Effects of chronic allergic lung inflammation on gut microbiota and depression-like behavior in mice

Akihiro Kanaya , Elvedin Luković , Charles Emala , Maya Mikami

Exploration of Asthma & Allergy ›› 2025, Vol. 3 ›› Issue (1) : 100978

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Exploration of Asthma & Allergy ›› 2025, Vol. 3 ›› Issue (1) :100978 DOI: 10.37349/eaa.2025.100978
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Effects of chronic allergic lung inflammation on gut microbiota and depression-like behavior in mice
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Abstract

Aim: Emerging epidemiological studies have reported a link between allergic diseases, including asthma, and depression. Evidently, the gut microbiota is involved in the pathogenesis of asthma and depression. Therefore, we investigated whether allergic lung inflammation in mice causes gut microbial dysbiosis, via the gut-brain axis, which is potentially associated with depression. Methods: Wild-type C57BL/6J female mice were sensitized with intranasal house dust mite (HDM) antigen or phosphate-buffered saline (PBS) for 6 weeks to induce chronic allergic lung inflammation. Sucrose preference tests were performed for assessing depression. Fecal samples were collected, and 16S ribosomal RNA gene sequencing was performed to detect differences in gut microbiota composition between the HDM and PBS groups. The distance calculation, clustering of operational taxonomic units, rarefaction analysis, and estimator calculation (α- and β-diversity) were performed. Results: There was a significant difference in β-diversity (Bray-Curtis dissimilarity, F-statistics=6.16, p=0.001) of the gut microbiota between HDM and PBS groups. However, there was no difference in the α-diversity. We observed multiple differentially abundant bacteria in the HDM and PBS groups. The order class Clostridia (p=0.0036) and genus Faecalibaculum (p=0.028) were more abundant in the HDM group, whereas the phylum Firmicutes (p=0.037) and genera Dubosiella (p=0.00024) and Turicibacter (p=0.037) were more abundant in the PBS group. Notably, the relative abundance of some bacteria was correlated with the sucrose preference test results. Conclusions: Six weeks of intranasal HDM administration to mimic the chronic status of lung inflammation in asthma changed the gut microbiome in mice and was associated with depression-like behavioral changes.

Keywords

Asthma / microbiome / gut-brain axis / allergy / depression

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Akihiro Kanaya, Elvedin Luković, Charles Emala, Maya Mikami. Effects of chronic allergic lung inflammation on gut microbiota and depression-like behavior in mice. Exploration of Asthma & Allergy, 2025, 3 (1) : 100978 DOI:10.37349/eaa.2025.100978

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References

[1]

GBD 2019 Diseases and Injuries Collaborators. Global burden of 369 diseases and injuries in 204 countries and territories, 1990-2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet. 2020; 396: 1204-22.

[2]

Han YY, Forno E, Marsland AL, Miller GE, Celedón JC. Depression, Asthma, and Bronchodilator Response in a Nationwide Study of US Adults. J Allergy Clin Immunol Pract. 2016; 4: 68-73.e1.

[3]

Choi HG, Kim JH, Park JY, Hwang YI, Jang SH, Jung KS. Association Between Asthma and Depression: A National Cohort Study. J Allergy Clin Immunol Pract. 2019; 7: 1239-45.e1.

[4]

Kanaya A, Yang M, Emala C, Mikami M. Chronic allergic lung inflammation negatively influences neurobehavioral outcomes in mice. J Neuroinflammation. 2022; 19: 210.

[5]

Guinane CM, Cotter PD. Role of the gut microbiota in health and chronic gastrointestinal disease: understanding a hidden metabolic organ. Therap Adv Gastroenterol. 2013; 6: 295-308.

[6]

Ihekweazu FD, Versalovic J. Development of the Pediatric Gut Microbiome: Impact on Health and Disease. Am J Med Sci. 2018; 356: 413-23.

[7]

Clemente JC, Manasson J, Scher JU. The role of the gut microbiome in systemic inflammatory disease. BMJ. 2018; 360: j5145.

[8]

Ghaisas S, Maher J, Kanthasamy A. Gut microbiome in health and disease: Linking the microbiome-gut-brain axis and environmental factors in the pathogenesis of systemic and neurodegenerative diseases. Pharmacol Ther. 2016; 158: 52-62.

[9]

de Miguel Díez J, Hernández Barrera V, Puente Maestu L, Carrasco Garrido P, Gómez García T, Jiménez García R. Psychiatric Comorbidity in Asthma Patients. Associated Factors. J Asthma. 2011; 48: 253-8.

[10]

Trueba AF, Ritz T, Trueba G. The Role of the Microbiome in the Relationship of Asthma and Affective Disorders. Adv Exp Med Biol. 2016; 874: 263-88.

[11]

Valverde-Molina J, García-Marcos L. Microbiome and Asthma: Microbial Dysbiosis and the Origins, Phenotypes, Persistence, and Severity of Asthma. Nutrients. 2023; 15: 486.

