Probiotics Function as Immunomodulators in the Intestine in C57Bl/6 Male Mice Exposed to Inhaled Diesel Exhaust Particles on a High-Fat Diet

Epidemiological studies reveal a correlation between air pollution exposure and gastrointestinal (GI) diseases, yet few studies have investigated the role of inhaled particulate matter on intestinal integrity in conjunction with a high-fat (HF) diet. Additionally, there is currently limited informat...

Full description

Bibliographic Details
Main Authors: Danielle T. Phillippi, Sarah Daniel, Kayla N. Nguyen, Bea Angella Penaredondo, Amie K. Lund
Format: Article
Language:English
Published: MDPI AG 2022-04-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/11/9/1445
_version_ 1797505297566138368
author Danielle T. Phillippi
Sarah Daniel
Kayla N. Nguyen
Bea Angella Penaredondo
Amie K. Lund
author_facet Danielle T. Phillippi
Sarah Daniel
Kayla N. Nguyen
Bea Angella Penaredondo
Amie K. Lund
author_sort Danielle T. Phillippi
collection DOAJ
description Epidemiological studies reveal a correlation between air pollution exposure and gastrointestinal (GI) diseases, yet few studies have investigated the role of inhaled particulate matter on intestinal integrity in conjunction with a high-fat (HF) diet. Additionally, there is currently limited information on probiotics in mitigating air-pollutant responses in the intestines. Thus, we investigated the hypothesis that exposure to inhaled diesel exhaust particles (DEP) and a HF diet can alter intestinal integrity and inflammation, which can be attenuated with probiotics. 4–6-w-old male C57Bl/6 mice on a HF diet (45% kcal fat) were randomly assigned to be exposed via oropharyngeal aspiration to 35 µg of DEP suspended in 35 µL of 0.9% sterile saline or sterile saline (CON) only twice a week for 4 w. A subset of mice was treated with 0.3 g/day of Winclove Ecologic<sup>®</sup> barrier probiotics (PRO) in drinking water throughout the duration of the study. Our results show that DEP exposure ± probiotics resulted in increased goblet cells and mucin (MUC)-2 expression, as determined by AB/PAS staining. Immunofluorescent quantification and/or RT-qPCR showed that DEP exposure increases claudin-3, occludin, zona occludens (ZO)-1, matrix metalloproteinase (MMP)-9, and toll-like receptor (TLR)-4, and decreases tumor necrosis factor (TNF)-α and interleukin (IL)-10 expression compared to CON. DEP exposure + probiotics increases expression of claudin-3, occludin, ZO-1, TNF-α, and IL-10 and decreases MMP-9 and TLR-4 compared to CON + PRO in the small intestine. Collectively, these results show that DEP exposure alters intestinal integrity and inflammation in conjunction with a HF diet. Probiotics proved fundamental in understanding the role of the microbiome in protecting and altering inflammatory responses in the intestines following exposure to inhaled DEP.
first_indexed 2024-03-10T04:16:37Z
format Article
id doaj.art-088bb0c139eb437c982af03272faffb1
institution Directory Open Access Journal
issn 2073-4409
language English
last_indexed 2024-03-10T04:16:37Z
publishDate 2022-04-01
publisher MDPI AG
record_format Article
series Cells
spelling doaj.art-088bb0c139eb437c982af03272faffb12023-11-23T07:59:20ZengMDPI AGCells2073-44092022-04-01119144510.3390/cells11091445Probiotics Function as Immunomodulators in the Intestine in C57Bl/6 Male Mice Exposed to Inhaled Diesel Exhaust Particles on a High-Fat DietDanielle T. Phillippi0Sarah Daniel1Kayla N. Nguyen2Bea Angella Penaredondo3Amie K. Lund4Department of Biological Sciences, Advanced Environmental Research Institute, University of North Texas, Denton, TX 76203, USADepartment of Biological Sciences, Advanced Environmental Research Institute, University of North Texas, Denton, TX 76203, USADepartment of Biological Sciences, Advanced Environmental Research Institute, University of North Texas, Denton, TX 76203, USADepartment of Biological Sciences, Advanced Environmental Research Institute, University of North Texas, Denton, TX 76203, USADepartment of Biological Sciences, Advanced Environmental Research Institute, University of North Texas, Denton, TX 76203, USAEpidemiological studies reveal a correlation between air pollution exposure and gastrointestinal (GI) diseases, yet few studies have investigated the role of inhaled particulate matter on intestinal integrity in conjunction with a high-fat (HF) diet. Additionally, there is currently limited information on probiotics in mitigating air-pollutant responses in the intestines. Thus, we investigated the hypothesis that exposure to inhaled diesel exhaust particles (DEP) and a HF diet can alter intestinal integrity and inflammation, which can be attenuated with probiotics. 