The Rb-E2F transcriptional regulatory pathway in tumor angiogenesis and metastasis

Advances in Cancer Research

Volumn 121, Issue , 2014, Pages 147-182

  Schaal, Courtney ^a   Pillai, Smitha ^a   Chellappan, Srikumar P ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

Cell cycle; MMP; Raf 1; Stemness; Transcription; VEGF

Indexed keywords

CYCLIN D1; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBRONECTIN; GELATINASE A; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INHIBITOR OF DIFFERENTIATION PROTEIN; INTERSTITIAL COLLAGENASE; KERATINOCYTE GROWTH FACTOR; MATRIX METALLOPROTEINASE 16; MICRORNA 210; P21 ACTIVATED KINASE 1; PLATELET DERIVED GROWTH FACTOR B; PROTEIN P130; PROTEIN P53; RAF PROTEIN; RAS PROTEIN; RETINOBLASTOMA BINDING PROTEIN 2; RETINOBLASTOMA BINDING PROTEIN 7; THROMBOSPONDIN 1; TRANSCRIPTION FACTOR E2F; TRANSCRIPTION FACTOR ZEB1; TUMOR MARKER; UNINDEXED DRUG; UVOMORULIN; VASCULOTROPIN; VASCULOTROPIN B; VASCULOTROPIN C; VASCULOTROPIN RECEPTOR; VIMENTIN; RETINOBLASTOMA PROTEIN;

ADIPOCYTE; AEROBIC METABOLISM; ANGIOGENESIS; APOPTOSIS; ARTICLE; BREAST METASTASIS; CANCER CELL LINE; CANCER STEM CELL; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL DEATH; CELL DIFFERENTIATION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL RENEWAL; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME 20Q; COLLAGEN DEGRADATION; COLORECTAL CANCER; DNA BINDING; DOWN REGULATION; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; ENERGY METABOLISM; ENZYME PHOSPHORYLATION; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; FIBROBLAST; FIBROSARCOMA; G1 PHASE CELL CYCLE CHECKPOINT; GENE DOSAGE; GENE MUTATION; GENE OVEREXPRESSION; GLUCOSE HOMEOSTASIS; GLYCOLYSIS; HEAD AND NECK CANCER; HUMAN; HYPOPHYSIS TUMOR; INSULIN RELEASE; LIPID METABOLISM; LYMPH NODE METASTASIS; MELANOMA; METASTASIS; METASTASIS POTENTIAL; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROMOTER REGION; THYROID MEDULLARY CARCINOMA; TRANSCRIPTION FACTOR E2F GENE; TRANSCRIPTION INITIATION; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; UPREGULATION; ANIMAL; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PHYSIOLOGY; VASCULARIZATION;

ANIMALS; E2F TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASM METASTASIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; RETINOBLASTOMA PROTEIN; TRANSCRIPTION, GENETIC;

EID: 84901482020     PISSN: 0065230X     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-800249-0.00004-4     Document Type: Chapter

References (158)

1. Ahluwalia A., Tarnawski A.S. Critical role of hypoxia sensor-HIF-1alpha in VEGF gene activation. Implications for angiogenesis and tissue injury healing. Current Medicinal Chemistry 2012, 19:90-97.
2. Aladowicz E., Ferro L., Vitali G.C., Venditti E., Fornasari L., Lanfrancone L. Molecular networks in melanoma invasion and metastasis. Future Oncology 2013, 9:713-726.
3. Alavi A., Hood J.D., Frausto R., Stupack D.G., Cheresh D.A. Role of Raf in vascular protection from distinct apoptotic stimuli. Science 2003, 301:94-96.
4. Arima Y., Hayashi H., Sasaki M., Hosonaga M., Goto T.M., Chiyoda T., et al. Induction of ZEB proteins by inactivation of RB protein is key determinant of mesenchymal phenotype of breast cancer. The Journal of Biological Chemistry 2012, 287:7896-7906.
5. Arima Y., Inoue Y., Shibata T., Hayashi H., Nagano O., Saya H., et al. Rb depletion results in deregulation of E-cadherin and induction of cellular phenotypic changes that are characteristic of the epithelial-to-mesenchymal transition. Cancer Research 2008, 68:5104-5112.
6. Arpino G., Generali D., Sapino A., Lucia del M., Frassoldati A., de Laurentis M., et al. Gene expression profiling in breast cancer: A clinical perspective. Breast 2013, 22:109-120.
7. Bakker W.J., Weijts B.G., Westendorp B., de Bruin A. HIF proteins connect the RB-E2F factors to angiogenesis. Transcription 2013, 4:62-66.
