Differential carcinogenicity of cigarette smoke in mice exposed either transplacentally, early in life or in adulthood

International Journal of Cancer

Volumn 130, Issue 5, 2012, Pages 1001-1010

  Balansky, Roumen ^a,b   Ganchev, Gancho ^a   Iltcheva, Marietta ^a   Nikolov, Manasi ^a   Steele, Vernon E ^c   De Flora, Silvio ^b  

^a National Oncology Center Bulgaria   (Bulgaria)

^b UNIVERSITY OF GENOA   (Italy)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

carcinogenicity in adult mice; cigarette smoke; neonatal carcinogenesis; transplacental carcinogenesis

Indexed keywords

ADULT ANIMAL; ADULTHOOD; AGE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL; BRONCHUS MUCOSA; CARCINOGENICITY; CELL HYPERPLASIA; CELL PROLIFERATION; CIGARETTE SMOKING; COMPARATIVE STUDY; CONTROLLED STUDY; DEGENERATION; FEMALE; HEMANGIOMA; HISTOPATHOLOGY; KIDNEY DISEASE; LIVER DISEASE; LIVER PARENCHYMA; LUNG ADENOMA; LUNG ALVEOLUS EPITHELIUM; LUNG CANCER; LUNG EMPHYSEMA; MALE; MICROADENOMA; MOUSE; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRENATAL EXPOSURE; PRENATAL PERIOD; PRIORITY JOURNAL; PROGENY;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BODY WEIGHT; CARCINOGENS; FEMALE; HUMANS; LUNG DISEASES; LUNG NEOPLASMS; MALE; MATERNAL-FETAL EXCHANGE; MICE; PREGNANCY; SURVIVAL ANALYSIS; TOBACCO SMOKE POLLUTION;

EID: 84155168014     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.26103     Document Type: Article

References (50)

