Fol. Biol. 2014, 60, 57-67

https://doi.org/10.14712/fb2014060020057

Wnt5a Influences Viability, Migration, Adhesion, Colony Formation, Eand N-Cadherin Expression of Human Ovarian Cancer Cell Line SKOV-3

F. Jannesari-Ladani1, Ghamartaj Hossein1, N. Monhasery1, S. H. Shahoei1, N. Izadimood2

1Department of Animal Physiology, Developmental Biology Laboratory, School of Biology, University College of Science, University of Tehran, Tehran, Iran
2Department of Pathology, Women’s Hospital, Tehran University of Medical Sciences, Tehran, Iran

Received August 2013
Accepted December 2013

References

1. Auersperg, N., Pan, J., Grove, B. D., Peterson, T., Fisher, J., Maines-Bandiera, S., Somasiri, A., Roskelley, C. D. (1999) E­cadherin induces mesenchymal­to­epithelial transition in human ovarian surface epithelium. Proc. Natl. Acad. Sci. USA 96, 6249-6254. <https://doi.org/10.1073/pnas.96.11.6249>
2. Badiglian Filho, L., Oshima, C. T., De Oliveira Lima, F., De Oliveira Costa, H., De Sousa Damião, R., Gomes, T. S., Gonçalves, W. J. (2009) Canonical and noncanonical Wnt pathway: a comparison among normal ovary, benign ovarian tumor and ovarian cancer. Oncol. Rep. 21, 313-320.
3. Bitler, B. G., Nicodemus, J. P., Li, H., Cai, Q., Wu, H., Hua, X., Li, T., Birrer, M. J., Godwin, A. K., Cairns, P., Zhang, R. (2011) Wnt5a suppresses epithelial ovarian cancer by promoting cellular senescence. Cancer Res. 71, 6184-6194. <https://doi.org/10.1158/0008-5472.CAN-11-1341>
4. Bordonaro, M., Tewari, S., Cicco, C. E., Atamna, W., Lazarova, D. L. (2011) A switch from canonical to noncanonical Wnt signaling mediates drug resistance in colon cancer cells. PLoS One, 6, e27308. <https://doi.org/10.1371/journal.pone.0027308>
5. Da Forno, P. D., Pringle, J. H., Hutchinson, P., Osborn, J., Huang, Q., Potter, L., Hancox, R. A., Fletcher, A., Saldanha, G. S. (2008) WNT5A expression increases during melanoma progression and correlates with outcome. Clin. Cancer Res. 14, 5825-5832. <https://doi.org/10.1158/1078-0432.CCR-07-5104>
6. Daraï, E., Scoazec, J. Y., Walker­Combrouze, F., MlikaCabanne, N., Feldmann, G., Madelenat, P., Potet, F. (1997) Expression of cadherins in benign, borderline and malignant ovarian epithelial tumors: a clinicopathologic study of 60 cases. Hum. Pathol. 28, 922-928. <https://doi.org/10.1016/S0046-8177(97)90007-1>
7. Daraï, E., Bringuier, A. F., Walker­Combrouze, F., Feldmann, G., Madelenat, P., Scoazec, J. Y. (1998) Soluble adhesion molecules in serum and cyst fluid from patients with cystic tumours of the ovary. Hum. Reprod. 13, 2831-2835. <https://doi.org/10.1093/humrep/13.10.2831>
8. Dejmek, J., Dejmek, A., Säfholm, A., Sjölander, A., Andersson, T. (2005) Wnt-5a protein expression in primary Dukes B colon cancers identifies a subgroup of patients with good prognosis. Cancer Res. 65, 9142-9146. <https://doi.org/10.1158/0008-5472.CAN-05-1710>
9. Dissanayake, S. K., Wade, M., Johnson, C. E., O’Connell, M. P., Leotlela, P. D., French, A. D., Shah, K. V., Hewitt, K. J., Rosenthal, D. T., Indig, F. E., Jiang, Y., Nickoloff, B. J., Taub, D. D., Trent, J. M., Moon, R. T., Bittner, M., Weeraratna, A. T. (2007) The Wnt5A/protein kinase C pathway mediates motility in melanoma cells via the inhibition of metastasis suppressors and initiation of an epithelial to mesenchymal transition. J. Biol. Chem. 282, 17259-17271. <https://doi.org/10.1074/jbc.M700075200>
