Advertisement

Proliferation of human aortic endothelial cells on Nitinol thin films with varying hole sizes

  • Ming Lun Wu
  • Mohanchandra K. Panduranga
  • Gregory P. Carman
Article
  • 124 Downloads

Abstract

In this paper, we present the effect of micron size holes on proliferation and growth of human aortic endothelial cells (HAECs). Square shaped micron size holes (5, 10, 15, 20 and 25 μm) separated by 10 μm wide struts are fabricated on 5 μm thick sputter deposited Nitinol films. HAECs are seeded onto these micropatterned films and analyzed after 30 days with fluorescence microscopy. Captured images are used to quantify the nucleus packing density, size, and aspect ratio. The films with holes ranging from 10 to 20 μm produce the highest cell packing densities with cell nucleus contained within the hole. This produces a geometrically regular grid like cellular distribution pattern. The cell nucleus aspect ratio on the 10–20 μm holes is more circular in shape when compared to aspect ratio on the continuous film or larger size holes. Finally, the 25 μm size holes prevented the formation of a continuous cell monolayer, suggesting the critical length that cells cannot bridge is between 20 to 25 μm.

Keywords

Nitinol Thin films scaffold Micropatterned holes Re-endothelialization Monolayer morphology 

Notes

Acknowledgements

This work was supported in part by National Science Foundation under Division of Materials Research (DMR #1310074). We thank the Department of Bioengineering, Nanoelectronic Research Facilities and California nanosystems institute at UCLA, and Prof. Dino Di Carlo for providing technical assistance and equipment throughout the experiment.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. D.W. Baker, X. Liu, H. Weng, C. Luo, L. Tang, Fibroblast/fibrocyte: Surface interaction dictates tissue reactions to micropillar implants. Biomacromolecules 12(4), 997–1005 (2011)CrossRefGoogle Scholar
  2. W.S. Barry, Covered stents in the treatment of superficial femoral artery disease. Vasc. Dis. Manag. 11, E76–E86 (2014)Google Scholar
  3. E. Burkarter, C.K. Saul, F. Thomazi, N.C. Cruz, L.S. Roman, W.H. Schreiner, Superhydrophobic electrosprayed PTFE. Surf. Coat. Technol. 202(1), 194–198 (2007)CrossRefGoogle Scholar
  4. C.D. Campbell, D. Goldfarb, R.A. Roe, Small arterial substitute: Expanded microporous polytetrafluoroethylene: Patency versus porosity. Ann. Surg. 182, 138–143 (1975)CrossRefGoogle Scholar
  5. M. Cejna, R. Virmani, R. Jones, H. Bergmeister, C. Loewe, M. Schoder, M. Grgurin, J. Lammer, Biocompatibility and performance of the Wallstent and the Wallgraft, Jostent, and Hemobahn stent-grafts in a sheep model. J. Vasc. Interv. Radiol. 13(8), 823–830 (2002)CrossRefGoogle Scholar
  6. M. Cejna, R. Virmani, R. Jones, H. Bergmeister, U. Losert, Z. Xu, P. Yang, M. Schoder, J. Lammer, Biocompatibility and performance of the Wallstent and several covered stents in a sheep iliac artery model. J Vasc Interv Radiol: JVIR 12(3), 351–358 (2003)CrossRefGoogle Scholar
  7. C. Chaabane, F. Otsuka, R. Virmani, M.L. Bochaton-Piallat, Biological responses in stented arteries. Cardiovasc. Res. 99, 353–363 (2013)CrossRefGoogle Scholar
  8. Q. Cheng, S. Li, K. Komvopoulos, Plasma-assisted surface chemical patterning for single-cell culture. Biomaterials 30(25), 4203–4210 (2009)Google Scholar
