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Erschienen in: Cancer and Metastasis Reviews 4/2022

14.06.2022 | Non-Thematic Review

Oncogenic functions of the FOXC2 transcription factor: a hallmarks of cancer perspective

verfasst von: Kristian M. Hargadon, Travis B. Goodloe III, Nathaniel D. Lloyd

Erschienen in: Cancer and Metastasis Reviews | Ausgabe 4/2022

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Abstract

Epigenetic regulation of gene expression is a fundamental determinant of molecular and cellular function, and epigenetic reprogramming in the context of cancer has emerged as one of the key enabling characteristics associated with acquisition of the core hallmarks of this disease. As such, there has been renewed interest in studying the role of transcription factors as epigenetic regulators of gene expression in cancer. In this review, we discuss the current state of knowledge surrounding the oncogenic functions of FOXC2, a transcription factor that frequently becomes dysregulated in a variety of cancer types. In addition to highlighting the clinical impact of aberrant FOXC2 activity in cancer, we discuss mechanisms by which this transcription factor becomes dysregulated in both tumor and tumor-associated cells, placing particular emphasis on the ways in which FOXC2 promotes key hallmarks of cancer progression. Finally, we bring attention to important issues related to the oncogenic dysregulation of FOXC2 that must be addressed going forward in order to improve our understanding of FOXC2-mediated cancer progression and to guide prognostic and therapeutic applications of this knowledge in clinical settings.
Literatur
2.
Zurück zum Zitat Xue, Y., Cao, R., Nilsson, D., Chen, S., Westergren, R., Hedlund, E. M., et al. (2008). FOXC2 controls Ang-2 expression and modulates angiogenesis, vascular patterning, remodeling, and functions in adipose tissue. Proceedings of the National Academy of Sciences of the United States of America, 105(29), 10167–10172. https://doi.org/10.1073/pnas.0802486105CrossRef Xue, Y., Cao, R., Nilsson, D., Chen, S., Westergren, R., Hedlund, E. M., et al. (2008). FOXC2 controls Ang-2 expression and modulates angiogenesis, vascular patterning, remodeling, and functions in adipose tissue. Proceedings of the National Academy of Sciences of the United States of America, 105(29), 10167–10172. https://​doi.​org/​10.​1073/​pnas.​0802486105CrossRef
8.
Zurück zum Zitat Grønning, L. M., Cederberg, A., Miura, N., Enerbäck, S., & Taskén, K. (2002). Insulin and TNF alpha induce expression of the forkhead transcription factor gene Foxc2 in 3T3-L1 adipocytes via PI3K and ERK 1/2-dependent pathways. Molecular Endocrinology, 16(4), 873–883. https://doi.org/10.1210/MEND.16.4.0803CrossRef Grønning, L. M., Cederberg, A., Miura, N., Enerbäck, S., & Taskén, K. (2002). Insulin and TNF alpha induce expression of the forkhead transcription factor gene Foxc2 in 3T3-L1 adipocytes via PI3K and ERK 1/2-dependent pathways. Molecular Endocrinology, 16(4), 873–883. https://​doi.​org/​10.​1210/​MEND.​16.​4.​0803CrossRef
9.
Zurück zum Zitat Paranjape, A. N., Soundararajan, R., Werden, S. J., Joseph, R., Taube, J. H., Liu, H., et al. (2016). Inhibition of FOXC2 restores epithelial phenotype and drug sensitivity in prostate cancer cells with stem-cell properties. Oncogene, 35(46), 5963–5976. https://doi.org/10.1038/onc.2015.498CrossRef Paranjape, A. N., Soundararajan, R., Werden, S. J., Joseph, R., Taube, J. H., Liu, H., et al. (2016). Inhibition of FOXC2 restores epithelial phenotype and drug sensitivity in prostate cancer cells with stem-cell properties. Oncogene, 35(46), 5963–5976. https://​doi.​org/​10.​1038/​onc.​2015.​498CrossRef
10.
Zurück zum Zitat Christofides, A., Papagregoriou, G., Dweep, H., Makrides, N., Gretz, N., Felekkis, K., & Deltas, C. (2020). Evidence for miR-548c-5p regulation of FOXC2 transcription through a distal genomic target site in human podocytes. Cellular and Molecular Life Sciences, 77(12), 2441–2459. https://doi.org/10.1007/S00018-019-03294-ZCrossRef Christofides, A., Papagregoriou, G., Dweep, H., Makrides, N., Gretz, N., Felekkis, K., & Deltas, C. (2020). Evidence for miR-548c-5p regulation of FOXC2 transcription through a distal genomic target site in human podocytes. Cellular and Molecular Life Sciences, 77(12), 2441–2459. https://​doi.​org/​10.​1007/​S00018-019-03294-ZCrossRef
19.
