SOX9 regulates low density lipoprotein receptor-related protein 6 (LRP6) and T-cell factor 4 (TCF4) expression and Wnt/β-catenin activation in breast cancer

Journal of Biological Chemistry

Volumn 288, Issue 9, 2013, Pages 6478-6487

  Wang, Hongyun ^a   He, Lingfeng ^a   Ma, Fen ^a   Regan, Meredith M ^b   Balk, Steven P ^a   Richardson, Andrea L ^b,c   Yuan, Xin ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER; CANCER CELL LINES; CATENIN SIGNALING; CELL LINES; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; LOW DENSITY LIPOPROTEINS; MOLECULAR MECHANISM; MOLECULAR SIGNALS; OVER-EXPRESSION; PATHWAY COMPONENTS; POSITIVE FEEDBACK LOOP; SIGNATURE GENES; T-CELL FACTORS; TRANSGENICS;

CELL CULTURE; CELL PROLIFERATION; PLANTS (BOTANY); TRANSCRIPTION;

DISEASES;

BETA CATENIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; PROTEIN TCF4; T CELL FACTOR PROTEIN; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER CELL CULTURE; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION PROFILING; GENE SILENCING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MOLECULAR MECHANICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; BETA CATENIN; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-6; MAMMARY GLANDS, ANIMAL; MAMMARY GLANDS, HUMAN; MAMMARY NEOPLASMS, ANIMAL; MICE; MICE, TRANSGENIC; NEOPLASM PROTEINS; SOX9 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTORS; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84874769801     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.419184     Document Type: Article

References (61)

