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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Main Authors: Lei Zhang, Jiaru Jing, Lin Han, Jingyu Wang, Wei Zhang, Ziyan Liu, Ai Gao
Format: Article
Language:English
Published: Elsevier 2021-12-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S014765132101068X
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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
collection DOAJ
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.
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spelling doaj.art-39ff9da26fb041ff94660a3e5d3497602022-12-21T23:38:38ZengElsevierEcotoxicology and Environmental Safety0147-65132021-12-01228112956Characterization of gut microbiota, metabolism and cytokines in benzene-induced hematopoietic damageLei Zhang0Jiaru Jing1Lin Han2Jingyu Wang3Wei Zhang4Ziyan Liu5Ai Gao6Department of Occupational Health and Environmental Health, School of Public Health, Capital Medical University, Beijing 100069, ChinaDepartment of Occupational Health and Environmental Health, School of Public Health, Capital Medical University, Beijing 100069, ChinaDepartment of Occupational Health and Environmental Health, School of Public Health, Capital Medical University, Beijing 100069, ChinaDepartment of Occupational Health and Environmental Health, School of Public Health, Capital Medical University, Beijing 100069, ChinaDepartment of Occupational Health and Environmental Health, School of Public Health, Capital Medical University, Beijing 100069, ChinaDepartment of Occupational Health and Environmental Health, School of Public Health, Capital Medical University, Beijing 100069, ChinaDepartment of Occupational Health and Environmental Health, School of Public Health, Capital Medical University, Beijing 100069, China; Beijing Key Laboratory of Environmental Toxicology, Capital Medical University, Beijing 100069, China; Correspondence to: Department of Occupational Health and Environmental Health, School of Public Health, Capital Medical University, 10 Xitoutiao, You An Men, Beijing 100069, China.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.http://www.sciencedirect.com/science/article/pii/S014765132101068XBenzeneGut microbiotaMetabolismCytokineHematopoietic toxicity
spellingShingle 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
Ecotoxicology and Environmental Safety
Benzene
Gut microbiota
Metabolism
Cytokine
Hematopoietic toxicity
title 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_short 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
topic Benzene
Gut microbiota
Metabolism
Cytokine
Hematopoietic toxicity
url http://www.sciencedirect.com/science/article/pii/S014765132101068X
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