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International Journal of Cell Biology
Volume 2012, Article ID 407431, 11 pages
http://dx.doi.org/10.1155/2012/407431
Research Article

Paternal Benzo[a]pyrene Exposure Modulates MicroRNA Expression Patterns in the Developing Mouse Embryo

Division of Environmental Medicine, Department of Chemical Toxicology, Norwegian Institute of Public Health, P.O. Box 4404 Nydalen, 0403 OSLO, Norway

Received 30 September 2011; Accepted 19 January 2012

Academic Editor: Noam Shomron

Copyright © 2012 Asgeir Brevik et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. M. Andersson, N. Jørgensen, K. M. Main et al., “Adverse trends in male reproductive health: we may have reached a crucial tipping point',” International Journal of Andrology, vol. 31, no. 2, pp. 74–80, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. R. Bergström, H. O. Adami, M. Möhner et al., “Increase in testicular cancer incidence in six European countries: a birth cohort phenomenon,” Journal of the National Cancer Institute, vol. 88, no. 11, pp. 727–733, 1996. View at Publisher · View at Google Scholar · View at Scopus
  3. F. Bray, Å. Klint, M. Gislum et al., “Trends in survival of patients diagnosed with male genital cancers in the Nordic countries 1964–2003 followed up until the end of 2006,” Acta Oncologica, vol. 49, no. 5, pp. 644–654, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Rosen, G. Jayram, M. Drazer, and S. E. Eggener, “Global trends in testicular cancer incidence and mortality,” European Urology, vol. 60, no. 2, pp. 374–379, 2011. View at Publisher · View at Google Scholar
  5. B. Eskenazi, S. A. Kidd, A. R. Marks, E. Sloter, G. Block, and A. J. Wyrobek, “Antioxidant intake is associated with semen quality in healthy men,” Human Reproduction, vol. 20, no. 4, pp. 1006–1012, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. A. Guven, A. Kayikci, K. Cam, P. Arbak, O. Balbay, and M. Cam, “Alterations in semen parameters of toll collectors working at motorways: does diesel exposure induce detrimental effects on semen?” Andrologia, vol. 40, no. 6, pp. 346–351, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Jurewicz, W. Hanke, M. Radwan, and J. Bonde, “Environmental factors and semen quality,” International Journal of Occupational Medicine and Environmental Health, vol. 22, no. 4, pp. 305–329, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. N. Pant, R. Kumar, N. Mathur, S. P. Srivastava, D. K. Saxena, and V. R. Gujrati, “Chlorinated pesticide concentration in semen of fertile and infertile men and correlation with sperm quality,” Environmental Toxicology and Pharmacology, vol. 23, no. 2, pp. 135–139, 2007. View at Publisher · View at Google Scholar
  9. O. Ståhl, J. Eberhard, K. Jepson et al., “Sperm DNA integrity in testicular cancer patients,” Human Reproduction, vol. 21, no. 12, pp. 3199–3205, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Vujkovic, J. H. de Vries, G. R. Dohle et al., “Associations between dietary patterns and semen quality in men undergoing IVF/ICSI treatment,” Human Reproduction, vol. 24, no. 6, pp. 1304–1312, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. T. M. Edwards, B. C. Moore, L. J. Guillette Jr., N. Olea, J. McLachlan, and D. Page, “Reproductive dysgenesis in wildlife: a comparative view,” International Journal of Andrology, vol. 29, no. 1, pp. 109–121, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. C. M. Somers, C. L. Yauk, P. A. White, C. L. J. Parfett, and J. S. Quinn, “Air pollution induces heritable DNA mutations,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 25, pp. 15904–15907, 2002. View at Google Scholar · View at Scopus
  13. C. M. Somers, “Ambient air pollution exposure and damage to male gametes: human studies and in situ “sentinel” animal experiments,” Systems Biology in Reproductive Medicine, vol. 57, no. 1-2, pp. 63–71, 2011. View at Publisher · View at Google Scholar
