Advertisement

Circulating Tumor Cell Enrichment Technologies

  • Mert Boya
  • Chia-Heng Chu
  • Ruxiu Liu
  • Tevhide Ozkaya-Ahmadov
  • Ali Fatih SariogluEmail author
Chapter
Part of the Recent Results in Cancer Research book series (RECENTCANCER, volume 215)

Abstract

Circulating tumor cells (CTCs) are responsible for the metastatic spread of cancer and therefore are extremely valuable not only for basic research on cancer metastasis but also as potential biomarkers in diagnosing and managing cancer in the clinic. While relatively non-invasive access to the blood tissue presents an opportunity, CTCs are mixed with approximately billion-times more-populated blood cells in circulation. Therefore, the accuracy of technologies for reliable enrichment of the rare CTC population from blood samples is critical to the success of downstream analyses. The focus of this chapter is to provide the reader an overview of significant advances made in the development of diverse CTC enrichment technologies by presenting the strengths of individual techniques in addition to specific challenges remaining to be addressed.

Keywords

Circulating tumor cells CTCs Cell enrichment techniques Cell separation techniques Microfluidics Metastasis 

References

  1. Aceto N, Bardia A, Miyamoto DT et al (2014) Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell 158(5):1110–1122PubMedPubMedCentralCrossRefGoogle Scholar
  2. Adams AA, Okagbare PI, Feng J et al (2008) 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 130(27):8633–8841PubMedPubMedCentralCrossRefGoogle Scholar
  3. Adams DL, Zhu P, Makarova OV et al (2014) The systematic study of circulating tumor cell isolation using lithographic microfilters. RSC Adv 4(9):4334–4342CrossRefGoogle Scholar
  4. Alix-Panabières C, Pantel K (2013) Circulating tumor cells: liquid biopsy of cancer. Clin Chem 59(1):110–118PubMedCrossRefGoogle Scholar
  5. Alix-Panabières C, Pantel K (2014) Challenges in circulating tumour cell research. Nat Rev Cancer 14(9):623–631PubMedCrossRefGoogle Scholar
  6. Allan AL, Keeney M (2009) Circulating tumor cell analysis: technical and statistical considerations for application to the clinic. J Oncol 2010:426218PubMedPubMedCentralGoogle Scholar
  7. Al-Mehdi AB, Tozawa K, Fisher AB et al (2000) Intravascular origin of metastasis from the proliferation of endothelium-attached tumor cells: a new model for metastasis. Nat Med 6(1):100–102PubMedCrossRefGoogle Scholar
  8. Antfolk M, Antfolk C, Lilja H et al (2015) A single inlet two-stage acoustophoresis chip enabling tumor cell enrichment from white blood cells. Lab Chip 15(9):2102–2109PubMedCrossRefGoogle Scholar
  9. Au SH, Edd J, Stoddard AE et al (2017) Microfluidic isolation of circulating tumor cell clusters by size and asymmetry. Sci Rep 7:2433PubMedPubMedCentralCrossRefGoogle Scholar
  10. Au SH, Storey BD, Moore JC et al (2016) Clusters of circulating tumor cells traverse capillary-sized vessels. Proc Natl Acad Sci U S A 113(18):4947–4952PubMedPubMedCentralCrossRefGoogle Scholar
  11. Augustsson P, Magnusson C, Nordin M et al (2012) Microfluidic, label-free enrichment of prostate cancer cells in blood based on acoustophoresis. Anal Chem 84(18):7954–7962PubMedPubMedCentralCrossRefGoogle Scholar
  12. Besant JD, Mohamadi RM, Aldridge PM et al (2015) Velocity valleys enable efficient capture and spatial sorting of nanoparticle-bound cancer cells. Nanoscale 7(14):6278–6285PubMedCrossRefGoogle Scholar
  13. Bruno JG (2015) Predicting the uncertain future of aptamer-based diagnostics and therapeutics. Molecules 20(4):6866–6887PubMedPubMedCentralCrossRefGoogle Scholar
  14. Budd GT, Cristofanilli M, Ellis MJ et al (2006) Circulating tumor cells versus imaging-predicting overall survival in metastatic breast cancer. Clin Cancer Res 12(21):6403–6409PubMedCrossRefGoogle Scholar
