Yin Yang 1 is associated with cancer stem cell transcription factors (SOX2, OCT4, BMI1) and clinical implication

Journal of Experimental and Clinical Cancer Research

Volumn 35, Issue 1, 2016, Pages

  Kaufhold, Samantha ^a   Garbán, Hermes ^b   Bonavida, Benjamin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

BMI1; Cancer stem cells; NANOG; OCT4; SOX2; Yin Yang 1

Indexed keywords

BMI1 PROTEIN; CISPLATIN; DOCETAXEL; GEMCITABINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; PACLITAXEL; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR YIN YANG 1; UNCLASSIFIED DRUG; BMI1 PROTEIN, HUMAN; POU5F1 PROTEIN, HUMAN; SOX2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX; TRANSCRIPTION FACTOR YY1; YY1 PROTEIN, HUMAN;

BINDING SITE; BREAST CANCER; CANCER STEM CELL; CARCINOGENESIS; CELL PROLIFERATION; CELL SELF-RENEWAL; CELL VIABILITY; COLORECTAL CANCER; DOWNSTREAM PROCESSING; ENDOMETRIUM CANCER; EPITHELIAL MESENCHYMAL TRANSITION; GENE PRODUCT; GLIOMA; HEMATOLOGIC MALIGNANCY; HUMAN; IMMUNITY; KIDNEY CANCER; LIVER CANCER; LUNG CANCER; LYMPHOMA; MELANOMA; METASTASIS; OVARY CANCER; PANCREAS CANCER; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEOMICS; REVIEW; SKIN CANCER; SOLID TUMOR; STOMACH CANCER; TESTIS CANCER; TRANSITIONAL CELL CARCINOMA; UTERINE CERVIX CANCER; ANIMAL; DATA MINING; GENE EXPRESSION REGULATION; METABOLISM; NEOPLASM; PROCEDURES; SIGNAL TRANSDUCTION;

ANIMALS; DATA MINING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASMS; NEOPLASTIC STEM CELLS; OCTAMER TRANSCRIPTION FACTOR-3; POLYCOMB REPRESSIVE COMPLEX 1; PROTEOMICS; SIGNAL TRANSDUCTION; SOXB1 TRANSCRIPTION FACTORS; YY1 TRANSCRIPTION FACTOR;

EID: 84971349323     PISSN: None     EISSN: 17569966     Source Type: Journal    
DOI: 10.1186/s13046-016-0359-2     Document Type: Review

References (141)

1. Zhou BB, Zhang H, Damelin M, Geles KG, Grindley JC, Dirks PB. Tumour-initiating cells: challenges and opportunities for anticancer drug discovery. Nat Rev Drug Discov. 2009;8(10):806-23.
2. Lobo NA, Shimono Y, Qian D, Clarke MF. The biology of cancer stem cells. Annu Rev Cell Dev Biol. 2007;23:675-99.
3. 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):704-15.
4. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer. 2009;9(4):265-73.
5. Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 2014;42(Database issue):D199-205.
6. HUGO Gene Nomenclature Committee (HGNC). http://www.genenames.org.
7. Entrez Gene [ http://www.ncbi.nlm.nih.gov/gene ]
8. Uniprot [ http://www.uniprot.org ]
9. Stevanovic M, Zuffardi O, Collignon J, Lovell-Badge R, Goodfellow P. The cDNA sequence and chromosomal location of the human SOX2 gene. Mamm Genome. 1994;5(10):640-2.
10. Weina K, Utikal J. SOX2 and cancer: current research and its implications in the clinic. Clin Transl Med. 2014;3:19.
11. Thiel G. How Sox2 maintains neural stem cell identity. Biochem J. 2013;450(3):e1-2.
12. Hassiotou F, Beltran A, Chetwynd E, Stuebe AM, Twigger AJ, Metzger P, Trengove N, Lai CT, Filgueira L, Blancafort P, et al. Breastmilk is a novel source of stem cells with multilineage differentiation potential. Stem Cells. 2012;30(10):2164-74.
13. Sherwood RI, Chen TY, Melton DA. Transcriptional dynamics of endodermal organ formation. Dev Dyn. 2009;238(1):29-42.
14. Guzel E, Karatas OF, Duz MB, Solak M, Ittmann M, Ozen M. Differential expression of stem cell markers and ABCG2 in recurrent prostate cancer. Prostate. 2014;74(15):1498-505.
15. Lee SH, Oh SY, Do SI, Lee HJ, Kang HJ, Rho YS, Bae WJ, Lim YC. SOX2 regulates self-renewal and tumorigenicity of stem-like cells of head and neck squamous cell carcinoma. Br J Cancer. 2014;111(11):2122-30.