8. Baldewijns M.M., van Vlodrop I.J., Vermeulen P.B., Soetekouw P.M., van Engeland M., de Bruine A.P. VHL and HIF signalling in renal cell carcinogenesis. The Journal of Pathology 2010, 221:125-138.
9. Banerjee D., Gorlick R., Liefshitz A., Danenberg K., Danenberg P.C., Danenberg P.V., et al. Levels of E2F-1 expression are higher in lung metastasis of colon cancer as compared with hepatic metastasis and correlate with levels of thymidylate synthase. Cancer Research 2000, 60:2365-2367.
10. Banerjee D., Schnieders B., Fu J.Z., Adhikari D., Zhao S.C., Bertino J.R. Role of E2F-1 in chemosensitivity. Cancer Research 1998, 58:4292-4296.
11. Berger B., Capper D., Lemke D., Pfenning P.N., Platten M., Weller M., et al. Defective p53 antiangiogenic signaling in glioblastoma. Neuro-Oncology 2010, 12:894-907.
12. Bergers G., Benjamin L.E. Tumorigenesis and the angiogenic switch. Nature Reviews. Cancer 2003, 3:401-410.
13. Bergh G., Ehinger M., Olsson I., Jacobsen S.E., Gullberg U. Involvement of the retinoblastoma protein in monocytic and neutrophilic lineage commitment of human bone marrow progenitor cells. Blood 1999, 94:1971-1978.
14. Bidard F.C., Pierga J.Y., Soria J.C., Thiery J.P. Translating metastasis-related biomarkers to the clinic-Progress and pitfalls. Nature Reviews. Clinical Oncology 2013, 10:169-179.
15. Biyashev D., Qin G. E2F and microRNA regulation of angiogenesis. American Journal of Cardiovascular Disease 2011, 1:110-118.
16. Blanchet E., Annicotte J.S., Fajas L. Cell cycle regulators in the control of metabolism. Cell Cycle 2009, 8:4029-4031.
17. Blanchet E., Annicotte J.S., Lagarrigue S., Aguilar V., Clape C., Chavey C., et al. E2F transcription factor-1 regulates oxidative metabolism. Nature Cell Biology 2011, 13:1146-1152.
18. Blomen V.A., Boonstra J. Cell fate determination during G1 phase progression. Cellular and Molecular Life Sciences 2007, 64:3084-3104.
19. Boyer L.A., Lee T.I., Cole M.F., Johnstone S.E., Levine S.S., Zucker J.P., et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005, 122:947-956.
20. Budde A., Schneiderhan-Marra N., Petersen G., Brune B. Retinoblastoma susceptibility gene product pRB activates hypoxia-inducible factor-1 (HIF-1). Oncogene 2005, 24:1802-1808.
21. Burdon T., Chambers I., Stracey C., Niwa H., Smith A. Signaling mechanisms regulating self-renewal and differentiation of pluripotent embryonic stem cells. Cells, Tissues, Organs 1999, 165:131-143.
22. Burdon T., Smith A., Savatier P. Signalling, cell cycle and pluripotency in embryonic stem cells. Trends in Cell Biology 2002, 12:432-438.
23. Calo E., Quintero-Estades J.A., Danielian P.S., Nedelcu S., Berman S.D., Lees J.A. Rb regulates fate choice and lineage commitment in vivo. Nature 2010, 466:1110-1114.
24. Canel M., Serrels A., Frame M.C., Brunton V.G. E-cadherin-integrin crosstalk in cancer invasion and metastasis. Journal of Cell Science 2013, 126:393-401.
25. Chaffer C.L., Weinberg R.A. A perspective on cancer cell metastasis. Science 2011, 331:1559-1564.
26. Chavez L., Bais A.S., Vingron M., Lehrach H., Adjaye J., Herwig R. In silico identification of a core regulatory network of OCT4 in human embryonic stem cells using an integrated approach. BMC Genomics 2009, 10:314.
27. Chellappan S.P., Hiebert S., Mudryj M., Horowitz J.M., Nevins J.R. The E2F transcription factor is a cellular target for the RB protein. Cell 1991, 65:1053-1061.
28. Chen D., Opavsky R., Pacal M., Tanimoto N., Wenzel P., Seeliger M.W., et al. Rb-mediated neuronal differentiation through cell-cycle-independent regulation of E2f3a. PLoS Biology 2007, 5:e179.
29. Chen H.Z., Tsai S.Y., Leone G. Emerging roles of E2Fs in cancer: An exit from cell cycle control. Nature Reviews. Cancer 2009, 9:785-797.
