The benzene metabolites hydroquinone and catechol act in synergy to induce dose-dependent hypoploidy and -5q31 in a human cell line

Leukemia and Lymphoma

Volumn 35, Issue 3-4, 1999, Pages 269-281

  Stillman, W S ^a   Varella Garcia, M ^a   Irons, R D ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

AML; Benzene; Catechol; FISH; Hydroquinone; Leukemogenesis; MDS

Indexed keywords

BENZENE; CATECHOL; HYDROQUINONE;

ACUTE GRANULOCYTIC LEUKEMIA; ARTICLE; BLOOD TOXICITY; BONE MARROW TOXICITY; CHROMOSOME 5; CHROMOSOME 5Q; CHROMOSOME 7; CHROMOSOME ABERRATION; CHROMOSOME DELETION; CYTOGENETICS; DOSE RESPONSE; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; HUMAN CELL; METABOLISM; MYELODYSPLASTIC SYNDROME; OCCUPATIONAL EXPOSURE; PRIORITY JOURNAL; TRISOMY 8;

EID: 0032748133     PISSN: 10428194     EISSN: None     Source Type: Journal    
DOI: 10.3109/10428199909145730     Document Type: Article

References (71)

1. Santesson, C.G. (1897) Chronic poisoning with coal tar benzene: Four deaths. Clinical and pathological-anatomical observations of several colleagues and illustrating animal experiments. Archiv fur Hygiene, 31, 336-376.
2. Greenburg, L., Mayers, M.R., Goldwater, L.J., and Smith, A.R. (1939) Benzene (benzol) poisoning in the rotogravure printing industry in New York City. Journal of Industrial Hygiene and Toxicology, 21(8), 395-420.
3. Laskin, S. and Goldstein, B.D. (1977) Benzene toxicity: a critical evaluation. Journal of Toxicology and Environmental Health, 2, 1-148.
4. Vigliani, E.C. and Saita, G. (1964) Benzene and leukemia. New England Journal of Medicine, 271, 872-876.
5. Vigliani, E.C. and Forni, A. (1976) Benzene and leukemia. Environmental Research, 11, 122-127.
6. Aksoy, M., Erdem, S., Dinçol, K., Hepyüksel, T., and Dinçol, G. (1974) Chronic exposure to benzene as a possible contributary etiologic factor in Hodgkin's Disease. Blut, 28, 293-298.
7. Aksoy, M., Erdem, S., and Dinçol, G. (1976) Types of leukemia in chronic benzene poisoning: a study in thirty-four patients. Acta Haematologica, 55, 65-72.
8. Infante, P.F., Rinsky, R.A., Wagoner, J.K., and Young, R.J. (1977) Leukaemia in benzene workers. Lancet, 2, 76-78.
9. Casciato, D.A. and Scott, J.L. (1979) Acute leukemia following prolonged cytotoxic agent therapy. Medicine, 58(1), 32-47.
10. Foucar, K., McKenna, R.W., Bloomfield, C.D., Bowers, T.K., and Brunning, R.D. (1979) Therapy-related leukemia. Cancer, 43, 1285-1296.
11. Pedersen-Bjergaard, J., Philip, P., Mortensen, B.T., Ersholl, J., Jensen, G., Panduro, J., and Thomsen, M. (1981) Acute nonlymphocytic leukemia, preleukemia, and acute myeloproliferative syndrome secondary to treatment of other malignant diseases. Clinical and cytogenetic characteristics and results of in vitro culture of bone marrow and HLA typing. Blood, 57(4), 712-723.
12. Pedersen-Bjergaard, J., Pedersen, M., Roulston, D., and Philip, P. (1995) Different genetic pathways in leukemogenesis for patients presenting with therapy-related myelodysplasia and therapy-related acute myeloid leukemia. Blood, 86, 3542-3552.
13. Anderson, R.L., Bagby, G.C., Jr., Richert-Boe, K., Magenis, R.E., and Koler, R.D. (1981) Therapy-related preleukemic syndrome. Cancer, 47, 1867-1871.
14. Coltman, C.A. and Dahlberg, S. (1990) Treatment-related leukemia. New England Journal of Medicine, 322, 52-53,
15. Advani, S.H., Doval, D.C., Gopal, R., Nair, C.N., and Kutty, P.M. (1983) Therapy-related leukemia. Oncology, 40, 268-272.
16. Rowley, J.D., Golomb, H.M., and Vardiman, J. (1977) Nonrandom chromosomal abnormalities in acute nonlymphocytic leukemia in patients treated for Hodgkin's disease and non-Hodgkin lymphomas. Blood, 50, 759-770.
17. Rowley, J.D., Golomb, H.M., and Vardiman, J.W. (1981) Nonrandom chromosome abnormalities in acute leukemia and dysmyelopoietic syndromes in patients with previously treated malignant disease. Blood, 58, 759-767.
