Micrometastasis in gastric cancer

Cancer Letters

Volumn 336, Issue 1, 2013, Pages 34-45

  Zhang, Zhen yu ^a   Ge, Hai yan ^a  

^a TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Circulating tumor cells; Clinical impact; Epithelial mesenchymal transition; Gastric cancer; Micrometastasis

Indexed keywords

CANCER DIAGNOSIS; CANCER GROWTH; CANCER LOCALIZATION; CANCER PROGNOSIS; CELL ASSAY; CELL FUNCTION; CELL MIGRATION; CIRCULATING TUMOR CELL; CIRCULATING TUMOR MICROEMBOLUS; CONVENTIONAL METHOD; DIAGNOSTIC ACCURACY; DISEASE ASSOCIATION; EMBOLISM; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; MEDICAL PROCEDURES; METASTASIS; MICROFLUIDIC ANALYSIS; MICROMETASTASIS; MOLECULAR DYNAMICS; PREDICTION; PRIORITY JOURNAL; RECURRENT CANCER; SHORT SURVEY; STOMACH CANCER;

EID: 84878977030     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.04.021     Document Type: Review

References (149)

1. Ferlay J., Parkin D.M., Steliarova-Foucher E. Estimates of cancer incidence and mortality in Europe in 2008. Eur. J. Cancer 2008, 46(2010):765-781.
2. Siegel R., Naishadham D., Jemal A. Cancer statistics. Cancer J. Clin. 2012, 62:10-29.
3. Lin Y.S., Ueda J., Kikuchi S., Totsuka Y., Wei W.Q., Qiao Y.L., Inoue M. Comparative epidemiology of gastric cancer between Japan and China. World J. Gastroenterol. 2011, 17:4421-4428.
4. Bidard F.C., Mathiot C., Degeorges A., Etienne-Grimaldi M.C., Delva R., Pivot X., Veyret C., Bergougnoux L., de Cremoux P., Milano G., Pierga J.Y. Clinical value of circulating endothelial cells and circulating tumor cells in metastatic breast cancer patients treated first line with bevacizumab and chemotherapy. Ann. Oncol. 2010, 21:1765-1771.
5. Iinuma H., Watanabe T., Mimori K., Adachi M., Hayashi N., Tamura J., Matsuda K., Fukushima R., Okinaga K., Sasako M., Mori M. 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, 29:1547-1555.
6. van de Stolpe A., Pantel K., Sleijfer S., Terstappen L.W., den Toonder J.M. Circulating tumor cell isolation and diagnostics: toward routine clinical use. Cancer Res. 2011, 71:5955-5960.
7. Hou J.M., Krebs M.G., Lancashire L., Sloane R., Backen A., Swain R.K., Priest L.J., Greystoke A., Zhou C., Morris K., Ward T., Blackhall F.H., Dive C. Clinical significance and molecular characteristics of circulating tumor cells and circulating tumor microemboli in patients with small-cell lung cancer. J. Clin. Oncol. 2012, 30:525-532.
8. Georgoulias V., Bozionelou V., Agelaki S., Perraki M., Apostolaki S., Kallergi G., Kalbakis K., Xyrafas A., Mavroudis D. Trastuzumab decreases the incidence of clinical relapses in patients with early breast cancer presenting chemotherapy-resistant CK-19mRNA-positive circulating tumor cells: results of a randomized phase II study. Ann. Oncol. 2012, 23:1744-1750.
9. Hiraiwa K., Takeuchi H., Hasegawa H., Saikawa Y., Suda K., Ando T., Kumagai K., Irino T., Yoshikawa T., Matsuda S., Kitajima M., Kitagawa Y. Clinical significance of circulating tumor cells in blood from patients with gastrointestinal cancers. Ann. Surg. Oncol. 2008, 15:3092-3100.
10. Valastyan S., Weinberg R.A. Tumor metastasis: molecular insights and evolving paradigms. Cell 2011, 147:275-292.
11. den Toonder J. Circulating tumor cells: the grand challenge. Lab Chip 2011, 11:375-377.
12. Attard G., de Bono J.S. Utilizing circulating tumor cells: challenges and pitfalls. Curr. Opin. Genet. Dev. 2011, 21:50-58.
13. Pantel K., Alix-Panabieres C. Circulating tumour cells in cancer patients: challenges and perspectives. Trends Mol. Med. 2010, 16:398-406.
14. Chen J., Li J., Sun Y. Microfluidic approaches for cancer cell detection, characterization, and separation. Lab Chip 2012, 12:1753-1767.
15. Nagrath S., Sequist L.V., Maheswaran S., Bell D.W., Irimia D., Ulkus L., Smith M.R., Kwak E.L., Digumarthy S., Muzikansky A., Ryan P., Balis U.J., Tompkins R.G., Haber D.A., Toner M. Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature 2007, 450:1235-1239.
16. Saliba A.E., Saias L., Psychari E., Minc N., Simon D., Bidard F.C., Mathiot C., Pierga J.Y., Fraisier V., Salamero J., Saada V., Farace F., Vielh P., Malaquin L., Viovy J.L. Microfluidic sorting and multimodal typing of cancer cells in self-assembled magnetic arrays. Proc. Natl. Acad. Sci. USA 2010, 107:14524-14529.
