The roles of FOXM1 in pancreatic stem cells and carcinogenesis

Molecular Cancer

Volumn 12, Issue 1, 2013, Pages

  Quan, Ming ^a,c   Wang, Peipei ^b   Cui, Jiujie ^a,c   Gao, Yong ^b   Xie, Keping ^c  

^a SHANGHAI FIRST PEOPLE S HOSPITAL   (China)

^b TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Molecular biomarkers; Oncogenic switch; Progression; Stem cells; Therapeutic targets; Transcription factors

Indexed keywords

BMI1 PROTEIN; CD133 ANTIGEN; CD24 ANTIGEN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; FORKHEAD TRANSCRIPTION FACTOR; FORKHEAD TRANSCRIPTION FACTOR M1; HERMES ANTIGEN; K RAS PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NESTIN; NOTCH RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 4; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P53; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; WNT PROTEIN;

APOPTOSIS; CANCER GROWTH; CANCER PROGNOSIS; CANCER SURVIVAL; CARCINOGENESIS; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL MATURATION; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; DNA BINDING; DNA DAMAGE; EPITHELIAL MESENCHYMAL TRANSITION; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; INTRADUCTAL PAPILLARY MUCINOUS TUMOR; MUCINOUS CYSTIC NEOPLASM; NONHUMAN; PANCREAS ADENOCARCINOMA; PANCREAS ADENOMA; PANCREAS CANCER; PANCREAS CARCINOMA; PANCREATIC CANCER STEM CELL; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SOMATIC MUTATION; STEM CELL; TUMOR ASSOCIATED LEUKOCYTE;

ERINACEIDAE; MOLONEY MURINE LEUKEMIA VIRUS;

ANIMALS; CARCINOMA, PANCREATIC DUCTAL; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DISEASE PROGRESSION; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASTIC STEM CELLS; SIGNAL TRANSDUCTION;

EID: 84889804910     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-12-159     Document Type: Review

References (147)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011, 61(2):69-90. 10.3322/caac.20107, 21296855.
2. Hidalgo M. Pancreatic cancer. N Engl J Med 2010, 362(17):1605-1617. 10.1056/NEJMra0901557, 20427809.
3. Li D, Xie K, Wolff R, Abbruzzese JL. Pancreatic cancer. Lancet 2004, 363(9414):1049-1057. 10.1016/S0140-6736(04)15841-8, 3062508, 15051286.
4. Siegel R, Ward E, Brawley O, Jemal A. Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin 2011, 61(4):212-236. 10.3322/caac.20121, 21685461.
5. Li Y, Kong D, Ahmad A, Bao B, Sarkar FH. Pancreatic cancer stem cells: emerging target for designing novel therapy. Cancer Lett 2013, 338(1):94-100. 10.1016/j.canlet.2012.03.018, 22445908.
6. Wicha MS. B4 androgen ablation: attacking the prostate cancer stem cell. J Clin Invest 2013, 123(2):563-565.
7. Schieber MS, Chandel NS. ROS links glucose metabolism to breast cancer stem cell and EMT phenotype. Cancer Cell 2013, 23(3):265-267. 10.1016/j.ccr.2013.02.021, 23518342.
8. Pasquier J, Rafii A. Role of the microenvironment in ovarian cancer stem cell maintenance. Biomed Res Int 2013, 2013:630782. 3591167, 23484135.
9. Major AG, Pitty LP, Farah CS. Cancer stem cell markers in head and neck squamous cell carcinoma. Stem Cells Int 2013, 2013:319489. 3603684, 23533441.
10. Lu J, Ye X, Fan F, Xia L, Bhattacharya R, Bellister S, Tozzi F, Sceusi E, Zhou Y, Tachibana I, et al. Endothelial cells promote the colorectal cancer stem cell phenotype through a soluble form of Jagged-1. Cancer Cell 2013, 23(2):171-185. 10.1016/j.ccr.2012.12.021, 23375636.
11. Dong HH, Xiang S, Liang HF, Li CH, Zhang ZW, Chen XP. The niche of hepatic cancer stem cell and cancer recurrence. Med Hypotheses 2013, 80(5):666-668. 10.1016/j.mehy.2013.01.021, 23419668.
12. Borovski T, De Sousa EMF, Vermeulen L, Medema JP. Cancer stem cell niche: the place to be. Cancer Res 2011, 71(3):634-639. 10.1158/0008-5472.CAN-10-3220, 21266356.
13. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, Wicha M, Clarke MF, Simeone DM. Identification of pancreatic cancer stem cells. Cancer Res 2007, 67(3):1030-1037. 10.1158/0008-5472.CAN-06-2030, 17283135.
14. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, Bruns CJ, Heeschen C. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007, 1(3):313-323. 10.1016/j.stem.2007.06.002, 18371365.
15. Wang Z, Park HJ, Carr JR, Chen YJ, Zheng Y, Li J, Tyner AL, Costa RH, Bagchi S, Raychaudhuri P. FoxM1 in tumorigenicity of the neuroblastoma cells and renewal of the neural progenitors. Cancer Res 2011, 71(12):4292-4302. 10.1158/0008-5472.CAN-10-4087, 3771352, 21507930.
16. Korver W, Roose J, Heinen K, Weghuis DO, de Bruijn D, van Kessel AG, Clevers H. The human TRIDENT/HFH-11/FKHL16 gene: structure, localization, and promoter characterization. Genomics 1997, 46(3):435-442. 10.1006/geno.1997.5065, 9441747.
17. Kalin TV, Ustiyan V, Kalinichenko VV. Multiple faces of FoxM1 transcription factor: lessons from transgenic mouse models. Cell Cycle 2011, 10(3):396-405. 10.4161/cc.10.3.14709, 3115014, 21270518.