1. International Agency for Research on Cancer. Tobacco smoke and involuntary smoking. IARC monographs on the evaluation of the carcinogenic risks to humans, vol. 83. Lyon: IARC, 2004.
2. US Department of Health and Human Services. Reducing the health consequences of smoking, 25 years of progress. Office on Smoking and Health, DHSS Publication, No. CDC-89-8411. Washington, DC: Government Printing Office, 1989. 43-54.
3. Hecht SS,. Tobacco smoke carcinogens and lung cancer. J Natl Cancer Inst 1999; 91: 1194-210. (Pubitemid 29357186)
4. Mertens VE,. Zigarettenrauch, eine Ursache des Lungenkrebses. Z Krebsforsch 1930; 32: 82.
5. Coggins CR,. A minireview of chronic animal inhalation studies with mainstream cigarette smoke. Inhal Toxicol 2002; 14: 991-1002. (Pubitemid 35230746)
6. Hecht SS,. Carcinogenicity studies of inhaled cigarette smoke in laboratory animals: old and new. Carcinogenesis 2005; 26: 1488-92. (Pubitemid 41236041)
7. De Flora S, D'Agostini F, Balansky R, Camoirano A, Bennicelli C, Bagnasco M, Cartiglia C, Tampa E, Longobardi MG, Lubet RA, Izzotti A,. Modulation of cigarette smoke-related end-points in mutagenesis and carcinogenesis. Mutat Res 2003; 523/524: 237-52. (Pubitemid 36293251)
8. De Flora S, D'Agostini F, Izzotti A, Zanesi N, Croce C, Balansky R,. Molecular and cytogenetical alterations induced by environmental cigarette smoke in mice heterozygous for Fhit. Cancer Res 2007; 67: 1001-6.
9. Izzotti A, Bagnasco M, Cartiglia C, Longobardi M, Balansky RM, Merello A, Lubet RA, De Flora S,. Chemoprevention of genome, transcriptome, and proteome alterations induced by cigarette smoke in rat lung. Eur J Cancer 2005; 41: 1864-74. (Pubitemid 41557674)
10. Izzotti A, Calin GA, Arrigo P, Steele VE, Croce CM, De Flora S,. Downregulation of microRNA expression in the lungs of rats exposed to cigarette smoke. FASEB J 2009; 23: 806-12.
11. Witschi H,. The complexities of an apparently simple lung tumor model: the A/J mouse. Exp Toxicol Pathol 2005; 57 (Suppl 1): 171-81. (Pubitemid 40884490)
12. Witschi H, Espiritu I, Peake JL, Wu K, Maronpot RR, Pinkerton KE,. The carcinogenicity of environmental tobacco smoke. Carcinogenesis 1997; 18: 575-86. (Pubitemid 28132497)
13. D'Agostini F, Balansky RM, Bennicelli C, Lubet RA, Kelloff GJ, De Flora S,. Pilot studies evaluating the lung tumor yield in cigarette smoke-exposed mice. Int J Oncol 2001; 18: 607-15.
14. Curtin GM, Higuchi MA, Ayres PH, Swauger JE, Mosberg AT,. Lung tumorigenicity in A/J and rasH2 transgenic mice following mainstream tobacco smoke inhalation. Toxicol Sci 2004; 81: 26-34. (Pubitemid 39199860)
15. Stinn W, Teredesai A, Kuhl P, Knorr-Wittmann C, Kindt R, Coggins C, Haussmann HJ,. Mechanisms involved in A/J mouse lung tumorigenesis induced by inhalation of an environmental tobacco smoke surrogate. Inhal Toxicol 2005; 17: 263-76. (Pubitemid 40563308)
16. De Flora S, Balansky RM, D'Agostini F, Izzotti A, Camoirano A, Bennicelli C, Zhang Z, Wang Y, Lubet RA, You M,. Molecular alterations and lung tumors in p53 mutant mice exposed to cigarette smoke. Cancer Res 2003; 63: 793-800. (Pubitemid 36231978)
17. Wang Y, Zhang Z, Lubet R, You M,. Tobacco smoke-induced lung tumorigenesis in mutant A/J mice with alterations in K-ras, p53, or Ink4a/Arf. Oncogene 2005; 24: 3042-9. (Pubitemid 40675535)
18. Witschi H, Espiritu I, Maronpot RR, Pinkerton KE, Jones AD,. The carcinogenic potential of the gas phase of environmental tobacco smoke. Carcinogenesis 1997; 18: 2035-42. (Pubitemid 28134726)
