmentioning

confidence: 99%

“…Patients with allergic eczema are more likely to have skin colonized with S. aureus than healthy control subjects, and disease severity is associated with S. aureus colonization. The dominant distribution of S. aureus in the upper respiratory tract of patients with asthma and aspirin sensitivity has been reported up to 87.5%, and higher nasal S. aureus colonization is significantly related to asthma [31,34]. In addition, patients with AR are more frequently colonized with nasal S. aureus or sensitized to S. aureus enterotoxins than healthy control subjects [32].…”

Section: Discussionmentioning

confidence: 99%

Symbiotic microbiome Staphylococcus aureus from human nasal mucus modulates IL-33-mediated type 2 immune responses in allergic nasal mucosa

Jeon

¹

,

Gil

²

,

Won

³

et al. 2020

Preprint

0

View full text Add to dashboard Cite

Background: The host-microbial commensalism can shapes the innate immune responses in respiratory mucosa and nasal microbiome also modulates front-line immune mechanism in the nasal mucosa. Inhaled allergens encounter the host immune system first in the nasal mucosa, and microbial characteristics of nasal mucus directly impact the mechanisms of initial allergic responses in nasal epithelium. However, the roles of the nasal microbiome in allergic nasal mucosa remain uncertain. We sought to determine the distribution of nasal microbiomes in allergic nasal mucosa and elucidate the interplay between nasal microbiome Staphylococcus species and Th2 cytokines in allergic rhinitis (AR) models.Results: Staphylococcus aureus (AR-SA) and S. epidermidis (AR-SE) were isolated from the nasal mucosa of patients with AR. The influence of nasal microbiome Staphylococcus species on allergic nasal mucosa was also tested with in vitro and in vivo AR models. Pyrosequencing data showed that colonization by S. epidermidis and S. aureus was more dominant in nasal mucus of AR subjects. The mRNA and protein levels of IL-33 and TSLP were significantly higher in AR nasal epithelial (ARNE) cells which were cultured from nasal mucosa of AR subjects, and exposure of ARNE cells to AR-SA reduced IL-33 mRNA and secreted protein levels. Particularly, OVA-driven AR mice inoculated with AR-SA by intranasal delivery exhibited significantly reduced IL-33 in their nasal mucosa. In the context of these results, allergic symptoms and Th2 cytokine levels were significantly downregulated after intranasal inoculation of AR-SA in vivo AR mice. Conclusion: Colonization by Staphylococcus species was more dominant in allergic nasal mucosa, and nasal commensal S. aureus from subjects with AR mediates anti-allergic effects by modulating IL-33-dependent Th2 inflammation. The results demonstrate the role of host-bacterial commensalism in shaping human allergic inflammation.

show abstract

“…Both S. epidermidis and S. aureus are well-known human pathogens that may cause serious opportunistic infections of the respiratory tract. However, Staphylococcus species are commonly detected in the normal micro ora of the skin, intestine, and upper airway and many studies implicate the role of Staphylococcus species as symbiotic commensal organisms that are also involved in allergic diseases [27][28][29]. Patients with allergic eczema are more likely to have skin colonized with S. aureus than healthy control subjects, and disease severity is associated with S. aureus colonization.…”

Section: Discussionmentioning

confidence: 99%

Symbiotic microbiome Staphylococcus aureus from human nasal mucus modulates IL-33-mediated type 2 immune responses in allergic nasal mucosa

Jeon

¹

,

Gil

²

,

Won

³

et al. 2020

Preprint

0

View full text Add to dashboard Cite

Background: The host-microbial commensalism can shape the innate immune responses in respiratory mucosa and nasal microbiome also modulates front-line immune mechanism in the nasal mucosa. Inhaled allergens encounter the host immune system first in the nasal mucosa, and microbial characteristics of nasal mucus directly impact the mechanisms of initial allergic responses in nasal epithelium. However, the roles of the nasal microbiome in allergic nasal mucosa remain uncertain. We sought to determine the distribution of nasal microbiomes in allergic nasal mucosa and elucidate the interplay between nasal microbiome Staphylococcus species and Th2 cytokines in allergic rhinitis (AR) models.Results: Staphylococcus aureus (AR-SA) and S. epidermidis (AR-SE) were isolated from the nasal mucosa of patients with AR. The influence of nasal microbiome Staphylococcus species on allergic nasal mucosa was also tested with in vitro and in vivo AR models. Pyrosequencing data showed that colonization by S. epidermidis and S. aureus was more dominant in nasal mucus of AR subjects. The mRNA and protein levels of IL-33 and TSLP were significantly higher in AR nasal epithelial (ARNE) cells which were cultured from nasal mucosa of AR subjects, and exposure of ARNE cells to AR-SA reduced IL-33 mRNA and secreted protein levels. Particularly, ovalbumin-driven AR mice inoculated with AR-SA by intranasal delivery exhibited significantly reduced IL-33 in their nasal mucosa. In the context of these results, allergic symptoms and Th2 cytokine levels were significantly downregulated after intranasal inoculation of AR-SA in vivo AR mice. Conclusion: Colonization by Staphylococcus species was more dominant in allergic nasal mucosa, and nasal commensal S. aureus from subjects with AR mediates anti-allergic effects by modulating IL-33-dependent Th2 inflammation. The results demonstrate the role of host-bacterial commensalism in shaping human allergic inflammation.

show abstract

Association of Staphylococcus aureus colonization with food allergy occurs independently of eczema severity

Abstract: the costs of phlebotomy. G.L. acknowledges the Davis Foundation for academic support. O.T. received a research fellowship from the Clemens von Pirquet Foundation (Geneva, Switzerland).

Cited by 94 publications

References 25 publications

Symbiotic microbiome Staphylococcus aureus from human nasal mucus modulates IL-33-mediated type 2 immune responses in allergic nasal mucosa

Symbiotic microbiome Staphylococcus aureus from human nasal mucus modulates IL-33-mediated type 2 immune responses in allergic nasal mucosa

Symbiotic microbiome Staphylococcus aureus from human nasal mucus modulates IL-33-mediated type 2 immune responses in allergic nasal mucosa

Symbiotic microbiome Staphylococcus aureus from human nasal mucus modulates IL-33-mediated type 2 immune responses in allergic nasal mucosa

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