Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-30T07:47:50.618Z Has data issue: false hasContentIssue false
  • English
  • Français

Nanostructured substrates for multi-cue investigations of single cells

Published online by Cambridge University Press:  30 January 2018

Joseph A. Christodoulides ,
Marc Christophersen ,
Jinny L. Liu ,
James B. Delehanty ,
Deepa Raghu ,
Michael Robitaille ,
Jeff M. Byers  and
Marc P. Raphael
Joseph A. Christodoulides
Affiliation:
Naval Research Laboratory, 4555 Overlook Ave SW, Washington, DC 20375-5320, USA
Marc Christophersen
Affiliation:
Naval Research Laboratory, 4555 Overlook Ave SW, Washington, DC 20375-5320, USA
Jinny L. Liu
Affiliation:
Naval Research Laboratory, 4555 Overlook Ave SW, Washington, DC 20375-5320, USA
James B. Delehanty
Affiliation:
Naval Research Laboratory, 4555 Overlook Ave SW, Washington, DC 20375-5320, USA
Deepa Raghu
Affiliation:
Naval Research Laboratory, 4555 Overlook Ave SW, Washington, DC 20375-5320, USA Current Address: BioReliance, Sigma-Aldrich Corp., Rockville, MD 20850, USA
Michael Robitaille
Affiliation:
Naval Research Laboratory, 4555 Overlook Ave SW, Washington, DC 20375-5320, USA
Jeff M. Byers
Affiliation:
Naval Research Laboratory, 4555 Overlook Ave SW, Washington, DC 20375-5320, USA
Marc P. Raphael*
Affiliation:
Naval Research Laboratory, 4555 Overlook Ave SW, Washington, DC 20375-5320, USA
*
Address all correspondence to Marc P. Raphael at[email protected]
Get access

Abstract

Cellular adhesion depends on the integration of numerous signaling inputs generated by the chemical and physical properties of the substrate. The complex coupling among inputs makes it challenging experimentally to deconvolve their individual contributions to the adhesion process. To address this roadblock, we have employed a combination of electron beam and optical lithographic techniques to fabricate substrates with independently tunable topographical and chemical signaling cues. Arrays of gold nanostructures were patterned atop quartz substrates, half of which were etched into gold-capped nanopillars. Individual A549 cells exposed simultaneously to Arg-Gly-Asp-functionalized etched and non-etched arrays exhibited strongly preferential adherence to the nanopillars.

