Table of Contents
Advances in Biology
Volume 2014 (2014), Article ID 179701, 13 pages
http://dx.doi.org/10.1155/2014/179701
Review Article

Sperm RNA as a Mediator of Genomic Plasticity

Leeds Institute of Genetics and Health Therapeutics, University of Leeds, Clarendon Way, Leeds, West Yorkshire LS2 9JT, UK

Received 2 July 2014; Revised 8 September 2014; Accepted 9 September 2014; Published 14 October 2014

Academic Editor: Angelo Veronese

Copyright © 2014 David Miller. 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. B. G. Dias and K. J. Ressler, “Parental olfactory experience influences behavior and neural structure in subsequent generations,” Nature Neuroscience, vol. 17, no. 1, pp. 89–96, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. K. Gapp, A. Jawaid, P. Sarkies et al., “Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice,” Nature Neuroscience, vol. 17, no. 5, pp. 667–669, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Rassoulzadegan, V. Grandjean, P. Gounon, S. Vincent, I. Gillot, and F. Cuzin, “RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse,” Nature, vol. 441, no. 7092, pp. 469–474, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. M. E. Pembrey, L. O. Bygren, G. Kaati et al., “Sex-specific, male-line transgenerational responses in humans,” European Journal of Human Genetics, vol. 14, no. 2, pp. 159–166, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. K. Northstone, J. Golding, G. Davey Smith, L. L. Miller, and M. Pembrey, “Prepubertal start of father's smoking and increased body fat in his sons: further characterisation of paternal transgenerational responses,” European Journal of Human Genetics, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. R. Balhorn, L. Brewer, and M. Corzett, “DNA condensation by protamine and arginine-rich peptides: analysis of toroid stability using single DNA molecules,” Molecular Reproduction and Development, vol. 56, supplement 2, pp. 230–234, 2000. View at Google Scholar · View at Scopus
  7. G. Fuentes-Mascorro, H. Serrano, and A. Rosado, “Sperm chromatin,” Archives of Andrology, vol. 45, no. 3, pp. 215–225, 2000. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Rathe, W. M. Baarends, S. Jayaramaiah-Raja, M. Bartkuhn, R. Renkawitz, and R. Renkawitz-Pohl, “Transition from a nucleosome-based to a protamine-based chromatin configuration during spermiogenesis in Drosophila,” Journal of Cell Science, vol. 120, part 9, pp. 1689–1700, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. R. Balhorn, “The protamine family of sperm nuclear proteins,” Genome Biology, vol. 8, no. 9, article 227, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. E. Rejon, C. Bajon, A. Blaize, and D. Robert, “RNA in the nucleus of a motile plant spermatozoid: characterization by enzyme-gold cytochemistry and in situ hybridization,” Molecular Reproduction and Development, vol. 1, no. 1, pp. 49–56, 1988. View at Publisher · View at Google Scholar · View at Scopus
  11. C. A. Pessot, M. Brito, J. Figueroa, I. I. Concha, A. Yanez, and L. O. Burzio, “Presence of RNA in the sperm nucleus,” Biochemical and Biophysical Research Communications, vol. 158, no. 1, pp. 272–278, 1989. View at Publisher · View at Google Scholar · View at Scopus
  12. S. M. Wykes and S. A. Krawetz, “The structural organization of sperm chromatin,” Journal of Biological Chemistry, vol. 278, no. 32, pp. 29471–29477, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. W. W. Franke, “Nuclear envelopes: structure and biochemistry of the nuclear envelope,” Philosophical Transactions of the Royal Society of London Series B: Biological Sciences, vol. 268, no. 891, pp. 67–93, 1974. View at Publisher · View at Google Scholar · View at Scopus