1. Perou, C. M., Sørlie, T., Eisen, M. B., van de Rijn, M., Jeffrey, S. S., Rees, C. A., Pollack, J. R., Ross, D. T., Johnsen, H., Akslen, L. A., Fluge, O., Pergamenschikov, A., Williams, C., Zhu, S. X., Lønning, P. E., Børresen- Dale, A. L., Brown, P. O., and Botstein, D. (2000) Molecular portraits of human breast tumours. Nature 406, 747-752
2. Sørlie, T., Perou, C. M., Tibshirani, R., Aas, T., Geisler, S., Johnsen, H., Hastie, T., Eisen, M. B., van de Rijn, M., Jeffrey, S. S., Thorsen, T., Quist, H., Matese, J. C., Brown, P. O., Botstein, D., Lønning, P.E., and Børresen-Dale, A. L. (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. U.S.A. 98, 10869-10874
3. Rakha, E., and Reis-Filho, J. S. (2009) Basal-like breast carcinoma: from expression profiling to routine practice. Arch. Pathol. Lab. Med. 133, 860-868
4. Carey, L., Winer, E., Viale, G., Cameron, D., and Gianni, L. (2010) Triplenegative breast cancer: disease entity or title of convenience? Nat. Rev. Clin. Oncol. 7, 683-692
5. Khramtsov, A. I., Khramtsova, G. F., Tretiakova, M., Huo, D., Olopade, O. I., and Goss, K. H. (2010) Wnt/β-catenin pathway activation is enriched in basal-like breast cancers and predicts poor outcome. Am. J. Pathol. 176, 2911-2920
6. Liu, C. C., Prior, J., Piwnica-Worms, D., and Bu, G. (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
7. Geyer, F. C., Lacroix-Triki, M., Savage, K., Arnedos, M., Lambros, M. B., MacKay, A., Natrajan, R., and Reis-Filho, J. S. (2011) β-catenin pathway activation in breast cancer is associated with triple-negative phenotype but not with CTNNB1 mutation. Mod. Pathol. 24, 209-231
8. Clevers, H. (2006) Wnt/β-catenin signaling in development and disease. Cell 127, 469-480
9. Lin, S. Y., Xia, W., Wang, J. C., Kwong, K. Y., Spohn, B., Wen, Y., Pestell, R. G., and Hung, M. C. (2000) β-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
10. Ryo, A., Nakamura, M., Wulf, G., Liou, Y. C., and Lu, K. P. (2001) Pin1 regulates turnover and subcellular localization of β-catenin by inhibiting its interaction with APC. Nat. Cell Biol. 3, 793-801
11. Nakopoulou, L., Mylona, E., Papadaki, I., Kavantzas, N., Giannopoulou, I., Markaki, S., and Keramopoulos, A. (2006) Study of phospho-β-catenin subcellular distribution in invasive breast carcinomas in relation to their phenotype and the clinical outcome. Mod. Pathol. 19, 556-563
12. Lindvall, C., Zylstra, C. R., Evans, N., West, R. A., Dykema, K., Furge, K. A., and Williams, B. O. (2009) The Wnt co-receptor Lrp6 is required for normal mouse mammary gland development. PLoS. ONE. 4, e5813
13. Yang, L., Wu, X., Wang, Y., Zhang, K., Wu, J., Yuan, Y. C., Deng, X., Chen, L., Kim, C. C., Lau, S., Somlo, G., and Yen, Y. (2011) FZD7 has a critical role in cell proliferation in triple negative breast cancer. Oncogene 30, 4437-4446
14. Jönsson, M., Borg, A., Nilbert, M., and Andersson, T. (2000) Involvement of adenomatous polyposis coli (APC)/β-catenin signalling in human breast cancer. Eur. J. Cancer 36, 242-248
15. Schlosshauer, P. W., Brown, S. A., Eisinger, K., Yan, Q., Guglielminetti, E. R., Parsons, R., Ellenson, L. H., and Kitajewski, J. (2000) APC truncation and increased β-catenin levels in a human breast cancer cell line. Carcinogenesis 21, 1453-1456
16. Brennan, K. R., and Brown, A. M. (2004) Wnt proteins in mammary development and cancer. J. Mammary Gland Biol. Neoplasia 9, 119-131
17. Sorlie, T., Tibshirani, R., Parker, J., Hastie, T., Marron, J. S., Nobel, A., Deng, S., Johnsen, H., Pesich, R., Geisler, S., Demeter, J., Perou, C. M., Lønning, P. E., Brown, P. O., Børresen-Dale, A. L., and Botstein, D. (2003) Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc. Natl. Acad. Sci. U.S.A. 100, 8418-8423
18. Schepers, G. E., Teasdale, R. D., and Koopman, P. (2002) Twenty pairs of sox: extent, homology, and nomenclature of the mouse and human sox transcription factor gene families. Dev. Cell 3, 167-170
19. Foster, J. W., Dominguez-Steglich, M. A., Guioli, S., Kwok, G., Weller, P. A., Stevanović, M., Weissenbach, J., Mansour, S., Young, I. D., and Goodfellow, P. N. (1994) Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 372, 525-530
20. Wagner, T., Wirth, J., Meyer, J., Zabel, B., Held, M., Zimmer, J., Pasantes, J., Bricarelli, F. D., Keutel, J., Hustert, E., Wolf, U., Tommerup, N., Schempp, W., and Scherer, G. (1994) Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 79, 1111-1120
