Immunocapture of prostate cancer cells by use of anti-PSMA antibodies in microdevices

Springer Science and Business Media LLC - Tập 14 - Trang 401-407 - 2011
Steven M. Santana1, He Liu2, Neil H. Bander2, Jason P. Gleghorn3, Brian J. Kirby1
1Sibley School of Mechanical and Aerospace Engineering, Cornell University, Ithaca, USA
2Laboratory of Urological Oncology, Weill Medical College of Cornell University, New York, USA
3School of Engineering and Applied Science, Department of Chemical and Biological Engineering, Princeton University, Princeton, USA

Tóm tắt

Patients suffering from cancer can shed tumor cells into the bloodstream, leading to one of the most important mechanisms of metastasis. As such, the capture of these cells is of great interest. Circulating tumor cells are typically extracted from circulation through positive selection with the epithelial cell-adhesion molecule (EpCAM), leading to currently unknown biases when cells are undergoing epithelial-to-mesenchymal transition. For prostate cancer, prostate-specific membrane antigen (PSMA) presents a compelling target for immunocapture, as PSMA levels increase in higher-grade cancers and metastatic disease and are specific to the prostate epithelium. This study uses monoclonal antibodies J591 and J415—antibodies that are highly specific for intact extracellular domains of PSMA on live cells—in microfluidic devices for the capture of LNCaPs, a PSMA-expressing immortalized prostate cancer cell line, over a range of concentrations and shear stresses relevant to immunocapture. Our results show that J591 outperforms J415 and a mix of the two for prostate cancer capture, and that capture performance saturates following incubation with antibody concentrations of 10 micrograms per milliliter.