16. Schoenhals M, Kassambara A, De Vos J, Hose D, Moreaux J, Klein B. Embryonic stem cell markers expression in cancers. Biochem Biophys Res Commun. 2009;383(2):157-62.
17. Hussenet T, Dali S, Exinger J, Monga B, Jost B, Dembele D, Martinet N, Thibault C, Huelsken J, Brambilla E, et al. SOX2 is an oncogene activated by recurrent 3q26.3 amplifications in human lung squamous cell carcinomas. PLoS ONE. 2010;5(1):e8960.
18. Albertson DG. Gene amplification in cancer. Trends Genet. 2006;22(8):447-55.
19. Annovazzi L, Mellai M, Caldera V, Valente G, Schiffer D. SOX2 expression and amplification in gliomas and glioma cell lines. Cancer Genomics Proteomics. 2011;8(3):139-47.
20. Alonso MM, Diez-Valle R, Manterola L, Rubio A, Liu D, Cortes-Santiago N, Urquiza L, Jauregi P, Lopez de Munain A, Sampron N, et al. Genetic and epigenetic modifications of Sox2 contribute to the invasive phenotype of malignant gliomas. PLoS ONE. 2011;6(11), e26740.
21. Bass AJ, Watanabe H, Mermel CH, Yu S, Perner S, Verhaak RG, Kim SY, Wardwell L, Tamayo P, Gat-Viks I, et al. SOX2 is an amplified lineage-survival oncogene in lung and esophageal squamous cell carcinomas. Nat Genet. 2009;41(11):1238-42.
22. Maier S, Wilbertz T, Braun M, Scheble V, Reischl M, Mikut R, Menon R, Nikolov P, Petersen K, Beschorner C, et al. SOX2 amplification is a common event in squamous cell carcinomas of different organ sites. Hum Pathol. 2011;42(8):1078-88.
23. Rudin CM, Durinck S, Stawiski EW, Poirier JT, Modrusan Z, Shames DS, Bergbower EA, Guan Y, Shin J, Guillory J, et al. Comprehensive genomic analysis identifies SOX2 as a frequently amplified gene in small-cell lung cancer. Nat Genet. 2012;44(10):1111-6.
24. Freier K, Knoepfle K, Flechtenmacher C, Pungs S, Devens F, Toedt G, Hofele C, Joos S, Lichter P, Radlwimmer B. Recurrent copy number gain of transcription factor SOX2 and corresponding high protein expression in oral squamous cell carcinoma. Genes Chromosomes Cancer. 2010;49(1):9-16.
25. Justilien V, Walsh MP, Ali SA, Thompson EA, Murray NR, Fields AP. The PRKCI and SOX2 oncogenes are coamplified and cooperate to activate Hedgehog signaling in lung squamous cell carcinoma. Cancer Cell. 2014;25(2):139-51.
26. Mansukhani A, Ambrosetti D, Holmes G, Cornivelli L, Basilico C. Sox2 induction by FGF and FGFR2 activating mutations inhibits Wnt signaling and osteoblast differentiation. J Cell Biol. 2005;168(7):1065-76.
27. Herreros-Villanueva M, Zhang JS, Koenig A, Abel EV, Smyrk TC, Bamlet WR, de Narvajas AA, Gomez TS, Simeone DM, Bujanda L, et al. SOX2 promotes dedifferentiation and imparts stem cell-like features to pancreatic cancer cells. Oncogenesis. 2013;2, e61.
28. Fang WT, Fan CC, Li SM, Jang TH, Lin HP, Shih NY, Chen CH, Wang TY, Huang SF, Lee AY, et al. Downregulation of a putative tumor suppressor BMP4 by SOX2 promotes growth of lung squamous cell carcinoma. Int J Cancer. 2014;135(4):809-19.
29. Gangemi RM, Griffero F, Marubbi D, Perera M, Capra MC, Malatesta P, Ravetti GL, Zona GL, Daga A, Corte G. SOX2 silencing in glioblastoma tumor-initiating cells causes stop of proliferation and loss of tumorigenicity. Stem Cells. 2009;27(1):40-8.
30. Stolzenburg S, Rots MG, Beltran AS, Rivenbark AG, Yuan X, Qian H, Strahl BD, Blancafort P. Targeted silencing of the oncogenic transcription factor SOX2 in breast cancer. Nucleic Acids Res. 2012;40(14):6725-40.
