Multiorgan transplacental and neonatal carcinogenicity of 3'-azido-3'- deoxythymidine in mice

Toxicology and Applied Pharmacology

Volumn 161, Issue 1, 1999, Pages 82-99

  Diwan, Bhalchandra A ^a   Riggs, Charles W ^a   Logsdon, Daniel ^a   Haines, Diana C ^a   Olivero, Ofelia A ^c   Rice, Jerry M ^b   Yuspa, Stuart H ^c   Poirier, Miriam C ^c   Anderson, Lucy M ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

AZT; Carcinogenesis; Fetus; Mice; Perinatal; Transplacental

Indexed keywords

ZIDOVUDINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; DRUG CARCINOGENICITY; FEMALE; HISTOPATHOLOGY; LUNG TUMOR; LYMPHOMA; MALE; MOUSE; NONHUMAN; ORAL DRUG ADMINISTRATION; PERINATAL PERIOD; PLACENTAL TRANSFER; TOXICITY TESTING;

ANIMALIA; TRIXIS;

EID: 0033571589     PISSN: 0041008X     EISSN: None     Source Type: Journal    
DOI: 10.1006/taap.1999.8782     Document Type: Article

References (71)

1. Anderson L. M., Jones A. B., Riggs C. W., Ohshima M. Fetal mouse susceptibility to transplacental lung and liver carcinogenesis by 3-methylcholanthrene: positive correlation with responsiveness to inducers of aromatic hydrocarbon metabolism. Carcinogenesis. 6:1985;1389-1393.
2. Anderson L. M., Jones A. B., Riggs C. W. Long-term (imprinting) effects of transplacental treatment of mice with 3-methylcholanthrene or β-naphthoflavone on hepatic metabolism of 3-methylcholanthrene. Pharmacol. Toxicol. 69:1991;178-188.
3. Anderson L. M., Ruskie S., Carter J., Pittinger S., Kovatch R. M., Riggs C. W. Fetal mouse susceptibility to transplacental carcinogenesis: Differential influence of Ah receptor phenotype on effects of 3-methylcholanthrene, 7,12-dimethylbenz[a]anthracene, and benzo[a]pyrene. Pharmacogenetics. 5:1995;364-372.
4. Anisimov V. N., Osipova G. Y. Effect of neonatal exposure to 5-bromo-2′deoxyuridine on life span, estrus function and tumor development in rats-an argument in favor of the mutation theory of aging? Mutat. Res. 275:1992;97-110.
5. Anisimov V. N., Osipova G. Y. Carcinogenesis induced by combined neonatal exposure to 5-bromo-2′-deoxyuridine and subsequent total-body X-ray irradiation in rats. Cancer Lett. 70:1993;81-90.
6. Armitage P. Statistical Methods in Medical Research. 1971;Blackwell Scientific Publications, Oxford.
7. Ayers K. M., Clive D., Tucker W. E. Jr., Hajian G., De Miranda P. Nonclinical toxicology studies with zidovudine: Genetic toxicity tests and carcinogenicity bioassays in mice and rats. Fundam. Appl. Toxicol. 32:1996;146-158.
8. Ayers K. M., Torrey C. E., Reynolds D. J. A transplacental carcinogenicity bioassay in CD-1 mice with zidovudine. Fundam. Appl. Toxicol. 38:1997;195-198.
9. Beach R. S., Gershwin M. E., Hurley L. S. Gestational zinc deprivation in mice: Persistence of immunodeficiency for three generations. Science. 218:1982;469-473.
10. Bilello J. A., MacAuley C., Fredrickson T. N., Bell M. M., Mckissik C., Shapiro S. G., Personette R., Eiseman J. L. Use of a neonatal murine model to evaluate the long-term efficacy and toxicity of antiviral agents. Ann. NY Acad. Sci. 616:1990;238-251.
11. Clemens L. G., Popham T. V., Ruppert P. H. Neonatal treatment of hamsters with barbiturate alters adult sexual behavior. Dev. Psychobiol. 12:1979;49-59.
12. Colquhoun D. Lectures on Biostatistics. 1979;Clarendon Press, Oxford.
13. Connor E. M., Sperling R. S., Gelber R., Kiselev P., Scott G., O'Sullivan M. J., Van Dyke R., Bey M., Shearer W., Jacobson R. L., Jimenez E., O'Neill E., Bazin B., Delfraissy J., Culnane M., Coombs R., Elkins M., Moye J., Stratton P., Balsley J. Reduction of maternal-fetal transmission of human immunodeficiency virus type 1 with zidovudine treatment. Pediatric AIDS Clinical Trials Group Protocol 076 Study Group. N. Engl. J. Med. 331:1994;1173-1180.