  14. C. L. Yauk, G. A. Fox, B. E. McCarry, and J. S. Quinn, “Induced minisatellite germline mutations in herring gulls (Larus argentatus) living near steel mills,” Mutation Research, vol. 452, no. 2, pp. 211–218, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. C. L. Yauk and J. S. Quinn, “Multilocus DNA fingerprinting reveals high rate of heritable genetic mutation in herring gulls nesting in an industrialized urban site,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 22, pp. 12137–12141, 1996. View at Publisher · View at Google Scholar · View at Scopus
  16. C. G. Fraga, P. A. Motchnik, A. J. Wyrobek, D. M. Rempel, and B. N. Ames, “Smoking and low antioxidant levels increase oxidative damage to sperm DNA,” Mutation Research, vol. 351, no. 2, pp. 199–203, 1996. View at Publisher · View at Google Scholar · View at Scopus
  17. Z. Y. Ni, Y. Q. Liu, H. M. Shen, S. E. Chia, and C. N. Ong, “Does the increase of 8-hydroxydeoxyguanosine lead to poor sperm quality?” Mutation Research, vol. 381, no. 1, pp. 77–82, 1997. View at Publisher · View at Google Scholar · View at Scopus
  18. H. M. Shen and C. N. Ong, “Detection of oxidative DNA damage in human sperm and its association with sperm function and male infertility,” Free Radical Biology and Medicine, vol. 28, no. 4, pp. 529–536, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. D. S. Irvine, J. P. Twigg, E. L. Gordon, N. Fulton, P. A. Milne, and R. J. Aitken, “DNA integrity in human spermatozoa: relationships with semen quality,” Journal of Andrology, vol. 21, no. 1, pp. 33–44, 2000. View at Google Scholar · View at Scopus
  20. S. Loft, T. Kold-Jensen, N. H. Hjollund et al., “Oxidative DNA damage in human sperm influences time to pregnancy,” Human Reproduction, vol. 18, no. 6, pp. 1265–1272, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. K. M. Mackenzie and D. M. Angevine, “Infertility in mice exposed in utero to benzo(a)pyrene,” Biology of Reproduction, vol. 24, no. 1, pp. 183–191, 1981. View at Google Scholar · View at Scopus
  22. F. Inyang, A. Ramesh, P. Kopsombut et al., “Disruption of testicular steroidogenesis and epididymal function by inhaled benzo(a)pyrene,” Reproductive Toxicology, vol. 17, no. 5, pp. 527–537, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. M. M. McCallister, M. Maguire, A. Ramesh et al., “Prenatal exposure to benzo(a)pyrene impairs later-life cortical neuronal function,” NeuroToxicology, vol. 29, no. 5, pp. 846–854, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Ramesh, F. Inyang, D. D. Lunstra et al., “Alteration of fertility endpoints in adult male F-344 rats by subchronic exposure to inhaled benzo(a)pyrene,” Experimental and Toxicologic Pathology, vol. 60, no. 4-5, pp. 269–280, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. E. S. A. Mohamed, W. H. Song, S. A. Oh et al., “The transgenerational impact of benzo(a)pyrene on murine male fertility,” Human Reproduction, vol. 25, no. 10, pp. 2427–2433, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. W. Xue and D. Warshawsky, “Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: a review,” Toxicology and Applied Pharmacology, vol. 206, no. 1, pp. 73–93, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. O. Pelkonen and D. W. Nebert, “Metabolism of polycyclic aromatic hydrocarbons: etiologic role in carcinogenesis,” Pharmacological Reviews, vol. 34, no. 2, pp. 189–222, 1982. View at Google Scholar · View at Scopus
  28. L. He and G. J. Hannon, “MicroRNAs: small RNAs with a big role in gene regulation,” Nature Reviews Genetics, vol. 5, no. 7, pp. 522–531, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. D. Sayed and M. Abdellatif, “Micrornas in development and disease,” Physiological Reviews, vol. 91, no. 3, pp. 827–887, 2011. View at Publisher · View at Google Scholar
