Effects of prenatal exposure to cigarette smoke on offspring tumor susceptibility and associated immune mechanisms

Toxicological Sciences

Volumn 89, Issue 1, 2006, Pages 135-144

  Ng, Sheung P ^a   Silverstone, Allen E ^b   Lai, Zhi Wei ^b   Zelikoff, Judith T ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

Cigarette smoke; Developmental immunotoxicology; Tumor surveillance mechanisms

Indexed keywords

CIGARETTE SMOKE; CYTOKINE;

AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INCIDENCE; CANCER RISK; CANCER SUSCEPTIBILITY; CELL ACTIVITY; CELL SUBPOPULATION; CIGARETTE SMOKING; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; ENVIRONMENTAL EXPOSURE; FEMALE; GENDER; GESTATIONAL AGE; HISTOPATHOLOGY; HOST RESISTANCE; IMMUNOCOMPETENT CELL; IMMUNOTOXICITY; LYMPHOID ORGAN; MALE; MALIGNANT NEOPLASTIC DISEASE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRENATAL EXPOSURE; RISK ASSESSMENT; SMOKING HABIT; TUMOR CELL;

ANIMALS; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; FEMALE; INHALATION EXPOSURE; LYMPHOID TISSUE; LYMPHOMA, T-CELL; MALE; MATERNAL EXPOSURE; MICE; MICE, INBRED STRAINS; NEOPLASM TRANSPLANTATION; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SPLEEN; T-LYMPHOCYTES, CYTOTOXIC; THYMUS GLAND; TOBACCO SMOKE POLLUTION;

ANIMALIA;

EID: 29544445384     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfj006     Document Type: Article

References (40)