30. Chiang A.C., Massague J. Molecular basis of metastasis. The New England Journal of Medicine 2008, 359:2814-2823.
31. Chong J.L., Wenzel P.L., Saenz-Robles M.T., Nair V., Ferrey A., Hagan J.P., et al. E2f1-3 switch from activators in progenitor cells to repressors in differentiating cells. Nature 2009, 462:930-934.
32. Clarke A.R., Maandag E.R., van Roon M., van der Lugt N.M., van der Valk M., Hooper M.L., et al. Requirement for a functional Rb-1 gene in murine development. Nature 1992, 359:328-330.
33. Claudio P.P., Stiegler P., Howard C.M., Bellan C., Minimo C., Tosi G.M., et al. RB2/p130 gene-enhanced expression down-regulates vascular endothelial growth factor expression and inhibits angiogenesis in vivo. Cancer Research 2001, 61:462-468.
34. Clem B.F., Chesney J. Molecular pathways: Regulation of metabolism by RB. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2012, 18:6096-6100.
35. Conklin J.F., Baker J., Sage J. The RB family is required for the self-renewal and survival of human embryonic stem cells. Nature Communications 2012, 3:1244.
36. Conklin J.F., Sage J. Keeping an eye on retinoblastoma control of human embryonic stem cells. Journal of Cellular Biochemistry 2009, 108:1023-1030.
37. Creighton C.J., Gibbons D.L., Kurie J.M. The role of epithelial-mesenchymal transition programming in invasion and metastasis: A clinical perspective. Cancer Management and Research 2013, 5:187-195.
38. Dali-Youcef N., Mataki C., Coste A., Messaddeq N., Giroud S., Blanc S., et al. Adipose tissue-specific inactivation of the retinoblastoma protein protects against diabesity because of increased energy expenditure. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:10703-10708.
39. Darville M.I., Antoine I.V., Mertens-Strijthagen J.R., Dupriez V.J., Rousseau G.G. An E2F-dependent late-serum-response promoter in a gene that controls glycolysis. Oncogene 1995, 11:1509-1517.
40. Dasgupta P., Sun J., Wang S., Fusaro G., Betts V., Padmanabhan J., et al. Disruption of the Rb-Raf-1 interaction inhibits tumor growth and angiogenesis. Molecular and Cellular Biology 2004, 24:9527-9541.
41. Davis R.K., Chellappan S. Disrupting the Rb-Raf-1 interaction: A potential therapeutic target for cancer. Drug News & Perspectives 2008, 21:331-335.
42. De Craene B., Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nature Reviews. Cancer 2013, 13:97-110.
43. DeGregori J., Johnson D.G. Distinct and overlapping roles for E2F family members in transcription, proliferation and apoptosis. Current Molecular Medicine 2006, 6:739-748.
44. Dick F.A., Rubin S.M. Molecular mechanisms underlying RB protein function. Nature Reviews. Molecular Cell Biology 2013, 14:297-306.
45. Di Fiore R., D'Anneo A., Tesoriere G., Vento R. RB1 in cancer: Different mechanisms of RB1 inactivation and alterations of pRb pathway in tumorigenesis. Journal of Cellular Physiology 2013, 228:1676-1687.
46. Enders G.H. Colon cancer metastasis: Is E2F-1 a driving force?. Cancer Biology & Therapy 2004, 3:400-401.
47. Engelmann D., Mayoli-Nussle D., Mayrhofer C., Furst K., Alla V., Stoll A., et al. E2F1 promotes angiogenesis through the VEGF-C/VEGFR-3 axis in a feedback loop for cooperative induction of PDGF-B. Journal of Molecular Cell Biology 2013, 5:391-403.
48. Fajas L., Annicotte J.S., Miard S., Sarruf D., Watanabe M., Auwerx J. Impaired pancreatic growth, beta cell mass, and beta cell function in E2F1 (-/-) mice. The Journal of Clinical Investigation 2004, 113:1288-1295.
49. Fajas L., Egler V., Reiter R., Hansen J., Kristiansen K., Debril M.B., et al. The retinoblastoma-histone deacetylase 3 complex inhibits PPARgamma and adipocyte differentiation. Developmental Cell 2002, 3:903-910.
50. Fajas L., Landsberg R.L., Huss-Garcia Y., Sardet C., Lees J.A., Auwerx J. E2Fs regulate adipocyte differentiation. Developmental Cell 2002, 3:39-49.
51. Farhang Ghahremani M., Goossens S., Nittner D., Bisteau X., Bartunkova S., Zwolinska A., et al. p53 promotes VEGF expression and angiogenesis in the absence of an intact p21-Rb pathway. Cell Death and Differentiation 2013, 20:888-897.