  14. G. D. Johnson, C. Lalancette, A. K. Linnemann, F. Leduc, G. Boissonneault, and S. A. Krawetz, “The sperm nucleus: chromatin, RNA, and the nuclear matrix,” Reproduction, vol. 141, no. 1, pp. 21–36, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. J.-P. Dadoune, “Spermatozoal RNAs: what about their functions?” Microscopy Research and Technique, vol. 72, no. 8, pp. 536–551, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Jodar, S. Selvaraju, E. Sendler, M. P. Diamond, and S. A. Krawetz, “The presence, role and clinical use of spermatozoal RNAs,” Human Reproduction Update, vol. 19, no. 6, pp. 604–624, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Lalancette, D. Miller, Y. Li, and S. A. Krawetz, “Paternal contributions: new functional insights for spermatozoal RNA,” Journal of Cellular Biochemistry, vol. 104, no. 5, pp. 1570–1579, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. D. Miller and G. C. Ostermeier, “Towards a better understanding of RNA carriage by ejaculate spermatozoa,” Human Reproduction Update, vol. 12, no. 6, pp. 757–767, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. N. B. Hecht, “Molecular mechanisms of male germ cell differentiation,” BioEssays, vol. 20, no. 7, pp. 555–561, 1998. View at Publisher · View at Google Scholar · View at Scopus
  20. R. Balhorn, M. Cosman, K. Thornton et al., “Protamine mediated condensation of DNA in mammalian sperm,” in The Male Gamete: From Basic Science to Clinical Applications, C. Gagnon, Ed., pp. 55–70, River Press, 1999. View at Google Scholar
  21. R. E. Braun, J. J. Peschon, R. R. Behringer, R. L. Brinster, and R. D. Palmiter, “Protamine 3′-untranslated sequences regulate temporal translational control and subcellular localization of growth hormone in spermatids of transgenic mice,” Genes & Development, vol. 3, no. 6, pp. 793–802, 1989. View at Publisher · View at Google Scholar · View at Scopus
  22. T. A. Brevini-Gandolfi, L. A. Favetta, L. Mauri, A. M. Luciano, F. Cillo, and F. Gandolfi, “Changes in poly(A) tail length of maternal transcripts during in vitro maturation of bovine oocytes and their relation with developmental competence,” Molecular Reproduction and Development, vol. 52, no. 4, pp. 427–433, 1999. View at Google Scholar
  23. B. Gold, H. Fujimoto, J. M. Kramer, R. P. Erickson, and N. B. Hecht, “Haploid accumulation and translational control of phosphoglycerate kinase-2 messenger RNA during mouse spermatogenesis,” Developmental Biology, vol. 98, no. 2, pp. 392–399, 1983. View at Publisher · View at Google Scholar · View at Scopus
  24. W. Gu and Y. K. Kwon, “In postmeiotic male germ cells poly (A) shortening accompanies translation of mRNA encoding gamma enteric actin but not cytoplasmic beta and gamma actin mRNAs,” Molecular Reproduction and Development, vol. 44, no. 2, pp. 141–145, 1996. View at Publisher · View at Google Scholar
  25. H. White-Cooper and I. Davidson, “Unique aspects of transcription regulation in male germ cells,” Cold Spring Harbor Perspectives in Biology, vol. 3, no. 7, 2011. View at Google Scholar · View at Scopus
  26. B. E. Fischer, E. Wasbrough, L. A. Meadows et al., “Conserved properties of Drosophila and human spermatozoal mRNA repertoires,” Proceedings of the Royal Society B: Biological Sciences, vol. 279, no. 1738, pp. 2636–2644, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. E. Sendler, G. D. Johnson, and S. A. Krawetz, “Local and global factors affecting RNA sequencing analysis,” Analytical Biochemistry, vol. 419, no. 2, pp. 317–322, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. G. D. Johnson, E. Sendler, C. Lalancette, R. Hauser, M. P. Diamond, and S. A. Krawetz, “Cleavage of rRNA ensures translational cessation in sperm at fertilization,” Molecular Human Reproduction, vol. 17, no. 12, pp. 721–726, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. E. Sendler, G. D. Johnson, S. Mao et al., “Stability, delivery and functions of human sperm RNAs at fertilization,” Nucleic Acids Research, vol. 41, no. 7, pp. 4104–4117, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. B. Sotolongo, T. T. F. Huang, E. Isenberger, and W. S. Ward, “An endogenous nuclease in hamster, mouse, and human spermatozoa cleaves DNA into loop-sized fragments,” Journal of Andrology, vol. 26, no. 2, pp. 272–280, 2005. View at Google Scholar · View at Scopus