17. Kang J.H., Krause S., Tobin H., Mammoto A., Kanapathipillai M., Ingber D.E. A combined micromagnetic-microfluidic device for rapid capture and culture of rare circulating tumor cells. Lab Chip 2012, 12:2175-2181.
18. Yu M., Stott S., Toner M., Maheswaran S., Haber D.A. Circulating tumor cells: approaches to isolation and characterization. J. Cell Biol. 2011, 192:373-382.
19. Diaz L.A., Williams R.T., Wu J., Kinde I., Hecht J.R., Berlin J., Allen B., Bozic I., Reiter J.G., Nowak M.A., Kinzler K.W., Oliner K.S., Vogelstein B. The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature 2012, 486:537-540.
20. Gillies R.J., Verduzco D., Gatenby R.A. Evolutionary dynamics of carcinogenesis and why targeted therapy does not work. Nat. Rev. Cancer 2012, 12:487-493.
21. Barbazan J., Alonso-Alconada L., Muinelo-Romay L., Vieito M., Abalo A., Alonso-Nocelo M., Candamio S., Gallardo E., Fernandez B., Abdulkader I., de Los Angeles Casares M., Gomez-Tato A., Lopez-Lopez R., Abal M. Molecular characterization of circulating tumor cells in human metastatic colorectal cancer. PLoS ONE 2012, 7:e40476.
22. Kallergi G., Agelaki S., Kalykaki A., Stournaras C., Mavroudis D., Georgoulias V. Phosphorylated EGFR and PI3K/Akt signaling kinases are expressed in circulating tumor cells of breast cancer patients. Breast Cancer Res. 2008, 10:R80.
23. 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.
24. Sirop S., Kanaan M., Korant A., Wiese D., Eilender D., Nagpal S., Arora M., Singh T., Saha S. Detection and prognostic impact of micrometastasis in colorectal cancer. J. Surg. Oncol. 2011, 103:534-537.
25. Arigami T., Uenosono Y., Yanagita S., Nakajo A., Ishigami S., Okumura H., Kijima Y., Ueno S., Natsugoe S. Clinical significance of lymph node micrometastasis in gastric cancer. Ann. Surg. Oncol. 2013, 20:515-521.
26. Chaffer C.L., Weinberg R.A. A perspective on cancer cell metastasis. Science 2011, 331:1559-1564.
27. Ksiazkiewicz M., Markiewicz A., Zaczek A.J. Epithelial-mesenchymal transition: a hallmark in metastasis formation linking circulating tumor cells and cancer stem cells. Pathobiology 2012, 79:195-208.
28. Bonnomet A., Brysse A., Tachsidis A., Waltham M., Thompson E.W., Polette M., Gilles C. Epithelial-to-mesenchymal transitions and circulating tumor cells. J. Mammary Gland Biol. Neoplasia 2010, 15:261-273.
29. Chang Y.S., di Tomaso E., McDonald D.M., Jones R., Jain R.K., Munn L.L. Mosaic blood vessels in tumors: frequency of cancer cells in contact with flowing blood. Proc. Natl. Acad. Sci. USA 2000, 97:14608-14613.
30. Luzzi K.J., MacDonald I.C., Schmidt E.E., Kerkvliet N., Morris V.L., Chambers A.F., Groom A.C. Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. Am. J. Pathol. 1998, 153:865-873.
31. Ikeguchi M., Kaibara N. Detection of circulating cancer cells after a gastrectomy for gastric cancer. Surg. Today 2005, 35:436-441.
32. Nanni P., Nicoletti G., Landuzzi L., Croci S., Murgo A., Palladini A., Antognoli A., Ianzano M.L., Stivani V., Grosso V., Maira S.M., Garcia-Echeverria C., Scotlandi K., De Giovanni C., Lollini P.L. High metastatic efficiency of human sarcoma cells in Rag2/gammac double knockout mice provides a powerful test system for antimetastatic targeted therapy. Eur. J. Cancer 2010, 46:659-668.
33. Chui M.H. Insights into cancer metastasis from a clinicopathologic perspective: epithelial-mesenchymal transition is not a necessary step. Int. J. Cancer 2012.
34. Thompson S.C. The colony forming efficiency of single cells and cell aggregates from a spontaneous mouse mammary tumour using the lung colony assay. Br. J. Cancer 1974, 30:332-336.
35. Yano H., Kitayama J., Hatano K., Tsuno N., Osada T., Watanabe T., Tsuruo T., Muto T., Nagawa H. Clustered cancer cells show a distinct adhesion behavior from single cell form under physiological shear conditions. J. Exp. Clin. Cancer Res. 2001, 20:407-412.
36. Fidler I.J. The relationship of embolic homogeneity, number, size and viability to the incidence of experimental metastasis. Eur. J. Cancer 1973, 9:223-227.
37. Al-Mehdi A.B., Tozawa K., Fisher A.B., Shientag L., Lee A., Muschel R.J. Intravascular origin of metastasis from the proliferation of endothelium-attached tumor cells: a new model for metastasis. Nat. Med. 2000, 6:100-102.
38. Vlodavsky I., Ariav Y., Atzmon R., Fuks Z. Tumor cell attachment to the vascular endothelium and subsequent degradation of the subendothelial extracellular matrix. Exp. Cell Res. 1982, 140:149-159.
