About this Journal Submit a Manuscript Table of Contents
Journal of Biomedicine and Biotechnology
Volume 2010 (2010), Article ID 369549, 29 pages
http://dx.doi.org/10.1155/2010/369549
Research Article

Differential Expression of MicroRNAs between Eutopic and Ectopic Endometrium in Ovarian Endometriosis

1Laboratory of Oncological Gynecology, Department of Clinical and Experimental Medicine, and Biotechnology Center for Applied Medical Research, University of Piemonte Orientale “Amedeo Avogadro”, 28100 Novara, Italy
2Laboratory of Biochemistry, Department of Clinical and Experimental Medicine, and Biotechnology Center for Applied Medical Research, University of Piemonte Orientale “Amedeo Avogadro”, 28100 Novara, Italy

Received 12 March 2009; Revised 10 August 2009; Accepted 19 December 2009

Academic Editor: Sorin Draghici

Copyright © 2010 Nicoletta Filigheddu 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. R. F. Kruitwagen, L. G. Poels, W. N. P. Willemsen, I. J. Y. de Ronde, P. H. K. Jap, and R. Rolland, “Endometrial epithelial cells in peritoneal fluid during the early follicular phase,” Fertility and Sterility, vol. 55, no. 2, pp. 297–303, 1991. View at Scopus
  2. W. P. Dmowski, R. W. Steele, and G. F. Baker, “Deficient cellular immunity in endometriosis,” American Journal of Obstetrics and Gynecology, vol. 141, no. 4, pp. 377–383, 1981. View at Scopus
  3. S. M. Gilmore, S. Aksel, C. Hoff, and R. D. A. Peterson, “In vitro lymphocyte activity in women with endometriosis—an altered immune response?” Fertility and Sterility, vol. 58, no. 6, pp. 1148–1152, 1992. View at Scopus
  4. S. Z. A. Badawy, V. Cuenca, H. Freliech, and C. Stefanu, “Endometrial antibodies in serum and peritoneal fluid of infertile patients with and without endometriosis,” Fertility and Sterility, vol. 53, no. 5, pp. 930–932, 1990. View at Scopus
  5. P. V. Taylor, M. D. Maloney, J. M. Campbell, et al., “Autoreactivity in women with endometriosis,” British Journal of Obstetrics and Gynaecology, vol. 98, no. 7, pp. 680–684, 1991. View at Scopus
  6. A. F. Haney, J. J. Muscato, and J. B. Weinberg, “Peritoneal fluid cell populations in infertility patients,” Fertility and Sterility, vol. 35, no. 6, pp. 696–698, 1981. View at Scopus
  7. L. Van Le, S.-T. Oh, J. A. Anners, C. A. Rinehart, and J. Halme, “Interleukin-1 inhibits growth of normal human endometrial stromal cells,” Obstetrics and Gynecology, vol. 80, no. 3, pp. 405–409, 1992. View at Scopus
  8. D. Semer, K. Reisler, P. C. MacDonald, and M. L. Casey, “Responsiveness of human endometrial stromal cells to cytokines,” Annals of the New York Academy of Sciences, vol. 622, pp. 99–110, 1991.