27.
Zurück zum Zitat Werden, S. J., Sphyris, N., Sarkar, T. R., Paranjape, A. N., LaBaff, A. M., Taube, J. H., et al. (2016). Phosphorylation of serine 367 of FOXC2 by p38 regulates ZEB1 and breast cancer metastasis, without impacting primary tumor growth. Oncogene, 35(46), 5977–5988. https://doi.org/10.1038/onc.2016.203CrossRef Werden, S. J., Sphyris, N., Sarkar, T. R., Paranjape, A. N., LaBaff, A. M., Taube, J. H., et al. (2016). Phosphorylation of serine 367 of FOXC2 by p38 regulates ZEB1 and breast cancer metastasis, without impacting primary tumor growth. Oncogene, 35(46), 5977–5988. https://​doi.​org/​10.​1038/​onc.​2016.​203CrossRef
28.
Zurück zum Zitat Danciu, T. E., Chupreta, S., Cruz, O., Fox, J. E., Whitman, M., & Iñiguez-Lluhí, J. A. (2012). Small ubiquitin-like modifier (SUMO) modification mediates function of the inhibitory domains of developmental regulators FOXC1 and FOXC2. The Journal of Biological Chemistry, 287(22), 18318–18329. https://doi.org/10.1074/JBC.M112.339424CrossRef Danciu, T. E., Chupreta, S., Cruz, O., Fox, J. E., Whitman, M., & Iñiguez-Lluhí, J. A. (2012). Small ubiquitin-like modifier (SUMO) modification mediates function of the inhibitory domains of developmental regulators FOXC1 and FOXC2. The Journal of Biological Chemistry, 287(22), 18318–18329. https://​doi.​org/​10.​1074/​JBC.​M112.​339424CrossRef
30.
31.
33.
Zurück zum Zitat Li, Y., Yang, W., Yang, Q., & Zhou, S. (2012). Nuclear localization of GLI1 and elevated expression of FOXC2 in breast cancer is associated with the basal-like phenotype. Histology and Histopathology, 27(4), 475–84. https://doi.org/10.14670/HH-27.475 Li, Y., Yang, W., Yang, Q., & Zhou, S. (2012). Nuclear localization of GLI1 and elevated expression of FOXC2 in breast cancer is associated with the basal-like phenotype. Histology and Histopathology, 27(4), 475–84. https://​doi.​org/​10.​14670/​HH-27.​475
34.
Zurück zum Zitat Li, Q., Wu, J., Wei, P., Xu, Y., Zhuo, C., Wang, Y., et al. (2015). Overexpression of forkhead Box C2 promotes tumor metastasis and indicates poor prognosis in colon cancer via regulating epithelial-mesenchymal transition. American Journal of Cancer Research, 5(6), 2022–34. http://www.ncbi.nlm.nih.gov/pubmed/26269761 Li, Q., Wu, J., Wei, P., Xu, Y., Zhuo, C., Wang, Y., et al. (2015). Overexpression of forkhead Box C2 promotes tumor metastasis and indicates poor prognosis in colon cancer via regulating epithelial-mesenchymal transition. American Journal of Cancer Research, 5(6), 2022–34. http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​26269761
36.
37.
Zurück zum Zitat Børretzen, A., Gravdal, K., Haukaas, S. A., Beisland, C., Akslen, L. A., & Halvorsen, O. J. (2019). FOXC2 expression and epithelial–mesenchymal phenotypes are associated with castration resistance, metastasis and survival in prostate cancer. The Journal of Pathology: Clinical Research, 5(4), 272–286. https://doi.org/10.1002/cjp2.142CrossRef Børretzen, A., Gravdal, K., Haukaas, S. A., Beisland, C., Akslen, L. A., & Halvorsen, O. J. (2019). FOXC2 expression and epithelial–mesenchymal phenotypes are associated with castration resistance, metastasis and survival in prostate cancer. The Journal of Pathology: Clinical Research, 5(4), 272–286. https://​doi.​org/​10.​1002/​cjp2.​142CrossRef
43.