21. De Santa Barbara, P., Bonneaud, N., Boizet, B., Desclozeaux, M., Moniot, B., Sudbeck, P., Scherer, G., Poulat, F., and Berta, P. (1998) Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Müllerian hormone gene. Mol. Cell Biol. 18, 6653-6665
22. de Crombrugghe, B., Lefebvre, V., Behringer, R. R., Bi, W., Murakami, S., and Huang, W. (2000) Transcriptional mechanisms of chondrocyte differentiation. Matrix Biol. 19, 389-394
23. Kamachi, Y., Uchikawa, M., and Kondoh, H. (2000) Pairing SOX off: with partners in the regulation of embryonic development. Trends Genet. 16, 182-187
24. Guo, W., Keckesova, Z., Donaher, J. L., Shibue, T., Tischler, V., Reinhardt, F., Itzkovitz, S., Noske, A., Zürrer-Härdi, U., Bell, G., Tam, W. L., Mani, S. A., van Oudenaarden, A., and Weinberg, R. A. (2012) Slug and Sox9 cooperatively determine the mammary stem cell state. Cell 148, 1015-1028
25. Wang, Z. C., Lin, M., Wei, L. J., Li, C., Miron, A., Lodeiro, G., Harris, L., Ramaswamy, S., Tanenbaum, D. M., Meyerson, M., Iglehart, J. D., and Richardson, A. (2004) Loss of heterozygosity and its correlation with expression profiles in subclasses of invasive breast cancers. Cancer Res. 64, 64-71
26. Lu, X., Lu, X., Wang, Z. C., Iglehart, J. D., Zhang, X., and Richardson, A. L. (2008) Predicting features of breast cancer with gene expression patterns. Breast Cancer Res. Treat. 108, 191-201
27. Matros, E., Wang, Z. C., Lodeiro, G., Miron, A., Iglehart, J. D., and Richardson, A. L. (2005) BRCA1 promoter methylation in sporadic breast tumors: relationship to gene expression profiles. Breast Cancer Res. Treat. 91, 179-186
28. Wang, H., Leav, I., Ibaragi, S., Wegner, M., Hu, G. F., Lu, M. L., Balk, S. P., and Yuan, X. (2008) SOX9 is expressed in human fetal prostate epithelium and enhances prostate cancer invasion. Cancer Res. 68, 1625-1630
29. Li, C., and Wong, W. H. (2001) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc. Natl. Acad. Sci. U.S.A. 98, 31-36
30. Wang, H., McKnight, N. C., Zhang, T., Lu, M. L., Balk, S. P., and Yuan, X. (2007) SOX9 is expressed in normal prostate basal cells and regulates androgen receptor expression in prostate cancer cells. Cancer Res. 67, 528-536
31. DasGupta, R., Kaykas, A., Moon, R. T., and Perrimon, N. (2005) Functional genomic analysis of the Wnt-wingless signaling pathway. Science 308, 826-833
32. Tamai, K., Zeng, X., Liu, C., Zhang, X., Harada, Y., Chang, Z., and He, X. (2004) A mechanism for Wnt coreceptor activation. Mol. Cell 13, 149-156
33. Shang, Y., Myers, M., and Brown, M. (2002) Formation of the androgen receptor transcription complex. Mol. Cell 9, 601-610
34. Hennighausen, L., Wall, R. J., Tillmann, U., Li, M., and Furth, P. A. (1995) Conditional gene expression in secretory tissues and skin of transgenic mice using theMMTV-LTRand the tetracycline responsive system. J. Cell Biochem. 59, 463-472
35. Kao, J., Salari, K., Bocanegra, M., Choi, Y. L., Girard, L., Gandhi, J., Kwei, K. A., Hernandez-Boussard, T., Wang, P., Gazdar, A. F., Minna, J. D., and Pollack, J. R. (2009) Molecular profiling of breast cancer cell lines defines relevant tumor models and provides a resource for cancer gene discovery. PLoS ONE 4, e6146
36. Neve, R. M., Chin, K., Fridlyand, J., Yeh, J., Baehner, F. L., Fevr, T., Clark, L., Bayani, N., Coppe, J. P., Tong, F., Speed, T., Spellman, P. T., DeVries, S., Lapuk, A., Wang, N. J., Kuo, W. L., Stilwell, J. L., Pinkel, D., Albertson, D. G., Waldman, F. M., McCormick, F., Dickson, R. B., Johnson, M. D., Lippman, M., Ethier, S., Gazdar, A., and Gray, J. W. (2006) A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10, 515-527
37. Blache, P., van de Wetering, M., Duluc, I., Domon, C., Berta, P., Freund, J. N., Clevers, H., and Jay, P. (2004) SOX9 is an intestine crypt transcription factor, is regulated by the Wnt pathway, and represses the CDX2 and MUC2 genes. J. Cell Biol. 166, 37-47
38. Miller, F. R., Santner, S. J., Tait, L., and Dawson, P. J. (2000) MCF10DCIS.com xenograft model of human comedo ductal carcinoma in situ. J. Natl. Cancer Inst. 92, 1185-1186
39. Zhou, G., Lefebvre, V., Zhang, Z., Eberspaecher, H., and de Crombrugghe, B. (1998) Three high mobility group-like sequences within a 48-base pair enhancer of the Col2a1 gene are required for cartilage-specific expression in vivo. J. Biol. Chem. 273, 14989-14997
40. Rother, K., Johne, C., Spiesbach, K., Haugwitz, U., Tschöp, K., Wasner, M., Klein-Hitpass, L., Möröy, T., Mössner, J., and Engeland, K. (2004) Identification of Tcf-4 as a transcriptional target of p53 signalling. Oncogene 23, 3376-3384
41. Roarty, K., and Rosen, J. M. (2010) Wnt and mammary stem cells: hormones cannot fly wingless. Curr. Opin. Pharmacol. 10, 643-649
