Expression of stemness genes in primary breast cancer tissues: The role of SOX2 as a prognostic marker for detection of early recurrence

Oncotarget

Volumn 5, Issue 20, 2014, Pages 9678-9688

  Finicelli, Mauro ^a   Benedetti, Giovanni ^b   Squillaro, Tiziana ^a   Pistilli, Barbara ^b   Marcellusi, Andrea ^c   Mariani, Paola ^b   Santinelli, Alfredo ^d   Latini, Luciano ^b   Galderisi, Umberto ^e,f   Giordano, Antonio ^a,e  

^a Human Health Foundation   (Italy)

^b Macerata Hospital   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^e TEMPLE UNIVERSITY   (United States)

^f SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

Breast cancer; Gene expression; Recurrence; SOX2; Stemness genes

Indexed keywords

GROWTH DIFFERENTIATION FACTOR 3; KRUPPEL LIKE FACTOR 4; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; SOX2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX; TRANSCRIPTOME; TUMOR MARKER;

ARTICLE; BREAST CANCER; CANCER GRADING; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER SIZE; CANCER TISSUE; CONTROLLED STUDY; EARLY CANCER; FEMALE; GDF3 GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GENETIC CORRELATION; GENETIC MARKER; GENETIC RISK; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; KLF4 GENE; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; NANOG GENE; OCT3 GENE; ONSET AGE; PRIMARY TUMOR; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOX2 GENE; TUMOR INVASION; ADULT; AGED; BREAST TUMOR; CANCER STEM CELL; DISEASE COURSE; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; MIDDLE AGED; PATHOLOGY; PHYSIOLOGY; PROGNOSIS; TUMOR RECURRENCE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; BIOMARKERS, TUMOR; BREAST NEOPLASMS; DISEASE PROGRESSION; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MIDDLE AGED; NEOPLASM RECURRENCE, LOCAL; NEOPLASTIC STEM CELLS; PROGNOSIS; SOXB1 TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84922425839     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1936     Document Type: Article

References (49)