39. Murata K., Miyoshi E., Ihara S., Noura S., Kameyama M., Ishikawa O., Doki Y., Yamada T., Ohigashi H., Sasaki Y., Higashiyama M., Tarui T., Takada Y., Kannagi R., Taniguchi N., Imaoka S. Attachment of human colon cancer cells to vascular endothelium is enhanced by N-acetylglucosaminyltransferase V. Oncology 2004, 66:492-501.
40. Sheski F.D., Natarajan V., Pottratz S.T. Tumor necrosis factor-alpha stimulates attachment of small cell lung carcinoma to endothelial cells. J. Lab. Clin. Med. 1999, 133:265-273.
41. Weigert O., Reindl W., Endres N., Lersch C. Low molecular weight heparin inhibits cytokine induced expression of adhesion molecules on endothelial cells and reduces attachment of pancreatic tumor cells. Gastroenterology 2001, 120:A167.
42. Kim M.Y., Oskarsson T., Acharyya S., Nguyen D.X., Zhang X.H.F., Norton L., Massague J. Tumor self-seeding by circulating cancer cells. Cell 2009, 139:1315-1326.
43. 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.
44. Wang N.F., Shi L., Li H.Y., Hu Y.J., Du W., Liu W., Zheng J.E., Huang S., Qu X.C. Detection of circulating tumor cells and tumor stem cells in patients with breast cancer by using flow cytometry. Tumor Biol. 2012, 33:561-569.
45. Soeth E., Vogel I., Roder C., Juhl H., Marxsen J., Kruger U., HenneBruns D., Kremer B., Kalthoff H. Comparative analysis of bone marrow and venous blood isolates from gastrointestinal cancer patients for the detection of disseminated tumor cells using reverse transcription PCR. Cancer Res. 1997, 57:3106-3110.
46. Kruger W., Jung R., Kroger N., Gutensohn K., Fiedler W., Neumaier M., Janicke F., Wagener C., Zander A.R. Sensitivity of assays designed for the detection of disseminated epithelial tumor cells is influenced by cell separation methods. Clin. Chem. 2000, 46:435-436.
47. Vona G., Sabile A., Louha M., Sitruk V., Romana S., Schutze K., Capron F., Franco D., Pazzagli M., Vekemans M., Lacour B., Brechot C., Paterlini-Brechot P. Isolation by size of epithelial tumor cells: a new method for the immunomorphological and molecular characterization of circulatingtumor cells. Am. J. Pathol. 2000, 156:57-63.
48. Hofman V., Ilie M.I., Long E., Selva E., Bonnetaud C., Molina T., Venissac N., Mouroux J., Vielh P., Hofman P. Detection of circulating tumor cells as a prognostic factor in patients undergoing radical surgery for non-small-cell lung carcinoma: comparison of the efficacy of the Cell Search Assay (TM) and the isolation by size of epithelial tumor cell method. Int. J. Cancer 2011, 129:1651-1660.
49. Hofman V., Long E., Ilie M., Bonnetaud C., Vignaud J.M., Flejou J.F., Lantuejoul S., Piaton E., Mourad N., Butori C., Selva E., Marquette C.H., Poudenx M., Sibon S., Kelhef S., Venissac N., Jais J.P., Mouroux J., Molina T.J., Vielh P., Hofman P. Morphological analysis of circulating tumour cells in patients undergoing surgery for non-small cell lung carcinoma using the isolation by size of epithelial tumour cell (ISET) method. Cytopathology 2012, 23:30-38.
50. Desitter I., Guerrouahen B.S., Benali-Furet N., Wechsler J., Janne P.A., Kuang Y., Yanagita M., Wang L., Berkowitz J.A., Distel R.J., Cayre Y.E. A new device for rapid isolation by size and characterization of rare circulating tumor cells. Anticancer Res. 2011, 31:427-441.
51. Vona G., Estepa L., Beroud C., Damotte D., Capron F., Nalpas B., Mineur A., Franco D., Lacour B., Pol S., Brechot C., Paterlini-Brechot P. Impact of cytomorphological detection of circulating tumor cells in patients with liver cancer. Hepatology 2004, 39:792-797.
52. Notta F., Doulatov S., Laurenti E., Poeppl A., Jurisica I., Dick J.E. Isolation of single human hematopoietic stem cells capable of long-term multilineage engraftment. Science 2011, 333:218-221.
53. Hwu D., Boutrus S., Greiner C., DiMeo T., Kuperwasser C., Georgakoudi I. Assessment of the role of circulating breast cancer cells in tumor formation and metastatic potential using in vivo flow cytometry. J. Biomed. Opt. 2011, 16:040501.
54. He W., Wang H., Hartmann L.C., Cheng J.X., Low P.S. In vivo quantitation of rare circulating tumor cells by multiphoton intravital flow cytometry. Proc. Natl. Acad. Sci. USA 2007, 104:11760-11765.
55. Hu Y., Fan L., Zheng J., Cui R., Liu W., He Y., Li X., Huang S. Detection of circulating tumor cells in breast cancer patients utilizing multiparameter flow cytometry and assessment of the prognosis of patients in different CTCs levels. Cytom. Part A: J. Int. Soc. Anal. Cytol. 2010, 77:213-219.
56. Konigsberg R., Gneist M., Jahn-Kuch D., Pfeiler G., Hager G., Hudec M., Dittrich C., Zeillinger R. Circulating tumor cells in metastatic colorectal cancer: efficacy and feasibility of different enrichment methods. Cancer Lett. 2010, 293:117-123.