19. Stinn W, Arts JHE, Buettner A, Duistermaat E, Janssens K, Kuper CF, Haussmann H-J,. Murine lung tumor response after exposure to cigarette mainstream smoke or its particulate and gas/vapor phase fractions. Toxicology 2010; 275: 10-20.
20. Mauderly JL, Gigliotti AP, Barr EB, Bechtold WE, Belinsky SA, Hahn FF, Hobbs CA, March TH, Seilkop SK, Finch GL,. Chronic inhalation exposure to mainstream cigarette smoke increases lung and nasal tumor incidence in rats. Toxicol Sci 2004; 81: 280-92. (Pubitemid 39377958)
21. Hutt JA, Vuillemenot BR, Barr EB, Grimes MJ, Hahn FF, Hobbs CH, March TH, Gigliotti AP, Seilkop SK, Finch GL, Mauderly JL, Belinsky SA,. Life-span inhalation exposure to mainstream cigarette smoke induces lung cancer in B6C3F1 mice through genetic and epigenetic pathways. Carcinogenesis 2005; 26: 1999-2009. (Pubitemid 41631274)
22. Izzotti A, Balansky RM, Camoirano A, Cartiglia C, Longobardi M, Tampa E, De Flora S,. Birth-related genomic and transcriptional changes in mouse lung. Modulation by transplacental N-acetylcysteine. Mutat Res 2003; 544: 441-9. (Pubitemid 37487687)
23. Balansky R, Ganchev G, Iltcheva M, Steele VE, D'Agostini F, De Flora S,. Potent carcinogenicity of cigarette smoke in mice exposed early in life. Carcinogenesis 2007; 28: 2236-43. (Pubitemid 47543386)
24. Balansky R, Ganchev G, Iltcheva M, Steele VE, De Flora S,. Prenatal N-acetylcysteine prevents cigarette smoke-induced lung cancer in neonatal mice. Carcinogenesis 2009; 30: 1398-401.
25. Balansky R, Ganchev G, Iltcheva M, Steele VE, De Flora S,. Prevention of cigarette smoke-induced lung cancer in mice by budesonide, phenethyl isothiocyanate, and N-acetylcysteine. Int J Cancer 2009; 126: 1047-54.
26. D'Agostini F, Balansky R, Steele VE, Ganchev G, Pesce C, De Flora S,. Preneoplastic and neoplastic lesions in the lung, liver, and urinary tract of mice exposed to environmental cigarette smoke and UV light since birth. Int J Cancer 2008; 123: 2497-502.
27. Shimkin MB, Stoner GD,. The genetic basis of susceptibility to lung tumors in mice. Adv Cancer Res 1975; 21: 1-56.
28. Balansky R, Blagoeva PM, Mircheva ZI,. Investigation of the mutagenic activity of tobacco smoke. Mutat Res 1987; 188: 13-19.
29. Barker DJP,. Maternal nutrition, fetal nutrition, and diseases in later life. Nutrition 1997; 13: 807-13.
30. Anderson LM,. Introduction and overview. Perinatal carcinogenesis: growing a node for epidemiology, risk management, and animal studies. Toxicol Appl Pharmacol 2004; 199: 85-90. (Pubitemid 39094527)
31. Winterhalder RC, Hirsch FR, Kotantoulas GK, Franklin WA, Bunn PA, Jr., Chemoprevention of lung cancer-from biology to clinical reality. Ann Oncol 2004; 15: 185-96. (Pubitemid 38262613)
32. De Flora S, D'Agostini F, Balansky R, Camoirano A, Cartiglia C, Longobardi M, Travaini G, Steele VE, Pesce C, Izzotti A,. High susceptibility of neonatal mice to molecular, biochemical and cytogenetical alterations induced by environmental cigarette smoke and light. Mutat Res Rev 2008; 659: 137-46.
33. Yee M, Vitiello PF, Roper JM, Staversky RJ, Wright TW, McGrath-Morrow SA, Maniscalco WM, Finkelstein JN, O'Reilly MA,. Type II epithelial cells are critical target for hyperoxia-mediated impairment of postnatal lung development. Am J Physiol Lung Cell Mol Physiol 2006; 291: L1101-L1111. (Pubitemid 44772072)
34. Foster JJ, Goss KL, George CL, Bangsund PJ, Snyder JM,. Galectin-1 in secondary alveolar septae of neonatal mouse lung. Am J Physiol Lung Cell Mol Physiol 2006; 291: L1142-L1149. (Pubitemid 44904520)
35. Shupe T, Sell S,. Low hepatic glutathione S-transferase and increased hepatic DNA adduction contribute to increased tumorigenicity of aflatoxin B1 in newborn and partially hepatectomized mice. Toxicol Lett 2004; 148: 1-9. (Pubitemid 38264517)
