doi: 10.1021/acs.est.4c10056.
Epub 2024 Dec 23.
Extracellular Vesicles Are Prevalent and Effective Carriers of Environmental Allergens in Indoor Dust
Affiliations
- PMID: 39711517
- PMCID: PMC11800389
- DOI: 10.1021/acs.est.4c10056
Item in Clipboard
Extracellular Vesicles Are Prevalent and Effective Carriers of Environmental Allergens in Indoor Dust
Environ Sci Technol.
.
Abstract
The global incidence of allergic diseases is rising and poses a substantial threat to human health. Allergenic proteins released by various allergenic species play a critical role in the pathogenesis of allergic diseases and have been widely detected in the environmental matrix. However, the release, presence and interaction of environmental allergens with human body remain to be elucidated. In this study, we reported the widespread of allergen-harboring extracellular vesicles (EVs) in indoor dust from 75 households across five provinces in China. Particle size and abundance of EVs were correlated with specific environmental factors. EVs showed long persistence and high resistance to environmental stress. Metagenomics and metaproteomics data revealed that most indoor allergenic species released allergens within the EVs into dust. A higher abundance of allergenic species and their derived EVs was observed in urban areas compared to rural areas. ELISA confirmed the allergenic activity of the EV-associated allergens. Allergens are common components and even markers of EVs, as evidenced by the data compilation of various allergenic species. The proportion of EV-associated allergens varied across species. EVs facilitated allergen entry into epithelial cells. Intranasally administered EVs can be rapidly transported to the lungs and gastrointestinal tract. EV-associated allergens exhibited higher allergenicity compared with non-EV allergens. Our findings elucidate a vesicle pathway through which environmental allergens are released, persist, and trigger allergic responses within EVs.
Keywords: allergic diseases; environmental allergens; extracellular vesicles; indoor dust.
Conflict of interest statement
The authors declare no competing financial interest.
Figures
Prevalence of allergenic
species-derived EVs in household dust.
(A) TEM images of EVs in household dust. Dust EVs were extracted from
rural (n = 5) and urban (n = 5)
areas in five provinces including Fujian (FJ), Henan (HA), Sichuan
(SC), Shaanxi (SN), and Shanxi (SX). The red arrow indicates the single-bilayer
EVs, while the yellow arrow denotes the OIMVs. Scale bar = 50 nm.
(B) Size distribution of EVs by NanoFCM. The band represents the standard
deviation. (C) Correlations among bacteria, fungi, particle concentration
of EVs and the ratio of EV particles to proteins. (D) Particle number
of dust EVs stored at room temperature for 0, 10, 25, and 50 days
(n = 3). Concentration of dust EV-associated proteins
and supernatant proteins (non-EVs) after long-term storage at room
temperature. All EVs were placed in EP tubes and stored under controlled
laboratory conditions at 25 °C with relative humidity 40–60%.
(E) Particle number of EVs from untreated, heated, and PK groups (n = 3). (F) PCoA plots of the Bray–Curtis distance
of biological composition at the genus level. Each dot represents
one sample. Colors were used to distinguish the rural and urban areas,
and the symbol of circle and plus indicated the dust samples and its
derived EVs samples, respectively. Ellipses represented the 95% confidence
interval (95% CI). (G) Distribution of allergenic species in dust
and their EV-associated DNA. The Venn diagram indicates the number
of allergenic species, while the bar graph shows the relative abundance
of allergenic species. (H) The number of predicted allergenic species
in dust and EVs in rural and urban areas. (I) The relative abundance
of allergenic species-associated DNA in dust and derived EVs in rural
and urban areas. Each dot represents one allergenic species. “ns” P > 0.05, * P < 0.05, ** P < 0.01, *** P < 0.001.
Allergens from household
dust EVs and the proportion of major allergens
in typical allergenic species. (A) Statistical classification of dust
EV-associated protein group sources at the kingdom and phylum level
using Sankey plots. The heights of the rectangles indicate the relative
abundance of taxonomic categories. (B) Relative abundance of dust
EV-associated protein groups derived from allergenic species. (C)
The number of predicted EV-associated allergens and other protein
groups. The radial bar chart shows the subcellular location of the
95 predicted EV-associated allergens. (D) The relative abundance of
predicted EV allergens and other protein groups in rural and urban
dust EVs. Each dotted line represents one protein group. (E) The concentration
of allergens (SEs, Art v 1 and Der f 1) in dust EVs by ELISA kits.
(F) The relative abundance of EV-associated allergens in the three
allergenic species. *** P < 0.001.
Data analysis
of allergenic species-derived EV-associated allergens.
(A) The number of predicted EV-associated allergens from different
allergenic species with strong and weak evidence for allergenicity.
(B) Subcellular localization and number of the 540 predicted EV-associated
allergens. (C) Subcellular localization of the 28 types of EV protein
markers predicted as allergens. Pie chart shows the proportion of
different subcellular localizations.
Effects of allergenic species-derived
EVs on human lung epithelial
cells. The cells were exposed to different concentrations of EVs (0,
1, and 10 μg). (A) Confocal laser microscopic images of BEAS-2B
cells after 6 h exposure to DiO-labeled EVs (green). The nuclei were
labeled with DAPI (blue) and the cytoskeleton with rhodamine (red).
Scale bar = 20 μm. ELISA was used to measure the levels of IL-6,
IL-8, IL-1β, and TNF-α secreted by BEAS-2B cells following
exposure to EVs derived fromS. aureus (B), A. annua pollen (C), and D. farinae (D) (n = 3). “ns” P > 0.05. * P < 0.05, ** P < 0.01, *** P < 0.001.
Tissue distribution and
allergenic activity of A.
annua pollen-derived EVs. (A) Representative IVIS
image of intranasal administration of 1 × 1010 particles/gram
body weight of DiR-EVs to a live mouse after 1 h and PBS-treated control
(n = 3). (B) Following in vivo imaging of PBS or
DiR-EVs mice, whole major organs (brain, heart, lungs, liver, spleen,
kidneys, and tract) were excised and imaged ex vivo. Representative
ex vivo images are shown. Organs are annotated on the left. (C) Quantitative
analysis of ex vivo imaging data of organs from PBS-treated and EV-treated
mice. Individual regions of interest (ROIs) were drawn for each organ
to obtain the respective fluorescence signals. Fluorescence signal
is expressed as total radiant efficiency [p/s]/[μW/cm2] per gram of tissue. (D) Protocol for modeling allergic airway inflammation
in mice (n = 5). (E) The nasal symptom scores were
different groups. (F) HE staining of paraffin-embedded lung and nasal
mucosa sections. Black arrows indicated inflammatory cell infiltration,
while yellow arrows indicated areas of congestion. (G, H) Serum levels
of total IgE, allergen-specific IgE, IgG2a, and IgG1 were measured
by ELISA. (I) Cytokines (IL-4, IL-5, and IL-13) in BALF were measured
by ELISA. * P < 0.05, ** P <
0.01, *** P < 0.001.
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