57. Guo J., Yao F., Lou Y., Xu C., Xiao B., Zhou W., Chen J., Hu Y., Liu Z. Detecting carcinoma cells in peripheral blood of patients with hepatocellular carcinoma by immunomagnetic beads and rt-PCR. J. Clin. Gastroenterol. 2007, 41:783-788.
58. Riethdorf S., Fritsche H., Muller V., Rau T., Schindlbeck C., Rack B., Janni W., Coith C., Beck K., Janicke F., Jackson S., Gornet T., Cristofanilli M., Pantel K. Detection of circulating tumor cells in peripheral blood of patients with metastatic breast cancer: a validation study of the cell search system. Clin. Cancer Res. 2007, 13:920-928.
59. Allard W.J., Matera J., Miller M.C., Repollet M., Connelly M.C., Rao C., Tibbe A.G., Uhr J.W., Terstappen L.W. 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, 10:6897-6904.
60. Andreopoulou E., Yang L.Y., Rangel K.M., Reuben J.M., Hsu L., Krishnamurthy S., Valero V., Fritsche H.A., Cristofanilli M. Comparison of assay methods for detection of circulating tumor cells in metastatic breast cancer: AdnaGen AdnaTest BreastCancer Select/Detect versus Veridex Cell Search system. Int. J. Cancer 2012, 130:1590-1597.
61. Whitesides G.M. The origins and the future of microfluidics. Nature 2006, 442:368-373.
62. Didar T.F., Tabrizian M. Adhesion based detection, sorting and enrichment of cells in microfluidic Lab-on-Chip devices. Lab Chip 2010, 10:3043-3053.
63. Stott S.L., Hsu C.H., Tsukrov D.I., Yu M., Miyamoto D.T., Waltman B.A., Rothenberg S.M., Shah A.M., Smas M.E., Korir G.K., Floyd F.P., Gilman A.J., Lord J.B., Winokur D., Springer S., Irimia D., Nagrath S., Sequist L.V., Lee R.J., Isselbacher K.J., Maheswaran S., Haber D.A., Toner M. Isolation of circulating tumor cells using a microvortex-generating herringbone-chip. Proc. Natl. Acad. Sci. USA 2010, 107:18392-18397.
64. Kirby B.J., Jodari M., Loftus M.S., Gakhar G., Pratt E.D., Chanel-Vos C., Gleghorn J.P., Santana S.M., Liu H., Smith J.P., Navarro V.N., Tagawa S.T., Bander N.H., Nanus D.M., Giannakakou P. Functional characterization of circulating tumor cells with a prostate-cancer-specific microfluidic device. PLoS ONE 2012, 7:e35976.
65. 2 nanofiber-based cell capture assay for detecting circulating tumor cells from colorectal and gastric cancer patients. Adv. Mater. 2012, 24:2756-2760.
66. Park G.S., Kwon H., Kwak D.W., Park S.Y., Kim M., Lee J.H., Han H., Heo S., Li X.S., Kim Y.H., Lee J.G., Yang W., Cho H.Y., Kim S.K., Kim K. Full surface embedding of gold clusters on silicon nanowires for efficient capture and photothermal therapy of circulating tumor cells. Nano Lett. 2012, 12:1638-1642.
67. Plouffe B.D., Lewis L.H., Murthy S.K. Computational design optimization for microfluidic magnetophoresis. Biomicrofluidics 2011, 5:13413.
68. Ito H., Inoue H., Sando N., Kimura S., Gohda K., Sato J., Murakami K., Ito S., Odaka N., Satodate H., Kudo S.E. Prognostic impact of detecting viable circulating tumour cells in gastric cancer patients using a telomerase-specific viral agent: a prospective study. BMC Cancer 2012, 12:346.
69. Tan S.J., Yobas L., Lee G.Y., Ong C.N., Lim C.T. Microdevice for the isolation and enumeration of cancer cells from blood. Biomed. Microdevices 2009, 11:883-892.
70. Hosokawa M., Hayata T., Fukuda Y., Arakaki A., Yoshino T., Tanaka T., Matsunaga T. Size-selective microcavity array for rapid and efficient detection of circulating tumor cells. Anal. Chem. 2010, 82:6629-6635.
71. Alazzam A., Stiharu I., Bhat R., Meguerditchian A.N. Interdigitated comb-like electrodes for continuous separation of malignant cells from blood using dielectrophoresis. Electrophoresis 2011, 32:1327-1336.
72. Hsieh H.B., Marrinucci D., Bethel K., Curry D.N., Humphrey M., Krivacic R.T., Kroener J., Kroener L., Ladanyi A., Lazarus N., Kuhn P., Bruce R.H., Nieva J. High speed detection of circulating tumor cells. Biosens. Bioelectron. 2006, 21:1893-1899.
73. Somlo G., Lau S.K., Frankel P., Ben Hsieh H., Liu X.H., Yang L.X., Krivacic R., Bruce R.H. Multiple biomarker expression on circulating tumor cells in comparison to tumor tissues from primary and metastatic sites in patients with locally advanced/inflammatory, and stage IV breast cancer, using a novel detection technology. Breast Cancer Res. Treat. 2011, 128:155-163.
74. Lu J., Fan T., Zhao Q., Zeng W., Zaslavsky E., Chen J.J., Frohman M.A., Golightly M.G., Madajewicz S., Chen W.T. Isolation of circulating epithelial and tumor progenitor cells with an invasive phenotype from breast cancer patients. Int. J. Cancer 2010, 126:669-683.