Type
Research Letters
Information
MRS Communications , Volume 8 , Issue 1 , March 2018 , pp. 49 - 58
Copyright
Copyright © Materials Research Society 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Knapp, D.M., Tower, T.T., Tranquillo, R.T., and Barocas, V.H.: Estimation of cell traction and migration in an isometric cell traction assay. AlChE J. 45, 2628 (1999).CrossRefGoogle Scholar
2. Stevens, M.M. and George, J.H.: Exploring and engineering the cell surface interface. Science 310, 1135 (2005).Google Scholar
3. Johnson, B.N., Lancaster, K.Z., Zhen, G.H., He, J.Y., Gupta, M.K., Kong, Y.L., Engel, E.A., Krick, K.D., Ju, A., Meng, F.B., Enquist, L.W., Jia, X.F., and McAlpine, M.C.: 3D Printed anatomical nerve regeneration pathways. Adv. Funct. Mater. 25, 6205 (2015).CrossRefGoogle ScholarPubMed
4. Melchiorri, A.J., Hibino, N., Best, C.A., Yi, T., Lee, Y.U., Kraynak, C.A., Kimerer, L.K., Krieger, A., Kim, P., Breuer, C.K., and Fisher, J.P.: 3D-Printed biodegradable polymeric vascular grafts. Adv. Healthcare Mater. 5, 319 (2016).Google Scholar
5. Griffin, D.R., Weaver, W.M., Scumpia, P.O., Di Carlo, D., and Segura, T.: Accelerated wound healing by injectable microporous gel scaffolds assembled from annealed building blocks. Nat. Mater. 14, 737 (2015).CrossRefGoogle ScholarPubMed
6. Riahi, R., Yang, Y.L., Zhang, D.D., and Wong, P.K.: Advances in wound-healing assays for probing collective cell migration. JALA 17, 59 (2012).Google ScholarPubMed
7. Samavedi, S., Whittington, A.R., and Goldstein, A.S.: Calcium phosphate ceramics in bone tissue engineering: A review of properties and their influence on cell behavior. Acta Biomater.. 9, 8037 (2013).CrossRefGoogle ScholarPubMed
8. Ren, X.Y., Tu, V., Bischoff, D., Weisgerber, D.W., Lewis, M.S., Yamaguchi, D.T., Miller, T.A., Harley, B.A.C., and Lee, J.C.: Nanoparticulate mineralized collagen scaffolds induce in vivo bone regeneration independent of progenitor cell loading or exogenous growth factor stimulation. Biomaterials 89, 67 (2016).CrossRefGoogle ScholarPubMed
9. Chen, C.S., Mrksich, M., Huang, S., Whitesides, G.M., and Ingber, D.E.: Geometric control of cell life and death. Science 276, 1425 (1997).Google Scholar
10. Jahed, Z., Zareian, R., Chau, Y.Y., Seo, B.B., West, M., Tsui, T.Y., Wen, W.J., and Mofrad, M.R.K.: Differential collective- and single-cell behaviors on silicon micropillar arrays. ACS Appl. Mater. Interfaces 8, 23604 (2016).Google Scholar
11. Park, J., Kim, D.H., Kim, H.N., Wang, C.J., Kwak, M.K., Hur, E., Suh, K.Y., An, S.S., and Levchenko, A.: Directed migration of cancer cells guided by the graded texture of the underlying matrix. Nat. Mater. 15, 792 (2016).CrossRefGoogle ScholarPubMed
12. Tzvetkova-Chevolleau, T., Stephanou, A., Fuard, D., Ohayon, J., Schiavone, P., and Tracqui, P.: The motility of normal and cancer cells in response to the combined influence of the substrate rigidity and anisotropic microstructure. Biomaterials 29, 1541 (2008).Google Scholar
13. Wirtz, D., Konstantopoulos, K., and Searson, P.C.: The physics of cancer: the role of physical interactions and mechanical forces in metastasis. Nat. Rev. Cancer 11, 512 (2011).CrossRefGoogle ScholarPubMed
14. Jiang, X.Y., Bruzewicz, D.A., Wong, A.P., Piel, M., and Whitesides, G.M.: Directing cell migration with asymmetric micropatterns. Proc. Natl. Acad. Sci. U.S.A. 102, 975 (2005).Google Scholar
15. Gupton, S.L. and Waterman-Storer, C.M.: Spatiotemporal feedback between actomyosin and focal-adhesion systems optimizes rapid cell migration. Cell 125, 1361 (2006).CrossRefGoogle ScholarPubMed
16. Muinonen-Martin, A.J., Susanto, O., Zhang, Q.F., Smethurst, E., Faller, W.J., Veltman, D.M., Kalna, G., Lindsay, C., Bennett, D.C., Sansom, O.J., Herd, R., Jones, R., Machesky, L.M., Wakelam, M.J.O., Knecht, D.A., and Insall, R.H.: Melanoma cells break down LPA to establish local gradients that drive chemotactic dispersal. PLoS Biol.. 12, 1 (2014).Google Scholar
17. Lo, C.M., Wang, H.B., Dembo, M., and Wang, Y.L.: Cell movement is guided by the rigidity of the substrate. Biophys. J. 79, 144 (2000).CrossRefGoogle ScholarPubMed
18. Hadjipanayi, E., Mudera, V., and Brown, R.A.: Guiding cell migration in 3D: a collagen matrix with graded directional stiffness. Cell Motil. Cytoskeleton 66, 121 (2009).CrossRefGoogle ScholarPubMed
19. Isenberg, B.C., DiMilla, P.A., Walker, M., Kim, S., and Wong, J.Y.: Vascular smooth muscle cell durotaxis depends on substrate stiffness gradient strength. Biophys. J. 97, 1313 (2009).Google Scholar
20. Xue, C.Y., Wong, D.Y., and Kasko, A.M.: Complex dynamic substrate control: dual-tone hydrogel photoresists allow double-dissociation of topography and modulus. Adv. Mater. 26, 1577 (2014).Google Scholar