4–6-w-old male C57Bl/6 mice on a HF diet (45% kcal fat) were randomly assigned to be exposed via oropharyngeal aspiration to 35 µg of DEP suspended in 35 µL of 0.9% sterile saline or sterile saline (CON) only twice a week for 4 w. A subset of mice was treated with 0.3 g/day of Winclove Ecologic<sup>®</sup> barrier probiotics (PRO) in drinking water throughout the duration of the study. Our results show that DEP exposure ± probiotics resulted in increased goblet cells and mucin (MUC)-2 expression, as determined by AB/PAS staining. Immunofluorescent quantification and/or RT-qPCR showed that DEP exposure increases claudin-3, occludin, zona occludens (ZO)-1, matrix metalloproteinase (MMP)-9, and toll-like receptor (TLR)-4, and decreases tumor necrosis factor (TNF)-α and interleukin (IL)-10 expression compared to CON. DEP exposure + probiotics increases expression of claudin-3, occludin, ZO-1, TNF-α, and IL-10 and decreases MMP-9 and TLR-4 compared to CON + PRO in the small intestine. Collectively, these results show that DEP exposure alters intestinal integrity and inflammation in conjunction with a HF diet. Probiotics proved fundamental in understanding the role of the microbiome in protecting and altering inflammatory responses in the intestines following exposure to inhaled DEP.https://www.mdpi.com/2073-4409/11/9/1445intestinal integritydiesel exhaust particulate mattermucosal barriertight junctionsprobioticshigh-fat diet
spellingShingle Danielle T. Phillippi
Sarah Daniel
Kayla N. Nguyen
Bea Angella Penaredondo
Amie K. Lund
Probiotics Function as Immunomodulators in the Intestine in C57Bl/6 Male Mice Exposed to Inhaled Diesel Exhaust Particles on a High-Fat Diet
Cells
intestinal integrity
diesel exhaust particulate matter
mucosal barrier
tight junctions
probiotics
high-fat diet
title Probiotics Function as Immunomodulators in the Intestine in C57Bl/6 Male Mice Exposed to Inhaled Diesel Exhaust Particles on a High-Fat Diet
title_full Probiotics Function as Immunomodulators in the Intestine in C57Bl/6 Male Mice Exposed to Inhaled Diesel Exhaust Particles on a High-Fat Diet
title_fullStr Probiotics Function as Immunomodulators in the Intestine in C57Bl/6 Male Mice Exposed to Inhaled Diesel Exhaust Particles on a High-Fat Diet
title_full_unstemmed Probiotics Function as Immunomodulators in the Intestine in C57Bl/6 Male Mice Exposed to Inhaled Diesel Exhaust Particles on a High-Fat Diet
title_short Probiotics Function as Immunomodulators in the Intestine in C57Bl/6 Male Mice Exposed to Inhaled Diesel Exhaust Particles on a High-Fat Diet
title_sort probiotics function as immunomodulators in the intestine in c57bl 6 male mice exposed to inhaled diesel exhaust particles on a high fat diet
topic intestinal integrity
diesel exhaust particulate matter
mucosal barrier
tight junctions
probiotics
high-fat diet
url https://www.mdpi.com/2073-4409/11/9/1445
work_keys_str_mv AT danielletphillippi probioticsfunctionasimmunomodulatorsintheintestineinc57bl6malemiceexposedtoinhaleddieselexhaustparticlesonahighfatdiet
AT sarahdaniel probioticsfunctionasimmunomodulatorsintheintestineinc57bl6malemiceexposedtoinhaleddieselexhaustparticlesonahighfatdiet
AT kaylannguyen probioticsfunctionasimmunomodulatorsintheintestineinc57bl6malemiceexposedtoinhaleddieselexhaustparticlesonahighfatdiet
AT beaangellapenaredondo probioticsfunctionasimmunomodulatorsintheintestineinc57bl6malemiceexposedtoinhaleddieselexhaustparticlesonahighfatdiet
AT amieklund probioticsfunctionasimmunomodulatorsintheintestineinc57bl6malemiceexposedtoinhaleddieselexhaustparticlesonahighfatdiet