  31. B. Sotolongo, E. Lino, and W. S. Ward, “Ability of hamster spermatozoa to digest their own DNA,” Biology of Reproduction, vol. 69, no. 6, pp. 2029–2035, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. P. Fang, P. Zeng, Z. Wang et al., “Estimated diversity of messenger RNAs in each murine spermatozoa and their potential function during early zygotic development,” Biology of Reproduction, vol. 90, no. 5, article 94, 2014. View at Publisher · View at Google Scholar
  33. J. Kiani and M. Rassoulzadegan, “A load of small RNAs in the sperm-how many bits of hereditary information?” Cell Research, vol. 23, no. 1, pp. 18–19, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. W.-M. Liu, R. T. K. Pang, P. C. N. Chiu et al., “Sperm-borne microRNA-34c is required for the first cleavage division in mouse,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 2, pp. 490–494, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Govindaraju, A. Uzun, L. Robertson et al., “Dynamics of microRNAs in bull spermatozoa,” Reproductive Biology and Endocrinology, vol. 10, article 82, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. S. A. Krawetz, A. Kruger, C. Lalancette et al., “A survey of small RNAs in human sperm,” Human Reproduction, vol. 26, no. 12, pp. 3401–3412, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. P. C. Au, S. Frankenberg, L. Selwood, and M. Familari, “A novel marsupial pri-miRNA transcript has a putative role in gamete maintenance and defines a vertebrate miRNA cluster paralogous to the miR-15a/miR-16-1 cluster,” Reproduction, vol. 142, no. 4, pp. 539–550, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. G. Le Trionnaire and D. Twell, “Small RNAs in angiosperm gametophytes: from epigenetics to gamete development,” Genes and Development, vol. 24, no. 11, pp. 1081–1085, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. F. Bouhallier, N. Allioli, F. Lavial et al., “Role of miR-34c microRNA in the late steps of spermatogenesis,” RNA, vol. 16, no. 4, pp. 720–731, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. Z. He, M. Kokkinaki, D. Pant, G. I. Gallicano, and M. Dym, “Small RNA molecules in the regulation of spermatogenesis,” Reproduction, vol. 137, no. 6, pp. 901–911, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. R. Grant-Downton, G. le Trionnaire, R. Schmid et al., “MicroRNA and tasiRNA diversity in mature pollen of Arabidopsis thaliana,” BMC Genomics, vol. 10, article no. 643, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. R. Grant-Downton, S. Hafidh, D. Twell, and H. G. Dickinson, “Small RNA pathways are present and functional in the angiosperm male gametophyte,” Molecular Plant, vol. 2, no. 3, pp. 500–512, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. C. Chambers and B. Shuai, “Profiling microRNA expression in Arabidopsis pollen using microRNA array and real-time PCR,” BMC Plant Biology, vol. 9, article 87, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. E. Marcon, T. Babak, G. Chua, T. Hughes, and P. B. Moens, “miRNA and piRNA localization in the male mammalian meiotic nucleus,” Chromosome Research, vol. 16, no. 2, pp. 243–260, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. S. T. Grivna, E. Beyret, Z. Wang, and H. Lin, “A novel class of small RNAs in mouse spermatogenic cells,” Genes and Development, vol. 20, no. 13, pp. 1709–1714, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. G. C. Ostermeier, R. J. Goodrich, J. S. Moldenhauer, M. P. Diamond, and S. A. Krawetz, “A suite of novel human spermatozoal RNAs,” Journal of Andrology, vol. 26, no. 1, pp. 70–74, 2005. View at Google Scholar · View at Scopus