21. Jiang, B., Suen, R., Wang, J.J., Zhang, Z.J., Wertheim, J.A., and Ameer, G.A.: Mechanocompatible polymer-extracellular-matrix composites for vascular tissue engineering. Adv. Healthcare Mater. 5, 1594 (2016).Google Scholar
22. Ricoult, S.G., Thompson-Steckel, G., Correia, J.P., Kennedy, T.E., and Juncker, D.: Tuning cell-surface affinity to direct cell specific responses to patterned proteins. Biomaterials 35, 727 (2014).CrossRefGoogle ScholarPubMed
23. Smith, J.T., Elkin, J.T., and Reichert, W.M.: Directed cell migration on fibronectin gradients: Effect of gradient slope. Exp. Cell Res. 312, 2424 (2006).Google Scholar
24. Humphries, J.D., Byron, A., and Humphries, M.J.: Integrin ligands at a glance. J. Cell Sci. 119, 3901 (2006).Google Scholar
25. DeLong, S.A., Gobin, A.S., and West, J.L.: Covalent immobilization of RGDS on hydrogel surfaces to direct cell alignment and migration. J. Controlled Release 109, 139 (2005).CrossRefGoogle ScholarPubMed
26. Huang, J.H., Grater, S.V., Corbellinl, F., Rinck, S., Bock, E., Kemkemer, R., Kessler, H., Ding, J.D., and Spatz, J.P.: Impact of order and disorder in RGD nanopatterns on cell adhesion. Nano Lett.. 9, 1111 (2009).Google Scholar
27. Cavalcanti-Adam, E.A., Volberg, T., Micoulet, A., Kessler, H., Geiger, B., and Spatz, J.P.: Cell spreading and focal adhesion dynamics are regulated by spacing of integrin ligands. Biophys. J. 92, 2964 (2007).Google Scholar
28. Palecek, S.P., Loftus, J.C., Ginsberg, M.H., Lauffenburger, D.A., and Horwitz, A.F.: Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 385, 537 (1997).CrossRefGoogle ScholarPubMed
29. Nikkhah, M., Edalat, F., Manoucheri, S., and Khademhosseini, A.: Engineering microscale topographies to control the cell-substrate interface. Biomaterials 33, 5230 (2012).CrossRefGoogle ScholarPubMed
30. Anselme, K. and Bigerelle, M.: Role of materials surface topography on mammalian cell response. Int. Mater. Rev. 56, 243 (2011).CrossRefGoogle Scholar
31. Giljean, S., Najjar, D., Bigerelle, B.M., and Iost, A.: Multiscale analysis of abrasion damage on stainless steel. Surf. Eng. 24, 8 (2008).Google Scholar
32. Galli, C., Coen, M.C., Hauert, R., Katanaev, V.L., Groning, P., and Schlapbach, L.: Creation of nanostructures to study the topographical dependency of protein adsorption. Colloids Surf.,B 26, 255 (2002).CrossRefGoogle Scholar
33. Lord, M.S., Foss, M., and Besenbacher, F.: Influence of nanoscale surface topography on protein adsorption and cellular response. Nano Today 5, 66 (2010).Google Scholar
34. Charras, G. and Sahai, E.: Physical influences of the extracellular environment on cell migration. Nat. Rev. Mol. Cell Biol. 15, 813 (2014).Google Scholar
35. Kim, D.H., Han, K., Gupta, K., Kwon, K.W., Suh, K.Y., and Levchenko, A.: Mechanosensitivity of fibroblast cell shape and movement to anisotropic substratum topography gradients. Biomaterials 30, 5433 (2009).Google Scholar
36. Fraser, S.A., Ting, Y.H., Mallon, K.S., Wendt, A.E., Murphy, C.J., and Nealey, P.F.: Sub-micron and nanoscale feature depth modulates alignment of stromal fibroblasts and corneal epithelial cells in serum-rich and serum-free media. J. Biomed. Mat. Res., Part A 86A, 725 (2008).CrossRefGoogle Scholar
37. Mahmud, G., Campbell, C.J., Bishop, K.J.M., Komarova, Y.A., Chaga, O., Soh, S., Huda, S., Kandere-Grzybowska, K., and Grzybowski, B.A.: Directing cell motions on micropatterned ratchets. Nat. Phys. 5, 606 (2009).CrossRefGoogle Scholar
38. Teixeira, A.I., Abrams, G.A., Bertics, P.J., Murphy, C.J., and Nealey, P.F.: Epithelial contact guidance on well-defined micro- and nanostructured substrates. J. Cell Sci. 116, 1881 (2003).Google Scholar
39. Teixeira, A.I., McKie, G.A., Foley, J.D., Berticsc, P.J., Nealey, P.F., and Murphy, C.J.: The effect of environmental factors on the response of human corneal epithelial cells to nanoscale substrate topography. Biomaterials 27, 3945 (2006).CrossRefGoogle ScholarPubMed
40. Gentile, F., Tirinato, L., Battista, E., Causa, F., Liberale, C., di Fabrizio, E.M., and Decuzzi, P.: Cells preferentially grow on rough substrates. Biomaterials 31, 7205 (2010).Google Scholar
41. Raghu, D., Christodoulides, J.A., Delehanty, J.B., Byers, J.M., and Raphael, M.P.: A label-free technique for the spatio-temporal imaging of single cell secretions. J. Visualized Exp. 105, 1 (2015).Google Scholar
42. Raphael, M.P., Christodoulides, J.A., Delehanty, J.B., Long, J.P., and Byers, J.M.: Quantitative imaging of protein secretions from single cells in real time. Biophys. J. 105, 602 (2013).Google Scholar
Supplementary material: File

Christodoulides et al. supplementary material

Christodoulides et al. supplementary material 1

Download Christodoulides et al. supplementary material(File)
File 18.4 MB