Benzene-Induced Hematopoietic Neoplasms Including Myeloid Leukemia in Trp 53-Deficient C57BL/6 and C3H/He Mice

Toxicological Sciences

Volumn 110, Issue 2, 2009, Pages 293-306

  Kawasaki, Yasushi ^a   Hirabayashi, Yoko ^a,b   Kaneko, Toyozo ^a   Kanno, Jun ^a   Kodama, Yukio ^a   Matsushima, Yuuko ^a   Ogawa, Yukio ^a   Saitoh, Minoru ^a   Sekita, Kiyoshi ^a   Uchida, Osayuki ^a   Umemura, Takashi ^a   Yoon, Byung Il ^a,b   Inoue, Tohru ^a  

^a NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

^b Kangwon National University   (South Korea)

Author keywords

Acute myeloid leukemia; Benzene; C3H He; C57BL 6; Hematopoietic neoplasms; Trp 53 deficient mice

Indexed keywords

BENZENE; GENE PRODUCT; PROTEIN TRP53; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; C3H MOUSE; C57BL MOUSE; CANCER INCIDENCE; CONTROLLED STUDY; DNA REPAIR; EMBRYO; HEMATOLOGIC MALIGNANCY; HETEROZYGOTE; LEUKEMIA CELL; LEUKEMOGENESIS; MOUSE; MOUSE STRAIN; NONHUMAN; PROTEIN DEFICIENCY; STRAIN DIFFERENCE; WILD TYPE;

ANIMALS; APOPTOSIS; BENZENE; CARCINOGENS; DNA REPAIR; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION, LEUKEMIC; HEMATOLOGIC NEOPLASMS; HETEROZYGOTE; INHALATION EXPOSURE; LETHAL DOSE 50; LEUKEMIA, MYELOID, ACUTE; MALE; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; SPECIES SPECIFICITY; TIME FACTORS; TUMOR SUPPRESSOR PROTEIN P53;

MURINAE; MUS;

EID: 67650723486     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfp107     Document Type: Article

References (46)

