Prognostic value of cytokeratin-7 mRNA expression in peripheral whole blood of advanced lung adenocarcinoma patients

Cellular Oncology

Volumn 38, Issue 5, 2015, Pages 387-395

  Koren, Ana ^a   Sodja, Eva ^a   Rijavec, Matija ^a   Jez, Mojca ^b   Kovac, Viljem ^c   Korosec, Peter ^a   Cufer, Tanja ^a  

^a UNIVERSITY CLINIC OF RESPIRATORY AND ALLERGIC DISEASES   (Slovenia)

^b BLOOD TRANSFUSION CENTRE OF SLOVENIA   (Slovenia)

^c INSTITUTE OF ONCOLOGY   (Slovenia)

Author keywords

Circulating tumour cells; KRT7; Lung adenocarcinoma; mRNA expression; Prognosis

Indexed keywords

CYTOKERATIN 7; ERLOTINIB; ETOPOSIDE; GEMCITABINE; MESSENGER RNA; PEMETREXED; ANTINEOPLASTIC AGENT;

A549 CELL LINE; ADULT; AGED; ARTICLE; BLOOD SAMPLING; CANCER CHEMOTHERAPY; CANCER PATIENT; CANCER PROGNOSIS; CANCER SURVIVAL; CIRCULATING TUMOR CELL; CONTROLLED STUDY; FEMALE; FOLLOW UP; GENE EXPRESSION; HUMAN; HUMAN CELL; LUNG ADENOCARCINOMA; MAJOR CLINICAL STUDY; MALE; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; REPRODUCIBILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSITIVITY ANALYSIS; SYSTEMIC THERAPY; TREATMENT RESPONSE; ADENOCARCINOMA; BLOOD; GENETICS; KAPLAN MEIER METHOD; LUNG NEOPLASMS; METABOLISM; MIDDLE AGED; PROGNOSIS; TREATMENT OUTCOME; TUMOR CELL LINE; TUMOR EMBOLISM;

ADENOCARCINOMA; ADULT; AGED; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CELL LINE, TUMOR; FEMALE; HUMANS; KAPLAN-MEIER ESTIMATE; KERATIN-7; LUNG NEOPLASMS; MALE; MIDDLE AGED; NEOPLASTIC CELLS, CIRCULATING; PROGNOSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TREATMENT OUTCOME;

EID: 84944174441     PISSN: 22113428     EISSN: 22113436     Source Type: Journal    
DOI: 10.1007/s13402-015-0238-4     Document Type: Article

References (56)

