FOXM1: A key oncofoetal transcription factor in health and disease

Seminars in Cancer Biology

Volumn 29, Issue C, 2014, Pages 32-39

  Bella, Laura ^a   Zona, Stefania ^a   Nestal de Moraes, Gabriela ^a   Lam, Eric W F ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Cancer; Development; FOXM1; Oncofoetal protein; Transcription factor

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXM1; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; FOXM1 PROTEIN, HUMAN; ONCOFETAL ANTIGENS; TUMOR ANTIGEN;

ANGIOGENESIS; CANCER DIAGNOSIS; CANCER THERAPY; CARCINOGENESIS; CELL AGING; CELL INVASION; CELL MIGRATION; CELL RENEWAL; CONGENITAL DISORDER; DEVELOPMENTAL DISORDER; DNA REPAIR; EMBRYO DEVELOPMENT; EMBRYO GROWTH; FETUS DEVELOPMENT; FETUS GROWTH; GENE ACTIVITY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HEALTH STATUS; HOMEOSTASIS; HUMAN; METASTASIS; NEOPLASM; NONHUMAN; REVIEW; STEM CELL; TISSUE REPAIR; TUMOR GROWTH; TUMOR RESISTANCE; UPREGULATION; BIOSYNTHESIS; CANCER STEM CELL; CELL MOTION; CELL PROLIFERATION; CELL TRANSFORMATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GENETICS; NEOVASCULARIZATION (PATHOLOGY); TRANSCRIPTION INITIATION;

ANTIGENS, NEOPLASM; CELL AGING; CELL MOVEMENT; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DNA REPAIR; EPITHELIAL-MESENCHYMAL TRANSITION; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASMS; NEOPLASTIC STEM CELLS; NEOVASCULARIZATION, PATHOLOGIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84927575175     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2014.07.008     Document Type: Review

References (79)

1. Gordeeva O.F. Normal and pathological development of pluripotent stem cells. J Stem cells 2011, 6:129-154.
2. Chan Y.S., Yang L., Ng H.H. Transcriptional regulatory networks in embryonic stem cells. Prog Drug Res 2011, 67:239-252.
3. Lam E.W., Brosens J.J., Gomes A.R., Koo C.Y. Forkhead box proteins: tuning forks for transcriptional harmony. Nat Rev Cancer 2013, 13:482-495.
4. Li Q., Zhang N., Jia Z., Le X., Dai B., Wei D., et al. Critical role and regulation of transcription factor FoxM1 in human gastric cancer angiogenesis and progression. Cancer Res 2009, 69:3501-3509.
5. Koo C.Y., Muir K.W., Lam E.W. FOXM1: from cancer initiation to progression and treatment. Biochim Biophys Acta 2012, 1819:28-37.
6. Ye H., Kelly T.F., Samadani U., Lim L., Rubio S., Overdier D.G., et al. Hepatocyte nuclear factor 3/fork head homolog 11 is expressed in proliferating epithelial and mesenchymal cells of embryonic and adult tissues. Mol Cell Biol 1997, 17:1626-1641.
7. Zhao Y.D., Huang X., Yi F., Dai Z., Qian Z., Tiruppathi C., et al. Endothelial FoxM1 mediates bone marrow progenitor cell-induced vascular repair and resolution of inflammation following inflammatory lung injury. Stem Cells 2014, 10.1002/stem.690.
8. Ye H., Holterman A.X., Yoo K.W., Franks R.R., Costa R.H. Premature expression of the winged helix transcription factor HFH-11B in regenerating mouse liver accelerates hepatocyte entry into S phase. Mol Cell Biol 1999, 19:8570-8580.
9. Zhang S., Teng H., Ding Q., Fan J., Shi W., Zhou Y., et al. FoxM1 involvement in astrocyte proliferation after spinal cord injury in rats. J Mol Neurosci 2013, 51:170-179.
10. Bolte C., Zhang Y., York A., Kalin T.V., Schultz Jel J., Molkentin J.D., et al. Postnatal ablation of Foxm1 from cardiomyocytes causes late onset cardiac hypertrophy and fibrosis without exacerbating pressure overload-induced cardiac remodeling. PLoS ONE 2012, 7:e48713.
