Co-expression of putative stemness and epithelial-to-mesenchymal transition markers on single circulating tumour cells from patients with early and metastatic breast cancer

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Papadaki, Maria A ^a   Kallergi, Galatea ^a   Zafeiriou, Zafeiris ^a,b   Manouras, Lefteris ^a   Theodoropoulos, Panayiotis A ^a   Mavroudis, Dimitris ^a,b   Georgoulias, Vassilis ^a,b   Agelaki, Sofia ^a,b  

^a UNIVERSITY OF CRETE   (Greece)

^b UNIVERSITY HOSPITAL OF HERAKLION   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE ISOENZYME 1; TRANSCRIPTION FACTOR TWIST; ISOENZYME; NUCLEAR PROTEIN; RETINAL DEHYDROGENASE; TUMOR MARKER; TWIST1 PROTEIN, HUMAN;

ARTICLE; BREAST CANCER; BREAST METASTASIS; CANCER STEM CELL; CELLULAR DISTRIBUTION; CIRCULATING TUMOR CELL; CONTROLLED STUDY; EARLY BREAST CANCER; EARLY CANCER; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; MAJOR CLINICAL STUDY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; BREAST TUMOR; CELL NUCLEUS; FEMALE; GENETICS; HEPG2 CELL LINE; MCF 7 CELL LINE; METABOLISM; METASTASIS; PATHOLOGY; PROCEDURES; SINGLE CELL ANALYSIS; TUMOR CELL LINE; TUMOR EMBOLISM;

BREAST NEOPLASMS; CELL LINE, TUMOR; CELL NUCLEUS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HEP G2 CELLS; HUMANS; ISOENZYMES; MCF-7 CELLS; NEOPLASM METASTASIS; NEOPLASTIC CELLS, CIRCULATING; NUCLEAR PROTEINS; RETINAL DEHYDROGENASE; SINGLE-CELL ANALYSIS; TUMOR MARKERS, BIOLOGICAL; TWIST TRANSCRIPTION FACTOR;

EID: 84906927974     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-651     Document Type: Article

References (47)

