Microslit on a chip: A simplified filter to capture circulating tumor cells enlarged with microbeads

English version

Autoři: Seung Joon Lee ^aff001; Tae Seok Sim ^aff003; Hyun Young Shin ^aff001; Jungmin Lee ^aff001; Min Young Kim ^aff001; Joseph Sunoo ^aff002; Jeong-Gun Lee ^aff003; Kyungmoo Yea ^aff001; Young Zoon Kim ^aff004; Danny van Noort ^aff001; Soo Kyung Park ^aff002; Woon-Hae Kim ^aff001; Kyun Woo Park ^aff006; Minseok S. Kim ^aff001
Působiště autorů: Department of New Biology, DGIST, Daegu, Republic of Korea ^aff001; CytoDx, Pangyo-ro, Beon-gil, Bundang-gu, Seongnam-si, Gyeonggi-do, Republic of Korea ^aff002; Samsung Electronics, Ltd., Maetan3-dong, Youngtong-gu, Suwon-si, Gyeonggi-do, Republic of Korea ^aff003; Division of Neurooncology and Department of Neurosurgery, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, Changwon, Republic of Korea ^aff004; Division of Biotechnology, IFM, Linköping University, Linköping, Sweden ^aff005; Daejeon Wellness Hospital, Beon-gil, Dongseo-daero, Daedeok-gu, Daejeon, Republic of Korea ^aff006; Translational Responsive Medicine Center, DGIST, Daegu, Republic of Korea ^aff007
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223193

Souhrn

Microchips are widely used to separate circulating tumor cells (CTCs) from whole blood by virtues of sophisticated manipulation for microparticles. Here, we present a chip with an 8 μm high and 27.9 mm wide slit to capture cancer cells bound to 3 μm beads. Apart from a higher purity and recovery rate, the slit design allows for simplified fabrication, easy cell imaging, less clogging, lower chamber pressure and, therefore, higher throughput. The beads were conjugated with anti-epithelial cell adhesion molecules (anti-EpCAM) to selectively bind to breast cancer cells (MCF-7) used to spike the whole blood. The diameter of the cell-bead construct was in average 23.1 μm, making them separable from other cells in the blood. As a result, the cancer cells were separated from 5 mL of whole blood with a purity of 52.0% and a recovery rate of 91.1%, and also we confirmed that the device can be applicable to clinical samples of human breast cancer patients. The simple design with microslit, by eliminating any high-aspect ratio features, is expected to reduce possible defects on the chip and, therefore, more suitable for mass production without false separation outputs.

Klíčová slova:

Blood – Blood cells – Breast cancer – Flow rate – Fluid flow – Glass – Microfluidics – Microbeads

Zdroje

1. 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. Clin Cancer Res. 2004;10(20):6897–904. doi: 10.1158/1078-0432.CCR-04-0378 15501967.

2. Giuliano M, Giordano A, Jackson S, De Giorgi U, Mego M, Cohen EN, et al. Circulating tumor cells as early predictors of metastatic spread in breast cancer patients with limited metastatic dissemination. Breast Cancer Res. 2014;16(5):440. doi: 10.1186/s13058-014-0440-8 25223629; PubMed Central PMCID: PMC4303121.

3. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science. 2011;331(6024):1559–64. doi: 10.1126/science.1203543 21436443.

4. Miller MC, Doyle GV, Terstappen LW. Significance of Circulating Tumor Cells Detected by the CellSearch System in Patients with Metastatic Breast Colorectal and Prostate Cancer. J Oncol. 2010;2010:617421. doi: 10.1155/2010/617421 20016752; PubMed Central PMCID: PMC2793426.

5. Khetani S, Mohammadi M, Nezhad AS. Filter-based isolation, enrichment, and characterization of circulating tumor cells. Biotechnol Bioeng. 2018;115(10):2504–29. Epub 2018/07/11. doi: 10.1002/bit.26787 29989145.

6. Aggarwal C, Meropol NJ, Punt CJ, Iannotti N, Saidman BH, Sabbath KD, et al. Relationship among circulating tumor cells, CEA and overall survival in patients with metastatic colorectal cancer. Ann Oncol. 2013;24(2):420–8. doi: 10.1093/annonc/mds336 23028040.