  47. Y. Gur and H. Breitbart, “Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes,” Genes & Development, vol. 20, no. 4, pp. 411–416, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. C. Zhao, X.-J. Guo, Z.-H. Shi et al., “Role of translation by mitochondrial-type ribosomes during sperm capacitation: an analysis based on a proteomic approach,” Proteomics, vol. 9, no. 5, pp. 1385–1399, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. D. Ickowicz, M. Finkelstein, and H. Breitbart, “Mechanism of sperm capacitation and the acrosome reaction: role of protein kinases,” Asian Journal of Andrology, vol. 14, no. 6, pp. 816–821, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. P. E. Visconti, D. Krapf, J. L. de la Vega-Beltrán, J. J. Acevedo, and A. Darszon, “Ion channels, phosphorylation and mammalian sperm capacitation,” Asian Journal of Andrology, vol. 13, no. 3, pp. 395–405, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. M. A. Baker, “The 'omics revolution and our understanding of sperm cell biology,” Asian Journal of Andrology, vol. 13, no. 1, pp. 6–10, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. R. R. Zhou, B. Wang, J. Wang, H. Schatten, and Y. Z. Zhang, “Is the mitochondrial cloud the selection machinery for preferentially transmitting wild-type mtDNA between generations? Rewinding müller’s ratchet efficiently,” Current Genetics, vol. 56, no. 2, pp. 101–107, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Markewitz, S. Graff, and R. J. Veenema, “Absence of RNA synthesis in shed human spermatozoa,” Nature, vol. 214, no. 5086, pp. 402–403, 1967. View at Publisher · View at Google Scholar · View at Scopus
  54. C. Díez-Sánchez, E. Ruiz-Pesini, J. Montoya, A. Pérez-Martos, J. A. Enríquez, and M. J. López-Pérez, “Mitochondria from ejaculated human spermatozoa do not synthesize proteins,” FEBS Letters, vol. 553, no. 1-2, pp. 205–208, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. D. Miller, P. Z. Tang, C. Skinner, and R. Lilford, “Differential RNA fingerprinting as a tool in the analysis of spermatozoal gene expression,” Human Reproduction, vol. 9, no. 5, pp. 864–869, 1994. View at Google Scholar · View at Scopus
  56. D. Miller, D. Briggs, H. Snowden et al., “A complex population of RNAs exists in human ejaculate spermatozoa: implications for understanding molecular aspects of spermiogenesis,” Gene, vol. 237, no. 2, pp. 385–392, 1999. View at Publisher · View at Google Scholar · View at Scopus
  57. S. M. Wykes, D. W. Visscher, and S. A. Krawetz, “Haploid transcripts persist in mature human spermatozoa,” Molecular Human Reproduction, vol. 3, no. 1, pp. 15–19, 1997. View at Publisher · View at Google Scholar · View at Scopus
  58. I. I. Concha, U. Urzua, A. Yanez, R. Schroeder, C. Pessot, and L. O. Burzio, “U1 and U2 snRNA are localized in the sperm nucleus,” Experimental Cell Research, vol. 204, no. 2, pp. 378–381, 1993. View at Publisher · View at Google Scholar · View at Scopus
  59. A. H. Balen and H. S. Jacobs, Infertility in Practice, Churchill Livingstone, 2003.
  60. R. H. Foote, “Value of testicular and sperm profiles in optimizing reproductive success: lessons learned from selective breeding programs of domestic and laboratory animals,” Progress in Clinical and Biological Research, vol. 302, pp. 107–126, 1989. View at Google Scholar · View at Scopus
  61. K. A. Abraham and P. M. Bhargava, “Nucleic acid metabolism of mammalian spermatozoa,” The Biochemical journal, vol. 86, pp. 298–307, 1963. View at Google Scholar · View at Scopus
  62. P. M. Bhargava, “Incorporation of radioactive amino-acids in the proteins of bull spermatozoa,” Nature, vol. 179, no. 4570, pp. 1120–1121, 1957. View at Publisher · View at Google Scholar · View at Scopus