10. Elloul, S., Vaksman, O., Stavnes, H. T., Trope, C. G., Davidson, B., Reich, R. (2010) Mesenchymal-to-epithelial transition determinants as characteristics of ovarian carcinoma effusions. Clin. Exp. Metastasis 27, 161-172. <https://doi.org/10.1007/s10585-010-9315-2>
11. Faleiro-­Rodrigues, C., Macedo­-Pinto, I., Pereira, D., Lopes, C. (2004) Prognostic value of Ecadherin immunoexpression in patients with primary ovarian carcinomas. Ann. Oncol. 15, 1535-1542. <https://doi.org/10.1093/annonc/mdh387>
12. Fujioka, T., Takebayashi, Y., Kihana, T., Kusanagi, Y., Hamada, K., Ochi, H., Uchida, T., Fukumoto, M., Ito, M. (2001) Expression of E-cadherin and b­catenin in primary and peritoneal metastatic ovarian carcinoma. Oncol. Rep. 8, 249-255.
13. Griesmann, H., Ripka, S., Pralle, M., Ellenrieder, V., Baumgart, S., Buchholz, M., Pilarsky, C., Aust, D., Gress, T. M., Michl, P. (2013) WNT5A-NFAT signaling mediates resistance to apoptosis in pancreatic cancer. Neoplasia 15, 11-22. <https://doi.org/10.1593/neo.121312>
14. Huang, C. L., Liu, D., Nakano, J., Ishikawa, S., Kontani, K., Yokomise, H., Ueno, M. (2005) Wnt5a expression is associated with the tumor proliferation and the stromal vascular endothelial growth factor – an expression in non-small-cell lung cancer. J. Clin. Oncol. 23, 8765-8773. <https://doi.org/10.1200/JCO.2005.02.2871>
15. Hudson, L. G., Zeineldin, R., Stack, M. S. (2008) Phenotypic plasticity of neoplastic ovarian epithelium: unique cadherin profiles in tumor progression. Clin. Exp. Metastasis 25, 643-655. <https://doi.org/10.1007/s10585-008-9171-5>
16. Imai, T., Horiuchi, A., Shiozawa, T., Osada, R., Kikuchi, N., Ohira, S., Oka, K., Konishi, I. (2004) Elevated expression of E-cadherin and γ-catenins in metastatic lesions compared with primary epithelial ovarian carcinomas. Hum. Pathol. 35, 1469-1476. <https://doi.org/10.1016/j.humpath.2004.09.014>
17. Jenei, V., Sherwood, V., Howlin, J., Linnskog, R., Säfholm, A., Axelsson, L., Andersson, T. (2009) A t-butyloxycarbonyl-modified Wnt5a-derived hexapeptide functions as a potent antagonist of Wnt5a­dependent melanoma cell invasion. Proc. Natl. Acad. Sci. USA 106, 19473-19478. <https://doi.org/10.1073/pnas.0909409106>
18. Jin, Z., Zhao, C., Han, X., Han, Y. (2012) Wnt5a promotes ewing sarcoma cell migration through upregulating CXCR4 expression. BMC Cancer 12, 480. <https://doi.org/10.1186/1471-2407-12-480>
19. Kamino, M., Kishida, M., Kibe, T., Ikoma, K., Iijima, M., Hirano, H., Tokudome, M., Chen, L., Koriyama, C., Yamada, K., Arita, K., Kishida, S. (2011) Wnt-5a signaling is correlated with infiltrative activity in human glioma by inducing cellular migration and MMP-2. Cancer Sci. 102, 540-548. <https://doi.org/10.1111/j.1349-7006.2010.01815.x>
20. Kikuchi, A., Yamamoto, H., Sato, A., Matsumoto, S. (2012) Wnt5a: its signalling, functions and implication in diseases. Acta Physiol. (Oxf) 204, 17-33. <https://doi.org/10.1111/j.1748-1716.2011.02294.x>
21. Klaus, A., Birchmeier, W. (2008) Wnt signalling and its impact on development and cancer. Nat. Rev. Cancer 8, 387-398. <https://doi.org/10.1038/nrc2389>
22. Kremenevskaja, N., von Wasielewski, R., Rao, A. S., Schöfl, C., Andersson, T., Brabant, G. (2005) Wnt-5a has tumor suppressor activity in thyroid carcinoma. Oncogene 24, 2144-2154. <https://doi.org/10.1038/sj.onc.1208370>
23. Kurayoshi, M., Oue, N., Yamamoto, H., Kishida, M., Inoue, A., Asahara, T., Yasui, W., Kikuchi, A. (2006) Expression of Wnt­5a is correlated with aggressiveness of gastric cancer by stimulating cell migration and invasion. Cancer Res. 66, 10439-10448. <https://doi.org/10.1158/0008-5472.CAN-06-2359>