18. Le Beau, M.M., Albain, K.S., Larson, R.A., Vardiman, J.W., Davis, E.M., Blough, R.R., Golomb, H.M., and Rowley, J.D. (1986) Clinical and cytogenetic correlations in 63 patients with therapy-related myelodysplastic syndromes and acute nonlymphocytic leukemia: further evidence for characteristic abnormalities of chromosomes no. 5 and 7. Journal of Clinical Oncology, 4(3), 325-345.
19. Pedersen-Bjergaard, J., Philip, P., Perdersen, N.T., Hou-Jensen, K., Svejgaard, A., Jensen, G., and Nissen, N.I. (1984) Acute nonlymphocytic leukemia, preleukemia, and acute myeloproliferative syndrome secondary to treatment of other malignant diseases. Cancer, 54, 452-462.
20. Johansson, B., Mertens, F., Heim, S., Kristoffersson, U., and Mitelman, F. (1991) Cytogenetics of secondary myelodysplasia (sMDS) and acute nonlymphocytic leukemia (sANLL). European Journal of Haematology, 47,17-27.
21. Bitter, M.A., Le Beau, M.M., Rowley, J.D., Larson, R.A., Golomb, H.M., and Vardiman, J.W. (1987) Associations between morphology, karyotype, and clinical features in myeloid leukemias. Human Pathology, 18, 211-225.
22. Fourth International Workshop on Chromosomes in Leukemia, 1982 (1984) The correlation of karyotype and occupational exposure to potential mutagenic/carcinogenic agents in acute nonlymphocytic leukemia. Cancer Genetics and Cytogenetics, 11, 326-331.
23. Bloomfield, C.D., Goldman, A., Hossfeld, D., and de la Chapelle, A. (1984) Clinical significance of chromosomal abnormalities in acute nonlymphoblastic leukemia. Cancer Genetics and Cytogenetics, 11, 332-350.
24. Mitelman, F., Nilsson, P.G., Brandt, L., Alimena, G., Gastaldi, R., and Dallapiccola, B. (1981) Chromosome pattern, occupation, and clinical features in patients with acute nonlymphocytic leukemia. Cancer Genetics and Cytogenetics, 4, 197-214.
25. Mitelman, F., Brandt, L., and Nilsson, P.G. (1978) Relation among occupational exposure to potential mutagenic/carcinogenic agents, clinical findings, and bone marrow chromosomes in acute nonlymphocytic leukemia. Blood, 52, 1229-1237.
26. Fagioli, F., Cuneo, A., Piva, N., Carli, M.G., Previali, R., Balboni, M., Tomasi, P., Cariani, D., Scapoli, G., and Castoldi, G. (1992) Distinct cytogenetic and clinicopathologic features in acute myeloid leukemia after occupational exposure to pesticides and organic solvents. Cancer, 70, 77-85.
27. Golomb, H.M., Alimena, G., Rowley, J.D., Vardiman, J.W., Testa, J.R., and Sovik, C. (1982) Correlation of occupation and karyotype in adults with acute nonlymphocytic leukemia. Blood, 60, 404-411.
28. Cuneo, A., Fagioli, F., Pazzi, I., Tallarico, A., Previati, R., Piva, N., Carli, G.M., Balboni, M., and Castoldi, G. (1992) Morphologic, immunologic and cytogenetic studies in acute myeloid leukemia following occupational exposure to pesticides and organic solvents. Leukemia Research, 16, 789-796.
29. Narod, S.A. and Dube, I.D. (1989) Occupational history and involvement of chromosomes 5 and 7 in acute nonlymphocytic leukemia. Cancer Genetics and Cytogenetics, 38, 261-269.
30. Crane, M.M., Keating, M.J., Trujillo, J.M., Labarthe, D.R., and Frankowski, R.F. (1989) Environmental exposures in cytogenetically defined subsets of acute nonlymphocytic leukemia. Journal of the American Medical Association, 262, 634-639.
31. Van den Berghe, H., Louwagie, A., Broeckaert-Van Orshoven, A., David, G., and Verwilghen, R. (1979) Chromosome analysis in two unusual malignant blood disorders presumably induced by benzene. Blood, 53, 558-566.
32. Vogelstein, B., Fearon, E.R., Hamilton, S.R., Kern, S.E., Preisinger, A.C., Leppert, M., Nakamura, Y., White, R., Smits, A.M.M., and Bos, J.L. (1988) Genetic alterations during colorectal-tumor development. New England Journal of Medicine, 319(9), 525-532.
33. Irons, R.D. Leukemogenesis as a toxic response. In: I.G. Sipes, C.A. McQueen, A.J. Gandolfi and J.C. Bloom (eds.), Comprehensive Toxicology, pp. 175-199, New York: Elsevier Science Ltd., 1997.