18. Bowman A, Nusse R. Location, location, location: FoxM1 mediates beta-catenin nuclear translocation and promotes glioma tumorigenesis. Cancer Cell 2011, 20(4):415-416. 10.1016/j.ccr.2011.10.003, 22014565.
19. Balli D, Zhang Y, Snyder J, Kalinichenko VV, Kalin TV. Endothelial cell-specific deletion of transcription factor FoxM1 increases urethane-induced lung carcinogenesis. Cancer Res 2011, 71(1):40-50. 10.1158/0008-5472.CAN-10-2004, 3075588, 21199796.
20. Yang C, Chen H, Yu L, Shan L, Xie L, Hu J, Chen T, Tan Y. Inhibition of FOXM1 transcription factor suppresses cell proliferation and tumor growth of breast cancer. Cancer Gene Ther 2013, 20(2):117-124. 10.1038/cgt.2012.94, 23306612.
21. Xia L, Huang W, Tian D, Zhu H, Zhang Y, Hu H, Fan D, Nie Y, Wu K. Upregulated FoxM1 expression induced by hepatitis B virus X protein promotes tumor metastasis and indicates poor prognosis in hepatitis B virus-related hepatocellular carcinoma. J Hepatol 2012, 57(3):600-612. 10.1016/j.jhep.2012.04.020, 22613004.
22. Xia JT, Wang H, Liang LJ, Peng BG, Wu ZF, Chen LZ, Xue L, Li Z, Li W. Overexpression of FOXM1 is associated with poor prognosis and clinicopathologic stage of pancreatic ductal adenocarcinoma. Pancreas 2012, 41(4):629-635. 10.1097/MPA.0b013e31823bcef2, 22249132.
23. Huang C, Qiu Z, Wang L, Peng Z, Jia Z, Logsdon CD, Le X, Wei D, Huang S, Xie K. A novel FoxM1-caveolin signaling pathway promotes pancreatic cancer invasion and metastasis. Cancer Res 2012, 72(3):655-665. 10.1158/0008-5472.CAN-11-3102, 3271134, 22194465.
24. Zhang N, Wei P, Gong A, Chiu WT, Lee HT, Colman H, Huang H, Xue J, Liu M, Wang Y, et al. FoxM1 promotes beta-catenin nuclear localization and controls Wnt target-gene expression and glioma tumorigenesis. Cancer Cell 2011, 20(4):427-442. 10.1016/j.ccr.2011.08.016, 3199318, 22014570.
25. Bao B, Wang Z, Ali S, Kong D, Banerjee S, Ahmad A, Li Y, Azmi AS, Miele L, Sarkar FH. Over-expression of FoxM1 leads to epithelial-mesenchymal transition and cancer stem cell phenotype in pancreatic cancer cells. J Cell Biochem 2011, 112(9):2296-2306. 10.1002/jcb.23150, 3155646, 21503965.
26. Macgregor-Das AM, Iacobuzio-Donahue CA. Molecular pathways in pancreatic carcinogenesis. J Surg Oncol 2013, 107(1):8-14. 10.1002/jso.23213, 3661191, 22806689.
27. Cooper CL, O'Toole SA, Kench JG. Classification, morphology and molecular pathology of premalignant lesions of the pancreas. Pathology 2013, 45(3):286-304. 10.1097/PAT.0b013e32835f2205, 23442735.
28. Hidalgo M. New insights into pancreatic cancer biology. Ann Oncol 2012, 23(Suppl 10):135-138. 10.1093/annonc/mds313, 21531784.
29. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Kamiyama H, Jimeno A, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008, 321(5897):1801-1806. 10.1126/science.1164368, 2848990, 18772397.
30. Kanda M, Matthaei H, Wu J, Hong SM, Yu J, Borges M, Hruban RH, Maitra A, Kinzler K, Vogelstein B, et al. Presence of somatic mutations in most early-stage pancreatic intraepithelial neoplasia. Gastroenterology 2012, 142(4):730-733. e739, 10.1053/j.gastro.2011.12.042, 3321090, 22226782.
31. Welsch T, Kleeff J, Friess H. Molecular pathogenesis of pancreatic cancer: advances and challenges. Curr Mol Med 2007, 7(5):504-521. 10.2174/156652407781387082, 17691965.
32. Lemoine NR, Jain S, Hughes CM, Staddon SL, Maillet B, Hall PA, Kloppel G. Ki-ras oncogene activation in preinvasive pancreatic cancer. Gastroenterology 1992, 102(1):230-236.
33. Hruban RH, van Mansfeld AD, Offerhaus GJ, van Weering DH, Allison DC, Goodman SN, Kensler TW, Bose KK, Cameron JL, Bos JL. K-ras oncogene activation in adenocarcinoma of the human pancreas. A study of 82 carcinomas using a combination of mutant-enriched polymerase chain reaction analysis and allele-specific oligonucleotide hybridization. Am J Pathol 1993, 143(2):545-554. 1887038, 8342602.
34. Schubbert S, Shannon K, Bollag G. Hyperactive Ras in developmental disorders and cancer. Nat Rev Cancer 2007, 7(4):295-308. 10.1038/nrc2109, 17384584.
35. Biankin AV, Waddell N, Kassahn KS, Gingras MC, Muthuswamy LB, Johns AL, Miller DK, Wilson PJ, Patch AM, Wu J, et al. Pancreatic cancer genomes reveal aberrations in axon guidance pathway genes. Nature 2012, 491(7424):399-405. 10.1038/nature11547, 3530898, 23103869.
36. Hingorani SR, Petricoin EF, Maitra A, Rajapakse V, King C, Jacobetz MA, Ross S, Conrads TP, Veenstra TD, Hitt BA, et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 2003, 4(6):437-450. 10.1016/S1535-6108(03)00309-X, 14706336.
