Pluripotency transcription factors in lung cancer—a review

Tumor Biology

Volumn 37, Issue 4, 2016, Pages 4241-4249

  Sławek, Sylwia ^a   Szmyt, Krzysztof ^a   Fularz, Maciej ^a   Dziudzia, Joanna ^a   Boruczkowski, Maciej ^a   Sikora, Jan ^a   Kaczmarek, Mariusz ^a  

^a POZNAN UNIVERSITY OF MEDICAL SCIENCES   (Poland)

Author keywords

Bmi1; c Myc; Cancer stem cells; KLF4; LIN28; Lung cancer; Nanog; Oct 4; SOX2

Indexed keywords

BMI1 PROTEIN; KRUPPEL LIKE FACTOR 4; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2;

BMI1 GENE; CANCER STEM CELL; ENZYME ACTIVATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE; GENE EXPRESSION; HUMAN; INTRACELLULAR SIGNALING; LIN28 GENE; LUNG CANCER; LUNG CARCINOGENESIS; MOLECULAR PATHOLOGY; NONHUMAN; NUCLEAR REPROGRAMMING; ONCOGENE C MYC; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; SOX GENE; BIOSYNTHESIS; CARCINOGENESIS; EARLY CANCER DIAGNOSIS; GENE EXPRESSION REGULATION; GENETICS; LUNG NEOPLASMS; METABOLISM; METASTASIS; PATHOLOGY;

CARCINOGENESIS; EARLY DETECTION OF CANCER; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; NEOPLASM METASTASIS; NEOPLASTIC STEM CELLS; PLURIPOTENT STEM CELLS; TRANSCRIPTION FACTORS;

EID: 84947445566     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-015-4407-x     Document Type: Review

References (87)

