New progress in detection and clinical application of circulating tumor cell markers_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

BAI Long ,  MENG Qinghui , LI Long

Department of Anorectal Surgical, The First Affiliated Hospital of Harbin Medical University, Harbin, Heilongjiang 150001, P.R.China;

Corresponding author：

MENG Qinghui, Email: hui-90@163.com

Keywords：

circulating tumor cell; marker; detection

DOI：

10.7507/1007-9424.201609065

Video：

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Objective To summarize the new progress of circulating tumor cell markers and their clinical application. Methods The related literatures about the detection and clinical application of circulating tumor cell markers in recent years were reviewed. Resuts Epithelial markers, other markers such as human epidermal growth factor receptor 2 (HER2), estrogen receptor (ER), and immuno-checkpoint genes have also become a useful means to detect the ability of malignant metastasis of circulating tumor cells (CTCs). Moreover, the epithelial-to-mesenchymal transition (EMT) and cancer stem cells (CSCs) have also received increasing attention as important CTCs markers owing to their roles in the biological progression of metastasis. Conclusions Through the detection of peripheral blood CTCs, to identify early cancer, monitoring the metastasis and recurrence of cancer and its treatment on all has the very good guiding significance. Signs of circulating tumor cells has great clinical application value in diagnosis and treatment of tumor and prognosis.

Citation： BAI Long, MENG Qinghui, LI Long. New progress in detection and clinical application of circulating tumor cell markers. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2017, 24(7): 890-894. doi: 10.7507/1007-9424.201609065 Copy