75. Galanzha E.I., Shashkov E.V., Kelly T., Kim J.W., Yang L.L., Zharov V.P. In vivo magnetic enrichment and multiplex photoacoustic detection of circulating tumour cells. Nat. Nanotechnol. 2009, 4:855-860.
76. Liu Z., Fusi A., Klopocki E., Schmittel A., Tinhofer I., Nonnenmacher A., Keilholz U. Negative enrichment by immunomagnetic nanobeads for unbiased characterization of circulating tumor cells from peripheral blood of cancer patients. J. Transl. Med. 2011, 9:70.
77. Eifler R.L., Lind J., Falkenhagen D., Weber V., Fischer M.B., Zeillinger R. Enrichment of circulating tumor cells from a large blood volume using leukapheresis and elutriation: proof of concept. Cytom. Part B: Clin. Cytom. 2011, 80B:100-111.
78. Farace F., Massard C., Vimond N., Drusch F., Jacques N., Billiot F., Laplanche A., Chauchereau A., Lacroix L., Planchard D., Le Moulec S., Andre F., Fizazi K., Soria J.C., Vielh P. A direct comparison of Cell Search and ISET for circulating tumour-cell detection in patients with metastatic carcinomas. Br. J. Cancer 2011, 105:847-853.
79. Wenqi D., Li W., Shanshan C., Bei C., Yafei Z., Feihu B., Jie L., Daiming F. EpCAM is overexpressed in gastric cancer and its downregulation suppresses proliferation of gastric cancer. J. Cancer Res. Clin. Oncol. 2009, 135:1277-1285.
80. Bonnomet A., Syne L., Brysse A., Feyereisen E., Thompson E.W., Noel A., Foidart J.M., Birembaut P., Polette M., Gilles C. A dynamic in vivo model of epithelial-to-mesenchymal transitions in circulating tumor cells and metastases of breast cancer. Oncogene 2012, 31:3741-3753.
81. 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.
82. 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.
83. 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. MCR 2011, 9:997-1007.
84. 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.
85. 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.
86. Hou J.M., Krebs M., Ward T., Sloane R., Priest L., Hughes A., Clack G., Ranson M., Blackhall F., Dive C. Circulating tumor cells as a window on metastasis biology in lung cancer. Am. J. Pathol. 2011, 178:989-996.
87. Mostert B., Kraan J., Bolt-de Vries J., van der Spoel P., Sieuwerts A.M., Schutte M., Timmermans A.M., Foekens R., Martens J.W.M., Gratama J.W., Foekens J.A., Sleijfer S. Detection of circulating tumor cells in breast cancer may improve through enrichment with anti-CD146. Breast Cancer Res. Treat. 2011, 127:33-41.
88. Mostert B., Kraan J., Sieuwerts A.M., van der Spoel P., Bolt-de Vries J., Prager-van der Smissen W.J.C., Smid M., Timmermans A.M., Martens J.W.M., Gratama J.W., Foekens J.A., Sleijfer S. CD49f-based selection of circulating tumor cells (CTCs) improves detection across breast cancer subtypes. Cancer Lett. 2012, 319:49-55.
89. Yang J., Weinberg R.A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 2008, 14:818-829.
90. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
91. Kalluri R., Neilson E.G. Epithelial-mesenchymal transition and its implications for fibrosis. J. Clin. Invest. 2003, 112:1776-1784.
92. Huber M.A., Kraut N., Beug H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr. Opin. Cell Biol. 2005, 17:548-558.
93. Turley E.A., Veiseh M., Radisky D.C., Bissell M.J. Mechanisms of disease: epithelial-mesenchymal transition-does cellular plasticity fuel neoplastic progression?. Nat. Clin. Pract. Oncol. 2008, 5:280-290.
94. Wan Y., Mahmood M.A., Li N., Allen P.B., Kim Y.T., Bachoo R., Ellington A.D., Iqbal S.M. Nanotextured substrates with immobilized aptamers for cancer cell isolation and cytology. Cancer 2012, 118:1145-1154.
95. Phillips J.A., Xu Y., Xia Z., Fan Z.H., Tan W.H. Enrichment of cancer cells using aptamers immobilized on a microfluidic channel. Anal. Chem. 2009, 81:1033-1039.
96. Dardaei L., Shahsavani R., Ghavamzadeh A., Behmanesh M., Aslankoohi E., Alimoghaddam K., Ghaffari S.H. The detection of disseminated tumor cells in bone marrow and peripheral blood of gastric cancer patients by multimarker (CEA, CK20, TFF1 and MUC2) quantitative real-time PCR. Clin. Biochem. 2011, 44:325-330.
97. Tani N., Ichikawa D., Ikoma D., Tomita H., Sai S., Ikoma H., Okamoto K., Ochiai T., Ueda Y., Otsuji E., Yamagishi H., Miura N., Shiota G. Circulating cell-free mRNA in plasma as a tumor marker for patients with primary and recurrent gastric cancer. Anticancer Res. 2007, 27:1207-1212.
98. Zhou H., Guo J.M., Lou Y.R., Zhang X.J., Zhong F.D., Jiang Z., Cheng J., Xiao B.X. Detection of circulating tumor cells in peripheral blood from patients with gastric cancer using microRNA as a marker. J. Mol. Med. (Berl.) 2010, 88:709-717.