  15. Bunka DH, Stockley PG (2006) Aptamers come of age-at last. Nat Rev Microbiol 4(8):588–596PubMedCrossRefGoogle Scholar
  16. Chandran K, Yoganathan A, Rittgers S (2007) Biofluid mechanics: the human circulation. CRC Press, Boca RatonGoogle Scholar
  17. Chen GD, Fachin F, Fernandez-Suarez M et al (2011) Nanoporous elements in microfluidics for multiscale manipulation of bioparticles. Small 7(8):1061–1067PubMedPubMedCentralCrossRefGoogle Scholar
  18. Cheng IF, Chang HC, Hou D et al (2007) An integrated dielectrophoretic chip for continuous bioparticle filtering, focusing, sorting, trapping, and detecting. Biomicrofluidics 1(2):021503PubMedCentralCrossRefPubMedGoogle Scholar
  19. Cheng IF, Huang WL, Chen TY et al (2015) Antibody-free isolation of rare cancer cells from blood based on 3D lateral dielectrophoresis. Lab Chip 15(14):2950–2959PubMedCrossRefGoogle Scholar
  20. Cheng SB, Xie M, Xu JQ et al (2016) High-efficiency capture of individual and cluster of circulating tumor cells by a microchip embedded with three-dimensional poly (dimethylsiloxane) scaffold. Anal Chem 88(13):6773–6780PubMedCrossRefPubMedCentralGoogle Scholar
  21. Cherdron W, Durst F, Whitelaw JH (1978) Asymmetric flows and instabilities in symmetric ducts with sudden expansions. J Fluid Mech 84(1):13–31CrossRefGoogle Scholar
  22. Chinen LT, de Carvalho FM, Rocha BM et al (2013) Cytokeratin-based CTC counting unrelated to clinical follow up. J Thorac Dis 5(5):593PubMedPubMedCentralGoogle Scholar
  23. Choi H, Kim KB, Jeon CS et al (2013) A label-free DC impedance-based microcytometer for circulating rare cancer cell counting. Lab Chip 13(5):970–977PubMedCrossRefPubMedCentralGoogle Scholar
  24. Coumans FAW, van Dalum G, Beck M et al (2013) Filtration parameters influencing circulating tumor cell enrichment from whole blood. PLoS ONE 8(4):e61774PubMedPubMedCentralCrossRefGoogle Scholar
  25. Cristofanilli M, Budd GT, Ellis MJ et al (2004) Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med 351:781–791PubMedCrossRefPubMedCentralGoogle Scholar
  26. Davies J, Dawkes AC, Haymes AG et al (1994) A scanning tunneling microscopy comparison of passive antibody adsorption and biotinylated antibody linkage to streptavidin on microtiter wells. J Immunolog Meth 167(1–2):263–269CrossRefGoogle Scholar
  27. Davis JA, Inglis DW, Morton KJ et al (2006) Deterministic hydrodynamics: taking blood apart. Proc Natl Acad Sci U S A 103(40):14779–14784PubMedPubMedCentralCrossRefGoogle Scholar
  28. De Bono JS, Scher HI, Montgomery RB et al (2008) Circulating tumor cells predict survival benefit from treatment in metastatic castration-resistant prostate cancer. Clin Cancer Res 14(19):6302–6309PubMedCrossRefPubMedCentralGoogle Scholar
  29. Desitter I, Guerrouahen BS, Benali-Furet N et al (2011) A new device for rapid isolation by size and characterization of rare circulating tumor cells. Anticancer Res 31(2):427–441PubMedPubMedCentralGoogle Scholar
  30. Dharmasiri U, Balamurugan S, Adams AA et al (2009) Highly efficient capture and enumeration of low abundance prostate cancer cells using prostate‐specific membrane antigen aptamers immobilized to a polymeric microfluidic device. Electrophoresis 30(18):3289–3300PubMedPubMedCentralCrossRefGoogle Scholar
  31. Di Carlo D (2009) Inertial microfluidics. Lab Chip 9(21):3038–3046PubMedCrossRefGoogle Scholar
  32. Di Carlo D, Irimia D, Tompkins RG et al (2007) Continuous inertial focusing, ordering, and separation of particles in microchannels. Proc Natl Acad Sci U S A 104(48):18892–18897PubMedPubMedCentralCrossRefGoogle Scholar
  33. Dickey DD, Giangrande PH (2016) Oligonucleotide aptamers: a next-generation technology for the capture and detection of circulating tumor cells. Methods 97:94–103PubMedCrossRefPubMedCentralGoogle Scholar
  34. Ding X, Peng Z, Lin SC et al (2014) Cell separation using tilted-angle standing surface acoustic waves. Proc Natl Acad Sci U S A 111(36):12992–12997PubMedPubMedCentralCrossRefGoogle Scholar
