A global toxicogenomic analysis investigating the mechanistic differences between tobacco and marijuana smoke condensates in vitro

Toxicology

Volumn 308, Issue , 2013, Pages 60-73

  Maertens, Rebecca M ^a   White, Paul A ^a   Williams, Andrew ^a   Yauk, Carole L ^a  

^a Health Canada   (Canada)

Author keywords

Gene expression; Marijuana; Pathway analysis; Smoke condensate; Tobacco; Toxicology

Indexed keywords

CANNABIS; CIGARETTE SMOKE CONDENSATE; DNA; RNA; TOBACCO SMOKE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANNABIS SMOKING; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; GENOME; IN VITRO STUDY; INFLAMMATION; LUNG ALVEOLUS EPITHELIUM; M PHASE CELL CYCLE CHECKPOINT; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RNA EXTRACTION; SMOKING; STEROIDOGENESIS; TOBACCO; TOXICOGENETICS; XENOBIOTIC METABOLISM;

ANIMALS; CANNABIS; CELL LINE; GENE EXPRESSION PROFILING; MICE; RESPIRATORY MUCOSA; SMOKE; TOBACCO; TOBACCO PRODUCTS; TOXICOGENETICS;

CANNABIS SATIVA; MURINAE; NICOTIANA TABACUM;

EID: 84876715001     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2013.03.008     Document Type: Article

References (78)

