Profiling gene promoter occupancy of Sox2 in two phenotypically distinct breast cancer cell subsets using chromatin immunoprecipitation and genome-wide promoter microarrays

Breast Cancer Research

Volumn 16, Issue 1, 2014, Pages

  Jung, Karen ^a   Wang, Peng ^a   Gupta, Nidhi ^a   Gopal, Keshav ^a   Wu, Fang ^a   Ye, Xiaoxia ^a   Alshareef, Abdulraheem ^a   Bigras, Gilbert ^a   McMullen, Todd P ^a   Abdulkarim, Bassam S ^b   Lai, Raymond ^a,c  

^a UNIVERSITY OF ALBERTA   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c DynaLIFE Dx   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MUCIN; MUCIN 15; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; BMI1 PROTEIN; BMI1 PROTEIN, HUMAN; CD133 ANTIGEN; G PROTEIN COUPLED RECEPTOR; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; LGR5 PROTEIN, HUMAN; MUC15 PROTEIN, HUMAN; PEPTIDE; SOX2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BMI1 GENE; BREAST CANCER; CANCER CELL; CANCER STEM CELL; CARCINOGENESIS; CCND1 GENE; CELL POPULATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA SEQUENCE; DOWN REGULATION; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENE TARGETING; GPR49 GENE; HUMAN; HUMAN CELL; MCF 7 CELL LINE; MUC15 GENE; NONHUMAN; PROM1 GENE; PROMOTER REGION; PROTEIN BINDING; PROTEIN LOCALIZATION; UPREGULATION; ADENOCARCINOMA; BREAST TUMOR; FEMALE; GENETICS; METABOLISM; PHENOTYPE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADENOCARCINOMA; ANTIGENS, CD; BREAST NEOPLASMS; CHROMATIN IMMUNOPRECIPITATION; FEMALE; GLYCOPROTEINS; HUMANS; MCF-7 CELLS; MUCINS; PEPTIDES; PHENOTYPE; POLYCOMB REPRESSIVE COMPLEX 1; PROMOTER REGIONS, GENETIC; RECEPTORS, G-PROTEIN-COUPLED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SOXB1 TRANSCRIPTION FACTORS;

EID: 84988859506     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/s13058-014-0470-2     Document Type: Article

References (56)

1. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S: Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
2. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, Gifford DK, Melton DA, Jaenisch R, Young RA: Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005, 122:947-956.
3. Sarkar A, Hochedlinger K: The sox family of transcription factors: versatile regulators of stem and progenitor cell fate. Cell Stem Cell 2013, 12:15-30.
4. Arnold K, Sarkar A, Yram MA, Polo JM, Bronson R, Sengupta S, Seandel M, Geijsen N, Hochedlinger K: Sox2(+) adult stem and progenitor cells are important for tissue regeneration and survival of mice. Cell Stem Cell 2011, 9:317-329.
5. Roy S, Gascard P, Dumont N, Zhao J, Pan D, Petrie S, Margeta M, Tlsty TD: Rare somatic cells from human breast tissue exhibit extensive lineage plasticity. Proc Natl Acad Sci U S A 2013, 110:4598-4603.
6. Wang Y, Dong J, Li D, Lai L, Siwko S, Li Y, Liu M: Lgr4 regulates mammary gland development and stem cell activity through the pluripotency transcription factor Sox2. Stem Cells 2013, 31:1921-1931.
7. Leis O, Eguiara A, Lopez-Arribillaga E, Alberdi MJ, Hernandez-Garcia S, Elorriaga K, Pandiella A, Rezola R, Martin AG: Sox2 expression in breast tumors and activation in breast cancer stem cells. Oncogene 2012, 31:1354-1365.
8. Chen Y, Shi L, Zhang L, Li R, Liang J, Yu W, Sun L, Yang X, Wang Y, Zhang Y, Shang Y: The molecular mechanism governing the oncogenic potential of SOX2 in breast cancer. J Biol Chem 2008, 283:17969-17978.
9. Rudin CM, Durinck S, Stawiski EW, Poirier JT, Modrusan Z, Shames DS, Bergbower EA, Guan Y, Shin J, Guillory J, Rivers CS, Foo CK, Bhatt D, Stinson J, Gnad F, Haverty PM, Gentleman R, Chaudhuri S, Janakiraman V, Jaiswal BS, Parikh C, Yuan W, Zhang Z, Koeppen H, Wu TD, Stern HM, Yauch RL, Huffman KE, Paskulin DD, Illei PB, et al: Comprehensive genomic analysis identifies SOX2 as a frequently amplified gene in small-cell lung cancer. Nat Genet 2012, 44:1111-1116.
10. Annovazzi L, Mellai M, Caldera V, Valente G, Schiffer D: SOX2 expression and amplification in gliomas and glioma cell lines. Cancer Genomics Proteomics 2011, 8:139-147.
11. Zhang J, Chang DY, Mercado-Uribe I, Liu J: Sex-determining region Y-box 2 expression predicts poor prognosis in human ovarian carcinoma. Hum Pathol 2012, 43:1405-1412.
12. Basu-Roy U, Seo E, Ramanathapuram L, Rapp TB, Perry JA, Orkin SH, Mansukhani A, Basilico C: Sox2 maintains self renewal of tumor-initiating cells in osteosarcomas. Oncogene 2012, 31:2270-2282.
13. Neumann J, Bahr F, Horst D, Kriegl L, Engel J, Luque RM, Gerhard M, Kirchner T, Jung A: SOX2 expression correlates with lymph-node metastases and distant spread in right-sided colon cancer. BMC Cancer 2011, 11:518.
14. Laga AC, Zhan Q, Weishaupt C, Ma J, Frank MH, Murphy GF: SOX2 and nestin expression in human melanoma: an immunohistochemical and experimental study. Exp Dermatol 2011, 20:339-345.
15. Lengerke C, Fehm T, Kurth R, Neubauer H, Scheble V, Muller F, Schneider F, Petersen K, Wallwiener D, Kanz L, Fend F, Perner S, Bareiss PM, Staebler A: Expression of the embryonic stem cell marker SOX2 in early-stage breast carcinoma. BMC Cancer 2011, 28:11:42.
16. Hagerstrand D, He X, Bradic Lindh M, Hoefs S, Hesselager G, Ostman A, Nister M: Identification of a SOX2-dependent subset of tumor-and sphere-forming glioblastoma cells with a distinct tyrosine kinase inhibitor sensitivity profile. Neuro Oncol 2011, 13:1178-1191.
17. Nakatsugawa M, Takahashi A, Hirohashi Y, Torigoe T, Inoda S, Murase M, Asanuma H, Tamura Y, Morita R, Michifuri Y, Kondo T, Hasegawa T, Takahashi H, Sato N: SOX2 is overexpressed in stem-like cells of human lung adenocarcinoma and augments the tumorigenicity. Lab Invest 2011, 91:1796-1804.
18. Wu F, Zhang J, Wang P, Ye X, Jung K, Bone KM, Pearson JD, Ingham RJ, McMullen TP, Ma Y, Lai R: Identification of two novel phenotypically distinct breast cancer cell subsets based on Sox2 transcription activity. Cell Signal 2012, 24:1989-1998.
