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Published on: September 22, 2023
Artemisia pollen-induced allergic rhinitis in mice: multi-omics dissection of local and systemic molecular
Jiaoni Chi1,2, Lin Chen1, Yuxuan Jin1
1Department of Allergy, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing, China.
Background:
Mugwort (Artemisia vulgaris) is a predominant aeroallergen for allergic rhinitis (AR) in northern China. However, the molecular changes linking local nasal mucosal inflammation with systemic alterations remain incompletely understood. This study aimed to explore the cross-level regulatory network in a mouse model of mugwort-induced AR by combining nasal mucosal transcriptomics and serum metabolomics.
Methods:
BALB/c mice were sensitized with mugwort extract and then challenged intranasally to establish an AR model. Nasal mucosal tissues were collected for RNA sequencing, and serum samples from the same cohort were subjected to non-targeted metabolomic analysis. Transcription factor (TF)-associated analysis, pathway enrichment analysis, and integrative multi-omics analysis were used to identify candidate regulatory factors and pathways involved in mugwort-induced allergic inflammation. Targeted validation of arginine-related changes was performed by measuring serum Arg1 and L-arginine levels, followed by ARG2 knockdown analysis in BEAS-2B epithelial cells after mugwort extract stimulation.
Results:
Transcriptomic analysis revealed a clear Th2-type immune response in the model group, with significant upregulation of Il13, Arg1, Ccl24 and Il6. In addition, many downregulated genes were enriched in pathways related to ciliary function and epithelial differentiation, accompanied by suppression of structural genes such as Krt25 and Krt71. Gene set enrichment and TF-associated analyses further highlighted cytokine-mediated signaling and potential upstream regulators, including Fos, Batf, and Mafb. Serum metabolomics showed increased 1-methylhistamine and enrichment of arachidonic acid metabolism in mugwort-treated mice. Integrated analysis of the two omics datasets further pointed to arginine-related metabolism as a shared altered pathway. Consistently, targeted assays showed increased serum Arg1 levels and decreased serum L-arginine concentrations in the mugwort group. In BEAS-2B cells, ARG2 knockdown attenuated the induction of IL6 and CCL26 after mugwort extract stimulation.
Conclusion:
Together, our findings indicate that mugwort-induced AR is accompanied by coordinated local and systemic changes, including immune activation, epithelial/ciliary dysfunction, and serum metabolic remodeling. The arginine-related alterations supported by both omics analysis and targeted validation provide a potential link between nasal mucosal inflammation and systemic metabolic changes in mugwort allergy.
Insights
Mugwort allergy causes nasal inflammation and systemic changes, involving immune responses and epithelial dysfunction. Arginine metabolism alterations link local and systemic effects in mugwort-induced allergic rhinitis.
Area of Science:
- Immunology
- Allergology
- Systems Biology
Background:
- Mugwort (Artemisia vulgaris) is a major cause of allergic rhinitis (AR) in northern China.
- The molecular mechanisms connecting nasal inflammation and systemic changes in mugwort allergy are not fully understood.
Purpose of the Study:
- To investigate the cross-level regulatory network in mugwort-induced AR.
- To combine nasal mucosal transcriptomics and serum metabolomics to identify key molecular pathways.
Main Methods:
- Established a mugwort-induced AR mouse model.
- Performed RNA sequencing on nasal tissues and non-targeted metabolomics on serum.
- Utilized TF-associated analysis, pathway enrichment, and multi-omics integration.
- Validated arginine-related changes and performed gene knockdown experiments.
Main Results:
- Transcriptomics showed a Th2 immune response with upregulated IL-13 and ARG1, and downregulated ciliary/epithelial genes.
- Metabolomics revealed increased 1-methylhistamine and altered arachidonic acid metabolism.
- Integrated analysis highlighted arginine metabolism as a shared pathway, with increased serum Arg1 and decreased L-arginine.
- ARG2 knockdown in epithelial cells reduced IL-6 and CCL26 induction.
Conclusions:
- Mugwort-induced AR involves coordinated local and systemic changes, including immune activation and epithelial dysfunction.
- Arginine metabolism alterations serve as a potential link between nasal inflammation and systemic metabolic changes in mugwort allergy.
