Inertial focusing for tumor antigen-dependent and -independent sorting of rare circulating tumor cells

Science Translational Medicine

Volumn 5, Issue 179, 2013, Pages

  Ozkumur, Emre ^a   Shah, Ajay M ^a   Ciciliano, Jordan C ^b   Emmink, Benjamin L ^a   Miyamoto, David T ^a,b   Brachtel, Elena ^a   Yu, Min ^b,c   Chen, Pin I ^a   Morgan, Bailey ^a   Trautwein, Julie ^b   Kimura, Anya ^b   Sengupta, Sudarshana ^b   Stott, Shannon L ^a,b   Karabacak, Nezihi Murat ^a   Barber, Thomas A ^a   Walsh, John R ^a   Smith, Kyle ^a   Spuhler, Philipp S ^a   Sullivan, James P ^a,b   Lee, Richard J ^a,b   Ting, David T ^a,b   Luo, Xi ^b,c   Shaw, Alice T ^a,b   Bardia, Aditya ^a,b   Sequist, Lecia V ^a,b   Louis, David N ^a   Maheswaran, Shyamala ^a,b   Kapur, Ravi ^a   Haber, Daniel A ^a,b,c   Toner, Mehmet ^a   more..

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD45 ANTIGEN; CYTOKERATIN 18; CYTOKERATIN 19; CYTOKERATIN 8; EML4 ALK FUSION PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; HYBRID PROTEIN; PROSTATE SPECIFIC ANTIGEN; PROSTATE SPECIFIC MEMBRANE ANTIGEN; TUMOR ANTIGEN; UNCLASSIFIED DRUG;

ANTIGEN DETECTION; ARTICLE; BREAST METASTASIS; CANCER DIAGNOSIS; CELL ISOLATION; CELL SELECTION; CIRCULATING TUMOR CELL; COLORECTAL CANCER; CONTROLLED STUDY; DIAGNOSTIC TEST ACCURACY STUDY; EQUIPMENT DESIGN; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOMAGNETIC SEPARATION; LUNG CANCER; MALE; MELANOMA; MICROCHIP ANALYSIS; MICROFLUIDIC ANALYSIS; PANCREAS CANCER; PRIORITY JOURNAL; PROSTATE CANCER; RNA ANALYSIS; SENSITIVITY AND SPECIFICITY; SINGLE CELL ANALYSIS; VALIDATION PROCESS;

ANTIGENS, NEOPLASM; CELL LINE, TUMOR; CELL SEPARATION; CELL SHAPE; CELL SIZE; FEMALE; HUMANS; MAGNETIC PHENOMENA; MALE; MICROFLUIDICS; NEOPLASTIC CELLS, CIRCULATING; RNA, NEOPLASM;

EID: 84875970076     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3005616     Document Type: Article

References (30)