24. Lau, M. T., So, W. K., Leung, P. C. (2013) Fibroblast growth factor 2 induces E-cadherin down-regulation via PI3K/ Akt/mTOR and MAPK/ERK signaling in ovarian cancer cells. PLoS One 8, e59083. <https://doi.org/10.1371/journal.pone.0059083>
25. Liang, H., Chen, Q., Coles, A. H., Anderson, S. J., Pihan, G., Bradley, A., Gerstein, R., Jurecic, R., Jones, S. N. (2003) Wnt5a inhibits B cell proliferation and functions as a tumor suppressor in hematopoietic tissue. Cancer Cell 4, 349-360. <https://doi.org/10.1016/S1535-6108(03)00268-X>
26. Liu, J., Zhang, Y., Xu, R., Du, J., Hu, Z., Yang, L., Chen, Y., Zhu, Y., Gu, L. (2013) PI3K/Akt-dependent phosphorylation of GSK3β and activation of RhoA regulate Wnt5ainduced gastric cancer cell migration. Cell. Signal. 25, 447-456. <https://doi.org/10.1016/j.cellsig.2012.10.012>
27. Matei, D., Graeber, T. G., Baldwin, R. L., Karlan, B. Y., Rao, J., Chang, D. D. (2002) Gene expression in epithelial ovarian carcinoma. Oncogene 21, 6289-6298. <https://doi.org/10.1038/sj.onc.1205785>
28. McDonald, S. L., Silver, A. (2009) The opposing roles of Wnt­5a in cancer. Br. J. Cancer 101, 209-214. <https://doi.org/10.1038/sj.bjc.6605174>
29. Medrek, C., Landberg, G., Andersson, T., Leandersson, K. (2009) Wnt-5a-CKIα signaling promotes b-catenin/E-cadherin complex formation and intercellular adhesion in human breast epithelial cells. J. Biol. Chem. 284, 10968-10979. <https://doi.org/10.1074/jbc.M804923200>
30. Mikels, A. J., Nusse, R. (2006) Purified Wnt5a protein activates or inhibits b­catenin­TCF signaling depending on receptor context. PLoS Biol. 4, e115. <https://doi.org/10.1371/journal.pbio.0040115>
31. Nishita, M., Enomoto, M., Yamagata, K., Minami, Y. (2010) Cell/tissue-tropic functions of Wnt5a signaling in normal and cancer cells. Trends Cell. Biol. 20, 346-354. <https://doi.org/10.1016/j.tcb.2010.03.001>
32. O’Connell, M. P., Fiori, J. L., Xu, M., Carter, A. D., Frank, B. P., Camilli, T. C., French, A. D., Dissanayake, S. K., Indig, F. E., Bernier, M., Taub, D. D., Hewitt, S. M., Weeraratna, A. T. (2010) The orphan tyrosine kinase receptor, ROR2, mediates Wnt5A signaling in metastatic melanoma. Oncogene 29, 34-44. <https://doi.org/10.1038/onc.2009.305>
33. Patel, I. S., Madan, P., Getsios, S., Bertrand, M. A., MacCalman, C. D. (2003) Cadherin switching in ovarian cancer progression. Int. J. Cancer 106, 172-177. <https://doi.org/10.1002/ijc.11086>
34. Peng, C., Zhang, X., Yu, H., Wu, D., Zheng, J. (2011) Wnt5a as a predictor in poor clinical outcome of patients and a mediator in chemoresistance of ovarian cancer. Int. J. Gynecol. Cancer 21, 280-288. <https://doi.org/10.1097/IGC.0b013e31820aaadb>
35. Peralta Soler, A., Knudsen, K. A., Tecson­Miguel, A., McBrearty, F. X., Han, A. C., Salazar, H. (1997) Expression of E­cadherin and N­cadherin in surface epithelial­stromal tumors of the ovary distinguishes mucinous from serous and endometrioid tumors. Hum. Pathol. 28, 734-739.
36. Pukrop, T., Binder, C. (2008) The complex pathways of Wnt5a in cancer progression. J. Mol. Med. 86, 259-266. <https://doi.org/10.1007/s00109-007-0266-2>
37. Pourreyron, C., Reilly, L., Proby, C., Panteleyev, A., Fleming, C., McLean, K., South, A. P., Foerster, J. (2012) Wnt5a is strongly expressed at the leading edge in non-melanoma skin cancer, forming active gradients, while canonical Wnt signalling is repressed. PLoS One 7, e31827. <https://doi.org/10.1371/journal.pone.0031827>
