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In Utero Ultrafine Particulate Matter Exposure Causes Offspring Pulmonary Immunosuppression

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In Utero Ultrafine Particulate Matter Exposure Causes Offspring Pulmonary Immunosuppression In utero ultrafine particulate matter exposure causes offspring pulmonary immunosuppression Kristal A. Rychlika,1,2, Jeremiah R. Secrestb,2, Carmen Lauc, Jairus Pulczinskia,1, Misti L. Zamorad,1, Jeann Lealc, Rebecca Langleya, Louise G. Myatta, Muppala Rajue, Richard C.-A. Changf, Yixin Lib, Michael C. Goldingf, Aline Rodrigues-Hoffmannc, Mario J. Molinag,3, Renyi Zhangb,d, and Natalie M. Johnsona,2,3 aDepartment of Environmental and Occupational Health, Texas A&M University, College Station, TX 77843; bDepartment of Chemistry, Texas A&M University, College Station, TX 77843; cDepartment of Veterinary Pathobiology, Texas A&M University, College Station, TX 77843; dDepartment of Atmospheric Sciences, Texas A&M University, College Station, TX 77843; eDepartment of Epidemiology and Biostatistics, Texas A&M University, College Station, TX 77843; fDepartment of Veterinary Physiology and Pharmacology, Texas A&M University, College Station, TX 77843; and gDepartment of Chemistry and Biochemistry, University of California, San Diego, La Jolla, CA 92093 Contributed by Mario J. Molina, December 6, 2018 (sent for review September 19, 2018; reviewed by Alexandra Noel and Tong Zhu) Early life exposure to fine particulate matter (PM) in air is predominance of T helper (Th) 2 cell-associated cytokine pro- associated with infant respiratory disease and childhood asthma, duction classically define the phenotypic response. This frame- but limited epidemiological data exist concerning the impacts of work has been extended to include an imbalanced Th17 and ultrafine particles (UFPs) on the etiology of childhood respiratory regulatory T cell (Treg) response (13). Knowledge on the disease. Specifically, the role of UFPs in amplifying Th2- and/or Th17- mechanisms of allergic inflammation has largely been derived driven inflammation (asthma promotion) or suppressing effector from murine models of asthma, which can replicate key features T cells (increased susceptibility to respiratory infection) remains unclear. of the human disease (14). Sensitization followed by inhalation Using a mouse model of in utero UFP exposure, we determined early challenge with the egg protein ovalbumin (OVA) results in air- immunological responses to house dust mite (HDM) allergen in way hyperreactivity and pulmonary inflammation driven by in- offspring challenged from 0 to 4 wk of age. Two mice strains were creased Th2-cytokine production. Th17 cells can exacerbate exposed throughout gestation: C57BL/6 (sensitive to oxidative stress) Th2-cell–mediated eosinophilic inflammation as well as pro- SCIENCES and BALB/C (sensitive to allergen exposure). Offspring exposed to UFPs mote airway neutrophilia. The house dust mite (HDM) asthma ENVIRONMENTAL in utero exhibited reduced inflammatory response to HDM. Compared model primes a strong Th17 response resulting in enhanced with filtered air (FA)-exposed/HDM-challenged mice, UFP-exposed off- spring had lower white blood cell counts in bronchoalveolar lavage pulmonary inflammation and airway hyperresponsiveness (15). Limited epidemiological studies have evaluated the specific fluid and less pronounced peribronchiolar inflammation in both strains, role of early life exposure to ultrafine particles (UFPs) with an albeit more apparent in C57BL/6 mice. In the C57BL/6 strain, offspring aerodynamic diameter of less than 0.1 μm in asthma development, exposed in utero to FA and challenged with HDM exhibited a robust response in inflammatory cytokines IL-13 and Il-17. In contrast, this response was lost in offspring exposed in utero to UFPs. Circulating IL- Significance 10 was significantly up-regulated in C57BL/6 offspring exposed to UFPs, suggesting increased regulatory T cell expression and suppressed Th2/ Particulate matter exposure causes infant respiratory morbidity Th17 response. Our results reveal that in utero UFP exposure at a level and mortality, but the role of ultrafine particles (UFPs) with an close to the WHO recommended PM guideline suppresses an early aerodynamic diameter of less than 0.1 μm in asthma and re- immune response to HDM allergen, likely predisposing neonates to spiratory tract infections is unclear. Limited mechanistic in- respiratory infection and altering long-term pulmonary health. formation is available concerning UFP influence on the etiology of childhood asthma or susceptibility to respiratory infections. air pollution | ultrafine particulate matter | in utero exposure | prenatal | Here we exposed two strains of mice (sensitive to oxidative pulmonary immunosuppression stress or allergen exposure) to UFPs throughout gestation at concentrations relevant to human exposures. Our results reveal arly life exposure to fine particulate matter (PM) in air is a window of pulmonary immunosuppression in offspring Eassociated with acute and chronic respiratory morbidities in following in utero UFP exposure. A dampened host immune infants and children (1–3). Fine PM is typically defined as par- response during early development underlies increased child- hood susceptibility to respiratory infections, highlighting the ticles with a diameter of smaller than 2.5 μm (or PM ), which 2.5 necessity to develop strategies to protect the fetus during this are directly emitted into the atmosphere (referred to as primary vulnerable period. particles) or formed in the atmosphere via the gas-to-particle – conversion process (referred to as secondary particles) (4 6). Author contributions: K.A.R., R.Z., and N.M.J. designed research; K.A.R., J.R.S., J.P., M.L.Z., Examples of the fine PM sources include vehicular and industrial J.L., R.L., L.G.M., M.R., R.C.