52. Fontemaggi G., Dell'Orso S., Trisciuoglio D., Shay T., Melucci E., Fazi F., et al. The execution of the transcriptional axis mutant p53, E2F1 and ID4 promotes tumor neo-angiogenesis. Nature Structural & Molecular Biology 2009, 16:1086-1093.
53. Fritz V., Fajas L. Metabolism and proliferation share common regulatory pathways in cancer cells. Oncogene 2010, 29:4369-4377.
54. Frolov M.V., Dyson N.J. Molecular mechanisms of E2F-dependent activation and pRB-mediated repression. Journal of Cell Science 2004, 117:2173-2181.
55. Fujiwara K., Yuwanita I., Hollern D.P., Andrechek E.R. Prediction and genetic demonstration of a role for activator E2Fs in Myc-induced tumors. Cancer Research 2011, 71:1924-1932.
56. Galderisi U., Cipollaro M., Giordano A. The retinoblastoma gene is involved in multiple aspects of stem cell biology. Oncogene 2006, 25:5250-5256.
57. Gauthier M.L., Berman H.K., Miller C., Kozakeiwicz K., Chew K., Moore D., et al. Abrogated response to cellular stress identifies DCIS associated with subsequent tumor events and defines basal-like breast tumors. Cancer Cell 2007, 12:479-491.
58. Giannakakis A., Sandaltzopoulos R., Greshock J., Liang S., Huang J., Hasegawa K., et al. miR-210 links hypoxia with cell cycle regulation and is deleted in human epithelial ovarian cancer. Cancer Biology & Therapy 2008, 7:255-264.
59. Gonzalez-Gonzalez M., Garcia J.G., Montero J.A., Fernandez L.M., Bengoechea O., Munez O.B., et al. Genomics and proteomics approaches for biomarker discovery in sporadic colorectal cancer with metastasis. Cancer Genomics & Proteomics 2013, 10:19-25.
60. Gorlick R., Metzger R., Danenberg K.D., Salonga D., Miles J.S., Longo G.S., et al. Higher levels of thymidylate synthase gene expression are observed in pulmonary as compared with hepatic metastases of colorectal adenocarcinoma. Journal of Clinical Oncology 1998, 16:1465-1469.
61. Gunaratne P.H. Embryonic stem cell microRNAs: Defining factors in induced pluripotent (iPS) and cancer (CSC) stem cells?. Current Stem Cell Research & Therapy 2009, 4:168-177.
62. Han T., Kang D., Ji D., Wang X., Zhan W., Fu M., et al. How does cancer cell metabolism affect tumor migration and invasion?. Cell Adhesion & Migration 2013, 7:395-403.
63. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
64. Hanahan D., Weinberg R.A. Hallmarks of cancer: The next generation. Cell 2011, 144:646-674.
65. Hao J., Zhao S., Zhang Y., Zhao Z., Ye R., Wen J., et al. Emerging role of microRNAs in cancer and cancer stem cells. Journal of Cellular Biochemistry 2014, 115:605-610.
66. Hiebert S.W., Chellappan S.P., Horowitz J.M., Nevins J.R. The interaction of RB with E2F coincides with an inhibition of the transcriptional activity of E2F. Genes & Development 1992, 6:177-185.
67. Ho G.H., Calvano J.E., Bisogna M., Van Zee K.J. Expression of E2F-1 and E2F-4 is reduced in primary and metastatic breast carcinomas. Breast Cancer Research and Treatment 2001, 69:115-122.
68. Hood J.D., Cheresh D.A. Targeted delivery of mutant Raf kinase to neovessels causes tumor regression. Cold Spring Harbor Symposia on Quantitative Biology 2002, 67:285-291.
69. Horm T.M., Schroeder J.A. MUC1 and metastatic cancer: Expression, function and therapeutic targeting. Cell Adhesion & Migration 2013, 7:187-198.
70. Hsieh M.C., Das D., Sambandam N., Zhang M.Q., Nahle Z. Regulation of the PDK4 isozyme by the Rb-E2F1 complex. The Journal of Biological Chemistry 2008, 283:27410-27417.
71. Hudson B.D., Kulp K.S., Loots G.G. Prostate cancer invasion and metastasis: Insights from mining genomic data. Briefings in Functional Genomics 2013, 12:397-410.
72. Hui A.M., Li X., Makuuchi M., Takayama T., Kubota K. Over-expression and lack of retinoblastoma protein are associated with tumor progression and metastasis in hepatocellular carcinoma. International Journal of Cancer 1999, 84:604-608.