31. Ji J, Zheng PS. Expression of Sox2 in human cervical carcinogenesis. Hum Pathol. 2010;41(10):1438-47.
32. Jia X, Li X, Xu Y, Zhang S, Mou W, Liu Y, Liu Y, Lv D, Liu CH, Tan X, et al. SOX2 promotes tumorigenesis and increases the anti-apoptotic property of human prostate cancer cell. J Mol Cell Biol. 2011;3(4):230-8.
33. Hutz K, Mejias-Luque R, Farsakova K, Ogris M, Krebs S, Anton M, Vieth M, Schuller U, Schneider MR, Blum H, et al. The stem cell factor SOX2 regulates the tumorigenic potential in human gastric cancer cells. Carcinogenesis. 2014;35(4):942-50.
34. Chen S, Li X, Lu D, Xu Y, Mou W, Wang L, Chen Y, Liu Y, Li X, Li LY, et al. SOX2 regulates apoptosis through MAP4K4-survivin signaling pathway in human lung cancer cells. Carcinogenesis. 2014;35(3):613-23.
35. Han X, Fang X, Lou X, Hua D, Ding W, Foltz G, Hood L, Yuan Y, Lin B. Silencing SOX2 induced mesenchymal-epithelial transition and its expression predicts liver and lymph node metastasis of CRC patients. PLoS ONE. 2012;7(8), e41335.
36. Sun C, Sun L, Li Y, Kang X, Zhang S, Liu Y. Sox2 expression predicts poor survival of hepatocellular carcinoma patients and it promotes liver cancer cell invasion by activating Slug. Med Oncol. 2013;30(2):503.
37. Girouard SD, Laga AC, Mihm MC, Scolyer RA, Thompson JF, Zhan Q, Widlund HR, Lee CW, Murphy GF. SOX2 contributes to melanoma cell invasion. Lab Invest. 2012;92(3):362-70.
38. Lou X, Han X, Jin C, Tian W, Yu W, Ding D, Cheng L, Huang B, Jiang H, Lin B. SOX2 targets fibronectin 1 to promote cell migration and invasion in ovarian cancer: new molecular leads for therapeutic intervention. OMICS. 2013;17(10):510-8.
39. Yang N, Hui L, Wang Y, Yang H, Jiang X. SOX2 promotes the migration and invasion of laryngeal cancer cells by induction of MMP-2 via the PI3K/Akt/mTOR pathway. Oncol Rep. 2014;31(6):2651-9.
40. Sussman RT, Stanek TJ, Esteso P, Gearhart JD, Knudsen KE, McMahon SB. The epigenetic modifier ubiquitin-specific protease 22 (USP22) regulates embryonic stem cell differentiation via transcriptional repression of sex-determining region Y-box 2 (SOX2). J Biol Chem. 2013;288(33):24234-46.
41. Rybak AP, Tang D. SOX2 plays a critical role in EGFR-mediated self-renewal of human prostate cancer stem-like cells. Cell Signal. 2013;25(12):2734-42.
42. 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):248-58.
43. Santini R, Pietrobono S, Pandolfi S, Montagnani V, D'Amico M, Penachioni JY, Vinci MC, Borgognoni L, Stecca B. SOX2 regulates self-renewal and tumorigenicity of human melanoma-initiating cells. Oncogene. 2014;33(38):4697-708.
44. Li D, Zhao LN, Zheng XL, Lin P, Lin F, Li Y, Zou HF, Cui RJ, Chen H, Yu XG. Sox2 is involved in paclitaxel resistance of the prostate cancer cell line PC-3 via the PI3K/Akt pathway. Mol Med Rep. 2014;10(6):3169-76.
45. Li Y, Chen K, Li L, Li R, Zhang J, Ren W. Overexpression of SOX2 is involved in paclitaxel resistance of ovarian cancer via the PI3K/Akt pathway. Tumour Biol. 2015.
46. Yang S, Zheng J, Xiao X, Xu T, Tang W, Zhu H, Yang L, Zheng S, Dong K, Zhou G, et al. SOX2 promotes tumorigenicity and inhibits the differentiation of I-type neuroblastoma cells. Int J Oncol. 2015;46(1):317-23.
47. Wang Q, He W, Lu C, Wang Z, Wang J, Giercksky KE, Nesland JM, Suo Z. Oct3/4 and Sox2 are significantly associated with an unfavorable clinical outcome in human esophageal squamous cell carcinoma. Anticancer Res. 2009;29(4):1233-41.
