The embryonic transcription cofactor LBH is a direct target of the Wnt signaling pathway in epithelial development and in aggressive basal subtype breast cancers

Molecular and Cellular Biology

Volumn 30, Issue 17, 2010, Pages 4267-4279

  Rieger, Megan E ^a   Sims, Andrew H ^b,c   Coats, Ebony R ^a,d   Clarke, Robert B ^b   Briegel, Karoline J ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c Edinburgh Cancer Research Centre   (United Kingdom)

^d UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; DICKKOPF 1 PROTEIN; T CELL FACTOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LBH; TRANSCRIPTION FACTOR LEF; TRANSCRIPTION FACTOR LMX1B; UNCLASSIFIED DRUG; WNT PROTEIN; WNT3A PROTEIN; WNT7A PROTEIN; LBH PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; BREAST CANCER; BREAST EPITHELIUM; CARCINOGENESIS; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; EPITHELIUM CELL; GENE IDENTIFICATION; GENE LOCUS; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LIMB DEVELOPMENT; MOUSE MAMMARY TUMOR ONCOVIRUS; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; TUMOR CELL; UPREGULATION; WESTERN BLOTTING; ANIMAL; BREAST TUMOR; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; LIMB; METABOLISM; MOUSE; PATHOLOGY; PRENATAL DEVELOPMENT; TRANSGENIC MOUSE; TUMOR CELL LINE;

MOUSE MAMMARY TUMOR VIRUS; MUS MUSCULUS; VERTEBRATA;

ANIMALS; BETA CATENIN; BREAST NEOPLASMS; CELL DIFFERENTIATION; CELL LINE, TUMOR; EPITHELIAL CELLS; EXTREMITIES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC LOCI; HUMANS; MICE; MICE, TRANSGENIC; TRANS-ACTIVATORS; WNT PROTEINS;

EID: 77956264304     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01418-09     Document Type: Article

References (81)

1. Adamska, M., B. T. MacDonald, Z. H. Sarmast, E. R. Oliver, and M. H. Meisler. 2004. En1 and Wnt7a interact with Dkk1 during limb development in the mouse. Dev. Biol. 272:134-144.
2. Al-Ali, H., M. E. Rieger, K. L. Seldeen, T. K. Harris, A. Farooq, and K. J. Briegel. 2010. Biophysical characterization reveals structural disorder in the developmental transcriptional regulator LBH. Biochem. Biophys. Res. Commun. 391:1104-1109.
3. Ball, R. K., R. R. Friis, C. A. Schoenenberger, W. Doppler, and B. Groner. 1988. Prolactin regulation of beta-casein gene expression and of a cytosolic 120-kd protein in a cloned mouse mammary epithelial cell line. EMBO J. 7:2089-2095.
4. Barrow, J. R., K. R. Thomas, O. Boussadia-Zahui, R. Moore, R. Kemler, M. R. Capecchi, and A. P. McMahon. 2003. Ectodermal Wnt3/beta-catenin signaling is required for the establishment and maintenance of the apical ectodermal ridge. Genes Dev. 17:394-409.
5. Ben-Porath, I., M. W. Thomson, V. J. Carey, R. Ge, G. W. Bell, A. Regev, and R. A. Weinberg. 2008. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat. Genet. 40:499-507.
6. Briegel, K. J. 2006. Embryonic transcription factors in human breast cancer. IUBMB Life 58:123-132. (Pubitemid 43786037)
7. Briegel, K. J., H. S. Baldwin, J. A. Epstein, and A. L. Joyner. 2005. Congenital heart disease reminiscent of partial trisomy 2p syndrome in mice transgenic for the transcription factor Lbh. Development 132:3305-3316.
8. Briegel, K. J., and A. L. Joyner. 2001. Identification and characterization of Lbh, a novel conserved nuclear protein expressed during early limb and heart development. Dev. Biol. 233:291-304.
9. Brisken, C., A. Heineman, T. Chavarria, B. Elenbaas, J. Tan, S. K. Dey, J. A. McMahon, A. P. McMahon, and R. A. Weinberg. 2000. Essential function of Wnt-4 in mammary gland development downstream of progesterone signaling. Genes Dev. 14:650-654.
10. Buhler, T. A., T. C. Dale, C. Kieback, R. C. Humphreys, and J. M. Rosen. 1993. Localization and quantification of Wnt-2 gene expression in mouse mammary development. Dev. Biol. 155:87-96.
