Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지

Spatio-temporal Expression and Regulation of Dermatopontin in the Early Pregnant Mouse Uterus

  • Kim, Hyun Sook (Department of Biology, Collage of Natural Sciences, Sungshin Women's University) ;
  • Cheon, Yong-Pil (Department of Biology, Collage of Natural Sciences, Sungshin Women's University)
  • Received : 2006.05.09
  • Accepted : 2006.10.16
  • Published : 2006.12.31
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Abstract

During endometrial differentiation the extracellular matrix (ECM) changes dramatically to prepare for implantation of the embryo. However, the genes regulating the ECM build-up in the uterine endometrium during early pregnancy are not well known. Using the PCR-select cDNA subtraction method, dermatopontin was identified in the uterus of a pregnant mouse on day 4 of gestation. Dermatopontin mRNA increased dramatically on day 3, and was at its highest level at the time of implantation. Administration of RU 486 significantly inhibited mRNA expression by day 4 of gestation, but ICI 182,780 did not. Progesterone markedly induced dermatopontin expression in ovariectomized uteri within 4 h of administration, whereas estrogen had little effect. In silico analysis revealed progesterone receptor binding sites in the dermatopontin promoter region. Decidualization did not induce expression of dermatopontin; instead dermatopontin mRNA became strongly localized at the interimplantation site. In situ hybridization revealed that expression gradually decreased in the luminal epithelial cells as pregnancy progressed, whereas it increased in the stromal cells. The pattern of localization and the changes of intensity of dermatopontin mRNA coincided with those of collagen. Collectively, these results strongly suggest that dermatopontin expression is steroid-dependent. They also suggest that, at the time of implantation, dermatopontin expression is primarily regulated spatio-temporally by progesterone via progesterone receptors, and is modulated by the decidual response during implantation. Dermatopontin may be one of the regulators used to remodel the uterine ECM for pregnancy.

