EpCAM-independent enrichment of circulating tumor cells in metastatic breast cancer

PLoS ONE

Volumn 10, Issue 12, 2015, Pages

  Schneck, Helen ^a   Gierke, Berthold ^b   Uppenkamp, Frauke ^a   Behrens, Bianca ^c   Niederacher, Dieter ^a   Stoecklein, Nikolas H ^c   Templin, Markus F ^b   Pawlak, Michael ^b   Fehm, Tanja ^a   Neubauer, Hans ^a  

^a UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA6 INTEGRIN; CD146 ANTIGEN; CD47 ANTIGEN; CELL SURFACE PROTEIN; COLLAGEN TYPE 1; CYTOKERATIN 8; EPITHELIAL CELL ADHESION MOLECULE; HERMES ANTIGEN; HYALURONIC ACID; LAMININ; PROTEIN ADAM8; PROTEIN TEM8; PROTEIN TROP2; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; EPCAM PROTEIN, HUMAN; MEMBRANE ANTIGEN; MONOCLONAL ANTIBODY; SCLEROPROTEIN; TUMOR ANTIGEN; TUMOR MARKER;

ADULT; AGED; ARTICLE; BREAST CANCER CELL LINE; BREAST METASTASIS; CELL ADHESION; CIRCULATING TUMOR CELL; CLINICAL ARTICLE; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENOMICS; HUMAN; HUMAN CELL; IMMOBILIZATION; IMMUNOFLUORESCENCE; MIDDLE AGED; MOLECULAR BIOLOGY; PROTEIN BINDING; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; SINGLE CELL ANALYSIS; STAINING; BLOOD; BREAST NEOPLASMS; FEMALE; IMMUNOLOGY; MCF-7 CELL LINE; METABOLISM; METASTASIS; PATHOLOGY; TUMOR CELL LINE; TUMOR EMBOLISM;

ADULT; AGED; ANTIBODIES, MONOCLONAL; ANTIGENS, NEOPLASM; ANTIGENS, SURFACE; BIOMARKERS, TUMOR; BREAST NEOPLASMS; CELL ADHESION MOLECULES; CELL LINE, TUMOR; COMPARATIVE GENOMIC HYBRIDIZATION; EPITHELIAL CELL ADHESION MOLECULE; EXTRACELLULAR MATRIX PROTEINS; FEMALE; HUMANS; MCF-7 CELLS; MIDDLE AGED; NEOPLASM METASTASIS; NEOPLASTIC CELLS, CIRCULATING; SINGLE-CELL ANALYSIS;

EID: 84957050335     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0144535     Document Type: Article

References (87)

1. Joosse SA, Gorges TM, Pantel K. Biology, detection, and clinical implications of circulating tumor cells. EMBO Molecular Medicine. 2014; 7(1):1-11. doi: 10.15252/emmm.201303698 PMID: 25398926
2. Zhang L, Riethdorf S, Wu G, Wang T, Yang K, Peng G, et al. Meta-Analysis of the Prognostic Value of Circulating Tumor Cells in Breast Cancer. Clinical Cancer Research. 2012; 18(20):5701-10. doi: 10.1158/1078-0432.CCR-12-1587 PMID: 22908097
3. Budd GT, Cristofanilli M, Ellis MJ, Stopeck A, Borden E, Miller MC, et al. Circulating Tumor Cells versus Imaging - Predicting Overall Survival in Metastatic Breast Cancer. Clinical Cancer Research. 2006; 12(21):6403-9. doi: 10.1158/1078-0432.CCR-05-1769 PMID: 17085652
4. Bidard F-C, Peeters DJ, Fehm T, Nolé F, Gisbert-Criado R, Mavroudis D, et al. Clinical validity of circulating tumour cells in patients with metastatic breast cancer: a pooled analysis of individual patient data. The Lancet Oncology. 2014; 15(4):406-14. doi: 10.1016/S1470-2045(14)70069-5 PMID: 24636208
5. Pantel K, Alix-Panabières C. Circulating tumour cells in cancer patients: challenges and perspectives. Trends in Molecular Medicine. 2010; 16(9):398-406. doi: 10.1016/j.molmed.2010.07.001 PMID: 20667783
6. Butler TP, Gullino PM. Quantitation of Cell Shedding into Efferent Blood of Mammary Adenocarcinoma. Cancer research. 1975; 35(3):512-6. PMID: 1090362
