Linking Benzene, in Utero Carcinogenicity and Fetal Hematopoietic Stem Cell Niches: A Mechanistic Review
Abstract
:1. Introduction
2. Survey Methodology
3. Hematopoiesis
3.1. Hematopoiesis in the Adult Phase
3.2. Hematopoiesis in the Fetal Phase
4. Benzene Metabolism Linked to Fetal Toxicity via Maternal and Paternal Exposure
5. Mechanisms of Benzene-Induced in Utero Carcinogenicity Involving Hematopoietic Stem Cells and Multilineage Progenitors
5.1. Covalent Binding
5.2. Oxidative Stress
5.3. Error in DNA Repair Pathways
5.4. Chromosomal Aberration and Genetic Damage
5.5. Epigenetic Modification
5.5.1. DNA Methylation
5.5.2. Histone Modification and Chromatin Remodeling
5.6. Placenta-Mediated Toxicity
6. The Origin of Hematological Diseases from In-Utero Benzene Exposure
7. Conclusions and Future Remarks
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
ACGIH | The American Conference of Governmental Industrial Hygienists |
AGM | Aorta-gonad-mesonephros |
ALL | Acute lymphocytic leukemia |
AML | Acute myeloid leukemia |
ATSDR | Agency for Toxic Substances and Disease Registry |
BER | Base excision repair |
BFU-E | Burst-forming unit erythroid |
BM | Bone marrow |
BM-YSCs | Bone marrow hematopoietic stem cells |
BQ | Benzoquinone |
1,4-BQ | 1,4-benzoquinone |
C6H6 | Benzene |
CFU-E | Colony-forming unit erythroid |
CFU-G | Colony-forming unit granulocyte |
CFU-GM | Colony-forming unit granulocyte-macrophage |
CLL | Chronic lymphoid leukemia |
CLP | Common lymphoid progenitor |
CMP | Common myeloid progenitor |
CpGs | Cytosine-phosphate-guanine dinucleotides |
CYP | Cytochrome |
DCFDA | 2′,7′-dichlorodihydrofluorescein diacetate |
DDR | Damage response and repair |
DNA | Deoxyribonucleic acid |
DNA-PKcs | DNA-dependent protein kinase |
DNMT | DNA methyltransferases |
DR | Direct reversal |
DSB | Double-strand break |
E | Embryonic day |
Fe2+ | Iron |
GD | Gestation day |
GSH | Glutathione |
GST | Glutathione S-transferase |
H2O2 | Hydrogen peroxide |
H3K4me3 | Histone H3 trimethylated at lysine 4 |
HPCs | Hematopoietic progenitor cells |
Hb | Hemoglobin |
HQ | Hydroquinone |
HR | Homologous recombination |
HSCs | Hematopoietic stem cells |
HSPCs | Hematopoietic stem/progenitor cells |
8-OHdG | 8-hydroxy-2′-deoxyguanosine |
IARC | International Agency for Research on Cancer |
ICR | Imprinting control region |
i.p | Intraperitoneal |
LSC | Leukemic stem cell |
MDA | Malondialdehyde |
MAPK | Mitogen-activated protein kinases |
MDR | Multidrug resistance |
MDS | Myelodysplastic syndromes |
mEH | Microsomal epoxide hydrolase |
MMR | Mismatch repair |
MN | Micronuclei |
MNPCE | Micronucleated bone marrow polychromatic erythrocytes |
MPO | Myeloperoxidase |
mtDNA | Mitochondria DNA |
MSC | Mesenchymal stem cell |
MSPC | Human mesenchymal stem and progenitor cell |
NER | Nucleotide excision repair |
NF-κB | Nuclear factor kappa B |
NHEJ | Non-homologous end-joining |
NIOSH | National Institute of Occupational Safety and Health |
NK | Natural killer |
NQO1 | NAD(P)H:quinone oxidoreductase 1 |
O2•− | Anion radical |
o-BQ | o-BQ |
OH | Hydroxide |
OSHA | Occupational Safety and Health Administration |
p-BQ | p-benzoquinone |
ppm | Parts per million |
PC | Protein carbonyl |
PTMs | Post-translationally modified |
RNA | Ribonucleic acid |
RNS | Reactive nitrogen species |
ROS | Reactive oxygen species |
SCE | Sister chromatid exchange |