1. Lu J., Steeg P.S., Price J.E., Krishnamurthy S., Mani S.A., Reuben J., Cristofanilli M., Dontu G., Bidaut L., Valero V., Hortobagyi G.N. Yu D. Breast cancer metastasis: challenges and opportunities. Cancer Res. 2009; 69, 4951-4953.
2. Al-Ejeh F., Smart C.E., Morrison B.J., Chenevix-Trench G., Lopez J.A., Lakhani S.R., Brown M.P. Khanna K.K. Breast cancer stem cells: treatment resistance and therapeutic opportunities. Carcinogenesis. 2011; 32, 650-658.
3. Nakshatri H., Srour E.F. Badve S. Breast cancer stem cells and intrinsic subtypes: controversies rage on. Curr Stem Cell Res Ther. 2009; 4, 50-60.
4. Polyak K. Heterogeneity in breast cancer. J Clin Invest. 2011; 121, 3786-3788.
5. McDermott S.P. Wicha M.S. Targeting breast cancer stem cells. Mol Oncol. 2010; 4, 404-419.
6. Badve S., Nakshatri H. Breast-cancer stem cells-beyond semantics. Lancet Oncol. 2012; 13, e43-48.
7. Ali H.R., Dawson S.J., Blows F.M., Provenzano E., Pharoah P.D. Caldas C. Cancer stem cell markers in breast cancer: pathological, clinical and prognostic significance. Breast Cancer Res. 2011; 13, R118.
8. Ahmad A. Pathways to breast cancer recurrence. ISRN Oncol 2013, 2013:290568.
9. Anderson EC, Hessman C, Levin TG, Monroe MM, Wong MH. The role of colorectal cancer stem cells in metastatic disease and therapeutic response. Cancers (Basel). 2011; 3(1):319-39.
10. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer. 2005; 5(4):275-84.
11. Frank N.Y., Schatton T. Frank M.H. The therapeutic promise of the cancer stem cell concept. J Clin Invest. 2010; 120, 41-50.
12. Magee J.A., Piskounova E. Morrison S.J. Cancer stem cells: impact, heterogeneity, and uncertainty. Cancer Cell. 2012; 21, 283-296.
13. O'Brien CS, Howell SJ, Farnie G, Clarke RB. Resistance to endocrine therapy: are breast cancer stem cells the culprits? J Mammary Gland Biol Neoplasia. 2009; 14(1):45-54.
14. Chen S, Song X, Chen Z, Li X, Li M, Liu H, Li J. CD133 expression and the prognosis of colorectal cancer: a systematic review and meta-analysis. PLoS One. 2013;8(2):e56380.
15. Driessens G, Beck B, Caauwe A, Simons BD, Blanpain C. Defining the mode of tumour growth by clonal analysis. Nature. 2012; 488(7412):527-30.
16. Schepers A, Clevers H. Wnt signaling, stem cells, and cancer of the gastrointestinal tract. Cold Spring Harb Perspect Biol. 2012; 4(4):a007989.
17. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003 ;100(7):3983-8.
18. Leis O, Eguiara A, Lopez-Arribillaga E, Alberdi MJ, Hernandez-Garcia S, Elorriaga K, Pandiella A, Rezola R, Martin AG. Sox2 expression in breast tumours and activation in breast cancer stem cells. Oncogene. 2012; 31(11):1354-65.
19. 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. 2008, NatGenet.40(5):499-507.
20. Ehira N, Oshiumi H, Matsumoto M, Kondo T, Asaka M, Seya T. An embryo-specific expressing TGF-β family protein, growth-differentiation factor 3 (GDF3), augments progression of B16 melanoma. J Exp Clin Canc Res. 2010; 29:135
21. Glinsky GV "Stemness" genomics law governs clinical behavior of human cancer: implications for decision making in disease management. J Clin Oncol. 2008;26(17):2846-53.
22. Weiglet B, Peterse JL, van't Veer LJ. Breast cancer metastasis: markers and models. Nat Rev Cancer. 2005; 5(8):591-602.
23. Forte A, Schettino MT, Finicelli M, Cipollaro M, Colacurci N, Cobellis L, Galderisi U. Expression pattern of stemnessrelated genes in human endometrial and endometriotic tissues. Mol Med. 2009;15(11-12):392-401.
24. Melone MA, Giuliano M, Squillaro T, Alessio N, Casale F, Mattioli E, Cipollaro M, Giordano A, Galderisi U. Genes involved in regulation of stem cell properties: studies on their expression in a small cohort ofneuroblastoma patients. Cancer Biol Ther. 2009; 8(13):1300-6.
25. Tashima R, Nishimur R. Evaluation of an optimal cut-off point for the Ki-67 index as a prognostic factor in primary breast cancer. Cancer Research. 2012; Volume 72, Issue 24, Supplement 3
26. Phi JH, Park SH, Paek SH, Kim SK, Lee YJ, Park CK, Cho BK, Lee DH, Wang KC. Expression of Sox2 in mature and immature teratomas of central nervous system. Mod Pathol. 2007; 20(7):742-8.