1.	Allard WJ, Matera J, Miller MC, et al. Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin Cancer Res, 2004, 10(20): 6897-6904.
2.	Ignatiadis M, Riethdorf S, Bidard FC, et al. International study on inter-reader variability for circulating tumor cells in breast cancer. Breast Cancer Res, 2014, 16(2): R43.
3.	Bidard FC, Peeters DJ, Fehm T, et al. Clinical validity of circulating tumour cells in patients with metastatic breast cancer: a pooled analysis of individual patient data. Lancet Oncol, 2014, 15(4): 406-414.
4.	Rack B, Schindlbeck C, Jückstock J, et al. Circulating tumor cells predict survival in early average-to-high risk breast cancer patients. J Natl Cancer Inst, 2014, 106(5). pii: dju066.
5.	Hiraiwa K, Takeuchi H, Hasegawa H, et al. Clinical significance of circulating tumor cells in blood from patients with gastrointestinal cancers. Ann Surg Oncol, 2008, 15(11): 3092-3100.
6.	Okabe H, Tsunoda S, Hosogi H, et al. Circulating tumor cells as an independent predictor of survival in advanced gastric cancer. Ann Surg Oncol, 2015, 22(12): 3954-3961.
7.	Bork U, Rahbari NN, Scholch S, et al. Circulating tumour cells and outcome in non-metastatic colorectal cancer: a prospective study. Br J Cancer, 2015, 112(8): 1306-1313.
8.	Becker S, Becker-Pergola G, Banys M, et al. Evaluation of a RT-PCR based routine screening tool for the detection of disseminated epithelial cells in the bone marrow of breast cancer patients. Breast Cancer Res Treat, 2009, 117(2): 227-233.
9.	Masuda TA, Kataoka A, Ohno S, et al. Detection of occult cancer cells in peripheral blood and bone marrow by quantitative RT-PCR assay for cytokeratin-7 in breast cancer patients. Int Oncol, 2005, 26(3): 721-730.
10.	Fehm T, Hoffmann O, Aktas B, et al. 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, 2009, 11(4): R59.
11.	Sun H, Zhu X, Lu PY, et al. Oligonucleotide aptamers: new tools for targeted cancer therapy. Mol Ther Nucleic Acids, 2014, 3: e182.
12.	Zamay GS, Kolovskaya OS, Zamay TN, et al. Aptamers selected to postoperative lung adenocarcinoma detect circulating tumor cells in human blood. Mol Ther, 2015, 23(9): 1486-1496.
13.	Beije N, Jager A, Sleijfer S, et al. Circulating tumor cell enumeration by the CellSearch system: the clinician’s guide to breast cancer treatment? Cancer Treat Rev, 2015, 41(2): 144-150.
14.	Hardingham JE, Grover P, Winter M, et al. Detection and clinical significance of circulating tumor cells in colorectal cancer-20 years of progress. Mol Med, 2015, 21 Suppl 1: S25-S31.
15.	Wicha MS, Hayes DF. Circulating tumor cells: not all detected cells are bad and not all bad cells are detected. J Clin Oncol, 2011, 29(12): 1508-1511.
16.	Ahmed S, Sami A, Xiang J, et al. HER2-directed therapy: current treatment options for HER2-positive breast cancer. Breast Cancer, 2015, 22(2): 101-116.
17.	Munzone E, Nole F, Goldhirsch A, et al. Changes of HER2 status in circulating tumor cells compared with the primary tumor during treatment for advanced breast cancer. Clin Breast Cancer, 2010, 10(5): 392-397.
18.	Riethdorf S, Müller V, Zhang L, et al. Detection and HER2 expression of circulating tumor cells: prospective monitoring in breast cancer patients treated in the neoadjuvant GeparQuattro trial. Clin Cancer Res, 2010, 16(9): 2634-2645.
19.	Fehm T, Muller V, Aktas B, et al. HER2 status of circulating tumor cells in patients with metastatic breast cancer: a prospective, multicenter trial. Breast Cancer Res Treat, 2010, 124(2): 403-412.
20.	Crowe JP Jr, Gordon NH, Hubay CA, et al. Estrogen receptor determination and long term survival of patients with carcinoma of the breast. Surg Gynecol Obstet, 1991, 173(4): 273-278.
21.	Paoletti C, Muniz MC, Thomas DG, et al. Development of circulating tumor cell-endocrine therapy index in patients with hormone receptor-positive breast cancer. Clin Cancer Res, 2015, 21(11): 2487-2498.
22.	Patel SP, Kurzrock R. PD-L1 expression as a predictive biomarker in Cancer immunotherapy. Mol Cancer Ther, 2015, 14(4): 847-856.