  9. C.K. Choi, M.T. Breckenridge, C.S. Chen, Engineered materials and the cellular microenvironment: A strengthening interface between cell biology and bioengineering. Trends Cell Biol. 20, 705–714 (2010)CrossRefGoogle Scholar
  10. Y. Chun, D.S. Levi, K.P. Mohanchandra, G.P. Carman, Superhydrophilic surface treatment for thin film NiTi vascular applications. Mater. Sci. Eng. C 29, 2436–2441 (2009)CrossRefGoogle Scholar
  11. Y.J. Chun, D.S. Levi, K.P. Mohanchandra, M.C. Fishbein, G.P. Carman, Novel micro-patterning processes for thin film NiTi vascular devices. Smart Mater. Struct. 19, 105021 (2010)CrossRefGoogle Scholar
  12. Y. Chun, K.P. Colin, D.S. Levi, D. Rigberg, Y. Chen, B.W. Tillman, K.P. Mohanchandra, M. Shayan, G.P. Carman, An in vivo pilot study of a microporous thin film nitinol-covered stent to assess the effect of porosity and pore geometry on device interaction with the vessel wall. J Biomater Appl 31(8), 1196–1202 (2017)CrossRefGoogle Scholar
  13. P.M. Davidson, H. Özçelik, V. Hasirci, G. Reiter, K. Anselme, Microstructured surfaces cause severe but non-detrimental deformation of the cell nucleus. Adv. Mater. 21(35), 3586–3590 (2009)Google Scholar
  14. N. Foin, R.D. Lee, R. Torii, J.L. Guitierrez-Chico, A. Mattesini, S. Nijjer, S. Sen, R. Petraco, J.E. Davies, C. Di Mario, M. Joner, Impact of stent strut design in metallic stents and biodegradable scaffolds. Int. J. Cardiol. 177(3), 800–808 (2014)CrossRefGoogle Scholar
  15. B. Garipcan, S. Maenz, T. Pham, U. Settmacher, K.D. Jandt, J. Zanow, J. Bossert, Image analysis of endothelial microstructure and endothelial cell dimensions of human arteries - a preliminary study. Adv. Eng. Mat. 13(1–2), B54–B57 (2011)Google Scholar
  16. M.A. Golden, S.R. Hanson, T.R. Kirkman, P.A. Schneider, A.W. Clowes, Healing of polytetrafluoroethylene arterial grafts is influenced by graft porosity. J. Vasc. Surg. 11, 838–845 (1990)CrossRefGoogle Scholar
  17. K. Hazama, H. Miura, T. Shimada, Y. Okuda, T. Murashita, T. Nishibe, Relationship between fibril length and tissue ingrowth in the healing of expanded polytetrafluoroethylene grafts. Surg. Today 34, 685–689 (2004)CrossRefGoogle Scholar
  18. K. Hirabayashi, E. Saitoh, H. Ijima, T. Takenawa, M. Kodama, M. Hori, Influence of fibril length upon ePTFE graft healing and host modification of the implant. J. Biomed. Mater. Res. 26, 1433–1447 (1992)CrossRefGoogle Scholar
  19. K. K. Ho, G. P. Carman, Sputter deposition of NiTi thin ® lm shape memory alloy using a heated target. 370, 18–29 (2000)Google Scholar
  20. H. Holubec, G. C. Hunter, C. W. Putnam, D. A .Bull, W. D. Rappaport, M. Chvapil, Effect of surgical manipulation of polytetrafluoroethylene grafts on microstructural properties and healing characteristics. Am. J. Surg. 164, 512–516 (1992)Google Scholar
  21. W.C. Johnson, K.K. Lee, A comparative evaluation of polytetrafluoroethylene, umbilical vein, and saphenous vein bypass grafts for femoral-popliteal above-knee revascularization: A prospective randomized department of veterans affairs cooperative study. J. Vasc. Surg. 32, 268–277 (2000)CrossRefGoogle Scholar
  22. D. Kim, S.B. Khatau, Y. Feng, S. Walcott, S.X. Sun, G.D. Longmore, D. Wirtz, Actin cap associated focal adhesions and their distinct role in cellular mechanosensing. Sci. Rep. (2012).  https://doi.org/10.1038/srep00555