37. Tuveson DA, Shaw AT, Willis NA, Silver DP, Jackson EL, Chang S, Mercer KL, Grochow R, Hock H, Crowley D, et al. Endogenous oncogenic K-ras(G12D) stimulates proliferation and widespread neoplastic and developmental defects. Cancer Cell 2004, 5(4):375-387. 10.1016/S1535-6108(04)00085-6, 15093544.
38. Calhoun ES, Jones JB, Ashfaq R, Adsay V, Baker SJ, Valentine V, Hempen PM, Hilgers W, Yeo CJ, Hruban RH, et al. BRAF and FBXW7 (CDC4, FBW7, AGO, SEL10) mutations in distinct subsets of pancreatic cancer: potential therapeutic targets. Am J Pathol 2003, 163(4):1255-1260. 10.1016/S0002-9440(10)63485-2, 1868306, 14507635.
39. Schutte M, Hruban RH, Geradts J, Maynard R, Hilgers W, Rabindran SK, Moskaluk CA, Hahn SA, Schwarte-Waldhoff I, Schmiegel W, et al. Abrogation of the Rb/p16 tumor-suppressive pathway in virtually all pancreatic carcinomas. Cancer Res 1997, 57(15):3126-3130.
40. Caldas C, Hahn SA, da Costa LT, Redston MS, Schutte M, Seymour AB, Weinstein CL, Hruban RH, Yeo CJ, Kern SE. Frequent somatic mutations and homozygous deletions of the p16 (MTS1) gene in pancreatic adenocarcinoma. Nat Genet 1994, 8(1):27-32. 10.1038/ng0994-27, 7726912.
41. Serrano M, Hannon GJ, Beach D. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 1993, 366(6456):704-707. 10.1038/366704a0, 8259215.
42. Li J, Poi MJ, Tsai MD. Regulatory mechanisms of tumor suppressor P16(INK4A) and their relevance to cancer. Biochemistry 2011, 50(25):5566-5582. 10.1021/bi200642e, 3127263, 21619050.
43. Rozenblum E, Schutte M, Goggins M, Hahn SA, Panzer S, Zahurak M, Goodman SN, Sohn TA, Hruban RH, Yeo CJ, et al. Tumor-suppressive pathways in pancreatic carcinoma. Cancer Res 1997, 57(9):1731-1734.
44. Scarpa A, Capelli P, Mukai K, Zamboni G, Oda T, Iacono C, Hirohashi S. Pancreatic adenocarcinomas frequently show p53 gene mutations. Am J Pathol 1993, 142(5):1534-1543. 1886920, 8494051.
45. DiGiuseppe JA, Redston MS, Yeo CJ, Kern SE, Hruban RH. p53-independent expression of the cyclin-dependent kinase inhibitor p21 in pancreatic carcinoma. Am J Pathol 1995, 147(4):884-888. 1871020, 7573363.
46. Karamitopoulou E, Zlobec I, Tornillo L, Carafa V, Schaffner T, Brunner T, Borner M, Diamantis I, Zimmermann A, Terracciano L. Differential cell cycle and proliferation marker expression in ductal pancreatic adenocarcinoma and pancreatic intraepithelial neoplasia (PanIN). Pathology 2010, 42(3):229-234. 10.3109/00313021003631379, 20350215.
47. Hingorani SR, Wang L, Multani AS, Combs C, Deramaudt TB, Hruban RH, Rustgi AK, Chang S, Tuveson DA. Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 2005, 7(5):469-483. 10.1016/j.ccr.2005.04.023, 15894267.
48. Hahn SA, Schutte M, Hoque AT, Moskaluk CA, da Costa LT, Rozenblum E, Weinstein CL, Fischer A, Yeo CJ, Hruban RH, et al. DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 1996, 271(5247):350-353. 10.1126/science.271.5247.350, 8553070.
49. Wilentz RE, Iacobuzio-Donahue CA, Argani P, McCarthy DM, Parsons JL, Yeo CJ, Kern SE, Hruban RH. Loss of expression of Dpc4 in pancreatic intraepithelial neoplasia: evidence that DPC4 inactivation occurs late in neoplastic progression. Cancer Res 2000, 60(7):2002-2006.
50. Siegel PM, Massague J. Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer 2003, 3(11):807-821. 10.1038/nrc1208, 14557817.
51. Kojima K, Vickers SM, Adsay NV, Jhala NC, Kim HG, Schoeb TR, Grizzle WE, Klug CA. Inactivation of Smad4 accelerates Kras(G12D)-mediated pancreatic neoplasia. Cancer Res 2007, 67(17):8121-8130. 10.1158/0008-5472.CAN-06-4167, 17804724.
52. Izeradjene K, Combs C, Best M, Gopinathan A, Wagner A, Grady WM, Deng CX, Hruban RH, Adsay NV, Tuveson DA, et al. Kras(G12D) and Smad4/Dpc4 haploinsufficiency cooperate to induce mucinous cystic neoplasms and invasive adenocarcinoma of the pancreas. Cancer Cell 2007, 11(3):229-243. 10.1016/j.ccr.2007.01.017, 17349581.
53. Tascilar M, Skinner HG, Rosty C, Sohn T, Wilentz RE, Offerhaus GJ, Adsay V, Abrams RA, Cameron JL, Kern SE, et al. The SMAD4 protein and prognosis of pancreatic ductal adenocarcinoma. Clin Cancer Res 2001, 7(12):4115-4121.
54. Iacobuzio-Donahue CA, Fu B, Yachida S, Luo M, Abe H, Henderson CM, Vilardell F, Wang Z, Keller JW, Banerjee P, et al. DPC4 gene status of the primary carcinoma correlates with patterns of failure in patients with pancreatic cancer. J Clin Oncol 2009, 27(11):1806-1813. 10.1200/JCO.2008.17.7188, 2668706, 19273710.
55. Dorado J, Lonardo E, Miranda-Lorenzo I, Heeschen C. Pancreatic cancer stem cells: new insights and perspectives. J Gastroenterol 2011, 46(8):966-973. 10.1007/s00535-011-0422-x, 21698355.