19. Zhang Y, Eades G, Yao Y, Li Q, Zhou Q: Estrogen receptor alpha signaling regulates breast tumor-initiating cells by down-regulating miR-140 which targets the transcription factor SOX2. J Biol Chem2012, 287:41514-41522.
20. Singh S, Trevino J, Bora-Singhal N, Coppola D, Haura E, Altiok S, Chellappan SP: 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.
21. Lin CW, Liao MY, Lin WW, Wang YP, Lu TY, Wu HC: Epithelial cell adhesion molecule regulates tumor initiation and tumorigenesis via activating reprogramming factors and epithelial-mesenchymal transition gene expression in colon cancer. J Biol Chem 2012, 287:39449-39459.
22. Chen YL, Wang SY, Liu RS, Wang HE, Chen JC, Chiou SH, Chang CA, Lin LT, Tan DT, Lee YJ: Remnant living cells that escape cell loss in late-stage tumors exhibit cancer stem cell-like characteristics. Cell Death Dis 2012, 3:e399.
23. 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:e41335.
24. Lu X, Deng Q, Li H, Suo Z: Altered characteristics of cancer stem/initiating cells in a breast cancer cell line treated with persistent 5-FU chemotherapy. Exp Ther Med 2011, 2:821-826.
25. Wang X, Liang Y, Chen Q, Xu HM, Ge N, Luo RZ, Shao JY, He Z, Zeng YX, Kang T, Yun JP, Xie F: Prognostic significance of SOX2 expression in nasopharyngeal carcinoma. Cancer Invest 2012, 30:79-85.
26. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, Weinberg RA: An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008, 40:499-507.
27. Gomez-Mateo Mdel C, Piqueras M, Pahlman S, Noguera R, Navarro S: Prognostic value of SOX2 expression in neuroblastoma. Genes Chromosomes Cancer 2011, 50:374-377.
28. 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, 34:1193-1198.
29. Simoes BM, Piva M, Iriondo O, Comaills V, Lopez-Ruiz JA, Zabalza I, Mieza JA, Acinas O, Vivanco MD: Effects of estrogen on the proportion of stem cells in the breast. Breast Cancer Res Treat 2011, 129:23-35.
30. Tomioka M, Nishimoto M, Miyagi S, Katayanagi T, Fukui N, Niwa H, Muramatsu M, Okuda A: Identification of Sox-2 regulatory region which is under the control of Oct-3/4-Sox-2 complex. Nucleic Acids Res 2002, 30:3202-3213.
31. O'Geen H, Nicolet CM, Blahnik K, Green R, Farnham PJ: Comparison of sample preparation methods for ChIP-chip assays. Biotechniques 2006, 41:577-580.
32. Spandidos A, Wang X, Wang H, Seed B: PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res 2010, 38:D792-D799.
33. Wang X, Spandidos A, Wang H, Seed B: PrimerBank: a PCR primer database for quantitative gene expression analysis, 2012 update. Nucleic Acids Res 2012, 40:D1144-D1149.
34. Zhang J, Wang P, Wu F, Li M, Sharon D, Ingham RJ, Hitt M, McMullen TP, Lai R: Aberrant expression of the transcriptional factor Twist1 promotes invasiveness in ALK-positive anaplastic large cell lymphoma. Cell Signal 2012, 24:852-858.
35. Mi H, Muruganujan A, Thomas PD: PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees. Nucleic Acids Res 2013, 41:D377-D386.
36. Medema JP: Cancer stem cells: the challenges ahead. Nat Cell Biol 2013, 15:338-344.
37. Alison MR, Islam S, Wright NA: Stem cells in cancer: instigators and propagators? J Cell Sci 2010, 123:2357-2368.
38. Gupta S, Iljin K, Sara H, Mpindi JP, Mirtti T, Vainio P, Rantala J, Alanen K, Nees M, Kallioniemi O: FZD4 as a mediator of ERG oncogene-induced WNT signaling and epithelial-to-mesenchymal transition in human prostate cancer cells. Cancer Res 2010, 70:6735-6745.
39. Jin X, Jeon HY, Joo KM, Kim JK, Jin J, Kim SH, Kang BG, Beck S, Lee SJ, Kim JK, Park AK, Park WY, Choi YJ, Nam DH, Kim H: Frizzled 4 regulates stemness and invasiveness of migrating glioma cells established by serial intracranial transplantation. Cancer Res 2011, 71:3066-3075.
40. Nielsen TO, Andrews HN, Cheang M, Kucab JE, Hsu FD, Ragaz J, Gilks CB, Makretsov N, Bajdik CD, Brookes C, Neckers LM, Evdokimova V, Huntsman DG, Dunn SE: Expression of the insulin-like growth factor I receptor and urokinase plasminogen activator in breast cancer is associated with poor survival: potential for intervention with 17-allylamino geldanamycin. Cancer Res 2004, 64:286-291.