Zurück zum Zitat Hargadon, K. M., Györffy, B., Strong, E. W., Tarnai, B. D., Thompson, J. C., Bushhouse, D. Z., et al. (2019). The FOXC2 transcription factor promotes melanoma outgrowth and regulates expression of genes associated with drug resistance and interferon responsiveness. Cancer Genomics & Proteomics, 16(6), 491–503. https://doi.org/10.21873/cgp.20152 Hargadon, K. M., Györffy, B., Strong, E. W., Tarnai, B. D., Thompson, J. C., Bushhouse, D. Z., et al. (2019). The FOXC2 transcription factor promotes melanoma outgrowth and regulates expression of genes associated with drug resistance and interferon responsiveness. Cancer Genomics & Proteomics, 16(6), 491–503. https://​doi.​org/​10.​21873/​cgp.​20152
45.
Zurück zum Zitat Xu, D. F., Tao, X. H., Yu, Y., Teng, Y., Huang, Y. M., Ma, J. W., & Fan, Y. B. (2020). LncRNA FOXC2-AS1 stimulates proliferation of melanoma via silencing p15 by recruiting EZH2. European Review for Medical and Pharmacological Sciences, 24(17), 8940–8946. https://doi.org/10.26355/EURREV_202009_22835 Xu, D. F., Tao, X. H., Yu, Y., Teng, Y., Huang, Y. M., Ma, J. W., & Fan, Y. B. (2020). LncRNA FOXC2-AS1 stimulates proliferation of melanoma via silencing p15 by recruiting EZH2. European Review for Medical and Pharmacological Sciences, 24(17), 8940–8946. https://​doi.​org/​10.​26355/​EURREV_​202009_​22835
49.
Zurück zum Zitat Pan, J., Yang, Q., Shao, J., Zhang, L., Ma, J., Wang, Y., et al. (2016). Cyclooxygenase-2 induced β1-integrin expression in NSCLC and promoted cell invasion via the EP1/MAPK/E2F-1/FoxC2 signal pathway. Scientific Reports, 6, 33823. https://doi.org/10.1038/srep33823CrossRef Pan, J., Yang, Q., Shao, J., Zhang, L., Ma, J., Wang, Y., et al. (2016). Cyclooxygenase-2 induced β1-integrin expression in NSCLC and promoted cell invasion via the EP1/MAPK/E2F-1/FoxC2 signal pathway. Scientific Reports, 6, 33823. https://​doi.​org/​10.​1038/​srep33823CrossRef
50.
Zurück zum Zitat Shibue, T., & Weinberg, R. A. (2009). Integrin beta1-focal adhesion kinase signaling directs the proliferation of metastatic cancer cells disseminated in the lungs. Proceedings of the National Academy of Sciences of the United States of America, 106(25), 10290–10295. https://doi.org/10.1073/PNAS.0904227106CrossRef Shibue, T., & Weinberg, R. A. (2009). Integrin beta1-focal adhesion kinase signaling directs the proliferation of metastatic cancer cells disseminated in the lungs. Proceedings of the National Academy of Sciences of the United States of America, 106(25), 10290–10295. https://​doi.​org/​10.​1073/​PNAS.​0904227106CrossRef
56.
Zurück zum Zitat Li, C., Ding, H., Tian, J., Wu, L., Wang, Y., Xing, Y., & Chen, M. (2016). Forkhead box protein C2 (FOXC2) promotes the resistance of human ovarian cancer cells to cisplatin in vitro and in vivo. Cellular Physiology and Biochemistry, 39(1), 242–252. https://doi.org/10.1159/000445620CrossRef Li, C., Ding, H., Tian, J., Wu, L., Wang, Y., Xing, Y., & Chen, M. (2016). Forkhead box protein C2 (FOXC2) promotes the resistance of human ovarian cancer cells to cisplatin in vitro and in vivo. Cellular Physiology and Biochemistry, 39(1), 242–252. https://​doi.​org/​10.​1159/​000445620CrossRef
60.
Zurück zum Zitat Mani, S. A., Yang, J., Brooks, M., Schwaninger, G., Zhou, A., Miura, N., A., et al. (2007). Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers. Proceedings of the National Academy of Sciences of the United States of America, 104(24), 10069–10074. https://doi.org/10.1073/pnas.0703900104CrossRef Mani, S. A., Yang, J., Brooks, M., Schwaninger, G., Zhou, A., Miura, N., A., et al. (2007). Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers. Proceedings of the National Academy of Sciences of the United States of America, 104(24), 10069–10074. https://​doi.​org/​10.​1073/​pnas.​0703900104CrossRef
61.
