Circulating tumor cells exhibit a biologically aggressive cancer phenotype accompanied by selective resistance to chemotherapy

Cancer Letters

Volumn 352, Issue 2, 2014, Pages 179-186

  Pavese, Janet M ^a   Bergan, Raymond C ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Circulating tumor cells; Drug resistance; EMT; Metastasis; MMP 2; Prostate cancer

Indexed keywords

ANTINEOPLASTIC AGENT; DOXORUBICIN; GELATINASE A; HEAT SHOCK PROTEIN 27; MITOXANTRONE; PACLITAXEL; PROTEIN TWIST1; TRANSCRIPTION FACTOR TWIST; TUMOR MARKER; UNCLASSIFIED DRUG; VIMENTIN; VINBLASTINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL LINE; CANCER GROWTH; CANCER INHIBITION; CANCER RESISTANCE; CELL FUNCTION; CELL INVASION; CIRCULATING TUMOR CELL; CONTROLLED STUDY; DISEASE ASSOCIATION; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; METASTASIS; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION;

MUS;

CIRCULATING TUMOR CELLS; DRUG RESISTANCE; EMT; METASTASIS; MMP-2; PROSTATE CANCER;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; MITOXANTRONE; NEOPLASM INVASIVENESS; NEOPLASTIC CELLS, CIRCULATING; PHENOTYPE; PROSTATIC NEOPLASMS; TUMOR BURDEN; TUMOR MARKERS, BIOLOGICAL; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84906053458     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.06.012     Document Type: Article

References (42)

