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Three Main SCFAs Mitigate Lung Inflammation and Tissue Remodeling Nlrp3-Dependent in Murine HDM-Induced Neutrophilic Asthma

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Abstract

Neutrophilic asthma is generally defined by poorly controlled symptoms and high levels of neutrophils in the lungs. Short-chain fatty acids (SCFAs) are proposed as nonpharmacological therapy for allergic asthma, but their impact on the neutrophilic asthma lacks evidence. SCFAs regulate immune cell responses and impact the inflammasome NLRP3, a potential pharmacological target for neutrophilic asthma. Here, we explored the capacity of SCFAs to mitigate murine-induced neutrophilic asthma and the contribution of NLRP3 to this asthma. The objective of this study is to analyze whether SCFAs can attenuate lung inflammation and tissue remodeling in murine neutrophilic asthma and NLRP3 contribution to this endotype. Wild-type (WT) C57BL6 mice orotracheally received 10 μg of HDM (house dust mite) in 80 μL of saline on days 0, 6–10. To explore SCFAs, each HDM group received 200 mM acetate, propionate, or butyrate. To explore NLRP3, Nlrp3 KO mice received the same protocol of HDM. On the 14th day, after euthanasia, bronchoalveolar lavage fluid (BALF) and lungs were collected to evaluate cellularity, inflammatory cytokines, and tissue remodeling. HDM group had increased BALF neutrophil influx, TNF-α, IFN-γ, IL-17A, collagen deposition, and mucus secretion compared to control. SCFAs distinctively attenuate lung inflammation. Only features of tissue remodeling were Nlrp3-dependent such as collagen deposition, mucus secretion, active TGF-β cytokine, and IMs CD206+. SCFAs greatly decreased inflammatory cytokines and tissue remodeling. Only tissue remodeling was dependent on NLRP3. It reveals the potential of SCFAs to act as an additional therapy to mitigate neutrophilic asthma and the NLRP3 contribution to asthma.

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AVAILABILITY OF DATA AND MATERIALS

All data are available upon reasonable request to the corresponding author.

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ACKNOWLEDGEMENTS

We acknowledge the generous support of the Science and Technology Institute (ICT) and Center for Development of Experimental Models for Biology and Medicine (CEDEME), both from UNIFESP.

Funding

The study was supported by Coordination for the Improvement of Higher Education Personnel (CAPES) and São Paulo State Research Support Foundation (FAPESP; Grant 2017/19029-2).

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Authors and Affiliations

  1. Department of Science and Technology, Federal University of São Paulo (UNIFESP), São José dos Campos, SP, 12247-014, Brazil

    Barbara S. S. Tagé & Flávio Aimbire

  2. Department of Microbiology, Immunology and Parasitology, Federal University of São Paulo (UNIFESP), São Paulo, SP, 05468-901, Brazil

    Michelangelo B. Gonzatti & Alexandre C. Keller

  3. Postgraduate Program in Human Movement and Rehabilitation and in Pharmaceutical Sciences, Evangelical University of Goiás (UniEvangélica), Anápolis, GO, 75083-515, Brazil

    Rodolfo P. Vieira

  4. Postgraduate Program in Bioengineering, University Brasil, São Paulo, SP, 08230-030, Brazil

    Rodolfo P. Vieira

  5. Postgraduate Program in Sciences of Human Movement and Rehabilitation, Federal University of São Paulo (UNIFESP), Santos, SP, 11010-150, Brazil

    Rodolfo P. Vieira

  6. Department of Pharmacology, Federal University of São Paulo (UNIFESP), São Paulo, SP, 04023-062, Brazil

    Karina R. Bortoluci

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Contributions

B.S.S.T. contributed to conceptualization, methodology, investigation, and to the writing of the manuscript and review process. F.A. contributed to conceptualization, investigation, and resources. B.S.S.T., M.B.G., R.P.V., A.C.K., K.R.B. contributed to the methodology.

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Correspondence to Barbara S. S. Tagé.

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All animal experiments were previously analyzed and approved by the Ethics Committee on the Use of Animal from the Federal University of São Paulo (CEUA—UNIFESP), which follows the National Council for the Control of Animal Experimentation (CONCEA), under the approval number: 5866211118. No human research was conducted.

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The authors declare no competing interests.

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Tagé, B.S.S., Gonzatti, M.B., Vieira, R.P. et al. Three Main SCFAs Mitigate Lung Inflammation and Tissue Remodeling Nlrp3-Dependent in Murine HDM-Induced Neutrophilic Asthma. Inflammation (2024). https://doi.org/10.1007/s10753-024-01983-x

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