publication . Article . 2016

Histone Deacetylase Inhibitors Trichostatin A and MCP30 Relieve Benzene-Induced Hematotoxicity via Restoring Topoisomerase IIα

Jingjing Chen; Zhouyi Zheng; Yi Chen; Jiaqi Li; Shanhu Qian; Yifen Shi; Lan Sun; Yixiang Han; Shenghui Zhang; Kang Yu;
Open Access English
  • Published: 08 Apr 2016 Journal: PLoS ONE, volume 11, issue 4 (eissn: 1932-6203, Copyright policy)
  • Publisher: Public Library of Science
Abstract
Dysfunction of histone acetylation inhibits topoisomerase IIα (Topo IIα), which is implicated in benzene-induced hematotoxicity in patients with chronic benzene exposure. Whether histone deacetylase (HDAC) inhibitors can relieve benzene-induced hematotoxicity remains unclear. Here we showed that hydroquinone, a main metabolite of benzene, increased the HDAC activity, decreased the Topo IIα expression and induced apoptosis in human bone marrow mononuclear cells in vitro, and treatment with two HDAC inhibitors, namely trichostatin A (TSA) or a mixture of ribosome-inactivating proteins MCP30, almost completely reversed these effects. We further established a benzen...
Subjects
free text keywords: Research Article, Physical Sciences, Chemistry, Chemical Compounds, Organic Compounds, Benzene, Organic Chemistry, Biology and Life Sciences, Cell Biology, Cellular Types, Animal Cells, Bone Marrow Cells, Biochemistry, Proteins, DNA-binding proteins, Histones, Chemical Reactions, Acetylation, Post-Translational Modification, Research and Analysis Methods, Model Organisms, Animal Models, Mouse Models, Cell Processes, Cell Death, Apoptosis, Medicine and Health Sciences, Diagnostic Medicine, Signs and Symptoms, Poisoning, Pathology and Laboratory Medicine, Histone Acetylation, Chromosome Biology, Chromatin, Chromatin Modification, Histone Modification, Genetics, Epigenetics, Gene Expression, Medicine, R, Science, Q, General Biochemistry, Genetics and Molecular Biology, General Agricultural and Biological Sciences, General Medicine, Topoisomerase, biology.protein, biology, Histone H4, Trichostatin A, medicine.drug, Cancer research, Histone deacetylase, Histone H3, Histone
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40 references, page 1 of 3

1 Aksoy M. Hematotoxicity and carcinogenicity of benzene. Environ Health Perspect. 1989; 82: 193–197. 2676498 [OpenAIRE] [PubMed]

2 Snyder R, Witz G, Goldstein BD. The toxicology of benzene. Environ Health Perspect. 1993; 100: 293–306. 8354177 [OpenAIRE] [PubMed]

3 Linet MS, Yin SN, Gilbert ES, Dores GM, Hayes RB, Vermeulen R, et al A retrospective cohort study of cause-specific mortality and incidence of hematopoietic malignancies in Chinese benzene-exposed workers. Int J Cancer. 2015; 137: 2184–2197. 10.1002/ijc.29591 25944549 [OpenAIRE] [PubMed] [DOI]

4 Chow PW, Abdul Hamid Z, Chan KM, Inayat-Hussain SH, Rajab NF. Lineage-related cytotoxicity and clonogenic profile of 1,4-benzoquinone-exposed hematopoietic stem and progenitor cells. Toxicol Appl Pharmacol. 2015; 284: 8–15. 10.1016/j.taap.2015.01.016 25645895 [OpenAIRE] [PubMed] [DOI]

5 Faiola B, Fuller ES, Wong VA, Pluta L, Abernethy DJ, Rose J, et al Exposure of hematopoietic stem cells to benzene or 1,4-benzoquinone induces gender-specific gene expression. Stem Cells. 2004; 22: 750–758. 15342939 [PubMed]

6 Wang L, He X, Bi Y, Ma Q. Stem cell and benzene-induced malignancy and hematotoxicity. Chem Res Toxicol. 2012; 25: 1303–1315. 10.1021/tx3001169 22540379 [OpenAIRE] [PubMed] [DOI]

7 Pogorelcnik B, Perdih A, Solmajer T. Recent developments of DNA poisons—human DNA topoisomerase IIalpha inhibitors—as anticancer agents. Curr Pharm Des. 2013; 19: 2474–2488. 23363399 [OpenAIRE] [PubMed]