  63. F. Martin and J. Brachet, “Autoradiographic studies on the incorporation of amino acids into spermatozoa,” Experimental Cell Research, vol. 17, no. 3, pp. 399–404, 1959. View at Publisher · View at Google Scholar · View at Scopus
  64. J. C. White, I. Leslie, and J. N. Davidson, “Nucleic acids of bone marrow cells, with special reference to pernicious anaemia,” The Journal of Pathology and Bacteriology, vol. 66, no. 1, pp. 291–306, 1953. View at Publisher · View at Google Scholar · View at Scopus
  65. C. M. Mauritzen, A. B. Roy, and E. Stedman, “The ribosenucleic acid content of isolated cell nuclei,” Proceedings of the Royal Society B: Biological Sciences, vol. 140, no. 898, pp. 18–31, 1952. View at Google Scholar · View at Scopus
  66. J. MacLaughlin and C. Terner, “Ribonucleic acid synthesis by spermatozoa from the rat and hamster,” Biochemical Journal, vol. 133, no. 4, pp. 635–639, 1973. View at Google Scholar · View at Scopus
  67. E. Premkumar and P. M. Bhargava, “Transcription and translation in bovine spermatozoa,” Nature: New biology, vol. 240, no. 100, pp. 139–143, 1972. View at Google Scholar · View at Scopus
  68. C. J. Betlach and R. P. Erickson, “28 s and 18 s ribonucleic acid from mammalian spermatozoa.,” Journal of Experimental Zoology, vol. 198, no. 1, pp. 49–55, 1976. View at Publisher · View at Google Scholar · View at Scopus
  69. N. Bissonnette, J.-P. Lévesque-Sergerie, C. Thibault, and G. Boissonneault, “Spermatozoal transcriptome profiling for bull sperm motility: a potential tool to evaluate semen quality,” Reproduction, vol. 138, no. 1, pp. 65–80, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. S. A. Krawetz, “Paternal contribution: new insights and future challenges,” Nature Reviews Genetics, vol. 6, no. 8, pp. 633–642, 2005. View at Publisher · View at Google Scholar · View at Scopus
  71. H. Cappallo-Obermann, W. Schulze, H. Jastrow, V. Baukloh, and A.-N. Spiess, “Highly purified spermatozoal RNA obtained by a novel method indicates an unusual 28S/18S rRNA ratio and suggests impaired ribosome assembly,” Molecular Human Reproduction, vol. 17, no. 11, pp. 669–678, 2011. View at Publisher · View at Google Scholar · View at Scopus
  72. T. G. Cooper, “Cytoplasmic droplets: the good, the bad or just confusing?” Human Reproduction, vol. 20, no. 1, pp. 9–11, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. T. G. Cooper and C.-H. Yeung, “Acquisition of volume regulatory response of sperm upon maturation in the epididymis and the role of the cytoplasmic droplet,” Microscopy Research and Technique, vol. 61, no. 1, pp. 28–38, 2003. View at Publisher · View at Google Scholar · View at Scopus
  74. C. J. Card, E. J. Anderson, S. Zamberlan, K. E. Krieger, M. Kaproth, and B. L. Sartini, “Cryopreserved bovine spermatozoal transcript profile as revealed by high-throughput ribonucleic acid sequencing,” Biology of Reproduction, vol. 88, no. 2, article 49, 2013. View at Publisher · View at Google Scholar · View at Scopus
  75. J. M. Feugang, N. Rodriguez-Osorio, A. Kaya et al., “Transcriptome analysis of bull spermatozoa: implications for male fertility,” Reproductive BioMedicine Online, vol. 21, no. 3, pp. 312–324, 2010. View at Publisher · View at Google Scholar · View at Scopus
  76. I. Gilbert, N. Bissonnette, G. Boissonneault, M. Vallée, and C. Robert, “A molecular analysis of the population of mRNA in bovine spermatozoa,” Reproduction, vol. 133, no. 6, pp. 1073–1086, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. C. Lalancette, C. Thibault, I. Bachand, N. Caron, and N. Bissonnette, “Transcriptome analysis of bull semen with extreme nonreturn rate: Use of suppression-subtractive hybridization to identify functional markers for fertility,” Biology of Reproduction, vol. 78, no. 4, pp. 618–635, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. Y. Zhao, Q. Li, C. Yao et al., “Characterization and quantification of mRNA transcripts in ejaculated spermatozoa of fertile men by serial analysis of gene expression,” Human Reproduction, vol. 21, no. 6, pp. 1583–1590, 2006. View at Publisher · View at Google Scholar · View at Scopus
