Profiling inflammatory outcomes of Candida albicans colonization and food allergy induction in the murine glandular stomach
ABSTRACT We investigated the effects of Candida albicans colonization on inflammatory responses in the murine glandular stomach, which is similar to the glandular mucosa of the human stomach. We also explored whether the presence of a food allergy could exacerbate C. albicans-induced inflammation or...
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American Society for Microbiology
2024-11-01
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| Series: | mBio |
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| Online Access: | https://journals.asm.org/doi/10.1128/mbio.02113-24 |
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| author | Karen D. Zeise Nicole R. Falkowski Kelsey G. Stark Christopher A. Brown Gary B. Huffnagle |
| author_facet | Karen D. Zeise Nicole R. Falkowski Kelsey G. Stark Christopher A. Brown Gary B. Huffnagle |
| author_sort | Karen D. Zeise |
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| description | ABSTRACT We investigated the effects of Candida albicans colonization on inflammatory responses in the murine glandular stomach, which is similar to the glandular mucosa of the human stomach. We also explored whether the presence of a food allergy could exacerbate C. albicans-induced inflammation or if C. albicans would amplify allergic inflammation in the glandular stomach. C. albicans successfully colonized the stomach of amoxicillin-pre-treated BALB/c mice and induced gastritis in the limiting ridge with minimal inflammation in the glandular stomach. There was significant upregulation of Il18, calprotectin (S100a8 and S100a9), and several antimicrobial peptides, but minimal induction of type 1, 2, or 3 responses in the glandular stomach. A robust type 2 response, inflammatory cell recruitment, and tissue remodeling occurred in the glandular stomach following oral ovalbumin challenges in sensitized mice. The type 2 response was not augmented by C. albicans colonization, but there was significant upregulation of Il1b, Il12a, Tnf, and Il17a in C. albicans-colonized food allergic mice. The presence of C. albicans did not affect the expression of genes involved in barrier integrity and signaling, many of which were upregulated during food allergy. Overall, our data indicate that C. albicans colonization induces minimal inflammation in the glandular stomach but augments antimicrobial peptide expression. Induction of a food allergy results in robust type 2 inflammation in the glandular stomach, and while C. albicans colonization does not exacerbate type 2 inflammation, it does activate a number of innate and type 3 immune responses amid the backdrop of allergic inflammation.IMPORTANCEFood allergy continues to be a growing public health concern, affecting at least 1 in 10 individuals in the United States alone. However, little is known about the involvement of the gastric mucosa in food allergy. Gastrointestinal Candida albicans colonization has been reported to promote gastrointestinal inflammation in a number of chronic diseases. Using a mouse model of food allergy to egg white protein, we demonstrate regionalization of the inflammatory response to C. albicans colonization, induction of robust type 2 (allergic) inflammation in the stomach, and augmentation of innate and type 3 responses by C. albicans colonization during food allergy. |
| format | Article |
| id | doaj-art-0eb96a9dd5f143b6b83cb8278b0d8d73 |
| institution | Kabale University |
| issn | 2150-7511 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | American Society for Microbiology |
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| series | mBio |
| spelling | doaj-art-0eb96a9dd5f143b6b83cb8278b0d8d732024-11-13T14:03:29ZengAmerican Society for MicrobiologymBio2150-75112024-11-01151110.1128/mbio.02113-24Profiling inflammatory outcomes of Candida albicans colonization and food allergy induction in the murine glandular stomachKaren D. Zeise0Nicole R. Falkowski1Kelsey G. Stark2Christopher A. Brown3Gary B. Huffnagle4Department of Microbiology & Immunology, University of Michigan, Ann Arbor, Michigan, USAMary H. Weiser Food Allergy Center, University of Michigan, Ann Arbor, Michigan, USAMary H. Weiser Food Allergy Center, University of Michigan, Ann Arbor, Michigan, USAAdvanced Research Computing, Information and Technology Services, University of Michigan, Ann Arbor, Michigan, USADepartment of Microbiology & Immunology, University of Michigan, Ann Arbor, Michigan, USAABSTRACT We investigated the effects of Candida albicans colonization on inflammatory responses in the murine glandular stomach, which is similar to the glandular mucosa of the human stomach. We also explored whether the presence of a food allergy could exacerbate C. albicans-induced inflammation or if C. albicans would amplify allergic inflammation in the glandular stomach. C. albicans successfully colonized the stomach of amoxicillin-pre-treated BALB/c mice and induced gastritis in the limiting ridge with minimal inflammation in the glandular stomach. There was significant upregulation of Il18, calprotectin (S100a8 and S100a9), and several antimicrobial peptides, but minimal induction of type 1, 2, or 3 responses in the glandular stomach. A robust type 2 response, inflammatory cell recruitment, and tissue remodeling occurred in the glandular stomach following oral ovalbumin challenges in sensitized mice. The type 2 response was not augmented by C. albicans colonization, but there was significant upregulation of Il1b, Il12a, Tnf, and Il17a in C. albicans-colonized food allergic mice. The presence of C. albicans did not affect the expression of genes involved in barrier integrity and signaling, many of which were upregulated during food allergy. Overall, our data indicate that C. albicans colonization induces minimal inflammation in the glandular stomach but augments antimicrobial peptide expression. Induction of a food allergy results in robust type 2 inflammation in the glandular stomach, and while C. albicans colonization does not exacerbate type 2 inflammation, it does activate a number of innate and type 3 immune responses amid the backdrop of allergic inflammation.IMPORTANCEFood allergy continues to be a growing public health concern, affecting at least 1 in 10 individuals in the United States alone. However, little is known about the involvement of the gastric mucosa in food allergy. Gastrointestinal Candida albicans colonization has been reported to promote gastrointestinal inflammation in a number of chronic diseases. Using a mouse model of food allergy to egg white protein, we demonstrate regionalization of the inflammatory response to C. albicans colonization, induction of robust type 2 (allergic) inflammation in the stomach, and augmentation of innate and type 3 responses by C. albicans colonization during food allergy.https://journals.asm.org/doi/10.1128/mbio.02113-24Candida albicansfood allergystomachimmunomodulationovalbumin |
| spellingShingle | Karen D. Zeise Nicole R. Falkowski Kelsey G. Stark Christopher A. Brown Gary B. Huffnagle Profiling inflammatory outcomes of Candida albicans colonization and food allergy induction in the murine glandular stomach mBio Candida albicans food allergy stomach immunomodulation ovalbumin |
| title | Profiling inflammatory outcomes of Candida albicans colonization and food allergy induction in the murine glandular stomach |
| title_full | Profiling inflammatory outcomes of Candida albicans colonization and food allergy induction in the murine glandular stomach |
| title_fullStr | Profiling inflammatory outcomes of Candida albicans colonization and food allergy induction in the murine glandular stomach |
| title_full_unstemmed | Profiling inflammatory outcomes of Candida albicans colonization and food allergy induction in the murine glandular stomach |
| title_short | Profiling inflammatory outcomes of Candida albicans colonization and food allergy induction in the murine glandular stomach |
| title_sort | profiling inflammatory outcomes of candida albicans colonization and food allergy induction in the murine glandular stomach |
| topic | Candida albicans food allergy stomach immunomodulation ovalbumin |
| url | https://journals.asm.org/doi/10.1128/mbio.02113-24 |
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