Cigarette smoke condensate induces aryl hydrocarbon receptor-dependent changes in gene expression in spermatocytes

Reproductive Toxicology

Volumn 34, Issue 4, 2012, Pages 665-676

  Esakky, Prabagaran ^a,b   Hansen, Deborah A ^a   Drury, Andrea M ^a,b   Moley, Kelle H ^b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AHR; Apoptosis; CSC; Cyp1a1; Oxidative stress; Spermatocytes

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; CELL PROTEIN; CIGARETTE SMOKE CONDENSATE; CYTOCHROME P450 1A1; HYPOXIA INDUCIBLE FACTOR 1BETA; MESSENGER RNA; PROTEIN HSP90AA1; PROTEIN SOD1; PROTEIN SOD2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL ASSAY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOARCHITECTURE; DNA DAMAGE; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; MALE; MALE FERTILITY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; SEMEN ANALYSIS; SEMINIFEROUS TUBULE; SPERMATOCYTE; SPERMATOZOON MOTILITY; TESTIS WEIGHT; UPREGULATION;

ANIMALS; APOPTOSIS; ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; CELL LINE; CYTOCHROME P-450 CYP1A1; DNA DAMAGE; GENE EXPRESSION REGULATION; GLUTATHIONE PEROXIDASE; HSP90 HEAT-SHOCK PROTEINS; ION CHANNELS; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIAL PROTEINS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RECEPTORS, ARYL HYDROCARBON; SMOKE; SPERMATOCYTES; SUPEROXIDE DISMUTASE; TESTIS; TOBACCO PRODUCTS;

MURINAE; MUS;

EID: 84868243202     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2012.10.005     Document Type: Article

References (60)