27. 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(4):317-29.
28. Mehta S, Shelling A, Muthukaruppan A, Lasham A, Blenkiron C, Laking G, Print C. Predictive and prognostic molecular markers for cancer medicine. Ther Adv Med Oncol. 2010; 2(2):125-48.
29. Li X, Xu Y, Chen Y, Chen S, Jia X, Sun T, Liu Y, Li X, Xiang R, Li N. SOX2 promotes tumor metastasis by stimulating epithelial-to-mesenchymal transition via regulation of WNT/β-catenin signal network. Cancer Lett. 2013; 336(2):379-89.
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. 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.
32. Lengerke C, Fehm T, Kurth R, Neubauer H, Scheble V, Müller 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;11:42.
33. Bae KM, Su Z, Frye C, McClellan S, Allan RW, Andrejewski JT, Kelley V, Jorgensen M, Steindler DA, Vieweg J, Siemann DW. Expression of pluripotent stem cell reprogramming factors by prostate tumor initiating cells. J Urol. 2010; 183(5):2045-53.
34. Lu Y, Futtner C, Rock JR, Xu X, Whitworth W, Hogan BL, Onaitis MW. Evidence that SOX2 overexpression is oncogenic in the lung. PLoS One. 2010; 5(6):e11022.
35. Xu XL, Xing BC, Han HB, Zhao W, Hu MH, Xu ZL, Li JY, Xie Y, Gu J, Wang Y, Zhang ZQ. The properties of tumor-initiating cells from a hepatocellular carcinoma patient's primary and recurrent tumor Carcinogenesis. 2010;31(2):167-74.
36. Rodriguez-Pinilla SM, Sarrio D, Moreno-Bueno G, Rodriguez-Gil Y, Martinez MA, Hernandez L, Hardisson D, Reis-Filho JS, Palacios J. Sox2: a possible driver of the basal-like phenotype in sporadic breast cancer. Mod Pathol. 2007; 20(4):474-81.
37. Piva M, Domenici G, Iriondo O, et al. Sox2 promotes tamoxifen resistance in breast cancer cells. Piva M, Domenici G, Iriondo O, Rábano M, Simões BM, Comaills V, Barredo I, López-Ruiz JA, Zabalza I, Kypta R, Vivanco Md. EMBO Mol Med. 2014; 6(1):66-79.
38. Silva E.O. and Zurridda S: "Breast Cancer- A Practical Guide-Third Edition", Elsevier Saunders
39. Inwald EC, Klinkhammer-Schalke M, Hofstädter F, Zeman F, Koller M, Gerstenhauer M, Ortmann O. Ki-67 is a prognostic parameter in breast cancer patients: results of a large population-based cohort of a cancer registry. Breast Cancer Res Treat. 2013;139(2):539-52.
40. Korkaya H, Paulson A, Iovino F, Wicha MS. HER2 regulates the mammary stem/progenitor cell population driving tumorigenesis and invasion. Oncogene. 2008; 27(47):6120-30.
41. Magnifico A, Albano L, Campaner S, Delia D, Castiglioni F, Gasparini P, Sozzi G, Fontanella E, Menard S, Tagliabue E. Tumor-initiating cells of HER2-positive carcinoma cell lines express the highest oncoprotein levels and are sensitive to trastuzumab. Clin Cancer Res. 2009; 15(6):2010-21.
42. Ivshina AV, George J, Senko O, Mow B, Putti TC, Smeds J, Lindahl T, Pawitan Y, Hall P, Nordgren H, Wong JE, Liu ET, Bergh J, Kuznetsov VA, Miller LD. Genetic reclassification of histologic grade delineates new clinical subtypes of breast cancer. Cancer Res. 2006; 66(21):10292-301.
43. Wang ML, Chiou SH, Wu CW. Targeting cancer stem cells: emerging role of Nanog transcription factor. Onco Targets Ther. 2013; 6:1207-1220.
44. 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.
45. 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.
46. Li Q, Ling Y, Yu L. GDF3 inhibits the growth of breast cancer cells and promotes the apoptosis induced by Taxol. J Cancer Res Clin Oncol. 2012;138(6):1073-9.
47. Sethi S, Ali S, Philip PA, Sarkar FH. Clinical advances in molecular biomarkers for cancer diagnosis and therapy. Int J Mol Sci. 2013;14(7):14771-84.
48. Ribeiro-Silva A1, Zhang H, Jeffrey SS. RNA extraction from ten year old formalin-fixed paraffin-embedded breast cancer samples: a comparison of column purification and magnetic bead-based technologies. BMC Mol Biol. 2007;8:118.
49. Bretschneider N1, Brand H, Miller N, Lowery AJ, Kerin MJ, Gannon F, Denger S. Estrogen induces repression of the breast cancer and salivary gland expression gene in an estrogen receptor alpha-dependent manner. Cancer Res. 2008; 68(1):106-14.