14. Craddock V. M. Shortening of life span caused by administration of 5-bromodeoxyuridine to neonatal rats. Chem.-Biol. Interact. 35:1981;139-144.
15. Culnane M., Fowler M., Lee S. S., McSherry G., Brady M., O'Donnell K., Mofenson L., Gortmaker S.L., Shapiro D. E., Scott G., Jimenez E. C., Diaz C., Flynn P. M., Cunningham B., Oleske J. Lack of long-term effects of in utero exposure to zidovudine among uninfected children born to HIV-infected women. J. Am. Med. Assoc. 281:1999;151-157.
16. Dertinger S. D., Torous D. K., Tometsko K. R. Induction of micronuclei by low doses of azidothymidine (AZT). Mutat. Res. 368:1996;301-307.
17. DiPaolo J. A. Polydactylism in the offspring of mice injected with 5-bromodeoxyuridine. Science. 145:1964;501-503.
18. Diwan B. A., Rice J. M., Ohshima M., Ward J. M., Dove L. F. Comparative tumor-promoting activities of phenobarbital, amobarbital, barbital sodium, and barbituric acid on liver and other organs of male F344/NCr rats following initiation with N-nitrosodiethylamine. J. Natl. Cancer Inst. 74:1985;509-516.
19. MTV- and DBA/2NCr mice. Carcinogenesis. 7:1986;215-220.
20. Diwan B. A., Ohshima M., Rice J. M. Promotion by sodium barbital of renal cortical and transitional cell tumors, but not intestinal tumors, in F344 rats given methyl-(acetoxymethyl)nitrosamine, and lack of effect of phenobarbital, amobarbital, or barbituric acid on development of either renal or intestinal tumors. Carcinogenesis. 10:1989a;183-188.
21. Diwan B. A., Ohshima M., Rice J. M. Effects of postnatal administration of tumor-promoting barbiturates on the development of tumors initiated by prenatal exposure of fetal rats and mice to N-alkylnitrosoureas. Napalkov N. P., Rice J. M., Tomatis L., Yamasaki H. Perinatal and Multigeneration Carcinogenesis. 1989b;75-80 International Agency for Research on Cancer, Lyon.
22. Diwan B. A., Rehm S., Rice J. M. Age- and dose-dependent transplacental carcinogenesis by N-nitrosoethylurea in Syrian golden hamsters. J. Cancer Res. Clin. Oncol. 122:1996;643-652.
23. Frith C. H., Ward J. M., Frederickson T., Harleman J. H. Neoplastic lesions of the hematopoietic system. Mohr U., Dungworth D. L., Capen C. C., Carlton W. W., Sundberg J. P., Ward J. M. Pathobiology of the Aging Mouse. 1996;219-235 ILSI Press, Washington.
24. Fujii K. Evaluation of the newborn mouse model for chemical tumorigenesis. Carcinogenesis. 12:1991;1409-1415.
25. Goerttler K., Loehrke H., Hesse B., Milz A., Schweizer J. Diaplacental initiation of NMRI mice with 7,12-dimethylbenz[a]anthracene during gestation days 6-20 and postnatal treatment of the F1 generation with phorbol ester 12-O-tetradecanoylphorbol-13-acetate: Tumor incidence in organs other than skin. Carcinogenesis. 2:1981;1087-1094.
26. Gordon L. R., Majka J. A., Boorman G. A. Spontaneous nonneoplastic and neoplastic lesions and experimentally induced neoplasms of the testes and accessory sex glands. Mohr U., Dungworth D. L., Capen C. C., Carlton W. W., Sundberg J. P., Ward J. M. Pathobiology of the Aging Mouse. 1996;421-441 ILSI Press, Washington.
27. Grdina D. J., Dale P., Weichselbaum R. Protection against AZT-induced mutagenesis at the HGRPT locus in a human cell line by WR-151326. Int. J. Radiat. Oncol. Biol. Phys. 22:1992;813-815.
28. 14C-pregnenolone and other metabolites during phenobarbital block of PMS-induced ovulation in immature rats: Inhibition of 3α-hydroxysteroid dehydrogenation. Endocrinology. 92:1973;117-124.
29. Gupta C., Yaffe S. J., Shapiro B. H. Prenatal exposure to phenobarbital permanently decreases testosterone and causes reproductive dysfunction. Science. 216:1982;640-641.
30. Hayakawa M., Ogawa T., Sugiyama S., Tanaka M., Ozawa T. Massive conversion of guanosine to 8-hydroxy-guanosine in mouse liver mitochondrial DNA by administration of azidothymidine. Biochem. Biophys. Res. Commun. 176:1991;87-92.