1. J. Ferlay, I. Soerjomataram, M. Ervik, R. Dikshit, S. Eser, C. Mathers, M. Rebelo, D. M. Parkin, D. Forman, F. Bray, in GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide. IARC CancerBase No. 11 [Internet]. Lyon, International Agency for Research on Cancer. http://globocan.iarc.fr Accessed 16 November 2014
2. N. Peled, M.W. Wynes, N. Ikeda, T. Ohira, K. Yoshida, J. Qian, M. Ilouze, R. Brenner, Y. Kato, C. Mascaux, F.R. Hirsch, Insulin-like growth factor-1 receptor (IGF-1R) as a biomarker for resistance to the tyrosine kinase inhibitor gefitinib in non-small cell lung cancer. Cell. Oncol. 36, 277–88 (2013)
3. S.H. Ahn, E.H. Jeong, T.G. Lee, S.Y. Kim, H.R. Kim, C.H. Kim, Gefitinib induces cytoplasmic translocation of the CDK inhibitor p27 and its binding to a cleaved intermediate of caspase 8 in non-small cell lung cancer cells. Cell. Oncol. 37, 377–386 (2014)
4. P. Ulivi, R. Silvestrini, Role of quantitative and qualitative characteristics of free circulating DNA in the management of patients with non-small cell lung cancer. Cell. Oncol. 36, 439–448 (2013)
5. L.G. Collins, C. Haines, R. Perkel, R.E. Enck, Lung cancer: diagnosis and management. Am. Fam. Physician 75, 56–63 (2007)
6. T. Cufer, L. Knez, Update on systemic therapy of advanced non-small-cell lung cancer. Expert Rev. Anticancer Ther. 14, 1189–1203 (2014)
7. B. Kubuschok, B. Passlick, J.R. Izbicki, O. Thetter, K. Pantel, Disseminated tumor cells in lymph nodes as a determinant for survival in surgically resected non-small-cell lung cancer. J. Clin. Oncol. 17, 19–24 (1999)
8. V. Hofman, C. Bonnetaud, M.I. Ilie, P. Vielh, J.M. Vignaud, J.F. Fléjou, S. Lantuejoul, E. Piaton, N. Mourad, C. Butori, E. Selva, M. Poudenx, S. Sibon, S. Kelhef, N. Vénissac, J.P. Jais, J. Mouroux, T.J. Molina, P. Hofman, Preoperative circulating tumor cell detection using the isolation by size of epithelial tumor cell method for patients with lung cancer is a new prognostic biomarker. Clin. Cancer Res. 17, 827–835 (2011)
9. M.G. Krebs, J.M. Hou, R. Sloane, L. Lancashire, L. Priest, D. Nonaka, T.H. Ward, A. Backen, G. Clack, A. Hughes, M. Ranson, F.H. Blackhall, C. Dive, Analysis of circulating tumor cells in patients with non-small cell lung cancer using epithelial marker-dependent and -independent approaches. J. Thorac. Oncol. 7, 306–315 (2012)
10. T.J.N. Hiltermann, M.M. Pore, A. van den Berg, W. Timens, H.M. Boezen, J.J. Liesker, J.H. Schouwink, W.J. Wijnands, G.S. Kerner, F.A. Kruyt, H. Tissing, A.G. Tibbe, L.W. Terstappen, H.J. Groen, Circulating tumor cells in small-cell lung cancer: a predictive and prognostic factor. Ann. Oncol. 23, 2937–2942 (2012)
11. W.J. Allard, J. Matera, M.C. Miller, M. Repollet, M.C. Connelly, C. Rao, A.G. Tibbe, J.W. Uhr, L.W. Terstappen, Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin. Cancer Res. 10, 6897–6904 (2004)
12. M. Cristofanilli, G.T. Budd, M.J. Ellis, A. Stopeck, J. Matera, M.C. Miller, J.M. Reuben, G.V. Doyle, W.J. Allard, L.W. Terstappen, D.F. Hayes, Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N. Engl. J. Med. 351, 781–791 (2004)
13. E.A. Punnoose, S. Atwal, W. Liu, R. Raja, B.M. Fine, B.G. Hughes, R.J. Hicks, G.M. Hampton, L.C. Amler, A. Pirzkall, M.R. Lackner, Evaluation of circulating tumor cells and circulating tumor DNA in non-small cell lung cancer: Association with clinical endpoints in a phase II clinical trial of pertuzumab and erlotinib. Clin. Cancer Res. 18, 2391–2401 (2012)
