Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015 (2015), Article ID 854056, 11 pages
http://dx.doi.org/10.1155/2015/854056
Review Article

Participation of WNT and β-Catenin in Physiological and Pathological Endometrial Changes: Association with Angiogenesis

1Department of Histology and Embryology, Faculty of Medical Sciences, University of Warmia and Mazury, Warszawska 30, 10-082 Olsztyn, Poland
2Department of Obstetrics and Gynecology, Faculty of Medical Sciences, University of Warmia and Mazury, Zołnierska 18, 10-561 Olsztyn, Poland

Received 21 November 2014; Accepted 15 January 2015

Academic Editor: Shi-Wen Jiang

Copyright © 2015 Jolanta Kiewisz 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. K. M. Cadigan and R. Nusse, “Wnt signaling: a common theme in animal development,” Genes & Development, vol. 11, no. 24, pp. 3286–3305, 1997. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Kikuchi, H. Yamamoto, and S. Kishida, “Multiplicity of the interactions of Wnt proteins and their receptors,” Cellular Signalling, vol. 19, no. 4, pp. 659–671, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. http://web.stanford.edu/group/nusselab/cgi-bin/wnt/.
  4. M. A. Torres, J. A. Yang-Snyder, S. M. Purcell, A. A. DeMarais, L. L. McGrew, and R. T. Moon, “Activities of the Wnt-1 class of secreted signaling factors are antagonized by the Wnt-5A class and by a dominant negative cadherin in early Xenopus development,” The Journal of Cell Biology, vol. 133, no. 5, pp. 1123–1137, 1996. View at Publisher · View at Google Scholar · View at Scopus
  5. D. Strutt, “Frizzled signalling and cell polarisation in Drosophila and vertebrates,” Development, vol. 130, no. 19, pp. 4501–4513, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Miller and D. A. Sassoon, “Wnt-7a maintains appropriate uterine patterning during the development of the mouse female reproductive tract,” Development, vol. 125, no. 16, pp. 3201–3211, 1998. View at Google Scholar · View at Scopus
  7. M. Mericskay, J. Kitajewski, and D. Sassoon, “Wnt5a is required for proper epithelial-mesenchymal interactions in the uterus,” Development, vol. 131, no. 9, pp. 2061–2072, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. O. A. Mohamed, M. Jonnaert, C. Labelle-Dumais, K. Kuroda, H. J. Clarke, and D. Dufort, “Uterine Wnt/beta-catenin signaling is required for implantation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 24, pp. 8579–8584, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. F. F. Bartol, A. A. Wiley, and C. A. Bagnell, “Uterine development and endometrial programming,” Society of Reproduction and Fertility supplement, vol. 62, pp. 113–130, 2006. View at Google Scholar · View at Scopus
  10. J. C. Chen, A. A. Wiley, T.-Y. Ho et al., “Transient estrogen exposure from birth affects uterine expression of developmental markers in neonatal gilts with lasting consequences in pregnant adults,” Reproduction, vol. 139, no. 3, pp. 623–630, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Tulac, N. R. Nayak, L. C. Kao et al., “Identification, characterization, and regulation of the canonical Wnt signaling pathway in human endometrium,” Journal of Clinical Endocrinology and Metabolism, vol. 88, no. 8, pp. 3860–3866, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. T. D. Bui, L. Zhang, M. C. P. Rees, R. Bicknell, and A. L. Harris, “Expression and hormone regulation of Wnt2, 3, 4, 5a, 7a, 7b and 10b in normal human endometrium and endometrial carcinoma,” British Journal of Cancer, vol. 75, no. 8, pp. 1131–1136, 1997. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Hayashi, R. C. Burghardt, F. W. Bazer, and T. E. Spencer, “WNTs in the ovine uterus: potential regulation of periimplantation ovine conceptus development,” Endocrinology, vol. 148, no. 7, pp. 3496–3506, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. M. O. Atli, A. Guzeloglu, and D. A. Dinc, “Expression of wingless type (WNT) genes and their antagonists at mRNA levels in equine endometrium during the estrous cycle and early pregnancy,” Animal Reproduction Science, vol. 125, no. 1–4, pp. 94–102, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. J. Kiewisz, M. M. Kaczmarek, A. Andronowska, A. Blitek, and A. J. Ziecik, “Gene expression of WNTs, β-catenin and E-cadherin during the periimplantation period of pregnancy in pigs—involvement of steroid hormones,” Theriogenology, vol. 76, no. 4, pp. 687–699, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Kiewisz, M. M. Kaczmarek, E. Morawska, A. Blitek, W. Kapelanski, and A. J. Ziecik, “Estrus synchronization affects WNT signaling in the porcine reproductive tract and embryos,” Theriogenology, vol. 76, no. 9, pp. 1684–1694, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. K. Stark, S. Vainio, G. Vassileva, and A. P. McMahon, “Epithelial transformation metanephric mesenchyme in the developing kidney regulated by Wnt-4,” Nature, vol. 372, no. 6507, pp. 679–683, 1994. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Vainio, M. Heikkilä, A. Kispert, N. Chin, and A. P. McMahon, “Female development in mammals is regulated by Wnt-4 signalling,” Nature, vol. 397, no. 6718, pp. 405–409, 1999. View at Publisher · View at Google Scholar · View at Scopus
  19. X. Hou, Y. Tan, M. Li, S. K. Dey, and S. K. Das, “Canonical Wnt signaling is critical to estrogen-mediated uterine growth,” Molecular Endocrinology, vol. 18, no. 12, pp. 3035–3049, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. T. P. Yamaguchi, A. Bradley, A. P. McMahon, and S. Jones, “A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo,” Development, vol. 126, no. 6, pp. 1211–1223, 1999. View at Google Scholar · View at Scopus
  21. M. Heikkil, H. Peltoketo, and S. Vainio, “Wnts and the female reproductive system,” Journal of Experimental Zoology, vol. 290, no. 6, pp. 616–623, 2001. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Pavlova, E. Boutin, G. Cunha, and D. Sassoon, “Msx1 (Hox-7.1) in the adult mouse uterus: cellular interactions underlying regulation of expression,” Development, vol. 120, no. 2, pp. 335–345, 1994. View at Google Scholar · View at Scopus
  23. C. Miller, A. Pavlova, and D. A. Sassoon, “Differential expression patterns of Wnt genes in the murine female reproductive tract during development and the estrous cycle,” Mechanisms of Development, vol. 76, no. 1-2, pp. 91–99, 1998. View at Publisher · View at Google Scholar · View at Scopus
  24. K. Hayashi, D. W. Erikson, S. A. Tilford et al., “Wnt genes in the mouse uterus: potential regulation of implantation,” Biology of Reproduction, vol. 80, no. 5, pp. 989–1000, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. M. C. Satterfield, G. Song, K. Hayashi, F. W. Bazer, and T. E. Spencer, “Progesterone regulation of the endometrial WNT system in the ovine uterus,” Reproduction, Fertility and Development, vol. 20, no. 8, pp. 935–946, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. X. Fan, S. Krieg, J. Y. Hwang et al., “Dynamic regulation of Wnt7a expression in the primate endometrium: Implications for postmenstrual regeneration and secretory transformation,” Endocrinology, vol. 153, no. 3, pp. 1063–1069, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. R. Gaetje, U. Holtrich, T. Karn et al., “Characterization of WNT7A expression in human endometrium and endometriotic lesions,” Fertility and Sterility, vol. 88, no. 6, pp. 1534–1540, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. C. Peng, X. Zhang, Y. Wang, L. Li, Q. Wang, and J. Zheng, “Expression and prognostic significance of Wnt7a in human endometrial carcinoma,” Obstetrics and Gynecology International, vol. 2012, Article ID 134962, 8 pages, 2012. View at Publisher · View at Google Scholar
  29. Y. Wang, P. Hanifi-Moghaddam, E. E. Hanekamp et al., “Progesterone inhibition of Wnt/β-catenin signaling in normal endometrium and endometrial cancer,” Clinical Cancer Research, vol. 15, no. 18, pp. 5784–5793, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. M. K. Oehler, I. Z. MacKenzie, D. Wallwiener, R. Bicknell, and M. C. Rees, “Wnt-7a is upregulated by norethisterone in human endometrial epithelial cells: a possible mechanism by which progestogens reduce the risk of estrogen-induced endometrial neoplasia,” Cancer Letters, vol. 186, no. 1, pp. 75–81, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. H. Aberle, S. Butz, J. Stappert, H. Weissig, R. Kemler, and H. Hoschuetzky, “Assembly of the cadherin-catenin complex in vitro with recombinant proteins,” Journal of Cell Science, vol. 107, no. 12, pp. 3655–3663, 1994. View at Google Scholar · View at Scopus