1. Gibson G, Loddenkemper R, Sibille Y, Lundbäck B. The European lung white book: sheffield; 2013. p. 224–235.
2. Wojciechowska U, Didkowska J. Zachorowania i zgony na nowotwory złośliwe w Polsce. Krajowy Rejestr Nowotworów, Centrum Onkologii - Instytut im. Marii Skłodowskiej - Curie. http://onkologia.org.pl/raporty/ Accessed 31.Oct 2015.
3. Qu H, Li R, Liu Z, Zhang J, Luo R. Prognostic value of cancer stem cell marker CD133 expression in non-small cell lung cancer: a systematic review. Int J Clin Exp Pathol. 2013;6(11):2644–50.
4. Tan Y, Chen B, Xu W, Zhao W, Wu J. Clinicopathological significance of CD133 in lung cancer: a meta-analysis. Mol Clin Oncol. 2014;2(1):111–5.
5. Succony L, Janes SM. Airway stem cells and lung cancer. QJM. 2014;107(8):607–12.
6. Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell. 2010;140(1):62–73.
7. Hadjimichael C, Chanoumidou K, Papadopoulou N, Arampatzi P, Papamatheakis J, Kretsovali A. Common stemness regulators of embryonic and cancer stem cells. World J Stem Cells. 2015;7(9):1150–84.
8. Liu A, Yu X, Liu S. Pluripotency transcription factors and cancer stem cells: small genes make a big difference. Chin J Cancer. 2013;32(9):483–7.
9. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126(4):663–76.
10. Zheng YW, Nie YZ, Taniguchi H. Cellular reprogramming and hepatocellular carcinoma development. World J Gastroenterol. 2014;19(47):8850–60.
11. Nagata S, Hirano K, Kanemori M, Sun LT, Tada T. Self-renewal and pluripotency acquired through somatic reprogramming to human cancer stem cells. PLoS One. 2012;7(11):e48699.
12. Somervaille TC, Matheny CJ, Spencer GJ, Iwasaki M, Rinn JL, Witten DM, et al. Hierarchical maintenance of MLL myeloid leukemia stem cells employs a transcriptional program shared with embryonic rather than adult stem cells. Cell Stem Cell. 2009;4(2):129–40.
13. Sholl LM, Barletta JA, Yeap BY, Chirieac LR, Hornick JL. Sox2 protein expression is an independent poor prognostic indicator in stage I lung adenocarcinoma. Am J Surg Pathol. 2010;34(8):1193–8.
14. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet. 2008;40(5):499–507.
15. Ji J, Zheng PS. Expression of Sox2 in human cervical carcinogenesis. Hum Pathol. 2010;41(10):1438–47.
16. Fyfe B, Amazon K, Poppiti Jr RJ, Razzetti A. Intraosseous echinococcosis: a rare manifestation of echinococcal disease. South Med J. 1990;83(1):66–8.
17. Gadgeel SM, Wozniak A. Preclinical rationale for PI3K/Akt/mTOR pathway inhibitors as therapy for epidermal growth factor receptor inhibitor-resistant non-small-cell lung cancer. Clin Lung Cancer. 2013;14(4):322–32.
18. Altomare DA, Testa JR. Perturbations of the AKT signaling pathway in human cancer. Oncogene. 2005;24(50):7455–64.
19. Kim DH, Sarbassov DD, Ali SM, King JE, Latek RR, Erdjument-Bromage H, et al. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell. 2002;110(2):163–75.
20. Lei N, Peng B, Zhang JY. CIP2A regulates cell proliferation via the AKT signaling pathway in human lung cancer. Oncol Rep. 2014;32(4):1689–94.
21. Liu CW, Li CH, Peng YJ, Cheng YW, Chen HW, Liao PL, et al. Snail regulates Nanog status during the epithelial-mesenchymal transition via the Smad1/Akt/GSK3beta signaling pathway in non-small-cell lung cancer. Oncotarget. 2014;5(11):3880–94.
22. Paplomata E, O’Regan R. The PI3K/AKT/mTOR pathway in breast cancer: targets, trials and biomarkers. Ther Adv Med Oncol. 2014;6(4):154–66.
23. Lin F, Lin P, Zhao D, Chen Y, Xiao L, Qin W, et al. Sox2 targets cyclinE, p27 and survivin to regulate androgen-independent human prostate cancer cell proliferation and apoptosis. Cell Prolif. 2012;45(3):207–16.
24. Heavey S, O’Byrne KJ, Gately K. Strategies for co-targeting the PI3K/AKT/mTOR pathway in NSCLC. Cancer Treat Rev. 2013;40(3):445–56.
25. Shan J, Shen J, Liu L, Xia F, Xu C, Duan G, et al. Nanog regulates self-renewal of cancer stem cells through the insulin-like growth factor pathway in human hepatocellular carcinoma. Hepatology. 2012;56(3):1004–14.