7. Vanharanta S, Massagué J. Origins of Metastatic Traits. Cancer cell. 2013; 24(4):410-21. doi: 10.1016/j.ccr.2013.09.007 PMID: 24135279
8. Allard WJ, Matera J, Miller MC, Repollet M, Connelly MC, Rao C, et al. Tumor Cells Circulate in the Peripheral Blood of All Major Carcinomas but not in Healthy Subjects or Patients With Nonmalignant Diseases. Clinical Cancer Research. 2004; 10(20):6897-904. doi: 10.1158/1078-0432.CCR-04-0378 PMID: 15501967
9. Coumans FAW, Ligthart ST, Uhr JW, Terstappen LWMM. Challenges in the Enumeration and Phenotyping of CTC. Clinical Cancer Research. 2012; 18(20):5711-8. doi: 10.1158/1078-0432.CCR-12-1585 PMID: 23014524
10. Barradas AMC, Terstappen LWMM. Towards the Biological Understanding of CTC: Capture Technologies, Definitions and Potential to Create Metastasis. Cancers. 2013; 5(4):1619-42. doi: 10.3390/cancers5041619 PMID: 24305653
11. Alix-Panabières C. EPISPOT Assay: Detection of Viable DTCs/CTCs in Solid Tumor Patients. In: Ignatiadis M, Sotiriou C, Pantel K, editors. Minimal Residual Disease and Circulating Tumor Cells in Breast Cancer. Recent Results in Cancer Research. 195: Springer Berlin Heidelberg; 2012. p. 69-76.
12. Nagrath S, Sequist LV, Maheswaran S, Bell DW, Irimia D, Ulkus L, et al. Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature. 2007; 450(7173):1235-9. PMID: 18097410
13. Lu J, Fan T, Zhao Q, Zeng W, Zaslavsky E, Chen JJ, et al. Isolation of circulating epithelial and tumor progenitor cells with an invasive phenotype from breast cancer patients. International Journal of Cancer. 2010; 126(3):669-83. doi: 10.1002/ijc.24814
14. Harb W, Fan A, Tran T, Danila DC, Keys D, Schwartz M, et al. Mutational Analysis of Circulating Tumor Cells Using a Novel Microfluidic Collection Device and qPCR Assay. Translational Oncology. 2013; 6(5):528-38. PMID: 24151533
15. Choi H, Kim KB, Jeon CS, Hwang I, Lee S, Kim HK, et al. A label-free DC impedance-based microcytometer for circulating rare cancer cell counting. Lab on a Chip. 2013; 13(5):970-7. doi: 10.1039/C2LC41376K PMID: 23340965
16. Coumans FAW, van Dalum G, Beck M, Terstappen LWMM. Filter Characteristics Influencing Circulating Tumor Cell Enrichment from Whole Blood. PLoS ONE. 2013; 8(4):e61770. doi: 10.1371/journal.pone.0061770 PMID: 23626725
17. Kim YJ, Koo G-B, Lee J-Y, Moon H-S, Kim D-G, Lee D-G, et al. A microchip filter device incorporating slit arrays and 3-D flow for detection of circulating tumor cells using CAV1-EpCAM conjugated microbeads. Biomaterials. 2014; 35(26):7501-10. doi: 10.1016/j.biomaterials.2014.05.039 PMID: 24917030
18. Ozkumur E, Shah AM, Ciciliano JC, Emmink BL, Miyamoto DT, Brachtel E, et al. Inertial Focusing for Tumor Antigen-Dependent and-Independent Sorting of Rare Circulating Tumor Cells. Science Translational Medicine. 2013; 5(179):179ra47. doi: 10.1126/scitranslmed.3005616 PMID: 23552373
19. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer. 2002; 2(6):442-54. PMID: 12189386
20. Onder TT, Gupta PB, Mani SA, Yang J, Lander ES, Weinberg RA. Loss of E-Cadherin Promotes Metastasis via Multiple Downstream Transcriptional Pathways. Cancer research. 2008; 68(10):3645-54. doi: 10.1158/0008-5472.CAN-07-2938 PMID: 18483246