SQ•− | Semiquinone |
SOD | Superoxide dismutase |
SPF | Specific pathogen-free |
TNF-α | Tumor Necrosis Factor alpha |
Topo II | Topoisomerase II |
TWA | Time-weighted average |
UGTs | Uridine 5′-diphospho-glucuronosyltransferase |
µM | Micromole |
YS-HSCs | Yolk sac hematopoietic stem cells |
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1. Is electrophile or can be metabolically activated to electrophiles. 2. Is genotoxic. 3. Alters DNA repair and causes genomic instability. 4. Induces epigenetic alterations. 5. Induces oxidative stress. 6. Induces chronic inflammation. 7. Is immunosuppressive. 8. Modulates receptor-mediated effects. 9. Causes immortalization. 10. Alters cell proliferation, cell death or nutrient supply. |
No | Category | Description |
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1 | Journal Databases |
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2 | Inclusion Criteria |
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3 | Exclusion Criteria | None |
4 | Types of articles |
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Exposure Time Windows | Periconception (Pre- and Around Conception) | Intrauterine (Gestational) | Postnatal |
Maternal |
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Paternal |
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Benzene or Metabolites | Study Design | Dose or Concentration | Experimental Model | Toxicity Effects | References |
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1,4-BQ | In vitro | 0, 1.25, 2.5, 5 μM | ICR mice | Induce concentration-dependent cytotoxicity & apoptosis in BM cells, ↓total counts of Sca-1+, CD11b+, Gr-1+ & CD45+ cells, ↓clonogenicity in 1,4-BQ-treated cells | [12] |
1,4-BQ | In vitro | 0, 5, 7, 12 μM | ICR mice | ↓colony-forming capacity of the myeloid progenitor at 1.25 & 2.5 μM, ↑expression HoxB4 level at all concentrations & ↑Bmi-1 expression level at 5 μM, ↑GATA3 expression level at 2.5 µM | [14] |
Benzene | Epidemiology | – | Pregnant women | ↑risk of childhood ALL | [18] |
BQ | In vitro | 6.25, 9.375 12.5, 15.625 μM | Murine CD-1 | ↓c-kit+Lin-Sca-1-Il7rα-cell population in BQ-treated, ↓Topo IIα activity in concentration-dependent, ↑γH2AX levels at 12.5 µM BQ exposure | [66] |
Benzene | In vivo (i.p.) | 200, 400 mg/kg (GD8, 10, 12, 14, 16) | Pregnant C57Bl/6N mice | ↑numbers of CFU-E, BFU-E, CFU-GM & CFU-G colonies at 200 mg/kg, ↓numbers of CFU-M colonies in hematopoietic tissue of GD16 C57Bl/6N fetuses at 200 mg/kg, ↑numbers of CFU-E & CFU-G colonies at 400 mg/kg benzene on GD8, 10, 12, 14, ↑ROS production in fetal liver | [67] |
Benzene | In vivo (i.p.) | 50, 100, 200, 400 mg/kg | B6C3F1 mice | ↑nitration of tyrosine residues in bone marrow proteins from 50 to 200 mg/kg | [90] |
Benzene | In vivo (inhalation) | 10 ppm (GD6–15) | Pregnant Swiss Webster mice | ↑alteration in cell numbers for progenitor & hematopoietic precursor | [91] |
Benzene | In vivo (inhalation) | 5, 10, 20 ppm (GD6–15) | Pregnant Swiss Webster mice | ↓numbers of circulating erythroid precursor cells, ↑numbers of hepatic hematopoietic blast cells & granulopoietic precursor cells, ↑granulopoiesis. | [92] |
Radio- labelled benzene | In vivo (inhalation) | – | Pregnant C57BL mice | Radioactivity detected in the embryonic hematopoietic tissue | [93] |
