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Review Article

Cancer stem cell characteristics of circulating tumor cells

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Pages 622-627 | Received 29 Oct 2013, Accepted 15 Jan 2014, Published online: 12 May 2014

References

  • Aktas B, Tewes M, Fehm T, Hauch S, Kimmig R, Kasimir-Bauer S. 2009. Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Res 11:R46.
  • Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. 2003. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100:3983–3988.
  • Andarawewa KL, Costes SV, Fernandez-Garcia I, Chou WS, Ravani SA, Park H, Barcellos-Hoff MH. 2011. Lack of radiation dose or quality dependence of epithelial-to-mesenchymal transition (EMT) mediated by transforming growth factor beta. Int J Radiat Oncol Biol Phys 79:1523–1531.
  • Baccelli I, Schneeweiss A, Riethdorf S, Stenzinger A, Schillert A, Vogel V, Klein C, Saini M, Bauerle T, Wallwiener M, et al. 2013. Identification of a population of blood circulating tumor cells from breast cancer patients that initiates metastasis in a xenograft assay. Nat Biotechnol 31:539–544.
  • Balic M, Lin H, Young L, Hawes D, Giuliano A, McNamara G, Datar RH, Cote RJ. 2006. Most early disseminated cancer cells detected in bone marrow of breast cancer patients have a putative breast cancer stem cell phenotype. Clin Cancer Res 12:5615–5621.
  • Banys M, Solomayer EF, Becker S, Krawczyk N, Gardanis K, Staebler A, Neubauer H, Wallwiener D, Fehm T. 2009. Disseminated tumor cells in bone marrow may affect prognosis of patients with gynecologic malignancies. Int J Gynecol Cancer 19:948–952.
  • Biswas S, Guix M, Rinehart C, Dugger TC, Chytil A, Moses HL, Freeman ML, Arteaga CL. 2007. Inhibition of TGF-beta with neutralizing antibodies prevents radiation-induced acceleration of metastatic cancer progression. J Clin Invest 117:1305–1313.
  • Bjerkvig R, Tysnes BB, Aboody KS, Najbauer J, Terzis AJ. 2005. Opinion: The origin of the cancer stem cell: Current controversies and new insights. Nat Rev Cancer 5:899–904.
  • Boman BM, Wicha MS. 2008. Cancer stem cells: A step toward the cure. J Clin Oncol 26:2795–2799.
  • Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A. 2004. Neutrophil extracellular traps kill bacteria. Science 303:1532–1535.
  • Camphausen K, Moses MA, Beecken WD, Khan MK, Folkman J, O’Reilly MS. 2001. Radiation therapy to a primary tumor accelerates metastatic growth in mice. Cancer Res 61:2207–2211.
  • Chaffer CL, Weinberg RA. 2011. A perspective on cancer cell metastasis. Science 331:1559–1564.
  • Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, Hur MH, Diebel ME, Monville F, Dutcher J, et al. 2009. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 69:1302–1313.
  • Chen CL, Mahalingam D, Osmulski P, Jadhav RR, Wang CM, Leach RJ, Chang TC, Weitman SD, Kumar AP, Sun L, et al. 2013. Single-cell analysis of circulating tumor cells identifies cumulative expression patterns of EMT-related genes in metastatic prostate cancer. Prostate 73:813–826.
  • Cohen SJ, Punt CJ, Iannotti N, Saidman BH, Sabbath KD, Gabrail NY, Picus J, Morse M, Mitchell E, Miller MC, et al. 2008. Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer. J Clin Oncol 26:3213–3221.
  • Cools-Lartigue J, Spicer J, McDonald B, Gowing S, Chow S, Giannias B, Bourdeau F, Kubes P, Ferri L. 2013. Neutrophil extracellular traps sequester circulating tumor cells and promote metastasis. J Clin Invest Jul 1 pii:67484.
  • Creighton CJ, Li X, Landis M, Dixon JM, Neumeister VM, Sjolund A, Rimm DL, Wong H, Rodriguez A, Herschkowitz JI, et al. 2009. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci USA 106:13820–13825.