56. Matsuda Y, Kure S, Ishiwata T. Nestin and other putative cancer stem cell markers in pancreatic cancer. Med Mol Morphol 2012, 45(2):59-65. 10.1007/s00795-012-0571-x, 22718289.
57. Kure S, Matsuda Y, Hagio M, Ueda J, Naito Z, Ishiwata T. Expression of cancer stem cell markers in pancreatic intraepithelial neoplasias and pancreatic ductal adenocarcinomas. Int J Oncol 2012, 41(4):1314-1324.
58. Wen J, Park JY, Park KH, Chung HW, Bang S, Park SW, Song SY. Oct4 and Nanog expression is associated with early stages of pancreatic carcinogenesis. Pancreas 2010, 39(5):622-626. 10.1097/MPA.0b013e3181c75f5e, 20173672.
59. De La OJ, Murtaugh LC. Notch and Kras in pancreatic cancer: at the crossroads of mutation, differentiation and signaling. Cell Cycle 2009, 8(12):1860-1864. 10.4161/cc.8.12.8744, 2719432, 19440048.
60. Mazur PK, Einwachter H, Lee M, Sipos B, Nakhai H, Rad R, Zimber-Strobl U, Strobl LJ, Radtke F, Kloppel G, et al. Notch2 is required for progression of pancreatic intraepithelial neoplasia and development of pancreatic ductal adenocarcinoma. Proc Natl Acad Sci U S A 2010, 107(30):13438-13443. 10.1073/pnas.1002423107, 2922150, 20624967.
61. Avila JL, Troutman S, Durham A, Kissil JL. Notch1 is not required for acinar-to-ductal metaplasia in a model of Kras-induced pancreatic ductal adenocarcinoma. PLoS One 2012, 7(12):e52133. 10.1371/journal.pone.0052133, 3526595, 23284900.
62. Hill R, Calvopina JH, Kim C, Wang Y, Dawson DW, Donahue TR, Dry S, Wu H. PTEN loss accelerates KrasG12D-induced pancreatic cancer development. Cancer Res 2010, 70(18):7114-7124. 10.1158/0008-5472.CAN-10-1649, 2940963, 20807812.
63. Martinez-Romero C, Rooman I, Skoudy A, Guerra C, Molero X, Gonzalez A, Iglesias M, Lobato T, Bosch A, Barbacid M, et al. The epigenetic regulators Bmi1 and Ring1B are differentially regulated in pancreatitis and pancreatic ductal adenocarcinoma. J Pathol 2009, 219(2):205-213. 10.1002/path.2585, 19585519.
64. Skoudy A, Hernandez-Munoz I, Navarro P. Pancreatic ductal adenocarcinoma and transcription factors: role of c-Myc. J Gastrointest Cancer 2011, 42(2):76-84. 10.1007/s12029-011-9258-0, 21279552.
65. Yu J, Ohuchida K, Mizumoto K, Ishikawa N, Ogura Y, Yamada D, Egami T, Fujita H, Ohashi S, Nagai E, et al. Overexpression of c-met in the early stage of pancreatic carcinogenesis; altered expression is not sufficient for progression from chronic pancreatitis to pancreatic cancer. World J Gastroenterol 2006, 12(24):3878-3882.
66. Li Q, Zhang N, Jia Z, Le X, Dai B, Wei D, Huang S, Tan D, Xie K. Critical role and regulation of transcription factor FoxM1 in human gastric cancer angiogenesis and progression. Cancer Res 2009, 69(8):3501-3509. 10.1158/0008-5472.CAN-08-3045, 19351851.
67. Halasi M, Gartel AL. Targeting FOXM1 in cancer. Biochem Pharmacol 2013, 85(5):644-652. 10.1016/j.bcp.2012.10.013, 23103567.
68. Koo CY, Muir KW, Lam EW. FOXM1: From cancer initiation to progression and treatment. Biochim Biophys Acta 2012, 1819(1):28-37. 10.1016/j.bbagrm.2011.09.004, 21978825.
69. Wang Z, Ahmad A, Li Y, Banerjee S, Kong D, Sarkar FH. Forkhead box M1 transcription factor: a novel target for cancer therapy. Cancer Treat Rev 2010, 36(2):151-156. 10.1016/j.ctrv.2009.11.006, 2838950, 20022709.
70. Ma RY, Tong TH, Leung WY, Yao KM. Raf/MEK/MAPK signaling stimulates the nuclear translocation and transactivating activity of FOXM1. Methods Mol Biol 2010, 647:113-123. 10.1007/978-1-60761-738-9_6, 20694663.
71. Bellelli R, Castellone MD, Garcia-Rostan G, Ugolini C, Nucera C, Sadow PM, Nappi TC, Salerno P, Cantisani MC, Basolo F, et al. FOXM1 is a molecular determinant of the mitogenic and invasive phenotype of anaplastic thyroid carcinoma. Endocr Relat Cancer 2012, 19(5):695-710. 10.1530/ERC-12-0031, 3637951, 22919068.
72. Wang IC, Zhang Y, Snyder J, Sutherland MJ, Burhans MS, Shannon JM, Park HJ, Whitsett JA, Kalinichenko VV. Increased expression of FoxM1 transcription factor in respiratory epithelium inhibits lung sacculation and causes Clara cell hyperplasia. Dev Biol 2010, 347(2):301-314. 10.1016/j.ydbio.2010.08.027, 2957513, 20816795.
73. Teh MT, Gemenetzidis E, Patel D, Tariq R, Nadir A, Bahta AW, Waseem A, Hutchison IL. FOXM1 induces a global methylation signature that mimics the cancer epigenome in head and neck squamous cell carcinoma. PLoS One 2012, 7(3):e34329. 10.1371/journal.pone.0034329, 3312909, 22461910.