Benzene | Epidemiology | – | Pregnant women | Benzene detected in fetal umbilical cord blood at the same or greater level than in the mother’s blood, ↑benzene accumulation in the fetal-placenta unit | [94] |
Benzene | In vivo (oral) | 50, 100, 200, 400 mg/kg | Fischer (F344) rats | ↑BQ adducts of Hb and bone-marrow proteins with dose-dependent manner | [95] |
Benzene | Epidemiology | ≤31, >31 ppm | Workers | ↑levels of BO & HQ adducts of Hb and albumin | [96] |
1,4-BQ | In vitro | 0, 1.25, 2.5, 5, 7, 12 μM | ICR mice | ↓GSH level, ↓SOD activity, ↑MDA level, ↑PC level, ↑DNA damage in BM cells (↑DNA in tail % at 7 & 12 μM as well as ↑tail moment at 12 μM), ↑DNA damage in myeloid & pre-B lymphoid progenitors at 2.5 µM, ↑DNA damage in the erythroid progenitor at 5 µM 1,4-BQ, ↑in tail moment at 7 µM & 12 µM 1,4-BQ exposure for all progenitors | [4] |
Benzene | In vivo (i.p.) | 200 mg/kg (GD8, 10, 12, 14) | Pregnant CD mice | ↑oxidative stress in fetal tissue from embryos, ↑ROS sensitive fluorescent probe DCFDA, ↑expression of fetal Pim-1, ↑Pim-1 phosphorylation, ↑c-Myb, ↑phosphorylated p38-MAPK, ↓protein levels of Iҡßα | [97] |
HQ | In vitro | 0, 5, 10, 15, 20 μM | Human | ↑frequency of the specific chromosomal aberrations in CD34+ bone marrow cells | [98] |
Benzene | In vivo (i.p.) | 0, 109, 219, 437, 874 mg/kg (GD14) | Pregnant Swiss Webster mice | ↑frequency of MNPCE in fetal liver & fetal peripheral blood cells at 219 to 874 mg/kg, ↑frequency of MNPCE in maternal bone marrow cells at 437 & 874 mg/kg | [99] |
HQ & 1,4-BQ | In vitro | 5, 10, 25, 50 μM | L02 cell line | ↑global DNA methylation, ↓DNMT activity | [100] |
Benzene | In vivo (i.p.) | 155, 800 µg/kg | B6C3F1 mice | ↑protein adducts in bone marrow & liver | [101] |
Hydroquinone | In vitro | 0, 0.1, 1.0, 10.0 µM | Worker’s blood | ↑global H3K4me3 modification & hematotoxicity, ↓white blood cells count, ↓neutrophils count, ↓lymphocytes count, ↓monocytes count | [102] |
Muconic acid | Epidemiology | – | Pregnant women | ↑muconic acid in urine of pregnant women living close to natural-gas hydraulic fracturing sites | [103] |
Hydroquinone | In vitro | 0, 1.25, 2.5, 5.0 µM | SPF Kunming mice | ↓proliferation & differentiation as well as ↓colony formation of both YS-HSCs & BM-HSCs, ↑apoptosis of both YS-HSCs & BM-HSCs | [104] |
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Yusoff, N.A.; Abd Hamid, Z.; Budin, S.B.; Taib, I.S. Linking Benzene, in Utero Carcinogenicity and Fetal Hematopoietic Stem Cell Niches: A Mechanistic Review. Int. J. Mol. Sci. 2023, 24, 6335. https://doi.org/10.3390/ijms24076335
Yusoff NA, Abd Hamid Z, Budin SB, Taib IS. Linking Benzene, in Utero Carcinogenicity and Fetal Hematopoietic Stem Cell Niches: A Mechanistic Review. International Journal of Molecular Sciences. 2023; 24(7):6335. https://doi.org/10.3390/ijms24076335
Chicago/Turabian StyleYusoff, Nur Afizah, Zariyantey Abd Hamid, Siti Balkis Budin, and Izatus Shima Taib. 2023. "Linking Benzene, in Utero Carcinogenicity and Fetal Hematopoietic Stem Cell Niches: A Mechanistic Review" International Journal of Molecular Sciences 24, no. 7: 6335. https://doi.org/10.3390/ijms24076335
APA StyleYusoff, N. A., Abd Hamid, Z., Budin, S. B., & Taib, I. S. (2023). Linking Benzene, in Utero Carcinogenicity and Fetal Hematopoietic Stem Cell Niches: A Mechanistic Review. International Journal of Molecular Sciences, 24(7), 6335. https://doi.org/10.3390/ijms24076335