Keywords

Acknowledgement

Supported by : Sungshin Women's University

References

  1. Aigner, A., Butscheid, M., Kunkel, P., Krause, E., Lamszus, K., et al. (2001) An FGF-binding protein (FGF-BP) exerts its biological function by parallel paracrine stimulation of tumor cell and endothelial cell proliferation through FGF-2 release. Int. J. Cancer. 92, 510−517 https://doi.org/10.1002/1097-0215(20010515)92:4<510::AID-IJC1227>3.0.CO;2-H
  2. Baxevanis, A. D. (2002) Current Protocols in Bioinformatics. John Wiley & Sons, New York
  3. Bijovsky, A. T., Zorn, T. M., and Abrahamsohn, P. A. (1992) Remodeling of the mouse endometrial stroma during the preimplantation period. Acta Anat. 144, 231−234
  4. Blankenship, T. N. and Given, R. L. (1995) Loss of laminin and type IV collagen in uterine luminal epithelial basement membranes during blastosyst implantation in the mouse. Anat. Rec. 243, 27−36
  5. Brown, J. J. and Papaioannou, V. E. (1992) Distribution of hyaluronan in the mouse endometrium during the periimplantation period of pregnancy. Differentiation 52, 61−68
  6. Catherino, W. H., Leppert, P. C., Stenmark, M. H., Payson, M., Potlog-Nahari, C., et al. (2004) Reduced dermatopontin expression is a molecular link between uterine leiomyomas and keloids. Genes Chromosomes Canser 40, 204−217 https://doi.org/10.1002/gcc.20035
  7. Cheon, Y. P., Li, Q., Xu, X., DeMayo, F. J., Bagchi, I. C., et al. (2002) A genomic approach to identify novel progesterone receptor regulated pathways in the uterus during implantation. Mol. Endocrinol. 16, 2853−2871
  8. Cheon, Y. P., Xu, X., Bagchi, M. K., and Bagchi, I. C. (2003) Immune-responsive gene 1 is a novel target of progesterone receptor and plays a critical role during implantation in the mouse. Endocrinology 144, 5623−5630 https://doi.org/10.1210/en.2003-0585
  9. Cheon, Y. P., DeMayo, F. J., Bagchi, M. K., and Bagchi, I. C. (2004) Induction of T-lymphocyte antigen-2$\beta$, a cysteine protease inhibitor in deciduas. J. Biol. Chem. 279, 10357−10363 https://doi.org/10.1074/jbc.M309434200
  10. Church, H. J., Vicovac, L. M., Williams, J. D., Hey, N. A., and Aplin, J. D. (1996) Laminins 2 and 4 are expressed by human decidual cells. Lab. Invest. 74, 21–32
  11. Cooper, L. J., Bentley, A. J., Nieduszynski, I. A., Talabani, S., Thomson, A., et al. (2006) The role of dermatopontin n the stromal organization of the cornea. Invest. Ophthalmol. Vis. Sci. 47, 3303−3310 https://doi.org/10.1167/iovs.05-1426
  12. Daimon, E. and Wada, Y. (2005) Role of neutrophils in matrix metalloproteinase activity in the preimplantation mouse uterus. Biol. Reprod. 73, 163−171 https://doi.org/10.1095/biolreprod.104.038539
  13. Fainstat, T. (1963) Ureteral dilatation in pregnancy: a review. Obstet. Gynecol. Surv. 18, 845−860
  14. Fukuda, M. N., Sato, T., Nakayama, J., Klier, G., Mikami, M., et al. (1995) Trophinin and tastin, a novel cell adhesion molecule complex with potential involvement in embryo implantation. Genes Dev. 9, 1199−1210
  15. Giangrande, P. H. and McDonnell, D. P. (1999) The A and B isoforms of the human progesterone receptor: two functionally different transcription factors encoded by a single gene. Recent Prog. Horm. Res. 54, 291−314
  16. Giudice, L. C. (2002) Implantation and endometrial function: in Molecular Biology in Reproductive Medicine, Fauser, B. C. J. M. (ed.), pp. 439−465, Parthenon Publishing, New York
  17. Grabe, N. (2002) AliBaba2: context specific identification of transcription factor binding sites. In Silico Biol. 2, S1−S15
  18. Haralson, M. A. and Hassell, J. R. (1995) The extracellular matrix- an overview; in Extracellular Matrix-A Practical Approach, Haralson, M. A. and Hassell, J. R. (eds.), pp. 1−30, Oxford University Press, Oxford UK
  19. Hurst, P. R., Gibbs, R. D., Clark, D. E., and Myers, D. B. (1994) Temporal changes to uterine collagen types I, III and V in relation to early pregnancy in the rat. Reprod. Fertil. Dev. 6, 669−677
  20. Kuroda, K., Okamoto, O., and Shinkai, H. (1999) Dermatopontin expression is decreased in hypertrophic scar and systemic scerosis skin fibroblasts and is regulated by transforming growth factor-$\beta$1, interleukin-4, and matrix collagen. J. Invest. Dermatol. 112, 706−710 https://doi.org/10.1046/j.1523-1747.1999.00563.x
