Cigarette smoke-induced transgenerational alterations in genome stability in cord blood of human F1 offspring

FASEB Journal

Volumn 26, Issue 10, 2012, Pages 3946-3956

  Laubenthal, Julian ^a   Zlobinskaya, Olga ^b   Poterlowicz, Krzysztof ^a   Baumgartner, Adolf ^a,c   Gdula, Michal R ^d   Fthenou, Eleni ^e   Keramarou, Maria ^e   Hepworth, Sarah J ^f   Kleinjans, Jos C S ^g   Van Schooten, Frederik Jan ^g   Brunborg, Gunnar ^h   Godschalk, Roger W ^g   Schmid, Thomas E ^a   Anderson, Diana ^a  

^a UNIVERSITY OF BRADFORD   (United Kingdom)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF LEIPZIG   (Germany)

^d BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF CRETE   (Greece)

^f UNIVERSITY OF LEEDS   (United Kingdom)

^g MAASTRICHT UNIVERSITY   (Netherlands)

^h NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

Author keywords

DNA damage; Germ cell mutagen; Male germline; Toxicants; Transmission

Indexed keywords

CIGARETTE SMOKE; DNA; GAMMA HISTONE H2AX; HISTONE H2AX; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BLOOD; CLINICAL ARTICLE; COMET ASSAY; CONCEPTION; DNA DAMAGE; FEMALE; GENOMIC INSTABILITY; GERM CELL; GREECE; HUMAN; MALE; MATERNAL BLOOD; NEWBORN; PASSIVE SMOKING; PATERNAL BLOOD; PATERNAL SMOKING; PREDICTION; PREGNANCY; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROGENY; SPERMATOZOON; UMBILICAL CORD BLOOD; UNITED KINGDOM;

ADOLESCENT; ADULT; COMET ASSAY; COTININE; DNA DAMAGE; FEMALE; FETAL BLOOD; GENOMIC INSTABILITY; HUMANS; INFANT, NEWBORN; MALE; MATERNAL EXPOSURE; MULTIVARIATE ANALYSIS; PREGNANCY; SMOKING; YOUNG ADULT;

EID: 84868149468     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-201194     Document Type: Article

References (60)