48. Toschi L, Finocchiaro G, Nguyen TT, Skokan MC, Giordano L, Gianoncelli L, Perrino M, Siracusano L, Di Tommaso L, Infante M, et al. Increased SOX2 gene copy number is associated with FGFR1 and PIK3CA gene gain in non-small cell lung cancer and predicts improved survival in early stage disease. PLoS ONE. 2014;9(4), e95303.
49. Wilbertz T, Wagner P, Petersen K, Stiedl AC, Scheble VJ, Maier S, Reischl M, Mikut R, Altorki NK, Moch H, et al. SOX2 gene amplification and protein overexpression are associated with better outcome in squamous cell lung cancer. Mod Pathol. 2011;24(7):944-53.
50. Dogan I, Kawabata S, Bergbower E, Gills JJ, Ekmekci A, Wilson W, 3rd, Rudin CM, Dennis PA. SOX2 expression is an early event in a murine model of EGFR mutant lung cancer and promotes proliferation of a subset of EGFR mutant lung adenocarcinoma cell lines. Lung Cancer. 2014;85(1):1-6.
51. Chen Y, Huang Y, Huang Y, Chen J, Wang S, Zhou J. The prognostic value of SOX2 expression in non-small cell lung cancer: a meta-analysis. PLoS ONE. 2013;8(8), e71140.
52. Velcheti V, Schalper K, Yao X, Cheng H, Kocoglu M, Dhodapkar K, Deng Y, Gettinger S, Rimm DL. High SOX2 levels predict better outcome in non-small cell lung carcinomas. PLoS ONE. 2013;8(4), e61427.
53. Dhodapkar KM, Gettinger SN, Das R, Zebroski H, Dhodapkar MV. SOX2-specific adaptive immunity and response to immunotherapy in non-small cell lung cancer. Oncoimmunology. 2013;2(7), e25205.
54. Niu CS, Li DX, Liu YH, Fu XM, Tang SF, Li J. Expression of NANOG in human gliomas and its relationship with undifferentiated glioma cells. Oncol Rep. 2011;26(3):593-601.
55. Ensemble [ http://uswest.ensembl.org/index.html ]
56. RefSeq [ http://www.ncbi.nlm.nih.gov/nuccore?LinkName=gene-nuccore-refseqrna&from-uid=5460 ]
57. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, Scholer H, Smith A. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell. 1998;95(3):379-91.
58. Scholer HR, Ciesiolka T, Gruss P. A nexus between Oct-4 and E1A: implications for gene regulation in embryonic stem cells. Cell. 1991;66(2):291-304.
59. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell. 2005;122(6):947-56.
60. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang W, Jiang J, et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell. 2008;133(6):1106-17.
61. Ambrosetti DC, Scholer HR, Dailey L, Basilico C. Modulation of the activity of multiple transcriptional activation domains by the DNA binding domains mediates the synergistic action of Sox2 and Oct-3 on the fibroblast growth factor-4 enhancer. J Biol Chem. 2000;275(30):23387-97.
62. Kuroda T, Tada M, Kubota H, Kimura H, Hatano SY, Suemori H, Nakatsuji N, Tada T. Octamer and Sox elements are required for transcriptional cis regulation of Nanog gene expression. Mol Cell Biol. 2005;25(6):2475-85.
63. Do HJ, Lee WY, Lim HY, Oh JH, Kim DK, Kim JH, Kim T, Kim JH. Two potent transactivation domains in the C-terminal region of human NANOG mediate transcriptional activation in human embryonic carcinoma cells. J Cell Biochem. 2009;106(6):1079-89.
64. Chew JL, Loh YH, Zhang W, Chen X, Tam WL, Yeap LS, Li P, Ang YS, Lim B, Robson P, et al. Reciprocal transcriptional regulation of Pou5f1 and Sox2 via the Oct4/Sox2 complex in embryonic stem cells. Mol Cell Biol. 2005;25(14):6031-46.
65. 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):8027-38.
66. Jerabek S, Merino F, Scholer HR, Cojocaru V. OCT4: dynamic DNA binding pioneers stem cell pluripotency. Biochim Biophys Acta. 2014;1839(3):138-54.
67. Chiou SH, Wang ML, Chou YT, Chen CJ, Hong CF, Hsieh WJ, Chang HT, Chen YS, Lin TW, Hsu HS, et al. Coexpression of Oct4 and Nanog enhances malignancy in lung adenocarcinoma by inducing cancer stem cell-like properties and epithelial-mesenchymal transdifferentiation. Cancer Res. 2010;70(24):10433-44.
68. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell. 2003;113(5):631-42.