1. Cristofanilli M, Broglio KR, Guarneri V, Jackson S, Fritsche HA, Islam R, Dawood S, Reuben JM, Kau SW, Lara JM, Krishnamurthy S, Ueno NT, Hortobagyi GN, Valero V. Circulating tumor cells in metastatic breast cancer: biologic staging beyond tumor burden. Clin Breast Cancer 2007, 7:471-479.
2. Xenidis N, Ignatiadis M, Apostolaki S, Perraki M, Kalbakis K, Agelaki S, Stathopoulos EN, Chlouverakis G, Lianidou E, Kakolyris S, Georgoulias V, Mavroudis D. Cytokeratin-19 mRNA-positive circulating tumor cells after adjuvant chemotherapy in patients with early breast cancer. J Clin Oncol 2009, 27:2177-2184. 10.1200/JCO.2008.18.0497, 19332733.
3. Bidard FC, Vincent-Salomon A, Sigal-Zafrani B, Dieras V, Mathiot C, Mignot L, Thiery JP, Sastre-Garau X, Pierga JY. Prognosis of women with stage IV breast cancer depends on detection of circulating tumor cells rather than disseminated tumor cells 11. Ann Oncol 2008, 19:496-500.
4. Androulakis N, Agelaki S, Perraki M, Apostolaki S, Bozionelou V, Pallis A, Kalbakis K, Xyrafas A, Mavroudis D, Georgoulias V. Clinical relevance of circulating CK-19mRNA-positive tumour cells before front-line treatment in patients with metastatic breast cancer. Br J Cancer 2012, 106:1917-1925. 10.1038/bjc.2012.202, 3388568, 22669159.
5. Hoon DS, Ferris R, Tanaka R, Chong KK, ix-Panabieres C, Pantel K. Molecular mechanisms of metastasis. J Surg Oncol 2011, 103:508-517. 10.1002/jso.21690, 21480243.
6. Croker AK, Goodale D, Chu J, Postenka C, Hedley BD, Hess DA, Allan AL. High aldehyde dehydrogenase and expression of cancer stem cell markers selects for breast cancer cells with enhanced malignant and metastatic ability. J Cell Mol Med 2008, 13:2236-2252.
7. Lohberger B, Rinner B, Stuendl N, Absenger M, Liegl-Atzwanger B, Walzer SM, Windhager R, Leithner A. Aldehyde dehydrogenase 1, a potential marker for cancer stem cells in human sarcoma 5. PLoS One 2012, 7:e43664. 10.1371/journal.pone.0043664, 3426519, 22928012.
8. Al-Hajj M, Wicha MS, ito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003, 100:3983-3988. 10.1073/pnas.0530291100, 153034, 12629218.
9. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, Hur MH, Diebel ME, Monville F, Dutcher J, Brown M, Viens P, Xerri L, Bertucci F, Stassi G, Dontu G, Birnbaum D, Wicha MS. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 2009, 69:1302-1313. 10.1158/0008-5472.CAN-08-2741, 2819227, 19190339.
10. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S, Schott A, Hayes D, Birnbaum D, Wicha MS, Dontu G. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007, 1:555-567. 10.1016/j.stem.2007.08.014, 2423808, 18371393.
11. Ohi Y, Umekita Y, Yoshioka T, Souda M, Rai Y, Sagara Y, Sagara Y, Sagara Y, Tanimoto A. Aldehyde dehydrogenase 1 expression predicts poor prognosis in triple-negative breast cancer. Histopathology 2011, 59:776-780. 10.1111/j.1365-2559.2011.03884.x, 22014057.
12. Yoshioka T, Umekita Y, Ohi Y, Souda M, Sagara Y, Sagara Y, Sagara Y, Rai Y, Tanimoto A. Aldehyde dehydrogenase 1 expression is a predictor of poor prognosis in node-positive breast cancers: a long-term follow-up study. Histopathology 2011, 58:608-616. 10.1111/j.1365-2559.2011.03781.x, 21371077.
13. Gradilone A, Naso G, Raimondi C, Cortesi E, Gandini O, Vincenzi B, Saltarelli R, Chiapparino E, Spremberg F, Cristofanilli M, Frati L, Agliano` AM, Gazzaniga P. Circulating tumor cells (CTCs) in metastatic breast cancer (MBC): prognosis, drug resistance and phenotypic characterization. Ann Oncol 2011, 22:86-92. 10.1093/annonc/mdq323, 20603432.
14. Theodoropoulos PA, Polioudaki H, Agelaki S, Kallergi G, Saridaki Z, Mavroudis D, Georgoulias V. Circulating tumor cells with a putative stem cell phenotype in peripheral blood of patients with breast cancer. Cancer Lett 2010, 288:99-106. 10.1016/j.canlet.2009.06.027, 19619935.
15. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 2009, 9:265-273. 10.1038/nrc2620, 19262571.