  9. N. Rana, D. P. Braun, R. House, H. Gebel, C. Rotman, and W. P. Dmowski, “Basal and stimulated secretion of cytokines by peritoneal macrophages in women with endometriosis,” Fertility and Sterility, vol. 65, no. 5, pp. 925–930, 1996. View at Scopus
  10. S. E. Rier, A. K. Parsons, and J. L. Becker, “Altered interleukin-6 production by peritoneal leukocytes from patients with endometriosis,” Fertility and Sterility, vol. 61, no. 2, pp. 294–299, 1994. View at Scopus
  11. I. E. Sasson and H. S. Taylor, “Stem cells and the pathogenesis of endometriosis,” Annals of the New York Academy of Sciences, vol. 1127, pp. 106–115, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. S. Kennedy, R. Hadfield, C. Westbrook, D. E. Weeks, D. Barlow, and S. Golding, “Magnetic resonance imaging to assess familial risk in relatives of women with endometriosis,” The Lancet, vol. 352, no. 9138, pp. 1440–1441, 1998. View at Publisher · View at Google Scholar · View at Scopus
  13. J. L. Simpson, S. Elias, L. R. Malinak, and V. C. Buttram Jr., “Heritable aspects of endometriosis. I. Genetic studies,” American Journal of Obstetrics and Gynecology, vol. 137, no. 3, pp. 327–331, 1980. View at Scopus
  14. D. Coxhead and E. J. Thomas, “Familial inheritance of endometriosis in a British population. A case control study,” Journal of Obstetrics and Gynaecology, vol. 13, no. 1, pp. 42–44, 1993. View at Scopus
  15. M. H. Moen and P. Magnus, “The familial risk of endometriosis,” Acta Obstetricia et Gynecologica Scandinavica, vol. 72, no. 7, pp. 560–564, 1993. View at Scopus
  16. S. Kennedy, R. Hadfield, H. Mardon, and D. Barlow, “Age of onset of pain symptoms in non-twin sisters concordant for endometriosis,” Human Reproduction, vol. 11, no. 2, pp. 403–405, 1996. View at Scopus
  17. S. Kennedy, “The genetics of endometriosis,” European Journal of Obstetrics Gynecology and Reproductive Biology, vol. 82, no. 2, pp. 129–133, 1999. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Kennedy, S. Bennett, and D. E. Weeks, “Affected sib-pair analysis in endometriosis,” Human Reproduction Update, vol. 7, no. 4, pp. 411–418, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Meola, J. C. Rosa e Silva, D. B. Dentillo, et al., “Differentially expressed genes in eutopic and ectopic endometrium of women with endometriosis,” 2009, Fertility and Sterility. [Epub ahead of print]. View at Publisher · View at Google Scholar · View at PubMed
  20. H. Honda, F. F. Barrueto, J. Gogusev, D. D. Im, and P. J. Morin, “Serial analysis of gene expression reveals differential expression between endometriosis and normal endometrium. Possible roles for AXL and SHC1 in the pathogenesis of endometriosis,” Reproductive Biology and Endocrinology, vol. 6, article 59, 2008. View at Publisher · View at Google Scholar · View at PubMed
  21. W.-P. Hu, S. K. Tay, and Y. Zhao, “Endometriosis-specific genes identified by real-time reverse transcription-polymerase chain reaction expression profiling of endometriosis versus autologous uterine endometrium,” Journal of Clinical Endocrinology and Metabolism, vol. 91, no. 1, pp. 228–238, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. Y. Wu, A. Kajdacsy-Balla, E. Strawn, et al., “Transcriptional characterizations of differences between eutopic and ectopic endometrium,” Endocrinology, vol. 147, no. 1, pp. 232–246, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  23. K. M. Eyster, O. Klinkova, V. Kennedy, and K. A. Hansen, “Whole genome deoxyribonucleic acid microarray analysis of gene expression in ectopic versus eutopic endometrium,” Fertility and Sterility, vol. 88, no. 6, pp. 1505–1533, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. M. L. Hull, C. R. Escareno, J. M. Godsland, et al., “Endometrial-peritoneal interactions during endometriotic lesion establishment,” American Journal of Pathology, vol. 173, no. 3, pp. 700–715, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. R. C. Lee, R. L. Feinbaum, and V. Ambros, “The C. elegance heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14,” Cell, vol. 75, pp. 843–854, 1993.
  26. E. C. Lai, P. Tomancak, R. W. Williams, and G. M. Rubin, “Computational identification of Drosophila microRNA genes,” Genome Biology, vol. 4, no. 7, article R42, 2003.