1. Aksoy, M., Erdem, S., and DinCol, G. (1974). Leukemia in shoe-workers exposed chronically to benzene. Blood 44, 837-841.
2. Cabot, R. C. (1927). Case 13321 bleeding from the gums. Boston M. & S.J. 197, 236.
3. Cronkite, E. P., Bullis, J., Inoue, T., and Drew, R. T. (1984). Benzene inhalation produces leukemia in mice. Toxicol. Appl. Pharmacol. 75, 358-361.
4. Cronkite, E. P., Drew, R. T., Inoue, T., and Bullis, J. E. (1985). Benzene hematotoxicity and leukemogenesis. Am. J. Ind. Med. 7 447-456.
5. Cronkite, E. P., Drew, R. T., Inoue, T., Hirabayashi, Y., and Bullis, J. E. (1989). Hematotoxicity and carcinogenicity of inhaled benzene. Environ. Health Perspect. 82, 97-108.
6. Cronkite, E. P., Inoue, T., Carsten, A. L., Miller, M. E., Bullis, J. E., and Drew, R. T. (1982). Effects of benzene inhalation on murine pluripotent stem cells. J. Toxicol. Environ. Health 9, 411-421.
7. Delore, P., and Borgomano, C. (1928). Leucémie aiguëau cours de l'intoxication benzénique. Sur l'origine toxique de certaines leucémies aiguës et leurs relations avec les ane'mies graves. J. de méd de Lyon 9, 227-233.
8. Feinstein, E., Gale, R. P., Reed, J., and Canaani, E. (1992). Expression of the normal p53 gene induces differentiation of K562 cells. Oncogene 7, 1853-1857.
9. French, J. E., Lacks, G. D., Trempus, C., Dunnick, J. K., Foley, J., Mahler, J., Tice, R. R., and Tennant, R. W. (2001). Loss of heterozygosity frequency at the Trp53 locus in p53-deficient (+/-) mouse tumors is carcinogen- and tissue-dependent. Carcinogenesis 22 99-106.
10. Frith, C. H., Ward, J. M., Harleman, J. H., Stromberg, P. C., Halm, S., Inoue, T., and Wright, J. A. (2001). Hematopoietic system. In International Classification of Rodent Tumors: The Mouse (U. Mohr, Ed.), pp. 417-451. Springer-Verlag Berlin, Heidelberg, Berlin.
11. Haines, B. B., Ryu, C. J., Chang, S., Protopopov, A., Luch, A., Kang, Y. H., Draganov, D. D., Fragoso, M. F., Paik, S. G., Hong, H. J., et al. (2006). Block of T cell development in P53-deficient mice accelerates development of lymphomas with characteristic RAG-dependent cytogenetic alterations. Cancer Cell 9, 109-120.
12. Harvey, M., McArthur, M. J., Montgomery, C. A., Jr., Butel, J. S., Bradley, A., and Donehower, L. A. (1993). Spontaneous and carcinogen-induced tumorigenesis in p53-deficient mice. Nat. Genet. 5, 225-229.
13. Hirabayashi, Y., Inoue, T., Suda, Y., Aizawa, S., Ikawa, Y., and Kanisawa, M. (1992). Hemopoietic neoplasms in lethally irradiated mice repopulated with bone marrow cells carrying the human c-myc oncogene: A repopulation assay. Exp. Hematol. 20, 167-172.
14. Hirabayashi, Y., Matsuda, M., Aizawa, S., Kodama, Y., Kanno, J., and Inoue, T. (2002). Serial transplantation of p53-deficient hemopoietic progenitor cells to assess their infinite growth potential. Exp. Biol. Med. (Maywood) 227, 474-479.
15. Hirabayashi, Y., Yoshida, K., Aizawa, S., Kodama, Y., Kanno, J., Kurokawa, Y., Yoshimura, I., and Inoue, T. (2003). Evaluation of nonthreshold leukemogenic response to methyl nitrosourea in p53-deficient C3H/He mice. Toxicol. Appl. Pharmacol. 190, 251-261.
16. Huff, J. E., Haseman, J. K., DeMarini, D. M., Eustis, S., Maronpot, R. R., Peters, A. C., Persing, R. L., Chrisp, C. E., and Jacobs, A. C. (1989). Multiple-site carcinogenicity of benzene in Fischer 344 rats and B6C3F1 mice. Environ. Health Perspect. 82, 125-163.
17. Kastan, M. B., Radin, A. I., Kuerbitz, S. J., Onyekwere, O., Wolkow, C. A., Civin, C. I., Stone, K. D., Woo, T., Ravindranath, Y., and Craig, R. W. (1991). Levels of p53 protein increase with maturation in human hematopoietic cells. Cancer Res. 51, 4279-4286.
18. Kemp, C. J., Wheldon, T., and Balmain, A. (1994). p53-deficient mice are extremely susceptible to radiation-induced tumorigenesis. Nat. Genet. 8, 66-69.
19. Lan, Q., Zhang, L., Li, G., Vermeulen, R., Weinberg, R. S., Dosemeci, M., Rappaport, S. M., Shen, M., Alter, B. P., Wu, Y., et al. (2004). Hematotoxicity in workers exposed to low levels of benzene. Science 306, 1774-1776.
20. Le Noir, M. M., and Claude, H. (1897). Sur un cas de purpura attribué a l'intoxication par la benzine. Bull. Med. Soc. Hop. Paris 14 1251-1260.
21. Li, G. X., Hirabayashi, Y., Yoon, B. I., Kawasaki, Y., Tsuboi, I., Kodama, Y., Kurokawa, Y., Yodoi, J., Kanno, J., and Inoue, T. (2006). Thioredoxin overexpression in mice, model of attenuation of oxidative stress, prevents benzene-induced hemato-lymphoid toxicity and thymic lymphoma. Exp. Hematol. 34, 1687-1697.
22. MacDonald, J., French, J. E., Gerson, R. J., Goodman, J., Inoue, T., Jacobs, A., Kasper, P., Keller, D., Lavin, A., Long, G., et al. (2004). The utility of genetically modified mouse assays for identifying human carcinogens: A basic understanding and path forward. The Alternatives to Carcinogenicity Testing Committee ILSI HESI. Toxicol. Sci. 77 188-194.