  35. Fan X, Jia C, Yang J et al (2015) A microfluidic chip integrated with a high-density PDMS-based microfiltration membrane for rapid isolation and detection of circulating tumor cells. Biosens Bioelectron 71:380–386PubMedCrossRefPubMedCentralGoogle Scholar
  36. Fan ZH, Vitha MF (2016) Circulating tumor cells: isolation and analysis. Wiley, HobokenCrossRefGoogle Scholar
  37. Farokhzad OC, Jon S, Khademhosseini A et al (2004) Nanoparticle-aptamer bioconjugates. Cancer Res 64(21):7668–7672PubMedCrossRefPubMedCentralGoogle Scholar
  38. Fawcett DW, Vallee BL, Soule MH (1950) A method for concentration and segregation of malignant cells from bloody, pleural and peritoneal fluids. Science 3:34–36CrossRefGoogle Scholar
  39. Ferreira MM, Ramani VC, Jeffrey SS (2016) Circulating tumor cell technologies. Mol Oncol 10(3):374–394PubMedPubMedCentralCrossRefGoogle Scholar
  40. Fidler IJ (2003) The pathogenesis of cancer metastasis: the ‘seed and soil’ hypothesis revisited. Nat Rev Cancer 3(6):453–459CrossRefGoogle Scholar
  41. Freidin MB, Tay A, Freydina DV et al (2014) An assessment of diagnostic performance of a filter-based antibody-independent peripheral blood circulating tumour cell capture paired with cytomorphologic criteria for the diagnosis of cancer. Lung Cancer 85(2):182–185PubMedCrossRefGoogle Scholar
  42. Fujii T (2002) PDMS-based microfluidic devices for biomedical applications. Microelectron Eng 61:907–914CrossRefGoogle Scholar
  43. Giordano A, Gao H, Anfossi S et al (2012) Epithelial-mesenchymal transition and stem cell markers in patients with HER2-positive metastatic breast cancer. Mol Cancer Ther 11(11):2526–2534PubMedPubMedCentralCrossRefGoogle Scholar
  44. Goto W, Kashiwagi S, Asano Y et al (2017) Circulating tumor cell clusters-associated gene plakoglobin is a significant prognostic predictor in patients with breast cancer. Biomark Res 5(1):19PubMedPubMedCentralCrossRefGoogle Scholar
  45. Gupta V, Jafferji I, Garza M et al (2012) ApoStream™, a new dielectrophoretic device for antibody independent isolation and recovery of viable cancer cells from blood. Biomicrofluidics 6(2):024133PubMedCentralCrossRefPubMedGoogle Scholar
  46. Harb W, Fan A, Tran T et al (2013) Mutational analysis of circulating tumor cells using a novel microfluidic collection device and qPCR assay. Transl Oncol 6(5):528IN1-538PubMedPubMedCentralCrossRefGoogle Scholar
  47. Hayes DF, Cristofanilli M, Budd GT et al (2006) 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 12(14):4218–4224PubMedCrossRefGoogle Scholar
  48. Holm SH, Beech JP, Barrett MP et al (2011) Separation of parasites from human blood using deterministic lateral displacement. Lab Chip 11(7):1326–1332PubMedCrossRefGoogle Scholar
  49. Hong Y, Fang F, Zhang Q (2016) Circulating tumor cell clusters: what we know and what we expect. Int J Oncol 49(6):2206–2216PubMedPubMedCentralCrossRefGoogle Scholar
  50. Hoshino K, Huang YY, Lane N et al (2011) Microchip-based immunomagnetic detection of circulating tumor cells. Lab Chip 11(20):3449–3457PubMedPubMedCentralCrossRefGoogle Scholar
  51. Hosic S, Murthy SK, Koppes AN (2015) Microfluidic sample preparation for single cell analysis. Anal Chem 88(1):354–380PubMedPubMedCentralCrossRefGoogle Scholar
  52. Hou HW, Warkiani ME, Khoo BL et al (2013a) Isolation and retrieval of circulating tumor cells using centrifugal forces. Sci Rep 3:1259PubMedPubMedCentralCrossRefGoogle Scholar
  53. Hou S, Zhao L, Shen Q et al (2013b) Polymer nanofiber-embedded microchips for detection, isolation, and molecular analysis of single circulating melanoma cells. Angew Chem Int Ed 52(12):3379–3383CrossRefGoogle Scholar
  54. Huang LR, Cox EC, Austin RH et al (2004) Continuous particle separation through deterministic lateral displacement. Science 304(5673):987–990CrossRefGoogle Scholar