  • Cristofanilli M, Budd GT, Ellis MJ, Stopeck A, Matera J, Miller MC, Reuben JM, Doyle GV, Allard WJ, Terstappen LW, et al. 2004. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med 351:781–791.
  • Danila DC, Fleisher M, Scher HI. 2011. Circulating tumor cells as biomarkers in prostate cancer. Clin Cancer Res 17:3903–3912.
  • Driemel C, Kremling H, Schumacher S, Will D, Wolters J, Lindenlauf N, Mack B, Baldus SA, Hoya V, Pietsch JM, et al. 2013. Context-dependent adaption of EpCAM expression in early systemic esophageal cancer. Oncogene doi: 10.1038/onc.2013.44. [Epub ahead of print].
  • Fehm T, Banys M, Rack B, Janni W, Marth C, Blassl C, Hartkopf A, Trope C, Kimmig R, Krawczyk N, et al. 2013. Pooled analysis of the prognostic relevance of disseminated tumor cells in the bone marrow of patients with ovarian cancer. Int J Gynecol Cancer 23:839–845.
  • Fehm T, Hoffmann O, Aktas B, Becker S, Solomayer EF, Wallwiener D, Kimmig R, Kasimir-Bauer S. 2009. Detection and characterization of circulating tumor cells in blood of primary breast cancer patients by RT-PCR and comparison to status of bone marrow disseminated cells. Breast Cancer Res 11:R59.
  • Friedl P, Wolf K. 2003. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 3:362–374.
  • Ghossein RA, Scher HI, Gerald WL, Kelly WK, Curley T, Amsterdam A, Zhang ZF, Rosai J. 1995. Detection of circulating tumor cells in patients with localized and metastatic prostatic carcinoma: clinical implications. J Clin Oncol 13:1195–1200.
  • Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S, et al. 2007. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1:555–567.
  • Giordano A, Gao H, Anfossi S, Cohen E, Mego M, Lee BN, Tin S, De Laurentiis M, Parker CA, Alvarez RH, et al. 2012. Epithelial- mesenchymal transition and stem cell markers in patients with HER2-positive metastatic breast cancer. Molec Cancer Ther 11: 2526–2534.
  • Gorges TM, Tinhofer I, Drosch M, Rose L, Zollner TM, Krahn T, von Ahsen O. 2012. Circulating tumour cells escape from EpCAM-based detection due to epithelial-to-mesenchymal transition. BMC Cancer 12:178.
  • Groot Koerkamp B, Rahbari NN, Buchler MW, Koch M, Weitz J. 2013. Circulating tumor cells and prognosis of patients with resectable colorectal liver metastases or widespread metastatic colorectal cancer: a meta-analysis. Ann Surg Oncol 20:2156–2165.
  • Gupta PB, Fillmore CM, Jiang G, Shapira SD, Tao K, Kuperwasser C, Lander ES. 2011. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 146:633–644.
  • He H, Yang X, Davidson AJ, Wu D, Marshall FF, Chung LW, Zhau HE, Wang R. 2011. Progressive epithelial to mesenchymal transitions in ARCaP E prostate cancer cells during xenograft tumor formation and metastasis. Prostate 70:518–528.
  • Holz C, Niehr F, Boyko M, Hristozova T, Distel L, Budach V, Tinhofer I. 2011. Epithelial-mesenchymal-transition induced by EGFR activation interferes with cell migration and response to irradiation and cetuximab in head and neck cancer cells. Radiother Oncol 101:158–164.
  • Hou JM, Krebs MG, Lancashire L, Sloane R, Backen A, Swain RK, Priest LJ, Greystoke A, Zhou C, Morris K, et al. 2012. Clinical significance and molecular characteristics of circulating tumor cells and circulating tumor microemboli in patients with small-cell lung cancer. J Clin Oncol 30:525–532.