  30. S. A. Hanina, W. Mifsud, T. A. Down et al., “Genome-wide identification of targets and function of individual microRNAs in mouse embryonic stem cells,” PLoS Genetics, vol. 6, no. 10, Article ID e1001163, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. J. P. Curley, R. Mashoodh, and F. A. Champagne, “Epigenetics and the origins of paternal effects,” Hormones and Behavior, vol. 59, no. 3, pp. 306–314, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. P. Mestdagh, T. Feys, N. Bernard et al., “High-throughput stem-loop RT-qPCR miRNA expression profiling using minute amounts of input RNA,” Nucleic Acids Research, vol. 36, no. 21, article e143, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. P. Mestdagh, P. Van Vlierberghe, A. De Weer et al., “A novel and universal method for microRNA RT-qPCR data normalization,” Genome Biology, vol. 10, no. 6, article R64, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. T. D. Schmittgen and K. J. Livak, “Analyzing real-time PCR data by the comparative CT method,” Nature Protocols, vol. 3, no. 6, pp. 1101–1108, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. K. J. Livak and T. D. Schmittgen, “Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method,” Methods, vol. 25, no. 4, pp. 402–408, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. A. I. Saeed, N. K. Bhagabati, J. C. Braisted et al., “TM4 microarray software suite,” Methods in Enzymology, vol. 411, pp. 134–193, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. B. Dysvik and I. Jonassen, “J-Express: exploring gene expression data using Java,” Bioinformatics, vol. 17, no. 4, pp. 369–370, 2001. View at Google Scholar · View at Scopus
  38. H. Dweep, C. Sticht, P. Pandey, and N. Gretz, “MiRWalk—database: prediction of possible miRNA binding sites by “walking” the genes of three genomes,” Journal of Biomedical Informatics, vol. 44, no. 5, pp. 839–847, 2011. View at Publisher · View at Google Scholar
  39. B. Zhang, S. Kirov, and J. Snoddy, “WebGestalt: an integrated system for exploring gene sets in various biological contexts,” Nucleic Acids Research, vol. 33, no. 2, pp. W741–W748, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Bischoff, D. E. Parfitt, and M. Zernicka-Goetz, “Formation of the embryonic-abembryonic axis of the mouse blastocyst: relationships between orientation of early cleavage divisions and pattern of symmetric/asymmetric divisions,” Development, vol. 135, no. 5, pp. 953–962, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. T. Fujimori, Y. Kurotaki, K. Komatsu, and Y. I. Nabeshima, “Morphological organization of the mouse preimplantation embryo,” Reproductive Sciences, vol. 16, no. 2, pp. 171–177, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. Y. Kurotaki, K. Hatta, K. Nakao, Y. I. Nabeshima, and T. Fujimori, “Blastocyst axis is specified independently of early cell lineage but aligns with the ZP shape,” Science, vol. 316, no. 5825, pp. 719–723, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Kanehisa, S. Goto, M. Furumichi, M. Tanabe, and M. Hirakawa, “KEGG for representation and analysis of molecular networks involving diseases and drugs,” Nucleic Acids Research, vol. 38, no. 1, supplement, pp. D355–D360, 2009. View at Publisher · View at Google Scholar
  44. R. Edgar, M. Domrachev, and A. E. Lash, “Gene expression omnibus: NCBI gene expression and hybridization array data repository,” Nucleic Acids Research, vol. 30, no. 1, pp. 207–210, 2002. View at Google Scholar · View at Scopus
  45. H. Parkinson, U. Sarkans, N. Kolesnikov et al., “Arrayexpress update—an archive of microarray and high-throughput sequencing-based functional genomics experiments,” Nucleic Acids Research, vol. 39, no. SUPPL. 1, pp. D1002–D1004, 2011. View at Publisher · View at Google Scholar