11. Calza, S., P. Hall, G. Auer, J. Bjohle, S. Klaar, U. Kronenwett, E. T. Liu, L. Miller, A. Ploner, J. Smeds, J. Bergh, and Y. Pawitan. 2006. Intrinsic molecular signature of breast cancer in a population-based cohort of 412 patients. Breast Cancer Res. 8:R34.
12. Carmon, K. S., and D. S. Loose. 2008. Secreted frizzled-related protein 4 regulates two Wnt7a signaling pathways and inhibits proliferation in endometrial cancer cells. Mol. Cancer Res. 6:1017-1028.
13. Chamorro, M. N., D. R. Schwartz, A. Vonica, A. H. Brivanlou, K. R. Cho, and H. E. Varmus. 2005. FGF-20 and DKK1 are transcriptional targets of beta-catenin and FGF-20 is implicated in cancer and development. EMBO J. 24:73-84.
14. Chen, H., and R. L. Johnson. 1999. Dorsoventral patterning of the vertebrate limb: a process governed by multiple events. Cell Tissue Res. 296:67-73.
15. Chen, H., Y. Lun, D. Ovchinnikov, H. Kokubo, K. C. Oberg, C. V. Pepicelli, L. Gan, B. Lee, and R. L. Johnson. 1998. Limb and kidney defects in Lmx1b mutant mice suggest an involvement of LMX1B in human nail patella syndrome. Nat. Genet. 19:51-55.
16. Chin, K., S. DeVries, J. Fridlyand, P. T. Spellman, R. Roydasgupta, W. L. Kuo, A. Lapuk, R. M. Neve, Z. Qian, T. Ryder, F. Chen, H. Feiler, T. Tokuyasu, C. Kingsley, S. Dairkee, Z. Meng, K. Chew, D. Pinkel, A. Jain, B. M. Ljung, L. Esserman, D. G. Albertson, F. M. Waldman, and J. W. Gray. 2006. Genomic and transcriptional aberrations linked to breast cancer pathophysiologies. Cancer Cell 10:529-541.
17. Civenni, G., T. Holbro, and N. E. Hynes. 2003. Wnt1 and Wnt5a induce cyclin D1 expression through ErbB1 transactivation in HC11 mammary epithelial cells. EMBO Rep. 4:166-171.
18. Clevers, H. 2006. Wnt/beta-catenin signaling in development and disease. Cell 127:469-480.
19. Conen, K. L., S. Nishimori, S. Provot, and H. M. Kronenberg. 2009. The transcriptional cofactor Lbh regulates angiogenesis and endochondral bone formation during fetal bone development. Dev. Biol. 333:348-358.
20. Crockford, G. P., R. Linger, S. Hockley, D. Dudakia, L. Johnson, R. Huddart, K. Tucker, M. Friedlander, K. A. Phillips, D. Hogg, M. A. Jewett, R. Lohynska, G. Daugaard, S. Richard, A. Chompret, C. Bonaiti-Pellie, A. Heidenreich, P. Albers, E. Olah, L. Geczi, I. Bodrogi, W. J. Ormiston, P. A. Daly, P. Guilford, S. D. Fossa, K. Heimdal, S. A. Tjulandin, L. Liubchenko, H. Stoll, W. Weber, D. Forman, T. Oliver, L. Einhorn, M. McMaster, J. Kramer, M. H. Greene, B. L. Weber, K. L. Nathanson, V. Cortessis, D. F. Easton, D. T. Bishop, M. R. Stratton, and E. A. Rapley. 2006. Genome-wide linkage screen for testicular germ cell tumour susceptibility loci. Hum. Mol. Genet. 15:443-451.
21. Desmedt, C., F. Piette, S. Loi, Y. Wang, F. Lallemand, B. Haibe-Kains, G. Viale, M. Delorenzi, Y. Zhang, M. S. d'Assignies, J. Bergh, R. Lidereau, P. Ellis, A. L. Harris, J. G. Klijn, J. A. Foekens, F. Cardoso, M. J. Piccart, M. Buyse, and C. Sotiriou. 2007. Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series. Clin. Cancer Res. 13:3207-3214.