Tài liệu tham khảo

W.J. Allard, J. Matera 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. 10(20), 6897–6904 (2004) H.J.K. Ananias, M.C. van den Heuvel et al., Expression of the gastrin-releasing peptide receptor, the prostate stem cell antigen and the prostate-specific membrane antigen in lymph node and bone metastases of prostate cancer. Prostate 69(10), 1101–1108 (2009) N.H. Bander, D.M. Nanus et al., Targeted systemic therapy of prostate cancer with a monoclonal antibody to prostate-specific membrane antigen. Semin. Oncol. 30(5), 667–676 (2003) S.S. Chang, D.S. O’Keefe et al., Prostate-specific membrane antigen is produced in tumor-associated neovasculature. Clin. Cancer Res. 5(10), 2674–2681 (1999a) S.S. Chang, V.E. Reuter et al., Five different anti-Prostate-specific Membrane Antigen (PSMA) antibodies confirm PSMA expression in tumor-associated neovasculature. Cancer Res. 59(13), 3192–3198 (1999b) S.J. Cohen, C.J.A. Punt et al., Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer. J. Clin. Oncol. 26(19), 3213–3221 (2008) F.A.W. Coumans, C.J.M. Doggen et al., All circulating EpCAM+CK+CD45- objects predict overall survival in castration-resistant prostate cancer. Ann. Oncol. 21(9), 1851–1857 (2010) D.C. Danila, G. Heller et al., Circulating tumor cell number and prognosis in progressive castration-resistant prostate cancer. Clin. Cancer Res. 13(23), 7053–7058 (2007) D.C. Danila, M. Fleisher et al., Circulating tumor cells as biomarkers in prostate cancer. Clin. Cancer Res. 17(12), 3903–3912 (2011) M.I. Davis, M.J. Bennett et al., Crystal structure of prostate-specific membrane antigen, a tumor marker and peptidase. Proc. Natl. Acad. Sci. U. S. A. 102(17), 5981–5986 (2005) J.S. de Bono, H.I. Scher et al., Circulating tumor cells predict survival benefit from treatment in metastatic castration-resistant prostate cancer. Clin. Cancer Res. 14(19), 6302–6309 (2008) J.P. Gleghorn, E.D. Pratt et al., Capture of circulating tumor cells from whole blood of prostate cancer patients using geometrically enhanced differential immunocapture (GEDI) and a prostate-specific antibody. Lab Chip 10(1), 27–29 (2010) J. Gostner, D. Fong et al., Effects of EpCAM overexpression on human breast cancer cell lines. BMC Cancer 11(1), 45 (2011) A. Gradilone, C. Raimondi, et al. Circulating tumor cells lacking cytokeratin in breast cancer: the importance of being mesenchymal. J. Cell. Mol. Med. (2011): no-no. M.C. Haffner, I.E. Kronberger et al., Prostate-specific membrane antigen expression in the neovasculature of gastric and colorectal cancers. Hum. Pathol. 40(12), 1754–1761 (2009) J.S. Horoszewicz, E. Kawinski et al., Monoclonal antibodies to a new antigenic marker in epithelial prostatic cells and serum of prostatic cancer patients. Anticancer Res. 7(5B), 927–935 (1987) R.S. Israeli, W.H. Miller et al., Sensitive tumor cells: comparison of prostate-specific membrane antigen and prostate-specific antigen-based assays. Cancer Res. 54(24), 6306–6310 (1994a) R.S. Israeli, C.T. Powell et al., Expression of the prostate-specific membrane antigen. Cancer Res. 54(7), 1807–1811 (1994b) B.J. Kirby, A.R. Wheeler et al., Programmable modification of cell adhesion and zeta potential in silica microchips. Lab Chip 3(1), 5–10 (2003) R.T. Krivacic, A. Ladanyi et al., A rare-cell detector for cancer. Proc. Natl. Acad. Sci. U. S. A. 101(29), 10501–10504 (2004) T. Kusumi, T. Koie et al., Immunohistochemical detection of carcinoma in radical prostatectomy specimens following hormone therapy. Pathol. Int. 58(11), 687–694 (2008) H. Liu, P. Moy et al., Monoclonal antibodies to the extracellular domain of prostate-specific membrane antigen also react with tumor vascular endothelium. Cancer Res. 57(17), 3629–3634 (1997) S. Maheswaran, D.A. Haber, Circulating tumor cells: a window into cancer biology and metastasis. Curr. Opin. Genet. Dev. 20(1), 96–99 (2010) S. Mannweiler, P. Amersdorfer et al., Heterogeneity of Prostate-Specific Membrane Antigen (PSMA) expression in prostate carcinoma with distant metastasis. Pathol. Oncol. Res. 15(2), 167–172 (2009) M. Mego, U. De Giorgi et al., Circulating tumor cells in metastatic inflammatory breast cancer. Ann. Oncol. 