69. Booth HA, Holland PW. Eleven daughters of NANOG. Genomics. 2004;84(2):229-38.
70. Ibrahim EE, Babaei-Jadidi R, Saadeddin A, Spencer-Dene B, Hossaini S, Abuzinadah M, Li N, Fadhil W, Ilyas M, Bonnet D, et al. Embryonic NANOG activity defines colorectal cancer stem cells and modulates through AP1- and TCF-dependent mechanisms. Stem Cells. 2012;30(10):2076-87.
71. Zhang J, Wang X, Li M, Han J, Chen B, Wang B, Dai J. NANOGP8 is a retrogene expressed in cancers. FEBS J. 2006;273(8):1723-30.
72. Fairbanks DJ, Fairbanks AD, Ogden TH, Parker GJ, Maughan PJ. NANOGP8: evolution of a human-specific retro-oncogene. G3 (Bethesda). 2012;2(11):1447-57.
73. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell. 2003;113(5):643-55.
74. Fu TY, Hsieh IC, Cheng JT, Tsai MH, Hou YY, Lee JH, et al. Association of OCT4, SOX2, and NANOG expression with oral squamous cell carcinoma progression. J Oral Pathol Med. 2015.
75. Han J, Zhang F, Yu M, Zhao P, Ji W, Zhang H, Wu B, Wang Y, Niu R. RNA interference-mediated silencing of NANOG reduces cell proliferation and induces G0/G1 cell cycle arrest in breast cancer cells. Cancer Lett. 2012;321(1):80-8.
76. Choi SC, Choi JH, Park CY, Ahn CM, Hong SJ, Lim DS. Nanog regulates molecules involved in stemness and cell cycle-signaling pathway for maintenance of pluripotency of P19 embryonal carcinoma stem cells. J Cell Physiol. 2012;227(11):3678-92.
77. Jeter CR, Liu B, Liu X, Chen X, Liu C, Calhoun-Davis T, Repass J, Zaehres H, Shen JJ, Tang DG. NANOG promotes cancer stem cell characteristics and prostate cancer resistance to androgen deprivation. Oncogene. 2011;30(36):3833-45.
78. Moon JH, Kwon S, Jun EK, Kim A, Whang KY, Kim H, Oh S, Yoon BS, You S. Nanog-induced dedifferentiation of p53-deficient mouse astrocytes into brain cancer stem-like cells. Biochem Biophys Res Commun. 2011;412(1):175-81.
79. Bourguignon LY, Earle C, Wong G, Spevak CC, Krueger K. Stem cell marker (Nanog) and Stat-3 signaling promote MicroRNA-21 expression and chemoresistance in hyaluronan/CD44-activated head and neck squamous cell carcinoma cells. Oncogene. 2012;31(2):149-60.
80. Bourillot PY, Aksoy I, Schreiber V, Wianny F, Schulz H, Hummel O, Hubner N, Savatier P. Novel STAT3 target genes exert distinct roles in the inhibition of mesoderm and endoderm differentiation in cooperation with Nanog. Stem Cells. 2009;27(8):1760-71.
81. Po A, Ferretti E, Miele E, De Smaele E, Paganelli A, Canettieri G, Coni S, Di Marcotullio L, Biffoni M, Massimi L, et al. Hedgehog controls neural stem cells through p53-independent regulation of Nanog. EMBO J. 2010;29(15):2646-58.
82. Golubovskaya VM. FAK and Nanog cross talk with p53 in cancer stem cells. Anticancer Agents Med Chem. 2013;13(4):576-80.
83. Suzuki A, Raya A, Kawakami Y, Morita M, Matsui T, Nakashima K, Gage FH, Rodriguez-Esteban C, Izpisua Belmonte JC. Nanog binds to Smad1 and blocks bone morphogenetic protein-induced differentiation of embryonic stem cells. Proc Natl Acad Sci U S A. 2006;103(27):10294-9.
84. Siu MK, Wong ES, Kong DS, Chan HY, Jiang L, Wong OG, Lam EW, Chan KK, Ngan HY, Le XF, et al. Stem cell transcription factor NANOG controls cell migration and invasion via dysregulation of E-cadherin and FoxJ1 and contributes to adverse clinical outcome in ovarian cancers. Oncogene. 2013;32(30):3500-9.
85. Nagata T, Shimada Y, Sekine S, Hori R, Matsui K, Okumura T, Sawada S, Fukuoka J, Tsukada K. Prognostic significance of NANOG and KLF4 for breast cancer. Breast Cancer. 2014;21(1):96-101.
