Effects of nasal allergens and environmental particulate matter on brainstem metabolites and the consequence of brain-spleen axis in allergic rhinitis

JianShu Guo; Lei Lei; Haibo Yang; Bin Zhou; DongXia Fan; Biao Wu; Ge Wang; Lu Yu; ChiHang Zhang; Wenqing Zhang; QingJian Han; Xiao-Yong Zhang; JinZhuo Zhao

Environment International (Aug 2024)

Effects of nasal allergens and environmental particulate matter on brainstem metabolites and the consequence of brain-spleen axis in allergic rhinitis

JianShu Guo,
Lei Lei,
Haibo Yang,
Bin Zhou,
DongXia Fan,
Biao Wu,
Ge Wang,
Lu Yu,
ChiHang Zhang,
Wenqing Zhang,
QingJian Han,
Xiao-Yong Zhang,
JinZhuo Zhao

Affiliations

JianShu Guo: Department of Environmental Health, School of Public Health and the Key Laboratory of Public Health Safety, Fudan University, Shanghai, China
Lei Lei: Department of Environmental Health, School of Public Health and the Key Laboratory of Public Health Safety, Fudan University, Shanghai, China; The Changning District Center for Disease Control and Prevention, Shanghai, China
Haibo Yang: Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China
Bin Zhou: State Key Laboratory of Medical Neurobiology and MOE Frontier Center for Brain Science, Institutes of Brain Science, Fudan University, Shanghai, China
DongXia Fan: Department of Environmental Health, School of Public Health and the Key Laboratory of Public Health Safety, Fudan University, Shanghai, China
Biao Wu: Department of Environmental Health, School of Public Health and the Key Laboratory of Public Health Safety, Fudan University, Shanghai, China
Ge Wang: Department of Environmental Health, School of Public Health and the Key Laboratory of Public Health Safety, Fudan University, Shanghai, China
Lu Yu: Department of Environmental Health, School of Public Health and the Key Laboratory of Public Health Safety, Fudan University, Shanghai, China
ChiHang Zhang: Department of Environmental Health, School of Public Health and the Key Laboratory of Public Health Safety, Fudan University, Shanghai, China
Wenqing Zhang: Department of Environmental Health, School of Public Health and the Key Laboratory of Public Health Safety, Fudan University, Shanghai, China
QingJian Han: State Key Laboratory of Medical Neurobiology and MOE Frontier Center for Brain Science, Institutes of Brain Science, Fudan University, Shanghai, China; Corresponding authors at: Department of Environmental Health, School of Public Health and the Key Laboratory of Public Health Safety, Fudan University, Shanghai, China (J.Z. Zhao). College of Health Science and Technology & Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China (X.-Y. Zhang). State Key Laboratory of Medical Neurobiology and MOE Frontier Center for Brain Science, Institutes of Brain Science, Fudan University, Shanghai, China (Q.J. Han).
Xiao-Yong Zhang: Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China; College of Health Science and Technology & Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China; Corresponding authors at: Department of Environmental Health, School of Public Health and the Key Laboratory of Public Health Safety, Fudan University, Shanghai, China (J.Z. Zhao). College of Health Science and Technology & Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China (X.-Y. Zhang). State Key Laboratory of Medical Neurobiology and MOE Frontier Center for Brain Science, Institutes of Brain Science, Fudan University, Shanghai, China (Q.J. Han).
JinZhuo Zhao: Department of Environmental Health, School of Public Health and the Key Laboratory of Public Health Safety, Fudan University, Shanghai, China; Corresponding authors at: Department of Environmental Health, School of Public Health and the Key Laboratory of Public Health Safety, Fudan University, Shanghai, China (J.Z. Zhao). College of Health Science and Technology & Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China (X.-Y. Zhang). State Key Laboratory of Medical Neurobiology and MOE Frontier Center for Brain Science, Institutes of Brain Science, Fudan University, Shanghai, China (Q.J. Han).

Journal volume & issue: Vol. 190
p. 108890

Abstract

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Background: The growing consensus links exposure to fine particulate matter (PM2.5) with an increased risk of respiratory diseases. However, little is known about the additional effects of particulate matter on brainstem function in allergic rhinitis (AR). Furthermore, it is unknown to what extent the PM2.5-induced effects in the brainstem affect the inflammatory response in AR. This study aimed to determine the effects, mechanisms and consequences of brainstem neural activity altered by allergenic stimulation and PM2.5 exposure. Methods: Using an AR model of ovalbumin (OVA) elicitation and whole-body PM2.5 exposure, the metabolic profile of the brainstem post-allergen stimulation was characterized through in vivo proton magnetic resonance imaging (1H-MRS). Then, the transient receptor potential vanilloid-1 (TRPV1) neuronal expression and sensitivity in the trigeminal nerve in AR were investigated. The link between TRPV1 expression and brainstem differential metabolites was also determined. Finally, we evaluated the mediating effects of brainstem metabolites and the consequences in the brain-spleen axis in the inflammatory response of AR. Results: Exposure to allergens and PM2.5 led to changes in the metabolic profiles of the brainstem, particularly affecting levels of glutamine (Gln) and glutamate (Glu). This exposure also increased the expression and sensitivity of TRPV1+ neurons in the trigeminal nerve, with the levels of TRPV1 expression closely linked to the brainstem metabolism of Glu and Gln. Moreover, allergens increased the activity of p38, while PM2.5 led to the phosphorylation of p38 and ERK, resulting in the upregulation of TRPV1 expression. The brainstem metabolites Glu and Gln were found to partially mediate the impact of TRPV1 on AR inflammation, which was supported by the presence of pro-inflammatory changes in the brain-spleen axis. Conclusion: Brainstem metabolites are altered under allergen stimulation and additional PM2.5 exposure in AR via sensitization of the trigeminal nerve, which exacerbates the inflammatory response via the brain-splenic axis.

Published in Environment International

ISSN: 0160-4120 (Print)
Publisher: Elsevier
Country of publisher: United Kingdom
LCC subjects: Geography. Anthropology. Recreation: Environmental sciences
Website: https://www.journals.elsevier.com/environment-international

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