  55. Hughes AD, King MR (2010) Use of naturally occurring halloysite nanotubes for enhanced capture of flowing cells. Langmuir 26(14):12155–12164PubMedCrossRefGoogle Scholar
  56. Hur SC, Mach AJ, Di Carlo D (2011) High-throughput size-based rare cell enrichment using microscale vortices. Biomicrofluidics 5(2):022206PubMedCentralCrossRefPubMedGoogle Scholar
  57. Hur SC, Tse HT, Di Carlo D (2010) Sheathless inertial cell ordering for extreme throughput flow cytometry. Lab Chip 10(3):274–280PubMedCrossRefGoogle Scholar
  58. Hyun KA, Lee TY, Jung HI (2013) Negative enrichment of circulating tumor cells using a geometrically activated surface interaction chip. Anal Chem 85(9):4439–4445PubMedCrossRefGoogle Scholar
  59. Inglis DW, Davis JA, Austin RH et al (2006) Critical particle size for fractionation by deterministic lateral displacement. Lab Chip 6(5):655–658PubMedCrossRefGoogle Scholar
  60. Jackson JM, Witek MA, Kamande JW et al (2017) Materials and microfluidics: enabling the efficient isolation and analysis of circulating tumour cells. Chem Soc Rev 46(14):4245–4280PubMedPubMedCentralCrossRefGoogle Scholar
  61. Jahr S, Hentze H, Englisch S et al (2001) DNA fragments in the blood plasma of cancer patients: quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Res 61(4):1659–1665PubMedGoogle Scholar
  62. Ji HM, Samper V, Chen Y et al (2008) Silicon-based microfilters for whole blood cell separation. Biomed Microdevices 10(2):251–257PubMedCrossRefGoogle Scholar
  63. Karabacak NM, Spuhler PS, Fachin F et al (2014) Microfluidic, marker-free isolation of circulating tumor cells from blood samples. Nat Protoc 9(3):694PubMedPubMedCentralCrossRefGoogle Scholar
  64. Karnis A, Goldsmith HL, Mason SG (1966) The flow of suspensions through tubes: V. Inertial effects. Can J Chem Eng 44(4):181–193CrossRefGoogle Scholar
  65. Katkov II, Mazur P (1999) Factors affecting yield and survival of cells when suspensions are subjected to centrifugation. Cell Biochem Biophys 31(3):231–245PubMedCrossRefGoogle Scholar
  66. Kim YJ, Koo GB, Lee JY et al (2014) A microchip filter device incorporating slit arrays and 3-D flow for detection of circulating tumor cells using CAV1-EpCAM conjugated microbeads. Biomaterials 35(26):7501–7510PubMedCrossRefGoogle Scholar
  67. Krishnamurthy S, Bischoff F, Ann Mayer J et al (2013) Discordance in HER2 gene amplification in circulating and disseminated tumor cells in patients with operable breast cancer. Cancer Med 2(2):226–233PubMedPubMedCentralCrossRefGoogle Scholar
  68. Kuczenski RS, Chang HC, Revzin A (2011) Dielectrophoretic microfluidic device for the continuous sorting of Escherichia coli from blood cells. Biomicrofluidics 5(3):032005PubMedCentralCrossRefPubMedGoogle Scholar
  69. Labib M, Green B, Mohamadi RM et al (2016) Aptamer and antisense-mediated two-dimensional isolation of specific cancer cell subpopulations. J Am Chem Soc 138(8):2476–2479PubMedCrossRefGoogle Scholar
  70. Lara O, Tong X, Zborowski M et al (2004) Enrichment of rare cancer cells through depletion of normal cells using density and flow-through, immunomagnetic cell separation. Exp Hematol 32(10):891–904PubMedCrossRefGoogle Scholar
  71. Lara O, Tong X, Zborowski M et al (2006) Comparison of two immunomagnetic separation technologies to deplete T cells from human blood samples. Biotechnol Bioeng 94(1):66–80PubMedCrossRefGoogle Scholar
  72. Lee HJ, Cho HY, Oh JH et al (2013a) Simultaneous capture and in situ analysis of circulating tumor cells using multiple hybrid nanoparticles. Biosens Bioelectron 47:508–514PubMedCrossRefGoogle Scholar
  73. Lee MG, Choi S, Park JK (2010) Rapid multivortex mixing in an alternately formed contraction-expansion array microchannel. Biomed Microdevices 12(6):1019–1026PubMedCrossRefGoogle Scholar
  74. Lee MG, Shin JH, Bae CY et al (2013b) Label-free cancer cell separation from human whole blood using inertial microfluidics at low shear stress. Anal Chem 85(13):6213–6218PubMedCrossRefGoogle Scholar