  • Hristozova T, Konschak R, Stromberger C, Fusi A, Liu Z, Weichert W, Stenzinger A, Budach V, Keilholz U, Tinhofer I. 2011. The presence of circulating tumor cells (CTCs) correlates with lymph node metastasis in nonresectable squamous cell carcinoma of the head and neck region (SCCHN). Ann Oncol 22:1878–1885.
  • Huh SJ, Liang S, Sharma A, Dong C, Robertson GP. 2010. Transiently entrapped circulating tumor cells interact with neutrophils to facilitate lung metastasis development. Cancer Res 70:6071–6082.
  • Jung JW, Hwang SY, Hwang JS, Oh ES, Park S, Han IO. 2007. Ionising radiation induces changes associated with epithelial-mesenchymal transdifferentiation and increased cell motility of A549 lung epithelial cells. Eur J Cancer 43:1214–1224.
  • Kallergi G, Papadaki MA, Politaki E, Mavroudis D, Georgoulias V, Agelaki S. 2011. Epithelial to mesenchymal transition markers expressed in circulating tumour cells of early and metastatic breast cancer patients. Breast Cancer Res 13:R59.
  • Kawamoto A, Yokoe T, Tanaka K, Saigusa S, Toiyama Y, Yasuda H, Inoue Y, Miki C, Kusunoki M. 2012. Radiation induces epithelial-mesenchymal transition in colorectal cancer cells. Oncol Rep 27:51–57.
  • Kim MY, Oskarsson T, Acharyya S, Nguyen DX, Zhang XH, Norton L, Massague J. 2009. Tumor self-seeding by circulating cancer cells. Cell 139:1315–1326.
  • Klein CA. 2009. Parallel progression of primary tumours and metastases. Nat Rev Cancer 9:302–312.
  • Labelle M, Begum S, Hynes RO. 2011. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell 20:576–590.
  • Lecharpentier A, Vielh P, Perez-Moreno P, Planchard D, Soria JC, Farace F. 2011. Detection of circulating tumour cells with a hybrid (epithelial/mesenchymal) phenotype in patients with metastatic non-small cell lung cancer. Br J Cancer 105:1338–1341.
  • Li YM, Xu SC, Li J, Han KQ, Pi HF, Zheng L, Zuo GH, Huang XB, Li HY, Zhao HZ, et al. 2013. Epithelial-mesenchymal transition markers expressed in circulating tumor cells in hepatocellular carcinoma patients with different stages of disease. Cell Death Dis 4:e831.
  • Lowes LE, Lock M, Rodrigues G, D’Souza D, Bauman G, Ahmad B, Venkatesan V, Allan AL, Sexton T. 2012. Circulating tumour cells in prostate cancer patients receiving salvage radiotherapy. Clin Transl Oncol 14:150–156.
  • Ma XL, Xiao ZL, Liu L, Liu XX, Nie W, Li P, Chen NY, Wei YQ. 2012. Meta-analysis of circulating tumor cells as a prognostic marker in lung cancer. Asian Pac J Cancer Prev 13:1137–1144.
  • Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, et al. 2008. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133:704–715.
  • Martin OA, Anderson RL, Russell PA, Ashley Cox R, Ivashkevich A, Swierczak A, Doherty JP, Jacobs DH, Smith J, Siva S, et al. 2014. Mobilization of viable tumor cells into the circulation during radiation therapy. Int J Radiat Oncol Biol Phys 88:395–403.
  • Pantel K, Alix-Panabieres C, Riethdorf S. 2009. Cancer micrometastases. Nat Rev Clin Oncol 6:339–351.
  • Patrawala L, Calhoun T, Schneider-Broussard R, Li H, Bhatia B, Tang S, Reilly JG, Chandra D, Zhou J, Claypool K, et al. 2006. Highly purified CD44 + prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 25:1696–1708.
  • Pilati P, Mocellin S, Bertazza L, Galdi F, Briarava M, Mammano E, Tessari E, Zavagno G, Nitti D. 2012. Prognostic value of putative circulating cancer stem cells in patients undergoing hepatic resection for colorectal liver metastasis. Ann Surg Oncol 19:402–408.