99. Zheng Y., Cui L., Sun W., Zhou H., Yuan X., Huo M., Chen J., Lou Y., Guo J. MicroRNA-21 is a new marker of circulating tumor cells in gastric cancer patients. Cancer Biomar. 2011, 10:71-77.
100. Zhou H., Xiao B., Zhou F., Deng H., Zhang X., Lou Y., Gong Z., Du C., Guo J. MiR-421 is a functional marker of circulating tumor cells in gastric cancer patients. Biomarkers 2012, 17:104-110.
101. Cui L., Lou Y., Zhang X., Zhou H., Deng H., Song H., Yu X., Xiao B., Wang W., Guo J. Detection of circulating tumor cells in peripheral blood from patients with gastric cancer using piRNAs as markers. Clin. Biochem. 2011, 44:1050-1057.
102. Miyazono F., Natsugoe S., Takao S., Tokuda K., Kijima F., Aridome K., Hokita S., Baba M., Eizuru Y., Aikou T. Surgical maneuvers enhance molecular detection of circulating tumor cells during gastric cancer surgery. Ann. Surg. 2001, 233:189-194.
103. Wu C.H., Lin S.R., Hsieh J.S., Chen F.M., Lu C.Y., Yu F.J., Cheng T.L., Huang T.J., Huang S.Y., Wang J.Y. Molecular detection of disseminated tumor cells in the peripheral blood of patients with gastric cancer: evaluation of their prognostic significance. Dis. Markers 2006, 22:103-109.
104. Wu C.H., Lin S.R., Yu F.J., Wu D.C., Pan Y.S., Hsieh J.S., Huang S.Y., Wang J.Y. Development of a high-throughput membrane-array method for molecular diagnosis of circulating tumor cells in patients with gastric cancers. Int. J. Cancer 2006, 119:373-379.
105. Gonzalez C.A., Agudo A. Carcinogenesis, prevention and early detection of gastric cancer: where we are and where we should go. Int. J. Cancer 2012, 130:745-753.
106. Youn H.G., An J.Y., Choi M.G., Noh J.H., Sohn T.S., Kim S. Recurrence after curative resection of early gastric cancer. Ann. Surg. Oncol. 2010, 17:448-454.
107. Lai J.F., Kim S., Kim K., Li C., Oh S.J., Hyung W.J., Rha S.Y., Chung H.C., Choi S.H., Wang L.B., Noh S.H. Prediction of recurrence of early gastric cancer after curative resection. Ann. Surg. Oncol. 2009, 16:1896-1902.
108. Sohn Y.J., Jang J.S., Choi S.R., Kwon H.C., Jung G.J., Kim M.C., Jeong J.S. Early detection of recurrence after endoscopic treatment for early gastric cancer. Scand. J. Gastroenterol. 2009, 44:1109-1114.
109. Kim J.J., Song K.Y., Hur H., Hur J.I., Park S.M., Park C.H. Lymph node micrometastasis in node negative early gastric cancer. Eur. J. Surg. Oncol. 2009, 35:409-414.
110. Cao L., Hu X., Zhang Y., Huang G. Adverse prognosis of clustered-cell versus single-cell micrometastases in pN0 early gastric cancer. J. Surg. Oncol. 2011, 103:53-56.
111. Maehara Y., Oshiro T., Endo K., Baba H., Oda S., Ichiyoshi Y., Kohnoe S., Sugimachi K. Clinical significance of occult micrometastasis lymph nodes from patients with early gastric cancer who died of recurrence. Surgery 1996, 119:397-402.
112. Nakajo A., Natsugoe S., Ishigami S., Matsumoto M., Nakashima S., Hokita S., Baba M., Takao S., Aikou T. Detection and prediction of micrometastasis in the lymph nodes of patients with pN0 gastric cancer. Ann. Surg. Oncol. 2001, 8:158-162.
113. Sonoda H., Yamamoto K., Kushima R., Okabe H., Tani T. Detection of lymph node micrometastasis in gastric cancer by MUC2 RT-PCR: usefulness in pT1 cases. J. Surg. Oncol. 2004, 88:63-70.
114. Sonoda H., Yamamoto K., Kushima R., Yamamoto H., Naitoh H., Okabe H., Tani T. Detection of lymph node micrometastasis in pN0 early gastric cancer: efficacy of duplex RT-PCR with MUC2 and TFF1 in mucosal cancer. Oncol. Rep. 2006, 16:411-416.
115. Husemann Y., Geigl J.B., Schubert F., Musiani P., Meyer M., Burghart E., Forni G., Eils R., Fehm T., RiethmUller G., Klein C.A. Systemic spread is an early step in breast cancer. Cancer Cell 2008, 13:58-68.
116. Noh Y.H., Im G., Ku J.H., Lee Y.S., Ahn M.J. Detection of tumor cell contamination in peripheral blood by RT-PCR in gastrointestinal cancer patients. J. Korean Med. Sci. 1999, 14:623-628.
117. Majima T., Ichikura T., Takayama E., Chochi K., Mochizuki H. Detecting circulating cancer cells using reverse transcriptase-polymerase chain reaction for cytokeratin mRNA in peripheral blood from patients with gastric cancer. Jpn. J. Clin. Oncol. 2000, 30:499-503.
