journal article·2013-09Open access

Bio-inspired soft polystyrene nanotube substrate for rapid and highly efficient breast cancer-cell capture

Xueli Liu, Li Chen, Hongliang Liu, Gao Yang, Pengchao Zhang, Dong Han, Shutao Wang, Lei Jiang

NPG Asia Materials· Volume 5· Issue 9

Abstract

The softness of materials is very important in cellular processes, such as cell adhesion, spread, proliferation and differentiation. Using soft materials benefits many biological studies and applications, such as wound healing, tissue engineering and clinical surgery. However, in other areas, such as rare cancer-cell capture and isolation, the importance of the softness of materials has not yet been studied. Extracellular matrix suitable for cell contact and survival is formed from soft materials with specific molecules and nanostructures. Herein, we report a soft polystyrene nanotube substrate inspired by the cell microenvironment that achieves rapid and highly efficient breast cancer-cell capture from whole-blood samples with high cell viability by integrating the soft nature of polystyrene polymer with specific capture agents and surface structures. This study provides a potentially optimal candidate for a high-quality breast cancer-cell detection platform and will provide new prospects for designing cell-material interfaces for advanced cell-based biological studies and clinical applications in the future. Soft Material Helps Cancer-Cell Capture: Soft polystyrene (PS) polymer nanotube substrate has been developed to realize rapid and highly efficient breast cancer-cell capture from whole-blood samples with high cell viability, by integrating the soft nature of PS with specific capture agents and surface structures to mimic the cell microenvironment. It is anticipated that this soft material-based substrate will provide a potentially optimal candidate for high-quality breast cancer-cell capture and detection technologies, and open a new view to design cell-material interfaces for advanced cell-based diagnostic and therapeutic platforms. Materials that efficiently isolate cells from whole-blood samples have important diagnostic and therapeutic applications. Shutao Wang at the Institute of Chemistry, Chinese Academy of Sciences, China, and co-workers have now devised soft substrates based on the polymer polystyrene that efficiently capture breast cancer cells. The researchers previously developed a three-dimensional cell-capture nanostructure comprising a silicon nanowire array coated with an antibody—anti-EpCAM—that detects the epithelial cell adhesion molecule overexpressed by many cancers. Now, inspired by the fact that cells and their environments are composed of soft materials—something that has led to soft polymers being exploited in other biological applications, including tissue engineering—Wang and co-workers have replaced the stiff nanowires of their cell-capturing substrate with soft polystyrene nanotubes. The resulting polystyrene/anti-EpCAM arrays are significantly more efficient than their silicon counterparts, rapidly detecting breast cancer cells. These findings point to softness as an important factor in cell capture and detection.
Source: openalex_inverted_index · Quality: baseline

Research context

OpenAlex topics: 3D Printing in Biomedical Research · Microfluidic and Bio-sensing Technologies · Nanofabrication and Lithography Techniques

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (40)