  • Rahbari NN, Aigner M, Thorlund K, Mollberg N, Motschall E, Jensen K, Diener MK, Buchler MW, Koch M, Weitz J. 2010. Meta-analysis shows that detection of circulating tumor cells indicates poor prognosis in patients with colorectal cancer. Gastroenterology 138:1714–1726.
  • Raimondi C, Gradilone A, Naso G, Vincenzi B, Petracca A, Nicolazzo C, Palazzo A, Saltarelli R, Spremberg F, Cortesi E, et al. 2011. Epithelial-mesenchymal transition and stemness features in circulating tumor cells from breast cancer patients. Breast Cancer Res Treat 130:449–455.
  • Reya T, Morrison SJ, Clarke MF, Weissman IL. 2001. Stem cells, cancer, and cancer stem cells. Nature 414:105–111.
  • Riethdorf S, Muller V, Zhang L, Rau T, Loibl S, Komor M, Roller M, Huober J, Fehm T, Schrader I, et al. 2010. Detection and HER2 expression of circulating tumor cells: prospective monitoring in breast cancer patients treated in the neoadjuvant GeparQuattro trial. Clin Cancer Res 16:2634–2645.
  • Scher HI, Jia X, de Bono JS, Fleisher M, Pienta KJ, Raghavan D, Heller G. 2009. Circulating tumour cells as prognostic markers in progressive, castration-resistant prostate cancer: A reanalysis of IMMC38 trial data. Lancet Oncol 10:233–239.
  • Spicer JD, McDonald B, Cools-Lartigue JJ, Chow SC, Giannias B, Kubes P, Ferri LE. 2012. Neutrophils promote liver metastasis via Mac-1-mediated interactions with circulating tumor cells. Cancer Res 72:3919–3927.
  • Stingl J, Caldas C. 2007. Molecular heterogeneity of breast carcinomas and the cancer stem cell hypothesis. Nat Rev Cancer 7:791–799.
  • Sun YF, Xu Y, Yang XR, Guo W, Zhang X, Qiu SJ, Shi RY, Hu B, Zhou J, Fan J. 2013. Circulating stem cell-like epithelial cell adhesion molecule-positive tumor cells indicate poor prognosis of hepatocellular carcinoma after curative resection. Hepatology 57:1458–1468.
  • Thiery JP. 2002. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2:442–454.
  • Tinhofer I, Hristozova T, Stromberger C, Keilholz U, Budach V. 2012. Monitoring of circulating tumor cells and their expression of EGFR/phospho-EGFR during combined radiotherapy regimens in locally advanced squamous cell carcinoma of the head and neck. Int J Radiat Oncol Biol Phys 83:e685–690.
  • Wang FB, Yang XQ, Yang S, Wang BC, Feng MH, Tu JC. 2011. A higher number of circulating tumor cells (CTC) in peripheral blood indicates poor prognosis in prostate cancer patients--a meta-analysis. Asian Pac J Cancer Prev 12:2629–2635.
  • Wang M, Hada M, Saha J, Sridharan DM, Pluth JM, Cucinotta FA. 2012. Protons sensitize epithelial cells to mesenchymal transition. PLoS One 7:e41249.
  • Wulfing P, Borchard J, Buerger H, Heidl S, Zanker KS, Kiesel L, Brandt B. 2006. HER2-positive circulating tumor cells indicate poor clinical outcome in stage I to III breast cancer patients. Clin Cancer Res 12:1715–1720.
  • Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, Isakoff SJ, Ciciliano JC, Wells MN, Shah AM, et al. 2013. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 339:580–584.
  • Zhang L, Riethdorf S, Wu G, Wang T, Yang K, Peng G, Liu J, Pantel K. 2012. Meta-analysis of the prognostic value of circulating tumor cells in breast cancer. Clin Cancer Res 18:5701–5710.

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