Gut microbiota-palmitoleic acid-interleukin-5 axis orchestrates benzene-induced hematopoietic toxicity

ABSTRACTDue to the annual increase in its production and consumption in occupational environments, the adverse blood outcomes caused by benzene are of concern. However, the mechanism of benzene-induced hematopoietic damage remains elusive. Here, we report that benzene exposure causes hematopoietic d...

Full description

Bibliographic Details
Main Authors: Lei Zhang, Ziyan Liu, Wei Zhang, Jingyu Wang, Huiwen Kang, Jiaru Jing, Lin Han, Ai Gao
Format: Article
Language:English
Published: Taylor & Francis Group 2024-12-01
Series:Gut Microbes
Subjects:
Online Access:https://www.tandfonline.com/doi/10.1080/19490976.2024.2323227
_version_ 1827330680826101760
author Lei Zhang
Ziyan Liu
Wei Zhang
Jingyu Wang
Huiwen Kang
Jiaru Jing
Lin Han
Ai Gao
author_facet Lei Zhang
Ziyan Liu
Wei Zhang
Jingyu Wang
Huiwen Kang
Jiaru Jing
Lin Han
Ai Gao
author_sort Lei Zhang
collection DOAJ
description ABSTRACTDue to the annual increase in its production and consumption in occupational environments, the adverse blood outcomes caused by benzene are of concern. However, the mechanism of benzene-induced hematopoietic damage remains elusive. Here, we report that benzene exposure causes hematopoietic damage in a dose-dependent manner and is associated with disturbances in gut microbiota-long chain fatty acids (LCFAs)-inflammation axis. C57BL/6J mice exposed to benzene for 45 days were found to have a significant reduction in whole blood cells and the suppression of hematopoiesis, an increase in Bacteroides acidifaciens and a decrease in Lactobacillus murinus. Recipient mice transplanted with fecal microbiota from benzene-exposed mice showed potential for hematopoietic disruption, LCFAs, and interleukin-5 (IL-5) elevation. Abnormally elevated plasma LCFAs, especially palmitoleic acid (POA) exacerbated benzene-induced immune-inflammation and hematopoietic damage via carnitine palmitoyltransferase 2 (CPT2)-mediated disorder of fatty acid oxidation. Notably, oral administration of probiotics protects the mice against benzene-induced hematopoietic toxicity. In summary, our data reveal that the gut microbiota-POA-IL-5 axis is engaged in benzene-induced hematopoietic damage. Probiotics might be a promising candidate to prevent hematopoietic abnormalities from benzene exposure.
first_indexed 2024-03-07T16:17:59Z
format Article
id doaj.art-8900428ab64b4a9fbc0476055dc83349
institution Directory Open Access Journal
issn 1949-0976
1949-0984
language English
last_indexed 2024-03-07T16:17:59Z
publishDate 2024-12-01
publisher Taylor & Francis Group
record_format Article
series Gut Microbes
spelling doaj.art-8900428ab64b4a9fbc0476055dc833492024-03-04T10:25:14ZengTaylor & Francis GroupGut Microbes1949-09761949-09842024-12-0116110.1080/19490976.2024.2323227Gut microbiota-palmitoleic acid-interleukin-5 axis orchestrates benzene-induced hematopoietic toxicityLei Zhang0Ziyan Liu1Wei Zhang2Jingyu Wang3Huiwen Kang4Jiaru Jing5Lin Han6Ai Gao7Department of Occupational Health and Environmental Health, School of Public Health, Capital Medical University, Beijing, ChinaDepartment of Occupational Health and Environmental Health, School of Public Health, Capital Medical University, Beijing, ChinaDepartment of Occupational Health and Environmental Health, School of Public Health, Capital Medical University, Beijing, ChinaDepartment of Occupational Health and Environmental Health, School of Public Health, Capital Medical University, Beijing, ChinaDepartment of Occupational Health and Environmental Health, School of Public Health, Capital Medical University, Beijing, ChinaDepartment of Occupational Health and Environmental Health, School of Public Health, Capital Medical University, Beijing, ChinaDepartment of Occupational Health and Environmental Health, School of Public Health, Capital Medical University, Beijing, ChinaDepartment of Occupational Health and Environmental Health, School of Public Health, Capital Medical University, Beijing, ChinaABSTRACTDue to the annual increase in its production and consumption in occupational environments, the adverse blood outcomes caused by benzene are of concern. However, the mechanism of benzene-induced hematopoietic damage remains elusive. Here, we report that benzene exposure causes hematopoietic damage in a dose-dependent manner and is associated with disturbances in gut microbiota-long chain fatty acids (LCFAs)-inflammation axis. C57BL/6J mice exposed to benzene for 45 days were found to have a significant reduction in whole blood cells and the suppression of hematopoiesis, an increase in Bacteroides acidifaciens and a decrease in Lactobacillus murinus. Recipient mice transplanted with fecal microbiota from benzene-exposed mice showed potential for hematopoietic disruption, LCFAs, and interleukin-5 (IL-5) elevation. Abnormally elevated plasma LCFAs, especially palmitoleic acid (POA) exacerbated benzene-induced immune-inflammation and hematopoietic damage via carnitine palmitoyltransferase 2 (CPT2)-mediated disorder of fatty acid oxidation. Notably, oral administration of probiotics protects the mice against benzene-induced hematopoietic toxicity. In summary, our data reveal that the gut microbiota-POA-IL-5 axis is engaged in benzene-induced hematopoietic damage. Probiotics might be a promising candidate to prevent hematopoietic abnormalities from benzene exposure.https://www.tandfonline.com/doi/10.1080/19490976.2024.2323227Benzenehematotoxicitygut microbiotalong-chain fatty acidsprobiotics
spellingShingle Lei Zhang
Ziyan Liu
Wei Zhang
Jingyu Wang
Huiwen Kang
Jiaru Jing
Lin Han
Ai Gao
Gut microbiota-palmitoleic acid-interleukin-5 axis orchestrates benzene-induced hematopoietic toxicity
Gut Microbes
Benzene
hematotoxicity
gut microbiota
long-chain fatty acids
probiotics
title Gut microbiota-palmitoleic acid-interleukin-5 axis orchestrates benzene-induced hematopoietic toxicity
title_full Gut microbiota-palmitoleic acid-interleukin-5 axis orchestrates benzene-induced hematopoietic toxicity
title_fullStr Gut microbiota-palmitoleic acid-interleukin-5 axis orchestrates benzene-induced hematopoietic toxicity
title_full_unstemmed Gut microbiota-palmitoleic acid-interleukin-5 axis orchestrates benzene-induced hematopoietic toxicity
title_short Gut microbiota-palmitoleic acid-interleukin-5 axis orchestrates benzene-induced hematopoietic toxicity
title_sort gut microbiota palmitoleic acid interleukin 5 axis orchestrates benzene induced hematopoietic toxicity
topic Benzene
hematotoxicity
gut microbiota
long-chain fatty acids
probiotics
url https://www.tandfonline.com/doi/10.1080/19490976.2024.2323227
work_keys_str_mv AT leizhang gutmicrobiotapalmitoleicacidinterleukin5axisorchestratesbenzeneinducedhematopoietictoxicity
AT ziyanliu gutmicrobiotapalmitoleicacidinterleukin5axisorchestratesbenzeneinducedhematopoietictoxicity
AT weizhang gutmicrobiotapalmitoleicacidinterleukin5axisorchestratesbenzeneinducedhematopoietictoxicity
AT jingyuwang gutmicrobiotapalmitoleicacidinterleukin5axisorchestratesbenzeneinducedhematopoietictoxicity
AT huiwenkang gutmicrobiotapalmitoleicacidinterleukin5axisorchestratesbenzeneinducedhematopoietictoxicity
AT jiarujing gutmicrobiotapalmitoleicacidinterleukin5axisorchestratesbenzeneinducedhematopoietictoxicity
AT linhan gutmicrobiotapalmitoleicacidinterleukin5axisorchestratesbenzeneinducedhematopoietictoxicity
AT aigao gutmicrobiotapalmitoleicacidinterleukin5axisorchestratesbenzeneinducedhematopoietictoxicity