86. Lee M, Nam EJ, Kim SW, Kim S, Kim JH, Kim YT. Prognostic impact of the cancer stem cell-related marker NANOG in ovarian serous carcinoma. Int J Gynecol Cancer. 2012;22(9):1489-96.
87. Meng HM, Zheng P, Wang XY, Liu C, Sui HM, Wu SJ, Zhou J, Ding YQ, Li J. Over-expression of Nanog predicts tumor progression and poor prognosis in colorectal cancer. Cancer Biol Ther. 2010;9(4):295-302.
88. Raaphorst FM. Deregulated expression of Polycomb-group oncogenes in human malignant lymphomas and epithelial tumors. Hum Mol Genet. 2005;14(Spec No 1):R93-100.
89. Huber GF, Albinger-Hegyi A, Soltermann A, Roessle M, Graf N, Haerle SK, Holzmann D, Moch H, Hegyi I. Expression patterns of Bmi-1 and p16 significantly correlate with overall, disease-specific, and recurrence-free survival in oropharyngeal squamous cell carcinoma. Cancer. 2011;117(20):4659-70.
90. Nowak K, Kerl K, Fehr D, Kramps C, Gessner C, Killmer K, Samans B, Berwanger B, Christiansen H, Lutz W. BMI1 is a target gene of E2F-1 and is strongly expressed in primary neuroblastomas. Nucleic Acids Res. 2006;34(6):1745-54.
91. Shafaroudi AM, Mowla SJ, Ziaee SA, Bahrami AR, Atlasi Y, Malakootian M. Overexpression of BMI1, a polycomb group repressor protein, in bladder tumors: a preliminary report. Urol J. 2008;5(2):99-105.
92. Fasano CA, Dimos JT, Ivanova NB, Lowry N, Lemischka IR, Temple S. shRNA knockdown of Bmi-1 reveals a critical role for p21-Rb pathway in NSC self-renewal during development. Cell Stem Cell. 2007;1(1):87-99.
93. Yadirgi G, Leinster V, Acquati S, Bhagat H, Shakhova O, Marino S. Conditional activation of Bmi1 expression regulates self-renewal, apoptosis, and differentiation of neural stem/progenitor cells in vitro and in vivo. Stem Cells. 2011;29(4):700-12.
94. Oguro H, Yuan J, Ichikawa H, Ikawa T, Yamazaki S, Kawamoto H, Nakauchi H, Iwama A. Poised lineage specification in multipotential hematopoietic stem and progenitor cells by the polycomb protein Bmi1. Cell Stem Cell. 2010;6(3):279-86.
95. Lukacs RU, Memarzadeh S, Wu H, Witte ON. Bmi-1 is a crucial regulator of prostate stem cell self-renewal and malignant transformation. Cell Stem Cell. 2010;7(6):682-93.
96. Lessard J, Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature. 2003;423(6937):255-60.
97. Molofsky AV, He S, Bydon M, Morrison SJ, Pardal R. Bmi-1 promotes neural stem cell self-renewal and neural development but not mouse growth and survival by repressing the p16Ink4a and p19Arf senescence pathways. Genes Dev. 2005;19(12):1432-7.
98. Park IK, Morrison SJ, Clarke MF. Bmi1, stem cells, and senescence regulation. J Clin Invest. 2004;113(2):175-9.
99. Dimri GP, Martinez JL, Jacobs JJ, Keblusek P, Itahana K, Van Lohuizen M, Campisi J, Wazer DE, Band V. The Bmi-1 oncogene induces telomerase activity and immortalizes human mammary epithelial cells. Cancer Res. 2002;62(16):4736-45.
100. Song LB, Li J, Liao WT, Feng Y, Yu CP, Hu LJ, Kong QL, Xu LH, Zhang X, Liu WL, et al. The polycomb group protein Bmi-1 represses the tumor suppressor PTEN and induces epithelial-mesenchymal transition in human nasopharyngeal epithelial cells. J Clin Invest. 2009;119(12):3626-36.
101. Dong P, Kaneuchi M, Watari H, Hamada J, Sudo S, Ju J, Sakuragi N. MicroRNA-194 inhibits epithelial to mesenchymal transition of endometrial cancer cells by targeting oncogene BMI-1. Mol Cancer. 2011;10:99.
102. Storci G, Sansone P, Trere D, Tavolari S, Taffurelli M, Ceccarelli C, Guarnieri T, Paterini P, Pariali M, Montanaro L, et al. The basal-like breast carcinoma phenotype is regulated by SLUG gene expression. J Pathol. 2008;214(1):25-37.