1. Smith C.J., Perfetti T.A., Garg R., Hansch C. IARC carcinogens reported in cigarette mainstream smoke and their calculated logP values. Food and Chemical Toxicology 2003, 41:807-817.
2. Pryor W.A., Hales B.J., Premovic P.I., Church D.F. The radicals in cigarette tar: their nature and suggested physiological implications. Science 1983, 220:425-427.
3. Smith C.J., Hansch C. The relative toxicity of compounds in mainstream cigarette smoke condensate. Food and Chemical Toxicology 2000, 38:637-646.
4. Zavos P.M., Zarmakoupis-Zavos P.N. Impact of cigarette smoking on human reproduction: its effects on male and female fecundity. Technology 1999, 6:9-16.
5. Saleh R.A., Agarwal A. Oxidative stress and male infertility: from research bench to clinical practice. Journal of Andrology 2002, 23:737-752.
6. Ramlau-Hansen C.H., Thulstrup A.M., Aggerholm A.S., Jensen M.S., Toft G., Bonde J.P. Is smoking a risk factor for decreased semen quality? A cross-sectional analysis. Human Reproduction 2007, 22:188-196.
7. Viczian M. The effect of cigarette smoke inhalation on spermatogenesis in rats. Experientia 1968, 24:511-513.
8. Saleh R.A., Agarwal A., Sharma R.K., Nelson D.R., Thomas A.J. Effect of cigarette smoking on levels of seminal oxidative stress in infertile men: a prospective study. Fertility and Sterility 2002, 78:491-499.
9. Aitken R.J., Baker M.A. Oxidative stress and male reproductive biology. Reproduction, Fertility, and Development 2004, 16:581-588.
10. Shen H.M., Chia S.E., Ni Z.Y., New A.L., Lee B.L., Ong C.N. Detection of oxidative DNA damage in human sperm and the association with cigarette smoking. Reproductive Toxicology 1997, 11:675-680.
11. Horak S., Polanska J., Widlak P. Bulky DNA adducts in human sperm: relationship with fertility, semen quality, smoking, and environmental factors. Mutation Research 2003, 537:53-65.
12. Robbins W.A., Vine M.F., Truong K.Y., Everson R.B. Use of fluorescence in situ hybridization (FISH) to assess effects of smoking, caffeine, and alcohol on aneuploidy load in sperm of healthy men. Environmental and Molecular Mutagenesis 1997, 30:175-183.
13. Jones R., Mann T., Sherins R.J. Peroxidative breakdown of phospholipids in human spermatozoa: spermicidal effects of fatty acid peroxides and protective action of seminal plasma. Fertility and Sterility 1979, 31:531-537.
14. de Lamirande E., Gagnon C. A positive role for the superoxide anion in the triggering of human sperm hyperactivation and capacitation. International Journal of Andrology 1993, 16:21-25.
15. de Lamirande E., Jiang H., Zini A., Kodama H., Gagnon C. Reactive oxygen species and sperm physiology. Reviews of Reproduction 1997, 2:48-54.
16. Aitken R.J., Roman S.D. Antioxidant systems and oxidative stress in the testes. Advances in Experimental Medicine and Biology 2008, 636:154-171.
17. Georgellis A., Montelius J., Rydström J. Evidence for a free-radical-dependent metabolism of 7,12-dimethylbenz[a]anthracene in rat testis. Toxicology and Applied Pharmacology 1987, 87:141-154.
18. Ding Y.S., Ashley D.L., Watson C.H. Determination of 10 carcinogenic polycyclic aromatic hydrocarbons in mainstream cigarette smoke. Journal of Agricultural and Food Chemistry 2007, 55:5966-5973.
19. Georgellis A., Toppari J., Veromaa T., Rydström J., Parvinen M. Inhibition of meiotic divisions of rat spermatocytes in vitro by polycyclic aromatic hydrocarbons. Mutation Research 1990, 231:125-135.
20. 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.
21. Nagaraj N.S., Beckersa S., Mensaha J.K., Waigela S., Vigneswaranc N., Zacharias W. Cigarette smoke condensate induces cytochromes P450 and aldo-keto reductases in oral cancer cells. Toxicology Letters 2006, 165:182-194.
22. Hellermann G.R., Nagy S.B., Koong X., Lockey R.F., Mohapatra S.S. Mechanisms of cigarette smoke condensate-induced acute inflammatory response in human bronchial epithelial cells. Respiratory Research 2002, 3:22-29.