1. Adam T., McAughey J., Mocker C., McGrath C., Zimmermann R. Influence of filter ventilation on the chemical composition of cigarette mainstream smoke. Anal. Chim. Acta 2010, 657:36-44.
2. Ahrendt S.A., Decker P.A., Alawi E.A., Zhu Yr Y.R., Sanchez-Cespedes M., Yang S.C., Haasler G.B., Kajdacsy-Balla A., Demeure M.J., Sidransky D. Cigarette smoking is strongly associated with mutation of the K-ras gene in patients with primary adenocarcinoma of the lung. Cancer 2001, 92:1525-1530.
3. Aldington S., Williams M., Nowitz M., Weatherall M., Pritchard A., McNaughton A., Robinson G., Beasley R. The effects of cannabis on pulmonary structure, function and symptoms. Thorax 2007, 62:1058-1063.
4. Aldington S., Harwood M., Cox B., Weatherall M., Beckert L., Hansell A., Pritchard A., Robinson G., Beasley R. Cannabis use and risk of lung cancer: a case-control study. Eur. Respir. J. 2008, 31:280-286.
5. Ammenheuser M.M., Berenson A.B., Babiak A.E., Singleton C.R., Whorton E.B. Frequencies of hprt mutant lymphocytes in marijuana-smoking mothers and their newborns. Mutat. Res. 1998, 403:55-64.
6. Amundson S.A., Myers T.G., Fornace A.J. Roles for p53 in growth arrest and apoptosis: putting on the brakes after genotoxic stress. Oncogene 1998, 17:3287-3299.
7. Baldwin G.C., Tashkin D.P., Buckley D.M., Park A.N., Dubinett S.M., Roth M.D. Marijuana and cocaine impair alveolar macrophage function and cytokine production. Am. J. Respir. Crit. Care Med. 1997, 156:1606-1613.
8. Bartsch H., Petruzzelli S., De Flora S., Hietanen E., Camus A.M., Castegnaro M., Alexandrov K., Rojas M., Saracci R., Giuntini C. Carcinogen metabolism in human lung tissues and the effect of tobacco smoking: results from a case-control multicenter study on lung cancer patients. Environ. Health Perspect. 1992, 98:119-124.
9. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 1995, 57:289-300.
10. Berndt-Weis M.L., Kauri L.M., Williams A., White P., Douglas G., Yauk C. Global transcriptional characterization of a mouse pulmonary epithelial cell line for use in genetic toxicology. Toxicol. In Vitro 2009, 23:816-833.
11. Bosio A., Knorr C., Janssen U., Gebel S., Haussmann H.J., Muller T. Kinetics of gene expression profiling in Swiss 3T3 cells exposed to aqueous extracts of cigarette smoke. Carcinogenesis 2002, 23:741-748.
12. Burstein S., Hunter S.A., Shoupe T.S., Taylor P. Cannabinoid inhibition of testosterone synthesis by mouse Leydig cells. Res. Commun. Chem. Pathol. Pharmacol. 1978, 19:557-560.
13. Burstein S., Hunter S.A., Shoupe T.S. Cannabinoid inhibition of rat luteal cell progesterone synthesis. Res. Commun. Chem. Pathol. Pharmacol. 1979, 24:413-416.
14. Busch F.W., Seid D.A., Wei E.T. Mutagenic activity of marihuana smoke condensates. Cancer Lett. 1979, 6:319-324.
15. Chiesara E., Cutrufello R., Rizzi R. Chromosome damage in heroin-marijuana and marijuana addicts. Arch. Toxicol. Suppl. 1983, 6:128-130.
16. Comandini A., Marzano V., Curradi G., Federici G., Urbani A., Saltini C. Markers of anti-oxidant response in tobacco smoke exposed subjects: a data-mining review. Pulm. Pharmacol. Ther. 2010, 23:482-492.
17. Cornicelli J.A., Gilman S.R., Krom B.A., Kottke B.A. Cannabinoids impair the formation of cholesteryl ester in cultured human cells. Arteriosclerosis 1981, 1:449-454.
18. Cui X., Hwang J.T., Qiu J., Blades N.J., Churchill G.A. Improved statistical tests for differential gene expression by shrinking variance components estimates. Biostatistics 2005, 6:59-75.
19. Dennis G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., Lempicki R.A. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 2003, 4:P3.
20. R Development CoreTeam R: A language and environment for statistical computing 2005, Foundation for Statistical Computing, Vienna, Austria.