  23. J. Lafaurie-Janvore, P. Maiuri, I. Wang, M. Pinot, J.-B. Manneville, T. Betz, M. Balland, M. Piel, ESCRT-III assembly and cytokinetic abscission are induced by tension release in the intercellular bridge. Science 339(6127), 1625–1629 (2013)Google Scholar
  24. P.P. Lee, A. Cerchiari, T.A. Desai, Nitinol-based nanotubular coatings for the modulation of human vascular cell function. Nano Lett. 14, 5021–5028 (2014)CrossRefGoogle Scholar
  25. D.S. Levi, R. Williams, J. Liu, S. Danon, L.L. Stepan, K.P. Mohanchandra, M.C. Fishbein, G.P. Carman, Thin film nitinol covered stents: Design and animal testing. ASAIO J. 54, 221–226 (2008)CrossRefGoogle Scholar
  26. K. Loger, A. Engel, J. Haupt, R.L. De Miranda, G. Lutter, E. Quandt, Microstructured nickel-titanium thin film leaflets for hybrid tissue engineered heart valves fabricated by magnetron sputter deposition. Cardiovasc. Eng. Technol. 7(1), 69–77 (2016)CrossRefGoogle Scholar
  27. J. Lu, C. Yao, L. Yang, T.J. Webster, Decreased platelet adhesion and enhanced endothelial cell functions on Nano and Submicron-rough titanium stents. Tissue Eng. Part A 18, 1389–1398 (2012)CrossRefGoogle Scholar
  28. A.S. Nair, M. Tilakchand, B.D. Naik, The effect of multiple autoclave cycles on the surface of rotary nickel-titanium endodontic files: An in vitro atomic force microscopy investigation. J Conserv Dent: JCD 18(3), 218 (2015)CrossRefGoogle Scholar
  29. D. Narayan, S.S. Venkatraman, Effect of pore size and interpore distance on endothelial cell growth on polymers. J. Biomed. Mater. Res. - Part A 87, 710–718 (2008)CrossRefGoogle Scholar
  30. S.D. Plant, D.M. Grant, L. Leach, Behaviour of human endothelial cells on surface modified NiTi alloy. Biomaterials 26(26), 5359–5367 (2005)CrossRefGoogle Scholar
  31. L. Ponsonnet, K. Reybier, N. Jaffrezic, V. Comte, C. Lagneau, M. Lissac, C. Martelet, Relationship between surface properties (roughness, wettability) of titanium and titanium alloys and cell behaviour. Mater. Sci. Eng. C 23, 551–560 (2003)CrossRefGoogle Scholar
  32. S. Raghavan, C.S. Chen, Micropatterned environments in cell biology. Adv. Mater. 16, 1303–1313 (2004)CrossRefGoogle Scholar
  33. D. Rigberg, A. Tulloch, Y. Chun, K.P. Mohanchandra, G.P. Carman, P. Lawrence, Thin-film nitinol (NiTi): A feasibility study for a novel aortic stent graft material. J. Vasc. Surg. 50, 375–380 (2009)CrossRefGoogle Scholar
  34. A.K. Salem, R. Stevens, R.G. Pearson, M.C. Davies, S.J.B. Tendler, C.J. Roberts, P.M. Williams, K.M. Shakesheff, Interactions of 3T3 fibroblasts and endothelial cells with defined pore features. J. Biomed. Mater. Res. 61, 212–217 (2002)CrossRefGoogle Scholar
  35. H.D. Samaroo, J. Lu, T.J. Webster, Enhanced endothelial cell density on NiTi surfaces with submicron to nanometer roughness. Int. J. Nanomedicine 3, 75 (2008)Google Scholar
  36. C.A. Schneider, W.S. Rasband, K.W. Eliceiri, NIH image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012)CrossRefGoogle Scholar
  37. M. Schwarzenbacher, M. Kaltenbrunner, M. Brameshuber, C. Hesch, W. Paster, J. Weghuber, B. Heise, A. Sonnleitner, H. Stockinger, G.J. Schütz, Micropatterning for quantitative analysis of protein-protein interactions in living cells. Nat. Methods 5, 1053–1060 (2008)CrossRefGoogle Scholar
  38. Y. Shen, G. Wang, L. Chen, H. Li, P. Yu, M. Bai, Q. Zhang, J. Lee, Q. Yu, Investigation of surface endothelialization on biomedical nitinol (NiTi) alloy: Effects of surface micropatterning combined with plasma nanocoatings. Acta Biomater. 5, 3593–3604 (2009)CrossRefGoogle Scholar