103. Yang MH, Hsu DS, Wang HW, Wang HJ, Lan HY, Yang WH, Huang CH, Kao SY, Tzeng CH, Tai SK, et al. Bmi1 is essential in Twist1-induced epithelial-mesenchymal transition. Nat Cell Biol. 2010;12(10):982-92.
104. Paranjape AN, Balaji SA, Mandal T, Krushik EV, Nagaraj P, Mukherjee G, Rangarajan A. Bmi1 regulates self-renewal and epithelial to mesenchymal transition in breast cancer cells through Nanog. BMC Cancer. 2014;14:785.
105. Wicha MS. Targeting self-renewal, an Achilles' heel of cancer stem cells. Nat Med. 2014;20(1):14-5.
106. Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, Jackson KW, Suri P, Wicha MS. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 2006;66(12):6063-71.
107. Mohty M, Yong AS, Szydlo RM, Apperley JF, Melo JV. The polycomb group BMI1 gene is a molecular marker for predicting prognosis of chronic myeloid leukemia. Blood. 2007;110(1):380-3.
108. Song LB, Zeng MS, Liao WT, Zhang L, Mo HY, Liu WL, Shao JY, Wu QL, Li MZ, Xia YF, et al. Bmi-1 is a novel molecular marker of nasopharyngeal carcinoma progression and immortalizes primary human nasopharyngeal epithelial cells. Cancer Res. 2006;66(12):6225-32.
109. Vormittag L, Thurnher D, Geleff S, Pammer J, Heiduschka G, Brunner M, Grasl M, Erovic BM. Co-expression of Bmi-1 and podoplanin predicts overall survival in patients with squamous cell carcinoma of the head and neck treated with radio(chemo)therapy. Int J Radiat Oncol Biol Phys. 2009;73(3):913-8.
110. Li J, Gong LY, Song LB, Jiang LL, Liu LP, Wu J, Yuan J, Cai JC, He M, Wang L, et al. Oncoprotein Bmi-1 renders apoptotic resistance to glioma cells through activation of the IKK-nuclear factor-kappaB Pathway. Am J Pathol. 2010;176(2):699-709.
111. van Kemenade FJ, Raaphorst FM, Blokzijl T, Fieret E, Hamer KM, Satijn DP, Otte AP, Meijer CJ. Coexpression of BMI-1 and EZH2 polycomb-group proteins is associated with cycling cells and degree of malignancy in B-cell non-Hodgkin lymphoma. Blood. 2001;97(12):3896-901.
112. Piva M, Domenici G, Iriondo O, Rabano M, Simoes BM, Comaills V, Barredo I, Lopez-Ruiz JA, Zabalza I, Kypta R, et al. Sox2 promotes tamoxifen resistance in breast cancer cells. EMBO Mol Med. 2014;6(1):66-79.
113. Yang L, Zhang X, Zhang M, Zhang J, Sheng Y, Sun X, Chen Q, Wang LX. Increased Nanog expression promotes tumor development and Cisplatin resistance in human esophageal cancer cells. Cell Physiol Biochem. 2012;30(4):943-52.
114. Du Y, Shi L, Wang T, Liu Z, Wang Z. Nanog siRNA plus Cisplatin may enhance the sensitivity of chemotherapy in esophageal cancer. J Cancer Res Clin Oncol. 2012;138(10):1759-67.
115. Tsai LL, Yu CC, Chang YC, Yu CH, Chou MY. Markedly increased Oct4 and Nanog expression correlates with cisplatin resistance in oral squamous cell carcinoma. J Oral Pathol Med. 2011;40(8):621-8.
116. Crea F, Duhagon Serrat MA, Hurt EM, Thomas SB, Danesi R, Farrar WL. BMI1 silencing enhances docetaxel activity and impairs antioxidant response in prostate cancer. Int J Cancer. 2011;128(8):1946-54.
117. Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, Yan PS, Huang TH, Nephew KP. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res. 2008;68(11):4311-20.
118. Wang E, Bhattacharyya S, Szabolcs A, Rodriguez-Aguayo C, Jennings NB, Lopez-Berestein G, Mukherjee P, Sood AK, Bhattacharya R. Enhancing chemotherapy response with Bmi-1 silencing in ovarian cancer. PLoS ONE. 2011;6(3), e17918.
119. 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):1595-604.
120. Shi Y, Seto E, Chang LS, Shenk T. Transcriptional repression by YY1, a human GLI-Kruppel-related protein, and relief of repression by adenovirus E1A protein. Cell. 1991;67(2):377-88.