22. DiMeo, T. A., K. Anderson, P. Phadke, C. Feng, C. M. Perou, S. Naber, and C. Kuperwasser. 2009. A novel lung metastasis signature links Wnt signaling with cancer cell self-renewal and epithelial-mesenchymal transition in basal-like breast cancer. Cancer Res. 69:5364-5373.
23. Eisen, M. B., P. T. Spellman, P. O. Brown, and D. Botstein. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U. S. A. 95:14863-14868.
24. Gavin, B. J., and A. P. McMahon. 1992. Differential regulation of the Wnt gene family during pregnancy and lactation suggests a role in postnatal development of the mammary gland. Mol. Cell. Biol. 12:2418-2423.
25. Giese, K., A. Amsterdam, and R. Grosschedl. 1991. DNA-binding properties of the HMG domain of the lymphoid-specific transcriptional regulator LEF-1. Genes Dev. 5:2567-2578. (Pubitemid 21905940)
26. Gonzalez-Sancho, J. M., O. Aguilera, J. M. Garcia, N. Pendas-Franco, C. Pena, S. Cal, A. Garcia de Herreros, F. Bonilla, and A. Munoz. 2005. The Wnt antagonist DICKKOPF-1 gene is a downstream target of beta-catenin/TCF and is downregulated in human colon cancer. Oncogene 24:1098-1103.
27. Griffin, C. A., A. L. Hawkins, C. Dvorak, C. Henkle, T. Ellingham, and E. J. Perlman. 1999. Recurrent involvement of 2p23 in inflammatory myofibroblastic tumors. Cancer Res. 59:2776-2780.
28. Hayes, M. J., D. Thomas, A. Emmons, T. J. Giordano, and C. G. Kleer. 2008. Genetic changes of Wnt pathway genes are common events in metaplastic carcinomas of the breast. Clin. Cancer Res. 14:4038-4044.
29. Hecht, A., K. Vleminckx, M. P. Stemmler, F. van Roy, and R. Kemler. 2000. The p300/CBP acetyltransferases function as transcriptional coactivators of beta-catenin in vertebrates. EMBO J. 19:1839-1850. (Pubitemid 30204395)
30. Herschkowitz, J. I., K. Simin, V. J. Weigman, I. Mikaelian, J. Usary, Z. Hu, K. E. Rasmussen, L. P. Jones, S. Assefnia, S. Chandrasekharan, M. G. Backlund, Y. Yin, A. I. Khramtsov, R. Bastein, J. Quackenbush, R. I. Glazer, P. H. Brown, J. E. Green, L. Kopelovich, P. A. Furth, J. P. Palazzo, O. I. Olopade, P. S. Bernard, G. A. Churchill, T. Van Dyke, and C. M. Perou. 2007. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol. 8:R76.
31. Howe, L. R., O. Watanabe, J. Leonard, and A. M. Brown. 2003. Twist is up-regulated in response to Wnt1 and inhibits mouse mammary cell differentiation. Cancer Res. 63:1906-1913.
32. Humphreys, R. C., and J. M. Rosen. 1997. Stably transfected HC11 cells provide an in vitro and in vivo model system for studying Wnt gene function. Cell Growth Differ. 8:839-849.
33. Imbert, A., R. Eelkema, S. Jordan, H. Feiner, and P. Cowin. 2001. Delta N89 beta-catenin induces precocious development, differentiation, and neoplasia in mammary gland. J. Cell Biol. 153:555-568.
34. Ivshina, A. V., J. George, O. Senko, B. Mow, T. C. Putti, J. Smeds, T. Lindahl, Y. Pawitan, P. Hall, H. Nordgren, J. E. Wong, E. T. Liu, J. Bergh, V. A. Kuznetsov, and L. D. Miller. 2006. Genetic reclassification of histologic grade delineates new clinical subtypes of breast cancer. Cancer Res. 66:10292-10301.
35. Kansal, R., S. N. Sait, A. W. Block, P. M. Ward, F. L. Kelly, R. T. Cheney, M. Czuczman, M. L. Brecher, and M. Barcos. 2005. Extra copies of chromosome 2 are a recurring aberration in ALK-negative lymphomas with anaplastic morphology. Mod. Pathol. 18:235-243.