14. O. Hoffmann, E. Solomayer, S. Kuemmel, M. Hahn, S. Kasimir-Bauer, R. Kimmig, D. Wallwiener, T. Fehm, Does primary systemic therapy erradicate disseminated and circulating tumor cells? Cancer Res. 69, 3001–3001 (2009)
15. L.H. Broersen, G.W. van Pelt, R.A.E.M. Tollenaar, W.E. Mesker, Clinical application of circulating tumor cells in breast cancer. Cell. Oncol. 37, 9–15 (2014)
16. M.J. Kim, N.Y. Choi, E.K. Lee, M.S. Kang, Identification of novel markers that outperform EpCAM in quantifying circulating tumor cells. Cell. Oncol. 37, 235–243 (2014)
17. G. Vona, A. Sabile, M. Louha, V. Sitruk, S. Romana, K. Schütze, F. Capron, D. Franco, M. Pazzagli, M. Vekemans, B. Lacour, C. Bréchot, P. Paterlini-Bréchot, Isolation by size of epithelial tumor cells: a new method for the immunomorphological and molecular characterization of circulating tumor cells. Am. J. Pathol. 156, 57–63 (2000)
18. S. Nagrath, L.V. Sequist, S. Maheswaran, D.W. Bell, D. Irimia, L. Ulkus, M.R. Smith, E.L. Kwak, S. Digumarthy, A. Muzikansky, P. Ryan, U.J. Balis, R.G. Tompkins, D.A. Haber, M. Toner, Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature 450, 1235–1239 (2007)
19. R.T. Krivacic, A. Ladanyi, D.N. Curry, H.B. Hsieh, P. Kuhn, D.E. Bergsrud, J.F. Kepros, T. Barbera, M.Y. Ho, L.B. Chen, R.A. Lerner, R.H. Bruce, A rare-cell detector for cancer. Proc. Natl. Acad. Sci. U. S. A. 10, 10501–10504 (2004)
20. T. Nolan, R.E. Hands, S.A. Austin, Quantification of mRNA using real-time RT-PCR. Nat. Protoc. 1, 1559–1582 (2006)
21. L. Rainen, U. Oelmueller, S. Jurgensen, R. Wyrich, C. Ballas, J. Schram, C. Herdman, D. Bankaitis-Davis, N. Nicholls, D. Trollinger, V. Tryon, Stabilization of mRNA expression in whole blood samples. Clin. Chem. 48, 1883–1890 (2002)
22. A.E. Ring, L. Zabaglo, M.G. Ormerod, I.E. Smith, M. Dowsett, Detection of circulating epithelial cells in the blood of patients with breast cancer: comparison of three techniques. Br. J. Cancer 92, 906–912 (2005)
23. R.A. Ghossein, S. Bhattacharya, R. Rosai, Molecular detection of micrometastases and circulating tumor cells in solid tumors. Clin. Cancer Res. 5, 1950–1960 (1999)
24. N.B. Tsui, E.K. Ng, Y.M. Lo, Stability of endogenous and added RNA in blood specimens, serum, and plasma. Clin. Chem. 48, 1647–1653 (2002)
25. E. Saloustros, M. Perraki, S. Apostolaki, G. Kallergi, A. Xyrafas, K. Kalbakis, S. Agelaki, A. Kalykaki, V. Georgoulias, D. Mavroudis, Cytokeratin-19 mRNA-positive circulating tumor cells during follow-up of patients with operable breast cancer: prognostic relevance for late relapse. Breast Cancer Res. 13, R60 (2011)
26. P. Chu, E. Wu, L.M. Weiss, Cytokeratin 7 and cytokeratin 20 expression in epithelial neoplasms: a survey of 435 cases. Mod. Pathol. 13, 962–972 (2000)
27. D.C. Chhieng, J.F. Cangiarella, M.F. Zakowski, S. Goswami, J.M. Cohen, H.T. Yee, Use of thyroid transcription factor 1, PE-10, and cytokeratins 7 and 20 in discriminating between primary lung carcinomas and metastatic lesions in fine-needle aspiration biopsy specimens. Cancer Cytopathol. 93, 330–336 (2001)
28. O. Arrieta, B. Pineda, S. Muñiz-Hernández, D. Flores, G. Ordóñez, J.R. Borbolla-Escoboza, D. Orta, Molecular detection and prognostic value of epithelial markers mRNA expression in peripheral blood of advanced non-small cell lung cancer patients. Cancer Biomark. 14, 215–223 (2014)