Zurück zum Zitat Li, C., Ding, H., Tian, J., Wu, L., Wang, Y., Xing, Y., & Chen, M. (2016). Forkhead box protein C2 promotes epithelial-mesenchymal transition, migration and invasion in cisplatin-resistant human ovarian cancer cell line (SKOV3/CDDP). Cellular Physiology and Biochemistry, 39(3), 1098–1110. https://doi.org/10.1159/000447818CrossRef Li, C., Ding, H., Tian, J., Wu, L., Wang, Y., Xing, Y., & Chen, M. (2016). Forkhead box protein C2 promotes epithelial-mesenchymal transition, migration and invasion in cisplatin-resistant human ovarian cancer cell line (SKOV3/CDDP). Cellular Physiology and Biochemistry, 39(3), 1098–1110. https://​doi.​org/​10.​1159/​000447818CrossRef
66.
70.
Zurück zum Zitat Watanabe, A., Suzuki, H., Yokobori, T., Altan, B., Kubo, N., Araki, K., et al. (2013). Forkhead box protein C2 contributes to invasion and metastasis of extrahepatic cholangiocarcinoma, resulting in a poor prognosis. Cancer Science, 104(11), 1427–1432. https://doi.org/10.1111/CAS.12249CrossRef Watanabe, A., Suzuki, H., Yokobori, T., Altan, B., Kubo, N., Araki, K., et al. (2013). Forkhead box protein C2 contributes to invasion and metastasis of extrahepatic cholangiocarcinoma, resulting in a poor prognosis. Cancer Science, 104(11), 1427–1432. https://​doi.​org/​10.​1111/​CAS.​12249CrossRef
78.
Zurück zum Zitat Lin, Y., Mckinnon, K. E., Ha, S. W., & Beck, G. R. (2015). Inorganic phosphate induces cancer cell mediated angiogenesis dependent on forkhead box protein C2 (FOXC2) regulated osteopontin expression. Molecular Carcinogenesis, 54(9), 926–934. https://doi.org/10.1002/MC.22153CrossRef Lin, Y., Mckinnon, K. E., Ha, S. W., & Beck, G. R. (2015). Inorganic phosphate induces cancer cell mediated angiogenesis dependent on forkhead box protein C2 (FOXC2) regulated osteopontin expression. Molecular Carcinogenesis, 54(9), 926–934. https://​doi.​org/​10.​1002/​MC.​22153CrossRef
85.
Zurück zum Zitat Xia, S., Menden, H. L., Korfhagen, T. R., Kume, T., & Sampath, V. (2018). Endothelial immune activation programmes cell-fate decisions and angiogenesis by inducing angiogenesis regulator DLL4 through TLR4-ERK-FOXC2 signalling. The Journal of Physiology, 596(8), 1397–1417. https://doi.org/10.1113/JP275453CrossRef Xia, S., Menden, H. L., Korfhagen, T. R., Kume, T., & Sampath, V. (2018). Endothelial immune activation programmes cell-fate decisions and angiogenesis by inducing angiogenesis regulator DLL4 through TLR4-ERK-FOXC2 signalling. The Journal of Physiology, 596(8), 1397–1417. https://​doi.​org/​10.​1113/​JP275453CrossRef
88.
Zurück zum Zitat Sphyris, N., King, C., Hoar, J., Werden, S. J., Vijay, G. V., Miura, N., et al. (2021). Carcinoma cells that have undergone an epithelial-mesenchymal transition differentiate into endothelial cells and contribute to tumor growth. Oncotarget, 12(8), 823–844. https://doi.org/10.18632/ONCOTARGET.27940 Sphyris, N., King, C., Hoar, J., Werden, S. J., Vijay, G. V., Miura, N., et al. (2021). Carcinoma cells that have undergone an epithelial-mesenchymal transition differentiate into endothelial cells and contribute to tumor growth. Oncotarget, 12(8), 823–844. https://​doi.​org/​10.​18632/​ONCOTARGET.​27940
91.