  46. N. Verhofstad, J. L. A. Pennings, C. T. van Oostrom et al., “Benzo(a)pyrene induces similar gene expression changes in testis of DNA repair proficient and deficient mice,” BMC Genomics, vol. 11, no. 1, article 333, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. N. Duale, B. Lindeman, M. Komada et al., “Molecular portrait of cisplatin induced response in human testis cancer cell lines based on gene expression profiles,” Molecular Cancer, vol. 6, article 53, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. V. G. Tusher, R. Tibshirani, and G. Chu, “Significance analysis of microarrays applied to the ionizing radiation response,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 9, pp. 5116–5121, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Hausser, P. Berninger, C. Rodak, Y. Jantscher, S. Wirth, and M. Zavolan, “MirZ: an integrated microRNA expression atlas and target prediction resource,” Nucleic Acids Research, vol. 37, no. 2, pp. W266–W272, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. M. A. Lewis and K. P. Steel, “MicroRNAs in mouse development and disease,” Seminars in Cell and Developmental Biology, vol. 21, no. 7, pp. 774–780, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. F. Tang, M. Kaneda, D. O'Carroll et al., “Maternal microRNAs are essential for mouse zygotic development,” Genes and Development, vol. 21, no. 6, pp. 644–648, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. P. H. O'Farrell, J. Stumpff, and T. T. Su, “Embryonic cleavage cycles: how is a mouse like a fly?” Current Biology, vol. 14, no. 1, pp. R35–R45, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Marson, S. S. Levine, M. F. Cole et al., “Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells,” Cell, vol. 134, no. 3, pp. 521–533, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. C. Berthet and P. Kaldis, “Cell-specific responses to loss of cyclin-dependent kinases,” Oncogene, vol. 26, no. 31, pp. 4469–4477, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. I. Ivanovska, A. S. Ball, R. L. Diaz et al., “MicroRNAs in the miR-106b family regulate p21/CDKN1A and promote cell cycle progression,” Molecular and Cellular Biology, vol. 28, no. 7, pp. 2167–2174, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. Y. Wang and R. Blelloch, “Cell cycle regulation by microRNAs in embryonic stem cells,” Cancer Research, vol. 69, no. 10, pp. 4093–4096, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. Y. Ohnishi, Y. Totoki, A. Toyoda et al., “Small RNA class transition from siRNA/piRNA to miRNA during pre-implantation mouse development,” Nucleic Acids Research, vol. 38, no. 15, pp. 5141–5151, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. R. Kulshreshtha, R. V. Davuluri, G. A. Calin, and M. Ivan, “A microRNA component of the hypoxic response,” Cell Death and Differentiation, vol. 15, no. 4, pp. 667–671, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. A. Giannakakis, R. Sandaltzopoulos, J. Greshock et al., “miR-210 links hypoxia with cell cycle regulation and is deleted in human epithelial ovarian cancer,” Cancer Biology and Therapy, vol. 7, no. 2, pp. 255–264, 2008. View at Google Scholar · View at Scopus
  60. P. Fasanaro, Y. D'Alessandra, V. Di Stefano et al., “MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand ephrin-A3,” Journal of Biological Chemistry, vol. 283, no. 23, pp. 15878–15883, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. M. E. Crosby, R. Kulshreshtha, M. Ivan, and P. M. Glazer, “MicroRNA regulation of DNA repair gene expression in hypoxic stress,” Cancer Research, vol. 69, no. 3, pp. 1221–1229, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. S. Y. Chan, Y. Y. Zhang, C. Hemann, C. E. Mahoney, J. L. Zweier, and J. Loscalzo, “MicroRNA-210 controls mitochondrial metabolism during hypoxia by repressing the iron-sulfur cluster assembly proteins ISCU1/2,” Cell Metabolism, vol. 10, no. 4, pp. 273–284, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. W. H. Tong and T. Rouault, “Distinct iron-sulfur cluster assembly complexes exist in the cytosol and mitochondria of human cells,” EMBO Journal, vol. 19, no. 21, pp. 5692–5700, 2000. View at Google Scholar · View at Scopus