36. Kao, J., K. Salari, M. Bocanegra, Y. L. Choi, L. Girard, J. Gandhi, K. A. Kwei, T. Hernandez-Boussard, P. Wang, A. F. Gazdar, J. D. Minna, and J. R. Pollack. 2009. Molecular profiling of breast cancer cell lines defines relevant tumor models and provides a resource for cancer gene discovery. PLoS One 4:e6146.
37. Kengaku, M., J. Capdevila, C. Rodriguez-Esteban, J. De La Pena, R. L. Johnson, J. C. I. Belmonte, and C. J. Tabin. 1998. Distinct WNT pathways regulating AER formation and dorsoventral polarity in the chick limb bud. Science 280:1274-1277.
38. Khramtsov, A. I., G. F. Khramtsova, M. Tretiakova, D. Huo, O. I. Olopade, and K. H. Goss. 2010. Wnt/{beta}-catenin pathway activation is enriched in basal-like breast cancers and predicts poor outcome. Am. J. Pathol. 176:2911-2920.
39. Komiya, Y., and R. Habas. 2008. Wnt signal transduction pathways. Organogenesis 4:68-75.
40. Le Grand, F., A. E. Jones, V. Seale, A. Scime, and M. A. Rudnicki. 2009. Wnt7a activates the planar cell polarity pathway to drive the symmetric expansion of satellite stem cells. Cell Stem Cell 4:535-547.
41. Lin, S. Y., W. Xia, J. C. Wang, K. Y. Kwong, B. Spohn, Y. Wen, R. G. Pestell, and M. C. Hung. 2000. Beta-catenin, a novel prognostic marker for breast cancer: its roles in cyclin D1 expression and cancer progression. Proc. Natl. Acad. Sci. U. S. A. 97:4262-4266.
42. Liu, C. C., J. Prior, D. Piwnica-Worms, and G. Bu. 2010. LRP6 overexpression defines a class of breast cancer subtype and is a target for therapy. Proc. Natl. Acad. Sci. U. S. A. 107:5136-5141.
43. Liu, Y., M. Asakura, H. Inoue, T. Nakamura, M. Sano, Z. Niu, M. Chen, R. J. Schwartz, and M. D. Schneider. 2007. Sox17 is essential for the specification of cardiac mesoderm in embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 104:3859-3864.
44. Logan, C. Y., and R. Nusse. 2004. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20:781-810.
45. Loomis, C. A., E. Harris, J. Michaud, W. Wurst, M. Hanks, and A. L. Joyner. 1996. The mouse Engrailed-1 gene and ventral limb patterning. Nature 382:360-363.
46. Lurie, I. W., H. G. Ilyina, D. B. Gurevich, N. V. Rumyantseva, I. V. Naumchik, C. Castellan, A. Hoeller, and A. Schinzel. 1995. Trisomy 2p: analysis of unusual phenotypic findings. Am. J. Med. Genet. 55:229-236.
47. Mani, S. A., J. Yang, M. Brooks, G. Schwaninger, A. Zhou, N. Miura, J. L. Kutok, K. Hartwell, A. L. Richardson, and R. A. Weinberg. 2007. Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers. Proc. Natl. Acad. Sci. U. S. A. 104:10069-10074.
48. Mikels, A. J., and R. Nusse. 2006. Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol. 4:e115.
49. Neve, R. M., K. Chin, J. Fridlyand, J. Yeh, F. L. Baehner, T. Fevr, L. Clark, N. Bayani, J. P. Coppe, F. Tong, T. Speed, P. T. Spellman, S. DeVries, A. Lapuk, N. J. Wang, W. L. Kuo, J. L. Stilwell, D. Pinkel, D. G. Albertson, F. M. Waldman, F. McCormick, R. B. Dickson, M. D. Johnson, M. Lippman, S. Ethier, A. Gazdar, and J. W. Gray. 2006. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10:515-527.
50. Niehrs, C. 2006. Function and biological roles of the Dickkopf family of Wnt modulators. Oncogene 25:7469-7481. (Pubitemid 44885746)
51. Niida, A., T. Hiroko, M. Kasai, Y. Furukawa, Y. Nakamura, Y. Suzuki, S. Sugano, and T. Akiyama. 2004. DKK1, a negative regulator of Wnt signaling, is target of the beta-catenin/TCF pathway. Oncogene 23:8520-8526. (Pubitemid 39540802)
52. Nusse, R., C. Fuerer, W. Ching, K. Harnish, C. Logan, A. Zeng, D. Ten Berge, and Y. Kalani. 2008. Wnt signaling and stem cell control. Cold Spring Harbor Symp. Quant Biol. 73:59-66.