1. Anderson L. M. Diwan B. A. Fear N. T. and Roman E. (2000) Critical windows of exposure for children's health: cancer in human epidemiological studies and neoplasms in experimental animal models. Environ. Health Perspect. 108(Suppl. 3) 573-594
2. Selevan S. G. Kimmel C. A. and Mendola P. (2000) Identifying critical windows of exposure for children's health. Environ. Health Perspect. 108(Suppl. 3) 451-455
3. Wild C. P. and Kleinjans J. (2003) Children and increased susceptibility to environmental carcinogens: evidence or empathy? Cancer Epidemiol. Biomarkers Prev. 12 1389-1394
4. Gluckman P. D. Hanson M. A. Cooper C. and Thornburg K. L. (2008) Effect of in utero and early-life conditions on adult health and disease. N. Engl. J. Med. 359 61-73
5. Merlo D. F. Wild C. P. Kogevinas M. Kyrtopoulos S. and Kleinjans J. (2009) NewGeneris: a European study on maternal diet during pregnancy and child health. Cancer Epidemiol. Biomarkers Prev. 18 5-10
6. Anderson D. (2005) Male-mediated developmental toxicity. Toxicol. Appl. Pharmacol. 207 506-513
7. Singer T. M. and Yauk C. L. (2010) Germ cell mutagens: risk assessment challenges in the 21st century. Environ. Mol. Mutagen 51 919-928
8. Olsen A. K. Andreassen A. Singh R. Wiger R. Duale N. Farmer P. B. and Brunborg G. (2010) Environmental exposure of the mouse germ line: DNA adducts in spermatozoa and formation of de novo mutations during spermatogenesis. PLoS One 5 e11349
9. Carone B. R. Fauquier L. Habib N. Shea J. M. Hart C. E. Li R. Bock C. Li C. Gu H. Zamore P. D. Meissner A. Weng Z. Hofmann H. A. Friedman N. and Rando O. J. (2010) Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143 1084-1096
10. Ng H. K. Novakovic B. Hiendleder S. Craig J. M. Roberts C. T. and Saffery R. (2010) Distinct patterns of gene-specific methylation in mammalian placentas: implications for placental evolution and function. Placenta 31 259-268
11. Dubrova Y. E. Plumb M. Gutierrez B. Boulton E. and Jeffreys A. J. (2000) Transgenerational mutation by radiation. Nature 405 37
12. Anway M. D. Cupp A. S. Uzumcu M. and Skinner M. K. (2005) Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308 1466-1469
13. Youngson N. A. and Whitelaw E. (2008) Transgenerational epigenetic effects. Annu. Rev. Genomics Hum. Genet. 9 233-257
14. Ng S. F. Lin R. C. Laybutt D. R. Barres R. Owens J. A. and Morris M. J. (2010) Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring. Nature 467 963-966
15. Dubrova Y. E. (2003) Radiation-induced transgenerational instability. Oncogene 22 7087-7093
16. Glen C. D. Smith A. G. and Dubrova Y. E. (2008) Singlemolecule PCR analysis of germ line mutation induction by anticancer drugs in mice. Cancer Res. 68 3630-3636
17. Bennett L. M. Wang Y. Ramsey M. J. Harger G. F. Bigbee W. L. and Tucker J. D. (2010) Cigarette smoking during pregnancy: chromosome translocations and phenotypic susceptibility in mothers and newborns. Mutat. Res. 696 81-88
18. Soares S. R. and Melo M. A. (2008) Cigarette smoking and reproductive function. Curr. Opin. Obstet. Gynecol. 20 281-291
19. ASRM (2008) Smoking and infertility. Fertil. Steril. 90 S254-259
20. Secretan B. Straif K. Baan R. Grosse Y. El Ghissassi F. Bouvard V. Benbrahim-Tallaa L. Guha N. Freeman C. Galichet L. and Cogliano V. (2009) A review of human carcinogens-part E: tobacco areca nut alcohol coal smoke and salted fish. Lancet Oncol. 10 1033-1034
21. Aitken R. J. Koopman P. and Lewis S. E. (2004) Seeds of concern. Nature 432 48-52
22. DeMarini D. M. (2004) Genotoxicity of tobacco smoke and tobacco smoke condensate: a review. Mutat. Res. 567 447-474
23. Marchetti F. Rowan-Carroll A. Williams A. Polyzos A. Berndt-Weis M. L. and Yauk C. L. (2011) Sidestream tobacco smoke is a male germ cell mutagen. Proc. Natl. Acad. Sci. U. S. A. 108 12811-12814