73. Iavarone A., Garg P., Lasorella A., Hsu J., Israel M.A. The helix-loop-helix protein Id-2 enhances cell proliferation and binds to the retinoblastoma protein. Genes & Development 1994, 8:1270-1284.
74. Indovina P., Marcelli E., Casini N., Rizzo V., Giordano A. Emerging roles of RB family: New defense mechanisms against tumor progression. Journal of Cellular Physiology 2013, 228:525-535.
75. Iwamoto M., Banerjee D., Menon L.G., Jurkiewicz A., Rao P.H., Kemeny N.E., et al. Overexpression of E2F-1 in lung and liver metastases of human colon cancer is associated with gene amplification. Cancer Biology & Therapy 2004, 3:395-399.
76. Jacks T., Fazeli A., Schmitt E.M., Bronson R.T., Goodell M.A., Weinberg R.A. Effects of an Rb mutation in the mouse. Nature 1992, 359:295-300.
77. Jang M., Kim S.S., Lee J. Cancer cell metabolism: Implications for therapeutic targets. Experimental & Molecular Medicine 2013, 45:e45.
78. Ji W., Zhang W., Xiao W. E2F-1 directly regulates thrombospondin 1 expression. PLoS One 2010, 5:e13442.
79. Johnson J.L., Pillai S., Pernazza D., Sebti S.M., Lawrence N.J., Chellappan S.P. Regulation of matrix metalloproteinase genes by E2F transcription factors: Rb-Raf-1 interaction as a novel target for metastatic disease. Cancer Research 2012, 72:516-526.
80. Joshi B., Ordonez-Ercan D., Dasgupta P., Chellappan S. Induction of human metallothionein 1G promoter by VEGF and heavy metals: Differential involvement of E2F and metal transcription factors. Oncogene 2005, 24:2204-2217.
81. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. The Journal of Clinical Investigation 2009, 119:1420-1428.
82. Kanai M., Tashiro E., Maruki H., Minato Y., Imoto M. Transcriptional regulation of human fibroblast growth factor receptor 1 by E2F-1. Gene 2009, 438:49-56.
83. Kim Y.C., Kim S.Y., Mellado-Gil J.M., Yadav H., Neidermyer W., Kamaraju A.K., et al. RB regulates pancreas development by stabilizing Pdx1. The EMBO Journal 2011, 30:1563-1576.
84. Kinkade R., Dasgupta P., Carie A., Pernazza D., Carless M., Pillai S., et al. A small molecule disruptor of Rb/Raf-1 interaction inhibits cell proliferation, angiogenesis, and growth of human tumor xenografts in nude mice. Cancer Research 2008, 68:3810-3818.
85. Labrecque M.P., Prefontaine G.G., Beischlag T.V. The aryl hydrocarbon receptor nuclear translocator (ARNT) family of proteins: Transcriptional modifiers with multi-functional protein interfaces. Current Molecular Medicine 2013, 13:1047-1065.
86. Lammens T., Li J., Leone G., De Veylder L. Atypical E2Fs: New players in the E2F transcription factor family. Trends in Cell Biology 2009, 19:111-118.
87. Lasorella A., Rothschild G., Yokota Y., Russell R.G., Iavarone A. Id2 mediates tumor initiation, proliferation, and angiogenesis in Rb mutant mice. Molecular and Cellular Biology 2005, 25:3563-3574.
88. Lee B.K., Bhinge A.A., Iyer V.R. Wide-ranging functions of E2F4 in transcriptional activation and repression revealed by genome-wide analysis. Nucleic Acids Research 2011, 39:3558-3573.
89. Lee E.Y., Chang C.Y., Hu N., Wang Y.C., Lai C.C., Herrup K., et al. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 1992, 359:288-294.
90. Lee E.Y., Hu N., Yuan S.S., Cox L.A., Bradley A., Lee W.H., et al. Dual roles of the retinoblastoma protein in cell cycle regulation and neuron differentiation. Genes & Development 1994, 8:2008-2021.
91. Li F.Q., Coonrod A., Horwitz M. Selection of a dominant negative retinoblastoma protein (RB) inhibiting satellite myoblast differentiation implies an indirect interaction between MyoD and RB. Molecular and Cellular Biology 2000, 20:5129-5139.
92. Li J., Ran C., Li E., Gordon F., Comstock G., Siddiqui H., et al. Synergistic function of E2F7 and E2F8 is essential for cell survival and embryonic development. Developmental Cell 2008, 14:62-75.
93. Li G.C., Wang Z.Y. Constitutive expression of RbAp46 induces epithelial-mesenchymal transition in mammary epithelial cells. Anticancer Research 2006, 26:3555-3560.