41. Oakes SR, Naylor MJ, Asselin-Labat ML, Blazek KD, Gardiner-Garden M, Hilton HN, Kazlauskas M, Pritchard MA, Chodosh LA, Pfeffer PL, Lindeman GJ, Visvader JE, Ormandy CJ: The Ets transcription factor Elf5 specifies mammary alveolar cell fate. Genes Dev 2008, 22:581-586.
42. Chen D, Bhat-Nakshatri P, Goswami C, Badve S, Nakshatri H: ANTXR1, a stem cell-enriched functional biomarker, connects collagen signaling to cancer stem-like cells and metastasis in breast cancer. Cancer Res 2013, 73:5821-5833.
43. Chaudhary A, Hilton MB, Seaman S, Haines DC, Stevenson S, Lemotte PK, Tschantz WR, Zhang XM, Saha S, Fleming T, St Croix B: TEM8/ANTXR1 blockade inhibits pathological angiogenesis and potentiates tumoricidal responses against multiple cancer types. Cancer Cell 2012, 21:212-226.
44. Pallesen LT, Berglund L, Rasmussen LK, Petersen TE, Rasmussen JT: Isolation and characterization of MUC15, a novel cell membrane-associated mucin. Eur J Biochem 2002, 269:2755-2763.
45. Oskarsson T, Acharyya S, Zhang XH, Vanharanta S, Tavazoie SF, Morris PG, Downey RJ, Manova-Todorova K, Brogi E, Massague J: Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat Med 2011, 17:867-874.
46. Medeiros RB, Papenfuss KJ, Hoium B, Coley K, Jadrich J, Goh SK, Elayaperumal A, Herrera JE, Resnik E, Ni HT: Novel sequential ChIP and simplified basic ChIP protocols for promoter co-occupancy and target gene identification in human embryonic stem cells. BMC Biotechnol 2009, 9:59.
47. Huang J, Che MI, Huang YT, Shyu MK, Huang YM, Wu YM, Lin WC, Huang PH, Liang JT, Lee PH, Huang MC: Overexpression of MUC15 activates extracellular signal-regulated kinase 1/2 and promotes the oncogenic potential of human colon cancer cells. Carcinogenesis 2009, 30:1452-1458.
48. Iida H, Suzuki M, Goitsuka R, Ueno H: Hypoxia induces CD133 expression in human lung cancer cells by up-regulation of OCT3/4 and SOX2. Int J Oncol 2012, 40:71-79.
49. Yu KR, Yang SR, Jung JW, Kim H, Ko K, Han DW, Park SB, Choi SW, Kang SK, Scholer H, Kang KS: CD49f enhances multipotency and maintains stemness through the direct regulation of OCT4 and SOX2. Stem Cells 2012, 30:876-887.
50. Apostolou P, Toloudi M, Chatziioannou M, Ioannou E, Papasotiriou I: Cancer stem cells stemness transcription factors expression correlates with breast cancer disease stage. Curr Stem Cell Res Ther 2012, 7:415-419.
51. Sato T, Clevers H: Growing self-organizing mini-guts from a single intestinal stem cell: mechanism and applications. Science 2013, 340:1190-1194.
52. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB: Identification of human brain tumor initiating cells. Nature 2004, 432:396-401.
53. Wu F, Ye X, Wang P, Jung K, Wu C, Douglas D, Kneteman N, Bigras G, Ma Y, Lai R: Sox2 suppresses the invasiveness of breast cancer cells via a mechanism that is dependent on Twist1 and the status of Sox2 transcription activity. BMC Cancer 2013, 13:317.
54. Wang RY, Chen L, Chen HY, Hu L, Li L, Sun HY, Jiang F, Zhao J, Liu GM, Tang J, Chen CY, Yang YC, Chang YX, Liu H, Zhang J, Yang Y, Huang G, Shen F, Wu MC, Zhou WP, Wang HY: MUC15 inhibits dimerization of EGFR and PI3K-AKT signaling and is associated with aggressive hepatocellular carcinomas in patients. Gastroenterology 2013, 145:1436-1448.
55. Nam KH, Noh TW, Chung SH, Lee SH, Lee MK, Hong SW, Chung WY, Lee EJ, Park CS: Expression of the membrane mucins MUC4 and MUC15, potential markers of malignancy and prognosis, in papillary thyroid carcinoma. Thyroid 2011, 21:745-750.
56. Riker AI, Enkemann SA, Fodstad O, Liu S, Ren S, Morris C, Xi Y, Howell P, Metge B, Samant RS, Shevde LA, Li W, Eschrich S, Daud A, Ju J, Matta J: The gene expression profiles of primary and metastatic melanoma yields a transition point of tumor progression and metastasis. BMC Med Genomics 2008, 1:13-8794-1-13.