  32. J.-W. Jeong, H. S. Lee, H. L. Franco et al., “Beta-catenin mediates glandular formation and dysregulation of beta-catenin induces hyperplasia formation in the murine uterus,” Oncogene, vol. 28, no. 1, pp. 31–40, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Tabibzadeh, A. Babaknia, Q. F. Kong et al., “Menstruation is associated with disordered expression of desmoplakin I/II and cadherin/catenins and conversion of F- to G-actin in endometrial epithelium,” Human Reproduction, vol. 10, no. 4, pp. 776–784, 1995. View at Google Scholar · View at Scopus
  34. J. Fujimoto, S. Ichigo, M. Hori, and T. Tamaya, “Alteration of E-cadherin, alpha- and beta-catenin mRNA expression in human uterine endometrium during the menstrual cycle,” Gynecological Endocrinology, vol. 10, no. 3, pp. 187–191, 1996. View at Publisher · View at Google Scholar · View at Scopus
  35. G. T. C. Chen, S. Getsios, and C. D. MacCalman, “Progesterone regulates β-catenin mRNA levels in human endometrial stromal cells in vitro,” Endocrine, vol. 9, no. 3, pp. 263–267, 1998. View at Publisher · View at Google Scholar · View at Scopus
  36. H. Nei, T. Saito, H. Yamasaki, H. Mizumoto, E. Ito, and R. Kudo, “Nuclear localization of β-catenin in normal and carcinogenic endometrium,” Molecular Carcinogenesis, vol. 25, no. 3, pp. 207–218, 1999. View at Publisher · View at Google Scholar
  37. A. G. Gunin, V. U. Emelianov, I. U. Mironkin, M. P. Morozov, and A. S. Tolmachev, “Lithium treatment enhances estradiol-induced proliferation and hyperplasia formation in the uterus of mice,” The European Journal of Obstetrics Gynecology and Reproductive Biology, vol. 114, no. 1, pp. 83–91, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. A. J. Polotsky, L. Zhu, N. Santoro, and J. W. Pollard, “Lithium chloride treatment induces epithelial cell proliferation in xenografted human endometrium,” Human Reproduction, vol. 24, no. 8, pp. 1960–1967, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. D.-H. Yang, J.-Y. Yoon, S.-H. Lee et al., “Wnt5a is required for endothelial differentiation of embryonic stem cells and vascularization via pathways involving both Wnt/β-Catenin and protein kinase Cα,” Circulation Research, vol. 104, no. 3, pp. 372–379, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Jemal, R. Siegel, and T. Murray, “Cancer statistics, 2011,” CA: A Cancer Journal for Clinicians, vol. 61, no. 4, pp. 212–236, 2011. View at Publisher · View at Google Scholar
  41. G. D'Andrilli, A. Bovicelli, M. G. Paggi, and A. Giordano, “New insights in endometrial carcinogenesis,” Journal of Cellular Physiology, vol. 227, no. 7, pp. 2842–2846, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. A. J. Ryan, B. Susil, T. W. Jobling, and M. K. Oehler, “Endometrial cancer,” Cell and Tissue Research, vol. 322, no. 1, pp. 53–61, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Prat, A. Gallardo, M. Cuatrecasas, and L. Catasús, “Endometrial carcinoma: pathology and genetics,” Pathology, vol. 39, no. 1, pp. 72–87, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. W. T. Creasman, F. Odicino, P. Mausinneuve, M. A. Quinn, U. Beller, and J. L. Benedet, “Carcinoma of the corpus uteri. FIGO Annual Report,” International Journal of Gynaecology & Obstetrics, vol. 26, no. 95, supplement 1, pp. 105–143, 2006. View at Google Scholar
