Nuclear localization of GLI1 and elevated expression of FOXC2 in breast cancer is associated with the basal-like phenotype

Histology and Histopathology

Volumn 27, Issue 4, 2012, Pages 475-484

  Li, Yuan ^a   Yang, Wentao ^a   Yang, Qin ^b   Zhou, Sheng ^b  

^a FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Forkhead box C2; FOXC2; Gli1; Gliomaassociated oncogene homolog 1; IBC; Invasive breast cancers; Shh; Sonic hedgehog

Indexed keywords

FORKHEAD TRANSCRIPTION FACTOR; GLI1 PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXC2;

ADENOCARCINOMA; ADULT; AGED; ARTICLE; BASAL CELL CARCINOMA; BREAST TUMOR; CELL NUCLEUS; CHINA; COLLOID CARCINOMA; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LUNG CARCINOMA; MASTECTOMY; MEDULLARY CARCINOMA; METABOLISM; METASTASIS; MIDDLE AGED; MORTALITY; MULTIMODALITY CANCER THERAPY; PAGET NIPPLE DISEASE; PATHOLOGY; PROGNOSIS; SURVIVAL RATE; TISSUE MICROARRAY;

ADENOCARCINOMA; ADENOCARCINOMA, MUCINOUS; ADULT; AGED; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CARCINOMA, LOBULAR; CARCINOMA, MEDULLARY; CELL NUCLEUS; CHINA; COMBINED MODALITY THERAPY; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MASTECTOMY; MIDDLE AGED; NEOPLASMS, BASAL CELL; PROGNOSIS; SURVIVAL RATE; TISSUE ARRAY ANALYSIS; TRANSCRIPTION FACTORS;

ERINACEIDAE;

EID: 84863256043     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (34)