Zurück zum Zitat Fang, J., Dagenais, S. L., Erickson, R. P., Arlt, M. F., Glynn, M. W., Gorski, J. L., et al. (2000). Mutations in FOXC2 (MFH-1), a forkhead family transcription factor, are responsible for the hereditary lymphedema-distichiasis syndrome. American Journal of Human Genetics, 67(6), 1382–1388. https://doi.org/10.1086/316915CrossRef Fang, J., Dagenais, S. L., Erickson, R. P., Arlt, M. F., Glynn, M. W., Gorski, J. L., et al. (2000). Mutations in FOXC2 (MFH-1), a forkhead family transcription factor, are responsible for the hereditary lymphedema-distichiasis syndrome. American Journal of Human Genetics, 67(6), 1382–1388. https://​doi.​org/​10.​1086/​316915CrossRef
92.
Zurück zum Zitat Tavian, D., Missaglia, S., Maltese, P. E., Michelini, S., Fiorentino, A., Ricci, M., et al. (2016). FOXC2 disease-mutations identified in lymphedema-distichiasis patients cause both loss and gain of protein function. Oncotarget, 7(34), 54228–54239. https://doi.org/10.18632/ONCOTARGET.9797 Tavian, D., Missaglia, S., Maltese, P. E., Michelini, S., Fiorentino, A., Ricci, M., et al. (2016). FOXC2 disease-mutations identified in lymphedema-distichiasis patients cause both loss and gain of protein function. Oncotarget, 7(34), 54228–54239. https://​doi.​org/​10.​18632/​ONCOTARGET.​9797
93.
Zurück zum Zitat González-Loyola, A., Bovay, E., Kim, J., Lozano, T. W., Sabine, A., Renevey, F., et al. (2021). FOXC2 controls adult lymphatic endothelial specialization, function, and gut lymphatic barrier preventing multiorgan failure. Science Advances, 7(29), eabf4335. https://doi.org/10.1126/SCIADV.ABF4335 González-Loyola, A., Bovay, E., Kim, J., Lozano, T. W., Sabine, A., Renevey, F., et al. (2021). FOXC2 controls adult lymphatic endothelial specialization, function, and gut lymphatic barrier preventing multiorgan failure. Science Advances, 7(29), eabf4335. https://​doi.​org/​10.​1126/​SCIADV.​ABF4335
96.
Zurück zum Zitat Fatima, A., Wang, Y., Uchida, Y., Norden, P., Liu, T., Culver, A., et al. (2016). Foxc1 and Foxc2 deletion causes abnormal lymphangiogenesis and correlates with ERK hyperactivation. The Journal of Clinical Investigation, 126(7), 2437–2451. https://doi.org/10.1172/JCI80465CrossRef Fatima, A., Wang, Y., Uchida, Y., Norden, P., Liu, T., Culver, A., et al. (2016). Foxc1 and Foxc2 deletion causes abnormal lymphangiogenesis and correlates with ERK hyperactivation. The Journal of Clinical Investigation, 126(7), 2437–2451. https://​doi.​org/​10.​1172/​JCI80465CrossRef
97.
105.
Zurück zum Zitat Peng, Y. H., Wang, P., He, X. Q., Hong, M. Z., & Liu, F. (2022). Micro ribonucleic acid-363 regulates the phosphatidylinositol 3-kinase/threonine protein kinase axis by targeting NOTCH1 and forkhead box C2, leading to hepatic glucose and lipids metabolism disorder in type 2 diabetes mellitus. Journal of Diabetes Investigation, 13(2), 236–248. https://doi.org/10.1111/JDI.13695CrossRef Peng, Y. H., Wang, P., He, X. Q., Hong, M. Z., & Liu, F. (2022). Micro ribonucleic acid-363 regulates the phosphatidylinositol 3-kinase/threonine protein kinase axis by targeting NOTCH1 and forkhead box C2, leading to hepatic glucose and lipids metabolism disorder in type 2 diabetes mellitus. Journal of Diabetes Investigation, 13(2), 236–248. https://​doi.​org/​10.​1111/​JDI.​13695CrossRef
106.
Zurück zum Zitat Lidell, M. E., Seifert, E. L., Westergren, R., Heglind, M., Gowing, A., Sukonina, V., et al. (2011). The adipocyte-expressed forkhead transcription factor Foxc2 regulates metabolism through altered mitochondrial function. Diabetes, 60(2), 427–435. https://doi.org/10.2337/DB10-0409CrossRef Lidell, M. E., Seifert, E. L., Westergren, R., Heglind, M., Gowing, A., Sukonina, V., et al. (2011). The adipocyte-expressed forkhead transcription factor Foxc2 regulates metabolism through altered mitochondrial function. Diabetes, 60(2), 427–435. https://​doi.​org/​10.​2337/​DB10-0409CrossRef
107.