21. Tam WL, Weinberg RA. The epigenetics of epithelial-mesenchymal plasticity in cancer. Nat Med. 2013; 19(11):1438-49. doi: 10.1038/nm.3336 PMID: 24202396
22. Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science. 2013; 339(6119):580-4. doi: 10.1126/science.1228522 PMID: 23372014
23. Gorges T, Tinhofer I, Drosch M, Rose L, Zollner T, Krahn T, et al. Circulating tumour cells escape from EpCAM-based detection due to epithelial-to-mesenchymal transition. BMC Cancer. 2012; 12(1):178. doi: 10.1186/1471-2407-12-178
24. Mikolajczyk SD, Millar LS, Tsinberg P, Coutts SM, Zomorrodi M, Pham T, et al. Detection of EpCAM-Negative and Cytokeratin-Negative Circulating Tumor Cells in Peripheral Blood. Journal of Oncology. 2011; 2011:252361. doi: 10.1155/2011/252361 PMID: 21577258
25. Mostert B, Kraan J, Bolt-de Vries J, van der Spoel P, Sieuwerts A, Schutte M, et al. Detection of circulating tumor cells in breast cancer may improve through enrichment with anti-CD146. Breast Cancer Research and Treatment. 2011; 127(1):33-41. doi: 10.1007/s10549-010-0879-y PMID: 20379845
26. Mostert B, Kraan J, Sieuwerts AM, van der Spoel P, Bolt-de Vries J, Prager-van der Smissen WJC, et al. CD49f-based selection of circulating tumor cells (CTCs) improves detection across breast cancer subtypes. Cancer Letters. 2012; 319(1):49-55. doi: 10.1016/j.canlet.2011.12.031 PMID: 22202642
27. Obermajer N, Doljak B, Kos J. Cytokeratin 8 ectoplasmic domain binds urokinase-type plasminogen activator to breast tumor cells and modulates their adhesion, growth and invasiveness. Molecular Cancer. 2009; 8(1):88.
28. Baccelli I, Schneeweiss A, Riethdorf S, Stenzinger A, Schillert A, Vogel V, et al. Identification of a population of blood circulating tumor cells from breast cancer patients that initiates metastasis in a xenograft assay. Nature biotechnology. 2013; 31(6):539-44. doi: 10.1038/nbt.2576 PMID: 23609047
29. Romagnoli M, Mineva ND, Polmear M, Conrad C, Srinivasan S, Loussouarn D, et al. ADAM8 expression in invasive breast cancer promotes tumor dissemination and metastasis. EMBO Molecular Medicine. 2013; 6(2):278-94. doi: 10.1002/emmm.201303373 PMID: 24375628
30. Chen D, Bhat-Nakshatri P, Goswami C, Badve S, Nakshatri H. ANTXR1, a stem cell-enriched functional biomarker, connects collagen signaling to cancer stem-like cells and metastasis in breast cancer. Cancer research. 2013; 73(18):5821-33. doi: 10.1158/0008-5472.CAN-13-1080 PMID: 23832666
31. Gozgit JM, Pentecost BT, Marconi SA, Otis CN, Wu C, Arcaro KF. Use of an Aggressive MCF-7 Cell Line Variant, TMX2-28, to Study Cell Invasion in Breast Cancer. Molecular Cancer Research. 2006; 4(12):905-13. doi: 10.1158/1541-7786.MCR-06-0147 PMID: 17189381
32. Schneck H, Blassl C, Meier-Stiegen F, Neves RP, Janni W, Fehm T, et al. Analysing the mutational status of PIK3CA in circulating tumor cells from metastatic breast cancer patients. Molecular oncology. 2013; 7(5):976-86. doi: 10.1016/j.molonc.2013.07.007 PMID: 23895914
33. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Meth. 2012; 9(7):676-82.