  39. V.S. Sottiurai, J.S.T. Yao, Y. Vikrom, W.R. Flinn, R.C. Batson, Intimal hyperplasia and neointima: an ultrastructural analysis of thrombosed grafts in humans. Surgery 93(6), 809–817 (1983)Google Scholar
  40. L.L. Stepan, D.S. Levi, G.P. Carman, A thin film nitinol heart valve. J. Biomech. Eng. 127(6), 915–918 (2005)CrossRefGoogle Scholar
  41. G. Tepe, H.P. Wendel, S. Khorchidi, J. Schmehl, J. Wiskirchen, B. Pusich, C.D. Claussen, S.H. Duda, Thrombogenicity of various endovascular stent types: An in vitro evaluation. J. Vasc. Intervent. Radiol. 13(10), 1029–1035 (2002)CrossRefGoogle Scholar
  42. M. Théry, V. Racine, A. Pépin, M. Piel, Y. Chen, J. Sibarita, M. Bornens, The extracellular matrix guides the orientation of the cell division axis. Nat. Cell Biol. 7(10), 947–953 (2005)Google Scholar
  43. A. Venault, Y. Chang, H. Hsu, J. Jhong, H. Yang, T. Wei, K. Tung, A. Higuchi, J. Huang, Biofouling-resistance control of expanded poly (tetrafluoroethylene) membrane via atmospheric plasma-induced surface PEGylation. J. Membr. Sci. 439, 48–57 (2013)CrossRefGoogle Scholar
  44. N. Wang, J.D. Tytell, D.E. Ingber, Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 10(1), 75–82 (2009)Google Scholar
  45. Z. Wang, Z. Du, J. Kok, Y. Chan, S. H. Teoh, E.S. Thian, M. Hong, Direct laser microperforation of bioresponsive surface-patterned films with through-hole arrays for vascular tissue-engineering application. (2015a).  https://doi.org/10.1021/acsbiomaterials.5b00455
  46. Z. Wang, S.H. Teoh, M. Hong, F. Luo, E.Y. Teo, J. Kok, Y. Chan, E.S. Thian, Dual-microstructured porous, anisotropic film for biomimicking of endothelial basement membrane. ACS Appl. Mater. Interfaces 7, 13445–13456 (2015b)CrossRefGoogle Scholar
  47. C.J. White, W.A. Gray, Endovascular therapies for peripheral arterial disease: an evidence-based review. Circulation 116(19), 2203–2215 (2007)Google Scholar
  48. M. Versaevel, T. Grevesse, S. Gabriele, Spatial coordination between cell and nuclear shape within micropatterned endothelial cells. Nat. Commun. 3, 671 (2012)Google Scholar
  49. H. Xu, R. Deshmukh, T. Timmons, K.T. Nguyen, Enhanced endothelialization on surface modified poly(L-lactic acid) substrates. Tissue Eng. Part A 17, 865–876 (2011)CrossRefGoogle Scholar
  50. H. Yeh, S. Lu, T. Tian, R. Hong, W. Lee, C. Tsa, Comparison of endothelial cells grown on different stent materials. J. Biomed. Mater. Res. 76A, 835–841 (2006)CrossRefGoogle Scholar
  51. S. Yoon, Y.K. Kim, E.D. Han, Y. Seo, B.H. Kim, M.R.K. Mofrad, Passive control of cell locomotion using micropatterns: The effect of micropattern geometry on the migratory behavior of adherent cells. Lab Chip 12, 2391 (2012)CrossRefGoogle Scholar
  52. Z. Zhang, Z. Wang, S. Liu, M. Kodama, Pore size, tissue ingrowth, and endothelialization of small-diameter microporous polyurethane vascular prostheses. Biomaterials 25, 177–187 (2004)CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Ming Lun Wu
    • 1
  • Mohanchandra K. Panduranga
    • 2
  • Gregory P. Carman
    • 1
    • 2
  1. 1.Department of BioengineeringUniversity of CaliforniaLos AngelesUSA
  2. 2.Department of Aerospace & Mechanical EngineeringUniversity of CaliforniaLos AngelesUSA

Personalised recommendations