1. ACOG (American College of Obstetricians and Gynecologists). (1994). Substance abuse in pregnancy. ACOG Technical Bulletin No. 195.
2. Andres, R. L., and Day, M. C. (2000). Perinatal complications associated with maternal tobacco use. Semin. Neonatol. 5, 231-241.
3. Anichini, A., and Mortarini, R. (2002). Cellular recognition of tumors by T and NK cells. In Tumor Immunology (G. Parmiani and M. T. Lotze, Eds.), pp. 77-98. Taylor and Francis, New York.
4. Basta, P. V., Basham, K. B., Ross, W. P., Brust, M. E., and Navarro, H. A. (2000). Gestational nicotine exposure alone or in combination with ethanol down-modulates offspring immune function. Int. J. Immunopharmacol. 22, 159-169.
5. Braun, K. M., Cornish, T., Valm, A., Cundiff, J., Pauly, J. L., and Fan, S. (1998). Immunotoxicology of cigarette smoke condensates: Suppression of macrophage responsiveness to interferon gamma. Toxicol. Appl. Pharmacol. 149, 136-143.
6. Byrd, R. S., and Howard, C. R. (1995). Children's passive and prenatal exposure to cigarette smoke. Pediatr. Ann. 24, 640-645.
7. Cederqvist, L. L., Eddey, G., Abdel-Latif, N., and Litwin, S. D. (1984). The effect of smoking during pregnancy on cord blood and maternal serum immunoglobulin levels. Am. J. Obstet. Gynecol. 148, 1123-1126.
8. Chalmer, J., Holt, P. G., and Keast, D. (1975). Cell-mediated immune responses to transplanted tumors in mice chronically exposed to cigarette smoke. J. Natl. Cancer Inst. 55, 1129-1134.
9. Corti, M., and Snyder, C. A. (1998). Gender- and age-specific cytotoxic susceptibility to benzene metabolites in vitro. Toxicol. Sci. 41, 42-48.
10. DeMarini, D. M. (2004). Genotoxicity of tobacco smoke and tobacco smoke condensate: A review. Mutat. Res. 567, 447-474.
11. Dempsey, D. A., and Benowitz, N. L. (2001). Risks and benefits of nicotine to aid smoking cessation in pregnancy. Drug Safety 24, 277-322.
12. Djeu, J. Y. (1995). Natural killer activity. In Methods in Immunotoxicology, Vol 1 (G. R. Burlesson, J. H. Dean, and A. E. Munson, Eds.), pp. 437-50. Wiley-Liss, New York.
13. Filippini, G., Farinotti, M., Lovicu, G., Maisonneuve, P., and Boyle, P. (1994). Mothers' active and passive smoking during pregnancy and risk of brain tumours in children. Int. J. Cancer 57, 769-774.
14. Filippini, G., Farinotti, M., and Ferrarini, M. (2000). Active and passive smoking during pregnancy and risk of central nervous system tumours in children. Paediatr. Perinat. Epidemiol. 14, 78-84.
15. Finette, B. A., O'Neill, J. P., Vacek, P. M., and Albertini, R. J. (1998). Gene mutations with characteristic deletions in cord blood T lymphocytes associated with passive maternal exposure to tobacco smoke. Nat. Med. 4, 1144-1151.
16. Fukuda, M., Fukuda, K., Shimizu, T., Andersen, C. Y., and Byskov, A. G. (2002). Parental periconceptional smoking and male:fEmale ratio of newborn infants. Lancet 359, 1407-1408.
17. Ho, R. L., Maccubbin, D. L., Ujhazy, P., Zaleskis, G., Eppolito, C., Mihich, E., and Ehrke, M. J. (1993). Immunological responses critical to the therapeutic effects of Adriamycin plus interleukin 2 in C57BL/6 mice bearing syngeneic EL4 lymphoma. Oncol. Res. 5, 363-372.
18. House, R. V., and Thomas, P. T. (1995). In vitro induction of cytotoxic T lymphocytes. In Methods in Immunotoxicology, Vol 1 (G. R. Burleson, J. H. Dean, and A. E. Munson, Eds.), pp. 159-72, Wiley-Liss, New York.
19. IARC (International Agency for Research on Cancer). (2004). Monographs on the Evaluation of Carcinogenic Risk of Chemicals to Humans, Vol. 83, Tobacco Smoke and Involuntary Smoking. IARC, Lyon, France.
20. Ikeda, M., Tamura, M., Yamashita, J., Suzuki, C., and Tomita, T. (2005). Repeated in utero and lactational 2,3,7, 8-tetrachlorodibenzo-p-dioxin exposure affects male gonads in offspring, leading to sex ratio changes in F(2) progeny. Toxicol. Appl. Pharmacol. 206, 351-355.
21. Johnson, J. D., Houchens, D. P., Kluwe, W. M., Craig, D. K., and Fisher, G. L. (1990). Effects of mainstream and environmental tobacco smoke on the immune system in animals and humans: A review. Crit Rev. Toxicol. 20, 369-395.