  79. C. C. Yang, Y. S. Lin, C. C. Hsu, S. C. Wu, E. C. Lin, and W. T. K. Cheng, “Identification and sequencing of remnant messenger RNAs found in domestic swine (Sus scrofa) fresh ejaculated spermatozoa,” Animal Reproduction Science, vol. 113, no. 1–4, pp. 143–155, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. P. J. Das, F. McCarthy, M. Vishnoi et al., “Stallion sperm transcriptome comprises functionally coherent coding and regulatory RNAs as revealed by microarray analysis and RNA-seq,” PLoS ONE, vol. 8, no. 2, Article ID e56535, 2013. View at Publisher · View at Google Scholar · View at Scopus
  81. G. C. Ostermeier, D. Miller, J. D. Huntriss, M. P. Diamond, and S. A. Krawetz, “Reproductive biology: delivering spermatozoan RNA to the oocyte,” Nature, vol. 429, no. 6988, article 154, 2004. View at Google Scholar · View at Scopus
  82. D. Miller, “Analysis and significance of messenger RNA in human ejaculated spermatozoa,” Molecular Reproduction and Development, vol. 56, supplement 2, pp. 259–264, 2000. View at Google Scholar · View at Scopus
  83. D. Bourc’his and O. Voinnet, “A small-RNA perspective on gametogenesis, fertilization, and early zygotic development,” Science, vol. 330, no. 6004, pp. 617–622, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. A. E. Peaston, B. B. Knowles, and K. W. Hutchison, “Genome plasticity in the mouse oocyte and early embryo,” Biochemical Society Transactions, vol. 35, part 3, pp. 618–622, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. T. Kono, Y. Obata, Q. Wu et al., “Birth of parthenogenetic mice that can develop to adulthood,” Nature, vol. 428, no. 6985, pp. 860–864, 2004. View at Publisher · View at Google Scholar · View at Scopus
  86. D. Miller, M. Brinkworth, and D. Iles, “Paternal DNA packaging in spermatozoa: more than the sum of its parts? DNA, histones, protamines and epigenetics,” Reproduction, vol. 139, no. 2, pp. 287–301, 2010. View at Publisher · View at Google Scholar · View at Scopus
  87. M. Pavone, J. Innes, J. Hirshfeld-Cytron, R. Kazer, and J. Zhang, “Comparing thaw survival, implantation and live birth rates from cryopreserved zygotes, embryos and blastocysts,” Journal of Human Reproductive Sciences, vol. 4, no. 1, pp. 23–28, 2011. View at Publisher · View at Google Scholar · View at Scopus
  88. S. Lambard, I. Galeraud-Denis, G. Martin, R. Levy, A. Chocat, and S. Carreau, “Analysis and significance of mRNA in human ejaculated sperm from normozoospermic donors: relationship to sperm motility and capacitation,” Molecular Human Reproduction, vol. 10, no. 7, pp. 535–541, 2004. View at Publisher · View at Google Scholar · View at Scopus
  89. R. Oliva, “Protamines and male infertility,” Human Reproduction Update, vol. 12, no. 4, pp. 417–435, 2006. View at Publisher · View at Google Scholar · View at Scopus
  90. C. Cho, H. Jung-Ha, W. D. Willis et al., “Protamine 2 deficiency leads to sperm DNA damage and embryo death in mice,” Biology of Reproduction, vol. 69, no. 1, pp. 211–217, 2003. View at Publisher · View at Google Scholar · View at Scopus
  91. S. García-Herrero, N. Garrido, J. A. Martínez-Conejero, J. Remohí, A. Pellicer, and M. Meseguer, “Differential transcriptomic profile in spermatozoa achieving pregnancy or not via ICSI,” Reproductive BioMedicine Online, vol. 22, no. 1, pp. 25–36, 2011. View at Publisher · View at Google Scholar · View at Scopus
  92. N. Garrido, J. A. Martínez-Conejero, J. Jauregui et al., “Microarray analysis in sperm from fertile and infertile men without basic sperm analysis abnormalities reveals a significantly different transcriptome,” Fertility and Sterility, vol. 91, no. 4, pp. 1307–1310, 2009. View at Publisher · View at Google Scholar · View at Scopus