74. Teh MT, Gemenetzidis E, Chaplin T, Young BD, Philpott MP. Upregulation of FOXM1 induces genomic instability in human epidermal keratinocytes. Mol Cancer 2010, 9:45. 10.1186/1476-4598-9-45, 2907729, 20187950.
75. Xie Z, Tan G, Ding M, Dong D, Chen T, Meng X, Huang X, Tan Y. Foxm1 transcription factor is required for maintenance of pluripotency of P19 embryonal carcinoma cells. Nucleic Acids Res 2010, 38(22):8027-8038. 10.1093/nar/gkq715, 3001083, 20702419.
76. Gu D, Liu H, Su GH, Zhang X, Chin-Sinex H, Hanenberg H, Mendonca MS, Shannon HE, Chiorean EG, Xie J. Combining hedgehog signaling inhibition with focal irradiation on reduction of pancreatic cancer metastasis. Mol Cancer Ther 2013, 12(6):1038-1048. 10.1158/1535-7163.MCT-12-1030, 23468532.
77. Fu J, Rodova M, Roy SK, Sharma J, Singh KP, Srivastava RK, Shankar S. GANT-61 inhibits pancreatic cancer stem cell growth in vitro and in NOD/SCID/IL2R gamma null mice xenograft. Cancer Lett 2013, 330(1):22-32. 10.1016/j.canlet.2012.11.018, 23200667.
78. Bao B, Wang Z, Ali S, Kong D, Li Y, Ahmad A, Banerjee S, Azmi AS, Miele L, Sarkar FH. Notch-1 induces epithelial-mesenchymal transition consistent with cancer stem cell phenotype in pancreatic cancer cells. Cancer Lett 2011, 307(1):26-36. 10.1016/j.canlet.2011.03.012, 3104092, 21463919.
79. Wang Z, Ahmad A, Li Y, Azmi AS, Miele L, Sarkar FH. Targeting notch to eradicate pancreatic cancer stem cells for cancer therapy. Anticancer Res 2011, 31(4):1105-1113.
80. Proctor E, Waghray M, Lee CJ, Heidt DG, Yalamanchili M, Li C, Bednar F, Simeone DM. Bmi1 enhances tumorigenicity and cancer stem cell function in pancreatic adenocarcinoma. PLoS One 2013, 8(2):e55820. 10.1371/journal.pone.0055820, 3577834, 23437065.
81. Lonardo E, Hermann PC, Mueller MT, Huber S, Balic A, Miranda-Lorenzo I, Zagorac S, Alcala S, Rodriguez-Arabaolaza I, Ramirez JC, et al. Nodal/Activin signaling drives self-renewal and tumorigenicity of pancreatic cancer stem cells and provides a target for combined drug therapy. Cell Stem Cell 2011, 9(5):433-446. 10.1016/j.stem.2011.10.001, 22056140.
82. Takao S, Ding Q, Matsubara S. Pancreatic cancer stem cells: regulatory networks in the tumor microenvironment and targeted therapy. J Hepatobiliary Pancreat Sci 2012, 19(6):614-620. 10.1007/s00534-012-0547-1, 22878838.
83. Lonardo E, Frias-Aldeguer J, Hermann PC, Heeschen C. Pancreatic stellate cells form a niche for cancer stem cells and promote their self-renewal and invasiveness. Cell Cycle 2012, 11(7):1282-1290. 10.4161/cc.19679, 22421149.
84. Yauch RL, Gould SE, Scales SJ, Tang T, Tian H, Ahn CP, Marshall D, Fu L, Januario T, Kallop D, et al. A paracrine requirement for hedgehog signalling in cancer. Nature 2008, 455(7211):406-410. 10.1038/nature07275, 18754008.
85. Thayer SP, di Magliano MP, Heiser PW, Nielsen CM, Roberts DJ, Lauwers GY, Qi YP, Gysin S, Fernandez-del Castillo C, Yajnik V, et al. Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis. Nature 2003, 425(6960):851-856. 10.1038/nature02009, 3688051, 14520413.
86. Katoh Y, Katoh M. Hedgehog target genes: mechanisms of carcinogenesis induced by aberrant hedgehog signaling activation. Curr Mol Med 2009, 9(7):873-886. 10.2174/156652409789105570, 19860666.
87. Hao K, Tian XD, Qin CF, Xie XH, Yang YM. Hedgehog signaling pathway regulates human pancreatic cancer cell proliferation and metastasis. Oncol Rep 2013, 29(3):1124-1132.
88. Tang SN, Fu J, Nall D, Rodova M, Shankar S, Srivastava RK. Inhibition of sonic hedgehog pathway and pluripotency maintaining factors regulate human pancreatic cancer stem cell characteristics. Int J Cancer 2012, 131(1):30-40. 10.1002/ijc.26323, 3480310, 21796625.
89. Rodova M, Fu J, Watkins DN, Srivastava RK, Shankar S. Sonic hedgehog signaling inhibition provides opportunities for targeted therapy by sulforaphane in regulating pancreatic cancer stem cell self-renewal. PLoS One 2012, 7(9):e46083. 10.1371/journal.pone.0046083, 3461003, 23029396.
90. Li SH, Fu J, Watkins DN, Srivastava RK, Shankar S. Sulforaphane regulates self-renewal of pancreatic cancer stem cells through the modulation of Sonic hedgehog-GLI pathway. Mol Cell Biochem 2013, 373(1-2):217-227. 10.1007/s11010-012-1493-6, 23129257.
91. Srivastava RK, Tang SN, Zhu W, Meeker D, Shankar S. Sulforaphane synergizes with quercetin to inhibit self-renewal capacity of pancreatic cancer stem cells. Front Biosci (Elite Ed) 2011, 3:515-528. 10.2741/e266, 21196331.
