Progesterone regulation of the endometrial WNT system in the ovine uterus

Reproduction, Fertility and Development

Volumn 20, Issue 8, 2008, Pages 935-946

  Satterfield, M Carey ^a   Song, Gwonhwa ^a   Hayashi, Kanako ^a,b   Bazer, Fuller W ^a   Spencer, Thomas E ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Endometrium

Indexed keywords

CORN OIL; DKK1 PROTEIN; DRUG VEHICLE; MESSENGER RNA; MIFEPRISTONE; PROGESTERONE; TRANSCRIPTION FACTOR 7 LIKE 2; TRANSCRIPTION FACTOR MSX1; TRANSCRIPTION FACTOR MSX2; UNCLASSIFIED DRUG; WNT PROTEIN; WNT11 PROTEIN; WNT2 PROTEIN; WNT7A PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CELL DIFFERENTIATION; CELL JUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOMETRIUM CELL; FEMALE; NONHUMAN; PROGESTERONE RELEASE; SHEEP; TIGHT JUNCTION; UTERUS FUNCTION;

ANIMALS; EMBRYONIC DEVELOPMENT; ENDOMETRIUM; FEMALE; HOMEODOMAIN PROTEINS; MSX1 TRANSCRIPTION FACTOR; PROGESTERONE; SHEEP; SIGNAL TRANSDUCTION; TCF TRANSCRIPTION FACTORS; UTERUS; WNT PROTEINS; WNT2 PROTEIN;

OVIS; OVIS ARIES; ZEA MAYS;

EID: 54349126949     PISSN: 10313613     EISSN: None     Source Type: Journal    
DOI: 10.1071/RD08069     Document Type: Article

References (65)