31. Hollander M., Wolfe D. A. Nonparametric Statistical Methods. 1973;John Wiley and Sons, New York.
32. Homburger F., Russfield A. B., Weisburger J. H., Lim S., Chak S. P., Weisburger E. K. Aging changes in CD-1 HaM/ICR mice reared under standard laboratory conditions. J. Natl. Cancer Inst. 55:1975;37-45.
33. Ivankovic S., Druckrey H. Transplacentare erzeugung maligner tumoren des nervensystem: Äthyl-nitroso-hornstoff (ÄNH) an BD IX-ratten. Z. Krebsforsch. 71:1968;320-360.
34. Klaunig J. E., Pereira M. A., Ruch R. J., Weghorst C. M. Dose-response relationship of diethylnitrosamine-initiated tumors in neonatal BALB/c mice: Effect of phenobarbital promotion. Toxicol. Pathol. 16:1988;381-385.
35. Kleihues P., Rajewsky M. F. Chemical neuro-oncogenesis: Role of structural DNA modifications, DNA repair, and neural target cell population. Prog. Exp. Tumor Res. 27:1984;1-16.
36. Maekawa A., Maita K., Harleman J. H. Changes in the ovary. Mohr U., Dungworth D. L., Capen C. C., Carlton W. W., Sundberg J. P., Ward J. M. Pathobiology of the Aging Mouse. 1996;452-467 ILSI Press, Washington.
37. Maekawa A., Yoshida A. Susceptibility of the female genital system to toxic substances. Mohr U., Dungworth D. L., Capen C. C., Carlton W. W., Sundberg J. P., Ward J. M. Pathobiology of the Aging Mouse. 1996;482-493 ILSI Press, Washington.
38. Medical Economics Co.1997. Retrovir. In Physicians' Desk Reference. pp. 1216-1225. Medical Economics Co. Montvale, NJ.
39. Miller R. G. Simultaneous Statistical Reference. 1966;McGraw Hill, New York.
40. Napalkov N. P., Anisimov V. N., Likhachev A. J., Tomatis L. 5-Bromodeoxyuridine-induced carcinogenesis and its modification by persistent estrus syndrome, unilateral nephrectomy, and X-irradiation in rats. Cancer Res. 49:1989;318-323.
41. Toxicology and Carcinogenesis Studies of AZT. 1996.
42. Nims R. W., Devor D. E., Henneman J. R., Lubet R. A. Induction of alkyoxyresorufin O-dealkylase, epoxide hydrase, and liver weight gain: Correlation with liver tumor-promoting potential of a series of barbiturates. Carcinogenesis. 8:1987;67-71.
43. Olivero O. A., Poirier M.C. Preferential incorporation of 3′-azido-2′,3′-dideoxythymidine into telomeric DNA and zDNA-containing regions of Chinese hamster ovary cells. Mol. Carcinog. 8:1993;81-88.
44. Olivero O. A., Beland F. A., Poirier M. C. Immunofluorescent localization and quantitation of 3′-azido-2′,3′-dideoxythymidine (AZT) incorporated into chromosomal DNA of human, hamster and mouse cell lines. Int. J. Oncol. 4:1994a;49-54.
45. Olivero O. A., Beland F. A., Fullerton N. F., Poirier M. C. Vaginal epithelial DNA damage and expression of preneoplastic markers in mice during chronic dosing with tumorigenic levels of 3′-azido-2′, 3′-dideoxythymidine. Cancer Res. 54:1994b;6235-6242.
46. Olivero O. A., Anderson L. M., Diwan B. A., Haines D. C., Harbaugh S. W., Moskal T. J., Jones A. B., Rice J. M., Riggs C. W., Logsdon D., Yuspa S. H., Poirier M. C. Transplacental effects of 3′-azido-2′,3′-dideoxythymidine (AZT): Tumorigenicity in mice and genotoxicity in mice and monkeys. J. Natl. Cancer Inst. 89:1997;1602-1608.
47. Olivero O. A., Shearer G. M., Chougnet C., Kovacs A., Patterson T. A., Binienda Z. K., Slikker W., Poirier M. C. 3′-Azido-3′ deoxythymidine (AZT) pharmacokinetics and AZT-DNA incorporation in pregnant monkeys and humans. Proc. Am. Assoc. Cancer Res. 39:1998a.
48. Olivero O. A., Pirilä R., Vähäkangas K., Poirier M. C. Placental transfer and incorporation of AZT (3′-azido-2′,3′-dideoxythymidine) into placental DNA in a human placental perfusion model. Proc. Am. Assoc. Cancer Res. 39:1998b;631.
49. Percy D. H., Jonas A. M. Incidence of spontaneous tumors in CD-1 HaM/ICR mice. J. Natl. Cancer Inst. 46:1971;1045-1065.