  27. L. P. Lim, N. C. Lau, E. G. Weinstein, et al., “The microRNAs of Caenorhabditis elegans,” Genes and Development, vol. 17, no. 8, pp. 991–1008, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  28. L. P. Lim, N. C. Lau, P. Garrett-Engele, et al., “Microarray analysis shows that some microRNAs downregulate large numbers of-target mRNAs,” Nature, vol. 433, no. 7027, pp. 769–773, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  29. B. P. Lewis, C. B. Burge, and D. P. Bartel, “Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets,” Cell, vol. 120, no. 1, pp. 15–20, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. P. Xu, S. Y. Vernooy, M. Guo, and B. A. Hay, “The Drosophila microRNA mir-14 suppresses cell death and is required for normal fat metabolism,” Current Biology, vol. 13, no. 9, pp. 790–795, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Brennecke, D. R. Hipfner, A. Stark, R. B. Russell, and S. M. Cohen, “bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila,” Cell, vol. 113, no. 1, pp. 25–36, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Dostie, Z. Mourelatos, M. Yang, A. Sharma, and G. Dreyfuss, “Numerous microRNPs in neuronal cells containing novel microRNAs,” RNA, vol. 9, no. 2, pp. 180–186, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Dostie, Z. Mourelatos, M. Yang, A. Sharma, and G. Dreyfuss, “Erratum: numerous microRNPs in neuronal cells containing novel microRNAs,” RNA, vol. 9, no. 5, pp. 631–632, 2003.
  34. V. Ambros, “The functions of animal microRNAs,” Nature, vol. 431, no. 7006, pp. 350–355, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  35. B. M. Engels and G. Hutvagner, “Principles and effects of microRNA-mediated post-transcriptional gene regulation,” Oncogene, vol. 25, no. 46, pp. 6163–6169, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. M. Jovanovic and M. O. Hengartner, “miRNAs and apoptosis: RNAs to die for,” Oncogene, vol. 25, no. 46, pp. 6176–6187, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. R. Garzon, M. Fabbri, A. Cimmino, G. A. Calin, and C. M. Croce, “MicroRNA expression and function in cancer,” Trends in Molecular Medicine, vol. 12, no. 12, pp. 580–587, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. G. A. Calin and C. M. Croce, “MicroRNA signatures in human cancers,” Nature Reviews Cancer, vol. 6, no. 11, pp. 857–866, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. M. Canis, J. G. Donnez, D. S. Guzick, et al., “Revised american society for reproductive medicine classification of endometriosis: 1996,” Fertility and Sterility, vol. 67, no. 5, pp. 817–821, 1997. View at Publisher · View at Google Scholar · View at Scopus
  40. X. Gao, E. Gulari, and X. Zhou, “In situ synthesis of oligonucleotide microarrays,” Biopolymers, vol. 73, no. 5, pp. 579–596, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. Q. Zhu, A. Hong, N. Sheng, et al., “microParaflo biochip for nucleic acid and protein analysis,” Methods in Molecular Biology, vol. 382, pp. 287–312, 2007. View at Scopus
  42. B. M. Bolstad, R. A. Irizarry, M. Astrandand, and T. P. Speed, “A comparison of normalization methods for high density oligonucleotide array data based on variance and bias,” Bioinformatics, vol. 19, no. 2, pp. 185–193, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. W. Pan, “A comparative review of statistical methods for discovering differentially expressed genes in replicated microarray experiments,” Bioinformatics, vol. 18, no. 4, pp. 546–554, 2002. View at Scopus
  44. M. B. Eisen, P. T. Spellman, P. O. Brown, and D. Botstein, “Cluster analysis and display of genome-wide expression patterns,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 25, pp. 14863–14868, 1998. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Fabbri, R. Garzon, A. Cimmino, et al., “MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 40, pp. 15805–15810, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  46. A. M. Duursma, M. Kedde, M. Schrier, C. le Sage, and R. Agami, “miR-148 targets human DNMT3b protein coding region,” RNA, vol. 14, no. 5, pp. 872–877, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. P. A. Jones and S. B. Baylin, “The epigenomics of cancer,” Cell, vol. 128, no. 4, pp. 683–692, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  48. Y. Wu, E. Strawn, Z. Basir, G. Halverson, and S.