11. Wang I.C., Zhang Y., Snyder J., Sutherland M.J., Burhans M.S., Shannon J.M., et al. Increased expression of FoxM1 transcription factor in respiratory epithelium inhibits lung sacculation and causes Clara cell hyperplasia. Dev Biol 2010, 347:301-314.
12. Wang Z., Ahmad A., Li Y., Banerjee S., Kong D., Sarkar F.H. Forkhead box M1 transcription factor: a novel target for cancer therapy. Cancer Treat Rev 2010, 36:151-156.
13. Karadedou C.T., Gomes A.R., Chen J., Petkovic M., Ho K.K., Zwolinska A.K., et al. FOXO3a represses VEGF expression through FOXM1-dependent and -independent mechanisms in breast cancer. Oncogene 2012, 31:1845-1858.
14. McGovern U.B., Francis R.E., Peck B., Guest S.K., Wang J., Myatt S.S., et al. Gefitinib (Iressa) represses FOXM1 expression via FOXO3a in breast cancer. Mol Cancer Ther 2009, 8:582-591.
15. Krol J., Francis R.E., Albergaria A., Sunters A., Polychronis A., Coombes R.C., et al. The transcription factor FOXO3a is a crucial cellular target of gefitinib (Iressa) in breast cancer cells. Mol Cancer Ther 2007, 6:3169-3179.
16. Millour J., Constantinidou D., Stavropoulou A.V., Wilson M.S., Myatt S.S., Kwok J.M., et al. FOXM1 is a transcriptional target of ERalpha and has a critical role in breast cancer endocrine sensitivity and resistance. Oncogene 2010, 29:2983-2995.
17. Madureira P.A., Varshochi R., Constantinidou D., Francis R.E., Coombes R.C., Yao K.M., et al. The Forkhead box M1 protein regulates the transcription of the estrogen receptor alpha in breast cancer cells. J Biol Chem 2006, 281:25167-25176.
18. Geng S., Wang X., Xu X., Zhang H., Ma Y., Zhang Y., et al. Steroid receptor co-activator-3 promotes osteosarcoma progression through up-regulation of FoxM1. Tumour Biol 2014, 35:3087-3094.
19. Millour J., de Olano N., Horimoto Y., Monteiro L.J., Langer J.K., Aligue R., et al. ATM and p53 regulate FOXM1 expression via E2F in breast cancer epirubicin treatment and resistance. Mol Cancer Ther 2011, 10:1046-1058.
20. Moschetta M., Mishima Y., Sahin I., Manier S., Glavey S., Vacca A., et al. Role of endothelial progenitor cells in cancer progression. Biochim Biophys Acta 2014, 10.1016/j.bbcan.2014.03.005.
21. Murohara T. Cord blood-derived early outgrowth endothelial progenitor cells. Microvasc Res 2010, 79:174-177.
22. Sood A.K., Fletcher M.S., Hendrix M.J. The embryonic-like properties of aggressive human tumor cells. J Soc Gynecol Investig 2002, 9:2-9.
23. Kim I.M., Ramakrishna S., Gusarova G.A., Yoder H.M., Costa R.H., Kalinichenko V.V. The Forkhead Box M1 transcription factor is essential for embryonic development of pulmonary vasculature. J Biol Chem 2005, 280:22278-22286.
24. Lohela M., Bry M., Tammela T., Alitalo K. VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr Opin Cell Biol 2009, 21:154-165.
25. Vaswani K., Hum M.W., Chan H.W., Ryan J., Wood-Bradley R.J., Nitert M.D., et al. The effect of gestational age on angiogenic gene expression in the rat placenta. PLOS ONE 2013, 8:e83762.
26. McDougall S.R., Anderson A.R., Chaplain M.A. Mathematical modelling of dynamic adaptive tumour-induced angiogenesis: clinical implications and therapeutic targeting strategies. J Theor Biol 2006, 241:564-589.
27. McDonald D.M., Baluk P. Significance of blood vessel leakiness in cancer. Cancer Res 2002, 62:5381-5385.
28. Capp C., Wajner S.M., Siqueira D.R., Brasil B.A., Meurer L., Maia A.L. Increased expression of vascular endothelial growth factor and its receptors, VEGFR-1 and VEGFR-2, in medullary thyroid carcinoma. Thyroid 2010, 20:863-871.