21. Fields W.R., Leonard R.M., Odom P.S., Nordskog B.K., Ogden M.W., Doolittle D.J. Gene expression in normal human bronchial epithelial (NHBE) cells following in vitro exposure to cigarette smoke condensate. Toxicol. Sci. 2005, 86:84-91.
22. -/- mice provides evidence for impaired cell cycle progression in the development of cigarette smoke-induced emphysematous changes. Toxicol. Sci. 2010, 115:238-252.
23. Goodnight, J.H., Harvey, W.R., 1978. SAS Technical Report R-103: Least-Squares Means in the Fixed-Effects General Linear Models. SAS Institute Inc., Cary, NC.
24. Hart S., Fischer O.M., Ullrich A. Cannabinoids induce cancer cell proliferation via tumor necrosis factor alpha-converting enzyme (TACE/ADAM17)-mediated transactivation of the epidermal growth factor receptor. Cancer Res. 2004, 64:1943-1950.
25. Hashibe M., Morgenstern H., Cui Y., Tashkin D.P., Zhang Z.F., Cozen W., Mack T.M., Greenland S. Marijuana use and the risk of lung and upper aerodigestive tract cancers: results of a population-based case-control study. Cancer Epidemiol. Biomarkers Prev. 2006, 15:1829-1834.
26. Iizuka T., Ishii Y., Itoh K., Kiwamoto T., Kimura T., Matsuno Y., Morishima Y., Hegab A.E., Homma S., Nomura A., Sakamoto T., Shimura M., Yoshida A., Yamamoto M., Sekizawa K. Nrf2-deficient mice are highly susceptible to cigarette smoke-induced emphysema. Genes Cells 2005, 10:1113-1125.
27. Ingenuity Systems, 2012. Ingenuity Pathway Analysis, , Redwood City, California. http://www.ingenuity.com/.
28. Jorgensen E.D., Dozmorov I., Frank M.B., Centola M., Albino A.P. Global gene expression analysis of human bronchial epithelial cells treated with tobacco condensates. Cell Cycle 2004, 3:1154-1168.
29. Kensler T.W., Wakabayashi N., Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 2007, 47:89-116.
30. Kerr M.K. Design considerations for efficient and effective microarray studies. Biometrics 2003, 59:822-828.
31. Kerr M.K., Churchill G.A. Statistical design and the analysis of gene expression microarray data. Genet. Res. 2001, 77:123-128.
32. Lee M.H., Hancox R.J. Effects of smoking cannabis on lung function. Expert Rev. Respir. Med. 2011, 5:537-547.
33. Lee S.Y., Oh S.M., Lee S.K., Chung K.H. Antiestrogenic effects of marijuana smoke condensate and cannabinoid compounds. Arch. Pharm. Res. 2005, 28:1365-1375.
34. Lee S.Y., Oh S.M., Chung K.H. Estrogenic effects of marijuana smoke condensate and cannabinoid compounds. Toxicol. Appl. Pharmacol. 2006, 214:270-278.
35. Leuchtenberger C., Leuchtenberger R., Ritter U., Inui N. Effects of marijuana and tobacco smoke on DNA and chromosomal complement in human lung explants. Nature 1973, 242:403-404.
36. Lu B., Kerepesi L., Wisse L., Hitchman K., Meng Q.R. Cytotoxicity and gene expression profiles in cell cultures exposed to whole smoke from three types of cigarettes. Toxicol. Sci. 2007, 98:469-478.
37. Maertens R.M., White P.A., Rickert W., Levasseur G., Douglas G.R., Bellier P.V., McNamee J.P., Thuppal V., Walker M., Desjardins S. The genotoxicity of mainstream and sidestream marijuana and tobacco smoke condensates. Chem. Res. Toxicol. 2009, 22:1406-1414.
38. Massi P., Vaccani A., Parolaro D. Cannabinoids, immune system and cytokine network. Curr. Pharm. Des. 2006, 12:3135-3146.
39. Maunders H., Patwardhan S., Phillips J., Clack A., Richter A. Human bronchial epithelial cell transcriptome: gene expression changes following acute exposure to whole cigarette smoke in vitro. Am. J. Physiol. Lung Cell Mol. Physiol. 2007, 292:L1248-L1256.
40. Moir D., Rickert W.S., Levasseur G., Larose Y., Maertens R., White P., Desjardins S. A comparison of mainstream and sidestream marijuana and tobacco cigarette smoke produced under two machine smoking conditions. Chem. Res. Toxicol. 2008, 21:494-502.
41. Nagaraj N.S., Beckers S., Mensah J.K., Waigel S., Vigneswaran N., Zacharias W. Cigarette smoke condensate induces cytochromes P450 and aldo-keto reductases in oral cancer cells. Toxicol. Lett. 2006, 165:182-194.