1. Bafico, A., Gazit, A., Pramila, T., Finch, P. W., Yaniv, A., and Aaronson, S. A. (1999). Interaction of frizzled related protein (FRP) with Wnt ligands and the frizzled receptor suggests alternative mechanisms for FRP inhibition of Wnt signaling. J. Biol. Chem. 274, 16 180-16 187. doi:10.1074/JBC.274.23.16180
2. Boutros, M., Paricio, N., Strutt, D. I., and Mlodzik, M. (1998). Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94, 109-118. doi:10.1016/S0092-8674(00)81226-X
3. Brenner, R. M., McClellan, M. C., West, N. B., Novy, M. J., Haluska, G. J., and Sternfeld, M. D. (1991). Estrogen and progestin receptors in the macaque endometrium. Ann. N. Y. Acad. Sci. 622, 149-166. doi:10.1111/J.1749-6632.1991.TB37859.X
4. Burghardt, R. C., Johnson, G. A., Jaeger, L. A., Ka, H., Garlow, J. E., Spencer, T. E., and Bazer, F. W. (2002). Integrins and extracellular matrix proteins at the maternal-fetal interface in domestic animals. Cells Tissues Organs 172, 202-217. doi:10.1159/000066969
5. Carson, D. D., Bagchi, I., Dey, S. K., Enders, A. C., Fazleabas, A. T., Lessey, B. A., and Yoshinaga, K. (2000). Embryo implantation. Dev. Biol. 223, 217-237. doi:10.1006/DBIO.2000.9767
6. Daikoku, T., Song, H., Guo, Y., Riesewijk, A., Mosselman, S., Das, S. K., and Dey, S. K. (2004). Uterine Msx-1 and Wnt4 signaling becomes aberrant in mice with the loss of leukemia inhibitory factor or Hoxa-10: evidence for a novel cytokine-homeobox-Wnt signaling in implantation. Mol. Endocrinol. 18, 1238-1250. doi:10.1210/ME.2003-0403
7. Dale, T. C. (1998). Signal transduction by the Wnt family of ligands. Biochem. J. 329, 209-223.
8. Davies, J. A. (2002). Do different branching epithelia use a conserved developmental mechanism? Bioessays 24, 937-948. doi:10.1002/BIES.10161
9. Davies, J. A., and Fisher, C. E. (2002). Genes and proteins in renal development. Exp. Nephrol. 10, 102-113. doi:10.1159/000049905
10. Federation of Animal Science Societies (FASS) (1999). 'Guide for the Care and Use of Agriculture Animals in Research and Teaching.' (FASS: Savoy, IL).
11. Flechon, J. E., Guillomot, M., Charlier, M., Flechon, B., and Martal, J. (1986). Experimental studies on the elongation of the ewe blastocyst. Reprod. Nutr. Dev. 26, 1017-1024. doi:10.1051/RND:19860609
12. Garrett, J. E., Geisert, R. D., Zavy, M. T., and Morgan, G. L. (1988). Evidence for maternal regulation of early conceptus growth and development in beef cattle. J. Reprod. Fertil. 84, 437-446.
13. Geisert, R. D., Pratt, T. N., Bazer, F. W., Mayes, J. S., and Watson, G. H. (1994). Immunocytochemical localization and changes in endometrial progestin receptor protein during the porcine oestrous cycle and early pregnancy. Reprod. Fertil. Dev. 6, 749-760. doi:10.1071/RD9940749
14. Glinka, A., Wu, W., Delius, H., Monaghan, A. P., Blumenstock, C., and Niehrs, C. (1998). Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 391, 357-362. doi:10.1038/34848
15. Gray, C. A., Adelson, D. L., Bazer, F. W., Burghardt, R. C., Meeusen, E. N., and Spencer, T. E. (2004). Discovery and characterization of an epithelial-specific galectin in the endometrium that forms crystals in the trophectoderm. Proc. Natl Acad. Sci. USA 101, 7982-7987. doi:10.1073/PNAS.0402669101
16. Guillomot, M. (1995). Cellular interactions during implantation in domestic ruminants. J. Reprod. Fertil. Suppl. 49, 39-51.
17. Habas, R., Dawid, I. B., and He, X. (2003). Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation. Genes Dev. 17, 295-309. doi:10.1101/GAD.1022203
18. Hartsock, A., and Nelson, W. J. (2007). Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim. Biophys. Acta 1778, 660-669.
19. Hayashi, K., Burghardt, R. C., Bazer, F. W., and Spencer, T. E. (2007). WNTs in the ovine uterus: potential regulation of periimplantation ovine conceptus development. Endocrinology 148, 3496-3506. doi:10.1210/EN.2007-0283
20. Heyman, Y., Camous, S., Fevre, J., Meziou, W., and Martal, J. (1984). Maintenance of the corpus luteum after uterine transfer of trophoblastic vesicles to cyclic cows and ewes. J. Reprod. Fertil. 70, 533-540.
21. Huelsken, J., and Birchmeier, W. (2001). New aspects of Wnt signaling pathways in higher vertebrates. Curr. Opin. Genet. Dev. 11, 547-553. doi:10.1016/S0959-437X(00)00231-8
22. Hussein, S. M., Duff, E. K., and Sirard, C. (2003). Smad4 and beta-catenin co-activators functionally interact with lymphoid-enhancing factor to regulate graded expression of Msx2. J. Biol. Chem. 278, 48 805-48 814. doi:10.1074/JBC.M305472200
23. Jamora, C., DasGupta, R., Kocieniewski, P., and Fuchs, E. (2003). Links between signal transduction, transcription and adhesion in epithelial bud development. Nature 422, 317-322. doi:10.1038/NATURE01458