20(11), 1824–1828 (2009) J.R. Mesters, C. Barinka et al., Structure of glutamate carboxypeptidase II, a drug target in neuronal damage and prostate cancer. EMBO J. 25(6), 1375–1384 (2006) S. Minner, C. Wittmer et al., High level PSMA expression is associated with early PSA recurrence in surgically treated prostate cancer. Prostate 71(3), 281–288 (2011) J.G. Moreno, M.C. Miller et al., Circulating tumor cells predict survival in patients with metastatic prostate cancer. Urology 65(4), 713–718 (2005) M. Munz, P.A. Baeuerle et al., The emerging role of EpCAM in cancer and stem cell signaling. Cancer Res. 69(14), 5627–5629 (2009) G.P. Murphy, A.-A.A. Elgamal et al., Current evaluation of the tissue localization and diagnostic utility of prostate specific membrane antigen. Cancer 83(11), 2259–2269 (1998) S.K. Murthy, A. Sin et al., Effect of flow and surface conditions on human lymphocyte isolation using microfluidic chambers. Langmuir 20(26), 11649 (2004) S. Nagrath, L.V. Sequist et al., Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature 450(7173), 1235–1239 (2007) D. Olmos, H.T. Arkenau et al., Circulating tumour cell (CTC) counts as intermediate end points in castration-resistant prostate cancer (CRPC): a single-centre experience. Ann. Oncol. 20(1), 27–33 (2009) K. Pantel, C. Alix-Panabières, Circulating tumour cells in cancer patients: challenges and perspectives. Trends Mol. Med. 16(9), 398–406 (2010) S. Perner, M.D. Hofer et al., Prostate-specific membrane antigen expression as a predictor of prostate cancer progression. Hum. Pathol. 38(5), 696–701 (2007) E.D. Pratt, C. Huang et al., Rare cell capture in microfluidic devices. Chem. Eng. Sci. 66(7), 1508–1522 (2011) A.K. Rajasekaran, G. Anilkumar et al., Is prostate-specific membrane antigen a multifunctional protein? Am. J. Physiol. Cell Physiol. 288(5), C975–C981 (2005) S. Riethdorf, K. Pantel, Advancing personalized cancer therapy by detection and characterization of circulating carcinoma cells Circulating tumor cells in cancer patients Riethdorf & Pantel. Ann. N. Y. Acad. Sci. 1210(1), 66–77 (2010) J.S. Ross, C.E. Sheehan et al., Correlation of primary tumor prostate-specific membrane antigen expression with disease recurrence in prostate cancer. Clin. Cancer Res. 9(17), 6357–6362 (2003) H.I. Scher, X. Jia et al., Circulating tumour cells as prognostic markers in progressive, castration-resistant prostate cancer: a reanalysis of IMMC38 trial data. Lancet Oncol. 10(3), 233–239 (2009) D.R. Shaffer, M.A. Leversha et al., Circulating tumor cell analysis in patients with progressive castration-resistant prostate cancer. Clin. Cancer Res. 13(7), 2023–2029 (2007) S. Shiah, K. Tai et al., Epigenetic regulation of EpCAM in tumor invasion and metastasis. J. Canc. Mol. 3, 165–168 (2008) D.A. Silver, I. Pellicer et al., Prostate-specific membrane antigen expression in normal and malignant human tissues. Clin. Cancer Res. 3(1), 81–85 (1997) A. Sin, S.K. Murthy et al., Enrichment using antibody-coated microfluidic chambers in shear flow: model mixtures of human lymphocytes. Biotechnol. Bioeng. 91(7), 816–826 (2005) P.M. Smith-Jones, S. Vallabahajosula et al., In vitro characterization of radiolabeled monoclonal antibodies specific for the extracellular domain of prostate-specific membrane antigen. Cancer Res. 60(18), 5237–5243 (2000) R.L. Sokoloff, K.C. Norton et al., A dual-monoclonal sandwich assay for prostate-specific membrane antigen: levels in tissues, seminal fluid and urine. Prostate 43(2), 150–157 (2000) S.L. Stott, C.-H. Hsu et al., Isolation of circulating tumor cells using a microvortex-generating herringbone-chip. Proc. Natl. Acad. Sci. 107(43), 18392–18397 (2010a) S.L. Stott, R.J. Lee et al., Isolation and characterization of circulating tumor cells from patients with localized and metastatic prostate cancer. Sci. Transl. Med. 2(25), 25ra23 (2010b) S.D. Sweat, A. Pacelli et al., Prostate-specific membrane antigen expression is greatest in prostate adenocarcinoma and lymph node metastases. Urology 52(4), 637–640 (1998) J.K. Trover, M.L. Beckett et al., Detection and characterization of the prostate-specific membrane antigen (PSMA) in tissue extracts and body fluids. Int. J. Cancer 62(5), 552–558 (1995) S. Usami, H.H. Chen et al., Design and construction of a linear shear stress flow chamber. Ann. Biomed. Eng. 21(1), 77–83 (1993) G.L. Wright, C. Haley et al., Expression of prostate-specific membrane antigen in normal, benign, and malignant prostate tissues. Urol. Oncol. 1(1), 18–28 (1995) J.G.L. Wright, B. Mayer Grob et al., Upregulation of prostate-specific membrane antigen after androgen-deprivation therapy. Urology 48(2), 326–334 (1996)