  45. E. Hiroki, J.-I. Akahira, F. Suzuki et al., “Changes in microRNA expression levels correlate with clinicopathological features and prognoses in endometrial serous adenocarcinomas,” Cancer Science, vol. 101, no. 1, pp. 241–249, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. Y. Liu, F. Meng, Y. Xu et al., “Overexpression of Wnt7a is associated with tumor progression and unfavorable prognosis in endometrial cancer,” International Journal of Gynecological Cancer, vol. 23, no. 2, pp. 304–311, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Wagner and L. Lehmann, “Estrogens modulate the gene expression of Wnt-7a in cultured endometrial adenocarcinoma cells,” Molecular Nutrition and Food Research, vol. 50, no. 4-5, pp. 368–372, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Newill, R. Loske, J. Wagner, C. Johannes, R. L. Lorenz, and L. Lehmann, “Oxidation products of stigmasterol interfere with the action of the female sex hormone 17beta-estradiol in cultured human breast and endometrium cell lines,” Molecular Nutrition and Food Research, vol. 51, no. 7, pp. 888–898, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. H. Chen, Y. Wang, and F. Xue, “Expression and the clinical significance of Wnt10a and Wnt10b in endometrial cancer are associated with the Wnt/β-catenin pathway,” Oncology Reports, vol. 29, no. 2, pp. 507–514, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. Y. Wang, M. van der Zee, R. Fodde, and L. J. Blok, “Wnt/Β-catenin and sex hormone signaling in endometrial homeostasis and cancer,” Oncotarget, vol. 1, no. 7, pp. 674–684, 2010. View at Google Scholar · View at Scopus
  51. T. H. Dellinger, K. Planutis, K. S. Tewari, and R. F. Holcombe, “Role of canonical Wnt signaling in endometrial carcinogenesis,” Expert Review of Anticancer Therapy, vol. 12, no. 1, pp. 51–62, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. T. Fukuchi, M. Sakamoto, H. Tsuda, K. Maruyama, S. Nozawa, and S. Hirohashi, “β-catenin mutation in carcinoma of the uterine endometrium,” Cancer Research, vol. 58, no. 16, pp. 3526–3528, 1998. View at Google Scholar · View at Scopus
  53. T. Ikeda, K. Yoshinaga, S. Semba, E. Kondo, H. Ohmori, and A. Horii, “Mutational analysis of the CTNNB1 (β-catenin) gene in human endometrial cancer: frequent mutations at codon 34 that cause nuclear accumulation,” Oncology Reports, vol. 7, no. 2, pp. 323–326, 2000. View at Google Scholar · View at Scopus
  54. H. Yano, A. Hara, J. Shinoda et al., “Immunohistochemical analysis of β-catenin in N-ethyl-N-nitrosourea-induced rat gliomas: implications in regulation of angiogenesis,” Neurological Research, vol. 22, no. 5, pp. 527–532, 2000. View at Google Scholar · View at Scopus
  55. H. Yano, A. Hara, K. Takenaka et al., “Differential expression of β-catenin in human glioblastoma multiforme and normal brain tissue,” Neurological Research, vol. 22, no. 7, pp. 650–656, 2000. View at Google Scholar · View at Scopus
  56. C. G. Eberhart, T. Tihan, and P. C. Burger, “Nuclear localization and mutation of beta-catenin in medulloblastomas,” Journal of Neuropathology and Experimental Neurology, vol. 59, no. 4, pp. 333–337, 2000. View at Google Scholar · View at Scopus
  57. M. Saegusa, M. Hashimura, T. Yoshida, and I. Okayasu, “β-catenin mutations and aberrant nuclear expression during endometrial tumorigenesis,” British Journal of Cancer, vol. 84, no. 2, pp. 209–217, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. P. W. Schlosshauer, E. C. Pirog, R. L. Levine, and L. H. Ellenson, “Mutational analysis of the CTNNB1 and APC genes in uterine endometrioid carcinoma,” Modern Pathology, vol. 13, no. 10, pp. 1066–1071, 2000. View at Publisher · View at Google Scholar · View at Scopus
  59. G. Moreno-Bueno, D. Hardisson, C. Sánchez et al., “Abnormalities of the APC/beta-catenin pathway in endometrial cancer,” Oncogene, vol. 21, no. 52, pp. 7981–7990, 2002. View at Publisher · View at Google Scholar · View at Scopus
  60. Q. Li, A. Kannan, W. Wang et al., “Bone morphogenetic protein 2 functions via a conserved signaling pathway involving Wnt4 to regulate uterine decidualization in the mouse and the human,” The Journal of Biological Chemistry, vol. 282, no. 43, pp. 31725–31732, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. P. S. Tanwar, H.-J. Lee, L. Zhang et al., “Constitutive activation of beta-catenin in uterine stroma and smooth muscle leads to the development of mesenchymal tumors in mice,” Biology of Reproduction, vol. 81, no. 3, pp. 545–552, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. M. van der Zee, Y. Jia, Y. Wang et al., “Alterations in Wnt-β-catenin and Pten signalling play distinct roles in endometrial cancer initiation and progression,” The Journal of Pathology, vol. 230, no. 1, pp. 48–58, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. N. Yi, Q.-P. Liao, T. Li, and Y. Xiong, “Novel expression profiles and invasiveness-related biology function of DKK1 in endometrial carcinoma,” Oncology Reports, vol. 21, no. 6, pp. 1421–1427, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. Y. Kubota, “Tumor angiogenesis and anti-angiogenic therapy,” The Keio Journal of Medicine, vol. 61, no. 2, pp. 47–56, 2012. View at Publisher · View at Google Scholar · View at Scopus