34. Möhlendick B, Bartenhagen C, Behrens B, Honisch E, Raba K, Knoefel WT, et al. A Robust Method to Analyze Copy Number Alterations of Less than 100 kb in Single Cells Using Oligonucleotide Array CGH. PLoS One. 2013; 8(6):e67031. doi: 10.1371/journal.pone.0067031 PMID: 23825608
35. Neves RPL, Raba K, Schmidt O, Honisch E, Meier-Stiegen F, Behrens B, et al. Genomic High-Resolution Profiling of Single CKpos/CD45neg Flow-Sorting Purified Circulating Tumor Cells from Patients with Metastatic Breast Cancer. Clinical Chemistry. 2014; 60(10):1290-7. doi: 10.1373/clinchem.2014.222331 PMID: 25267515
36. Möhlendick B, Stoecklein N. Analysis of Copy-Number Alterations in Single Cells Using Microarray-Based Comparative Genomic Hybridization (aCGH). Curr Protoc Cell Biol. 2014; 1(65):22.19.1-22.19.23. doi: 10.1002/0471143030.cb2219s65
37. Gancberg D, Di Leo A, Cardoso F, Rouas G, Pedrocchi M, Paesmans M, et al. Comparison of HER-2 status between primary breast cancer and corresponding distant metastatic sites. Annals of Oncology. 2002; 13(7):1036-43. doi: 10.1093/annonc/mdf252 PMID: 12176781
38. Meng S, Tripathy D, Frenkel EP, Shete S, Naftalis EZ, Huth JF, et al. Circulating Tumor Cells in Patients with Breast Cancer Dormancy. Clinical Cancer Research. 2004; 10(24):8152-62. doi: 10.1158/1078-0432.CCR-04-1110 PMID: 15623589
39. Mueller V, Pantel K. HER2 as marker for the detection of circulating tumor cells. Breast Cancer Research and Treatment. 2009; 117(3):535-7. doi: 10.1007/s10549-008-0276-y PMID: 19115105
40. Powell AA, Talasaz AH, Zhang H, Coram MA, Reddy A, Deng G, et al. Single cell profiling of Circulating tumor cells: Transcriptional heterogeneity and diversity from breast cancer cell lines. PLoS ONE. 2012; 7(5):e33788. doi: 10.1371/journal.pone.0033788 PMID: 22586443
41. Qu Q, Zong Y, Fei X-c, Chen X-s, Xu C, Lou G-y, et al. The importance of biopsy in clinically diagnosed metastatic lesions in patients with breast cancer. World Journal of Surgical Oncology. 2014; 12:93. doi: 10.1186/1477-7819-12-93 PMID: 24721777
42. Gasch C, Bauernhofer T, Pichler M, Langer-Freitag S, Reeh M, Seifert AM, et al. Heterogeneity of Epidermal Growth Factor Receptor Status and Mutations of KRAS/PIK3CA in Circulating Tumor Cells of Patients with Colorectal Cancer. Clinical Chemistry. 2013; 59(1):252-60. doi: 10.1373/clinchem.2012.188557 PMID: 23136247
43. Balzar M, Winter MJ, de Boer CJ, Litvinov SV. The biology of the 17-1A antigen (Ep-CAM). Journal of Molecular Medicine. 1999; 77(10):699-712. doi: 10.1007/s001099900038 PMID: 10606205
44. Went PTH, Lugli A, Meier S, Bundi M, Mirlacher M, Sauter G, et al. Frequent EpCam protein expression in human carcinomas. Human Pathology. 2004; 35(1):122-8. doi: 10.1016/j.humpath.2003.08.026 PMID: 14745734
45. Massoner P, Thomm T, Mack B, Untergasser G, Martowicz A, Bobowski K, et al. EpCAM is overexpressed in local and metastatic prostate cancer, suppressed by chemotherapy and modulated by MET-associated miRNA-200c/205. Br J Cancer. 2014; 111(5):955-64. doi: 10.1038/bjc.2014.366 PMID: 24992580