42. Gavin, B. J., and McMahon, A. P. (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
43. Bühler, T. A., Dale, T. C., Kieback, C., Humphreys, R. C., and Rosen, J. M. (1993) Localization and quantification of Wnt-2 gene expression in mouse mammary development. Dev. Biol. 155, 87-96
44. Weber-Hall, S. J., Phippard, D. J., Niemeyer, C. C., and Dale, T. C. (1994) Developmental and hormonal regulation of Wnt gene expression in the mouse mammary gland. Differentiation 57, 205-214
45. Kouros-Mehr, H., and Werb, Z. (2006) Candidate regulators of mammary branching morphogenesis identified by genome-wide transcript analysis. Dev. Dyn. 235, 3404-3412
46. Brisken, C., Heineman, A., Chavarria, T., Elenbaas, B., Tan, J., Dey, S. K., McMahon, J. A., McMahon, A. P., and Weinberg, R. A. (2000) Essential function of Wnt-4 in mammary gland development downstream of progesterone signaling. Genes Dev. 14, 650-654
47. Lindvall, C., Evans, N. C., Zylstra, C. R., Li, Y., Alexander, C. M., and Williams, B. O. (2006) The Wnt signaling receptor Lrp5 is required for mammary ductal stem cell activity and Wnt1-induced tumorigenesis. J. Biol. Chem. 281, 35081-35087
48. Imbert, A., Eelkema, R., Jordan, S., Feiner, H., and Cowin, P. (2001) δ N89 β-catenin induces precocious development, differentiation, and neoplasia in mammary gland. J. Cell Biol. 153, 555-568
49. Zhang, J., Li, Y., Liu, Q., Lu, W., and Bu, G. (2010) Wnt signaling activation and mammary gland hyperplasia in MMTV-LRP6 transgenic mice: implication for breast cancer tumorigenesis. Oncogene 29, 539-549
50. Badders, N. M., Goel, S., Clark, R. J., Klos, K. S., Kim, S., Bafico, A., Lindvall, C., Williams, B. O., and Alexander, C. M. (2009) The Wnt receptor, Lrp5, is expressed by mouse mammary stem cells and is required to maintain the basal lineage. PLoS ONE 4, e6594
51. Zeng, Y. A., and Nusse, R. (2010) Wnt proteins are self-renewal factors for mammary stem cells and promote their long-term expansion in culture. Cell Stem Cell 6, 568-577
52. Bastide, P., Darido, C., Pannequin, J., Kist, R., Robine, S., Marty-Double, C., Bibeau, F., Scherer, G., Joubert, D., Hollande, F., Blache, P., and Jay, P. (2007) Sox9 regulates cell proliferation and is required for Paneth cell differentiation in the intestinal epithelium. J. Cell Biol. 178, 635-648
53. Mori-Akiyama, Y., van den Born, M., van Es, J. H., Hamilton, S. R., Adams, H. P., Zhang, J., Clevers, H., and de Crombrugghe, B. (2007) SOX9 is required for the differentiation of paneth cells in the intestinal epithelium. Gastroenterology 133, 539-546
54. Vidal, V. P., Chaboissier, M. C., Lützkendorf, S., Cotsarelis, G., Mill, P., Hui, C. C., Ortonne, N., Ortonne, J. P., and Schedl, A. (2005) Sox9 is essential for outer root sheath differentiation and the formation of the hair stem cell compartment. Curr. Biol. 15, 1340-1351
55. Furuyama, K., Kawaguchi, Y., Akiyama, H., Horiguchi, M., Kodama, S., Kuhara, T., Hosokawa, S., Elbahrawy, A., Soeda, T., Koizumi, M., Masui, T., Kawaguchi, M., Takaori, K., Doi, R., Nishi, E., Kakinoki, R., Deng, J. M., Behringer, R. R., Nakamura, T., and Uemoto, S. (2011) Continuous cell supply from a Sox9-expressing progenitor zone in adult liver, exocrine pancreas and intestine. Nat. Genet. 43, 34-41
56. Topol, L., Chen, W., Song, H., Day, T. F., and Yang, Y. (2009) Sox9 inhibits Wnt signaling by promoting β-catenin phosphorylation in the nucleus. J. Biol. Chem. 284, 3323-3333
57. Akiyama, H., Lyons, J. P., Mori-Akiyama, Y., Yang, X., Zhang, R., Zhang, Z., Deng, J. M., Taketo, M. M., Nakamura, T., Behringer, R. R., McCrea, P. D., and de Crombrugghe, B. (2004) Interactions between Sox9 and β-catenin control chondrocyte differentiation. Genes Dev. 18, 1072-1087
58. Afonja, O., Raaka, B. M., Huang, A., Das, S., Zhao, X., Helmer, E., Juste, D., and Samuels, H. H. (2002) RAR agonists stimulate SOX9 gene expression in breast cancer cell lines: evidence for a role in retinoid-mediated growth inhibition. Oncogene 21, 7850-7860
59. Müller, P., Crofts, J. D., Newman, B. S., Bridgewater, L. C., Lin, C. Y., Gustafsson, J. A., and Ström, A. (2010) SOX9 mediates the retinoic acidinduced HES-1 gene expression in human breast cancer cells. Breast Cancer Res. Treat 120, 317-326
60. Polakis, P. (2000) Wnt signaling and cancer. Genes Dev. 14, 1837-1851
61. Hatsell, S., Rowlands, T., Hiremath, M., and Cowin, P. (2003) β-catenin and Tcfs in mammary development and cancer. J. Mammary Gland Biol. Neoplasia 8, 145-158