92. Huang FT, Zhuan-Sun YX, Zhuang YY, Wei SL, Tang J, Chen WB, Zhang SN. Inhibition of hedgehog signaling depresses self-renewal of pancreatic cancer stem cells and reverses chemoresistance. Int J Oncol 2012, 41(5):1707-1714.
93. Santisteban M. ABC transporters as molecular effectors of pancreatic oncogenic pathways: the Hedgehog-GLI model. J Gastrointest Cancer 2010, 41(3):153-158. 10.1007/s12029-010-9144-1, 20333482.
94. Mueller MT, Hermann PC, Witthauer J, Rubio-Viqueira B, Leicht SF, Huber S, Ellwart JW, Mustafa M, Bartenstein P, D'Haese JG, et al. Combined targeted treatment to eliminate tumorigenic cancer stem cells in human pancreatic cancer. Gastroenterology 2009, 137(3):1102-1113. 10.1053/j.gastro.2009.05.053, 19501590.
95. Singh BN, Fu J, Srivastava RK, Shankar S. Hedgehog signaling antagonist GDC-0449 (Vismodegib) inhibits pancreatic cancer stem cell characteristics: molecular mechanisms. PLoS One 2011, 6(11):e27306. 10.1371/journal.pone.0027306, 3210776, 22087285.
96. LoRusso PM, Rudin CM, Reddy JC, Tibes R, Weiss GJ, Borad MJ, Hann CL, Brahmer JR, Chang I, Darbonne WC, et al. Phase I trial of hedgehog pathway inhibitor vismodegib (GDC-0449) in patients with refractory, locally advanced or metastatic solid tumors. Clin Cancer Res 2011, 17(8):2502-2511. 10.1158/1078-0432.CCR-10-2745, 21300762.
97. Mullendore ME, Koorstra JB, Li YM, Offerhaus GJ, Fan X, Henderson CM, Matsui W, Eberhart CG, Maitra A, Feldmann G. Ligand-dependent Notch signaling is involved in tumor initiation and tumor maintenance in pancreatic cancer. Clin Cancer Res 2009, 15(7):2291-2301. 10.1158/1078-0432.CCR-08-2004, 2711441, 19258443.
98. Miele L. Notch signaling. Clin Cancer Res 2006, 12(4):1074-1079. 10.1158/1078-0432.CCR-05-2570, 16489059.
99. Wang Z, Li Y, Banerjee S, Sarkar FH. Emerging role of Notch in stem cells and cancer. Cancer Lett 2009, 279(1):8-12. 10.1016/j.canlet.2008.09.030, 2699045, 19022563.
100. Zhou ZC, Dong QG, Fu DL, Gong N, Ni QX. Characteristics of Notch2 pancreatic cancer stem-like cells and the relationship with centroacinar cells. Cell Biol Int 2013, 37(8):805-811. 10.1002/cbin.10102, 23536545.
101. Yabuuchi S, Pai SG, Campbell NR, Wilde RD, Oliveira ED, Korangath P, Streppel M, Rasheed ZA, Hidalgo M, Maitra A, et al. Notch signaling pathway targeted therapy suppresses tumor progression and metastatic spread in pancreatic cancer. Cancer Lett 2013, 335(1):41-51. 10.1016/j.canlet.2013.01.054, 23402814.
102. Fan X, Khaki L, Zhu TS, Soules ME, Talsma CE, Gul N, Koh C, Zhang J, Li YM, Maciaczyk J, et al. NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells 2010, 28(1):5-16. 2878196, 19904829.
103. Song W, Tao K, Li H, Jin C, Song Z, Li J, Shi H, Li X, Dang Z, Dou K. Bmi-1 is related to proliferation, survival and poor prognosis in pancreatic cancer. Cancer Sci 2010, 101(7):1754-1760. 10.1111/j.1349-7006.2010.01577.x, 20426791.
104. Yin T, Wei H, Gou S, Shi P, Yang Z, Zhao G, Wang C. Cancer stem-like cells enriched in panc-1 spheres possess increased migration ability and resistance to gemcitabine. Int J Mol Sci 2011, 12(3):1595-1604. 3111620, 21673909.
105. Moon SH, Kim DK, Cha Y, Jeon I, Song J, Park KS. PI3K/Akt and Stat3 signaling regulated by PTEN control of the cancer stem cell population, proliferation and senescence in a glioblastoma cell line. Int J Oncol 2013, 42(3):921-928.
106. Wei Y, Jiang Y, Zou F, Liu Y, Wang S, Xu N, Xu W, Cui C, Xing Y, Cao B, et al. Activation of PI3K/Akt pathway by CD133-p85 interaction promotes tumorigenic capacity of glioma stem cells. Proc Natl Acad Sci U S A 2013, 110(17):6829-6834. 10.1073/pnas.1217002110, 3637720, 23569237.
107. Shenoy AK, Fisher RC, Butterworth EA, Pi L, Chang LJ, Appelman HD, Chang M, Scott EW, Huang EH. Transition from colitis to cancer: high Wnt activity sustains the tumor-initiating potential of colon cancer stem cell precursors. Cancer Res 2012, 72(19):5091-5100. 10.1158/0008-5472.CAN-12-1806, 3463774, 22902411.
108. Teh MT, Wong ST, Neill GW, Ghali LR, Philpott MP, Quinn AG. FOXM1 is a downstream target of Gli1 in basal cell carcinomas. Cancer Res 2002, 62(16):4773-4780.
109. Pignot G, Vieillefond A, Vacher S, Zerbib M, Debre B, Lidereau R, Amsellem-Ouazana D, Bieche I. Hedgehog pathway activation in human transitional cell carcinoma of the bladder. Br J Cancer 2012, 106(6):1177-1186. 10.1038/bjc.2012.55, 3304423, 22361633.