29. D.G. Altman, L.M. McShane, W. Sauerbrei, S.E. Taube, Reporting Recommendations for Tumor Marker Prognostic Studies (REMARK): explanation and elaboration. PLoS Med. 9, e1001216 (2012)
30. E.A. Eisenhauer, P. Therasse, J. Bogaerts, L.H. Schwartz, D. Sargent, R. Ford, J. Dancey, S. Arbuck, S. Gwyther, M. Mooney, L. Rubinstein, L. Shankar, L. Dodd, R. Kaplan, D. Lacombe, J. Verweij, New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur. J. Cancer 45, 228–247 (2009)
31. M.M. Oken, R.H. Creech, D.C. Tormey, J. Horton, T.E. Davis, E.T. McFadden, P.P. Carbone, Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am. J. Clin. Oncol. 5, 649–655 (1982)
32. K.J. Livak, T.D. Schmittgen, Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 25, 402–408 (2001)
33. I.H. Al-Zahrani, The value of immunohistochemical expression of TTF-1, CK7 and CK20 in the diagnosis of primary and secondary lung carcinomas. Saudi Med. J. 29, 957–961 (2008)
34. S. Paget, The distribution of secondary growths in cancer of the breast. Cancer Metastasis Rev. 8, 98–101 (1989)
35. Y. Liu, J. Qian, J.G. Feng, H.X. Ju, Y.P. Zhu, H.Y. Feng, D.C. Li, Detection of circulating tumor cells in peripheral blood of colorectal cancer patients without distant organ metastases. Cell. Oncol. 36, 43–53 (2013)
36. J. Wang, J. Huang, K. Wang, J. Xu, J. Huang, T. Zhang, Prognostic significance of circulating tumor cells in non-small-cell lung cancer patients: a meta-analysis. PLoS One 8, e78070 (2013)
37. E. Borgen, B. Naume, J.M. Nesland, G. Kvalheim, K. Beiske, O. Fodstad, I. Diel, E.F. Solomayer, P. Theocharous, R.C. Coombes, B.M. Smith, E. Wunder, J.P. Marolleau, J. Garcia, K. Pantel, Standardization of the immunocytochemical detection of cancer cells in BM and blood: I. establishment of objective criteria for the evaluation of immunostained cells. Cytotherapy 1, 377–388 (1999)
38. M.G. Krebs, R. Sloane, L. Priest, L. Lancashire, J. Hou, A. Greystoke, T.H. Ward, R. Ferraldeschi, A. Hughes, G. Clack, M. Ranson, C. Dive, F.H. Blackhall, Evaluation and prognostic significance of circulating tumor cells in patients with non-small-cell lung cancer. J. Clin. Oncol. 29, 1556–1563 (2011)
39. A. Stathopoulou, Molecular detection of cytokeratin-19-positive cells in the peripheral blood of patients with operable breast cancer: evaluation of their prognostic significance. J. Clin. Oncol. 20, 3404–3412 (2002)
40. T.A. Masuda, A. Kataoka, S. Ohno, S. Murakami, K. Mimori, T. Utsunomiya, H. Inoue, S. Tsutsui, J. Kinoshita, N. Masuda, N. Moriyama, M. Mori, Detection of occult cancer cells in peripheral blood and bone marrow by quantitative RT-PCR assay for cytokeratin-7 in breast cancer patients. Int. J. Oncol. 26, 721–730 (2005)
41. S.O. Yoon, Y.T. Kim, K.C. Jung, Y.K. Jeon, B.H. Kim, C.W. Kim, TTF-1 mRNA-positive circulating tumor cells in the peripheral blood predict poor prognosis in surgically resected non-small cell lung cancer patients. Lung Cancer 71, 209–216 (2011)
42. K. Peck, Y.P. Sher, J.Y. Shih, S.R. Roffler, C.W. Wu, P.C. Yang, Detection and quantitation of circulating cancer cells in the peripheral blood of lung cancer patients. Cancer Res. 58, 2761–2765 (1998)
43. W.F. Zhu, J. Li, L.C. Yu, Y. Wu, X.P. Tang, Y.M. Hu, Y.C. Chen, Prognostic value of EpCAM/MUC1 mRNA-positive cells in non-small cell lung cancer patients. Tumor Biol. 35, 1211–1219 (2013)