94. Liu Y., Sanchez-Tillo E., Lu X., Huang L., Clem B., Telang S., et al. Sequential inductions of the ZEB1 transcription factor caused by mutation of Rb and then Ras proteins are required for tumor initiation and progression. The Journal of Biological Chemistry 2013, 288:11572-11580.
95. Ma Y., Kurtyka C.A., Boyapalle S., Sung S.S., Lawrence H., Guida W., et al. A small-molecule E2F inhibitor blocks growth in a melanoma culture model. Cancer Research 2008, 68:6292-6299.
96. Merdzhanova G., Gout S., Keramidas M., Edmond V., Coll J.L., Brambilla C., et al. The transcription factor E2F1 and the SR protein SC35 control the ratio of pro-angiogenic versus antiangiogenic isoforms of vascular endothelial growth factor-A to inhibit neovascularization in vivo. Oncogene 2010, 29:5392-5403.
97. Minato Y., Tashiro E., Kanai M., Nihei Y., Kodama Y., Imoto M. Transcriptional regulation of a new variant of human platelet-derived growth factor receptor alpha transcript by E2F-1. Gene 2007, 403:89-97.
98. Miyashita H., Sato Y. Metallothionein 1 is a downstream target of vascular endothelial zinc finger 1 (VEZF1) in endothelial cells and participates in the regulation of angiogenesis. Endothelium 2005, 12:163-170.
99. Morris E.J., Dyson N.J. Retinoblastoma protein partners. Advances in Cancer Research 2001, 82:1-54.
100. Nag S., Qin J., Srivenugopal K.S., Wang M., Zhang R. The MDM2-p53 pathway revisited. Journal of Biomedical Research 2013, 27:254-271.
101. Nelson M.A., Reynolds S.H., Rao U.N., Goulet A.C., Feng Y., Beas A., et al. Increased gene copy number of the transcription factor E2F1 in malignant melanoma. Cancer Biology & Therapy 2006, 5:407-412.
102. Nevins J.R. The Rb/E2F pathway and cancer. Human Molecular Genetics 2001, 10:699-703.
103. Nicolay B.N., Dyson N.J. The multiple connections between pRB and cell metabolism. Current Opinion in Cell Biology 2013, 25:735-740.
104. Nicolay B.N., Gameiro P.A., Tschop K., Korenjak M., Heilmann A.M., Asara J.M., et al. Loss of RBF1 changes glutamine catabolism. Genes & Development 2013, 27:182-196.
105. Novitch B.G., Mulligan G.J., Jacks T., Lassar A.B. Skeletal muscle cells lacking the retinoblastoma protein display defects in muscle gene expression and accumulate in S and G2 phases of the cell cycle. The Journal of Cell Biology 1996, 135:441-456.
106. Nowak K., Kerl K., Fehr D., Kramps C., Gessner C., Killmer K., et al. BMI1 is a target gene of E2F-1 and is strongly expressed in primary neuroblastomas. Nucleic acids research 2006, 34:1745-1754.
107. Papadimou E., Menard C., Grey C., Puceat M. Interplay between the retinoblastoma protein and LEK1 specifies stem cells toward the cardiac lineage. The EMBO Journal 2005, 24:1750-1761.
108. Perk J., Iavarone A., Benezra R. Id family of helix-loop-helix proteins in cancer. Nature Reviews. Cancer 2005, 5:603-614.
109. Perlikos F., Harrington K.J., Syrigos K.N. Key molecular mechanisms in lung cancer invasion and metastasis: A comprehensive review. Critical Reviews in Oncology/Hematology 2013, 87:1-11.
110. Pickard A., Cichon A.C., Barry A., Kieran D., Patel D., Hamilton P., et al. Inactivation of Rb in stromal fibroblasts promotes epithelial cell invasion. The EMBO Journal 2012, 31:3092-3103.
111. Pillai S., Kovacs M., Chellappan S. Regulation of vascular endothelial growth factor receptors by Rb and E2F1: Role of acetylation. Cancer Research 2010, 70:4931-4940.
112. Proulx S.T., Detmar M. Molecular mechanisms and imaging of lymphatic metastasis. Experimental Cell Research 2013, 319:1611-1617.
113. Qin G., Kishore R., Dolan C.M., Silver M., Wecker A., Luedemann C.N., et al. Cell cycle regulator E2F1 modulates angiogenesis via p53-dependent transcriptional control of VEGF. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:11015-11020.
114. Rakha E.A., Pinder S.E., Paish E.C., Robertson J.F., Ellis I.O. Expression of E2F-4 in invasive breast carcinomas is associated with poor prognosis. The Journal of Pathology 2004, 203:754-761.