24. Karner, C., Wharton, K. A., and Carroll, T. J. (2006a). Apical-basal polarity, Wnt signaling and vertebrate organogenesis. Semin. Cell Dev. Biol. 17, 214-222. doi:10.1016/J.SEMCDB.2006.05.007
25. Karner, C., Wharton, K. A., Jr, and Carroll, T. J. (2006b). Planar cell polarity and vertebrate organogenesis. Semin. Cell Dev. Biol. 17, 194-203. doi:10.1016/J.SEMCDB.2006.05.003
26. Kawano, Y., and Kypta, R. (2003). Secreted antagonists of the Wnt signalling pathway. J. Cell Sci. 116, 2627-2634. doi:10.1242/JCS.00623
27. Kim, S., Choi, Y., Bazer, F. W., and Spencer, T. E. (2003). Identification of genes in the ovine endometrium regulated by interferon tau independent of signal transducer and activator of transcription 1. Endocrinology 144, 5203-5214. doi:10.1210/EN.2003-0665
28. 2+ pathway: a new vertebrate Wnt signaling pathway takes shape. Trends Genet. 16, 279-283. doi:10.1016/S0168-9525(00) 02028-X
29. Lee, R. S., Wheeler, T. T., and Peterson, A. J. (1998). Large-format, two-dimensional polyacrylamide gel electrophoresis of ovine periimplantation uterine luminal fluid proteins: identification of aldose reductase, cytoplasmic actin, and transferrin as conceptus-synthesized proteins. Biol. Reprod. 59, 743-752. doi:10.1095/BIOLREPROD59.4.743
30. Lessey, B. A., Killam, A. P., Metzger, D. A., Haney, A. F., Greene, G. L., and McCarty, K. S., Jr (1988). Immunohistochemical analysis of human uterine estrogen and progesterone receptors throughout the menstrual cycle. J. Clin. Endocrinol. Metab. 67, 334-340.
31. Li, Q., Wang, J., Armant, D. R., Bagchi, M. K., and Bagchi, I. C. (2002). Calcitonin down-regulates E-cadherin expression in rodent uterine epithelium during implantation. J. Biol. Chem. 277, 46 447-46 455.
32. Logan, C. Y., and Nusse, R. (2004). The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810. doi:10.1146/ANNUREV.CELLBIO.20.010403.113126
33. Mankertz, J., Hillenbrand, B., Tavalali, S., Huber, O., Fromm, M., and Schulzke, J. D. (2004). Functional crosstalk between Wnt signaling and Cdx-related transcriptional activation in the regulation of the claudin-2 promoter activity. Biochem. Biophys. Res. Commun. 314, 1001-1007. doi:10.1016/J.BBRC.2003.12.185
34. Miwa, N., Furuse, M., Tsukita, S., Niikawa, N., Nakamura, Y., and Furukawa, Y. (2001). Involvement of claudin-1 in the beta-catenin/Tcf signaling pathway and its frequent upregulation in human colorectal cancers. Oncol. Res. 12, 469-476.
35. Mohamed, O.A., Jonnaert, M., Labelle-Dumais, C., Kuroda, K., Clarke, H. J., and Dufort, D. (2005). Uterine Wnt/beta-catenin signaling is required for implantation. Proc. Natl Acad. Sci. USA 102, 8579-8584. doi:10.1073/PNAS.0500612102
36. Nelson, W. J., and Nusse, R. (2004). Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303, 1483-1487. doi:10.1126/SCIENCE.1094291
37. Nishina, H., Wada, T., and Katada, T. (2004). Physiological roles of SAPK/JNK signaling pathway. J. Biochem. 136, 123-126. doi:10.1093/JB/MVH117
38. Nusse, R. (2001). Developmental biology. Making head or tail of Dickkopf. Nature 411, 255-256. doi:10.1038/35077199
39. Oehler, M. K., MacKenzie, I. Z., Wallwiener, D., Bicknell, R., and Rees, M. C. (2002). 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 Lett. 186, 75-81. doi:10.1016/S0304-3835(02)00259-8
40. Orchard, M. D., and Murphy, C. R. (2002). Alterations in tight junction molecules of uterine epithelial cells during early pregnancy in the rat. Acta Histochem. 104, 149-155. doi:10.1078/0065-1281-00644
41. Pandur, P., Lasche, M., Eisenberg, L. M., and Kuhl, M. (2002a). Wnt-11 activation of a non-canonical Wnt signalling pathway is required for cardiogenesis. Nature 418, 636-641. doi:10.1038/NATURE00921
42. Pandur, P., Maurus, D., and Kuhl, M. (2002b). Increasingly complex: new players enter the Wnt signaling network. Bioessays 24, 881-884. doi:10.1002/BIES.10164
43. Paria, B. C., Zhao, X., Das, S. K., Dey, S. K., and Yoshinaga, K. (1999). Zonula occludens-1 and E-cadherin are coordinately expressed in the mouse uterus with the initiation of implantation and decidualization. Dev. Biol. 208, 488-501. doi:10.1006/DBIO.1999.9206
44. Pinson, K. I., Brennan, J., Monkley, S., Avery, B. J., and Skarnes, W. C. (2000). An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 407, 535-538. doi:10.1038/35035124
45. Robinson, G. W., Hennighausen, L., and Johnson, P. F. (2000). Side-branching in the mammary gland: the progesterone-Wnt connection. Genes Dev. 14, 889-894.
46. Roose, J., Huls, G., van Beest, M., Moerer, P., van der Horn, K., Goldschmeding, R., Logtenberg, T., and Clevers, H. (1999). Synergy between tumor suppressor APC and the beta-catenin-Tcf4 target Tcf1. Science 285, 1923-1926. doi:10.1126/SCIENCE.285.5435.1923