23. Maltoni, C., Ciliberti, A., Cotti, G., Conti, B., and Belpoggi, F. (1989). Benzene, an experimental multipotential carcinogen: Results of the longterm bioassays performed at the Bologna Institute of Oncology. Environ. Health Perspect. 82, 109-124.
24. Mouse Genome Informatics. (2009). Trp53tm1Sia Targeted Allele Detail, ID: MGI: 1926340HAvailable at: http://www.informatics.jax.org/ javawi2/servlet/WIFetch?page=alleleDetail&key=2871. Accessed June 4, 2009.
25. NTP. (1986). Toxicology and carcinogenesis studies of benzene (CAS No. 71-43-2) in F344/N rats and B6C3F1 mice (Gavage Studies). Natl. Toxicol. Program Tech. Rep. Ser. 289, 1-277.
26. Penati, F., and Vigliani, E. C. (1938). Sul problema delle mielopatie aplastische pseudoaplastische e leucemiche d benzolo. Ras. Med. Ind. 9, 345-361.
27. Santesson, C. G. (1897). Über chronischeVergiftungen mit Steinkohlenteerbenzin: Vier Todesfälle. Arch. Hyg. Berl. 31 336-376.
28. Seki, M., Yoshida, K., Nishimura, M., and Nemoto, K. (1991). Radiation-induced myeloid leukemia in C3H/He mice and the effect of prednisolone acetate on leukemogenesis. Radiat. Res. 127, 146-149.
29. Selling, L. (1910). A preliminary report on some cases of purpura hoemorrhagica due to benzol poisoning. Bull. Johns Hopkins Hosp. 21, 33-37.
30. Skorski, T., Nieborowska-Skorska, M., Wlodarski, P., Perrotti, D., Martinez, R., Wasik, M. A., and Calabretta, B. (1996). Blastic transformation of p53-deficient bone marrow cells by p210bcr/abl tyrosine kinase. Proc. Natl. Acad. Sci. U. S. A. 93, 13137-13142.
31. Smith, A. R. (1928). Chronic benzol poisoning among women industrial workers: A study of the women exposed to benzol fumes in six factories. J. Indust. Hyg. 10, 73-93.
32. Snyder, C. A., Goldstein, B. D., Sellakumar, A. R., Bromberg, I., Laskin, S., and Albert, R. E. (1980). The inhalation toxicology of benzene: Incidence of hematopoietic neoplasms and hematotoxicity in ARK/ J and C57BL/6J mice. Toxicol. Appl. Pharmacol. 54, 323-331.
33. Snyder, R. (2002). Benzene and leukemia. Crit. Rev. Toxicol. 32 155-210.
34. Snyder, R. (2007). Benzene's toxicity: A consolidated short review of human and animal studies by HA Khan. Hum. Exp. Toxicol. 26, 687-696.
35. Soddu, S., Blandino, G., Citro, G., Scardigli, R., Piaggio, G., Ferber, A., Calabretta, B., and Sacchi, A. (1994). Wild-type p53 gene expression induces granulocytic differentiation of HL-60 cells. Blood 83 2230-2237.
36. Storer, R. D., French, J. E., Haseman, J., Hajian, G., LeGrand, E. K., Long, G. G., Mixson, L. A., Ochoa, R., Sagartz, J. E., and Soper, K. A. (2001). P53+/- hemizygous knockout mouse: Overview of available data. Toxicol. Pathol. 29(Suppl), 30-50.
37. Tsukada, T., Tomooka, Y., Takai, S., Ueda, Y., Nishikawa, S., Yagi, T., Tokunaga, T., Takeda, N., Suda, Y., Abe, S., et al. (1993). Enhanced proliferative potential in culture of cells from p53-deficient mice. Oncogene 8, 3313-3322.
38. Vigliani, E. C., and Forni, A. (1976). Benzene and leukemia. Environ. Res. 11, 122-127.
39. WHO. (2003). Benzene in Drinking-Water. Background Document for Development of WHO Guidelines for Drinking-Water Quality. WHO/SDE/ WSH/03.04/24. Accessed June 4, 2009. Originally published in Guidelines for drinking-water quality, 2nd ed. Vol. 2. Health criteria and other supporting information. World Health Organization, Geneva.
40. Yagi, T., Tokunaga, T., Furuta, Y., Nada, S., Yoshida, M., Tsukada, T., Saga, Y., Takeda, N., Ikawa, Y., and Aizawa, S. (1993). A novel ES cell line, TT2, with high germline-differentiating potency. Anal. Biochem. 214, 70-76.
41. Yoon, B. I., Hirabayashi, Y., Kawasaki, Y., Kodama, Y., Kaneko, T., Kanno, J., Kim, D. Y., Fujii-Kuriyama, Y., and Inoue, T. (2002). Aryl hydrocarbon receptor mediates benzene-induced hematotoxicity. Toxicol. Sci. 70, 150-156.
42. Yoon, B. I., Hirabayashi, Y., Kawasaki, Y., Kodama, Y., Kaneko, T., Kim, D. Y., and Inoue, T. (2001). Mechanism of action of benzene toxicity: Cell cycle suppression in hemopoietic progenitor cells (CFU-GM). Exp. Hematol. 29, 278-285.
43. Yoon,B. I., Li,G.X.,Kitada,K.,Kawasaki,Y., Igarashi,K.,Kodama,Y., Inoue, T., Kobayashi, K., Kanno, J., Kim, D. Y., et al. (2003). Mechanisms of benzene-induced hematotoxicity and leukemogenicity: CDNA microarray analyses using mouse bone marrow tissue. Environ. Health Perspect. 111, 1411-1420.
44. Yoshida, K., Aizawa, S., Watanabe, K., Hirabayashi, Y., and Inoue, T. (2002). Stem-cell leukemia: P53 deficiency mediated suppression of leukemic differentiation in C3H/He myeloid leukemia. Leuk. Res. 26, 1085-1092.
45. Yoshida, K., Hirabayashi, Y., Wada, S., Watanabe, F., Watanabe, K., Aizawa, S., and Inoue, T. (2007). p53 (TRP53) deficiency-mediated antiapoptosis escape after 5 Gy X irradiation still induces stem cell leukemia in C3H/He mice: Comparison between whole-body assay and bone marrow transplantation (BMT) assay. Radiat. Res. 167, 703-710.
46. Yoshida, K., Nojima, K., Seki, M., and Inoue, T. (1996). Radiation-induced myeloid leukemia following splenectomy in C3H/He mice. J. Radiat. Res. 37, 380.