https://orcid.org/0000-0002-0764-4656
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ABSTRACT
Due 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.
Acknowledgments
This study was funded by the National Natural Science Foundation of China (82073520, 81773397), the Beijing Natural Science Program and Scientific Research Key Program of Beijing Municipal Commission of Education (KZ201810025032).
Disclosure statement
No potential conflict of interest was reported by the author(s).
Abbreviations
| ALL | = | Acute lymphoblastic leukemia |
| AB-PAS | = | Alcian Blue-Periodic Acid Schiff |
| BM | = | Bone marrow |
| CPT2 | = | Carnitine palmitoyltransferase 2 |
| DHA | = | Docosahexanoic acid |
| FAO | = | Fatty acid oxidation |
| FMT | = | Fecal microbiota transplantation |
| HSC | = | Hematopoietic stem cell |
| HGB | = | Hemoglobin |
| HA | = | 10Z-Heptadecenoic acid |
| H&E | = | Hematoxylin and eosin |
| IL-5 | = | Interleukin-5 |
| LCFAs | = | Long chain fatty acids |
| LSK | = | Lin/Scal-1/c-Kit cells |
| LT-HSCs | = | Long-term hematopoietic stem cells |
| LDA | = | Linear discriminant analysis |
| MPPs | = | Multipotent hematopoietic progenitor cells |
| MOA | = | Myristoleic acid |
| MA | = | Myristic acid |
| OA | = | Oleic acid |
| POA | = | Palmitoleic acid |
| PLT | = | Platelet |
| RBC | = | Red blood cells |
| ST-HSCs | = | Short-term HSCs |
| UPLC-MS/MS | = | Ultra-performance liquid chromatography coupled to a tandem mass spectrometry |
| WBC | = | White blood cells |
Author contributions
Lei Zhang: Study concept and design, Performed experiments, Acquisition of data, Analysis and Interpretation of data, Statistical analysis and Drafting of the manuscript and review; Ziyan Liu, Wei Zhang, Jingyu Wang, Huiwen Kang, Jiaru Jing, Lin Han: Performed experiments and Acquisition of data; Ai Gao: Study concept and design, Foundation support and Study supervision.
Data availability statement
The microbial raw data reported in this paper have been deposited in the China National Center for Bioinformation (https://ngdc.cncb.ac.cn) and the accession numbers are PRJNA1068769.
Ethics statement
Before the implementation of the study, the animal (Approval no. AEEI-2020-168) and population (Approval no. 2017054) study protocols were reviewed and approved by the Ethics Committee of Capital Medical University, Beijing, China. In addition, all subjects had signed an informed consent form.
Supplementary material
Supplemental data for this article can be accessed online at https://doi.org/10.1080/19490976.2024.2323227