  75. Li H, Meng QH, Noh H et al (2017) Detection of circulating tumor cells from cryopreserved human sarcoma peripheral blood mononuclear cells. Cancer Lett 403:216–223PubMedPubMedCentralCrossRefGoogle Scholar
  76. Li P, Mao Z, Peng Z et al (2015) Acoustic separation of circulating tumor cells. Proc Natl Acad Sci U S A 112(16):4970–4975PubMedPubMedCentralCrossRefGoogle Scholar
  77. Lin H, Balic M, Zheng S et al (2011) Disseminated and circulating tumor cells: role in effective cancer management. Crit Rev Oncol Hematol 77(1):1–11PubMedCrossRefGoogle Scholar
  78. Lin HK, Zheng S, Williams AJ et al (2010) Portable filter-based microdevice for detection and characterization of circulating tumor cells. Clin Cancer Res 16(20):5011–5018PubMedPubMedCentralCrossRefGoogle Scholar
  79. Liu G, Mao X, Phillips JA et al (2009) Aptamer−nanoparticle strip biosensor for sensitive detection of cancer cells. Anal Chem 81(24):10013–10018PubMedPubMedCentralCrossRefGoogle Scholar
  80. Loutherback K, Chou KS, Newman J et al (2010) Improved performance of deterministic lateral displacement arrays with triangular posts. Microfluid Nanofluid 9(6):1143–1149CrossRefGoogle Scholar
  81. Loutherback K, D’Silva J, Liu L et al (2012) Deterministic separation of cancer cells from blood at 10 mL/min. AIP Adv 2(4):042107PubMedCentralCrossRefPubMedGoogle Scholar
  82. Lu B, Zheng S, Quach BQ et al (2010a) A study of the autofluorescence of parylene materials for μTAS applications. Lab Chip 10(14):1826–1834PubMedCrossRefGoogle Scholar
  83. Lu J, Fan T, Zhao Q et al (2010b) Isolation of circulating epithelial and tumor progenitor cells with an invasive phenotype from breast cancer patients. Int J Cancer 126(3):669–683PubMedPubMedCentralCrossRefGoogle Scholar
  84. Lu YT, Zhao L, Shen Q et al (2013) NanoVelcro Chip for CTC enumeration in prostate cancer patients. Nat Methods 64(2):144–152Google Scholar
  85. Lu Y, Liang H, Yu T et al (2015) Isolation and characterization of living circulating tumor cells in patients by immunomagnetic negative enrichment coupled with flow cytometry. Cancer 121(17):3036–3045PubMedCrossRefGoogle Scholar
  86. Lucci A, Hall CS, Lodhi AK et al (2012) Circulating tumour cells in non-metastatic breast cancer: a prospective study. Lancet Oncol 13(7):688–695PubMedCrossRefGoogle Scholar
  87. Lustberg M, Jatana KR, Zborowski M et al (2012) Emerging technologies for CTC detection based on depletion of normal cells. In: Ignatiadis M, Sotiriou C, Pantel K (eds) Minimal residual disease and circulating tumor cells in breast cancer. Springer, Heidelberg, pp 97–110CrossRefGoogle Scholar
  88. Ma H, Liu J, Ali MM et al (2015) Nucleic acid aptamers in cancer research, diagnosis and therapy. Chem Soc Rev 44(5):1240–1256PubMedCrossRefGoogle Scholar
  89. McDonald JC, Whitesides GM (2002) Poly(dimethylsiloxane) as a material for fabricating microfluidic devices. Acc Chem Res 35(7):491–499PubMedCrossRefGoogle Scholar
  90. Meng S, Tripathy D, Frenkel EP et al (2004) Circulating tumor cells in patients with breast cancer dormancy. Clin Cancer Res 10(24):8152–8162PubMedCrossRefPubMedCentralGoogle Scholar
  91. Miltenyi S, Müller W, Weichel W et al (1990) High gradient magnetic cell separation with MACS. Cytometry Part A 11(2):231–238CrossRefGoogle Scholar
  92. Mittal S, Wong IY, Deen WM et al (2012) Antibody-functionalized fluid-permeable surfaces for rolling cell capture at high flow rates. Biophys J 102(4):721–730PubMedPubMedCentralCrossRefGoogle Scholar
  93. Moffatt HK (1964) Viscous and resistive eddies near a sharp corner. J Fluid Mech 18(1):1–8CrossRefGoogle Scholar
  94. Myung JH, Hong S (2015) Microfluidic devices to enrich and isolate circulating tumor cells. Lab Chip 15(24):4500–4511PubMedPubMedCentralCrossRefGoogle Scholar