  64. H. Zhang, M. Bosch-Marce, L. A. Shimoda et al., “Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia,” Journal of Biological Chemistry, vol. 283, no. 16, pp. 10892–10903, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. J. Zhang, F. Zhang, X. Didelot et al., “Maternal high fat diet during pregnancy and lactation alters hepatic expression of insulin like growth factor-2 and key microRNAs in the adult offspring,” BMC Genomics, vol. 10, article 1471, p. 478, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. P. Landgraf, M. Rusu, R. Sheridan et al., “A mammalian microRNA expression atlas based on small RNA library sequencing,” Cell, vol. 129, no. 7, pp. 1401–1414, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. N. Ma, X. Wang, Y. Qiao et al., “Coexpression of an intronic microRNA and its host gene reveals a potential role for miR-483-5p as an IGF2 partner,” Molecular and Cellular Endocrinology, vol. 333, no. 1, pp. 96–101, 2011. View at Publisher · View at Google Scholar
  68. R. Randhawa and P. Cohen, “The role of the insulin-like growth factor system in prenatal growth,” Molecular Genetics and Metabolism, vol. 86, no. 1-2, pp. 84–90, 2005. View at Publisher · View at Google Scholar · View at Scopus
  69. T. H. M. D. A. Da Costa, D. H. Williamson, A. Ward et al., “High plasma insulin-like growth factor-II and low lipid content in transgenic mice: measurements of lipid metabolism,” Journal of Endocrinology, vol. 143, no. 3, pp. 433–439, 1994. View at Google Scholar · View at Scopus
  70. B. K. Jones, J. Levorse, and S. M. Tilghman, “Deletion of a nuclease-sensitive region between the Igf2 and H19 genes leads to Igf2 misregulation and increased adiposity,” Human Molecular Genetics, vol. 10, no. 8, pp. 807–814, 2001. View at Google Scholar · View at Scopus
  71. G. Alsaleh, G. Suffert, N. Semaan et al., “Bruton's tyrosine kinase is involved in miR-346-related regulation of IL-18 release by lipopolysaccharide-activated rheumatoid fibroblast-like synoviocytes,” Journal of Immunology, vol. 182, no. 8, pp. 5088–5097, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. A. Z. Oskowitz, J. Lu, P. Penfornis et al., “Human multipotent stromal cells from bone marrow and microRNA: regulation of differentiation and leukemia inhibitory factor expression,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 47, pp. 18372–18377, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. F. Weber, R. E. Teresi, C. E. Broelsch, A. Frilling, and C. Eng, “A limited set of human MicroRNA Is deregulated in follicular thyroid carcinoma,” Journal of Clinical Endocrinology and Metabolism, vol. 91, no. 9, pp. 3584–3591, 2006. View at Publisher · View at Google Scholar · View at Scopus
  74. N. P. Tsai, Y. L. Lin, and L. N. Wei, “MicroRNA mir-346 targets the 5′-untranslated region of receptor-interacting protein 140 (RIP140) mRNA and up-regulates its protein expression,” Biochemical Journal, vol. 424, no. 3, pp. 411–418, 2009. View at Publisher · View at Google Scholar · View at Scopus
  75. L. N. Wei, “Retinoids and receptor interacting protein 140 (RIP140) in gene regulation,” Current Medicinal Chemistry, vol. 11, no. 12, pp. 1527–1532, 2004. View at Google Scholar · View at Scopus
  76. M. Christian, E. Kiskinis, D. Debevec, G. Leonardsson, R. White, and M. G. Parker, “RIP140-targeted repression of gene expression in adipocytes,” Molecular and Cellular Biology, vol. 25, no. 21, pp. 9383–9391, 2005. View at Publisher · View at Google Scholar · View at Scopus
  77. B. Herzog, M. Hallberg, A. Seth, A. Woods, R. White, and M. G. Parker, “The nuclear receptor cofactor, receptor-interacting protein 140, is required for the regulation of hepatic lipid and glucose metabolism by liver X receptor,” Molecular Endocrinology, vol. 21, no. 11, pp. 2687–2697, 2007. View at Publisher · View at Google Scholar · View at Scopus
  78. A. M. Powelka, A. Seth, J. V. Virbasius et al., “Suppression of oxidative metabolism and mitochondrial biogenesis by the transcriptional corepressor RIP140 in mouse adipocytes,” Journal of Clinical Investigation, vol. 116, no. 1, pp. 125–136, 2006. View at Publisher · View at Google Scholar · View at Scopus
  79. A. Seth, J. H. Steel, D. Nichol et al., “The transcriptional corepressor RIP140 regulates oxidative metabolism in skeletal muscle,” Cell Metabolism, vol. 6, no. 3, pp. 236–245, 2007. View at Publisher · View at Google Scholar · View at Scopus