44. T.F. Chen, G.L. Jiang, X.L. Fu, L.J. Wang, H. Qian, K.L. Wu, S. Zhao, CK19 mRNA expression measured by reverse-transcription polymerase chain reaction (RT-PCR) in the peripheral blood of patients with non-small cell lung cancer treated by chemo-radiation: an independent prognostic factor. Lung Cancer 56, 105–114 (2007)
45. S.A. Joosse, J. Hannemann, J. Spötter, A. Bauche, A. Andreas, V. Müller, K. Pantel, Changes in keratin expression during metastatic progression of breast cancer: impact on the detection of circulating tumor cells. Clin. Cancer Res. 18, 993–1003 (2012)
46. N. Xenidis, I. Vlachonikolis, D. Mavroudis, M. Perraki, A. Stathopoulou, N. Malamos, C. Kouroussis, S. Kakolyris, S. Apostolaki, N. Vardakis, E. Lianidou, V. Georgoulias, Peripheral blood circulating cytokeratin-19 mRNA-positive cells after the completion of adjuvant chemotherapy in patients with operable breast cancer. Ann. Oncol. 14, 849–855 (2003)
47. A.M. Sieuwerts, J. Kraan, J. Bolt-de Vries, P. van der Spoel, B. Mostert, J.W. Martens, J.W. Gratama, S. Sleijfer, J.A. Foekens, Molecular characterization of circulating tumor cells in large quantities of contaminating leukocytes by a multiplex real-time PCR. Breast Cancer Res. Treat. 118, 455–468 (2009)
48. J.P. Thiery, J.P. Sleeman, Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7, 131–142 (2006)
49. M. Perán, J.A. Marchal, M.A. García, J. Kenyon, D. Tosh, In vitro treatment of carcinoma cell lines with pancreatic (pro)enzymes suppresses the EMT programme and promotes cell differentiation. Cell. Oncol. 36, 289–301 (2013)
50. A. Koren, H. Motaln, T. Cufer, Lung cancer stem cells: a biological and clinical perspective. Cell. Oncol. 36, 265–275 (2013)
51. M. Sabbah, S. Emami, G. Redeuilh, S. Julien, G. Prévost, A. Zimber, R. Ouelaa, M. Bracke, O. De Wever, C. Gespach, Molecular signature and therapeutic perspective of the epithelial-to-mesenchymal transitions in epithelial cancers. Drug Resist. Updat. 11, 123–151 (2008)
52. B. Willipinski-Stapelfeldt, S. Riethdorf, V. Assmann, U. Woelfle, T. Rau, G. Sauter, J. Heukeshoven, K. Pantel, Changes in cytoskeletal protein composition indicative of an epithelial-mesenchymal transition in human micrometastatic and primary breast carcinoma cells. Clin. Cancer Res. 11, 8006–8014 (2005)
53. A.J. Armstrong, M.S. Marengo, S. Oltean, G. Kemeny, R.L. Bitting, J.D. Turnbull, C.I. Herold, P.K. Marcom, D.J. George, M.A. Garcia-Blanco, Circulating tumor cells from patients with advanced prostate and breast cancer display both epithelial and mesenchymal markers. Mol. Cancer Res. 9, 997–1007 (2011)
54. M. Yu, A. Bardia, B.S. Wittner, S.L. Stott, M.E. Smas, D.T. Ting, S.J. Isakoff, J.C. Ciciliano, M.N. Wells, A.M. Shah, K.F. Concannon, M.C. Donaldson, L.V. Sequist, E. Brachtel, D. Sgroi, J. Baselga, S. Ramaswamy, M. Toner, D.A. Haber, S. Maheswaran, Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 339, 580–584 (2013)
55. A. Lecharpentier, P. Vielh, P. Perez-Moreno, D. Planchard, J.C. Soria, F. Farace, 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 (2011)
56. A. Gradilone, C. Raimondi, C. Nicolazzo, A. Petracca, O. Gandini, B. Vincenzi, G. Naso, A.M. Aglianò, E. Cortesi, P. Gazzaniga, Circulating tumour cells lacking cytokeratin in breast cancer: the importance of being mesenchymal. J. Cell. Mol. Med. 15, 1066–1070 (2011)