16. Willipinski-Stapelfeldt B, Riethdorf S, Assmann V, Woelfle U, Rau T, Sauter G, Heukeshoven J, Pantel K. Changes in cytoskeletal protein composition indicative of an epithelial-mesenchymal transition in human micrometastatic and primary breast carcinoma cells. Clin Cancer Res 2005, 11:8006-8014. 10.1158/1078-0432.CCR-05-0632, 16299229.
17. Zeisberg M, Neilson EG. Biomarkers for epithelial-mesenchymal transitions. J Clin Invest 2009, 119:1429-1437. 10.1172/JCI36183, 2689132, 19487819.
18. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis 1. Cell 2004, 117:927-939. 10.1016/j.cell.2004.06.006, 15210113.
19. Martin TA, Goyal A, Watkins G, Jiang WG. Expression of the transcription factors snail, slug, and twist and their clinical significance in human breast cancer. Ann Surg Oncol 2005, 12:488-496. 10.1245/ASO.2005.04.010, 15864483.
20. Yang J, Mani SA, Weinberg RA. Exploring a new twist on tumor metastasis. Cancer Res 2006, 66:4549-4552. 10.1158/0008-5472.CAN-05-3850, 16651402.
21. Watson MA, Ylagan LR, Trinkaus KM, Gillanders WE, Naughton MJ, Weilbaecher KN, Fleming TP, Aft RL. Isolation and molecular profiling of bone marrow micrometastases identifies TWIST1 as a marker of early tumor relapse in breast cancer patients 1. Clin Cancer Res 2007, 13:5001-5009. 10.1158/1078-0432.CCR-07-0024, 2680916, 17785550.
22. Kallergi G, Papadaki MA, Politaki E, Mavroudis D, Georgoulias V, Agelaki S. Epithelial-mesenchymal transition markers expressed in circulating tumor cells of early and metastatic breast cancer patients. Breast Cancer Res 2011, 13:R59. 10.1186/bcr2896, 3218948, 21663619.
23. Strati A, Markou A, Parisi C, Politaki E, Mavroudis D, Georgoulias V, Lianidou E. Gene expression profile of circulating tumor cells in breast cancer by RT-qPCR 2. BMC Cancer 2011, 11:422. 10.1186/1471-2407-11-422, 3224356, 21967632.
24. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA. The epithelial-mesenchymal transition generates cells with properties of stem cells 16. Cell 2008, 133:704-715. 10.1016/j.cell.2008.03.027, 2728032, 18485877.
25. Shipitsin M, Campbell LL, Argani P, Weremowicz S, Bloushtain-Qimron N, Yao J, Nikolskaya T, Serebryiskaya T, Beroukhim R, Hu M, Halushka MK, Sukumar S, Parker LM, Anderson KS, Harris LN, Garber JE, Richardson AL, Schnitt SJ, Nikolsky Y, Gelman RS, Polyak K. Molecular definition of breast tumor heterogeneity4. Cancer Cell 2007, 11:259-273. 10.1016/j.ccr.2007.01.013, 17349583.
26. Morel AP, Lievre M, Thomas C, Hinkal G, Ansieau S, Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One 2008, 3:e2888. 10.1371/journal.pone.0002888, 2492808, 18682804.
27. Aktas B, Tewes M, Fehm T, Hauch S, Kimmig R, Kasimir-Bauer S. Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Res 2009, 11:R46. 10.1186/bcr2333, 2750105, 19589136.
28. Raimondi C, Gradilone A, Naso G, Vincenzi B, Petracca A, Nicolazzo C, Palazzo A, Saltarelli R, Spremberg F, Cortesi E, Gazzaniga P. Epithelial-mesenchymal transition and stemness features in circulating tumor cells from breast cancer patients. Breast Cancer Res Treat 2011, 130:449-455. 10.1007/s10549-011-1373-x, 21298334.
29. Kallergi G, Mavroudis D, Georgoulias V, Stournaras C. Phosphorylation of FAK, PI-3 K, and impaired actin organization in CK-positive micrometastatic breast cancer cells. Mol Med 2007, 13:79-88. 1869618, 17515959.
30. Kallergi G, Markomanolaki H, Giannoukaraki V, Papadaki MA, Strati A, Lianidou ES, Georgoulias V, Mavroudis D, Agelaki S. Hypoxia-inducible factor-1alpha and vascular endothelial growth factor expression in circulating tumor cells of breast cancer patients. Breast Cancer Res 2009, 11:R84. 10.1186/bcr2452, 2815547, 19919679.
31. Meng S, Tripathy D, Frenkel EP, Shete S, Naftalis EZ, Huth JF, Beitsch PD, Leitch M, Hoover S, Euhus D, Haley B, Morrison L, Fleming TP, Herlyn D, Terstappen LW, Fehm T, Tucker TF, Lane N, Wang J, Uhr JW. Circulating tumor cells in patients with breast cancer dormancy. Clin Cancer Res 2004, 10:8152-8162. 10.1158/1078-0432.CCR-04-1110, 15623589.
32. Hollier BG, Evans K, Mani SA. The epithelial-to-mesenchymal transition and cancer stem cells: a coalition against cancer therapies. J Mammary Gland Biol Neoplasia 2009, 14:29-43. 10.1007/s10911-009-9110-3, 19242781.