7. Hou JM, Krebs MG, Lancashire L, Sloane R, Backen A, Swain RK, et al. 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(5):525–32. doi: 10.1200/JCO.2010.33.3716 22253462.

8. Khan MS, Kirkwood A, Tsigani T, Garcia-Hernandez J, Hartley JA, Caplin ME, et al. Circulating tumor cells as prognostic markers in neuroendocrine tumors. J Clin Oncol. 2013;31(3):365–72. doi: 10.1200/JCO.2012.44.2905 23248251.

9. Riethdorf S, Muller V, Loibl S, Nekljudova V, Weber K, Huober J, et al. Prognostic Impact of Circulating Tumor Cells for Breast Cancer Patients Treated in the Neoadjuvant "Geparquattro" Trial. Clin Cancer Res. 2017;23(18):5384–93. doi: 10.1158/1078-0432.CCR-17-0255 28679772.

10. Liu H, Sun B, Wang S, Liu C, Lu Y, Li D, et al. Circulating Tumor Cells as a Biomarker in Pancreatic Ductal Adenocarcinoma. Cell Physiol Biochem. 2017;42(1):373–82. doi: 10.1159/000477481 28558380.

11. Friedlander TW, Fong L. The end of the beginning: circulating tumor cells as a biomarker in castration-resistant prostate cancer. J Clin Oncol. 2014;32(11):1104–6. doi: 10.1200/JCO.2013.54.7307 24616311.

12. Barradas AM, Terstappen LW. Towards the Biological Understanding of CTC: Capture Technologies, Definitions and Potential to Create Metastasis. Cancers (Basel). 2013;5(4):1619–42. doi: 10.3390/cancers5041619 24305653; PubMed Central PMCID: PMC3875957.

13. 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. doi: 10.1038/nature06385 18097410; PubMed Central PMCID: PMC3090667.

14. Mohamed H, Murray M, Turner JN, Caggana M. Isolation of tumor cells using size and deformation. J Chromatogr A. 2009;1216(47):8289–95. doi: 10.1016/j.chroma.2009.05.036 19497576.

15. Zhe X, Cher ML, Bonfil RD. Circulating tumor cells: finding the needle in the haystack. Am J Cancer Res. 2011;1(6):740–51. 22016824; PubMed Central PMCID: PMC3195935.

16. Zheng S, Lin HK, Lu B, Williams A, Datar R, Cote RJ, et al. 3D microfilter device for viable circulating tumor cell (CTC) enrichment from blood. Biomed Microdevices. 2011;13(1):203–13. doi: 10.1007/s10544-010-9485-3 20978853; PubMed Central PMCID: PMC3809998.

17. Harouaka R, Kang Z, Zheng SY, Cao L. Circulating tumor cells: advances in isolation and analysis, and challenges for clinical applications. Pharmacol Ther. 2014;141(2):209–21. doi: 10.1016/j.pharmthera.2013.10.004 24134902; PubMed Central PMCID: PMC3947247.

18. Adams AA, Okagbare PI, Feng J, Hupert ML, Patterson D, Gottert J, et al. Highly efficient circulating tumor cell isolation from whole blood and label-free enumeration using polymer-based microfluidics with an integrated conductivity sensor. J Am Chem Soc. 2008;130(27):8633–41. doi: 10.1021/ja8015022 18557614; PubMed Central PMCID: PMC2526315.

19. Wang S, Liu K, Liu J, Yu ZT, Xu X, Zhao L, et al. Highly efficient capture of circulating tumor cells by using nanostructured silicon substrates with integrated chaotic micromixers. Angew Chem Int Ed Engl. 2011;50(13):3084–8. doi: 10.1002/anie.201005853 21374764; PubMed Central PMCID: PMC3085082.

20. Sheng W, Ogunwobi OO, Chen T, Zhang J, George TJ, Liu C, et al. Capture, release and culture of circulating tumor cells from pancreatic cancer patients using an enhanced mixing chip. Lab Chip. 2014;14(1):89–98. doi: 10.1039/c3lc51017d 24220648; PubMed Central PMCID: PMC3918168.