46. Tai KY, Shiah SG, Shieh YS, Kao YR, Chi CY, Huang E, et al. DNA methylation and histone modification regulate silencing of epithelial cell adhesion molecule for tumor invasion and progression. Oncogene. 2007; 26(27):3989-97. PMID: 17213811
47. Punnoose EA, Atwal SK, Spoerke JM, Savage H, Pandita A, Yeh R-F, et al. Molecular Biomarker Analyses Using Circulating Tumor Cells. PLoS ONE. 2010; 5(9):e12517. doi: 10.1371/journal.pone.0012517 PMID: 20838621
48. Thurm H, Ebel S, Kentenich C, Hemsen A, Riethdorf S, Coith C, et al. Rare Expression of Epithelial Cell Adhesion Molecule on Residual Micrometastatic Breast Cancer Cells after Adjuvant Chemotherapy. Clinical Cancer Research. 2003; 9(7):2598-604. PMID: 12855636
49. Gires O, Stoecklein NH. Dynamic EpCAM expression on circulating and disseminating tumor cells: causes and consequences. Cellular and Molecular Life Sciences. 2014; 71(22):4393-402. doi: 10.1007/s00018-014-1693-1 PMID: 25103341
50. Patriarca C, Macchi RM, Marschner AK, Mellstedt H. Epithelial cell adhesion molecule expression (CD326) in cancer: A short review. Cancer Treatment Reviews. 2012; 38(1):68-75. doi: 10.1016/j.ctrv.2011.04.002 PMID: 21576002
51. Songun I, Litvinov SV, van de Velde CJH, Pals ST, Hermans J, van Krieken JHJM. Loss of Ep-CAM (CO17-1A) expression predicts survival in patients with gastric cancer. Br J Cancer. 2005; 92(9):1767-72. PMID: 15870832
52. van der Gun BTF, Melchers LJ, Ruiters MHJ, de Leij LFMH, McLaughlin PMJ, Rots MG. EpCAM in carcinogenesis: the good, the bad or the ugly. Carcinogenesis. 2010; 31(11):1913-21. doi: 10.1093/carcin/bgq187 PMID: 20837599
53. Rao CG, Chianese D, Doyle GV, Miller MC, Russell T, Sanders RA, et al. Expression of epithelial cell adhesion molecule in carcinoma cells present in blood and primary and metastatic tumors. International Journal of Oncology. 2005; 27(1):49-57. PMID: 15942643
54. Vannier C, Mock K, Brabletz T, Driever W. Zeb1 Regulates E-cadherin and Epcam (Epithelial Cell Adhesion Molecule) Expression to Control Cell Behavior in Early Zebrafish Development. Journal of Biological Chemistry. 2013; 288(26):18643-59. doi: 10.1074/jbc.M113.467787 PMID: 23667256
55. Gosens MJEM, van Kempen LCL, van de Velde CJH, van Krieken JHJM, Nagtegaal ID. Loss of membranous Ep-CAM in budding colorectal carcinoma cells. Mod Pathol. 2007; 20(2):221-32. PMID: 17361206
56. Driemel C, Kremling H, Schumacher S, Will D, Wolters J, Lindenlauf N, et al. Context-dependent adaption of EpCAM expression in early systemic esophageal cancer. Oncogene. 2014; 33(41):4904-15. doi: 10.1038/onc.2013.441 PMID: 24141784
57. Wang Y, Shenouda S, Baranwal S, Rathinam R, Jain P, Bao L, et al. Integrin subunits alpha5 and alpha6 regulate cell cycle by modulating the chk1 and Rb/E2F pathways to affect breast cancer metastasis. Molecular Cancer. 2011; 10(1):84.