23.	Thompson RH, Gillett MD, Cheville JC, et al. Costimulatory B7-H1 in renal cell carcinoma patients: Indicator of tumor aggressiveness and potential therapeutic target. Proc Natl Acad Sci U S A, 2004, 101(49): 17174-17179.
24.	Hamanishi J, Mandai M, Iwasaki M, et al. Programmed cell death 1 ligand 1 and tumor-infiltrating CD8⁺ T lymphocytes are prognostic factors of human ovarian cancer. Proc Natl Acad Sci U S A, 2007, 104(9): 3360-3365.
25.	Ali HR, Glont SE, Blows FM, et al. PD-L1 protein expression in breast cancer is rare, enriched in basal-like tumours and associated with infiltrating lymphocytes. Ann Oncol, 2015, 26(7): 1488-1498.
26.	Mazel M, Jacot W, Pantel K, et al. Frequent expression of PD-L1 on circulating breast cancer cells. Mol Oncol, 2015, 9(9): 1773-1782.
27.	Grover P, Cummins AG, Price TJ, et al. Circulating tumour cells: the evolving concept and the inadequacy of their enrichment by EpCAM based methodology for basic and clinical cancer research. Ann Oncol, 2014, 25(8): 1506-1516.
28.	Kasimir-Bauer S, Hoffmann O, Wallwiener D, et al. Expression of stem cell and epithelial-mesenchymal transition markers in primary breast cancer patients with circulating tumor cells. Breast Cancer Res, 2012, 14(1), R15.
29.	Ma F, Li H, Li Y, et al. Aldehyde dehydrogenase 1 (ALDH1) expression is an independent prognostic factor in triple negative breast cancer (TNBC). Medicine (Baltimore), 2017, 96(14): e6561.
30.	Zhu B, Zhou L, Yu L, et al. Evaluation of the correlation of vasculogenic mimicry, ALDH1, KAI1 and microvessel density in the prediction of metastasis and prognosis in colorectal carcinoma. BMC Surg, 2017, 17(1): 47.
31.	Baccelli I, Schneeweiss A, Riethdorf S, et al. Identification of a population of blood circulating tumorcells frombreast cancerpatients thatinitiates metastasis in a xenograft assay. Nat Biotechnol, 2013, 31(6): 539-544.
32.	Trusolino L, Bertotti A, Comoglio PM, et al. MET signalling: principles and functions in development, organ regeneration and cancer. Nat Rev Mol Cell Biol, 2010, 11(12): 834-848.
33.	Sun YF, Xu Y, Yang XR, et al. Circulating stem cell-like epithelial cell adhesion molecule-positive tumor cells indicate poor prognosis of hepatocellular carcinoma after curative resection. Hepatology, 2013, 57(4): 1458-1468.
34.	O’Brien CA, Pollett A, Gallinger S, et al. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature, 2007, 445(7123): 106-110.
35.	Iinuma H, Watanabe T, Mimori K, et al. Clinical significance of circulating tumor cells, including cancer stem-like cells, in peripheral blood for recurrence and prognosis in patients with Dukes’ stage B and C colorectal cancer. J Clin Oncol, 2011, 29(12): 1547-1555.
36.	Aceto N, Bardia A, Miyamoto DT, et al. Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell, 2014, 158(5): 1110-1122.
37.	Fischer KR, Durrans A, Lee S, et al. Epithelial-to-mesenchymal transition is not required for lung metastasis but contributes to chemoresistance. Nature, 2015, 527(7579): 472-476.
38.	Bitting RL, Boominathan R, Rao C, et al. Development of a method to isolate circulating tumor cells using mesenchymal-based capture. Methods, 2013, 64(2): 129-136.
39.	Pecot CV, Bischoff FZ, Mayer JA, et al. A novel platform for detection of CK⁺ and CK^- CTCs. Cancer Discov, 2011, 1(7): 580-586.
40.	Yu M, Bardia A, Wittner BS, et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science, 2013, 339(6119): 580-584.
41.	Sugimachi K, Yokobori T, Iinuma H, et al. Aberrant expression of plastin-3 via copy number gain induces the epithelial-mesenchymal transition in circulating colorectal cancer cells. Ann Surg Oncol, 2014, 21(11): 3680-3690.
42.	Yokobori T, Iinuma H, Shimamura T, et al. Plastin3 is a novel marker for circulating tumor cells undergoing the epithelial-mesenchymal transition and is associated with colorectal cancer prognosis. Cancer Res, 2013, 73(7): 2059-2069.
43.	Liu S, Cong Y, Wang D, et al. Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts. Stem Cell Reports, 2013, 2(1): 78-91.