115. Ruzinova M.B., Benezra R. Id proteins in development, cell cycle and cancer. Trends in Cell Biology 2003, 13:410-418.
116. Sage J. The retinoblastoma tumor suppressor and stem cell biology. Genes & Development 2012, 26:1409-1420.
117. Salon C., Merdzhanova G., Brambilla C., Brambilla E., Gazzeri S., Eymin B. E2F-1, Skp2 and cyclin E oncoproteins are upregulated and directly correlated in high-grade neuroendocrine lung tumors. Oncogene 2007, 26:6927-6936.
118. Saxena M., Christofori G. Rebuilding cancer metastasis in the mouse. Molecular Oncology 2013, 7:283-296.
119. Schaffer B.E., Park K.S., Yiu G., Conklin J.F., Lin C., Burkhart D.L., et al. Loss of p130 accelerates tumor development in a mouse model for human small-cell lung carcinoma. Cancer Research 2010, 70:3877-3883.
120. Scheel C., Weinberg R.A. Cancer stem cells and epithelial-mesenchymal transition: Concepts and molecular links. Seminars in Cancer Biology 2012, 22:396-403.
121. Schlisio S., Halperin T., Vidal M., Nevins J.R. Interaction of YY1 with E2Fs, mediated by RYBP, provides a mechanism for specificity of E2F function. The EMBO Journal 2002, 21:5775-5786.
122. Schoeftner S., Scarola M., Comisso E., Schneider C., Benetti R. An Oct4-pRb axis, controlled by MiR-335, integrates stem cell self-renewal and cell cycle control. Stem Cells 2013, 31:717-728.
123. Schreiber C., Vormbrock K., Ziebold U. Genes involved in the metastatic cascade of medullary thyroid tumours. Methods in Molecular Biology 2012, 878:217-228.
124. Semenza G.L. Hypoxia-inducible factor 1 and cancer pathogenesis. IUBMB Life 2008, 60:591-597.
125. Shen G., Li X., Jia Y.F., Piazza G.A., Xi Y. Hypoxia-regulated microRNAs in human cancer. Acta Pharmacologica Sinica 2013, 34:336-341.
126. Sherr C.J., McCormick F. The RB and p53 pathways in cancer. Cancer Cell 2002, 2:103-112.
127. Siegel R., Naishadham D., Jemal A. Cancer statistics, 2013. CA: A Cancer Journal for Clinicians 2013, 63:11-30.
128. Singh B., Berry J.A., Shoher A., Ramakrishnan V., Lucci A. COX-2 overexpression increases motility and invasion of breast cancer cells. International Journal of Oncology 2005, 26:1393-1399.
129. Singh S., Johnson J., Chellappan S. Small molecule regulators of Rb-E2F pathway as modulators of transcription. Biochimica et Biophysica Acta 2010, 1799:788-794.
130. Stanelle J., Stiewe T., Theseling C.C., Peter M., Putzer B.M. Gene expression changes in response to E2F1 activation. Nucleic Acids Research 2002, 30:1859-1867.
131. Takahashi C., Sasaki N., Kitajima S. Twists in views on RB functions in cellular signaling, metabolism and stem cells. Cancer Science 2012, 103:1182-1188.
132. Tashiro E., Minato Y., Maruki H., Asagiri M., Imoto M. Regulation of FGF receptor-2 expression by transcription factor E2F-1. Oncogene 2003, 22:5630-5635.
133. Teng Y.C., Lee C.F., Li Y.S., Chen Y.R., Hsiao P.W., Chan M.Y., et al. Histone demethylase RBP2 promotes lung tumorigenesis and cancer metastasis. Cancer Research 2013, 73:4711-4721.
134. Teodoro J.G., Evans S.K., Green M.R. Inhibition of tumor angiogenesis by p53: A new role for the guardian of the genome. Journal of Molecular Medicine 2007, 85:1175-1186.
135. Thomassen M., Tan Q., Kruse T.A. Gene expression meta-analysis identifies metastatic pathways and transcription factors in breast cancer. BMC Cancer 2008, 8:394.
136. Toma J.G., El-Bizri H., Barnabe-Heider F., Aloyz R., Miller F.D. Evidence that helix-loop-helix proteins collaborate with retinoblastoma tumor suppressor protein to regulate cortical neurogenesis. The Journal of Neuroscience 2000, 20:7648-7656.
137. Trimarchi J.M., Lees J.A. Sibling rivalry in the E2F family. Nature Reviews. Molecular Cell Biology 2002, 3:11-20.
138. Tsai J.H., Yang J. Epithelial-mesenchymal plasticity in carcinoma metastasis. Genes & Development 2013, 27:2192-2206.