34. Irons, R.D. and Stillman, W.S. (1996) The process of leukemogenesis. Environmental Health Perspectives, 104 Suppl. 6, 1239-1246.
35. Andrews, L.S., Lee, E.W. Winner, C.M., Kocsis, J.J., and Snyder, R.S. (1977) Effects of toluene on the metabolism, disposition and hemopoietic toxicity of benzene. Biochemical Pharmacology, 26, 293-300.
36. 3H-benzene metabolism in rabbit bone marrow. Life Sciences, 25, 567-572.
37. Sammett, D., Lee, E.W., Kocsis, J.J., and Snyder, R. (1979) Partial hepatectomy reduced both metabolism and toxicity of benzene. Journal of Toxicology and Environmental Health, 5, 785-792.
38. Eastmond, D.A., Smith, M.T., and Irons, R.D. (1987) An interaction of benzene metabolites reproduces the myelotoxicity observed with benzene exposure. Toxicology and Applied Pharmacology, 91, 85-95.
39. Rickert, D.E., Baker, T.S., Bus, J.S., Barrow, C.S., and Irons, R.D. (1979) Benzene disposition in the rat after exposure by inhalation. Toxicology and Applied Pharmacology, 49, 417-423.
40. Wierda, D. and Irons, R.D. (1982) Hydroquinone and catechol reduce the frequency of progenitor B lymphocytes in mouse spleen and bone marrow. Immunopharmacology, 4, 41-54.
41. Irons, R.D. (1985) Quinones as toxic metabolites of benzene. Journal of Toxicology and Environmental Health, 16, 673-678.
42. Tice, R.R., Costa, D.L., and Drew, R.T. (1980) Cytogenetic Effects of Inhaled Benzene in Murine Bone Marrow: Induction of Sister Chromatid Exchanges, Chromosomal Aberrations, and Cellular Proliferation Inhibition in DBA/2 Mice. Proceedings of the National Academy of Sciences of the United States of America, 77(4), 2148-2152.
43. Luke, C.A., Tice, R.R., and Drew, R.T. (1989) The Effect of Gender and Exposure Regimen and Duration on Benzene-Induced Bone Marrow Damage. Environmental Health Perspectives, 82, 65-74.
44. Forni, A. and Moreo, L. (1969) Chromosome Studies in a Case of Benzene-Induced Erythroleukaemia. European Journal of Cancer, 5, 459-463.
45. Forni, A. (1979) Chromosome changes and benzene exposure. A review. Reviews on Environmental Health, 3, 5-17.
46. Morimoto, K. (1976) Analysis of Combined Effects of Benzene With Radiation on Chromosomes in Cultured Human Leukocytes. Japanese Journal of Industrial Health, 18, 23-34.
47. Tsutsui, T., Nayashi, N., Maizuni, H., Huff, J., and Barrett, J.C. (1997) Benzene-, catechol-, hydroquinone- and phenol-induced cell transformation, gene mutations, chromosome aberrations, aneuploidy, sister chromatid exchanges and unscheduled DNA synthesis in Syrian hamster embryo cells. Mutation Research, 373, 113-123.
48. Muirhead, K.A., Irons, R.D., Bruns, R., and Horan, P.K. (1980) A rabbit bone marrow model system for evaluation of cytotoxicity: characterization of normal bone marrow cell cycle parameters by flow cytometry. Journal of Histochemistry and Cytochemistry, 28(6), 526-532.
49. Horan, P.K., Muirhead, K.A., Gorton, S., and Irons, R.D. (1980) Aseptic aspiration of rabbit bone marrow and enrichment for cycling cells. Laboratory Animal Science, 30(1), 76-79.
50. Irons, R.D. (1981) Benzene-induced myelotoxicity: application of flow cytofluorometry for the evaluation of early proliferative change in bone marrow. Environmental Health Perspectives, 39, 39-49.
51. Irons, R.D., Neptun, D.A., and Pfeifer, R.W. (1981) Inhibition of lymphocyte transformation and microtubule assembly by quinone metabolites of benzene: evidence for a common mechanism. Journal of the Reticuloendothelial Society, 30(5), 359-372.
52. Irons, R.D. and Neptun, D.A. (1980) Effects of the principal hydroxymetabolites of benzene on microtubule polymerization. Archives of Toxicology, 45, 297-305.
53. Irons, R.D., Pfeifer, R.W., Aune, T.M., and Pierce, C.W. (1984) Soluble immune response suppressor (sirs) inhibits microtubule function in vivo and microtubule assembly in vitro. Journal of mmunology, 133, 2032-2036.