121. Park K, Atchison ML. Isolation of a candidate repressor/activator, NF-E1 (YY-1, delta), that binds to the immunoglobulin kappa 3' enhancer and the immunoglobulin heavy-chain mu E1 site. Proc Natl Acad Sci U S A. 1991;88(21):9804-8.
122. Hariharan N, Kelley DE, Perry RP. Delta, a transcription factor that binds to downstream elements in several polymerase II promoters, is a functionally versatile zinc finger protein. Proc Natl Acad Sci U S A. 1991;88(21):9799-803.
123. Flanagan JR, Becker KG, Ennist DL, Gleason SL, Driggers PH, Levi BZ, Appella E, Ozato K. Cloning of a negative transcription factor that binds to the upstream conserved region of Moloney murine leukemia virus. Mol Cell Biol. 1992;12(1):38-44.
124. Thomas MJ, Seto E. Unlocking the mechanisms of transcription factor YY1: are chromatin modifying enzymes the key? Gene. 1999;236(2):197-208.
125. Shi Y, Lee JS, Galvin KM. Everything you have ever wanted to know about Yin Yang 1. Biochim Biophys Acta. 1997;1332(2):F49-66.
126. Liu H, Shi Y. Yin Yang 1. In: Iuchi S, Kuldell N, editors. Zinc Finger Proteins: From Atomic Contact to Cellular Function. 1st ed. New York: Springer US; 2005. p. 182-94.
127. Gordon S, Akopyan G, Garban H, Bonavida B. Transcription factor YY1: structure, function, and therapeutic implications in cancer biology. Oncogene. 2006;25(8):1125-42.
128. Wilkinson FH, Park K, Atchison ML. Polycomb recruitment to DNA in vivo by the YY1 REPO domain. Proc Natl Acad Sci U S A. 2006;103(51):19296-301.
129. Thomassen M, Tan Q, Kruse TA. Gene expression meta-analysis identifies metastatic pathways and transcription factors in breast cancer. BMC Cancer. 2008;8:394.
130. Wan M, Huang W, Kute TE, Miller LD, Zhang Q, Hatcher H, Wang J, Stovall DB, Russell GB, Cao PD, et al. Yin Yang 1 plays an essential role in breast cancer and negatively regulates p27. Am J Pathol. 2012;180(5):2120-33.
131. Chinnappan D, Xiao D, Ratnasari A, Andry C, King TC, Weber HC. Transcription factor YY1 expression in human gastrointestinal cancer cells. Int J Oncol. 2009;34(5):1417-23.
132. Kang W, Tong JH, Chan AW, Zhao J, Dong Y, Wang S, Yang W, Sin FM, Ng SS, Yu J, et al. Yin Yang 1 contributes to gastric carcinogenesis and its nuclear expression correlates with shorter survival in patients with early stage gastric adenocarcinoma. J Transl Med. 2014;12:80.
133. Seligson D, Horvath S, Huerta-Yepez S, Hanna S, Garban H, Roberts A, Shi T, Liu X, Chia D, Goodglick L, et al. Expression of transcription factor Yin Yang 1 in prostate cancer. Int J Oncol. 2005;27(1):131-41.
134. Bonavida B, Kaufhold S. Prognostic significance of YY1 protein expression and mRNA levels by bioinformatics analysis in human cancers: a therapeutic target. Pharmacol Ther. 2015;150:149-68.
135. Gao F, Wei Z, An W, Wang K, Lu W. The interactomes of POU5F1 and SOX2 enhancers in human embryonic stem cells. Sci Rep. 2013;3:1588.
136. Wang AM, Huang TT, Hsu KW, Huang KH, Fang WL, Yang MH, Lo SS, Chi CW, Lin JJ, Yeh TS. Yin Yang 1 is a target of microRNA-34 family and contributes to gastric carcinogenesis. Oncotarget. 2014;5(13):5002-16.
137. Satijn DP, Hamer KM, den Blaauwen J, Otte AP. The polycomb group protein EED interacts with YY1, and both proteins induce neural tissue in Xenopus embryos. Mol Cell Biol. 2001;21(4):1360-9.
138. Uhlen M, Fagerberg L, Hallstrom BM, Lindskog C, Oksvold P, Mardinoglu A, Sivertsson A, Kampf C, Sjostedt E, Asplund A, et al. Proteomics. Tissue-based map of the human proteome. Science. 2015;347(6220):1260419.
139. Human Protein Atlas [ http://www.proteinatlas.org/cancer ]
140. SABioscience's Text-Mining Application [ http://www.sabiosciences.com/chipqpcrsearch.php?app=TFBS ]
141. University of California, Santa Cruz (UCSC) Genome Browser [ https://genome.ucsc.edu ]