  95. Nagrath S, Sequist LV, Maheswaran S et al (2007) Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature 450(7173):1235–1239PubMedPubMedCentralCrossRefGoogle Scholar
  96. Neurauter AA, Bonyhadi M, Lien E et al (2007) Cell isolation and expansion using Dynabeads®. In: Scheper T, Belkin S, Bley T et al (eds) Advances in biochemical engineering/biotechnology. Springer, Heidelberg, pp 41–73Google Scholar
  97. Ozkumur E, Shah AM, Ciciliano JC et al (2013) Inertial focusing for tumor antigen–dependent and–independent sorting of rare circulating tumor cells. Sci Transl Med 5(179):179ra47PubMedPubMedCentralCrossRefGoogle Scholar
  98. Pantel K, Alix-Panabières C (2010) Circulating tumour cells in cancer patients: challenges and perspectives. Trends Mol Med 16(9):398–406PubMedCrossRefGoogle Scholar
  99. Pantel K, Brakenhoff RH, Brandt B (2008) Detection, clinical relevance and specific biological properties of disseminating tumour cells. Nat Rev Cancer 8(5):329–340PubMedCrossRefGoogle Scholar
  100. Park JM, Lee JY, Lee JG et al (2012) Highly efficient assay of circulating tumor cells by selective sedimentation with a density gradient medium and microfiltration from whole blood. Anal Chem 84(17):7400–7407PubMedCrossRefPubMedCentralGoogle Scholar
  101. Phillips JA, Xu Y, Xia Z et al (2008) Enrichment of cancer cells using aptamers immobilized on a microfluidic channel. Anal Chem 81(3):1033–1039CrossRefGoogle Scholar
  102. Poudineh M, Aldridge PM, Ahmed S et al (2017a) Tracking the dynamics of circulating tumour cell phenotypes using nanoparticle-mediated magnetic ranking. Nat Nanotechnol 12(3):274–281PubMedCrossRefPubMedCentralGoogle Scholar
  103. Poudineh M, Labib M, Ahmed S et al (2017b) Profiling functional and biochemical phenotypes of circulating tumor cells using a two-dimensional sorting device. Angew Chem Int Ed 56(1):163–168CrossRefGoogle Scholar
  104. Powell AA, Talasaz AH, Zhang H et al (2012) Single cell profiling of circulating tumor cells: transcriptional heterogeneity and diversity from breast cancer cell lines. PLoS ONE 7(5):e33788PubMedPubMedCentralCrossRefGoogle Scholar
  105. Qian W, Zhang Y, Chen W (2015) Capturing cancer: emerging microfluidic technologies for the capture and characterization of circulating tumor cells. Small 11(32):3850–3872PubMedCrossRefPubMedCentralGoogle Scholar
  106. Riethdorf S, Fritsche H, Müller V et al (2007) 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 13(3):920–928PubMedCrossRefPubMedCentralGoogle Scholar
  107. Saliba AE, Saias L, Psychari E et al (2010) Microfluidic sorting and multimodal typing of cancer cells in self-assembled magnetic arrays. Proc Natl Acad Sci U S A 107(33):14524–14529PubMedPubMedCentralCrossRefGoogle Scholar
  108. Sarioglu AF, Aceto N, Kojic N et al (2015) A microfluidic device for label-free, physical capture of circulating tumor cell clusters. Nat Methods 12(7):685–691PubMedPubMedCentralCrossRefGoogle Scholar
  109. Sawyers CL (2008) The cancer biomarker problem. Nature 452(7187):548–552PubMedCrossRefPubMedCentralGoogle Scholar
  110. Seal SH (1959) Silicone flotation: a simple quantitative method for the isolation of free-floating cancer cells from the blood. Cancer 12(3):590–595PubMedCrossRefGoogle Scholar
  111. Seal SH (1964) A sieve for the isolation of cancer cells and other large cells from the blood. Cancer 17(5):637–642PubMedCrossRefGoogle Scholar
  112. Segré G (1961) Radial particle displacements in Poiseuille flow of suspensions. Nature 189:209–210CrossRefGoogle Scholar
  113. Segré G, Silberberg A (1962) Behaviour of macroscopic rigid spheres in Poiseuille flow Part 2. Experimental results and interpretation. J Fluid Mech 14(1):136–157CrossRefGoogle Scholar
  114. Shaffer DR, Leversha MA, Danila DC et al (2007) Circulating tumor cell analysis in patients with progressive castration-resistant prostate cancer. Clin Cancer Res 13(7):2023–2029PubMedCrossRefGoogle Scholar