110. Douard R, Moutereau S, Pernet P, Chimingqi M, Allory Y, Manivet P, Conti M, Vaubourdolle M, Cugnenc PH, Loric S. Sonic Hedgehog-dependent proliferation in a series of patients with colorectal cancer. Surgery 2006, 139(5):665-670. 10.1016/j.surg.2005.10.012, 16701100.
111. Gialmanidis IP, Bravou V, Amanetopoulou SG, Varakis J, Kourea H, Papadaki H. Overexpression of hedgehog pathway molecules and FOXM1 in non-small cell lung carcinomas. Lung Cancer 2009, 66(1):64-74. 10.1016/j.lungcan.2009.01.007, 19200615.
112. Lin M, Guo LM, Liu H, Du J, Yang J, Zhang LJ, Zhang B. Nuclear accumulation of glioma-associated oncogene 2 protein and enhanced expression of forkhead-box transcription factor M1 protein in human hepatocellular carcinoma. Histol Histopathol 2010, 25(10):1269-1275.
113. Park HJ, Gusarova G, Wang Z, Carr JR, Li J, Kim KH, Qiu J, Park YD, Williamson PR, Hay N, et al. Deregulation of FoxM1b leads to tumour metastasis. EMBO Mol Med 2011, 3(1):21-34. 10.1002/emmm.201000107, 3401999, 21204266.
114. Park HJ, Carr JR, Wang Z, Nogueira V, Hay N, Tyner AL, Lau LF, Costa RH, Raychaudhuri P. FoxM1, a critical regulator of oxidative stress during oncogenesis. EMBO J 2009, 28(19):2908-2918. 10.1038/emboj.2009.239, 2760115, 19696738.
115. Wang Z, Li Y, Ahmad A, Banerjee S, Azmi AS, Kong D, Wojewoda C, Miele L, Sarkar FH. Down-regulation of Notch-1 is associated with Akt and FoxM1 in inducing cell growth inhibition and apoptosis in prostate cancer cells. J Cell Biochem 2011, 112(1):78-88. 10.1002/jcb.22770, 3792569, 20658545.
116. Li SK, Smith DK, Leung WY, Cheung AM, Lam EW, Dimri GP, Yao KM. FoxM1c counteracts oxidative stress-induced senescence and stimulates Bmi-1 expression. J Biol Chem 2008, 283(24):16545-16553. 10.1074/jbc.M709604200, 2423239, 18408007.
117. Gong A, Huang S. FoxM1 and Wnt/beta-Catenin Signaling in Glioma Stem Cells. Cancer Res 2012, 72(22):5658-5662. 10.1158/0008-5472.CAN-12-0953, 3500394, 23139209.
118. Fuchs E, Tumbar T, Guasch G. Socializing with the neighbors: stem cells and their niche. Cell 2004, 116(6):769-778. 10.1016/S0092-8674(04)00255-7, 15035980.
119. Filatova A, Acker T, Garvalov BK. The cancer stem cell niche(s): the crosstalk between glioma stem cells and their microenvironment. Biochim Biophys Acta 2013, 1830(2):2496-2508. 10.1016/j.bbagen.2012.10.008, 23079585.
120. Takakura N. Formation and regulation of the cancer stem cell niche. Cancer Sci 2012, 103(7):1177-1181. 10.1111/j.1349-7006.2012.02270.x, 22416970.
121. McCord AM, Jamal M, Shankavaram UT, Lang FF, Camphausen K, Tofilon PJ. Physiologic oxygen concentration enhances the stem-like properties of CD133+ human glioblastoma cells in vitro. Mol Cancer Res 2009, 7(4):489-497. 10.1158/1541-7786.MCR-08-0360, 19372578.
122. Mathieu J, Zhang Z, Zhou W, Wang AJ, Heddleston JM, Pinna CM, Hubaud A, Stadler B, Choi M, Bar M, et al. HIF induces human embryonic stem cell markers in cancer cells. Cancer Res 2011, 71(13):4640-4652. 10.1158/0008-5472.CAN-10-3320, 3129496, 21712410.
123. Hashimoto O, Shimizu K, Semba S, Chiba S, Ku Y, Yokozaki H, Hori Y. Hypoxia induces tumor aggressiveness and the expansion of CD133-positive cells in a hypoxia-inducible factor-1alpha-dependent manner in pancreatic cancer cells. Pathobiology 2011, 78(4):181-192. 10.1159/000325538, 21778785.
124. Xia LM, Huang WJ, Wang B, Liu M, Zhang Q, Yan W, Zhu Q, Luo M, Zhou ZZ, Tian DA. Transcriptional up-regulation of FoxM1 in response to hypoxia is mediated by HIF-1. J Cell Biochem 2009, 106(2):247-256. 10.1002/jcb.21996, 19097132.
125. Masamune A, Kikuta K, Watanabe T, Satoh K, Hirota M, Shimosegawa T. Hypoxia stimulates pancreatic stellate cells to induce fibrosis and angiogenesis in pancreatic cancer. Am J Physiol Gastrointest Liver Physiol 2008, 295(4):G709-G717. 10.1152/ajpgi.90356.2008, 18669622.
126. Hamada S, Masamune A, Takikawa T, Suzuki N, Kikuta K, Hirota M, Hamada H, Kobune M, Satoh K, Shimosegawa T. Pancreatic stellate cells enhance stem cell-like phenotypes in pancreatic cancer cells. Biochem Biophys Res Commun 2012, 421(2):349-354. 10.1016/j.bbrc.2012.04.014, 22510406.
127. Katsuno Y, Lamouille S, Derynck R. TGF-beta signaling and epithelial-mesenchymal transition in cancer progression. Curr Opin Oncol 2013, 25(1):76-84. 10.1097/CCO.0b013e32835b6371, 23197193.
128. Kabashima A, Higuchi H, Takaishi H, Matsuzaki Y, Suzuki S, Izumiya M, Iizuka H, Sakai G, Hozawa S, Azuma T, et al. Side population of pancreatic cancer cells predominates in TGF-beta-mediated epithelial to mesenchymal transition and invasion. Int J Cancer 2009, 124(12):2771-2779. 10.1002/ijc.24349, 19296540.