8 Baker RK, Kurz EU, Pyatt DW, Irons RD, Kroll DJ. Benzene metabolites antagonize etoposide-stabilized cleavable complexes of DNA topoisomerase IIalpha. Blood. 2001; 98: 830–833. 11468185 [PubMed]

9 Hirabayashi Y, Yoon BI, Li GX, Kanno J, Inoue T. Mechanism of benzene-induced hematotoxicity and leukemogenicity: current review with implication of microarray analyses. Toxicol Pathol. 2004; 32 Suppl 2: 12–16. 15503659 [PubMed]

10 Ji Z, Zhang L, Peng V, Ren X, McHale CM, Smith MT. A comparison of the cytogenetic alte rations and global DNA hypomethylation induced by the benzene metabolite, hydroquinone, with those induced by melphalan and etoposide. Leukemia. 2010; 24: 986–991. 10.1038/leu.2010.43 20339439 [OpenAIRE] [PubMed] [DOI]

11 Fung J, Hoffmann MJ, Kim DD, Snyder R. Inhibition of topoisomerase II in 32D.3(G) cells by hydroquinone is associated with cell death. J Appl Toxicol. 2004; 24: 183–188. 15211611 [PubMed]

12 Yu K, Shi YF, Yang KY, Zhuang Y, Zhu RH, Xu X, et al Decreased topoisomerase IIalpha expression and altered histone and regulatory factors of topoisomerase IIalpha promoter in patients with chronic benzene poisoning. Toxicol Lett. 2011; 203: 111–117. 10.1016/j.toxlet.2011.02.020 21382456 [OpenAIRE] [PubMed] [DOI]

13 Ruthenburg AJ, Li H, Patel DJ, Allis CD. Multivalent engagement of chromatin modifications by linked binding modules. Nat Rev Mol Cell Biol. 2007; 8: 983–994. 18037899 [OpenAIRE] [PubMed]

14 Urnov FD, Wolffe AP. Chromatin remodeling and transcriptional activation: the cast (in order of appearance). Oncogene. 2001; 20: 2991–3006. 11420714 [OpenAIRE] [PubMed]

15 Backs J, Olson EN. Control of cardiac growth by histone acetylation/deacetylation. Circ Res. 2006; 98: 15–24. 16397154 [OpenAIRE] [PubMed]

40 references, page 1 of 3
Related research
Abstract
Dysfunction of histone acetylation inhibits topoisomerase IIα (Topo IIα), which is implicated in benzene-induced hematotoxicity in patients with chronic benzene exposure. Whether histone deacetylase (HDAC) inhibitors can relieve benzene-induced hematotoxicity remains unclear. Here we showed that hydroquinone, a main metabolite of benzene, increased the HDAC activity, decreased the Topo IIα expression and induced apoptosis in human bone marrow mononuclear cells in vitro, and treatment with two HDAC inhibitors, namely trichostatin A (TSA) or a mixture of ribosome-inactivating proteins MCP30, almost completely reversed these effects. We further established a benzen...
Subjects
free text keywords: Research Article, Physical Sciences, Chemistry, Chemical Compounds, Organic Compounds, Benzene, Organic Chemistry, Biology and Life Sciences, Cell Biology, Cellular Types, Animal Cells, Bone Marrow Cells, Biochemistry, Proteins, DNA-binding proteins, Histones, Chemical Reactions, Acetylation, Post-Translational Modification, Research and Analysis Methods, Model Organisms, Animal Models, Mouse Models, Cell Processes, Cell Death, Apoptosis, Medicine and Health Sciences, Diagnostic Medicine, Signs and Symptoms, Poisoning, Pathology and Laboratory Medicine, Histone Acetylation, Chromosome Biology, Chromatin, Chromatin Modification, Histone Modification, Genetics, Epigenetics, Gene Expression, Medicine, R, Science, Q, General Biochemistry, Genetics and Molecular Biology, General Agricultural and Biological Sciences, General Medicine, Topoisomerase, biology.protein, biology, Histone H4, Trichostatin A, medicine.drug, Cancer research, Histone deacetylase, Histone H3, Histone
Related Organizations
Download fromView all 3 versions
PLoS ONE
Article . 2016
PLoS ONE
Article . 2016
Provider: Crossref
PLoS ONE
Article
Provider: UnpayWall
40 references, page 1 of 3