  115. Shen Q, Xu L, Zhao L et al (2013) Specific capture and release of circulating tumor cells using aptamer-modified nanosubstrates. Adv Mater 25(16):2368–2373PubMedPubMedCentralCrossRefGoogle Scholar
  116. Sheng W, Chen T, Kamath R et al (2012) Aptamer-enabled efficient isolation of cancer cells from whole blood using a microfluidic device. Anal Chem 84(9):4199–4206PubMedPubMedCentralCrossRefGoogle Scholar
  117. Sheng W, Chen T, Tan W et al (2013) Multivalent DNA nanospheres for enhanced capture of cancer cells in microfluidic devices. ACS Nano 7(8):7067–7076PubMedPubMedCentralCrossRefGoogle Scholar
  118. Smirnov DA, Zweitzig DR, Foulk BW et al (2005) Global gene expression profiling of circulating tumor cells. Cancer Res 65(12):4993–4997PubMedCrossRefGoogle Scholar
  119. Sollier E, Go DE, Che J et al (2014) Size-selective collection of circulating tumor cells using Vortex technology. Lab Chip 14(1):63–77PubMedCrossRefGoogle Scholar
  120. Song KM, Lee S, Ban C (2012) Aptamers and their biological applications. Sensors 12(1):612–631PubMedGoogle Scholar
  121. Song Y, Tian T, Shi Y et al (2017) Enrichment and single-cell analysis of circulating tumor cells. Chem Sci 8(3):1736–1751PubMedCrossRefGoogle Scholar
  122. Stone HA, Kim S (2001) Microfluidics: basic issues, applications, and challenges. AIChE J 47(6):1250–1254CrossRefGoogle Scholar
  123. Stott SL, Hsu CH, Tsukrov DI et al (2010) Isolation of circulating tumor cells using a microvortex-generating herringbone-chip. Proc Natl Acad Sci U S A 107(43):18392–18397PubMedPubMedCentralCrossRefGoogle Scholar
  124. Stroock AD, Dertinger SKW, Ajdari A et al (2002) Chaotic mixer for microchannels. Science 295(5555):647–651CrossRefGoogle Scholar
  125. Sun H, Zhu X, Lu PY et al (2014) Oligonucleotide aptamers: new tools for targeted cancer therapy. Mol Ther Nucleic Acids 3:e182PubMedPubMedCentralCrossRefGoogle Scholar
  126. Tachibana M (1973) On the behaviour of a sphere in the laminar tube flows. Rheol Acta 12(1):58–69CrossRefGoogle Scholar
  127. Talasaz AH, Powell AA, Huber DE et al (2009) 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(10):3970–3975PubMedPubMedCentralCrossRefGoogle Scholar
  128. Tan SJ, Yobas L, Lee GY et al (2009) Microdevice for the isolation and enumeration of cancer cells from blood. Biomed Microdevices 11(4):883–892PubMedCrossRefGoogle Scholar
  129. Tuerk C, Gold L (1990) Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249(4968):505–510PubMedCrossRefGoogle Scholar
  130. van de Stolpe A, Pantel K, Sleijfer S et al (2011) Circulating tumor cell isolation and diagnostics: toward routine clinical use. Cancer Res 71(18):5955–5960PubMedCrossRefGoogle Scholar
  131. Viraka Nellore BP, Kanchanapally R, Pramanik A et al (2015) Aptamer-conjugated graphene oxide membranes for highly efficient capture and accurate identification of multiple types of circulating tumor cells. Bioconjug Chem 26(2):235–242PubMedPubMedCentralCrossRefGoogle Scholar
  132. Vona G, Sabile A, Louha M et al (2000) Isolation by size of epithelial tumor cells: a new method for the immunomorphological and molecular characterization of circulating tumor cells. Am J Pathol 156(1):57–63PubMedPubMedCentralCrossRefGoogle Scholar
  133. Wan Y, Liu Y, Allen PB et al (2012) Capture, isolation and release of cancer cells with aptamer-functionalized glass bead array. Lab Chip 12(22):4693–4701PubMedPubMedCentralCrossRefGoogle Scholar
  134. Wang L, Zheng Q, Zhang QA et al (2012) Detection of single tumor cell resistance with aptamer biochip. Oncol Lett 4(5):935–940PubMedPubMedCentralCrossRefGoogle Scholar
  135. Wang S, Liu K, Liu J et al (2011) Highly efficient capture of circulating tumor cells by using nanostructured silicon substrates with integrated chaotic micromixers. Angew Chem Int Ed 50(13):3084–3088CrossRefGoogle Scholar