29. Wang Z., Banerjee S., Kong D., Li Y., Sarkar F.H. Down-regulation of Forkhead Box M1 transcription factor leads to the inhibition of invasion and angiogenesis of pancreatic cancer cells. Cancer Res 2007, 67:8293-8300.
30. Ahmad A., Wang Z., Kong D., Ali S., Li Y., Banerjee S., et al. FoxM1 down-regulation leads to inhibition of proliferation, migration and invasion of breast cancer cells through the modulation of extra-cellular matrix degrading factors. Breast Cancer Res Treat 2010, 122:337-346.
31. Cheng S.X., Tu Y., Zhang S. FoxM1 promotes glioma cells progression by up-regulating Anxa1 expression. PLOS ONE 2013, 8:e72376.
32. Dawe G.S., Tan X.W., Xiao Z.C. Cell migration from baby to mother. Cell Adh Migr 2007, 1:19-27.
33. Zeng Z.S., Cohen A.M., Guillem J.G. Loss of basement membrane type IV collagen is associated with increased expression of metalloproteinases 2 and 9 (MMP-2 and MMP-9) during human colorectal tumorigenesis. Carcinogenesis 1999, 20:749-755.
34. Wang X., Bhattacharyya D., Dennewitz M.B., Kalinichenko V.V., Zhou Y., Lepe R., et al. Rapid hepatocyte nuclear translocation of the Forkhead Box M1B (FoxM1B) transcription factor caused a transient increase in size of regenerating transgenic hepatocytes. Gene Expr 2003, 11:149-162.
35. Chen P.M., Wu T.C., Shieh S.H., Wu Y.H., Li M.C., Sheu G.T., et al. MnSOD promotes tumor invasion via upregulation of FoxM1-MMP2 axis and related with poor survival and relapse in lung adenocarcinomas. Mol Cancer Res 2013, 11:261-271.
36. Dai B., Kang S.H., Gong W., Liu M., Aldape K.D., Sawaya R., et al. Aberrant FoxM1B expression increases matrix metalloproteinase-2 transcription and enhances the invasion of glioma cells. Oncogene 2007, 26:6212-6219.
37. Chetty C., Bhoopathi P., Rao J.S., Lakka S.S. Inhibition of matrix metalloproteinase-2 enhances radiosensitivity by abrogating radiation-induced FoxM1-mediated G2/M arrest in A549 lung cancer cells. Int J Cancer 2009, 124:2468-2477.
38. Xu N., Jia D., Chen W., Wang H., Liu F., Ge H., et al. FoxM1 is associated with poor prognosis of non-small cell lung cancer patients through promoting tumor metastasis. PLOS ONE 2013, 8:e59412.
39. Wang I.C., Chen Y.J., Hughes D.E., Ackerson T., Major M.L., Kalinichenko V.V., et al. FoxM1 regulates transcription of JNK1 to promote the G1/S transition and tumor cell invasiveness. J Biol Chem 2008, 283:20770-20778.
40. Huang C., Xie D., Cui J., Li Q., Gao Y., Xie K. FOXM1c promotes pancreatic cancer epithelial-to-mesenchymal transition and metastasis via upregulation of expression of the urokinase plasminogen activator system. Clin Cancer Res 2014, 20:1477-1488.
41. Huang C., Qiu Z., Wang L., Peng Z., Jia Z., Logsdon C.D., et al. A novel FoxM1-caveolin signaling pathway promotes pancreatic cancer invasion and metastasis. Cancer Res 2012, 72:655-665.
42. Xia L., Huang W., Tian D., Chen Z., Zhang L., Li Y., et al. ACP5, a direct transcriptional target of FoxM1, promotes tumor metastasis and indicates poor prognosis in hepatocellular carcinoma. Oncogene 2014, 33:1395-1406.
43. Salhia B., Kiefer J., Ross J.T., Metapally R., Martinez R.A., Johnson K.N., et al. Integrated genomic and epigenomic analysis of breast cancer brain metastasis. PLOS ONE 2014, 9:e85448.
44. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
45. Sarrio D., Rodriguez-Pinilla S.M., Hardisson D., Cano A., Moreno-Bueno G., Palacios J. Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res 2008, 68:989-997.
46. Kong F.F., Qu Z.Q., Yuan H.H., Wang J.Y., Zhao M., Guo Y.H., et al. Overexpression of FOXM1 is associated with EMT and is a predictor of poor prognosis in non-small cell lung cancer. Oncol Rep 2014, 10.3892/or.2014.3129.
47. Bao B., Wang Z., Ali S., Kong D., Banerjee S., Ahmad A., et al. Over-expression of FoxM1 leads to epithelial-mesenchymal transition and cancer stem cell phenotype in pancreatic cancer cells. J Cell Biochem 2011, 112:2296-2306.
48. Ke Y., Zhao W., Xiong J., Cao R. miR-149 inhibits non-small-cell lung cancer cells EMT by targeting FOXM1. Biochem Res Int 2013, 2013:506731.
49. Li J., Wang Y., Luo J., Fu Z., Ying J., Yu Y., et al. miR-134 inhibits epithelial to mesenchymal transition by targeting FOXM1 in non-small cell lung cancer cells. FEBS Lett 2012, 586:3761-3765.
50. Yang C., Chen H., Tan G., Gao W., Cheng L., Jiang X., et al. FOXM1 promotes the epithelial to mesenchymal transition by stimulating the transcription of Slug in human breast cancer. Cancer Lett 2013, 340:104-112.
51. Levi B.P., Morrison S.J. Stem cells use distinct self-renewal programs at different ages. Cold Spring Harb Symp Quant Biol 2008, 73:539-553.
52. Mani S.A., Guo W., Liao M.J., Eaton E.N., Ayyanan A., Zhou A.Y., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
53. Gemenetzidis E., Elena-Costea D., Parkinson E.K., Waseem A., Wan H., Teh M.T. Induction of human epithelial stem/progenitor expansion by FOXM1. Cancer Res 2010, 70:9515-9526.
54. Xie Z., Tan G., Ding M., Dong D., Chen T., Meng X., et al. Foxm1 transcription factor is required for maintenance of pluripotency of P19 embryonal carcinoma cells. Nucleic Acids Res 2010, 38:8027-8038.
55. Wang I.C., Ustiyan V., Zhang Y., Cai Y., Kalin T.V., Kalinichenko V.V. Foxm1 transcription factor is required for the initiation of lung tumorigenesis by oncogenic Kras. Oncogene 2013, [Epub ahead of print]. 10.1038/onc.2013.475.
56. Moumen M., Chiche A., Decraene C., Petit V., Gandarillas A., Deugnier M.A., et al. Myc is required for beta-catenin-mediated mammary stem cell amplification and tumorigenesis. Mol Cancer 2013, 12:132.
57. Moumen M., Chiche A., Deugnier M.A., Petit V., Gandarillas A., Glukhova M.A., et al. The proto-oncogene Myc is essential for mammary stem cell function. Stem Cells 2012, 30:1246-1254.
58. Wang I.C., Snyder J., Zhang Y., Lander J., Nakafuku Y., Lin J., et al. Foxm1 mediates cross talk between Kras/mitogen-activated protein kinase and canonical Wnt pathways during development of respiratory epithelium. Mol Cell Biol 2012, 32:3838-3850.
59. Park I.H., Zhao R., West J.A., Yabuuchi A., Huo H., Ince T.A., et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 2008, 451:141-146.
60. Schwarz B.A., Bar-Nur O., Silva J.C., Hochedlinger K. Nanog is dispensable for the generation of induced pluripotent stem cells. Curr Biol 2014, 24:347-350.
61. Delpuech O., Griffiths B., East P., Essafi A., Lam E.W., Burgering B., et al. Induction of Mxi1-SR alpha by FOXO3a contributes to repression of Myc-dependent gene expression. Mol Cell Biol 2007, 27:4917-4930.
62. Quan M., Wang P., Cui J., Gao Y., Xie K. The roles of FOXM1 in pancreatic stem cells and carcinogenesis. Mol Cancer 2013, 12:159.