1. Cheang M.C., Voduc D., Bajdik C., Leung S., McKinney S., Chia S.K., Perou C.M. and Nielsen T.O. (2008). Basal-like breast cancer defined by five biomarkers has superior prognostic value than triplenegative phenotype. Clin. Cancer Res. 14, 1368-1376.
2. Dahmane N., Lee J., Robins P., Heller P. and Ruiz i Altaba A. (1997). Activation of the transcription factor Gli1 and the Sonic hedgehog signalling pathway in skin tumours. Nature 389, 876-881.
3. Karhadkar S.S., Bova G.S., Abdallah N., Dhara S., Gardner D., Maitra A., Isaacs J.T., Berman D.M. and Beachy P.A. (2004). Hedgehog signalling in prostate regeneration, neoplasia and metastasis. Nature 431,707-712.
4. Katoh M. and Katoh M. (2009).Transcriptional mechanisms of WNT5A based on NF-kappaB, Hedgehog, TGFbeta, and Notch signaling cascades. Int. J. Mol. Med. 23, 763-769.
5. Kasper M., Regl G., Frischauf A.M. and Aberger F. (2006).GLI transcription factors: mediators of oncogenic Hedgehog signalling. Eur. J. Cancer 42, 437-445.
6. Kononen J., Bubendorf L., Kallioniemi A., Bärlund M., Schraml P., Leighton S., Torhorst J., Mihatsch M.J., Sauter G. and Kallioniemi O.P. (1998).Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nat. Med. 4, 844-847.
7. Kubo M., Nakamura M., Tasaki A., Yamanaka N., Nakashima H., Nomura M., Kuroki S. and Katano M. (2004). Hedgehog signaling pathway is a new therapeutic target for patients with breast cancer. Cancer Res. 64, 6071-6074.
8. Kume T., Deng K. and Hogan B.L. (2000). Murine forkhead/winged helix genes Foxc1 (Mf1) and Foxc2 (Mfh1) are required for the early organogenesis of the kidney and urinary tract. Development 127, 1387-1395.
9. Lauth M. and Toftgard R. (2007). Non-canonical activation of GLI transcription factors: implications for targeted anti-cancer therapy. Cell Cycle 6, 2458-2463.
10. Lee J., Platt K.A., Censullo P. and Ruiz i Altaba A.(1997). Gli1 is a target of Sonic hedgehog that induces ventral neural tube development. Development 124, 2537-2552.
11. Livasy C.A., Karaca G., Nanda R., Tretiakova M.S., Olopade O.I., Moore D.T. and Perou C.M. (2006). Phenotypic evaluation of the basal-like subtype of invasive breast carcinoma. Mod. Pathol. 19, 264-271.
12. Ma X., Chen K., Huang S., Zhang X., Adegboyega P.A., Evers B.M., Zhang H. and Xie J. (2005). Frequent activation of the hedgehog pathway in advanced gastric adenocarcinomas. Carcinogenesis 26, 1698-1705.
13. Ma X., Sheng T., Zhang Y., Zhang X., He J., Huang S., Chen K., Sultz J., Adegboyega P.A., Zhang H. and Xie J. (2006). Hedgehog signaling is activated in subsets of esophageal cancers. Int. J. Cancer 118, 139-148.
14. Maeda Y., Davé V. and Whitsett J.A. (2007). Transcriptional control of lung morphogenesis. Physiol. Rev. 87, 219-244.
15. Mani S.A., Yang J., Brooks M., Schwaninger G., Zhou A., Miura N., Kutok J.L., Hartwell K., Richardson A.L. and Weinberg R.A. (2007). Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers. Proc. Natl. Acad. Sci. USA 104, 10069-10074.
16. Mimeault M. and Batra S.K. (2010). Frequent deregulations in the hedgehog signaling network and cross-talks with the epidermal growth factor receptor pathway involved in cancer progression and targeted therapies. Pharmacol. Rev. 62, 497-524.
17. Mori Y., Okumura T., Tsunoda S., Sakai Y. and Shimada Y. (2006). Gli-1 expression is associated with lymph node metastasis and tumor progression in esophageal squamous cell carcinoma. Oncology 70, 378-389.
18. Myatt S.S. and Lam E.W. (2007). The emerging roles of forkhead box (Fox) proteins in cancer. Nat. Rev. Cancer 7, 847-859.
19. Nielsen T.O., Hsu F.D., Jensen K., Cheang M., Karaca G., Hu Z., Hernandez-Boussard T., Livasy C., Cowan D., Dressler L., Akslen L.A., Ragaz J., Gown A.M., Gilks C.B., van de Rijn M. and Perou C.M. (2004). Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin. Cancer Res. 10, 5367-5374.
20. Parikh R.R., Housman D., Yang Q., Toppmeyer D., Wilson L.D. and Haffty B.G. (2008). Prognostic value of triple-negative phenotype at the time of locally recurrent, conservatively treated breast cancer. Int. J. Radiat. Oncol. Biol. Phys. 72, 1056-1063.
21. 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.
22. Ray P.S., Wang J., Qu Y., Sim M.S., Shamonki J.M., Bagaria S.P., Ye X., Liu B., Elashoff D., Hoon D.S., Walter M.A., Martens J.W., Richardson A.L., Giuliano A.E. and Cui X. (2010). FOXC1 is a potential prognostic biomarker with functional significance in basallike breast cancer. Cancer Res. 70, 3870-3876
23. Ray P.S., Bagaria S.P., Wang J., Shamonki J.M., Ye X., Sim M.S., Steen S., Qu Y., Cui X. and Giuliano A.E. (2011), Basal-like breast cancer defined by FOXC1 expression offers superior prognostic value: a retrospective immunochistochemical study. Ann. Surg. Oncol. (in press).
24. Sano H., Leboeuf J.P., Novitskiy S.V., Seo S., Zaja-Milatovic S., Dikov M.M. and Kume T. (2010). The Foxc2 transcription factor regulates tumor angiogenesis. Biochem. Biophys. Res. Commun. 392, 201-206.
25. 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., Lonning P.E., Brown P.O., Borresen-Dale A.L. and Botstein D. (2003). Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc. Natl. Acad. Sci. USA 100, 8418-8423.
26. Taube J.H., Herschkowitz J.I., Komurov K., Zhou A.Y., Gupta S., Yang J., Hartwell K., Onder T.T., Gupta P.B., Evans K.W., Hollier B.G., Ram P.T., Lander E.S., Rosen J.M., Weinberg R.A. and Mani SA. (2010) Core epithelial-to-mesenchymal transition interactome geneexpression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc. Natl. Acad. Sci. USA 107, 15449-15454.
27. Teh M.T., Wong S.T., Neill G.W., Ghali L.R., Philpott M.P. and Quinn A.G. (2002). FOXM1 is a downstream target of Gli1 in basal cell carcinomas. Cancer Res. 62, 4773-4780.
28. Ten Haaf A., Bektas N., von Serenyi S., Losen I., Arweiler E.C., Hartmann A., Knüchel R. and Dahl E. (2009). Expression of the glioma-associated oncogene homolog (GLI) 1 in human breast cancer is associated with unfavourable overall survival. BMC Cancer 9, 298.
29. Thayer S.P., di Magliano M.P., Heiser P.W., Nielsen C.M., Roberts D.J., Lauwers G.Y., Qi Y.P., Gysin S., Fernández-del Castillo C., Yajnik V., Antoniu B., McMahon M., Warshaw A.L. and Hebrok M. (2003). Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis. Nature 425, 851-856.
30. Watkins D.N., Berman D.M., Burkholder S.G., Wang B., Beachy P.A. and Baylin S.B. (2003). Hedgehog signalling within airway epithelial progenitors and in small-cell lung cancer. Nature 422, 313-317.
31. Xu L., Kwon Y.J., Frolova N., Steg A.D., Yuan K., Johnson M.R., Grizzle W.E., Desmond R.A. and Frost A.R. (2010). Gli1 promotes cell survival and is predictive of a poor outcome in ERalpha-negative breast cancer. Breast Cancer Res. Treat. 123, 59-71.
32. Yoo Y.A., Kang M.H., Kim J.S. and Oh S.C. (2008). Sonic hedgehog signaling promotes motility and invasiveness of gastric cancer cells through TGF-beta-mediated activation of the ALK5-Smad 3 pathway. Carcinogenesis 29, 480-490.
33. Yoon J.W., Kita Y., Frank D.J., Majewski R.R., Konicek B.A., Nobrega M.A., Jacob H., Walterhouse D., and Iannaccone P. (2002). Gene expression profiling leads to identification of GLI1-binding elements in target genes and a role for multiple downstream pathways in GLI1-induced cell transformation. J. Biol. Chem. 277, 5548-5555.
34. Zhao J., Chen G., Cao D., Li Y., Diao F., Cai H., Jin Y. and Lu J. (2010). Expression of Gli1 correlates with the transition of breast cancer cells to estrogen-independent growth. Breast Cancer Res. Treat. 119, 39-51.