Show source-provided references
1. Schwarz, U. Soft matters in cell adhesion: rigidity sensing on soft elastic substrates. Soft Matter 3, 263–266 (2007).10.1039/B606409D ↗
2. Discher, D. E., Janmey, P. & Wang, Y. L. Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139–1143 (2005).10.1126/science.1116995 ↗
3. Vogel, V. & Sheetz, M. Local force and geometry sensing regulate cell functions. Nat. Rev. Mol. Cell Bio. 7, 265–275 (2006).10.1038/nrm1890 ↗
4. Ross, A. M., Jiang, Z., Bastmeyer, M. & Lahann, J. Physical aspects of cell culture substrates: topography, roughness, and elasticity. Small 8, 336–355 (2012).10.1002/smll.201100934 ↗
5. Pelham, R. J. & Wang, Y. L. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl Acad. Sci. USA 94, 13661–13665 (1997).10.1073/pnas.94.25.13661 ↗
6. Engler, A. J., Sen, S., Sweeney, H. L. & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677–689 (2006).10.1016/j.cell.2006.06.044 ↗
7. Trappmann, B., Gautrot, J. E., Connelly, J. T., Strange, D. G. T., Li, Y., Oyen, M. L., Stuart, M. A. C., Boehm, H., Li, B. J., Vogel, V., Spatz, J. P., Watt, F. M. & Huck, W. T. S. Extracellular-matrix tethering regulates stem-cell fate. Nat. Mater. 11, 642–649 (2012).10.1038/nmat3339 ↗
8. Discher, D. E., Mooney, D. J. & Zandstra, P. W. Growth factors, matrices, and forces combine and control stem cells. Science 324, 1673–1677 (2009).10.1126/science.1171643 ↗
9. Paszek, M. J., Zahir, N., Johnson, K. R., Lakins, J. N., Rozenberg, G. I., Gefen, A., Reinhart-King, C. A., Margulies, S. S., Dembo, M., Boettiger, D., Hammer, D. A. & Weaver, V. M. Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241–254 (2005).10.1016/j.ccr.2005.08.010 ↗
10. Levental, I., Georges, P. C. & Janmey, P. A. Soft biological materials and their impact on cell function. Soft Matter 3, 299–306 (2007).10.1039/B610522J ↗
11. Flanagan, L. A., Ju, Y. E., Marg, B., Osterfield, M. & Janmey, P. A. Neurite branching on deformable substrates. Neuroreport 13, 2411–2415 (2002).10.1097/00001756-200212200-00007 ↗
12. Engler, A. J., Griffin, M. A., Sen, S., Bonnetnann, C. G., Sweeney, H. L. & Discher, D. E. Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J. Cell Biol. 166, 877–887 (2004).10.1083/jcb.200405004 ↗
13. Tirrell, M., Kokkoli, E. & Biesalski, M. The role of surface science in bioengineered materials. Surf. Sci. 500, 61–83 (2002).10.1016/S0039-6028(01)01548-5 ↗
14. Lee, K. Y. & Mooney, D. J. Hydrogels for tissue engineering. Chem. Rev. 101, 1869–1879 (2001).10.1021/cr000108x ↗
15. Shalek, A. K., Robinson, J. T., Karp, E. S., Lee, J. S., Ahn, D.-R., Yoon, M.-H., Sutton, A., Jorgolli, M., Gertner, R. S., Gujral, T. S., MacBeath, G., Yang, E. G. & Park, H. Vertical silicon nanowires as a universal platform for delivering biomolecules into living cells. Proc. Natl Acad. Sci. USA 107, 1870–1875 (2010).10.1073/pnas.0909350107 ↗
16. Fischer, K. E., Aleman, B. J., Tao, S. L., Daniels, R. H., Li, E. M., Bunger, M. D., Nagaraj, G., Singh, P., Zettl, A. & Desai, T. A. Biomimetic nanowire coatings for next generation adhesive drug delivery systems. Nano Lett. 9, 716–720 (2009).10.1021/nl803219f ↗
17. Chen, L., Liu, X. L., Su, B., Li, J., Jiang, L., Han, D. & Wang, S. T. Aptamer-mediated efficient capture and release of T lymphocytes on nanostructured surfaces. Adv. Mater. 23, 4376–4380 (2011).10.1002/adma.201102435 ↗
18. Kim, S. T., Kim, D. J., Kim, T. J., Seo, D. W., Kim, T. H., Lee, S. Y., Kim, K., Lee, K. M. & Lee, S. K. Novel streptavidin-functionalized silicon nanowire arrays for CD4 (+) T lymphocyte separation. Nano Lett. 10, 2877–2883 (2010).10.1021/nl100942p ↗
19. Hughes, A. D. & King, M. R. Nanobiotechnology for the capture and manipulation of circulating tumor cells. WIREs Nanomed. Nanobi. 4, 291–309 (2012).10.1002/wnan.168 ↗
20. Pantel, K., Brakenhoff, R. H. & Brandt, B. Detection, clinical relevance and specific biological properties of disseminating tumour cells. Nat. Rev. Cancer 8, 329–340 (2008).10.1038/nrc2375 ↗
21. Nagrath, S., Sequist, L. V., Maheswaran, S., Bell, D. W., Irimia, D., Ulkus, L., Smith, M. R., Kwak, E. L., Digumarthy, S., Muzikansky, A., Ryan, P., Balis, U. J., Tompkins, R. G., Haber, D. A. & Toner, M. Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature 450, 1235–U1210 (2007).10.1038/nature06385 ↗
22. Wang, S. T., Wang, H., Jiao, J., Chen, K. J., Owens, G. E., Kamei, K. I., Sun, J., Sherman, D. J., Behrenbruch, C. P., Wu, H. & Tseng, H. R. Three-dimensional nanostructured substrates toward efficient capture of circulating tumor cells. Angew. Chem. Int. Ed. 48, 8970–8973 (2009).10.1002/anie.200901668 ↗