63. Wang Z., Park H.J., Carr J.R., Chen Y.J., Zheng Y., Li J., et al. FoxM1 in tumorigenicity of the neuroblastoma cells and renewal of the neural progenitors. Cancer Res 2011, 71:4292-4302.
64. Kong X., Li L., Li Z., Le X., Huang C., Jia Z., et al. Dysregulated expression of FOXM1 isoforms drives progression of pancreatic cancer. Cancer Res 2013, 73:3987-3996.
65. Li Q., Jia Z., Wang L., Kong X., Li Q., Guo K., et al. Disruption of Klf4 in villin-positive gastric progenitor cells promotes formation and progression of tumors of the antrum in mice. Gastroenterology 2012, 142:531-542.
66. Joshi K., Banasavadi-Siddegowda Y., Mo X., Kim S.H., Mao P., Kig C., et al. MELK-dependent FOXM1 phosphorylation is essential for proliferation of glioma stem cells. Stem Cells 2013, 31:1051-1063.
67. Zhang N., Wei P., Gong A., Chiu W.T., Lee H.T., Colman H., et al. FoxM1 promotes beta-catenin nuclear localization and controls Wnt target-gene expression and glioma tumorigenesis. Cancer Cell 2011, 20:427-442.
68. Pachkowski B.F., Guyton K.Z., Sonawane B. DNA repair during in utero development: a review of the current state of knowledge, research needs, and potential application in risk assessment. Mutat Res 2011, 728:35-46.
69. Behrens A., van Deursen J.M., Rudolph K.L., Schumacher B. Impact of genomic damage and ageing on stem cell function. Nat Cell Biol 2014, 16:201-207.
70. Sousounis K., Baddour J.A., Tsonis P.A. Aging and regeneration in vertebrates. Curr Top Dev Biol 2014, 108:217-246.
71. Li S.K., Smith D.K., Leung W.Y., Cheung A.M., Lam E.W., Dimri G.P., et al. FoxM1c counteracts oxidative stress-induced senescence and stimulates Bmi-1 expression. J Biol Chem 2008, 283:16545-16553.
72. Zeng J., Wang L., Li Q., Li W., Bjorkholm M., Jia J., et al. FoxM1 is up-regulated in gastric cancer and its inhibition leads to cellular senescence, partially dependent on p27 kip1. J Pathol 2009, 218:419-427.
73. Liu G., Sun Y., Ji P., Li X., Cogdell D., Yang D., et al. MiR-506 suppresses proliferation and induces senescence by directly targeting the CDK4/6-FOXM1 axis in ovarian cancer. J Pathol 2014, 10.1002/path.4348.
74. Rader J., Russell M.R., Hart L.S., Nakazawa M.S., Belcastro L.T., Martinez D., et al. Dual CDK4/CDK6 inhibition induces cell-cycle arrest and senescence in neuroblastoma. Clin Cancer Res 2013, 19:6173-6182.
75. Zhang X., Zeng J., Zhou M., Li B., Zhang Y., Huang T., et al. The tumor suppressive role of miRNA-370 by targeting FoxM1 in acute myeloid leukemia. Mol Cancer 2012, 11:56.
76. Khongkow P., Karunarathna U., Khongkow M., Gong C., Gomes A.R., Yague E., et al. FOXM1 targets NBS1 to regulate DNA damage-induced senescence and epirubicin resistance. Oncogene 2013, 10.1038/onc.2013.457.
77. Tan Y., Raychaudhuri P., Costa R.H. Chk2 mediates stabilization of the FoxM1 transcription factor to stimulate expression of DNA repair genes. Mol Cell Biol 2007, 27:1007-1016.
78. Zhang N., Wu X., Yang L., Xiao F., Zhang H., Zhou A., et al. FoxM1 inhibition sensitizes resistant glioblastoma cells to temozolomide by downregulating the expression of DNA-repair gene Rad51. Clin Cancer Res 2012, 18:5961-5971.
79. Monteiro L.J., Khongkow P., Kongsema M., Morris J.R., Man C., Weekes D., et al. The Forkhead Box M1 protein regulates BRIP1 expression and DNA damage repair in epirubicin treatment. Oncogene 2013, 32:4634-4645.