53. Nusse, R., and H. E. Varmus. 1982. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell 31:99-109.
54. Oosterwegel, M., M. van de Wetering, J. Timmerman, A. Kruisbeek, O. Destree, F. Meijlink, and H. Clevers. 1993. Differential expression of the HMG box factors TCF-1 and LEF-1 during murine embryogenesis. Development 118:439-448. (Pubitemid 23214031)
55. Parr, B. A., and A. P. McMahon. 1995. Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374:350-353.
56. Pawitan, Y., J. Bjohle, L. Amler, A. L. Borg, S. Egyhazi, P. Hall, X. Han, L. Holmberg, F. Huang, S. Klaar, E. T. Liu, L. Miller, H. Nordgren, A. Ploner, K. Sandelin, P. M. Shaw, J. Smeds, L. Skoog, S. Wedren, and J. Bergh. 2005. Gene expression profiling spares early breast cancer patients from adjuvant therapy: derived and validated in two population-based cohorts. Breast Cancer Res. 7:R953-R964.
57. Perou, C. M., T. Sorlie, M. B. Eisen, M. van de Rijn, S. S. Jeffrey, C. A. Rees, J. R. Pollack, D. T. Ross, H. Johnsen, L. A. Akslen, O. Fluge, A. Pergamenschikov, C. Williams, S. X. Zhu, P. E. Lonning, A. L. Borresen-Dale, P. O. Brown, and D. Botstein. 2000. Molecular portraits of human breast tumours. Nature 406:747-752.
58. Qian, D., C. Jones, A. Rzadzinska, S. Mark, X. Zhang, K. P. Steel, X. Dai, and P. Chen. 2007. Wnt5a functions in planar cell polarity regulation in mice. Dev. Biol. 306:121-133.
59. Rodriguez-Pinilla, S. M., D. Sarrio, G. Moreno-Bueno, Y. Rodriguez-Gil, M. A. Martinez, L. Hernandez, D. Hardisson, J. S. Reis-Filho, and J. Palacios. 2007. Sox2: a possible driver of the basal-like phenotype in sporadic breast cancer. Mod. Pathol. 20:474-481.
60. Satge, D., S. W. Moore, C. A. Stiller, F. K. Niggli, K. Pritchard-Jones, N. Bown, J. Benard, and D. Plantaz. 2003. Abnormal constitutional karyotypes in patients with neuroblastoma: a report of four new cases and review of 47 others in the literature. Cancer Genet. Cytogenet. 147:89-98.
61. Seifert, J. R., and M. Mlodzik. 2007. Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility. Nat. Rev. Genet. 8:126-138.
62. Semenov, M. V., R. Habas, B. T. Macdonald, and X. He. 2007. SnapShot: noncanonical Wnt signaling pathways. Cell 131:1378.
63. Sims, A. H., G. J. Smethurst, Y. Hey, M. J. Okoniewski, S. D. Pepper, A. Howell, C. J. Miller, and R. B. Clarke. 2008. The removal of multiplicative, systematic bias allows integration of breast cancer gene expression data-sets - improving meta-analysis and prediction of prognosis. BMC Med. Genomics 1:42.
64. Smid, M., Y. Wang, Y. Zhang, A. M. Sieuwerts, J. Yu, J. G. Klijn, J. A. Foekens, and J. W. Martens. 2008. Subtypes of breast cancer show preferential site of relapse. Cancer Res. 68:3108-3114.
65. Sorlie, T., C. M. Perou, R. Tibshirani, T. Aas, S. Geisler, H. Johnsen, T. Hastie, M. B. Eisen, M. van de Rijn, S. S. Jeffrey, T. Thorsen, H. Quist, J. C. Matese, P. O. Brown, D. Botstein, P. Eystein Lonning, and A. L. Borresen-Dale. 2001. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. U. S. A. 98:10869-10874.
66. Sorlie, T., R. Tibshirani, J. Parker, T. Hastie, J. S. Marron, A. Nobel, S. Deng, H. Johnsen, R. Pesich, S. Geisler, J. Demeter, C. M. Perou, P. E. Lonning, P. O. Brown, A. L. Borresen-Dale, and D. Botstein. 2003. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc. Natl. Acad. Sci. U. S. A. 100:8418-8423.