1. K. Pantel, R. H. Brakenhoff, B. Brandt, Detection, clinical relevance and specific biological properties of disseminating tumour cells. Nat. Rev. Cancer 8, 329-340 (2008).
2. M. Yu, S. Stott, M. Toner, S. Maheswaran, D. A. Haber, Circulating tumor cells: Approaches to isolation and characterization. J. Cell Biol. 192, 373-382 (2011).
3. M. C. Miller, G. V. Doyle, L. W. Terstappen, Significance of circulating tumor cells detected by the cellsearch system in patients with metastatic breast colorectal and prostate cancer. J. Oncol. 2010, 617421 (2010).
4. S. Maheswaran, L. V. Sequist, S. Nagrath, L. Ulkus, B. Brannigan, C. V. Collura, E. Inserra, S. Diederichs, A. J. Iafrate, D. W. Bell, S. Digumarthy, A. Muzikansky, D. Irimia, J. Settleman, R. G. Tompkins, T. J. Lynch, M. Toner, D. A. Haber, Detection of mutations in EGFR in circulating lung-cancer cells. N. Engl. J. Med. 359, 366-377 (2008).
5. J. M. Lang, B. P. Casavant, D. J. Beebe, Circulating tumor cells: Getting more from less. Sci. Transl. Med. 4, 141ps13 (2012).
6. 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. 101, 10501-10504 (2004).
7. D. Marrinucci, K. Bethel, A. Kolatkar, M. S. Luttgen, M. Malchiodi, F. Baehring, K. Voigt, D. Lazar, J. Nieva, L. Bazhenova, A. H. Ko, W. M. Korn, E. Schram, M. Coward, X. Yang, T. Metzner, R. Lamy, M. Honnatti, C. Yoshioka, J. Kunken, Y. Petrova, D. Sok, D. Nelson, P. Kuhn, Fluid biopsy in patients with metastatic prostate, pancreatic and breast cancers. Phys. Biol. 9, 016003 (2012).
8. D. Issadore, J. Chung, H. Shao, M. Liong, A. A. Ghazani, C. M. Castro, R. Weissleder, H. Lee, Ultrasensitive clinical enumeration of rare cells ex vivo using a micro-Hall detector. Sci. Transl. Med. 4, 141ra92 (2012).
9. S. Miltenyi, W. Müller, W. Weichel, A. Radbruch, High gradient magnetic cell separation with MACS. Cytometry 11, 231-238 (1990).
10. G. Deng, M. Herrler, D. Burgess, E. Manna, D. Krag, J. F. Burke, Enrichment with anti-cytokeratin alone or combined with anti-EpCAM antibodies significantly increases the sensitivity for circulating tumor cell detection in metastatic breast cancer patients. Breast Cancer Res. 10, R69 (2008).
11. A. H. Talasaz, A. A. Powell, D. E. Huber, J. G. Berbee, K. H. Roh, W. Yu, W. Xiao, M. M. Davis, R. F. Pease, M. N. Mindrinos, S. S. Jeffrey, R. W. Davis, Isolating highly enriched populations of circulating epithelial cells and other rare cells from blood using a magnetic sweeper device. Proc. Natl. Acad. Sci. U.S.A. 106, 3970-3975 (2009).
12. R. Kalluri, R. A. Weinberg, The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119, 1420-1428 (2009).
13. O. Lara, X. Tong, M. Zborowski, J. J. Chalmers, Enrichment of rare cancer cells through depletion of normal cells using density and flow-through, immunomagnetic cell separation. Exp. Hematol. 32, 891-904 (2004).
14. L. Yang, J. C. Lang, P. Balasubramanian, K. R. Jatana, D. Schuller, A. Agrawal, M. Zborowski, J. J. Chalmers, Optimization of an enrichment process for circulating tumor cells from the blood of head and neck cancer patients through depletion of normal cells. Biotechnol. Bioeng. 102, 521-534 (2009).
15. 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).
16. S. L. Stott, C. H. Hsu, D. I. Tsukrov, M. Yu, D. T. Miyamoto, B. A. Waltman, S. M. Rothenberg, A. M. Shah, M. E. Smas, G. K. Korir, F. P. Floyd Jr., A. J. Gilman, J. B. Lord, D. Winokur, S. Springer, D. Irimia, S. Nagrath, L. V. Sequist, R. J. Lee, K. J. Isselbacher, S. Maheswaran, D. A. Haber, M. Toner, Isolation of circulating tumor cells using a microvortex-generating herringbone-chip. Proc. Natl. Acad. Sci. U.S.A. 107, 18392-18397 (2010).
17. S. Wang, K. Liu, J. Liu, Z. T. F. Yu, X. Xu, L. Zhao, T. Lee, E. K. Lee, J. Reiss, Y.-K. Lee, L.W. K. Chung, J. Huang, M. Rettig, D. Seligson, K. N. Duraiswamy, C. K. Shen, H. R. Tseng, Highly efficient capture of circulating tumor cells by using nanostructured silicon substrates with integrated chaotic micromixers. Angew. Chem. Int. Ed. Engl. 50, 3084-3088 (2011).
18. U. Dharmasiri, S. K. Njoroge, M. A. Witek, M.G. Adebiyi, J. W. Kamande, M. L. Hupert, F. Barany, S. A. Soper, High-throughput selection, enumeration, electrokinetic manipulation, and molecular profiling of low-abundance circulating tumor cells using a microfluidic system. Anal. Chem. 83, 2301-2309 (2011).
19. S. L. Stott, R. J. Lee, S. Nagrath, M. Yu, D. T.Miyamoto, L. Ulkus, E. J. Inserra, M. Ulman, S. Springer, Z. Nakamura, A. L. Moore, D. I. Tsukrov, M. E. Kempner, D. M. Dahl, C. L. Wu, A. J. Iafrate, M. R. Smith, R. G. Tompkins, L. V. Sequist, M. Toner, D. A. Haber, S. Maheswaran, Isolation and characterization of circulating tumor cells from patients with localized and metastatic prostate cancer. Sci. Transl. Med. 2, 25ra23 (2010).
20. 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).
21. D. T. Miyamoto, R. J. Lee, S. L. Stott, D. T. Ting, B. S. Wittner, M. Ulman, M. E. Smas, J. B. Lord, B. W. Brannigan, J. Trautwein, N. H. Bander, C. L. Wu, L. V. Sequist, M. R. Smith, S. Ramaswamy, M. Toner, S. Maheswaran, D. A. Haber, Androgen receptor signaling in circulating tumor cells as a marker of hormonally responsive prostate cancer. Cancer Discov. 2, 995-1003 (2012).
22. L. R. Huang, E. C. Cox, R. H. Austin, J. C. Sturm, Continuous particle separation through deterministic lateral displacement. Science 304, 987-990 (2004).
23. D. Di Carlo, D. Irimia, R. G. Tompkins, M. Toner, Continuous inertial focusing, ordering, and separation of particles in microchannels. Proc. Natl. Acad. Sci. U.S.A. 104, 18892-18897 (2007).
24. R. Huang, T. A. Barber, M. A. Schmidt, R. G. Tompkins, M. Toner, D. W. Bianchi, R. Kapur, W. L. Flejter, A microfluidics approach for the isolation of nucleated red blood cells (NRBCs) from the peripheral blood of pregnant women. Prenat. Diagn. 28, 892-899 (2008).
25. G. Segré, A. Silberberg, Radial particle displacements in Poiseuille flow of suspensions. Nature 189, 209-210 (1961).
26. A. M. Sieuwerts, J. Kraan, J. Bolt, P. van der Spoel, F. Elstrodt, M. Schutte, J. W. M. Martens, J. W. Gratama, S. Sleijfer, J. A. Foekens, Anti-epithelial cell adhesion molecule antibodies and the detection of circulating normal-like breast tumor cells. J. Natl. Cancer Inst. 101, 61-66 (2009).
27. M. Yu, G. A. Smolen, J. Zhang, B.Wittner, B. J. Schott, E. Brachtel, S. Ramaswamy, S. Maheswaran, D. A. Haber, A developmentally regulated inducer of EMT, LBX1, contributes to breast cancer progression. Genes Dev. 23, 1737-1742 (2009).
28. D. A. Haber, N. S. Gray, J. Baselga, The evolving war on cancer. Cell 145, 19-24 (2011).
29. B. D. Plouffe, L. H. Lewis, S. K. Murthy, Computational design optimization for microfluidic magnetophoresis. Biomicrofluidics 5, 13413 (2011).
30. 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).