139. Tsujii M., Kawano S., DuBois R.N. Cyclooxygenase-2 expression in human colon cancer cells increases metastatic potential. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:3336-3340.
140. Valastyan S., Weinberg R.A. Tumor metastasis: Molecular insights and evolving paradigms. Cell 2011, 147:275-292.
141. Viatour P., Somervaille T.C., Venkatasubrahmanyam S., Kogan S., McLaughlin M.E., Weissman I.L., et al. Hematopoietic stem cell quiescence is maintained by compound contributions of the retinoblastoma gene family. Cell Stem Cell 2008, 3:416-428.
142. Visvader J.E., Lindeman G.J. Cancer stem cells in solid tumours: Accumulating evidence and unresolved questions. Nature Reviews. Cancer 2008, 8:755-768.
143. Visvader J.E., Lindeman G.J. Cancer stem cells: Current status and evolving complexities. Cell Stem Cell 2012, 10:717-728.
144. Wang K.C., Garmire L.X., Young A., Nguyen P., Trinh A., Subramaniam S., et al. Role of microRNA-23b in flow-regulation of Rb phosphorylation and endothelial cell growth. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:3234-3239.
145. Wang S., Ghosh R.N., Chellappan S.P. Raf-1 physically interacts with Rb and regulates its function: A link between mitogenic signaling and cell cycle regulation. Molecular and Cellular Biology 1998, 18:7487-7498.
146. Wang S., Nath N., Adlam M., Chellappan S. Prohibitin, a potential tumor suppressor, interacts with RB and regulates E2F function. Oncogene 1999, 18:3501-3510.
147. Wang S., Nath N., Fusaro G., Chellappan S. Rb and prohibitin target distinct regions of E2F1 for repression and respond to different upstream signals. Molecular and Cellular Biology 1999, 19:7447-7460.
148. Wang H., Scott R.E. Inhibition of distinct steps in the adipocyte differentiation pathway in 3T3T mesenchymal stem cells by dimethyl sulphoxide (DMSO). Cell Proliferation 1993, 26:55-66.
149. Weijts B.G., Bakker W.J., Cornelissen P.W., Liang K.H., Schaftenaar F.H., Westendorp B., et al. E2F7 and E2F8 promote angiogenesis through transcriptional activation of VEGFA in cooperation with HIF1. The EMBO Journal 2012, 31:3871-3884.
150. Wenzel P.L., Wu L., de Bruin A., Chong J.L., Chen W.Y., Dureska G., et al. Rb is critical in a mammalian tissue stem cell population. Genes & Development 2007, 21:85-97.
151. Yamanaka S. Ekiden to iPS Cells. Nature Medicine 2009, 15:1145-1148.
152. Yasui W., Naka K., Suzuki T., Fujimoto J., Hayashi K., Matsutani N., et al. Expression of p27Kip1, cyclin E and E2F-1 in primary and metastatic tumors of gastric carcinoma. Oncology Reports 1999, 6:983-987.
153. Yoon S.O., Shin S., Mercurio A.M. Ras stimulation of E2F activity and a consequent E2F regulation of integrin alpha6beta4 promote the invasion of breast carcinoma cells. Cancer Research 2006, 66:6288-6295.
154. Zbinden S., Wang J., Adenika R., Schmidt M., Tilan J.U., Najafi A.H., et al. Metallothionein enhances angiogenesis and arteriogenesis by modulating smooth muscle cell and macrophage function. Arteriosclerosis, Thrombosis, and Vascular Biology 2010, 30:477-482.
155. Zhang S.Y., Liu S.C., Johnson D.G., Klein-Szanto A.J. E2F-1 gene transfer enhances invasiveness of human head and neck carcinoma cell lines. Cancer Research 2000, 60:5972-5976.
156. Zhang X., Neganova I., Przyborski S., Yang C., Cooke M., Atkinson S.P., et al. A role for NANOG in G1 to S transition in human embryonic stem cells through direct binding of CDK6 and CDC25A. The Journal of Cell Biology 2009, 184:67-82.
157. Zhou W., Srinivasan S., Nawaz Z., Slingerland J.M. ERalpha, SKP2 and E2F-1 form a feed forward loop driving late ERalpha targets and G1 cell cycle progression. Oncogene 2013, 192:1-13.
158. Ziebold U., Lee E.Y., Bronson R.T., Lees J.A. E2F3 loss has opposing effects on different pRB-deficient tumors, resulting in suppression of pituitary tumors but metastasis of medullary thyroid carcinomas. Molecular and Cellular Biology 2003, 23:6542-6552.