111.
Zurück zum Zitat Ramirez-Peña, E., Arnold, J., Shivakumar, V., Joseph, R., Vidhya Vijay, G., den Hollander, P., … Mani, S. A. (2019). The epithelial to mesenchymal transition promotes glutamine independence by suppressing GLS2 expression. Cancers, 11(10), 1610. https://doi.org/10.3390/cancers11101610 Ramirez-Peña, E., Arnold, J., Shivakumar, V., Joseph, R., Vidhya Vijay, G., den Hollander, P., … Mani, S. A. (2019). The epithelial to mesenchymal transition promotes glutamine independence by suppressing GLS2 expression. Cancers, 11(10), 1610. https://​doi.​org/​10.​3390/​cancers11101610
112.
Zurück zum Zitat Liu, M., Zhong, J., Zeng, Z., Huang, K., Ye, Z., Deng, S., et al. (2019). Hypoxia-induced feedback of HIF-1α and lncRNA-CF129 contributes to pancreatic cancer progression through stabilization of p53 protein. Theranostics, 9(16), 4795–4810. https://doi.org/10.7150/THNO.30988CrossRef Liu, M., Zhong, J., Zeng, Z., Huang, K., Ye, Z., Deng, S., et al. (2019). Hypoxia-induced feedback of HIF-1α and lncRNA-CF129 contributes to pancreatic cancer progression through stabilization of p53 protein. Theranostics, 9(16), 4795–4810. https://​doi.​org/​10.​7150/​THNO.​30988CrossRef
116.
Zurück zum Zitat Hargadon, K. M., & Williams, C. J. (2020). RNA-seq analysis of wild-type vs. FOXC2-deficient melanoma cells reveals a role for the FOXC2 transcription factor in the regulation of multiple oncogenic pathways. Frontiers in Oncology, 10, 267. https://doi.org/10.3389/fonc.2020.00267 Hargadon, K. M., & Williams, C. J. (2020). RNA-seq analysis of wild-type vs. FOXC2-deficient melanoma cells reveals a role for the FOXC2 transcription factor in the regulation of multiple oncogenic pathways. Frontiers in Oncology, 10, 267. https://​doi.​org/​10.​3389/​fonc.​2020.​00267
121.
122.
128.
Zurück zum Zitat Imayama, N., Yamada, S.-I., Yanamoto, S., Naruse, T., Matsushita, Y., Takahashi, H., et al. (2015). FOXC2 expression is associated with tumor proliferation and invasion potential in oral tongue squamous cell carcinoma. Pathology Oncology Research, 21(3), 783–791. https://doi.org/10.1007/s12253-014-9891-6CrossRef Imayama, N., Yamada, S.-I., Yanamoto, S., Naruse, T., Matsushita, Y., Takahashi, H., et al. (2015). FOXC2 expression is associated with tumor proliferation and invasion potential in oral tongue squamous cell carcinoma. Pathology Oncology Research, 21(3), 783–791. https://​doi.​org/​10.​1007/​s12253-014-9891-6CrossRef
132.
133.
Zurück zum Zitat Zhu, Q., Tang, M., & Wu, L. (2020). Expression of combined interference of slug and FoxC2 in endometrial carcinoma and its clinicopathological relationship. Translational Cancer Research, 9(9), 5268–5280. https://doi.org/10.21037/TCR-20-809 Zhu, Q., Tang, M., & Wu, L. (2020). Expression of combined interference of slug and FoxC2 in endometrial carcinoma and its clinicopathological relationship. Translational Cancer Research, 9(9), 5268–5280. https://​doi.​org/​10.​21037/​TCR-20-809
Metadaten
Titel
Oncogenic functions of the FOXC2 transcription factor: a hallmarks of cancer perspective
verfasst von
Kristian M. Hargadon
Travis B. Goodloe III
Nathaniel D. Lloyd
Publikationsdatum
14.06.2022
Verlag
Springer US
Erschienen in
Cancer and Metastasis Reviews / Ausgabe 4/2022
Print ISSN: 0167-7659
Elektronische ISSN: 1573-7233
DOI
https://doi.org/10.1007/s10555-022-10045-3

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