24. Vande Loock K. Fthenou E. Decordier I. Chalkiadaki G. Keramarou M. Plas G. Roelants M. Kleinjans J. Chatzi L. Merlo F. Kogevinas M. and Kirsch-Volders M. (2011) Maternal and gestational factors and micronuclei frequencies in umbilical blood: the NewGeneris Rhea Cohort in Crete. Environ. Health Perspect. 119 1460-1465
25. Chatzi L. Plana E. Daraki V. Karakosta P. Alegkakis D. Tsatsanis C. Kafatos A. Koutis A. and Kogevinas M. (2009) Metabolic syndrome in early pregnancy and risk of preterm birth. Am. J. Epidemiol. 170 829-836
26. World Health Organization. (1999) WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction. Cambridge University Press Cambridge UK
27. Vardavas C. I. Fthenou E. Patelarou E. Bagkeris E. Murphy S. Hecht S. S. Connolly G. N. Chatzi L. and Kogevinas M. (2012) Exposure to different sources of second-hand smoke during pregnancy and its effect on urinary cotinine and tobacco-specific nitrosamine (NNAL) concentrations. [E-pub ahead of print] Tob. Control. doi: 10.1136/tobaccocontrol-2011-050144
28. Hecht S. S. Carmella S. G. Le K. A. Murphy S. E. Boettcher A. J. Le C. Koopmeiners J. An L. and Hennrikus D. J. (2006) 4-(Methylnitrosamino)-1-(3- pyridyl)-1-butanol and its glucuronides in the urine of infants exposed to environmental tobacco smoke. Cancer Epidemiol. Biomarkers Prev. 15 988-992
29. Hecht S. S. Carmella S. G. Chen M. Dor Koch J. F. Miller A. T. Murphy S. E. Jensen J. A. Zimmerman C. L. and Hatsukami D. K. (1999) Quantitation of urinary metabolites of a tobacco-specific lung carcinogen after smoking cessation. Cancer Res. 59 590-596
30. Hammadeh M. E. Hamad M. F. Montenarh M. and Fischer-Hammadeh C. (2010) Protamine contents and P1/P2 ratio in human spermatozoa from smokers and non-smokers. Hum. Reprod. 25 2708-2720
31. Singh N. P. McCoy M. T. Tice R. R. and Schneider E. L. (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell. Res. 175 184-191
32. Sipinen V. Laubenthal J. Baumgartner A. Cemeli E. Linschooten J. O. Godschalk R. W. Van Schooten F. J. Anderson D. and Brunborg G. (2010) In vitro evaluation of baseline and induced DNA damage in human sperm exposed to benzo[a]pyrene or its metabolite benzo[a]pyrene-78-diol-910-epoxide using the comet assay. Mutagenesis 25 417-425
33. Schmid T. E. Dollinger G. Beisker W. Hable V. Greubel C. Auer S. Mittag A. Tarnok A. Friedl A. A. Molls M. and Roper B. (2010) Differences in the kinetics of γ-H2AX fluorescence decay after exposure to low and high LET radiation. Int. J. Radiat. Biol. 86 682-691
34. Shutin D. and Zlobinskaya O. (2010) Application of information-theoretic measures to quantitative analysis of immunofluorescent microscope imaging. Comput. Methods Programs Biomed. 97 114-129
35. Zlobinskaya O. Dollinger G. Michalski D. Hable V. Greubel C. Du G. Multhoff G. Roper B. Molls M. and Schmid T. E. (2012) Induction and repair of DNA double-strand breaks assessed by gamma-H2AX foci after irradiation with pulsed or continuous proton beams. Radiat. Environ. Biophys. 51 23-32
36. Demarini D. M. (2012) Declaring the existence of human germ-cell mutagens. Environ. Mol. Mutagen 53 166-172
37. Barber R. C. Hickenbotham P. Hatch T. Kelly D. Topchiy N. Almeida G. M. Jones G. D. Johnson G. E. Parry J. M. Rothkamm K. and Dubrova Y. E. (2006) Radiation-induced transgenerational alterations in genome stability and DNA damage. Oncogene 25 7336-7342
38. Yauk C. L. Berndt M. L. Williams A. Rowan-Carroll A. Douglas G. R. and Stampfli M. R. (2007) Mainstream tobacco smoke causes paternal germ-line DNA mutation. Cancer Res. 67 5103-5106
39. Holliday R. (1987) The inheritance of epigenetic defects. Science 238 163-170
40. Yauk C. Polyzos A. Rowan-Carroll A. Somers C. M. Godschalk R. W. Van Schooten F. J. Berndt M. L. Pogribny I. P. Koturbash I. Williams A. Douglas G. R. and Kovalchuk O. (2008) Germ-line mutations DNA damage and global hypermethylation in mice exposed to particulate air pollution in an urban/industrial location. Proc. Natl. Acad. Sci. U. S. A. 105 605-610