21. Hayes DF, Cristofanilli M, Budd GT, Ellis MJ, Stopeck A, Miller MC, et al. Circulating tumor cells at each follow-up time point during therapy of metastatic breast cancer patients predict progression-free and overall survival. Clin Cancer Res. 2006;12(14 Pt 1):4218–24. doi: 10.1158/1078-0432.CCR-05-2821 16857794.

22. Talasaz AH, Powell AA, Huber DE, Berbee JG, Roh KH, Yu W, et al. 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. 2009;106(10):3970–5. doi: 10.1073/pnas.0813188106 19234122; PubMed Central PMCID: PMC2645911.

23. Kim MS, Sim TS, Kim YJ, Kim SS, Jeong H, Park JM, et al. SSA-MOA: a novel CTC isolation platform using selective size amplification (SSA) and a multi-obstacle architecture (MOA) filter. Lab Chip. 2012;12(16):2874–80. doi: 10.1039/c2lc40065k 22684249.

24. Kim MS, Kim J, Lee W, Cho SJ, Oh JM, Lee JY, et al. A trachea-inspired bifurcated microfilter capturing viable circulating tumor cells via altered biophysical properties as measured by atomic force microscopy. Small. 2013;9(18):3103–10. doi: 10.1002/smll.201202317 23401221.

25. Ahmed MG, Abate MF, Song Y, Zhu Z, Yan F, Xu Y, et al. Isolation, Detection, and Antigen-Based Profiling of Circulating Tumor Cells Using a Size-Dictated Immunocapture Chip. Angew Chem Int Ed Engl. 2017;56(36):10681–5. doi: 10.1002/anie.201702675 28675606.

26. Yang L, Lang JC, Balasubramanian P, Jatana KR, Schuller D, Agrawal A, et al. 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. 2009;102(2):521–34. Epub 2008/08/30. doi: 10.1002/bit.22066 18726961; PubMed Central PMCID: PMC3906726.

27. Lee HJ, Oh JH, Oh JM, Park JM, Lee JG, Kim MS, et al. Efficient isolation and accurate in situ analysis of circulating tumor cells using detachable beads and a high-pore-density filter. Angew Chem Int Ed Engl. 2013;52(32):8337–40. doi: 10.1002/anie.201302278 23825032.

28. Weitz J, Kienle P, Lacroix J, Willeke F, Benner A, Lehnert T, et al. Dissemination of tumor cells in patients undergoing surgery for colorectal cancer. Clin Cancer Res. 1998;4(2):343–8. 9516921.

29. Muller V, Stahmann N, Riethdorf S, Rau T, Zabel T, Goetz A, et al. Circulating tumor cells in breast cancer: correlation to bone marrow micrometastases, heterogeneous response to systemic therapy and low proliferative activity. Clin Cancer Res. 2005;11(10):3678–85. doi: 10.1158/1078-0432.CCR-04-2469 15897564.

30. Park JM, Kim MS, Moon HS, Yoo CE, Park D, Kim YJ, et al. Fully automated circulating tumor cell isolation platform with large-volume capacity based on lab-on-a-disc. Anal Chem. 2014;86(8):3735–42. doi: 10.1021/ac403456t 24641782.

31. Tian F, Cai L, Chang J, Li S, Liu C, Li T, et al. Label-free isolation of rare tumor cells from untreated whole blood by interfacial viscoelastic microfluidics. Lab Chip. 2018;18(22):3436–45. doi: 10.1039/c8lc00700d 30328446.

32. Vona G, Sabile A, Louha M, Sitruk V, Romana S, Schutze K, et al. Isolation by size of epithelial tumor cells: a new method for the immunomorphological and molecular characterization of circulatingtumor cells. Am J Pathol. 2000;156(1):57–63. doi: 10.1016/S0002-9440(10)64706-2 10623654; PubMed Central PMCID: PMC1868645.