[12]

Nelson JW, Phillips SC, Ganesh BP, Petrosino JF, Durgan DJ, Bryan RM. The gut microbiome contributes to blood-brain barrier disruption in spontaneously hypertensive stroke prone rats. FASEB J. 2021; 35: e21201.

[13]

Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013; 10: 996-8.

[14]

Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011; 27: 2194-200.

[15]

Kyrpides NC. Genomes OnLine Database (GOLD 1.0): a monitor of complete and ongoing genome projects world-wide. Bioinformatics. 1999; 15: 773-4.

[16]

Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013; 41: D590-6.

[17]

Chiu CY, Chan YL, Tsai YS, Chen SA, Wang CJ, Chen KF, et al. Airway Microbial Diversity is Inversely Associated with Mite-Sensitized Rhinitis and Asthma in Early Childhood. Sci Rep. 2017; 7: 1820.

[18]

Alashkar Alhamwe B, Gao Z, Alhamdan F, Harb H, Pichene M, Garnier A, et al. Intranasal administration of Acinetobacter lwoffii in a murine model of asthma induces IL-6-mediated protection associated with cecal microbiota changes . Allergy. 2023; 78: 1245-57.

[19]

Bermon S, Petriz B, Kajėnienė A, Prestes J, Castell L, Franco OL. The microbiota: an exercise immunology perspective. Exerc Immunol Rev. 2015; 21: 70-9.

[20]

Nakov T, Ashworth M, Theriot EC. Comparative analysis of the interaction between habitat and growth form in diatoms. ISME J. 2015; 9: 246-55.

[21]

Hashikawa-Hobara N, Otsuka A, Okujima C, Hashikawa N. Lactobacillus paragasseri OLL2809 Improves Depression-Like Behavior and Increases Beneficial Gut Microbes in Mice . Front Neurosci. 2022; 16: 918953.

[22]

Li L, Fang Z, Liu X, Hu W, Lu W, Lee YK, et al. Lactobacillus reuteri attenuated allergic inflammation induced by HDM in the mouse and modulated gut microbes . PLoS One. 2020; 15: e0231865.

[23]

Tsai WH, Yeh WL, Chou CH, Wu CL, Lai CH, Yeh YT, et al. Suppressive Effects of Lactobacillus on Depression through Regulating the Gut Microbiota and Metabolites in C57BL/6J Mice Induced by Ampicillin . Biomedicines. 2023; 11: 1068.

[24]

Breit S, Kupferberg A, Rogler G, Hasler G. Vagus Nerve as Modulator of the Brain-Gut Axis in Psychiatric and Inflammatory Disorders. Front Psychiatry. 2018; 9: 44.

[25]

Rastogi S, Singh A. Gut microbiome and human health: Exploring how the probiotic genus Lactobacillus modulate immune responses . Front Pharmacol. 2022; 13: 1042189.

[26]

Fujimura KE, Demoor T, Rauch M, Faruqi AA, Jang S, Johnson CC, et al. House dust exposure mediates gut microbiome Lactobacillus enrichment and airway immune defense against allergens and virus infection . Proc Natl Acad Sci U S A. 2014; 111: 805-10.

[27]

Spacova I, Van Beeck W, Seys S, Devos F, Vanoirbeek J, Vanderleyden J, et al. Lactobacillus rhamnosus probiotic prevents airway function deterioration and promotes gut microbiome resilience in a murine asthma model . Gut Microbes. 2020; 11: 1729-44.

[28]

Galeana-Cadena D, Gómez-García IA, Lopez-Salinas KG, Irineo-Moreno V, Jiménez-Juárez F, Tapia-García AR, et al. Winds of change a tale of: asthma and microbiome. Front Microbiol. 2023; 14: 1295215.

[29]

Lee MK, Wyss AB, Carnes MU, Richards M, Parks CG, Beane Freeman LE, et al. House dust microbiota in relation to adult asthma and atopy in a US farming population. J Allergy Clin Immunol. 2021; 147: 910-20.

[30]

Holt PG, Macaubas C, Stumbles PA, Sly PD. The role of allergy in the development of asthma. Nature. 1999; 402: B12-7.

[31]

McDonald VM, Hiles SA, Godbout K, Harvey ES, Marks GB, Hew M, et al. Treatable traits can be identified in a severe asthma registry and predict future exacerbations. Respirology. 2019; 24: 37-47.

[32]

Lin P, Ding B, Feng C, Yin S, Zhang T, Qi X, et al. Prevotella and Klebsiella proportions in fecal microbial communities are potential characteristic parameters for patients with major depressive disorder. J Affect Disord. 2017; 207: 300-4.

[33]

Liu Y, Zhang L, Wang X, Wang Z, Zhang J, Jiang R, et al. Similar Fecal Microbiota Signatures in Patients With Diarrhea-Predominant Irritable Bowel Syndrome and Patients With Depression. Clin Gastroenterol Hepatol. 2016; 14: 1602-11.e5.

[34]

Jiang H, Ling Z, Zhang Y, Mao H, Ma Z, Yin Y, et al. Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav Immun. 2015; 48: 186-94.

[35]

Manos J. The human microbiome in disease and pathology. APMIS. 2022; 130: 690-705.

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