129. Liu Z, Bandyopadhyay A, Nichols RW, Wang L, Hinck AP, Wang S, Sun LZ. Blockade of autocrine TGF-beta signaling inhibits stem cell phenotype, survival, and metastasis of murine breast cancer cells. J Stem Cell Res Ther 2012, 2(1):1-8. 3593047, 23482850.
130. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133(4):704-715. 10.1016/j.cell.2008.03.027, 2728032, 18485877.
131. Asiedu MK, Ingle JN, Behrens MD, Radisky DC, Knutson KL. TGFbeta/TNF(alpha)-mediated epithelial-mesenchymal transition generates breast cancer stem cells with a claudin-low phenotype. Cancer Res 2011, 71(13):4707-4719. 10.1158/0008-5472.CAN-10-4554, 3129359, 21555371.
132. Watabe T, Miyazono K. Roles of TGF-beta family signaling in stem cell renewal and differentiation. Cell Res 2009, 19(1):103-115. 10.1038/cr.2008.323, 19114993.
133. Medici D, Shore EM, Lounev VY, Kaplan FS, Kalluri R, Olsen BR. Conversion of vascular endothelial cells into multipotent stem-like cells. Nat Med 2010, 16(12):1400-1406. 10.1038/nm.2252, 3209716, 21102460.
134. Li J, Wang Y, Luo J, Fu Z, Ying J, Yu Y, Yu W. miR-134 inhibits epithelial to mesenchymal transition by targeting FOXM1 in non-small cell lung cancer cells. FEBS Lett 2012, 586(20):3761-3765. 10.1016/j.febslet.2012.09.016, 23010597.
135. Balli D, Ustiyan V, Zhang Y, Wang IC, Masino AJ, Ren X, Whitsett JA, Kalinichenko VV, Kalin TV. Foxm1 transcription factor is required for lung fibrosis and epithelial-to-mesenchymal transition. EMBO J 2013, 32(2):231-244. 10.1038/emboj.2012.336, 23288041.
136. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011, 144(5):646-674. 10.1016/j.cell.2011.02.013, 21376230.
137. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell 2010, 140(6):883-899. 10.1016/j.cell.2010.01.025, 2866629, 20303878.
138. Hao NB, Lu MH, Fan YH, Cao YL, Zhang ZR, Yang SM. Macrophages in tumor microenvironments and the progression of tumors. Clin Dev Immunol 2012, 2012:948098. 3385963, 22778768.
139. Mitchem JB, Brennan DJ, Knolhoff BL, Belt BA, Zhu Y, Sanford DE, Belaygorod L, Carpenter D, Collins L, Piwnica-Worms D, et al. Targeting tumor-infiltrating macrophages decreases tumor-initiating cells, relieves immunosuppression, and improves chemotherapeutic responses. Cancer Res 2013, 73(3):1128-1141. 10.1158/0008-5472.CAN-12-2731, 23221383.
140. Kurahara H, Takao S, Kuwahata T, Nagai T, Ding Q, Maeda K, Shinchi H, Mataki Y, Maemura K, Matsuyama T, et al. Clinical significance of folate receptor beta-expressing tumor-associated macrophages in pancreatic cancer. Ann Surg Oncol 2012, 19(7):2264-2271. 10.1245/s10434-012-2263-0, 22350599.
141. Yang J, Liao D, Chen C, Liu Y, Chuang TH, Xiang R, Markowitz D, Reisfeld RA, Luo Y. Tumor-associated macrophages regulate murine breast cancer stem cells through a novel paracrine EGFR/Stat3/Sox-2 signaling pathway. Stem Cells 2013, 31(2):248-258. 10.1002/stem.1281, 23169551.
142. Ding J, Jin W, Chen C, Shao Z, Wu J. Tumor associated macrophage x cancer cell hybrids may acquire cancer stem cell properties in breast cancer. PLoS One 2012, 7(7):e41942. 10.1371/journal.pone.0041942, 3405038, 22848668.
143. Wu A, Wei J, Kong LY, Wang Y, Priebe W, Qiao W, Sawaya R, Heimberger AB. Glioma cancer stem cells induce immunosuppressive macrophages/microglia. Neuro Oncol 2010, 12(11):1113-1125. 10.1093/neuonc/noq082, 3098021, 20667896.
144. Pallini R, Ricci-Vitiani L, Banna GL, Signore M, Lombardi D, Todaro M, Stassi G, Martini M, Maira G, Larocca LM, et al. Cancer stem cell analysis and clinical outcome in patients with glioblastoma multiforme. Clin Cancer Res 2008, 14(24):8205-8212. 10.1158/1078-0432.CCR-08-0644, 19088037.
145. Ren X, Zhang Y, Snyder J, Cross ER, Shah TA, Kalin TV, Kalinichenko VV. Forkhead box M1 transcription factor is required for macrophage recruitment during liver repair. Mol Cell Biol 2010, 30(22):5381-5393. 10.1128/MCB.00876-10, 2976366, 20837707.
146. Ren X, Shah TA, Ustiyan V, Zhang Y, Shinn J, Chen G, Whitsett JA, Kalin TV, Kalinichenko VV. FOXM1 promotes allergen-induced goblet cell metaplasia and pulmonary inflammation. Mol Cell Biol 2013, 33(2):371-386. 10.1128/MCB.00934-12, 3554115, 23149934.
147. Balli D, Ren X, Chou FS, Cross E, Zhang Y, Kalinichenko VV, Kalin TV. Foxm1 transcription factor is required for macrophage migration during lung inflammation and tumor formation. Oncogene 2012, 31(34):3875-3888. 10.1038/onc.2011.549, 3297705, 22139074.