33. Avoranta ST, Korkeila EA, Ristamaki RH, Syrjanen KJ, Carpen OM, Pyrhonen SO, Sundstrom JT. ALDH1 expression indicates chemotherapy resistance and poor outcome in node-negative rectal cancer. Hum Pathol 2013, 44:966-974. 10.1016/j.humpath.2012.10.003, 23332924.
34. Neumeister V, Agarwal S, Bordeaux J, Camp RL, Rimm DL. In situ identification of putative cancer stem cells by multiplexing ALDH1, CD44, and cytokeratin identifies breast cancer patients with poor prognosis. Am J Pathol 2010, 176:2131-2138. 10.2353/ajpath.2010.090712, 2861079, 20228222.
35. Su Y, Qiu Q, Zhang X, Jiang Z, Leng Q, Liu Z, Stass SA, Jiang F. Aldehyde dehydrogenase 1 A1-positive cell population is enriched in tumor-initiating cells and associated with progression of bladder cancer. Cancer Epidemiol Biomarkers Prev 2010, 19:327-337. 10.1158/1055-9965.EPI-09-0865, 3544173, 20142235.
36. Li T, Su Y, Mei Y, Leng Q, Leng B, Liu Z, Stass SA, Jiang F. ALDH1A1 is a marker for malignant prostate stem cells and predictor of prostate cancer patients' outcome. Lab Invest 2010, 90:234-244. 10.1038/labinvest.2009.127, 3552330, 20010854.
37. Deng S, Yang X, Lassus H, Liang S, Kaur S, Ye Q, Li C, Wang LP, Roby KF, Orsulic S, Connolly DC, Zhang Y, Montone K, Bu¨tzow R, Coukos G, Zhang L. Distinct expression levels and patterns of stem cell marker, aldehyde dehydrogenase isoform 1 (ALDH1), in human epithelial cancers. PLoS One 2010, 5:e10277. 10.1371/journal.pone.0010277, 2858084, 20422001.
38. Kang Y, Massague J. Epithelial-mesenchymal transitions: twist in development and metastasis 1. Cell 2004, 118:277-279. 10.1016/j.cell.2004.07.011, 15294153.
39. Schwoebel ED, Moore MS. The control of gene expression by regulated nuclear transport. Essays Biochem 2000, 36:105-113.
40. Yuen HF, Chua CW, Chan YP, Wong YC, Wang X, Chan KW. Significance of TWIST and E-cadherin expression in the metastatic progression of prostatic cancer. Histopathology 2007, 50:648-658. 10.1111/j.1365-2559.2007.02665.x, 17394502.
41. Gong T, Xue Z, Tang S, Zheng X, Xu G, Gao L, Zhao G, Hong L, Tang G, Zhang H, Wang R, Jiang Y, Fan D. Nuclear expression of Twist promotes lymphatic metastasis in esophageal squamous cell carcinoma. Cancer Biol Ther 2012, 13:606-613. 10.4161/cbt.19851, 22441818.
42. Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, Isakoff SJ, Ciciliano JC, Wells MN, Shah AM, Concannon KF, Donaldson MC, Sequist LV, Brachtel E, Sgroi D, Baselga J, Ramaswamy S, Toner M, Haber DA, Maheswaran S. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 2013, 339:580-584. 10.1126/science.1228522, 3760262, 23372014.
43. Kasimir-Bauer S, Hoffmann O, Wallwiener D, Kimmig R, Fehm T. Expression of stem cell and epithelial-mesenchymal transition markers in primary breast cancer patients with circulating tumor cells. Breast Cancer Res 2012, 14:R15. 10.1186/bcr3099, 3496132, 22264265.
44. Vazquez-Martin A, Oliveras-Ferraros C, Cufi S, Del BS, Martin-Castillo B, Menendez JA. Metformin regulates breast cancer stem cell ontogeny by transcriptional regulation of the epithelial-mesenchymal transition (EMT) status 7. Cell Cycle 2010, 9:3807-3814. 10.4161/cc.9.18.13131, 20890129.
45. Yang MH, Hsu DS, Wang HW, Wang HJ, Lan HY, Yang WH, Huang CH, Kao SY, Tzeng CH, Tai SK, Chang SY, Lee OK, Wu KJ. Bmi1 is essential in Twist1-induced epithelial-mesenchymal transition. Nat Cell Biol 2010, 12:982-992. 10.1038/ncb2099, 20818389.
46. Vesuna F, Lisok A, Kimble B, Domek J, Kato Y, van der Groep P, Artemov D, Kowalski J, Carraway H, van Diest P, Raman V. Twist contributes to hormone resistance in breast cancer by downregulating estrogen receptor-alpha 16. Oncogene 2012, 31:3223-3234. 10.1038/onc.2011.483, 3276743, 22056872.
47. Li J, Zhou BP. Activation of beta-catenin and Akt pathways by Twist are critical for the maintenance of EMT associated cancer stem cell-like characters. BMC Cancer 2011, 11:49. 10.1186/1471-2407-11-49, 3040162, 21284870.