58. Welm BE, Tepera SB, Venezia T, Graubert TA, Rosen JM, Goodell MA. Sca-1pos Cells in the Mouse Mammary Gland Represent an Enriched Progenitor Cell Population. Developmental Biology. 2002; 245(1):42-56. doi: 10.1006/dbio.2002.0625 PMID: 11969254
59. Cariati M, Naderi A, Brown JP, Smalley MJ, Pinder SE, Caldas C, et al. Alpha-6 integrin is necessary for the tumourigenicity of a stem cell-like subpopulation within the MCF7 breast cancer cell line. International Journal of Cancer. 2008; 122(2):298-304. doi: 10.1002/ijc.23103
60. Honeth G, Bendahl P-O, Ringnér M, Saal LH, Gruvberger-Saal SK, Lövgren K, et al. The CD44+/CD24- phenotype is enriched in basal-like breast tumors. Breast Cancer Research: BCR. 2008; 10(3):R53. doi: 10.1186/bcr2108 PMID: 18559090
61. Lawson DA, Xin L, Lukacs RU, Cheng D, Witte ON. Isolation and functional characterization of murine prostate stem cells. Proceedings of the National Academy of Sciences of the United States of America. 2007; 104(1):181-6. doi: 10.1073/pnas.0609684104 PMID: 17185413
62. Grossman HB, Lee C, Bromberg J, Liebert M. Expression of the alpha6beta4 integrin provides prognostic information in bladder cancer. Oncology Reports. 2000; 7(1):13-9. PMID: 10601583
63. Lim E, Vaillant F, Wu D, Forrest NC, Pal B, Hart AH, et al. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med. 2009; 15(8):907-13. doi: 10.1038/nm.2000 PMID: 19648928
64. Vieira AF, Ricardo S, Ablett MP, Dionísio MR, Mendes N, Albergaria A, et al. P-Cadherin Is Coexpressed with CD44 and CD49f and Mediates Stem Cell Properties in Basal-like Breast Cancer. STEM CELLS. 2012; 30(5):854-64. doi: 10.1002/stem.1075 PMID: 22389315
65. Fornaro M, Dell'Arciprete R, Stella M, Bucci C, Nutini M, Capri MG, et al. Cloning of the gene encoding Trop-2, a cell-surface glycoprotein expressed by human carcinomas. Int J Cancer. 1995; 65(5):610-8.
66. Guerra E, Trerotola M, Aloisi AL, Tripaldi R, Vacca G, La Sorda R, et al. The Trop-2 signalling network in cancer growth. Oncogene. 2013; 32(12):1594-600. doi: 10.1038/onc.2012.151 PMID: 22562244
67. Trerotola M, Jernigan DL, Liu Q, Siddiqui J, Fatatis A, Languino LR. Trop-2 promotes prostate cancer metastasis by modulating β(1) integrin functions. Cancer research. 2013; 73(10):3155-67. doi: 10.1158/0008-5472.CAN-12-3266 PMID: 23536555
68. Baccelli I, Stenzinger A, Vogel V, Maria Pfitzner B, Klein C, Wallwiener M, et al. Co-expression of MET and CD47 is a novel prognosticator for survival of luminal-type breast cancer patients. Oncotarget. 2014; 5(18):8147-60. PMID: 25230070
69. Hembrough TA, Vasudevan J, Allietta MM, Glass WF, Gonias SL. A cytokeratin 8-like protein with plasminogen-binding activity is present on the external surfaces of hepatocytes, HepG2 cells and breast carcinoma cell lines. J Cell Sci. 1995; 108:1071-82. PMID: 7542667
70. Hembrough TA, Li L, Gonias S. Cell-surface cytokeratin 8 is the major plasminogen receptor on breast cancer cells and is required for the accelerated activation of cell-associated plasminogen by tissue-type plasminogen activator. J Biol Chem. 1996; 271:25684-91. PMID: 8810346
71. Godfroid E, Geuskens M, Dupressoir T, Parent I, Szpirer C. Cytokeratins are exposed on the outer surface of established human mammary carcinoma cells. Journal of Cell Science. 1991; 99(3):595-607.
72. Gonias S, Hembrough T, Sankovic M. Cytokeratin 8 functions as a major plasminogen receptor in select epithelial and carcinoma cells. Front Biosci. 2001; 6:D1403-11. PMID: 11689350
73. Liu F, Chen Z, Wang J, Shao X, Cui Z, Yang C, et al. Overexpression of Cell Surface Cytokeratin 8 in Multidrug-Resistant MCF-7/MX Cells Enhances Cell Adhesion to the Extracellular Matrix. Neoplasia (New York, NY). 2008; 10(11):1275-84.
74. Hanahan D, Weinberg RA. Hallmarks of Cancer: The Next Generation. Cell. 2011; 144(5):646-74. doi: 10.1016/j.cell.2011.02.013 PMID: 21376230
75. Brown TJ, Thomas NK. Role of Hyaluronan Metabolism in the Initiation, Invasion, and Metastasis of Breast Cancer. In: Stern RBT, editor. Hyaluronan in Cancer Biology. San Diego: Academic Press; 2009.