38. Reddy, P., Liu, L., Ren, C., Lindgren, P., Boman, K., Shen, Y., Lundin, E., Ottander, U., Rytinki, M., Liu, K. (2005) Formation of E­cadherin­mediated cell­cell adhesion activates akt and mitogen activated protein kinase via phosphatidylinositol 3 kinase and ligand-independent activation of epidermal growth factor receptor in ovarian cancer cells. Mol. Endocrinol. 19, 2564-2578. <https://doi.org/10.1210/me.2004-0342>
39. Ren, D., Minami, Y., Nishita, M. (2011) Critical role of Wnt5a-Ror2 signaling in motility and invasiveness of carcinoma cells following Snail­mediated epithelial­mesenchymal transition. Genes Cells 16, 304-315. <https://doi.org/10.1111/j.1365-2443.2011.01487.x>
40. Ricken, A., Lochhead, P., Kontogiannea, M., Farookhi, R. (2002) Wnt signaling in the ovary: identification and compartmentalized expression of Wnt-2, Wnt-2b and frizzled-4 mRNAs. Endocrinology 143, 2741-2749. <https://doi.org/10.1210/endo.143.7.8908>
41. Säfholm, A., Tuomela, J., Rosenkvist, J., Dejmek, J., Härkönen, P., Andersson, T. (2008) The Wnt-5a-derived hexapeptide Foxy-5 inhibits breast cancer metastasis in vivo by targeting cell motility. Clin. Cancer Res. 14, 6556-6563. <https://doi.org/10.1158/1078-0432.CCR-08-0711>
42. Sawada, K., Mitra, A. K., Radjabi, A. R., Bhaskar, V., Kistner, E. O., Tretiakova, M., Jagadeeswaran, S., Montag, A., Becker, A., Kenny, H. A., Peter, M. E., Ramakrishnan, V., Yamada, S. D., Lengyel, E. (2008) Loss of E-cadherin promotes ovarian cancer metastasis via α5-integrin, which is a therapeutic target. Cancer Res. 68, 2329-2339. <https://doi.org/10.1158/0008-5472.CAN-07-5167>
43. Sundfeldt, K., Piontkewitz, Y., Ivarsson, K., Nilsson, O., Hellberg, P., Brännström, M., Janson, P. O., Enerback, S., Hedin, L. (1997) E-cadherin expression in human epithelial ovarian cancer and normal ovary. Int. J. Cancer 74, 275-280. <https://doi.org/10.1002/(SICI)1097-0215(19970620)74:3<275::AID-IJC7>3.0.CO;2-W>
44. Sundfeldt, K. (2003) Cell-cell adhesion in the normal ovary and ovarian tumors of epithelial origin; an exception to the rule. Mol. Cell. Endocrinol. 202, 89-96. <https://doi.org/10.1016/S0303-7207(03)00068-6>
45. Wu, C., Cipollone, J., Maines­Bandiera, S., Tan, C., Karsan, A., Auersperg, N., Roskelley, C. D. (2008) The morphogenic function of E­cadherin­mediated adherens junctions in epithelial ovarian carcinoma formation and progression. Differentiation 76, 193-205. <https://doi.org/10.1111/j.1432-0436.2007.00193.x>
46. Yamamoto, H., Oue, N., Sato, A., Hasegawa, Y., Yamamoto, H., Matsubara, A., Yasui, W., Kikuchi, A. (2010) Wnt5a signaling is involved in the aggressiveness of prostate cancer and expression of metalloproteinase. Oncogene 29, 2036-3046. <https://doi.org/10.1038/onc.2009.496>
47. Ying, J., Li, H., Chen, Y. W., Srivastava, G., Gao, Z., Tao, Q. (2007) WNT5A is epigenetically silenced in hematologic malignancies and inhibits leukemia cell growth as a tumor suppressor. Blood 110, 4130-4132. <https://doi.org/10.1182/blood-2007-06-094870>
48. Yook, J. I., Li, X. Y., Ota, I., Fearon, E. R., Weiss, S. J. (2005) Wnt­dependent regulation of the E­cadherin repressor Snail. J. Biol. Chem. 280, 11740-11748. <https://doi.org/10.1074/jbc.M413878200>
49. Zhu, Y., Tian, Y., Du, J., Hu, Z., Yang, L., Liu, J., Gu, L. (2012) Dvl2-dependent activation of Daam1 and RhoA regulates Wnt5a­induced breast cancer cell migration. PLoS One 7, e37823. <https://doi.org/10.1371/journal.pone.0037823>
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