  93. WHO, WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction, World Health Organisation, 1999.
  94. S. Bonache, A. Mata, M. D. Ramos, L. Bassas, and S. Larriba, “Sperm gene expression profile is related to pregnancy rate after insemination and is predictive of low fecundity in normozoospermic men,” Human Reproduction, vol. 27, no. 6, pp. 1556–1567, 2012. View at Publisher · View at Google Scholar · View at Scopus
  95. A. E. Platts, D. J. Dix, H. E. Chemes et al., “Success and failure in human spermatogenesis as revealed by teratozoospermic RNAs,” Human Molecular Genetics, vol. 16, no. 7, pp. 763–773, 2007. View at Publisher · View at Google Scholar · View at Scopus
  96. A. N. Yatsenko, A. Roy, R. Chen et al., “Non-invasive genetic diagnosis of male infertility using spermatozoal RNA: KLHL 10 mutations in oligozoospermic patients impair homodimerization,” Human Molecular Genetics, vol. 15, no. 23, pp. 3411–3419, 2006. View at Publisher · View at Google Scholar · View at Scopus
  97. V. Grandjean, P. Gounon, N. Wagner et al., “The miR-124-Sox9 paramutation: RNA-mediated epigenetic control of embryonic and adult growth,” Development, vol. 136, no. 21, pp. 3647–3655, 2009. View at Publisher · View at Google Scholar · View at Scopus
  98. X. Liang, D. Zhou, C. Wei et al., “MicroRNA-34c enhances murine male germ cell apoptosis through targeting ATF1,” PLoS ONE, vol. 7, no. 3, Article ID e33861, 2012. View at Publisher · View at Google Scholar · View at Scopus
  99. C. P. Concepcion, Y.-C. Han, P. Mu et al., “Intact p53-dependent responses in miR-34-deficient mice,” PLoS Genetics, vol. 8, no. 7, Article ID e1002797, 2012. View at Publisher · View at Google Scholar · View at Scopus
  100. M. D. Anway, A. S. Cupp, N. Uzumcu, and M. K. Skinner, “Epigenetic transgenerational actions of endocrine disruptors and male fertility,” Science, vol. 308, no. 5727, pp. 1466–1469, 2005. View at Publisher · View at Google Scholar · View at Scopus
  101. J. Bender, “RNA-directed DNA methylation: getting a grip on mechanism,” Current Biology, vol. 22, no. 10, pp. R400–R401, 2012. View at Publisher · View at Google Scholar · View at Scopus
  102. C. Belleannée, É. Calvo, J. Caballero, and R. Sullivan, “Epididymosomes convey different repertoires of micrornas throughout the bovine epididymis,” Biology of Reproduction, vol. 89, no. 2, article 30, 2013. View at Publisher · View at Google Scholar · View at Scopus
  103. J. Caballero, G. Frenette, and R. Sullivan, “Post testicular sperm maturational changes in the bull: important role of the epididymosomes and prostasomes,” Veterinary Medicine International, vol. 2011, Article ID 757194, 13 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  104. A. Etheridge, C. P. C. Gomes, R. W. Pereira, D. Galas, and K. Wang, “The complexity, function, and applications of RNA in circulation,” Frontiers in Genetics, vol. 4, article 115, 2013. View at Publisher · View at Google Scholar · View at Scopus
  105. A. Dean and R. M. Sharpe, “Anogenital distance or digit length ratio as measures of fetal androgen exposure: relationship to male reproductive development and its disorders,” Journal of Clinical Endocrinology and Metabolism, vol. 98, no. 6, pp. 2230–2238, 2013. View at Publisher · View at Google Scholar · View at Scopus
  106. N. E. Skakkebæk, E. Rajpert-De Meyts, and K. M. Main, “Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects,” Human Reproduction, vol. 16, no. 5, pp. 972–978, 2001. View at Publisher · View at Google Scholar · View at Scopus
  107. P. M. Foster, E. Mylchreest, K. W. Gaido, and M. Sar, “Effects of phthalate esters on the developing reproductive tract of male rats,” Human Reproduction Update, vol. 7, no. 3, pp. 231–235, 2001. View at Publisher · View at Google Scholar · View at Scopus
  108. J. R. Seckl and M. C. Holmes, “Mechanisms of disease: glucocorticoids, their placental metabolism and fetal 'programming' of adult pathophysiology,” Nature Clinical Practice Endocrinology and Metabolism, vol. 3, no. 6, pp. 479–488, 2007. View at Publisher · View at Google Scholar · View at Scopus
  109. J. Lamarck, Philosophie zoologique ou exposition des considérations relatives à l'histoire naturelle des animaux, University of California Press, 1809.