1. 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.
2. Armstrong A.J., Marengo M.S., Oltean S., Kemeny G., Bitting R.L., Turnbull J.D., Herold C.I., Marcom P.K., George D.J., Garcia-Blanco M.A. Circulating tumor cells from patients with advanced prostate and breast cancer display both epithelial and mesenchymal markers. Mol. Cancer Res. 2011, 9:997-1007.
3. Baccelli I., Schneeweiss A., Riethdorf S., Stenzinger A., Schillert A., Vogel V., Klein C., Saini M., Bauerle T., Wallwiener M., Holland-Letz T., Hofner T., Sprick M., Scharpff M., Marme F., Sinn H.P., Pantel K., Weichert W., Trumpp A. Identification of a population of blood circulating tumor cells from breast cancer patients that initiates metastasis in a xenograft assay. Nat. Biotechnol. 2013, 31:539-544.
4. Breen M.J., Moran D.M., Liu W., Huang X., Vary C.P., Bergan R.C. Endoglin-mediated suppression of prostate cancer invasion is regulated by activin and bone morphogenetic protein type II receptors. PLoS ONE 2013, 8:e72407.
5. Carvalho F.L., Simons B.W., Antonarakis E.S., Rasheed Z., Douglas N., Villegas D., Matsui W., Berman D.M. Tumorigenic potential of circulating prostate tumor cells. Oncotarget 2013, 4:413-421.
6. Danila D.C., Anand A., Schultz N., Heller G., Wan M., Sung C.C., Dai C., Khanin R., Fleisher M., Lilja H., Scher H.I. Analytic and Clinical Validation of a Prostate Cancer-Enhanced Messenger RNA Detection Assay in Whole Blood as a Prognostic Biomarker for Survival. Eur. Urol. 2013.
7. Danila D.C., Fleisher M., Scher H.I. Circulating tumor cells as biomarkers in prostate cancer. Clin. Cancer Res. 2011, 17:3903-3912.
8. de Bono J.S., Scher H.I., Montgomery R.B., Parker C., Miller M.C., Tissing H., Doyle G.V., Terstappen L.W., Pienta K.J., Raghavan D. Circulating tumor cells predict survival benefit from treatment in metastatic castration-resistant prostate cancer. Clin. Cancer Res. 2008, 14:6302-6309.
9. De Cicco C., Ravasi L., Zorzino L., Sandri M.T., Botteri E., Verweij F., Granchi D., de Cobelli O., Paganelli G. Circulating levels of VCAM and MMP-2 may help identify patients with more aggressive prostate cancer. Curr. Cancer Drug Targets 2008, 8:199-206.
10. dos Reis S.T., Villanova F.E., Andrade P.M., Pontes J., de Sousa-Canavez J.M., Sanudo A., Antunes A.A., Dall'oglio M.F., Srougi M., Moreira Leite K.R. Matrix metalloproteinase-2 polymorphism is associated with prognosis in prostate cancer. Urol. Oncol. 2010, 28:624-627.
11. Foster C.S., Dodson A.R., Ambroisine L., Fisher G., Moller H., Clark J., Attard G., De-Bono J., Scardino P., Reuter V.E., Cooper C.S., Berney D.M., Cuzick J. Hsp-27 expression at diagnosis predicts poor clinical outcome in prostate cancer independent of ETS-gene rearrangement. Br. J. Cancer 2009, 101:1137-1144.
12. Glaessgen A., Jonmarker S., Lindberg A., Nilsson B., Lewensohn R., Ekman P., Valdman A., Egevad L. Heat shock proteins 27, 60 and 70 as prognostic markers of prostate cancer. APMIS 2008, 116:888-895.
13. Goodman O.B., Fink L.M., Symanowski J.T., Wong B., Grobaski B., Pomerantz D., Ma Y., Ward D.C., Vogelzang N.J. Circulating tumor cells in patients with castration-resistant prostate cancer baseline values and correlation with prognostic factors. Cancer Epidemiol. Biomarkers Prev. 2009, 18:1904-1913.
14. Goodman O.B., Symanowski J.T., Loudyi A., Fink L.M., Ward D.C., Vogelzang N.J. Circulating tumor cells as a predictive biomarker in patients with hormone-sensitive prostate cancer. Clin. Genitourin. Cancer 2011, 9:31-38.
15. Groot Koerkamp B., Rahbari N.N., Buchler M.W., Koch M., Weitz J. Circulating tumor cells and prognosis of patients with resectable colorectal liver metastases or widespread metastatic colorectal cancer: a meta-analysis. Ann. Surg. Oncol. 2013, 20:2156-2165.
16. Han L., Chen W., Zhao Q. Prognostic value of circulating tumor cells in patients with pancreatic cancer: a meta-analysis. Tumour Biol. 2014, 35:2473-2480.
17. Huang J., Wang K., Xu J., Zhang T. Prognostic significance of circulating tumor cells in non-small-cell lung cancer patients: a meta-analysis. PLoS ONE 2013, 8:e78070.
18. Huang X., Chen S., Xu L., Liu Y., Deb D.K., Platanias L.C., Bergan R.C. Genistein inhibits p38 map kinase activation, matrix metalloproteinase type 2, and cell invasion in human prostate epithelial cells. Cancer Res. 2005, 65:3470-3478.
19. Kallergi G., Papadaki M.A., Politaki E., Mavroudis D., Georgoulias V., Agelaki S. Epithelial to mesenchymal transition markers expressed in circulating tumour cells of early and metastatic breast cancer patients. Breast Cancer Res. 2011, 13:R59.
20. 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.