-W. Guo, “Aberrant expression of deoxyribonucleic acid methyltransferases DNMT1, DNMT3A, and DNMT3B in women with endometriosis,” Fertility and Sterility, vol. 87, no. 1, pp. 24–32, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  49. A. Kharfi, Y. Labelle, J. Mailloux, and A. Akoum, “Deficient expression of tumor necrosis factor receptor type 2 in the endometrium of women with endometriosis,” American Journal of Reproductive Immunology, vol. 50, no. 1, pp. 33–40, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. Y. S. Antsiferova, N. Yu. Sotnikova, L. V. Posiseeva, and A. L. Shor, “Changes in the T-helper cytokine profile and in lymphocyte activation at the systemic and local levels in women with endometriosis,” Fertility and Sterility, vol. 84, no. 6, pp. 1705–1711, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  51. O. A. Odukoya, R. Ajjan, K. Lim, P. F. Watson, A. P. Weetman, and I. D. Cooke, “The pattern of cytokine mRNA expression in ovarian endometriomata,” Molecular Human Reproduction, vol. 3, no. 5, pp. 393–397, 1997. View at Scopus
  52. T. Tsudo, T. Harada, T. Iwabe, et al., “Altered gene expression and secretion of interleukin-6 in stromal cells derived from endometriotic tissues,” Fertility and Sterility, vol. 73, no. 2, pp. 205–211, 2000. View at Publisher · View at Google Scholar · View at Scopus
  53. C. M. Kyama, L. Overbergh, S. Debrock, et al., “Increased peritoneal and endometrial gene expression of biologically relevant cytokines and growth factors during the menstrual phase in women with endometriosis,” Fertility and Sterility, vol. 85, no. 6, pp. 1667–1675, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  54. R. O. Burney, S. Talbi, A. E. Hamilton, et al., “Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis,” Endocrinology, vol. 148, no. 8, pp. 3814–3826, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. K. Shazand, S. Baban, C. Prive, et al., “FOXO1 and c-jun transcription factors mRNA are modulated in endometriosis,” Molecular Human Reproduction, vol. 10, no. 12, pp. 871–877, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  56. S. Matsuzaki, M. Canis, C. Vaurs-Barrière, O. Boespflug-Tanguy, B. Dastugue, and G. Mage, “DNA microarray analysis of gene expression in eutopic endometrium from patients with deep endometriosis using laser capture microdissection,” Fertility and Sterility, vol. 84, supplement 2, pp. 1180–1190, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  57. P. A. Gregory, A. G. Bert, E. L. Paterson, et al., “The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1,” Nature Cell Biology, vol. 10, no. 5, pp. 593–601, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  58. P. Khatri, P. Bhavsar, G. Bawa, and S. Draghici, “Onto-tools: an ensemble of web-accessible ontology-based tools for the functional design and interpretation of high-throughput gene expression experiments,” Nucleic Acids Research, vol. 32, pp. W449–W456, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  59. S. Draghici, P. Khatri, A. L. Tarca, et al., “A systems biology approach for pathway level analysis,” Genome Research, vol. 17, no. 10, pp. 1537–1545, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  60. Y. Zhou, R.-A. F. Gunput, and R. J. Pasterkamp, “Semaphorin signaling: progress made and promises ahead,” Trends in Biochemical Sciences, vol. 33, no. 4, pp. 161–170, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  61. F. Shen, X. Liu, J.-G. Geng, and S.-W. Guo, “Increased immunoreactivity to SLIT/ROBO1 in ovarian endometriomas: a likely constituent biomarker for recurrence,” American Journal of Pathology, vol. 175, no. 2, pp. 479–488, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  62. Q. Pan, X. Luo, T. Toloubeydokhti, and N. Chegini, “The expression profile of micro-RNA in endometrium and endometriosis and the influence of ovarian steroids on their expression,” Molecular Human Reproduction, vol. 13, no. 11, pp. 797–806, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  63. E. M. C. O. Teague, K. H. Van der Hoek, M. B. Van der Hoek, et al., “MicroRNA-regulated pathways associated with endometriosis,” Molecular Endocrinology, vol. 23, no. 2, pp. 265–275, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus