Characterization of gut microbiota, metabolism and cytokines in benzene-induced hematopoietic damage

Benzene exposure leads to hematopoietic dysfunction and is characterized clinically by a decrease in blood cells, but the underlying mechanisms remain elusive. Disturbed gut microbiota may induce host metabolic, immune disorders and the onset of disease. However, the characterization of gut microbio...

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Autores principales:	Lei Zhang, Jiaru Jing, Lin Han, Jingyu Wang, Wei Zhang, Ziyan Liu, Ai Gao
Formato:	article
Lenguaje:	EN
Publicado:	Elsevier 2021
Materias:	Benzene Gut microbiota Metabolism Cytokine Hematopoietic toxicity Environmental pollution TD172-193.5 Environmental sciences GE1-350
Acceso en línea:	https://doaj.org/article/39ff9da26fb041ff94660a3e5d349760
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spelling	oai:doaj.org-article:39ff9da26fb041ff94660a3e5d3497602021-11-14T04:28:19ZCharacterization of gut microbiota, metabolism and cytokines in benzene-induced hematopoietic damage0147-651310.1016/j.ecoenv.2021.112956https://doaj.org/article/39ff9da26fb041ff94660a3e5d3497602021-12-01T00:00:00Zhttp://www.sciencedirect.com/science/article/pii/S014765132101068Xhttps://doaj.org/toc/0147-6513Benzene exposure leads to hematopoietic dysfunction and is characterized clinically by a decrease in blood cells, but the underlying mechanisms remain elusive. Disturbed gut microbiota may induce host metabolic, immune disorders and the onset of disease. However, the characterization of gut microbiota, metabolism, cytokines and their association with benzene-induced hematopoietic toxicity lacks systematic evidence. Here, the microbiomics, metabolomics and cytokine network were applied to find out the critical characteristics of gut microbiota, metabolism and cytokines in mice involved in the benzene-induced hematopoietic toxicity. We found that the decline in hematopoietic stem cells was earlier than the hematological changes in the 5 mg/kg and 25 mg/kg benzene exposure groups. While 125 mg/kg benzene exposure resulted in a significant decline in whole blood cells. High-throughput sequencing results showed that benzene exposure disrupted homeostasis of gut microbiota, metabolism and cytokine in mice. 6 bacteria, 12 plasma metabolites and 6 cytokines were associated with benzene-induced hematopoietic damage. Notably, IL-5 was significantly increased in benzene exposure group in a dose-dependent manner, and a significant negative correlation was found between IL-5 and hematopoietic damage. We further found that increased Family_XIII_AD3011_group at the genus level and decreased Anaerotruncus_sp at the species level in benzene-exposed group were strongly associated with hematopoietic toxicity and IL-5. Furthermore, the abundance of Family_XIII_AD3011_group and Anaerotruncus_sp were negatively correlated with Adipic acid and 4-Hydroxyproline, respectively. Our findings indicated that altered flora structure of gut microbiota affects the metabolic phenotype which acts as messengers for the gut microbes, affecting host inflammation. This preliminary study provides new insight into the potential mechanisms of benzene-induced hematopoietic toxicity, further exploration by functional studies is required in the future.Lei ZhangJiaru JingLin HanJingyu WangWei ZhangZiyan LiuAi GaoElsevierarticleBenzeneGut microbiotaMetabolismCytokineHematopoietic toxicityEnvironmental pollutionTD172-193.5Environmental sciencesGE1-350ENEcotoxicology and Environmental Safety, Vol 228, Iss , Pp 112956- (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Benzene Gut microbiota Metabolism Cytokine Hematopoietic toxicity Environmental pollution TD172-193.5 Environmental sciences GE1-350
spellingShingle	Benzene Gut microbiota Metabolism Cytokine Hematopoietic toxicity Environmental pollution TD172-193.5 Environmental sciences GE1-350 Lei Zhang Jiaru Jing Lin Han Jingyu Wang Wei Zhang Ziyan Liu Ai Gao Characterization of gut microbiota, metabolism and cytokines in benzene-induced hematopoietic damage