  21. Lewandowska, K., Choi, H. U., Rosenberg, L. C., Sasse, J., Neame, P. J., et al. (1991) Extracellular matrix adhesionpromoting activities of a dermatan sulfate proteoglycanassociated protein (22K) from bovine fetal skin. J. Cell Sci. 99, 657−668
  22. Liu, G., Zhang, X., Lin, H., Wang, H., Li, Q., et al (2006) Effects of E-cadherin on mouse embryo implantation and expression of matrix methalloproteinase-2 and -9. Biochem. Biophys. Res. Commun. 343, 832−838 https://doi.org/10.1016/j.bbrc.2006.02.189
  23. MacBeath, J. R., Shackleton, D. R., and Hulmes, D. J. (1993) Tyrosine-rich acidic matrix protein (TRAMP) accelerates collagen fibril formation in vitro. J. Biol. Chem. 268, 19826−19832
  24. Mosacatello, D. K., Santra, M., Mann, D. M., McQuillan, D. J., Wong, A. J., et al. (1998) Decorin suppresses tumor cell growth by activating the epidermal growth factor receptor. J. Clin. Invest. 101, 406–412
  25. Mulholland, J., Aplin, J. D., Ayad, S., Hong, L., and Glasser, S. R. (1992) Loss of collagen type VI from rat endometrial stoma during decidualization. Biol. Reprod. 46, 1136−1143
  26. Myers, D. B., Clark, D. E., and Hurst, P. R. (1990) Decreased collagen concentration in rat uterine implantation sites compared with nonimplantation tissue at days 6−11 of pregnancy. Reprod. Fertil. Dev. 2, 607−612
  27. Okamoto, O., Suzuki, Y., Kimura, S., and Shinkai, H. (1996) Extracellular matrix 22-$\kappa$Da protein interacts with decorin core protein and is expressed in cutaneous fibrosis. J. Biochem. 119, 106−114 https://doi.org/10.1093/oxfordjournals.jbchem.a021194
  28. Reese, M. G. (2001) Application of a time-delay neural network to promoter annotation in the Drosophila melanogaster genome. Comput. Chem. 26, 51−56 https://doi.org/10.1016/S0097-8485(01)00099-7
  29. Schutze, J., Skorokhod, A., Muller, I. M., and Muller, W. E. (2001) Molecular evolution of the metazoan extracellular matrix: cloning and expression of structural proteins from the demosponges Suberites domuncula and Geodia cydonium. J. Mol. Evol. 5, 402−415
  30. Son, Y. O., Lee, K. Y., Choi, K. C., Chung, Y., Kim, J. G., et al. (2004) Inhibitory effects of glycoprotein-120 (G-120) from Ulmus davidiana Nakai on cell growth and activation of matrix metalloproteinases. Mol. Cells 18, 163−170
  31. Strakova, Z., Srisuparp, S., and Fazleabas, A. T. (2002) IL-1beta during in vitro decidualization in primate. J. Reprod. Immunol. 55, 35−47 https://doi.org/10.1016/S0165-0378(01)00141-3
  32. Surveyor, G. A., Gendler, S. J., Pemberton, L., Das, S. K., Chakraborty, I., et al. (1995) Expression and steroid hormonal control of Muc-1 in the mouse uterus. Endocronology 136, 3639−3647 https://doi.org/10.1210/en.136.8.3639
  33. Takeda, U., Utani, A., Wu, J., Adachi, E., Koseki, H., et al. (2002) Targeted distruption of dermatopontin causes abnormal collagen fibrillogenesis. J. Invest. Dermatol. 119, 678−683
  34. Takemoto, S., Murakami, T., Kusachi, S., Iwabu, A., Hirohata, S., et al. (2002) Increase expression of dermatopontin mRNA in the infarct zone of experimentally induced myocardial infarction in rats: comparison with decorin and type I collagen mRNAs. Basic Res. Cardiol. 97, 461−468
  35. Tan, J., Paria, B. C., Dey, S. K., and Das, S. K. (1999) Differential uterine expression of estrogen and progesterone receptors correlated with uterine preparation for implantation and decidualization in the mouse. Endocrinology 140, 5310−5321
  36. Tang, M., Xu, Y., Julian. J., Carson, D., and Tabibzadeh, S. (2005) Lefty is expressed in mouse endometrium in estrous cycle and peri-implantation period. Hum. Reprod. 20, 872−880 https://doi.org/10.1093/humrep/deh717
  37. White, C. A., Robb, L., and Salamonsen, L. A. (2004) Uterine extracellular matrix components are altered during decidualization n interleukin-11 receptor alpha deficient mice. Reprod. Biol. Endocrinol. 2, 76−91 https://doi.org/10.1186/1477-7827-2-76
  38. Yao, M. W., Lim, H., Schust, D. J., Choe, S. E., Farago, A., et al. (2003) Gene expression profiling reveals progesteronemediated cell cycle and immunoregulatory roles of Hoxa-10 in the preimplantation uterus. Mol. Endocrinol. 17, 610−627 https://doi.org/10.1210/me.2002-0290
  39. Zhang, L., Yang, N., Huang, J., and Coukos, G. (2005) Transcriptional coactivator Drosophila eyes absent homologue 2 is up-regulated in epithelial ovarian cancer and promotes fumor growth. Cancer Res. 65, 925−932