42. Nordskog B.K., Blixt A.D., Morgan W.T., Fields W.R., Hellmann G.M. Matrix-degrading and pro-inflammatory changes in human vascular endothelial cells exposed to cigarette smoke condensate. Cardiovasc. Toxicol. 2003, 3:101-117.
43. O'Connor R.J., Hurley P.J. Existing technologies to reduce specific toxicant emissions in cigarette smoke. Tob. Control 2008, 17(Suppl. 1):i39L 48.
44. Pfaffl M.W., Horgan G.W., Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002, 30:e36.
45. Pickett G., Seagrave J., Boggs S., Polzin G., Richter P., Tesfaigzi Y. Effects of 10 cigarette smoke condensates on primary human airway epithelial cells by comparative gene and cytokine expression studies. Toxicol. Sci. 2010, 114:79-89.
46. Pinot F., el Yaagoubi A., Christie P., Dinh-Xuan A.T., Polla B.S. Induction of stress proteins by tobacco smoke in human monocytes: modulation by antioxidants. Cell Stress Chaperones 1997, 2:156-161.
47. Rangasamy T., Cho C.Y., Thimmulappa R.K., Zhen L., Srisuma S.S., Kensler T.W., Yamamoto M., Petrache I., Tuder R.M., Biswal S. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J. Clin. Invest. 2004, 114:1248-1259.
48. Rickert W.S., Trivedi A.H., Momin R.A., Wright W.G., Lauterbach J.H. Effect of smoking conditions and methods of collection on the mutagenicity and cytotoxicity of cigarette mainstream smoke. Toxicol. Sci. 2007, 96:285-293.
49. Rieder S.A., Chauhan A., Singh U., Nagarkatti M., Nagarkatti P. Cannabinoid-induced apoptosis in immune cells as a pathway to immunosuppression. Immunobiology 2010, 215:598-605.
50. Rimmerman N., Juknat A., Kozela E., Levy R., Bradshaw H.B., Vogel Z. The non-psychoactive plant cannabinoid, cannabidiol affects cholesterol metabolism-related genes in microglial cells. Cell. Mol. Neurobiol. 2011, 31:921-930.
51. Roth M.D., Arora A., Barsky S.H., Kleerup E.C., Simmons M., Tashkin D.P. Airway inflammation in young marijuana and tobacco smokers. Am. J. Respir. Crit. Care Med. 1998, 157:928-937.
52. Roth M.D., Marques-Magallanes J.A., Yuan M., Sun W., Tashkin D.P., Hankinson O. Induction and regulation of the carcinogen-metabolizing enzyme CYP1A1 by marijuana smoke and delta (9)-tetrahydrocannabinol. Am. J. Respir. Cell Mol. Biol. 2001, 24:339-344.
53. Rouault J.P., Falette N., Guehenneux F., Guillot C., Rimokh R., Wang Q., Berthet C., Moyret-Lalle C., Savatier P., Pain B., Shaw P., Berger R., Samarut J., Magaud J.P., Ozturk M., Samarut C., Puisieux A. Identification of BTG2, an antiproliferative p53-dependent component of the DNA damage cellular response pathway. Nat. Genet. 1996, 14:482-486.
54. Sacks P.G., Zhao Z.L., Kosinska W., Fleisher K.E., Gordon T., Guttenplan J.B. Concentration dependent effects of tobacco particulates from different types of cigarettes on expression of drug metabolizing proteins, and benzo(a)pyrene metabolism in primary normal human oral epithelial cells. Food Chem. Toxicol. 2011, 49:2348-2355.
55. Sarafian T.A., Magallanes J.A., Shau H., Tashkin D., Roth M.D. Oxidative stress produced by marijuana smoke. An adverse effect enhanced by cannabinoids. Am. J. Respir. Cell Mol. Biol. 1999, 20:1286-1293.
56. Sarafian T.A., Tashkin D.P., Roth M.D. Marijuana smoke and Delta(9)-tetrahydrocannabinol promote necrotic cell death but inhibit Fas-mediated apoptosis. Toxicol. Appl. Pharmacol. 2001, 174:264-272.
57. Sarafian T., Habib N., Mao J.T., Tsu I.H., Yamamoto M.L., Hsu E., Tashkin D.P., Roth M.D. Gene expression changes in human small airway epithelial cells exposed to Delta9-tetrahydrocannabinol. Toxicol. Lett. 2005, 158:95-107.
58. Sasco A.J., Merrill R.M., Dari I., Benhaim-Luzon V., Carriot F., Cann C.I., Bartal M. A case-control study of lung cancer in Casablanca, Morocco. Cancer Causes Control 2002, 13:609-616.