  65. E. Dejana, “The role of wnt signaling in physiological and pathological angiogenesis,” Circulation Research, vol. 107, no. 8, pp. 943–952, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. R. Demir, A. Yaba, and B. Huppertz, “Vasculogenesis and angiogenesis in the endometrium during menstrual cycle and implantation,” Acta Histochemica, vol. 112, no. 3, pp. 203–214, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. R. D. Koos, “Minireview: putting physiology back into estrogens' mechanism of action,” Endocrinology, vol. 152, no. 12, pp. 4481–4488, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. C. E. Gargett and P. A. W. Rogers, “Human endometrial angiogenesis,” Reproduction, vol. 121, no. 2, pp. 181–186, 2001. View at Publisher · View at Google Scholar · View at Scopus
  69. H. O. D. Critchley, J. Osei, T. A. Henderson et al., “Hypoxia-inducible factor-1 expression in human endometrium and its regulation by prostaglandin E-series prostanoid receptor 2 (EP2),” Endocrinology, vol. 147, no. 2, pp. 744–753, 2006. View at Publisher · View at Google Scholar · View at Scopus
  70. L. G. Nardo, “Vascular endothelial growth factor expression in the endometrium during the menstrual cycle, implantation window and early pregnancy,” Current Opinion in Obstetrics & Gynecology, vol. 17, no. 4, pp. 419–423, 2005. View at Publisher · View at Google Scholar · View at Scopus
  71. P. Carmeliet, L. Moons, and D. Collen, “Mouse models of angiogenesis, arterial stenosis, atherosclerosis and hemostasis,” Cardiovascular Research, vol. 39, no. 1, pp. 8–33, 1998. View at Publisher · View at Google Scholar · View at Scopus
  72. T. N. H. Masckauchán, C. J. Shawber, Y. Funahashi, C.-M. Li, and J. Kitajewski, “Wnt/β-catenin signaling induces proliferation, survival and interleukin-8 in human endothelial cells,” Angiogenesis, vol. 8, no. 1, pp. 43–51, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. M. M. Bakre, A. Hoi, J. C. Y. Mong, Y. Y. Koh, K. Y. Wong, and L. W. Stanton, “Generation of multipotential mesendodermal progenitors from mouse embryonic stem cells via sustained Wnt pathway activation,” The Journal of Biological Chemistry, vol. 282, no. 43, pp. 31703–31712, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. P. S. Woll, J. K. Morris, M. S. Painschab et al., “Wnt signaling promotes hematoendothelial cell development from human embryonic stem cells,” Blood, vol. 111, no. 1, pp. 122–131, 2008. View at Publisher · View at Google Scholar · View at Scopus
  75. A. M. Goodwin, J. Kitajewski, and P. A. D'Amore, “Wnt1 and Wnt5a affect endothelial proliferation and capillary length; Wnt2 does not,” Growth Factors, vol. 25, no. 1, pp. 25–32, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. C.-W. Cheng, S. K. Smith, and D. S. Charnock-Jones, “Wnt-1 signaling inhibits human umbilical vein endothelial cell proliferation and alters cell morphology,” Experimental Cell Research, vol. 291, no. 2, pp. 415–425, 2003. View at Publisher · View at Google Scholar · View at Scopus
  77. S. J. Monkley, S. J. Delaney, D. J. Pennisi, J. H. Christiansen, and B. J. Wainwright, “Targeted disruption of the Wnt2 gene results in placentation defects,” Development, vol. 122, no. 11, pp. 3343–3353, 1996. View at Google Scholar · View at Scopus
  78. X. Ye, Y. Wang, H. Cahill et al., “Norrin, frizzled-4, and Lrp5 signaling in endothelial cells controls a genetic program for retinal vascularization,” Cell, vol. 139, no. 2, pp. 285–298, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. T.-O. Ishikawa, Y. Tamai, A. M. Zorn et al., “Mouse Wnt receptor gene Fzd5 is essential for yolk sac and placental angiogenesis,” Development, vol. 128, no. 1, pp. 25–33, 2001. View at Google Scholar · View at Scopus