21. Lakshman M., Huang X., Ananthanarayanan V., Jovanovic B., Liu Y., Craft C.S., Romero D., Vary C.P., Bergan R.C. Endoglin suppresses human prostate cancer metastasis. Clin. Exp. Metastasis 2011, 28:39-53.
22. Lakshman M., Xu L., Ananthanarayanan V., Cooper J., Takimoto C.H., Helenowski I., Pelling J.C., Bergan R.C. Dietary genistein inhibits metastasis of human prostate cancer in mice. Cancer Res. 2008, 68:2024-2032.
23. Lee J.M., Dedhar S., Kalluri R., Thompson E.W. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J. Cell Biol. 2006, 172:973-981.
24. Li Y.M., Xu S.C., Li J., Han K.Q., Pi H.F., Zheng L., Zuo G.H., Huang X.B., Li H.Y., Zhao H.Z., Yu Z.P., Zhou Z., Liang P. Epithelial-mesenchymal transition markers expressed in circulating tumor cells in hepatocellular carcinoma patients with different stages of disease. Cell Death Dis. 2013, 4:e831.
25. Ligthart S.T., Coumans F.A., Bidard F.C., Simkens L.H., Punt C.J., de Groot M.R., Attard G., de Bono J.S., Pierga J.Y., Terstappen L.W. Circulating tumor cells count and morphological features in breast, colorectal and prostate cancer. PLoS One 2013, 8:e67148.
26. Liu Y., Jovanovic B., Pins M., Lee C., Bergan R.C. Over expression of endoglin in human prostate cancer suppresses cell detachment, migration and invasion. Oncogene 2002, 21:8272-8281.
27. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 2001, 25:402-408.
28. Miyake H., Muramaki M., Kurahashi T., Takenaka A., Fujisawa M. Expression of potential molecular markers in prostate cancer: correlation with clinicopathological outcomes in patients undergoing radical prostatectomy. Urol. Oncol. 2010, 28:145-151.
29. Miyake H., Muramaki M., Kurahashi T., Yamanaka K., Hara I., Fujisawa M. Enhanced expression of heat shock protein 27 following neoadjuvant hormonal therapy is associated with poor clinical outcome in patients undergoing radical prostatectomy for prostate cancer. Anticancer Res. 2006, 26:1583-1587.
30. Msaouel P., Koutsilieris M. Diagnostic value of circulating tumor cell detection in bladder and urothelial cancer: systematic review and meta-analysis. BMC Cancer 2011, 11:336.
31. Okegawa T., Hayashi K., Hara H., Nutahara K., Higashihara E. Immunomagnetic quantification of circulating tumor cells in patients with urothelial cancer. Int. J. Urol. 2010, 17:254-258.
32. Pavese J., Ogden I.M., Bergan R.C. An orthotopic murine model of human prostate cancer metastasis. J. Vis. Exp. 2013, e50873.
33. Pavese J.M., Farmer R.L., Bergan R.C. Inhibition of cancer cell invasion and metastasis by genistein. Cancer Metastasis Rev. 2010, 29:465-482.
34. Resel Folkersma L., San Jose Manso L., Galante Romo I., Moreno Sierra J., Olivier Gomez C. Prognostic significance of circulating tumor cell count in patients with metastatic hormone-sensitive prostate cancer. Urology 2012, 80:1328-1332.
35. Siegel R., Naishadham D., Jemal A. Cancer statistics. CA Cancer J. Clin. 2013, 63(2013):11-30.
36. Strijbos M.H., Gratama J.W., Schmitz P.I., Rao C., Onstenk W., Doyle G.V., Miller M.C., de Wit R., Terstappen L.W., Sleijfer S. Circulating endothelial cells, circulating tumour cells, tissue factor, endothelin-1 and overall survival in prostate cancer patients treated with docetaxel. Eur. J. Cancer 2010, 46:2027-2035.
37. Trudel D., Fradet Y., Meyer F., Harel F., Tetu B. Membrane-type-1 matrix metalloproteinase, matrix metalloproteinase 2, and tissue inhibitor of matrix proteinase 2 in prostate cancer: identification of patients with poor prognosis by immunohistochemistry. Hum. Pathol. 2008, 39:731-739.
38. Xu L., Chen S., Bergan R.C. MAPKAPK2 and HSP27 are downstream effectors of p38 MAP kinase-mediated matrix metalloproteinase type 2 activation and cell invasion in human prostate cancer. Oncogene 2006, 25:2987-2998.
39. Xu L., Ding Y., Catalona W.J., Yang X.J., Anderson W.F., Jovanovic B., Wellman K., Killmer J., Huang X., Scheidt K.A., Montgomery R.B., Bergan R.C. MEK4 function, genistein treatment, and invasion of human prostate cancer cells. J. Natl Cancer Inst. 2009, 101:1141-1155.
40. Yu M., Bardia A., Wittner B.S., Stott S.L., Smas M.E., Ting D.T., Isakoff S.J., Ciciliano J.C., Wells M.N., Shah A.M., Concannon K.F., Donaldson M.C., Sequist L.V., Brachtel E., Sgroi D., Baselga J., Ramaswamy S., Toner M., Haber D.A., Maheswaran S. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 2013, 339:580-584.
41. Zhang L., Ridgway L.D., Wetzel M.D., Ngo J., Yin W., Kumar D., Goodman J.C., Groves M.D., Marchetti D. The identification and characterization of breast cancer CTCs competent for brain metastasis. Sci. Trans. Med. 2013, 5:180ra-148.
42. Zhang L., Riethdorf S., Wu G., Wang T., Yang K., Peng G., Liu J., Pantel K. Meta-analysis of the prognostic value of circulating tumor cells in breast cancer. Clin. Cancer Res. 2012, 18:5701-5710.