59. Searle S.R., Speed F.M., Milliken G.A. The population marginal means in the linear model: an alternative to least squares means. Am. Stat. 1980, 34:216-221.
60. Sen B., Mahadevan B., DeMarini D.M. Transcriptional responses to complex mixtures: a review. Mutat. Res. 2007, 636:144-177.
61. Sherman M.P., Aeberhard E.E., Wong V.Z., Simmons M.S., Roth M.D., Tashkin D.P. Effects of smoking marijuana, tobacco or cocaine alone or in combination on DNA damage in human alveolar macrophages. Life Sci. 1995, 56:2201-2207.
62. Sidney S., Quesenberry C.P., Friedman G.D., Tekawa I.S. Marijuana use and cancer incidence (California, United States). Cancer Causes Control 1997, 8:722-728.
63. Spira A., Beane J., Shah V., Liu G., Schembri F., Yang X., Palma J., Brody J.S. Effects of cigarette smoke on the human airway epithelial cell transcriptome. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:10143-10148.
64. Spurgers K.B., Gold D.L., Coombes K.R., Bohnenstiehl N.L., Mullins B., Meyn R.E., Logothetis C.J., McDonnell T.J. Identification of cell cycle regulatory genes as principal targets of p53-mediated transcriptional repression. J. Biol. Chem. 2006, 281:25134-25142.
65. Stenchever M.A., Kunysz T.J., Allen M.A. Chromosome breakage in users of marihuana. Am. J. Obstet. Gynecol. 1974, 118:106-113.
66. Tashkin D.P. Smoked marijuana as a cause of lung injury. Monaldi Arch. Chest Dis. 2005, 63:93-100.
67. Tomar, R.S., Beaumont, J., Hsieh, J.C.Y., 2009. Evidence on the Carcinogenicity of Marijuana Smoke. Office of Environmental Health Hazard Assessment of the California Environmental Protection Agency, California, 150 pp.
68. Vassiliades N., Mourelatos D., Dozi-Vassiliades J., Epivatianos P., Hatzitheodoridou P. Induction of sister-chromatid exchanges in heroin-cannabis, heroin and cannabis addicts. Mutat. Res. 1986, 170:125-127.
69. Voirin N., Berthiller J., Benhaim-Luzon V., Boniol M., Straif K., Ayoub W.B., Ayed F.B., Sasco A.J. Risk of lung cancer and past use of cannabis in Tunisia. J. Thorac. Oncol. 2006, 1:577-579.
70. Warner W., Harris L.S., Carchman R.A. Inhibition of cortiocosteroidogenesis by delta-9-tetrahydrocannabinol. Endocrinology 1977, 101:1815-1820.
71. Wehner F.C., van Rensburg S.J., Thiel P.G. Mutagenicity of marijuana and Transkei tobacco smoke condensates in the Salmonella/microsome assay. Mutat. Res. 1980, 77:135-142.
72. White P.A., Douglas G.R., Gingerich J., Parfett C., Shwed P., Seligy V., Soper L., Berndt L., Bayley J., Wagner S., Pound K., Blakey D. Development and characterization of a stable epithelial cell line from Muta Mouse lung. Environ. Mol. Mutagen. 2003, 42:166-184.
73. Wing D.R., Paton W.D. An effect of cannabis treatment in vivo on noradrenaline-stimulated lipolysis in rat adipocytes. J. Pharm. Pharmacol. 1978, 30:802-803.
74. Wu H., Kerr M.K., Cui X., Churchill G.A. MAANOVA: a software package for the analysis of spotted cDNA microarray experiments. The Analysis of Gene Expression Data: Methods and Software 2003, 313-431. Springer-Verlag, New York. G.G.E. Parmigiani, R.A. Irizarry, S. Zeger (Eds.).
75. Yamaori S., Kushihara M., Yamamoto I., Watanabe K. Characterization of major phytocannabinoids, cannabidiol and cannabinol, as isoform-selective and potent inhibitors of human CYP1 enzymes. Biochem. Pharmacol. 2010, 79:1691-1698.
76. Yang Y.H., Dudoit S., Luu P., Lin D.M., Peng V., Ngai J., Speed T.P. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 2002, 30:e15.
77. Yang L., Allen B.C., Thomas R.S. BMDExpress: a software tool for the benchmark dose analyses of genomic data. BMC Genomics 2007, 8:387.
78. Yauk C., Williams A., Buick J., Chen G., Maertens R., Halappanavar S., White P. Genetic toxicology and toxicogenomic analysis of 3 cigarette smoke condensates in vitro reveals few differences among full-flavour, blonde and light brands. Environ. Mol. Mutagen. 2011, 53:281-296.