Regulatory T cells and IL10 suppress pulmonary host defense during early-life exposure to radical containing combustion derived ultrafine particulate matter
Open accessAbstract
Exposure to elevated levels of particulate matter (PM) is associated with increased risk of morbidity and mortality due to respiratory tract viral infections in infants. Recent identification of environmentally persistent free radicals (EPFRs) in the PM from a variety of combustion sources suggests its role in the enhancement of disease severity of lower respiratory tract infections (LRTI). Our previous studies demonstrated that acute exposure to EPFRs induces pulmonary immunosuppression allowing for enhanced influenza disease severity. Here, we determine the mechanism of EPFR-induced immunosuppression and its impact on the immune response towards influenza infection. Neonatal mice (3 days old) were acutely exposed to DCB (combustion derived PM with chemisorbed EPFR) for seven consecutive days. Four days post-exposure (dpe), mice were infected with influenza virus. Pulmonary T cell phenotypes including regulatory T cells (Tregs) were analyzed by flow cytometry. The role of IL10 in EPFR-induced exacerbation of influenza disease severity was determined by administering recombinant IL10 (rIL10) to wild type mice or by using IL10 deficient (IL10 −/− ) neonatal mice. Mice were assessed for morbidity by measuring percent weight change and pulmonary viral load. Neonatal mice exposed to EPFRs had a significant increase in pulmonary Tregs and the immunosuppressive cytokine IL10 following influenza infection, which coincided with decreased protective T cell responses to influenza infection at 6 dpi. Depletion of Tregs in EPFR-exposed neonatal mice resulted in increased protective, adaptive T cell responses, whereas adoptive transfer of Tregs from EPFR-exposed neonates to air-exposed neonatal mice suppressed adaptive T cell responses towards influenza infection. Further, treatment with rIL10 could recapitulate EPFR-induced exacerbation of morbidity and pulmonary viral load compared to air exposed and influenza infected mice, whereas, EPFR-exposed IL10 −/− neonates exhibited significant reductions in morbidity, pulmonary viral load and adaptive T cell responses following influenza infection. Neonatal exposure to EPFRs induced Tregs and IL10 resulting in suppressed adaptive T cell responses and enhanced influenza disease severity in neonatal mice. Depletion of Tregs increased adaptive T cell responses and deficiency of IL10 reduced morbidity and conferred enhanced protection against influenza virus.
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IL-10 and Tregs suppress the adaptive response following early life PM0.1 exposure.
“Jaligama et al. confirmed the role of IL-10 and Tregs in suppressing the adaptive response following early life PM0.1 exposure [76].”
From Air pollution and children’s health—a review of adverse effects associated with prenatal exposure from fine to ultrafine particulate matter (2021) · cites this paper as [76]
The Conclusions report that neonatal exposure to EPFR-containing particulate matter induced Tregs and IL-10 and suppressed adaptive T-cell responses in mice challenged with influenza. However, the Methods (“Combustion derived PM”) give the tested particles a mean aerodynamic diameter of 0.195 µm, so the paper does not support specifying the exposure as PM0.1. (LLM, conf=0.88)
Experimental — accuracy not yet measuredDepletion of Tregs reduced morbidity and conferred enhanced protection against influenza virus after early life PM0.1 exposure.
“Depletion of Tregs reduced morbidity and conferred enhanced protection against influenza virus.”
From Air pollution and children’s health—a review of adverse effects associated with prenatal exposure from fine to ultrafine particulate matter (2021) · cites this paper as [76]
The Results section on Treg depletion reports increased protective Tc1 and Th1 responses in EPFR-exposed neonatal mice after influenza infection, but does not report reduced morbidity from Treg depletion. The Abstract Conclusions and the Results section on IL10 deficiency attribute reduced morbidity and enhanced protection to IL10 deficiency, not Treg depletion. No page numbers are available in our copy. (LLM, conf=0.90)
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“This shift in the immune response reduces the effectiveness of CD8 + and CD4 + T lymphocytes, which are vital for virus elimination [84].”
Kumar, A., Nde, D. B., Guo, C., Pathak, R., Foley, F., Ahmad, S., Dangal, P., Hasan, F., Lard, M. L., Aryal, A., et al. (2025) · Journal of Toxicology and Environmental Health Part B · doi:10.1080/10937404.2025.2602154 · Cited by 4 · see citing works
Self-citationWang, R.-R., Kong, D., & Ma, X. (2025) · Therapeutic Advances in Endocrinology and Metabolism · doi:10.1177/20420188251321600 · Cited by 2
“29 The number of regulatory T cells is reduced in the peripheral blood of SAT patients, but their expression is elevated in the thyroid gland, and this redistribution state may be an important factor in the pathogenesis of SAT.”
Dolgikh, O., Dianova, D., & Nikonoshina, N. (2022) · ЗДОРОВЬЕ НАСЕЛЕНИЯ И СРЕДА ОБИТАНИЯ - ЗНиСО / PUBLIC HEALTH AND LIFE ENVIRONMENT · doi:10.35627/2219-5238/2022-30-4-63-69 · Cited by 2
Heil, L. (2019) · doi:10.13023/etd.2019.403
“Partially depleting Tregs in pups that over-express them improves viral clearance (Jaligama et al., 2017), but we have previously shown that mouse pups without Tregs have diminished influenza virus clearance (Oliphant et al., 2015).”
BackgroundInfluential
- Authors
- Jaligama, S., Saravia, J., You, D., Yadav, N., Lee, G. I., Shrestha, B., & Cormier, S. A.
- Affiliations
- University of Tennessee Health Science Center (US)
- Corresponding author
- Cormier, Stephania A.
- Venue
- Respiratory Research
- Published
- 2017-01-13
- Volume
- 18
- Issue
- 1
- Pages
- 15-15
- ISSN
- 1465-9921 (ISSN-L)
- 1465-993X
- PMC
- PMC5237352
- OpenAlex
- W2572120777
- Cited by
- 40
- References
- 38
- Citations by year
- 2025: 4 · 2024: 7 · 2023: 6 · 2022: 5 · 2021: 9 · 2020: 6 · 2019: 1 · 2018: 1 · 2017: 1
- FWCI
- 1.11
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Respiratory Research (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Civil War Book Review (submittedVersion)
- Funders
- National Institute of Environmental Health Sciences (P42ES013648, R01ES015050)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immunotoxicology and immune responses
- Health Sciences › Medicine › Physiology › Asthma and respiratory diseases
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Air Quality and Health Impacts
- Keywords
- regulatory T cells, IL-10, ultrafine particles, influenza, neonatal mice, Treg depletion, adoptive transfer
- MeSH terms
- Animals, Animals, Newborn, Environmental Exposure, Female, Free Radicals, Humans, Influenza, Human, Lung, Male, Mice, Inbred C57BL, Cytokines, Immunocompromised Host, T-Lymphocytes, Regulatory, Mice, Particulate Matter
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