  136. Wang S, Wang H, Jiao J et al (2009) Three-dimensional nanostructured substrates toward efficient capture of circulating tumor cells. Angew Chem Int Ed 48(47):8970–8973CrossRefGoogle Scholar
  137. Warkiani ME, Khoo BL, Wu L et al (2016) Ultra-fast, label-free isolation of circulating tumor cells from blood using spiral microfluidics. Nat Protoc 11(1):134–148PubMedCrossRefGoogle Scholar
  138. Watanabe S (1954) The metastasizability of tumor cells. Cancer 7(2):215–223PubMedCrossRefGoogle Scholar
  139. Went PT, Lugli A, Meier S et al (2004) Frequent EpCam protein expression in human carcinomas. Hum Pathol 35(1):122–128PubMedCrossRefGoogle Scholar
  140. Wunsch BH, Smith JT, Gifford SM et al (2016) Nanoscale lateral displacement arrays for the separation of exosomes and colloids down to 20 nm. Nat Nanotechnol 11:936–940PubMedCrossRefGoogle Scholar
  141. Xu Y, Phillips JA, Yan J et al (2009) Aptamer-based microfluidic device for enrichment, sorting, and detection of multiple cancer cells. Anal Chem 81(17):7436–7442PubMedPubMedCentralCrossRefGoogle Scholar
  142. Yang L, Lang JC, Balasubramanian P et al (2009) 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(2):521–534PubMedPubMedCentralCrossRefGoogle Scholar
  143. Yoo CE, Moon HS, Kim YJ et al (2016) Highly dense, optically inactive silica microbeads for the isolation and identification of circulating tumor cells. Biomaterials 75:271–278PubMedCrossRefGoogle Scholar
  144. Yoon Y, Kim S, Lee J et al (2016) Clogging-free microfluidics for continuous size-based separation of microparticles. Sci Rep 6:26531PubMedPubMedCentralCrossRefGoogle Scholar
  145. Yu M, Bardia A, Aceto N et al (2014) Ex vivo culture of circulating breast tumor cells for individualized testing of drug susceptibility. Science 345(6193):216–220PubMedPubMedCentralCrossRefGoogle Scholar
  146. Yu M, Stott S, Toner M et al (2011) Circulating tumor cells: approaches to isolation and characterization. J Cell Biol 192(3):373–382PubMedPubMedCentralCrossRefGoogle Scholar
  147. Zamay GS, Kolovskaya OS, Zamay TN et al (2015) Aptamers selected to postoperative lung adenocarcinoma detect circulating tumor cells in human blood. Mol Ther 23(9):1486–1496PubMedPubMedCentralCrossRefGoogle Scholar
  148. Zhao L, Tang C, Xu L et al (2016) Enhanced and differential capture of circulating tumor cells from lung cancer patients by microfluidic assays using aptamer cocktail. Small 12(8):1072–1081PubMedPubMedCentralCrossRefGoogle Scholar
  149. Zhao W, Ali MM, Brook MA et al (2008) Rolling circle amplification: applications in nanotechnology and biodetection with functional nucleic acids. Angew Chem Int Ed 47(34):6330–6337CrossRefGoogle Scholar
  150. Zhao W, Cui CH, Bose S et al (2012) Bioinspired multivalent DNA network for capture and release of cells. Proc Natl Acad Sci U S A 109(48):19626–19631PubMedPubMedCentralCrossRefGoogle Scholar
  151. Zhao Y, Xu D, Tan W (2017) Aptamer-functionalized nano/micro-materials for clinical diagnosis: isolation, release and bioanalysis of circulating tumor cells. Integr Biol 9(3):188–205CrossRefGoogle Scholar
  152. Zheng S, Lin H, Liu JQ et al (2007) Membrane microfilter device for selective capture, electrolysis and genomic analysis of human circulating tumor cells. J Chromatogr A 1162(2):154–161PubMedCrossRefGoogle Scholar
  153. Zhou J, Rossi JJ (2014) Cell-type-specific, aptamer-functionalized agents for targeted disease therapy. Mol Ther Nucleic Acids 3(6):e169PubMedPubMedCentralCrossRefGoogle Scholar
  154. Zhou MD, Hao S, Williams AJ et al (2014) Separable bilayer microfiltration device for viable label-free enrichment of circulating tumour cells. Sci Rep 4:7392PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Mert Boya
    • 1
  • Chia-Heng Chu
    • 1
  • Ruxiu Liu
    • 1
  • Tevhide Ozkaya-Ahmadov
    • 1
  • Ali Fatih Sarioglu
    • 1
    Email author
  1. 1.Georgia Institute of TechnologyAtlantaUSA

Personalised recommendations