54. Yager, J.W., Eastmond, D.A., Robertson, M.L., Pardisin, W.M., and Smith, M.T. (1990) Characterization of micronuclei induced in human lymphocytes by benzene metabolites. Cancer Research, 50, 393-399.
55. Marrazzini, A., Chelotti, L., Barrai, I., Loprieno, N., and Barale, R. (1994) In vivo genotoxic interactions among three phenolic benzene metabolites. Mutat. Res. Genet. Toxicol. Testing, 341, 29-46.
56. Stillman, W.S., Varella-Garcia, M., Gruntmeir, J.J., and Irons, R.D. (1997) The benzene metabolite, hydroquinone, induces dose-dependent hypoploidy in a human cell line. Leukemia, 11, 1540-1545.
57. Robertson, M.L., Eastmond, D.A., and Smith, M.T. (1991) Two benzene metabolites, catechol and hydroquinone, produce a synergistic induction of micronuclei and toxicity in cultured human lymphocytes. Mutation Research, 249, 201-209.
58. Levay, G. and Bodell, W.J. (1992) Potentiation of DNA adduct formation in HL-60 cells by combinations of benzene metabolites. Proceedings of the National Academy of Sciences of the United States of America, 89, 7105-7109.
59. Natarajan, A.T., Tates, A.D., Meijers, M., Neuteboom, M., and Vogel, N. (1983) Induction of sister chromatid exchanges (SCEs) and chromosomal aberrations by mitomycin C and methyl methanosulfonate in Chinese hamster oveary cells. Mutation Research, 121, 211-223.
60. Preston, R.J., Dean, B.J., Galloway, S., Holden, H., McFee, A.F., and Shelby, M. (1987) Mammalian in vivo cytogenetic assays: analysis of chromosome aberrations in bone marrow cells. Mutation Research, 189, 157-165.
61. Cox, D.M. and Puck, T.T. (1969) Chromosomal non-disjunction: the action of colcemid on Chinese hamster cells in vitro. Cytogenetics, 8, 158-169.
62. Draper, N.P. and Smith, H. Applied Regression Analysis. New York: John Wiley & Sons, 1981.
63. Fairman, J., Chumakov, I., Chinault, A.C., Nowell, P.C., and Nagarajan, L. (1995) Physical mapping of the minimal region of loss in 5q-chromosome. Proceedings of the National Academy of Sciences of the United States of America, 92, 7406-7410.
64. Le Beau, M.M., Espinosa, R., III, Neuman, W.L., Stock, W., Roulston, D., Larson, R.A., Keinanen, M., and Westbrook, C.A. (1993) Cytogenetic and molecular delineation of the smallest commonly deleted region of chromosome 5 in malignant myeloid diseases. Proceedings of the National Academy of Sciences of the United States of America, 90, 5484-5488.
65. Horrigan, S.K., Westbrook, C.A., Kim, A.H., Banerjee, M., Stock, W., and Larson, R.A. (1996) Polymerase chain reaction-based diagnosis of Del(5q) in acute myeloid leukemia and myelodysplastic syndrome identifies a minimal deletion interval. Blood, 88, 2665-2670.
66. Van den Berghe, H., Vermaelen, K., Mecucci, C., Barbieri, D., and Tricot, G. (1985) The 5q-anomaly. Cancer Genetics and Cytogenetics, 17, 189-225.
67. Eastmond, D.A., Schuler, M., and Rupa, D.S. (1995) Advantages and limitations of using fluorescence in situ hybridization for the detection of aneuploidy in interphase human cells. Mutation Research, 348, 153-162.
68. Eastmond, D.A., Rupa, D.S., and Hasegawa, L.S. (1994) Detection of hyperdiploidy and chromosome breakage in interphase human lymphocytes following exposure to the benzene metabolite hydroquinone using multicolor fluorescence in situ hybridization with DNA probes. Mutation Research, 322, 9-20.
69. Lee, S.-F. and Lin, J.-K. (1994) Generation of hydrogen peroxide, superoxide anion and the hydroxyl free radical from polyphenols and active benzene metabolites: Their possible role in mutagenesis. J. Biomed. Sci. 1, 125-130.
70. Irons, R.D. and Stillman, W.S. (1993) Cell proliferation and differentiation in chemical leukemogenesis. Stem Cells, 11, 235-242.
71. Irons, R.D. and Stillman, W.S. (1996) Impact of benzene metabolites on differentiation of bone marrow progenitor cells. Environmental Health Perspectives, 104 Suppl. 6, 1247-1250.