76. Peach RJ, Hollenbaugh D, Stamenkovic I, Aruffo A. Identification of hyaluronic acid binding sites in the extracellular domain of CD44. The Journal of Cell Biology. 1993; 122(1):257-64. doi: 10.1083/jcb.122.1.257 PMID: 8314845
77. Wang C, Thor AD, Moore DH, Zhao Y, Kerschmann R, Stern R, et al. The overexpression of RHAMM, a hyaluronan-binding protein that regulates ras signaling, correlates with overexpression of mitogen-activated protein kinase and is a significant parameter in breast cancer progression. Clinical Cancer Research. 1998; 4(3):567-76. PMID: 9533523
78. Hamilton SR, Fard SF, Paiwand FF, Tolg C, Veiseh M, Wang C, et al. The hyaluronan receptors CD44 and RHAMM (CD168) form Complexes with ERK1/2, which sustain high basal motility in breast cancer cells. The Journal of biological chemistry. 2007; 282(22):16667-80. doi: 10.1074/jbc.M702078200 PMID: 17392272
79. Yu M, Stott S, Toner M, Maheswaran S, Haber DA. Circulating tumor cells: approaches to isolation and characterization. The Journal of Cell Biology. 2011; 192(3):373-82. doi: 10.1083/jcb.201010021 PMID: 21300848
80. Nel I, Jehn U, Gauler T, Hoffmann A-C. Individual profiling of circulating tumor cell composition in patients with non-small cell lung cancer receiving platinum based treatment. Translational Lung Cancer Research. 2014; 3(2):100-6. doi: 10.3978/j.issn.2218-6751.2014.03.05 PMID: 25806288
81. Khoo BL, Warkiani ME, Tan DS-W, Bhagat AAS, Irwin D, Lau DP, et al. Clinical Validation of an Ultra High-Throughput Spiral Microfluidics for the Detection and Enrichment of Viable Circulating Tumor Cells. PLoS ONE. 2014; 9(7):e99409. doi: 10.1371/journal.pone.0099409 PMID: 24999991
82. Stott SL, Hsu C-H, Tsukrov DI, Yu M, Miyamoto DT, Waltman BA, et al. Isolation of circulating tumor cells using a microvortex-generating herringbone-chip. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107(43):18392-7. doi: 10.1073/pnas.1012539107 PMID: 20930119
83. Ramakrishnan M, Mathur SR, Mukhopadhyay A. Fusion-Derived Epithelial Cancer Cells Express Hematopoietic Markers and Contribute to Stem Cell and Migratory Phenotype in Ovarian Carcinoma. Cancer research. 2013; 73(17):5360-70. doi: 10.1158/0008-5472.CAN-13-0896 PMID: 23856249
84. Fischer JC, Niederacher D, Topp SA, Honisch E, Schumacher S, Schmitz N, et al. Diagnostic leukapheresis enables reliable detection of circulating tumor cells of nonmetastatic cancer patients. Proceedings of the National Academy of Sciences of the United States of America. 2013; 110(41):16580-5. doi: 10.1073/pnas.1313594110 PMID: 24065821
85. Cho EH, Wendel M, Luttgen M, Yoshioka C, Marrinucci D, Lazar D, et al. Characterization of circulating tumor cell aggregates identified in patients with epithelial tumors. Physical Biology. 2012; 9(1):16001. doi: 10.1088/1478-3975/9/1/016001
86. Aceto N, Bardia A, Miyamoto DT, Donaldson MC, Wittner BS, Spencer JA, et al. Circulating Tumor Cell Clusters Are Oligoclonal Precursors of Breast Cancer Metastasis. Cell. 2014; 158(5):1110-22. doi: 10.1016/j.cell.2014.07.013 PMID: 25171411
87. Harris TJC, Tepass U. Adherens junctions: from molecules to morphogenesis. Nature Reviews Molecular Cell Biology. 2010; 11:502-14. doi: 10.1038/nrm2927 PMID: 20571587