67. Soshnikova, N., D. Zechner, J. Huelsken, Y. Mishina, R. R. Behringer, M. M. Taketo, E. B. Crenshaw III, and W. Birchmeier. 2003. Genetic interaction between Wnt/beta-catenin and BMP receptor signaling during formation of the AER and the dorsal-ventral axis in the limb. Genes Dev. 17:1963-1968. (Pubitemid 36999323)
68. Sotiriou, C., P. Wirapati, S. Loi, A. Harris, S. Fox, J. Smeds, H. Nordgren, P. Farmer, V. Praz, B. Haibe-Kains, C. Desmedt, D. Larsimont, F. Cardoso, H. Peterse, D. Nuyten, M. Buyse, M. J. Van de Vijver, J. Bergh, M. Piccart, and M. Delorenzi. 2006. Gene expression profiling in breast cancer: understanding the molecular basis of histologic grade to improve prognosis. J. Natl. Cancer Inst. 98:262-272.
69. Teuliere, J., M. M. Faraldo, M. A. Deugnier, M. Shtutman, A. Ben-Ze'ev, J. P. Thiery, and M. A. Glukhova. 2005. Targeted activation of beta-catenin signaling in basal mammary epithelial cells affects mammary development and leads to hyperplasia. Development 132:267-277.
70. Tickle, C. 1999. Morphogen gradients in vertebrate limb development. Semin. Cell Dev. Biol. 10:345-351.
71. Tsukamoto, A. S., R. Grosschedl, R. C. Guzman, T. Parslow, and H. E. Varmus. 1988. Expression of the int-1 gene in transgenic mice is associated with mammary gland hyperplasia and adenocarcinomas in male and female mice. Cell 55:619-625.
72. Turashvili, G., J. Bouchal, G. Burkadze, and Z. Kolar. 2006. Wnt signaling pathway in mammary gland development and carcinogenesis. Pathobiology 73:213-223. (Pubitemid 46332829)
73. van Amerongen, R., A. Mikels, and R. Nusse. 2008. Alternative wnt signaling is initiated by distinct receptors. Sci. Signal. 1:re9.
74. van de Wetering, M., N. Barker, I. C. Harkes, M. van der Heyden, N. J. Dijk, A. Hollestelle, J. G. Klijn, H. Clevers, and M. Schutte. 2001. Mutant E-cadherin breast cancer cells do not display constitutive Wnt signaling. Cancer Res. 61:278-284.
75. van de Wetering, M., M. Oosterwegel, D. Dooijes, and H. Clevers. 1991. Identification and cloning of TCF-1, a T lymphocyte-specific transcription factor containing a sequence-specific HMG box. EMBO J. 10:123-132.
76. Wang, Y., J. G. Klijn, Y. Zhang, A. M. Sieuwerts, M. P. Look, F. Yang, D. Talantov, M. Timmermans, M. E. Meijer-van Gelder, J. Yu, T. Jatkoe, E. M. Berns, D. Atkins, and J. A. Foekens. 2005. Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 365:671-679.
77. Winn, R. A., L. Marek, S. Y. Han, K. Rodriguez, N. Rodriguez, M. Hammond, M. Van Scoyk, H. Acosta, J. Mirus, N. Barry, Y. Bren-Mattison, T. J. Van Raay, R. A. Nemenoff, and L. E. Heasley. 2005. Restoration of Wnt-7a expression reverses non-small cell lung cancer cellular transformation through frizzled-9-mediated growth inhibition and promotion of cell differentiation. J. Biol. Chem. 280:19625-19634.
78. Xu, L., R. B. Corcoran, J. W. Welsh, D. Pennica, and A. J. Levine. 2000. WISP-1 is a Wnt-1- and beta-catenin-responsive oncogene. Genes Dev. 14:585-595.
79. Yang, J., S. A. Mani, J. L. Donaher, S. Ramaswamy, R. A. Itzykson, C. Come, P. Savagner, I. Gitelman, A. Richardson, and R. A. Weinberg. 2004. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117:927-939.
80. Yang, J., and R. A. Weinberg. 2008. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14:818-829.
81. Zecca, M., K. Basler, and G. Struhl. 1996. Direct and long-range action of a wingless morphogen gradient. Cell 87:833-844. (Pubitemid 26404283)