Impact of Benzene Metabolites on Differentiation of Bone Marrow Progenitor Cells

Overview

Journal Environ Health Perspect

Date 1996 Dec 1

PMID 9118900

Citations 6

Authors

R D Irons

W S Stillman

Affiliations

Soon will be listed here.

Abstract

Interleukin-3 (IL-3) and granulocyte/macrophage-colony-stimulating factor (GM-CSF) are responsible for maintaining survival and stimulating growth of early dormant hematopoietic progenitor cells (HPC). These cytokines exhibit extensive overlap, with GM-CSF supporting growth and differentiation of myeloid HPC. A characteristic shared by a diverse group of leukemogens is the ability to act synergistically with GM-CSF to increase clonogenic response. Previous studies have revealed that pretreatment of murine HPC with hydroquinone (HQ) but not phenol, catechol, or trans-trans-muconaldehyde results in a selective enhancement of GM-CSF but not IL-3-mediated clonogenic response. Pretreatment of murine bone marrow cells with these agents or their metabolites in vitro results in increased numbers of HPC dividing and forming colonies in response to GM-CSF but not IL-3. The present studies explored the molecular mechanisms associated with altered cytokine response in early HPC in murine bone marrow and extended our initial observations in murine bone marrow to human bone marrow cells. HQ pretreatment of murine HPC did not induce either an up- or a down-regulation of GM-CSF receptors or any change in receptor affinity. CD34+ cells, which represent between 1 and 5% of human bone marrow, contain virtually all clonogenic stem and HPC. Pretreatment of CD34+ cells (approximately 95% purity) with HQ also results in enhanced clonogenic response with GM-CSF but not IL-3. These findings suggest that an early step in chemical leukemogenesis may involve transient alterations in the regulation of cytokine response to GM-CSF.

Citing Articles

Chronic benzene exposure impairs the self-renewal capacity of HSPCs in C57BL/6 mice.

Zhang Y, Zhou J, Zhao J, Cheng X, Xing C Toxicol Res (Camb). 2025; 14(1):tfaf021.

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Cytokine network involvement in subjects exposed to benzene.

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Large-scale evaluation of candidate genes identifies associations between DNA repair and genomic maintenance and development of benzene hematotoxicity.

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References

De Meyts P, Roth J, Neville Jr D, Gavin 3rd J, Lesniak M . Insulin interactions with its receptors: experimental evidence for negative cooperativity. Biochem Biophys Res Commun. 1973; 55(1):154-61. DOI: 10.1016/s0006-291x(73)80072-5. View

Hoffman B, Liebermann D . Molecular controls of apoptosis: differentiation/growth arrest primary response genes, proto-oncogenes, and tumor suppressor genes as positive & negative modulators. Oncogene. 1994; 9(7):1807-12. View

Calvo J, Radicella J, Charreau E . Measurement of specific radioactivities in labelled hormones by self-displacement analysis. Biochem J. 1983; 212(2):259-64. PMC: 1152042. DOI: 10.1042/bj2120259. View

Dower S, Ozato K, Segal D . The interaction of monoclonal antibodies with MHC class I antigens on mouse spleen cells. I. Analysis of the mechanism of binding. J Immunol. 1984; 132(2):751-8. View

Walker F, Burgess A . Specific binding of radioiodinated granulocyte-macrophage colony-stimulating factor to hemopoietic cells. EMBO J. 1985; 4(4):933-9. PMC: 554282. DOI: 10.1002/j.1460-2075.1985.tb03721.x. View

Young K . Myeloproliferative disorders. Vet Clin North Am Small Anim Pract. 1985; 15(4):769-81. DOI: 10.1016/s0195-5616(85)50035-2. View

Lang R, Metcalf D, Gough N, Dunn A, Gonda T . Expression of a hemopoietic growth factor cDNA in a factor-dependent cell line results in autonomous growth and tumorigenicity. Cell. 1985; 43(2 Pt 1):531-42. DOI: 10.1016/0092-8674(85)90182-5. View

Park L, Friend D, Gillis S, Urdal D . Characterization of the cell surface receptor for granulocyte-macrophage colony-stimulating factor. J Biol Chem. 1986; 261(9):4177-83. View

Stocking C, Loliger C, Kawai M, Suciu S, Gough N, Ostertag W . Identification of genes involved in growth autonomy of hematopoietic cells by analysis of factor-independent mutants. Cell. 1988; 53(6):869-79. DOI: 10.1016/s0092-8674(88)90329-7. View

10.

Chang J, Metcalf D, Lang R, Gonda T, Johnson G . Nonneoplastic hematopoietic myeloproliferative syndrome induced by dysregulated multi-CSF (IL-3) expression. Blood. 1989; 73(6):1487-97. View

11.

CRONKITE E, DREW R, Inoue T, Hirabayashi Y, Bullis J . Hematotoxicity and carcinogenicity of inhaled benzene. Environ Health Perspect. 1989; 82:97-108. PMC: 1568102. DOI: 10.1289/ehp.898297. View

12.

Williams G, Smith C, Spooncer E, Dexter T, Taylor D . Haemopoietic colony stimulating factors promote cell survival by suppressing apoptosis. Nature. 1990; 343(6253):76-9. DOI: 10.1038/343076a0. View

13.

Miltenyi S, Muller W, Weichel W, Radbruch A . High gradient magnetic cell separation with MACS. Cytometry. 1990; 11(2):231-8. DOI: 10.1002/cyto.990110203. View

14.

Sutherland H, Lansdorp P, Henkelman D, Eaves A, Eaves C . Functional characterization of individual human hematopoietic stem cells cultured at limiting dilution on supportive marrow stromal layers. Proc Natl Acad Sci U S A. 1990; 87(9):3584-8. PMC: 53946. DOI: 10.1073/pnas.87.9.3584. View

15.

Preston-Martin S, Pike M, Ross R, Jones P, Henderson B . Increased cell division as a cause of human cancer. Cancer Res. 1990; 50(23):7415-21. View

16.

Willman C, Whittaker M . The molecular biology of acute myeloid leukemia. Proto-oncogene expression and function in normal and neoplastic myeloid cells. Clin Lab Med. 1990; 10(4):769-96. View

17.

Dempster A, SNYDER C . Short term benzene exposure provides a growth advantage for granulopoietic progenitor cells over erythroid progenitor cells. Arch Toxicol. 1990; 64(7):539-44. DOI: 10.1007/BF01971832. View

18.

Irons R, Stillman W, Colagiovanni D, Henry V . Synergistic action of the benzene metabolite hydroquinone on myelopoietic stimulating activity of granulocyte/macrophage colony-stimulating factor in vitro. Proc Natl Acad Sci U S A. 1992; 89(9):3691-5. PMC: 525556. DOI: 10.1073/pnas.89.9.3691. View

19.

Leary A, Zeng H, Clark S, Ogawa M . Growth factor requirements for survival in G0 and entry into the cell cycle of primitive human hemopoietic progenitors. Proc Natl Acad Sci U S A. 1992; 89(9):4013-7. PMC: 525622. DOI: 10.1073/pnas.89.9.4013. View

20.

Tweardy D, Morel P, Mott P, Glazer E, Zeh H, Sakurai M . Modulation of myeloid proliferation and differentiation by monoclonal antibodies directed against a protein that interacts with the interleukin-3 receptor. Blood. 1992; 80(2):359-66. View