118. * as blood-based markers for discriminating malignant from benign lung tumors. PLoS ONE 2012, 7:e38248.
119. Zachariah R.R., Schmid S., Buerki N., Radpour R., Holzgreve W., Zhong X. Levels of circulating cell-free nuclear and mitochondrial DNA in benign and malignant ovarian tumors. Obstet. Gynecol. 2008, 112:843-850.
120. Liu H.S., Zhu L., Liu B.Y., Yang L., Meng X.X., Zhang W., Ma Y.Y., Xiao H.S. Genome-wide microRNA profiles identify miR-378 as a serum biomarker for early detection of gastric cancer. Cancer Lett. 2012, 316:196-203.
121. Arigami T., Uenosono Y., Hirata M., Yanagita S., Ishigami S., Natsugoe S. B7-H3 expression in gastric cancer: a novel molecular blood marker for detecting circulating tumor cells. Cancer Sci. 2011, 102:1019-1024.
122. Cao W.G., Yang W.P., Li H., Lou G.Y., Jiang J.S., Geng M., Xi W.Q., Ren R.B., Qu Q., Jin X.L., Zhu Y.B., Jin Y.N. Using detection of survivin-expressing circulating tumor cells in peripheral blood to predict tumor recurrence following curative resection of gastric cancer. J. Surg. Oncol. 2011, 103:110-115.
123. Tao H.Q., He X.J., Ma Y.Y., Wang H.J., Xia Y.J., Ye Z.Y., Zhao Z.S. Evaluation of REG4 for early diagnosis and prognosis of gastric cancer. Hum. Pathol. 2011, 42:1401-1409.
124. Song J., Lee H.J., Cho G.S., Han S.U., Kim M.C., Ryu S.W., Kim W., Song K.Y., Kim H.H., Hyung W.J. Recurrence following laparoscopy-assisted gastrectomy for gastric cancer: a multicenter retrospective analysis of 1417 patients. Ann. Surg. Oncol. 2010, 17:1777-1786.
125. Huang K.H., Chen J.H., Wu C.W., Lo S.S., Hsieh M.C., Li A.F., Lui W.Y. Factors affecting recurrence in node-negative advanced gastric cancer. J. Gastroenterol. Hepatol. 2009, 24:1522-1526.
126. Sumikura S., Ishigami S., Natsugoe S., Miyazono F., Tokuda K., Nakajo A., Okumura H., Matsumoto M., Hokita S., Aikou T. Disseminated cancer cells in the blood and expression of sialylated antigen in gastric cancer. Cancer Lett. 2003, 200:77-83.
127. Yie S.M., Lou B., Ye S.R., Cao M., He X., Li P., Hu K., Rao L., Wu S.M., Xiao H.B., Gao E. Detection of survivin-expressing circulating cancer cells (CCCs) in peripheral blood of patients with gastric and colorectal cancer reveals high risks of relapse. Ann. Surg. Oncol. 2008, 15:3073-3082.
128. Seo J.H., Choi C.W., Kim B.S., Shin S.W., Kim Y.H., Kim J.S., Lee S.W., Choi J.H., Park Y.T., Mok Y.J., Kim C.S. Follow-up study of peripheral blood carcinoembryonic antigen mRNA using reverse transcription-polymerase chain reaction as an early marker of clinical recurrence in patients with curatively resected gastric cancer. Am. J. Clin. Oncol. 2005, 28:24-29.
129. Saad A.A., Awed N.M., Abd Elkerim N.N., El-Shennawy D., Alfons M.A., Elserafy M.E., Darwish Y.W., Barakat E.M., Ezz-Elarab S.S. Prognostic significance of E-cadherin expression and peripheral blood micrometastasis in gastric carcinoma patients. Ann. Surg. Oncol. 2010, 17:3059-3067.
130. Han T.S., Kong S.H., Lee H.J., Ahn H.S., Hur K., Yu J., Kim W.H., Yang H.K. Dissemination of free cancer cells from the gastric lumen and from perigastric lymphovascular pedicles during radical gastric cancer surgery. Ann. Surg. Oncol. 2011, 18:2818-2825.
131. Garcia-Olmo D.C., Gutierrez-Gonzalez L., Samos J., Picazo M.G., Atienzar M., Garcia-Olmo D. Surgery and hematogenous dissemination: comparison between the detection of circulating tumor cells and of tumor DNA in plasma before and after tumor resection in rats. Ann. Surg. Oncol. 2006, 13:1136-1144.
132. Nishida S., Kitamura K., Ichikawa D., Koike H., Tani N., Yamagishi H. Molecular detection of disseminated cancer cells in the peripheral blood of patients with gastric cancer. Anticancer Res. 2000, 20:2155-2159.
133. Matsusaka S., Chin K., Ogura M., Suenaga M., Shinozaki E., Mishima Y., Terui Y., Mizunuma N., Hatake K. Circulating tumor cells as a surrogate marker for determining response to chemotherapy in patients with advanced gastric cancer. Cancer Sci. 2010, 101:1067-1071.
134. Powell A.A., Talasaz A.H., Zhang H., Coram M.A., Reddy A., Deng G., Telli M.L., Advani R.H., Carlson R.W., Mollick J.A., Sheth S., Kurian A.W., Ford J.M., Stockdale F.E., Quake S.R., Pease R.F., Mindrinos M.N., Bhanot G., Dairkee S.H., Davis R.W., Jeffrey S.S. Single cell profiling of circulating tumor cells: transcriptional heterogeneity and diversity from breast cancer cell lines. PLoS ONE 2012, 7:e33788.