-A.C., Y.L., and N.M.J. performed research; A.R.-H., M.J.M., and emissions as well as combustion of coal and wood for primary R.Z. contributed new reagents/analytic tools; C.L., M.C.G., A.R.-H., M.J.M., and R.Z. ana- particles and new particle formation from biogenic and anthro- lyzed data; and K.A.R. and N.M.J. wrote the paper. pogenic emissions (7–9). Epidemiologic studies indicate that Reviewers: A.N., Louisiana State University; and T.Z., Peking University. increased susceptibility to lower respiratory infections correlates The authors declare no conflict of interest. This open access article is distributed under Creative Commons Attribution-NonCommercial- with in utero exposure to PM2.5 (3, 10, 11). Furthermore, there is NoDerivatives License 4.0 (CC BY-NC-ND). increasing evidence showing that developmental exposure to 1Present address: Department of Environmental Health and Engineering, Bloomberg PM2.5 increases wheeze and asthma risk in childhood (12). School of Public Health, Johns Hopkins University, Baltimore, MD 21205. Asthma is a heterogeneous immunologically mediated disease 2K.A.R., J.R.S., and N.M.J. contributed equally to this work. with a number of distinct clinical phenotypes. The most common 3To whom correspondence may be addressed. Email: [email protected] or form is allergic asthma, which results from an exacerbated im- [email protected]. mune response to inhaled allergens in individuals who are This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. termed “atopic asthmatics.” Eosinophilic inflammation, antigen- 1073/pnas.1816103116/-/DCSupplemental. specific IgE reactivity, airway hyperresponsiveness, and the www.pnas.org/cgi/doi/10.1073/pnas.1816103116 PNAS Latest Articles | 1of6 Downloaded by guest on September 29, 2021 although exposure has been associated with asthma exacerba- fractions of 44, 39, 10, and 7%, respectively (Fig. 1A). The tion in children (16). UFPs represent an important component particle size ranged from 20 to 220 nm, with a peak diameter of of ambient PM and traffic-related air pollution (17). However, about 50 nm (Fig. 1B) and a total surface area of (3.2 ± 0.3) × the current National Ambient Air Quality Standard does not 103 μm2/cm3. The particle number concentration was measured specifically classify UFPs as a criteria pollutant (18). A few by a condensational particle counter. In our model, we admin- mouse models have investigated the offspring allergic inflam- istered UFPs to time-mated mice 6/h per day from gestation days matory response to inhaled allergens following in utero exposure 0–18 (Fig. 1C). Daily exposure values over the gestational period to diesel exhaust particulate matter (DEPM), a primary com- had an average mass concentration of 101.94 μg/m3 ± 0.0784 ponent of traffic-related pollutants. Findings from the previous (SE), corresponding to a 24-h daily mean dose of 25 μg/m3. studies vary considerably, demonstrating either increased airway While there is no current regulatory standard for UFPs (18), this inflammation and airway hyperreactivity indicative of an asth- level is under the US Environmental Protection Agency national – 3 matic phenotype (19 21), no effect (22), or even protection from ambient air quality standard of 35 μg/m for PM2.5 and similar to airway inflammation in response to allergen challenge (23). The the WHO recommended guideline of 25 μg/m3 for 24-h average source and size of particles as well as timing of both PM and exposure. In utero exposure to UFPs had no effect on litter size. allergen exposure may be critical due to the complexity of fetal Furthermore, in utero UFP exposure did not affect offspring and infant lung and immune system development during this growth, including weight and length, which were measured be- period. In neonatal mice, which represent an immunologically ginning on postnatal day 3 until 4 wk of age. immature population, coexposure to DEPM (with a mean di- ameter between 0.1 and 0.3 μm) and HDM from 0 to 3 wk of age In Utero Exposure to UFPs Dampens Offspring Pulmonary markedly enhanced airway inflammation through a mixed Th2 Inflammatory Response to HDM and Th17 response compared with HDM treatment alone (24). Following birth, offspring exposed to filtered air (FA) or UFPs in Conversely, a model where neonatal mice were exposed to utero were placed onto a subchronic allergen challenge using combustion-derived PM (CDPM) with a mean diameter of μ – HDM from 0 to 4 wk of age and killed on postnatal day 31 (72 h 0.2 mbefore(0 1 wk) and throughout HDM dosing from 1 to after the final dose) (Fig.
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