1. Allard WJ, Matera J, Miller MC, et al. Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin Cancer Res, 2004, 10(20): 6897-6904.
2. Ignatiadis M, Riethdorf S, Bidard FC, et al. International study on inter-reader variability for circulating tumor cells in breast cancer. Breast Cancer Res, 2014, 16(2): R43.
3. Bidard FC, Peeters DJ, Fehm T, et al. Clinical validity of circulating tumour cells in patients with metastatic breast cancer: a pooled analysis of individual patient data. Lancet Oncol, 2014, 15(4): 406-414.
4. Rack B, Schindlbeck C, Jückstock J, et al. Circulating tumor cells predict survival in early average-to-high risk breast cancer patients. J Natl Cancer Inst, 2014, 106(5). pii: dju066.
5. Hiraiwa K, Takeuchi H, Hasegawa H, et al. Clinical significance of circulating tumor cells in blood from patients with gastrointestinal cancers. Ann Surg Oncol, 2008, 15(11): 3092-3100.
6. Okabe H, Tsunoda S, Hosogi H, et al. Circulating tumor cells as an independent predictor of survival in advanced gastric cancer. Ann Surg Oncol, 2015, 22(12): 3954-3961.
7. Bork U, Rahbari NN, Scholch S, et al. Circulating tumour cells and outcome in non-metastatic colorectal cancer: a prospective study. Br J Cancer, 2015, 112(8): 1306-1313.
8. Becker S, Becker-Pergola G, Banys M, et al. Evaluation of a RT-PCR based routine screening tool for the detection of disseminated epithelial cells in the bone marrow of breast cancer patients. Breast Cancer Res Treat, 2009, 117(2): 227-233.
9. Masuda TA, Kataoka A, Ohno S, et al. Detection of occult cancer cells in peripheral blood and bone marrow by quantitative RT-PCR assay for cytokeratin-7 in breast cancer patients. Int Oncol, 2005, 26(3): 721-730.
10. Fehm T, Hoffmann O, Aktas B, et al. 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, 2009, 11(4): R59.
11. Sun H, Zhu X, Lu PY, et al. Oligonucleotide aptamers: new tools for targeted cancer therapy. Mol Ther Nucleic Acids, 2014, 3: e182.
12. Zamay GS, Kolovskaya OS, Zamay TN, et al. Aptamers selected to postoperative lung adenocarcinoma detect circulating tumor cells in human blood. Mol Ther, 2015, 23(9): 1486-1496.
13. Beije N, Jager A, Sleijfer S, et al. Circulating tumor cell enumeration by the CellSearch system: the clinician’s guide to breast cancer treatment? Cancer Treat Rev, 2015, 41(2): 144-150.
14. Hardingham JE, Grover P, Winter M, et al. Detection and clinical significance of circulating tumor cells in colorectal cancer-20 years of progress. Mol Med, 2015, 21 Suppl 1: S25-S31.
15. Wicha MS, Hayes DF. Circulating tumor cells: not all detected cells are bad and not all bad cells are detected. J Clin Oncol, 2011, 29(12): 1508-1511.
16. Ahmed S, Sami A, Xiang J, et al. HER2-directed therapy: current treatment options for HER2-positive breast cancer. Breast Cancer, 2015, 22(2): 101-116.
17. Munzone E, Nole F, Goldhirsch A, et al. Changes of HER2 status in circulating tumor cells compared with the primary tumor during treatment for advanced breast cancer. Clin Breast Cancer, 2010, 10(5): 392-397.
18. Riethdorf S, Müller V, Zhang L, et al. Detection and HER2 expression of circulating tumor cells: prospective monitoring in breast cancer patients treated in the neoadjuvant GeparQuattro trial. Clin Cancer Res, 2010, 16(9): 2634-2645.
19. Fehm T, Muller V, Aktas B, et al. HER2 status of circulating tumor cells in patients with metastatic breast cancer: a prospective, multicenter trial. Breast Cancer Res Treat, 2010, 124(2): 403-412.
20. Crowe JP Jr, Gordon NH, Hubay CA, et al. Estrogen receptor determination and long term survival of patients with carcinoma of the breast. Surg Gynecol Obstet, 1991, 173(4): 273-278.
21. Paoletti C, Muniz MC, Thomas DG, et al. Development of circulating tumor cell-endocrine therapy index in patients with hormone receptor-positive breast cancer. Clin Cancer Res, 2015, 21(11): 2487-2498.
22. Patel SP, Kurzrock R. PD-L1 expression as a predictive biomarker in Cancer immunotherapy. Mol Cancer Ther, 2015, 14(4): 847-856.