36. Coccia P, Salmona M, Diomede L, Citti L, Mariani L, Romano M,. Liver DNA alkylation after a single carcinogenic dose of dimethylnitrosamine to newborn and adult CFW Swiss mice. Chem Biol Interact 1988; 68: 259-71. (Pubitemid 19012624)
37. Singh SP, Razani-Boroujerdi S, Pena-Philippides JC, Langley RJ, Mishra NC, Sopori ML,. Early postnatal exposure to cigarette smoke impairs the antigen-specific T-cell responses in the spleen. Toxicol Lett 2006; 167: 231-7. (Pubitemid 44780052)
38. O'Donnell EP, Zerbe LK, Dwyer-Nield LD, Kisley LR, Malkinson AM,. Quantitative analysis of early chemically induced pulmonary lesions in mice of varying susceptibilities to lung tumorigenesis. Cancer Lett 2006; 241: 197-202. (Pubitemid 44163033)
39. Anderson LM, Ruskie S, Carter J, Pittinger S, Kovatch RM, Riggs CW,. Fetal mouse susceptibility to transplacental carcinogenesis: differential influence of Ah receptor phenotype on effects of 3-methylcholanthrene, 12-dimethylbenz[a]anthracene, and benzo[a]pyrene. Pharmacogenetics 1995; 5: 364-72. (Pubitemid 26011442)
40. Miller MS, Gressani KM, Leone-Kabler S, Townsend AJ, Malkinson AM, O'Sullivan MG,. Differential sensitivity to lung tumorigenesis following transplacental exposure of mice to polycyclic hydrocarbons, heterocyclic amines, and lung tumor promoters. Exp Lung Res 2000; 26: 709-30. (Pubitemid 32044587)
41. Beebe LE, Kim YE, Amin S, Riggs CW, Kovatch RM, Anderson LM,. Comparison of transplacental and neonatal initiation of mouse lung and liver tumors by N-nitrosodimethylamine (NDMA) and 4-(methylnitrosamino)-1-(3-pyridyl)-1- butanone (NNK) and promotability by a polychlorinated biphenyls mixture (Aroclor 1254). Carcinogenesis 1993; 14: 1545-8. (Pubitemid 23249356)
42. Umezawa I, Komiyama K, Kawakubo Y, Nishiyama Y, Hata T,. Tumor development in lung of ddY mice following transplacental exposure to 1-ethyl-1-nitrosourea. Gann 1979; 70: 379-82. (Pubitemid 9243958)
43. Anderson LM,. Two crops of primary lung tumors in BALB/c mice after a single transplacental exposure to urethane. Cancer Lett 1978; 5: 55-9. (Pubitemid 8397834)
44. Maekawa A, Onodera H, Furuta K, Odashima S,. Transplacental and neonatal carcinogenesis by 1-butyl-1-nitrosourethan in the ACI/N rat. Gann 1980; 71: 811-15. (Pubitemid 11130560)
45. Balansky RM, Blagoeva PM,. Tobacco smoke-induced clastogenicity in mouse fetuses and in newborn mice. Mutat Res 1989; 223: 1-6. (Pubitemid 19130693)
46. Miller MS,. Transplacental lung carcinogenesis: molecular mechanisms and pathogenesis. Toxicol Appl Pharmacol 2004; 198: 95-110. (Pubitemid 38952831)
47. Izzotti A, Balansky RM, Cartiglia C, Camoirano A, Longobardi M, De Flora S,. Genomic and transcriptional alterations in mouse fetus liver after transplacental exposure to cigarette smoke. FASEB J 2003; 17: 1127-9.
48. Likhacev AJ,. Blastomogenesis induced by the combined tranplacental and postnatal exposure to N-nitrosodiethylamine (NDEA) in mice. Vopr Onkol 1971; 17: 64-9 (in Russian).
49. Anderson LM, Jones AB, Miller MS, Chauhan DP,. Metabolism of transplacental carcinogens. In:, Napalkov NP, Rice JM, Tomatis L, Yamasaki H, eds. Transplacental and multigenerational carcinogenesis. Lyon, France: IARC Sci Publ, 1983; 155-188.
50. Brown BG, Richter E, Tricker AR, Ayres PH, Doolittle DJ,. The effect of a 2-h exposure to cigarette smoke on the metabolic activation of the tobacco-specific nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl)-1- butanone in A/J mice. Chem Biol Interact 2001; 138: 125-35. (Pubitemid 32973847)