135. Pestrin M., Bessi S., Puglisi F., Minisini A.M., Masci G., Battelli N., Ravaioli A., Gianni L., Di Marsico R., Tondini C., Gori S., Coombes C.R., Stebbing J., Biganzoli L., Buyse M., Di Leo A. Final results of a multicenter phase II clinical trial evaluating the activity of single-agent lapatinib in patients with HER2-negative metastatic breast cancer and HER2-positive circulating tumor cells. A proof-of-concept study. Breast Cancer Res. Treat. 2012, 134:283-289.
136. Pituch-Noworolska A., Kolodziejczyk P., Kulig J., Drabik G., Szczepanik A., Czupryna A., Popiela T., Zembala M. Circulating tumour cells and survival of patients with gastric cancer. Anticancer Res. 2007, 27:635-640.
137. Yeh K.H., Chen Y.C., Yeh S.H., Chen C.P., Lin J.T., Cheng A.L. Detection of circulating cancer cells by nested reverse transcription-polymerase chain reaction of cytokeratin-19 (K19)-possible clinical significance in advanced gastric cancer. Anticancer Res. 1998, 18:1283-1286.
138. Noh Y.H., Kim J.A., Lim G.R., Ro Y.T., Koo J.H., Lee Y.S., Han D.S., Park H.K., Ahn M.J. Detection of circulating tumor cells in patients with gastrointestinal tract cancer using RT-PCR and its clinical implications. Exp. Mol. Med. 2001, 33:8-14.
139. Illert B., Fein M., Otto C., Cording F., Stehle D., Thiede A., Timmermann W. Disseminated tumor cells in the blood of patients with gastric cancer are an independent predictive marker of poor prognosis. Scand. J. Gastroenterol. 2005, 40:843-849.
140. Uen Y.H., Lin S.R., Wu C.H., Hsieh J.S., Lu C.Y., Yu F.J., Huang T.J., Wang J.Y. Clinical significance of MUC1 and c-Met RT-PCR detection of circulating tumor cells in patients with gastric carcinoma. Clin. Chim. Acta 2006, 367:55-61.
141. Bertazza L., Mocellin S., Marchet A., Pilati P., Gabrieli J., Scalerta R., Nitti D. Survivin gene levels in the peripheral blood of patients with gastric cancer independently predict survival. J. Transl. Med. 2009, 7:111.
142. Ren C., Han C., Wang D., Wang B., Xu X., Zhang J., Zhou L., Wu Z. A new isolation method for peripheral blood circulating solid tumor cells with EpCAM antibodylinked nanobeads. Chin. J. Lab. Med. 2011, 34:218-223.
143. Wang G.Y., Li Y., Yu Y.M., Yu B., Zhang Z.Y., Liu Y., Wang S.J. Detection of disseminated tumor cells in bone marrow of gastric cancer using magnetic activated cell sorting and fluorescent activated cell sorting. J. Gastroenterol. Hepatol. 2009, 24:299-306.
144. Scheunemann P., Stoecklein N.H., Hermann K., Rehders A., Eisenberger C.F., Knoefel W.T., Hosch S.B. Occult disseminated tumor cells in lymph nodes of patients with gastric carcinoma. A critical appraisal of assessment and relevance, Langenbecks. Arch. Surg. 2009, 394:105-113.
145. Buergy D., Fuchs T., Kambakamba P., Mudduluru G., Maurer G., Post S., Tang Y., Nakada M.T., Yan L., Allgayer H. Prognostic impact of extracellular matrix metalloprotease inducer: immunohistochemical analyses of colorectal tumors and immunocytochemical screening of disseminated tumor cells in bone marrow from patients with gastrointestinal cancer. Cancer 2009, 115:4667-4678.
146. Koga T., Tokunaga E., Sumiyoshi Y., Oki E., Oda S., Takahashi I., Kakeji Y., Baba H., Maehara Y. Detection of circulating gastric cancer cells in peripheral blood using real time quantitative RT-PCR. Hepatogastroenterology 2008, 55:1131-1135.
147. Heiss M.M., Simon E.H., Beyer B.C., Gruetzner K.U., Tarabichi A., Babic R., Schildberg F.W., Allgayer H. Minimal residual disease in gastric cancer: evidence of an independent prognostic relevance of urokinase receptor expression by disseminated tumor cells in the bone marrow. J. Clin. Oncol. 2002, 20:2005-2016.
148. Ramskold D., Luo S., Wang Y.C., Li R., Deng Q., Faridani O.R., Daniels G.A., Khrebtukova I., Loring J.F., Laurent L.C., Schroth G.P., Sandberg R. Full-length mRNA-Seq from single-cell levels of RNA and individual circulating tumor cells. Nat. Biotechnol. 2012, 30:777-782.
149. Yu M., Ting D.T., Stott S.L., Wittner B.S., Ozsolak F., Paul S., Ciciliano J.C., Smas M.E., Winokur D., Gilman A.J., Ulman M.J., Xega K., Contino G., Alagesan B., Brannigan B.W., Milos P.M., Ryan D.P., Sequist L.V., Bardeesy N., Ramaswamy S., Toner M., Maheswaran S., Haber D.A. RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis. Nature 2012, 487:510-513.