23. Thompson RH, Gillett MD, Cheville JC, et al. Costimulatory B7-H1 in renal cell carcinoma patients: Indicator of tumor aggressiveness and potential therapeutic target. Proc Natl Acad Sci U S A, 2004, 101(49): 17174-17179.
24. Hamanishi J, Mandai M, Iwasaki M, et al. Programmed cell death 1 ligand 1 and tumor-infiltrating CD8⁺ T lymphocytes are prognostic factors of human ovarian cancer. Proc Natl Acad Sci U S A, 2007, 104(9): 3360-3365.
25. Ali HR, Glont SE, Blows FM, et al. PD-L1 protein expression in breast cancer is rare, enriched in basal-like tumours and associated with infiltrating lymphocytes. Ann Oncol, 2015, 26(7): 1488-1498.
26. Mazel M, Jacot W, Pantel K, et al. Frequent expression of PD-L1 on circulating breast cancer cells. Mol Oncol, 2015, 9(9): 1773-1782.
27. Grover P, Cummins AG, Price TJ, et al. Circulating tumour cells: the evolving concept and the inadequacy of their enrichment by EpCAM based methodology for basic and clinical cancer research. Ann Oncol, 2014, 25(8): 1506-1516.
28. Kasimir-Bauer S, Hoffmann O, Wallwiener D, et al. Expression of stem cell and epithelial-mesenchymal transition markers in primary breast cancer patients with circulating tumor cells. Breast Cancer Res, 2012, 14(1), R15.
29. Ma F, Li H, Li Y, et al. Aldehyde dehydrogenase 1 (ALDH1) expression is an independent prognostic factor in triple negative breast cancer (TNBC). Medicine (Baltimore), 2017, 96(14): e6561.
30. Zhu B, Zhou L, Yu L, et al. Evaluation of the correlation of vasculogenic mimicry, ALDH1, KAI1 and microvessel density in the prediction of metastasis and prognosis in colorectal carcinoma. BMC Surg, 2017, 17(1): 47.
31. Baccelli I, Schneeweiss A, Riethdorf S, et al. Identification of a population of blood circulating tumorcells frombreast cancerpatients thatinitiates metastasis in a xenograft assay. Nat Biotechnol, 2013, 31(6): 539-544.
32. Trusolino L, Bertotti A, Comoglio PM, et al. MET signalling: principles and functions in development, organ regeneration and cancer. Nat Rev Mol Cell Biol, 2010, 11(12): 834-848.
33. Sun YF, Xu Y, Yang XR, et al. Circulating stem cell-like epithelial cell adhesion molecule-positive tumor cells indicate poor prognosis of hepatocellular carcinoma after curative resection. Hepatology, 2013, 57(4): 1458-1468.
34. O’Brien CA, Pollett A, Gallinger S, et al. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature, 2007, 445(7123): 106-110.
35. Iinuma H, Watanabe T, Mimori K, et al. Clinical significance of circulating tumor cells, including cancer stem-like cells, in peripheral blood for recurrence and prognosis in patients with Dukes’ stage B and C colorectal cancer. J Clin Oncol, 2011, 29(12): 1547-1555.
36. Aceto N, Bardia A, Miyamoto DT, et al. Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell, 2014, 158(5): 1110-1122.
37. Fischer KR, Durrans A, Lee S, et al. Epithelial-to-mesenchymal transition is not required for lung metastasis but contributes to chemoresistance. Nature, 2015, 527(7579): 472-476.
38. Bitting RL, Boominathan R, Rao C, et al. Development of a method to isolate circulating tumor cells using mesenchymal-based capture. Methods, 2013, 64(2): 129-136.
39. Pecot CV, Bischoff FZ, Mayer JA, et al. A novel platform for detection of CK⁺ and CK^- CTCs. Cancer Discov, 2011, 1(7): 580-586.
40. Yu M, Bardia A, Wittner BS, et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science, 2013, 339(6119): 580-584.
41. Sugimachi K, Yokobori T, Iinuma H, et al. Aberrant expression of plastin-3 via copy number gain induces the epithelial-mesenchymal transition in circulating colorectal cancer cells. Ann Surg Oncol, 2014, 21(11): 3680-3690.
42. Yokobori T, Iinuma H, Shimamura T, et al. Plastin3 is a novel marker for circulating tumor cells undergoing the epithelial-mesenchymal transition and is associated with colorectal cancer prognosis. Cancer Res, 2013, 73(7): 2059-2069.
43. Liu S, Cong Y, Wang D, et al. Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts. Stem Cell Reports, 2013, 2(1): 78-91.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

New progress in detection and clinical application of circulating tumor cell markers

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