23. Narayan S., Jaiswal A.S., Kang D., Srivastava P., Das G.M., Gairola C.G. Cigarette smoke condensate-induced transformation of normal human breast epithelial cells in vitro. Oncogene 2004, 23:5880-5889.
24. 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. Toxicological Sciences 2005, 86:84-91.
25. van Leeuwen D.M., Gottschalk R.W.H., van Herwijnen M.H., Moonen E.J., Kleinjans J.C.S., van Delft J.H.M. Differential gene expression in human peripheral blood mononuclear cells induced by cigarette smoke and its constituents. Toxicological Sciences 2005, 86:200-210.
26. Han E.S., Muller F.L., Perez V.I., Qi W., Liang H., Xi L., et al. The in vivo gene expression signature of oxidative stress. Physiological Genomics 2008, 34:112-126.
27. Essenberg J.M., Fagan L., Mallerstein A.J. Chronic poisoning of the ovaries and testes of albino rats by nicotine and cigarette smoke. The Western Journal of Surgery, Obstetrics and Gynecology 1951, 59:27-32.
28. Mattison D.R. The effects of smoking on fertility from gametogenesis to implantation. Environmental Research 1982, 28:410-433.
29. Wyrobeck A.J., Bruce W.R. Chemical induction of sperm abnormalities in mice. Proceedings of the National Academy of Sciences of the United States of America 1975, 72:4425-4429.
30. Wolkowicz M.J., Coonrod S.A., Reddi P.P., Millan J.L., Hofmann M.C., Herr J.C. Refinement of the differentiated phenotype of the spermatogenic cell line GC-2spd(ts). Biology of Reproduction 1996, 55:923-932.
31. Kim S.H., Henry E.C., Kim D.K., Kim Y.H., Shin K.J., Han M.S., et al. Novel compound 2-methyl-2H-pyrazole-3-carboxylic acid(2-methyl-4-o-tolylazo-phenyl)-amide (CH-223191) prevents 2,3,7,8-TCDD-induced toxicity by antagonizing the aryl hydrocarbon receptor. Molecular Pharmacology 2006, 69:1871-1878.
32. Choi E.Y., Lee H., Dingle R.W.C., Kim K.B., Swanson H.I. Development of novel CH223191-based antagonists of the aryl hydrocarbon receptor. Molecular Pharmacology 2012, 81:3-11.
33. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., et al. The MIQE guidelines - minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 2009, 55:611-622.
34. -ΔΔCT method. Methods 2001, 25:402-408.
35. Dertinger S.D., Silverstone A.E., Gasiewicz T.A. Influence of aromatic hydrocarbon receptor-mediated events on the genotoxicity of cigarette smoke condensate. Carcinogenesis 1998, 19:2037-2042.
36. Van Binh P.N., Zhou D., Baudouin F., Martin C., Radionoff M., Dutertre H., et al. Modulation of the primary and the secondary antibody response by tobacco smoke condensates. Biomedicine and Pharmacotherapy 2004, 58:527-530.
37. Esakky P., Hansen D.A., Drury A.M., Moley K.H. Molecular analysis of cell type-specific gene expression profile during mouse spermatogenesis by laser microdissection and qRT-PCR. Reproduction Sciences 2012, 1-15. 10.1177/1933719112452939.
38. Goodson S.G., Zhang Z., Tsuruta J.K., Wang W., O'Brien D.A. Classification of mouse sperm motility patterns using an automated multiclass support vector machines model. Biology of Reproduction 2011, 84:1207-1215.
39. Putnam K.P., Bombick D.W., Doolittle D.J. Evaluation of eight in vitro assays for assessing the cytotoxicity of cigarette smoke condensate. Toxicology In Vitro 2002, 16:599-607.
40. Lodovici M., Luceri C., Guglielmi F., Bacci C., Akpan V., Fonnesu M.L., et al. Benzo(a)pyrene diolepoxide (BPDE)-DNA adduct levels in leukocytes of smokers in relation to polymorphism of CYP1A1, GSTM1, GSTP1, GSTT1, and mEH. Cancer Epidemiology, Biomarkers and Prevention 2004, 13:1342-1348.
41. Schecter A., McGee H., Stanley J.S., Boggess K., Brandt-Rauf P. Dioxins and dioxin-like chemicals in blood and semen of American Vietnam veterans from the state of Michigan. American Journal of Industrial Medicine 1996, 30:647-654.
42. Cavarra E., Fardin P., Fineschi S. Early response of gene clusters is associated with mouse lung resistance or sensitivity to cigarette smoke. American Journal of Physiology Lung Cellular and Molecular Physiology 2009, 296:418-429.