33. Hofman VJ, Ilie MI, Bonnetaud C, Selva E, Long E, Molina T, et al. Cytopathologic detection of circulating tumor cells using the isolation by size of epithelial tumor cell method: promises and pitfalls. Am J Clin Pathol. 2011;135(1):146–56. doi: 10.1309/AJCP9X8OZBEIQVVI 21173137.

34. Sun J, Li M, Liu C, Zhang Y, Liu D, Liu W, et al. Double spiral microchannel for label-free tumor cell separation and enrichment. Lab Chip. 2012;12(20):3952–60. doi: 10.1039/c2lc40679a 22868446.

35. Hou HW, Warkiani ME, Khoo BL, Li ZR, Soo RA, Tan DS, et al. Isolation and retrieval of circulating tumor cells using centrifugal forces. Sci Rep. 2013;3:1259. doi: 10.1038/srep01259 23405273; PubMed Central PMCID: PMC3569917.

36. Riethdorf S, Fritsche H, Muller V, Rau T, Schindlbeck C, Rack B, et al. Detection of circulating tumor cells in peripheral blood of patients with metastatic breast cancer: a validation study of the CellSearch system. Clin Cancer Res. 2007;13(3):920–8. doi: 10.1158/1078-0432.CCR-06-1695 17289886.

37. Furukawa K, Abumiya T, Sakai K, Hirano M, Osanai T, Shichinohe H, et al. Measurement of human blood viscosity by an electromagnetic spinning sphere viscometer. J Med Eng Technol. 2016;40(6):285–92. doi: 10.1080/03091902.2016.1181216 27167739.

38. Ren J BGaSS. Experimental analysis of the surface roughness evolution of etched glass for micro/nanofluidic devices. J Micromech Microeng 2011;21:025012. doi: 10.1088/0960-1317/21/2/025012

39. Slomka N, Oomens CW, Gefen A. Evaluating the effective shear modulus of the cytoplasm in cultured myoblasts subjected to compression using an inverse finite element method. J Mech Behav Biomed Mater. 2011;4(7):1559–66. doi: 10.1016/j.jmbbm.2011.04.006 21783166.

40. Kim MS, Jo S, Park JT, Shin HY, Kim SS, Gurel O, et al. Method to purify and analyze heterogeneous senescent cell populations using a microfluidic filter with uniform fluidic profile. Anal Chem. 2015;87(19):9584–8. doi: 10.1021/acs.analchem.5b00445 26322520.

41. Turgeon ML. Clinical Hematology: Theory and Procedures.: Lippincott Williams & Wilkins, Forth edition; 2004.

42. Daniels VG WP, Burkitt HG Functional histology: A text and colour atlas: Edinburgh; 1979.

43. Shapiro HM, Schildkraut ER, Curbelo R, Laird CW, Turner B, Hirschfeld T. Combined blood cell counting and classification with fluorochrome stains and flow instrumentation. J Histochem Cytochem. 1976;24(1):396–401. doi: 10.1177/24.1.56391 56391.

44. Khoo BL, Grenci G, Jing T, Lim YB, Lee SC, Thiery JP, et al. Liquid biopsy and therapeutic response: Circulating tumor cell cultures for evaluation of anticancer treatment. Sci Adv. 2016;2(7):e1600274. Epub 2016/07/28. doi: 10.1126/sciadv.1600274 27453941; PubMed Central PMCID: PMC4956185.

45. Lee TY, Hyun KA, Kim SI, Jung HI. An integrated microfluidic chip for one-step isolation of circulating tumor cells. Sensor Actuat B-Chem. 2017;238:1144–50. doi: 10.1016/j.snb.2016.05.163 WOS:000388948600138.

46. Park GS, Kwon H, Kwak DW, Park SY, Kim M, Lee JH, et al. Full surface embedding of gold clusters on silicon nanowires for efficient capture and photothermal therapy of circulating tumor cells. Nano Lett. 2012;12(3):1638–42. Epub 2012/03/01. doi: 10.1021/nl2045759 22364234.

Microslit on a chip: A simplified filter to capture circulating tumor cells enlarged with microbeads

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