50. Pereira M. A., Klaunig J. E., Herren-Freund S. L., Ruch R. J. Effect of phenobarbital on the development of liver tumors in juvenile and adult mice. J. Natl. Cancer Inst. 77:1986;449-452.
51. Rao A. R., Hashim S. Chemopreventive action of Oriental food-seasoning spices mixture garam masala on DMBA-induced transplacental and translactational carcinogenesis in mice. Nutr. Cancer. 23:1995;91-101.
52. Rao G. N., Collins B. J., Giles H. D., Heath J. E., Foley J. F., May R. D., Buckley L. A. Carcinogenicity of 2′,3′-dideoxycytidine in mice. Cancer Res. 56:1996;4666-4672.
53. Schmahl W., Geber E., Lehmacher W. Diaplacental carcinogenic effects of 5-azacytidine in NMRI mice. Cancer Lett. 27:1985;81-89.
54. Seillkop S. K. The effect of body weight on tumor incidence and carcinogenicity testing in B6C3F1 mice and F344 rats. Fundam. Appl. Toxicol. 24:1995;247-259.
55. Shafik H. M., Nokta M. A., Pollard R. B. Recombinant human interferon beta serum protects against zidovudine-induced genetic damage in AIDS patients. Antiviral Res. 16:1991;205-212.
56. Shay J. W., Bacchetti S. A survey of telomerase activity in human cancer. Eur. J. Cancer. 33:1997;787-791.
57. Sperling R. S., Shapiro D. E., Coombs R. W., Todd J. A., Herman S. A., McSherry G. D., O'Sullivan M. J., Van Dyke R. B., Jimenez E., Rouzioux C., Flynn P. M., Sullivan J. L. Maternal viral load, zidovudine treatment, and the risk of transmission of human immunodeficiency virus type 1 from mother to infant. Pediatric AIDS Clinical Trials Group Protocol 076 Study Group. N. Engl. J. Med. 335:1996;1621-1629.
58. Steel R. G. D., Torrie J. H. Principles and Procedures of Statistics, A Biometrical Approach. 1980.
59. Sussman H. E., Walker V. E. Mutagenicity of AZT in the human lymphoblastoid cell line, TK6. Second National AIDS Malignancy Conference. (Abstract). J. AIDS. 17:1998;35.
60. Sutherland S., Gorski R. A. An evaluation of the inhibition of androgenization of the neonatal female rat brain by barbiturate. Neuroendocrinology. 10:1972;94-108.
61. Tapscott S. J., Lassar A., Davis R. L., Weintraub H. 5-Bromo-2′-deoxyuridine blocks myogenesis by extinguishing expression of MyoD1. Science. 245:1989;532-536.
62. Tarone R. W. Testing the goodness of fit of the binomial distribution. Biometrika. 66:1979;585-590.
63. Thomas D. G., Breslow N., Gart J. J. Trend and homogeneity analyses of proportions and life table data. Comput. Biomed. Res. 10:1977;373-381.
64. Toth B. A critical review of experiments in chemical carcinogenesis using newborn animals. Cancer Res. 28:1968;727-738.
65. Tsuchiya E., Concetti H. F., Sugano H., Kitagava T. Lack of promotion effect of phenobarbital on pulmonary tumorigenesis in ddY mice initiated by transplacental exposure to 1-ethyl-1-nitrosourea. Gann. 75:1984;305-310.
66. Morb. Mortal Wkly. Rep. 43:1994;1-20.
67. Vesselinovitch S. D., Rao K. V. N., Mihailovich N. Neoplastic responses of mouse tissues during perinatal age periods and its significance in chemical carcinogenesis. Natl. Cancer Inst. Monogr. 51:1979;239-250.
68. Ward J. M., Rice J. M., Creasia D., Lynch P., Riggs C. Dissimilar patterns of promotion by Di(2-ethylhexyl)phthalate and phenobarbital of hepatocellular neoplasia initiated by diethylnitrosamine in B6C3F1 mice. Carcinogenesis. 4:1983;1021-1029.
69. Ward J. M., Henneman J. R., Osipova G. Y., Anisimov V. N. Persistence of 5-bromo-2′-deoxyuridine in tissues of rats after exposure in early life. Toxicology. 70:1991;345-352.
70. Yaffe S. J., Dorn L. D. Effects of prenatal treatment with phenobarbital. Dev. Pharmacol. Ther. 15:1990;215-223.
71. Zhang Z., Diwan B. A., Anderson L. M., Logsdon D., Olivero O. A., Haines D. C., Rice J. M., Yuspa S. H., Poirier M. C. Skin tumorigenesis and K-ras and H-ras mutations in tumors from adult mice exposed in utero to 3′-azido-2′,3′-dideoxythymidine (AZT). Mol. Carcinog. 23:1998;45-51.