22. Kalra, R., Singh, S. P., Savage, S. M., Finch, G. L., and Sopori, M. L. (2000). Effects of cigarette smoke on immune response: Chronic exposure to cigarette smoke impairs antigen-mediated signaling in T cells and depletes IP3-sensitive Ca(2+) stores. J. Pharmacol. Exp. Ther. 293, 166-171.
23. Kalra, R., Singh, S. P., Pena-Philippides, J. C., Langley, R. J., Razani-Boroujerdi, S., and Sopori M. L. (2004). Immunosuppressive and anti-inflammatory effects of nicotine administered by patch in an animal model. Clin. Diagn. Lab. Immunol. 11, 563-568.
24. Maccubbin, D. L., Mace, K. F., Ehrke, M. J., and Mihich, E. (1989). Modification of host antitumor defense mechanisms in mice by progressively growing tumor. Cancer Res. 49, 4216-4224.
25. Magnani, C., Pastore, G., Luzzatto, L., and Terracini, B. (1990). Parental occupation and other environmental factors in the etiology of leukemias and non-Hodgkin's lymphomas in childhood: A case-control study. Tumori 76, 413-419.
26. McAllister-Sistilli, C. G., Caggiula, A. R., Knopf, S., Rose, C. A., Miller, A. L., and Donny, E. C. (1998). The effects of nicotine on the immune system. Psychoneuroendocrinology 23, 175-187.
27. Mercelina-Roumans, P. E., Breukers, R. B., Ubachs, J. M., and van Wersch, J. W. (1996). Hematological variables in cord blood of neonates of smoking and nonsmoking mothers. J. Clin. Epidemiol. 49, 449-454.
28. Pauly, J. R., Sparks, J. A., Hauser, K. F., and Pauly, T. H. (2004). In utero nicotine exposure causes persistent, sex-dependant changes in locomotor activity and sensitivity to nicotine in C57B1/6 mice. Int. J. Dev. Neurosci. 22, 329-337.
29. Perera, F. P., Tang, D., Tu, Y. H., Cruz, L. A., Borjas, M., Bernert, T., and Whyatt, R. M. (2004). Biomarkers in maternal and newborn blood indicate heightened fetal susceptibility to procarcinogenic DNA damage. Environ. Health Perspect. 112, 1133-1136.
30. Pichini, S., Basagana, X. B., Pacifici, R., Garcia, O., Puig, C., Vall, O., Harris, J., Zuccaro, P., Segura, J., and Sunyer, J. (2000). Cord serum cotinine as a biomarker of fetal exposure to cigarette smoke at the end of pregnancy. Environ. Health. Perspect. 108, 1079-1083.
31. Rodriguez, J. W., Kohan, M. J., King, L. C., and Kirlin, W. G. (2002). Detection of DNA adducts in developing CD4+ CD8+ thymocytes and splenocytes following in utero exposure to benzo[a]pyrene. Immunopharmacol. Immunotoxicol. 24, 365-381.
32. Ryan, J. J., Amirova, Z., and Carrier, G. (2002). Sex ratios of children of Russian pesticide producers exposed to dioxin. Environ. Health Perspect. 110, A699-A701.
33. Sasco, A. J., and Vainio, H. (1999). From in utero and childhood exposure to parental smoking to childhood cancer: A possible link and the need for action. Hum. Exp. Toxicol. 18, 192-201.
34. Schuz, J., Kaletsch, U., Kaatsch, P., Meinert, R., and Michaelis, J. (2001). Risk factors for pediatric tumors of the central nervous system: Results from a German population-based case-control study. Med. Pediatr. Oncol. 36, 274-282.
35. Shimizu, J., Yamazaki, S., and Sakaguchi, S. (1999). Induction of tumor immunity by removing CD25+CD4+ T cells: A common basis between tumor immunity and autoimmunity. J. Immunol. 163, 5211-5218.
36. Sopori, M. L., and Kozak, W. (1998). Immunomodulatory effects of cigarette smoke. J. Neuroimmunol. 83, 148-156.
37. Sopori, M. (2002). Effects of cigarette smoke on the immune system. Nat. Rev. Immunol. 2, 372-377.
38. Urso, P., and Gengozian, N. (1984). Subnormal expression of cell-mediated and humoral immune responses in progeny disposed toward a high incidence of tumors after in utero exposure to benzo[a]pyrene. J. Toxicol. Environ. Health 14, 569-584.
39. Ward, E. C., Murray, M. J., Lauer, L. D., House, R. V., and Dean, J. H. (1986). Persistent suppression of humoral and cell-mediated immunity in mice following exposure to the polycyclic aromatic hydrocarbon 7,12-dimethylbenz[a]anthracene. Int. J. Immunopharmacol. 8, 13-22.
40. Yang, Z., Knight, C. A., Mamerow, M. M., Vickers, K., Penn, A., Postlethwait, E. M., and Ballinger, S. W. (2004). Prenatal environmental tobacco smoke exposure promotes adult atherogenesis and mitochondrial damage in apolipoprotein E-/- mice fed a chow diet. Circulation 110, 3715-3720.