  110. R. W. Burkhardt Jr., “Lamarck, evolution, and the inheritance of acquired characters,” Genetics, vol. 194, no. 4, pp. 793–805, 2013. View at Publisher · View at Google Scholar · View at Scopus
  111. W. Reik, K. Davies, W. Dean, G. Kelsey, and M. Constância, “Imprinted genes and the coordination of fetal and postnatal growth in mammals,” Novartis Foundation Symposium, vol. 237, pp. 19–35, 2001. View at Google Scholar · View at Scopus
  112. P. Hajkova, S. Erhardt, N. Lane et al., “Epigenetic reprogramming in mouse primordial germ cells,” Mechanisms of Development, vol. 117, no. 1-2, pp. 15–23, 2002. View at Publisher · View at Google Scholar · View at Scopus
  113. C. Pittoggi, L. Renzi, G. Zaccagnini et al., “A fraction of mouse sperm chromatin is organized in nucleosomal hypersensitive domains enriched in retroposon DNA,” Journal of Cell Science, vol. 112, no. 20, pp. 3537–3548, 1999. View at Google Scholar · View at Scopus
  114. M. Benchaib, V. Braun, D. Ressnikof et al., “Influence of global sperm DNA methylation on IVF results,” Human Reproduction, vol. 20, no. 3, pp. 768–773, 2005. View at Publisher · View at Google Scholar · View at Scopus
  115. S. Houshdaran, V. K. Cortessis, K. Siegmund, A. Yang, P. W. Laird, and R. Z. Sokol, “Widespread epigenetic abnormalities suggest a broad DNA methylation erasure defect in abnormal human sperm,” PLoS ONE, vol. 2, no. 12, Article ID e1289, 2007. View at Publisher · View at Google Scholar · View at Scopus
  116. P. N. Moreira, R. Fernández-González, D. Rizos, M. Ramirez, M. Perez-Crespo, and A. Gutiérrez-Adán, “Inadvertent transgenesis by conventional ICSI in mice,” Human Reproduction, vol. 20, no. 12, pp. 3313–3317, 2005. View at Publisher · View at Google Scholar · View at Scopus
  117. K. Smith and C. Spadafora, “Sperm-mediated gene transfer: applications and implications,” BioEssays, vol. 27, no. 5, pp. 551–562, 2005. View at Publisher · View at Google Scholar · View at Scopus
  118. A. Vargiolu, S. Manzini, M. De Cecco et al., “In vitro production of multigene transgenic blastocysts via sperm-mediated gene transfer allows rapid screening of constructs to be used in xenotransplantation experiments,” Transplantation Proceedings, vol. 42, no. 6, pp. 2142–2145, 2010. View at Publisher · View at Google Scholar · View at Scopus
  119. C. Cossetti, L. Lugini, L. Astrologo, I. Saggio, S. Fais, and C. Spadafora, “Soma-to-germline transmission of RNA in mice xenografted with human tumour cells: possible transport by exosomes,” PloS one, vol. 9, no. 7, Article ID e101629, 2014. View at Publisher · View at Google Scholar
  120. K. Gapp, L. von Ziegler, R. Y. Tweedie-Cullen, and I. M. Mansuy, “Early life epigenetic programming and transmission of stress-induced traits in mammals: how and when can environmental factors influence traits and their transgenerational inheritance?” BioEssays, vol. 36, no. 5, pp. 491–502, 2014. View at Publisher · View at Google Scholar · View at Scopus