26. Ambady S, Malcuit C, Kashpur O, Kole D, Holmes WF, Hedblom E, et al. Expression of NANOG and NANOGP8 in a variety of undifferentiated and differentiated human cells. Int J Dev Biol. 2010;54(11–12):1743–54.
27. Jeter CR, Badeaux M, Choy G, Chandra D, Patrawala L, Liu C, et al. Functional evidence that the self-renewal gene NANOG regulates human tumor development. Stem Cells. 2009;27(5):993–1005.
28. Chiou SH, Wang ML, Chou YT, Chen CJ, Hong CF, Hsieh WJ, 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.
29. Li L, Yu H, Wang X, Zeng J, Li D, Lu J, et al. Expression of seven stem-cell-associated markers in human airway biopsy specimens obtained via fiberoptic bronchoscopy. J Exp Clin Cancer Res. 2013;32:28.
30. Li XQ, Yang XL, Zhang G, Wu SP, Deng XB, Xiao SJ, et al. Nuclear beta-catenin accumulation is associated with increased expression of Nanog protein and predicts poor prognosis of non-small cell lung cancer. J Transl Med. 2013;11:114.
31. Du Y, Ma C, Wang Z, Liu Z, Liu H, Wang T. Nanog, a novel prognostic marker for lung cancer. Surg Oncol. 2013;22(4):224–9.
32. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer. 2007;7(6):415–28.
33. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, Chen X, et al. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet. 2006;38(4):431–40.
34. Hu T, Liu S, Breiter DR, Wang F, Tang Y, Sun S. Octamer 4 small interfering RNA results in cancer stem cell-like cell apoptosis. Cancer Res. 2008;68(16):6533–40.
35. Mirza AM, Gysin S, Malek N, Nakayama K, Roberts JM, McMahon M. Cooperative regulation of the cell division cycle by the protein kinases RAF and AKT. Mol Cell Biol. 2004;24(24):10868–81.
36. Moreira AL, Gonen M, Rekhtman N, Downey RJ. Progenitor stem cell marker expression by pulmonary carcinomas. Mod Pathol. 2010;23(6):889–95.
37. Cantz T, Key G, Bleidissel M, Gentile L, Han DW, Brenne A, et al. Absence of OCT4 expression in somatic tumor cell lines. Stem Cells. 2008;26(3):692–7.
38. Li XL, Jia LL, Shi MM, Li X, Li ZH, Li HF, et al. Downregulation of KPNA2 in non-small-cell lung cancer is associated with Oct4 expression. J Transl Med. 2013;11:232.
39. Chen YC, Hsu HS, Chen YW, Tsai TH, How CK, Wang CY, et al. Oct-4 expression maintained cancer stem-like properties in lung cancer-derived CD133-positive cells. PLoS One. 2008;3(7):e2637.
40. Gomez-Casal R, Bhattacharya C, Ganesh N, Bailey L, Basse P, Gibson M, et al. Non-small cell lung cancer cells survived ionizing radiation treatment display cancer stem cell and epithelial-mesenchymal transition phenotypes. Mol Cancer. 2013;12(1):94.
41. Xu C, Xie D, Yu SC, Yang XJ, He LR, Yang J, et al. beta-Catenin/POU5F1/SOX2 transcription factor complex mediates IGF-I receptor signaling and predicts poor prognosis in lung adenocarcinoma. Cancer Res. 2013;73(10):3181–9.
42. Chen Z, Wang T, Cai L, Su C, Zhong B, Lei Y, et al. Clinicopathological significance of non-small cell lung cancer with high prevalence of Oct-4 tumor cells. J Exp Clin Cancer Res. 2012;31:10.
43. Yet SF, McA’Nulty MM, Folta SC, Yen HW, Yoshizumi M, Hsieh CM, et al. Human EZF, a Kruppel-like zinc finger protein, is expressed in vascular endothelial cells and contains transcriptional activation and repression domains. J Biol Chem. 1998;273(2):1026–31.
44. Shields JM, Yang VW. Identification of the DNA sequence that interacts with the gut-enriched Kruppel-like factor. Nucleic Acids Res. 1998;26(3):796–802.
45. Yanagida A, Sogawa K, Yasumoto KI, Fujii-Kuriyama Y. A novel cis-acting DNA element required for a high level of inducible expression of the rat P-450c gene. Mol Cell Biol. 1990;10(4):1470–5.
46. Hu W, Hofstetter WL, Li H, Zhou Y, He Y, Pataer A, et al. Putative tumor-suppressive function of Kruppel-like factor 4 in primary lung carcinoma. Clin Cancer Res. 2009;15(18):5688–95.