1 Aksoy M. Hematotoxicity and carcinogenicity of benzene. Environ Health Perspect. 1989; 82: 193–197. 2676498 [OpenAIRE] [PubMed]

2 Snyder R, Witz G, Goldstein BD. The toxicology of benzene. Environ Health Perspect. 1993; 100: 293–306. 8354177 [OpenAIRE] [PubMed]

3 Linet MS, Yin SN, Gilbert ES, Dores GM, Hayes RB, Vermeulen R, et al A retrospective cohort study of cause-specific mortality and incidence of hematopoietic malignancies in Chinese benzene-exposed workers. Int J Cancer. 2015; 137: 2184–2197. 10.1002/ijc.29591 25944549 [OpenAIRE] [PubMed] [DOI]

4 Chow PW, Abdul Hamid Z, Chan KM, Inayat-Hussain SH, Rajab NF. Lineage-related cytotoxicity and clonogenic profile of 1,4-benzoquinone-exposed hematopoietic stem and progenitor cells. Toxicol Appl Pharmacol. 2015; 284: 8–15. 10.1016/j.taap.2015.01.016 25645895 [OpenAIRE] [PubMed] [DOI]

5 Faiola B, Fuller ES, Wong VA, Pluta L, Abernethy DJ, Rose J, et al Exposure of hematopoietic stem cells to benzene or 1,4-benzoquinone induces gender-specific gene expression. Stem Cells. 2004; 22: 750–758. 15342939 [PubMed]

6 Wang L, He X, Bi Y, Ma Q. Stem cell and benzene-induced malignancy and hematotoxicity. Chem Res Toxicol. 2012; 25: 1303–1315. 10.1021/tx3001169 22540379 [OpenAIRE] [PubMed] [DOI]

7 Pogorelcnik B, Perdih A, Solmajer T. Recent developments of DNA poisons—human DNA topoisomerase IIalpha inhibitors—as anticancer agents. Curr Pharm Des. 2013; 19: 2474–2488. 23363399 [OpenAIRE] [PubMed]

8 Baker RK, Kurz EU, Pyatt DW, Irons RD, Kroll DJ. Benzene metabolites antagonize etoposide-stabilized cleavable complexes of DNA topoisomerase IIalpha. Blood. 2001; 98: 830–833. 11468185 [PubMed]

9 Hirabayashi Y, Yoon BI, Li GX, Kanno J, Inoue T. Mechanism of benzene-induced hematotoxicity and leukemogenicity: current review with implication of microarray analyses. Toxicol Pathol. 2004; 32 Suppl 2: 12–16. 15503659 [PubMed]

10 Ji Z, Zhang L, Peng V, Ren X, McHale CM, Smith MT. A comparison of the cytogenetic alte rations and global DNA hypomethylation induced by the benzene metabolite, hydroquinone, with those induced by melphalan and etoposide. Leukemia. 2010; 24: 986–991. 10.1038/leu.2010.43 20339439 [OpenAIRE] [PubMed] [DOI]

11 Fung J, Hoffmann MJ, Kim DD, Snyder R. Inhibition of topoisomerase II in 32D.3(G) cells by hydroquinone is associated with cell death. J Appl Toxicol. 2004; 24: 183–188. 15211611 [PubMed]

12 Yu K, Shi YF, Yang KY, Zhuang Y, Zhu RH, Xu X, et al Decreased topoisomerase IIalpha expression and altered histone and regulatory factors of topoisomerase IIalpha promoter in patients with chronic benzene poisoning. Toxicol Lett. 2011; 203: 111–117. 10.1016/j.toxlet.2011.02.020 21382456 [OpenAIRE] [PubMed] [DOI]

13 Ruthenburg AJ, Li H, Patel DJ, Allis CD. Multivalent engagement of chromatin modifications by linked binding modules. Nat Rev Mol Cell Biol. 2007; 8: 983–994. 18037899 [OpenAIRE] [PubMed]

14 Urnov FD, Wolffe AP. Chromatin remodeling and transcriptional activation: the cast (in order of appearance). Oncogene. 2001; 20: 2991–3006. 11420714 [OpenAIRE] [PubMed]

15 Backs J, Olson EN. Control of cardiac growth by histone acetylation/deacetylation. Circ Res. 2006; 98: 15–24. 16397154 [OpenAIRE] [PubMed]

40 references, page 1 of 3
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