description	Benzene exposure leads to hematopoietic dysfunction and is characterized clinically by a decrease in blood cells, but the underlying mechanisms remain elusive. Disturbed gut microbiota may induce host metabolic, immune disorders and the onset of disease. However, the characterization of gut microbiota, metabolism, cytokines and their association with benzene-induced hematopoietic toxicity lacks systematic evidence. Here, the microbiomics, metabolomics and cytokine network were applied to find out the critical characteristics of gut microbiota, metabolism and cytokines in mice involved in the benzene-induced hematopoietic toxicity. We found that the decline in hematopoietic stem cells was earlier than the hematological changes in the 5 mg/kg and 25 mg/kg benzene exposure groups. While 125 mg/kg benzene exposure resulted in a significant decline in whole blood cells. High-throughput sequencing results showed that benzene exposure disrupted homeostasis of gut microbiota, metabolism and cytokine in mice. 6 bacteria, 12 plasma metabolites and 6 cytokines were associated with benzene-induced hematopoietic damage. Notably, IL-5 was significantly increased in benzene exposure group in a dose-dependent manner, and a significant negative correlation was found between IL-5 and hematopoietic damage. We further found that increased Family_XIII_AD3011_group at the genus level and decreased Anaerotruncus_sp at the species level in benzene-exposed group were strongly associated with hematopoietic toxicity and IL-5. Furthermore, the abundance of Family_XIII_AD3011_group and Anaerotruncus_sp were negatively correlated with Adipic acid and 4-Hydroxyproline, respectively. Our findings indicated that altered flora structure of gut microbiota affects the metabolic phenotype which acts as messengers for the gut microbes, affecting host inflammation. This preliminary study provides new insight into the potential mechanisms of benzene-induced hematopoietic toxicity, further exploration by functional studies is required in the future.
format	article
author	Lei Zhang Jiaru Jing Lin Han Jingyu Wang Wei Zhang Ziyan Liu Ai Gao
author_facet	Lei Zhang Jiaru Jing Lin Han Jingyu Wang Wei Zhang Ziyan Liu Ai Gao
author_sort	Lei Zhang
title	Characterization of gut microbiota, metabolism and cytokines in benzene-induced hematopoietic damage
title_short	Characterization of gut microbiota, metabolism and cytokines in benzene-induced hematopoietic damage
title_full	Characterization of gut microbiota, metabolism and cytokines in benzene-induced hematopoietic damage
title_fullStr	Characterization of gut microbiota, metabolism and cytokines in benzene-induced hematopoietic damage
title_full_unstemmed	Characterization of gut microbiota, metabolism and cytokines in benzene-induced hematopoietic damage
title_sort	characterization of gut microbiota, metabolism and cytokines in benzene-induced hematopoietic damage
publisher	Elsevier
publishDate	2021
url	https://doaj.org/article/39ff9da26fb041ff94660a3e5d349760
work_keys_str_mv	AT leizhang characterizationofgutmicrobiotametabolismandcytokinesinbenzeneinducedhematopoieticdamage AT jiarujing characterizationofgutmicrobiotametabolismandcytokinesinbenzeneinducedhematopoieticdamage AT linhan characterizationofgutmicrobiotametabolismandcytokinesinbenzeneinducedhematopoieticdamage AT jingyuwang characterizationofgutmicrobiotametabolismandcytokinesinbenzeneinducedhematopoieticdamage AT weizhang characterizationofgutmicrobiotametabolismandcytokinesinbenzeneinducedhematopoieticdamage AT ziyanliu characterizationofgutmicrobiotametabolismandcytokinesinbenzeneinducedhematopoieticdamage AT aigao characterizationofgutmicrobiotametabolismandcytokinesinbenzeneinducedhematopoieticdamage
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Characterization of gut microbiota, metabolism and cytokines in benzene-induced hematopoietic damage

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