  80. I. Samarzija, P. Sini, T. Schlange, G. MacDonald, and N. E. Hynes, “Wnt3a regulates proliferation and migration of HUVEC via canonical and non-canonical Wnt signaling pathways,” Biochemical and Biophysical Research Communications, vol. 386, no. 3, pp. 449–454, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. C.-W. Cheng, J.-C. Yeh, T.-P. Fan, S. K. Smith, and D. S. Charnock-Jones, “Wnt5a-mediated non-canonical Wnt signalling regulates human endothelial cell proliferation and migration,” Biochemical and Biophysical Research Communications, vol. 365, no. 2, pp. 285–290, 2008. View at Publisher · View at Google Scholar · View at Scopus
  82. R. Daneman, D. Agalliu, L. Zhou, F. Kuhnert, C. J. Kuo, and B. A. Barres, “Wnt/β-catenin signaling is required for CNS, but not non-CNS, angiogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 2, pp. 641–646, 2009. View at Publisher · View at Google Scholar · View at Scopus
  83. W. Shu, Y. Q. Jiang, M. M. Lu, and E. E. Morrisey, “Wnt7b regulates mesenchymal proliferation and vascular development in the lung,” Development, vol. 129, no. 20, pp. 4831–4842, 2002. View at Google Scholar · View at Scopus
  84. A. Cattelino, S. Liebner, R. Gallini et al., “The conditional inactivation of the beta-catenin gene in endothelial cells causes a defective vascular pattern and increased vascular fragility,” The Journal of Cell Biology, vol. 162, no. 6, pp. 1111–1122, 2003. View at Publisher · View at Google Scholar · View at Scopus
  85. H. Madjar, H. J. Prömpeler, W. Sauerbrei, R. Wolfarth, and A. Pfleiderer, “Color Doppler flow criteria of breast lesions,” Ultrasound in Medicine and Biology, vol. 20, no. 9, pp. 849–858, 1994. View at Publisher · View at Google Scholar · View at Scopus
  86. M. Perrot-Applanat, M. T. Groyer-Picard, E. Garcia, F. Lorenzo, and E. Milgrom, “Immunocytochemical demonstration of estrogen and progesterone receptors in muscle cells of uterine arteries in rabbits and humans,” Endocrinology, vol. 123, no. 3, pp. 1511–1519, 1988. View at Publisher · View at Google Scholar · View at Scopus
  87. G. Krikun, F. Schatz, and C. J. Lockwood, “Endometrial angiogenesis: from physiology to pathology,” Annals of the New York Academy of Sciences, vol. 1034, pp. 27–35, 2004. View at Publisher · View at Google Scholar · View at Scopus
  88. K. Y. Lee, J.-W. Jeong, J. Wang et al., “Bmp2 is critical for the murine uterine decidual response,” Molecular and Cellular Biology, vol. 27, no. 15, pp. 5468–5478, 2007. View at Publisher · View at Google Scholar · View at Scopus
  89. K. A. Dunlap, J. Filant, K. Hayashi et al., “Postnatal deletion of Wnt7a inhibits uterine gland morphogenesis and compromises adult fertility in mice,” Biology of Reproduction, vol. 85, no. 2, pp. 386–396, 2011. View at Publisher · View at Google Scholar · View at Scopus
  90. G. L. Mutter, M.-C. Lin, J. T. Fitzgerald et al., “Altered PTEN expression as a diagnostic marker for the earliest endometrial precancers,” The Journal of the National Cancer Institute, vol. 92, no. 11, pp. 924–931, 2000. View at Publisher · View at Google Scholar · View at Scopus
  91. P. W. Schlosshauer, L. H. Ellenson, and R. A. Soslow, “Beta-catenin and E-cadherin expression patterns in high-grade endometrial carcinoma are associated with histological subtype,” Modern Pathology, vol. 15, no. 10, pp. 1032–1037, 2002. View at Publisher · View at Google Scholar · View at Scopus
  92. S. Erkanli, F. Eren, S. Pekin, and T. Bagis, “BCL-2 and P53 expression in endometrial carcinoma,” Journal of Experimental and Clinical Cancer Research, vol. 23, no. 1, pp. 97–103, 2004. View at Google Scholar · View at Scopus
  93. S. F. Lax, B. Kendall, H. Tashiro, R. J. C. Slebos, and L. H. Ellenson, “The frequency of p53, k-ras mutations, and microsatellite instability differs in uterine endometrioid and serous carcinoma,” Cancer, vol. 88, no. 4, pp. 814–824, 2000. View at Publisher · View at Google Scholar