47. Zhou Y, Hofstetter WL, He Y, Hu W, Pataer A, Wang L, et al. KLF4 inhibition of lung cancer cell invasion by suppression of SPARC expression. Cancer Biol Ther. 2010;9(7):507–13.
48. Vaira V, Faversani A, Martin NM, Garlick DS, Ferrero S, Nosotti M, et al. Regulation of lung cancer metastasis by Klf4-Numb-like signaling. Cancer Res. 2013;73(8):2695–705.
49. Naranjo Gomez JM, Bernal JF, Arranz PG, Fernandez SL, Roman JJ. Alterations in the expression of p53, KLF4, and p21 in neuroendocrine lung tumors. Arch Pathol Lab Med. 2014;138(7):936–42.
50. Su QL, Li SQ, Wang DN, Liu F, Yuan B. Effects of MicroRNA-10b on lung cancer cell proliferation and invasive metastasis and the underlying mechanism. Asian Pac J Trop Med. 2014;7(5):364–7.
51. Sarkar A, Hochedlinger K. The sox family of transcription factors: versatile regulators of stem and progenitor cell fate. Cell Stem Cell. 2013;12(1):15–30.
52. Chen S, Xu Y, Chen Y, Li X, Mou W, Wang L, et al. SOX2 gene regulates the transcriptional network of oncogenes and affects tumorigenesis of human lung cancer cells. PLoS One. 2012;7(5):e36326.
53. Rudin CM, Durinck S, Stawiski EW, Poirier JT, Modrusan Z, Shames DS, et al. Comprehensive genomic analysis identifies SOX2 as a frequently amplified gene in small-cell lung cancer. Nat Genet. 2012;44(10):1111–6.
54. Xu W, Wei Y, Tan Y, Cheng SY, Wu J. The expression and significance of stem cell transcription factor Sox2 in lung carcinoma. Zhongguo Fei Ai Za Zhi. 2013;16(11):591–5.
55. Yuan P, Kadara H, Behrens C, Tang X, Woods D, Solis LM, et al. Sex determining region Y-Box 2 (SOX2) is a potential cell-lineage gene highly expressed in the pathogenesis of squamous cell carcinomas of the lung. PLoS One. 2010;5(2):e9112.
56. Lu Y, Futtner C, Rock JR, Xu X, Whitworth W, Hogan BL, et al. Evidence that SOX2 overexpression is oncogenic in the lung. PLoS One. 2010;5(6):e11022.
57. Cortes-Dericks L, Galetta D, Spaggiari L, Schmid RA, Karoubi G. High expression of octamer-binding transcription factor 4A, prominin-1 and aldehyde dehydrogenase strongly indicates involvement in the initiation of lung adenocarcinoma resulting in shorter disease-free intervals. Eur J Cardiothorac Surg. 2012;41(6):e173–81.
58. Toschi L, Finocchiaro G, Nguyen TT, Skokan MC, Giordano L, Gianoncelli L, 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.
59. Bass AJ, Watanabe H, Mermel CH, Yu S, Perner S, Verhaak RG, et al. SOX2 is an amplified lineage-survival oncogene in lung and esophageal squamous cell carcinomas. Nat Genet. 2009;41(11):1238–42.
60. Hussenet T, Dali S, Exinger J, Monga B, Jost B, Dembele D, et al. SOX2 is an oncogene activated by recurrent 3q26.3 amplifications in human lung squamous cell carcinomas. PLoS One. 2010;5(1):e8960.
61. Chen S, Li X, Lu D, Xu Y, Mou W, Wang L, et al. SOX2 regulates apoptosis through MAP4K4-survivin signaling pathway in human lung cancer cells. Carcinogenesis. 2014;35(3):613–23.
62. Fang WT, Fan CC, Li SM, Jang TH, Lin HP, Shih NY, 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.
63. Singh S, Trevino J, Bora-Singhal N, Coppola D, Haura E, Altiok S, et al. EGFR/Src/Akt signaling modulates Sox2 expression and self-renewal of stem-like side-population cells in non-small cell lung cancer. Mol Cancer. 2012;11:73.
64. Thornton JE, Gregory RI. How does Lin28 let-7 control development and disease? Trends Cell Biol. 2012;22(9):474–82.
65. Viswanathan SR, Powers JT, Einhorn W, Hoshida Y, Ng TL, Toffanin S, et al. Lin28 promotes transformation and is associated with advanced human malignancies. Nat Genet. 2009;41(7):843–8.
66. Kumar MS, Erkeland SJ, Pester RE, Chen CY, Ebert MS, Sharp PA, et al. Suppression of non-small cell lung tumor development by the let-7 microRNA family. Proc Natl Acad Sci U S A. 2008;105(10):3903–8.
67. Oh JS, Kim JJ, Byun JY, Kim IA. Lin28-let7 modulates radiosensitivity of human cancer cells with activation of K-Ras. Int J Radiat Oncol Biol Phys. 2010;76(1):5–8.