43. Stringer K.A., Freed B.M., Dunn J.S., Sayers S., Gustafson D.L., Flores S.C. Particulate phase cigarette smoke increases MnSOD, NQO1, and CINC-1 in rat lungs. Free Radical Biology and Medicine 2004, 37:1527-1533.
44. Onorato T.M., Petrice W., Brown P.W., Morris P.L. Mono-(2-ethylhexyl) phthalate increases spermatocyte mitochondrial peroxiredoxin 3 and cyclooxygenase 2. Journal of Andrology 2008, 29:293-303.
45. Russo M., Cocco S., Secondo A., Adornetto A., Bassi A., Nunziata A., et al. Cigarette smoke condensate causes a decrease of the gene expression of Cu-Zn superoxide dismutase, Mn superoxide dismutase, glutathione peroxidase, catalase, and free radical-induced cell injury in SH-SY5Y human neuroblastoma cells. Neurotoxicity Research 2011, 19:49-54.
46. Viloria T., Meseguer M., Martinez-Conejero J.A., O'Connor J.E., Remohi J., Pellicer A., et al. Cigarette smoking affects specific sperm oxidative defenses but does not cause oxidative DNA damage in infertile man. Fertility and Sterility 2010, 94:631-637.
47. Kitamura M., Kasai A. Cigarette smoke as a trigger for the dioxin receptor-mediated signaling pathway. Cancer Letters 2007, 252:184-194.
48. Hakkola J., Pasanen M., Hukkanen J., Pelkonen O., Maenpaa J., Edwards R.J., et al. Expression of xenobiotic-metabolizing cytochrome P450 forms in human full-term placenta. Biochemical Pharmacology 1996, 51:403-411.
49. Levine-Fridman A., Chen L., Elferink C.J. Cytochrome P4501A1 promotes G1 phase cell cycle progression by controlling aryl hydrocarbon receptor activity. Molecular Pharmacology 2004, 65:461-469.
50. Backer J.M., Weinstein I.B. Interaction of benzo(a)pyrene and its dihydrodiol-epoxide derivative with nuclear and mitochondrial DNA in C3H10T 1/2 cell cultures. Cancer Research 1982, 42:2764-2769.
51. Miao W., Hu L., Scrivens P.J. Transcriptional regulation of NF-E2 p45-related factor (NRF2) expression by the aryl hydrocarbon receptor-xenobiotic response element signaling pathway: direct cross-talk between phase I and II drug-metabolizing enzymes. Journal of Biological Chemistry 2005, 280:20340-20348.
52. Yeager R.L., Reisman S.A., Aleksunes L.M., Klaassen C.D. Introducing the " TCDD-inducible AhR-Nrf2 gene battery" Toxicological Sciences 2009, 111:238-246.
53. Ma Q., Kinneer K., Bi Y., Chan J.Y., Kan Y.W. Induction of murine NAD(P)H:quinone oxidoreductase by 2,3,7,8-tetrachlorodibenzo-p-dioxin requires the CNC (cap 'n' collar) basic leucine zipper transcription factor Nrf2 (nuclear factor erythroid 2-related factor 2): cross-interaction between AhR (aryl hydrocarbon receptor) and Nrf2 signal transduction. Biochemical Journal 2004, 377:205-213.
54. Kensler T.W., Wakabayashi N., Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE-pathway. Annual Review of Pharmacology and Toxicology 2007, 47:89-116.
55. Storz P., Döppler H., Toker A. Protein kinase D mediates mitochondrion-to-nucleus signaling and detoxification from mitochondrial reactive oxygen species. Molecular and Cellular Biology 2005, 25:8520-8530.
56. Minig V., Kattan Z., van Beeumen J., Brunner E., Becuwe P. Identification of DDB2 protein as a transcriptional regulator of constitutive SOD2 gene expression in human breast cancer cells. Journal of Biological Chemistry 2009, 284:14165-14176.
57. Song Z., Pollenz R.S. Functional analysis of murine aryl hydrocarbon (AH) receptors defective in nuclear import: impact of receptor degradation and gene activation. Molecular Pharmacology 2003, 63:597-606.
58. Pollenz R.S., Buggy C. Ligand-dependent and -independent degradation of the human aryl hydrocarbon receptor (hAHR) in cell culture models. Chemico-Biological Interactions 2006, 164:49-59.
59. Marlowe J.L., Fan Y., Chang X., Peng L., Knudsen E.S., Xia Y., et al. The aryl hydrocarbon receptor binds to E2F1 and inhibits E2F1-induced apoptosis. Molecular Biology of the Cell 2008, 19:3263-3271.
60. Giannone J.V., Li W., Probst M., Okey A.B. Prolonged depletion of AH receptor without alteration of receptor mRNA levels after treatment of cells in culture with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Biochemical Pharmacology 1998, 55:489-497.