47. Rozen, S., and Skaletsky, H. (2000). Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132, 365-386.
48. Satterfield, M. C., Bazer, F. W., and Spencer, T. E. (2006). Progesterone regulation of preimplantation conceptus growth and galectin 15 (LGALS15) in the ovine uterus. Biol. Reprod. 75, 289-296. doi:10.1095/BIOLREPROD. 106.052944
49. Satterfield, M. C., Dunlap, K. A., Hayashi, K., Burghardt, R. C., Spencer, T. E., and Bazer, F. W. (2007). Tight and adherens junctions in the ovine uterus: differential regulation by pregnancy and progesterone. Endocrinology 148, 3922-3931. doi:10.1210/EN.2007-0321
50. Spencer, T. E., and Bazer, F. W. (1995). Temporal and spatial alterations in uterine estrogen receptor and progesterone receptor gene expression during the estrous cycle and early pregnancy in the ewe. Biol. Reprod. 53, 1527-1543. doi:10.1095/BIOLREPROD53.6.1527
51. Spencer, T. E., Stagg, A. G., Joyce, M. M., Jenster, G., Wood, C. G., Bazer, F. W., Wiley, A. A., and Bartol, F. F. (1999). Discovery and characterization of endometrial epithelial messenger ribonucleic acids using the ovine uterine gland knockout model. Endocrinology 140, 4070-4080. doi:10.1210/EN.140.9.4070
52. Spencer, T. E., Johnson, G. A., Bazer, F. W., and Burghardt, R. C. (2004a). Implantation mechanisms: insights from the sheep. Reproduction 128, 657-668. doi:10.1530/REP.1.00398
53. Spencer, T. E., Johnson, G. A., Burghardt, R. C., and Bazer, F. W. (2004b). Progesterone and placental hormone actions on the uterus: insights from domestic animals. Biol. Reprod. 71, 2-10. doi:10.1095/BIOLREPROD.103.024133
54. Stewart, M. D., Johnson, G. A., Gray, C. A., Burghardt, R. C., Schuler, L. A., Joyce, M. M., Bazer, F. W., and Spencer, T. E. (2000). Prolactin receptor and uterine milk protein expression in the ovine endometrium during the estrous cycle and pregnancy. Biol. Reprod. 62, 1779-1789. doi:10.1095/BIOLREPROD62.6.1779
55. Tan, J., Paria, B. C., Dey, S. K., and Das, S. K. (1999). Differential uterine expression of estrogen and progesterone receptors correlates with uterine preparation for implantation and decidualization in the mouse. Endocrinology 140, 5310-5321. doi:10.1210/EN.140.11.5310
56. Taylor, K. M., Gray, C. A., Joyce, M. M., Stewart, M. D., Bazer, F. W., and Spencer, T. E. (2000). Neonatal ovine uterine development involves alterations in expression of receptors for estrogen, progesterone, and prolactin. Biol. Reprod. 63, 1192-1204. doi:10.1095/BIOLREPROD63. 4.1192
57. Thie, M., Fuchs, P., Butz, S., Sieckmann, F., Hoschutzky, H., Kemler, R., and Denker, H. W. (1996). Adhesiveness of the apical surface of uterine epithelial cells: the role of junctional complex integrity. Eur. J. Cell Biol. 70, 221-232.
58. Tranguch, S., Daikoku, T., Wang, G. H., and Dey, S. K. (2005). Molecular complexity in establishing uterine receptivity and implantation. Cell. Mol. Life Sci. 62, 1964-1973. doi:10.1007/S00018-005-5230-0
59. Tulac, S., Overgaard, M. T., Hamilton, A. E., Jumbe, N. L., Suchanek, E., and Giudice, L. C. (2006). Dickkopf-1, an inhibitor of Wnt signaling, is regulated by progesterone in human endometrial stromal cells. J. Clin. Endocrinol. Metab. 91, 1453-1461. doi:10.1210/JC.2005-0769
60. Veeman, M. T., Axelrod, J. D., and Moon, R. T. (2003). A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev. Cell 5, 367-377. doi:10.1016/S1534-5807(03)00266-1
61. Wang, X., Matsumoto, H., Zhao, X., Das, S. K., and Paria, B. C. (2004). Embryonic signals direct the formation of tight junctional permeability barrier in the decidualizing stroma during embryo implantation. J. Cell Sci. 117, 53-62. doi:10.1242/JCS.00826
62. Widelitz, R. (2005). Wnt signaling through canonical and non-canonical pathways: recent progress. Growth Factors 23, 111-116. doi:10.1080/08977190500125746
63. Willert, J., Epping, M., Pollack, J. R., Brown, P. O., and Nusse, R. (2002). A transcriptional response to Wnt protein in human embryonic carcinoma cells. BMC Dev. Biol. 2, 8. doi:10.1186/1471-213X-2-8
64. Xie, H., Tranguch, S., Jia, X., Zhang, H., Das, S. K., Dey, S. K., Kuo, C. J., and Wang, H. (2008). Inactivation of nuclear Wnt-{beta}-catenin signaling limits blastocyst competency for implantation. Development 135, 717-727. doi:10.1242/DEV.015339
65. Yamanaka, H., Moriguchi, T., Masuyama, N., Kusakabe, M., Hanafusa, H., Takada, R., Takada, S., and Nishida, E. (2002). JNK functions in the non-canonical Wnt pathway to regulate convergent extension movements in vertebrates. EMBO Rep. 3, 69-75. doi:10.1093/EMBOREPORTS/KVF008