68. Wen J, Liu H, Wang Q, Liu Z, Li Y, Xiong H, et al. Genetic variants of the LIN28B gene predict severe radiation pneumonitis in patients with non-small cell lung cancer treated with definitive radiation therapy. Eur J Cancer. 2014;50(10):1706–16.
69. Sodir NM, Swigart LB, Karnezis AN, Hanahan D, Evan GI, Soucek L. Endogenous Myc maintains the tumor microenvironment. Genes Dev. 2011;25(9):907–16.
70. Karachaliou N, Papadaki C, Lagoudaki E, Trypaki M, Sfakianaki M, Koutsopoulos A, et al. Predictive value of BRCA1, ERCC1, ATP7B, PKM2, TOPOI, TOPOmicron-IIA, TOPOIIB and C-MYC genes in patients with small cell lung cancer (SCLC) who received first line therapy with cisplatin and etoposide. PLoS One. 2013;8(9):e74611.
71. Sato M, Larsen JE, Lee W, Sun H, Shames DS, Dalvi MP, et al. Human lung epithelial cells progressed to malignancy through specific oncogenic manipulations. Mol Cancer Res. 2013;11(6):638–50.
72. Johnson BE, Russell E, Simmons AM, Phelps R, Steinberg SM, Ihde DC, et al. MYC family DNA amplification in 126 tumor cell lines from patients with small cell lung cancer. J Cell Biochem Suppl. 1996;24:210–7.
73. Teicher BA. Targets in small cell lung cancer. Biochem Pharmacol. 2014;87(2):211–9.
74. D’Angelo SP, Pietanza MC. The molecular pathogenesis of small cell lung cancer. Cancer Biol Ther. 2010;10(1):1–10.
75. Castro IC, Breiling A, Luetkenhaus K, Ceteci F, Hausmann S, Kress S, et al. MYC-induced epigenetic activation of GATA4 in lung adenocarcinoma. Mol Cancer Res. 2012;11(2):161–72.
76. Liao P, Wang W, Shen M, Pan W, Zhang K, Wang R, et al. A positive feedback loop between EBP2 and c-Myc regulates rDNA transcription, cell proliferation, and tumorigenesis. Cell Death Dis. 2014;5:e1032.
77. Jiang L, Li J, Song L. Bmi-1, stem cells and cancer. Acta Biochim Biophys Sin (Shanghai). 2009;41(7):527–34.
78. Glinsky GV, Berezovska O, Glinskii AB. Microarray analysis identifies a death-from-cancer signature predicting therapy failure in patients with multiple types of cancer. J Clin Invest. 2005;115(6):1503–21.
79. Lowe SW, Sherr CJ. Tumor suppression by Ink4a-Arf: progress and puzzles. Curr Opin Genet Dev. 2003;13(1):77–83.
80. Bhattacharya R, Mustafi SB, Street M, Dey A, Dwivedi SK. Bmi-1: at the crossroads of physiological and pathological biology. Genes Dis. 2015;2(3):225–39.
81. Chen T, Xu C, Chen J, Ding C, Xu Z, Li C, et al. MicroRNA-203 inhibits cellular proliferation and invasion by targeting Bmi1 in non-small cell lung cancer. Oncol Lett. 2015;9(6):2639–46.
82. Hu J, Liu YL, Piao SL, Yang DD, Yang YM, Cai L. Expression patterns of USP22 and potential targets BMI-1, PTEN, p-AKT in non-small-cell lung cancer. Lung Cancer. 2012;77(3):593–9.
83. Shao Y, Geng Y, Gu W, Ning Z, Jiang J, Pei H. Prognostic role of high Bmi-1 expression in Asian and Caucasian patients with solid tumors: a meta-analysis. Biomed Pharmacother. 2014;68(8):969–77.
84. Zhang XY, Dong QG, Huang JS, Huang AM, Shi CL, Jin B, et al. The expression of stem cell-related indicators as a prognostic factor in human lung adenocarcinoma. J Surg Oncol. 2010;102(7):856–62.
85. He Z, Xia Y, Pan C, Ma T, Liu B, Wang J, et al. Upregulation of MiR-452 inhibits metastasis of non-small-cell lung cancer by regulating BMI1. Cell Physiol Biochem. 2015;37(1):387–98.
86. Zhang Y, Li X, Chen Z, Bepler G. Ubiquitination and degradation of ribonucleotide reductase M1 by the polycomb group proteins RNF2 and Bmi1 and cellular response to gemcitabine. PLoS One. 2014;9(3):e91186.
87. Udagawa H, Ishii G, Morise M, Umemura S, Matsumoto S, Yoh K, et al. Comparison of the expression levels of molecular markers among the peripheral area and central area of primary tumor and metastatic lymph node tumor in patients with squamous cell carcinoma of the lung. J Cancer Res Clin Oncol. 2015;141(8):1417–25.