41. Waters D. J. Shen S. Xu H. Kengeri S. S. Cooley D. M. Chiang E. C. Chen Y. Schlittler D. Oteham C. Combs G. F. Jr. Glickman L. T. Morris J. S. and Bostwick D. G. (2007) Noninvasive prediction of prostatic DNA damage by oxidative stress challenge of peripheral blood lymphocytes. Cancer Epidemiol. Biomarkers Prev. 16 1906-1910
42. Chandler V. L. and Stam M. (2004) Chromatin conversations: mechanisms and implications of paramutation. Nat. Rev. Genet. 5 532-544
43. Rassoulzadegan M. Grandjean V. Gounon P. Vincent S. Gillot I. and Cuzin F. (2006) RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature 441 469-474
44. Linschooten J. O. Van Schooten F. J. Baumgartner A. Cemeli E. Van Delft J. Anderson D. and Godschalk R. W. (2009) Use of spermatozoal mRNA profiles to study geneenvironment interactions in human germ cells. Mutat. Res. 667 70-76
45. Linschooten J. O. Laubenthal J. Cemeli E. Baumgartner A. Anderson D. Sipinen V. E. Brunborg G. Haenen G. R. Fthenou E. Briede J. J. van Schooten F. J. and Godschalk R. W. (2011) Incomplete protection of genetic integrity of mature spermatozoa against oxidative stress. Reprod. Toxicol. 32 106-111
46. Brevik A. Rusnakova V. Duale N. Slagsvold H. H. Olsen A. K. Storeng R. Kubista M. Brunborg G. and Lindeman B. (2011) Preconceptional paternal glycidamide exposure affects embryonic gene expression: single embryo gene expression study following in vitro fertilization. Reprod. Toxicol. 32 463-471
47. Brevik A. Lindeman B. Brunborg G. and Duale N. (2012) Paternal benzo[a]pyrene exposure modulates microRNA expression patterns in the developing mouse embryo. Int. J. Cell Biol. 2012:407-431
48. Bernstein E. and Allis C. D. (2005) RNA meets chromatin. Genes Dev. 19 1635-1655
49. Verhofstad N. van Oostrom C. T. van Benthem J. van Schooten F. J. van Steeg H. and Godschalk R. W. (2010) DNA adduct kinetics in reproductive tissues of DNA repair proficient and deficient male mice after oral exposure to benzo(a)pyrene. Environ. Mol. Mutagen 51 123-129
50. Verhofstad N. van Oostrom C. T. Zwart E. Maas L. M. van Benthem J. van Schooten F. J. van Steeg H. and Godschalk R. W. (2011) Evaluation of benzo(a)pyrene-induced gene mutations in male germ cells. Toxicol. Sci. 119 218-223
51. Zenzes M. T. Puy L. A. Bielecki R. and Reed T. E. (1999) Detection of benzo[a]pyrene diol epoxide-DNA adducts in embryos from smoking couples: evidence for transmission by spermatozoa. Mol. Hum. Reprod. 5 125-131
52. 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
53. Wyatt N. P. Falque-Gonzalez C. Farrar D. Tuffnell D. Whitelaw D. Knudsen L. E. and Anderson D. (2007) In vitro susceptibilities in lymphocytes from mothers and cord blood to the monofunctional alkylating agent EMS. Mutagenesis 22 123-127
54. Demarini D. M. and Preston R. J. (2005) Smoking while pregnant: transplacental mutagenesis of the fetus by tobacco smoke. JAMA 293 1264-1265
55. de la Chica R. A. Ribas I. Giraldo J. Egozcue J. and Fuster C. (2005) Chromosomal instability in amniocytes from fetuses of mothers who smoke. JAMA 293 1212-1222
56. Keohavong P. Xi L. Day R. D. Zhang L. Grant S. G. Day B. W. Ness R. B. and Bigbee W. L. (2005) HPRT gene alterations in umbilical cord blood T-lymphocytes in newborns of mothers exposed to tobacco smoke during pregnancy. Mutat. Res. 572 156-166
57. American Society of Reproductive Medicine (2008) Smoking and infertility. Fertil. Steril. 90 S254-S259
58. Leonardi-Bee J. Britton J. and Venn A. (2011) Secondhand smoke and adverse fetal outcomes in nonsmoking pregnant women: a meta-analysis. Pediatrics 127 734-741
59. Venners S. A. Wang X. Chen C. Wang L. Chen D. Guang W. Huang A. Ryan L. O'Connor J. Lasley B. Overstreet J. Wilcox A. and Xu X. (2004) Paternal smoking and pregnancy loss: a prospective study using a biomarker of pregnancy. Am. J. Epidemiol. 159 993-1001
60. Hanahan D. and Weinberg R. A. (2011) Hallmarks of cancer: the next generation. Cell 144 646-674