23. Wang, S. T., Liu, K., Liu, J. A., Yu, Z. T. F., Xu, X. W., Zhao, L. B., Lee, T., Lee, E. K., Reiss, J., Lee, Y. K., Chung, L. W. K., Huang, J. T., Rettig, M., Seligson, D., Duraiswamy, K. N., Shen, C. K. F. & Tseng, H. R. Highly efficient capture of circulating tumor cells by using nanostructured silicon substrates with integrated chaotic micromixers. Angew. Chem. Int. Ed. 50, 3084–3088 (2011).10.1002/anie.201005853 ↗
24. Park, G.-S., Kwon, H., Kwak, D. W., Park, S. Y., Kim, M., Lee, J.-H., Han, H., Heo, S., Li, X. S., Lee, J. H., Kim, Y. H., Lee, J.-G., Yang, W., Cho, H. Y., Kim, S. K. & Kim, K. Full surface embedding of gold clusters on silicon nanowires for efficient capture and photothermal therapy of circulating tumor cells. Nano Lett. 12, 1638–1642 (2012).10.1021/nl2045759 ↗
25. Lee, S. K., Kim, G. S., Wu, Y., Kim, D. J., Lu, Y., Kwak, M., Han, L., Hyung, J. H., Seol, J. K., Sander, C., Gonzalez, A., Li, J. & Fan, R. Nanowire substrate-based laser scanning cytometry for quantitation of circulating tumor cells. Nano Lett. 12, 2697–2704 (2012).10.1021/nl2041707 ↗
26. Zhang, N. A., Deng, Y. L., Tai, Q. D., Cheng, B. R., Zhao, L. B., Shen, Q. L., He, R. X., Hong, L. Y., Liu, W., Guo, S. S., Liu, K., Tseng, H. R., Xiong, B. & Zhao, X. Z. Electrospun TiO2 nanofiber-based cell capture assay for detecting Circulating tumor cells from colorectal and gastric cancer patients. Adv. Mater. 24, 2756–2760 (2012).10.1002/adma.201200155 ↗
27. Sekine, J., Luo, S.-C., Wang, S. T., Zhu, B., Tseng, H.-R. & Yu, H.-h. Functionalized conducting polymer nanodots for enhanced cell capturing: the synergistic effect of capture agents and nanostructures. Adv. Mater. 23, 4788–4792 (2011).10.1002/adma.201102151 ↗
28. Sun, T. L., Qing, G. Y., Su, B. L. & Jiang, L. Functional biointerface materials inspired from nature. Chem. Soc. Rev. 40, 2909–2921 (2011).10.1039/c0cs00124d ↗
29. Sun, T. L., Feng, L., Gao, X. F. & Jiang, L. Bioinspired surfaces with special wettability. Acc. Chem. Res. 38, 644–652 (2005).10.1021/ar040224c ↗
30. Liu, X. L., Zhou, J., Xue, Z. X., Gao, J., Meng, J. X., Wang, S. T. & Jiang, L. Clam’s shell inspired high-energy inorganic coatings with underwater low adhesive superoleophobicity. Adv. Mater. 24, 3401–3405 (2012).10.1002/adma.201200797 ↗
31. Liu, X. L., Gao, J., Xue, Z. X., Chen, L., Lin, L., Jiang, L. & Wang, S. T. Bioinspired oil strider floating at the oil/water interface supported by huge superoleophobic force. ACS Nano 6, 5614–5620 (2012).10.1021/nn301550v ↗
32. Jin, M. H., Feng, X. J., Feng, L., Sun, T. L., Zhai, J., Li, T. J. & Jiang, L. Superhydrophobic aligned polystyrene nanotube films with high adhesive force. Adv. Mater. 17, 1977–1981 (2005).10.1002/adma.200401726 ↗
33. Went, P. T., Lugli, A., Meier, S., Bundi, M., Mirlacher, M., Sauter, G. & Dirnhofer, S. Frequent EpCam protein expression in human carcinomas. Hum. Pathol. 35, 122–128 (2004).10.1016/j.humpath.2003.08.026 ↗
34. Liu, H. L., Liu, X. L., Meng, J. X., Zhang, P. C., Yang, G., Su, B., Sun, K., Chen, L., Han, D., Wang, S. T. & Jiang, L. Hydrophobic interaction-mediated capture and release of cancer cells on thermoresponsive nanostructured surfaces. Adv. Mater. 25, 922–927 (2013).10.1002/adma.201203826 ↗
35. Huang, T. T., Sturgis, J., Gomez, R., Geng, T., Bashir, R., Bhunia, A. K., Robinson, J. P. & Ladisch, M. R. Composite surface for blocking bacterial adsorption on protein biochips. Biotechnol. Bioeng. 81, 618–624 (2003).10.1002/bit.10507 ↗
36. Yang, D. Y., Niu, X., Liu, Y. Y., Wang, Y., Gu, X., Song, L. S., Zhao, R., Ma, L. Y., Shao, Y. M. & Jiang, X. Y. Electrospun nanofibrous membranes: a novel solid substrate for microfluidic immunoassays for HIV. Adv. Mater. 20, 4770–4775 (2008).10.1002/adma.200801302 ↗
37. Sorelli, L., Constantinides, G., Ulm, F. J. & Toutlemonde, F. The nano-mechanical signature of ultra high performance concrete by statistical nanoindentation techniques. Cement Concrete. Res. 38, 1447–1456 (2008).10.1016/j.cemconres.2008.09.002 ↗
38. Yim, E. K. F., Darling, E. M., Kulangara, K., Guilak, F. & Leong, K. W. Nanotopography-induced changes in focal adhesions, cytoskeletal organization, and mechanical properties of human mesenchymal stem cells. Biomaterials 31, 1299–1306 (2010).10.1016/j.biomaterials.2009.10.037 ↗
39. Chen, W. Q., Weng, S. N., Zhang, F., Allen, S., Li, X., Bao, L. W., Lam, R. H. W., Macoska, J. A., Merajver, S. D. & Fu, J. P. Nanoroughened surfaces for efficient capture of circulating tumor cells without using capture antibodies. ACS Nano 7, 566–575 (2013).10.1021/nn304719q ↗
40. Rao, C. G., Chianese, D., Doyle, G. V., Miller, M. C., Russell, T., Sanders, R. A. & Terstappen, L. W. M. M. Expression of epithelial cell adhesion molecule in carcinoma cells present in blood and primary and metastatic tumors. Int. J. Oncol. 27, 49–57 (2005).