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Journal of Nanomaterials
Volume 2017 (2017), Article ID 9234627, 14 pages
https://doi.org/10.1155/2017/9234627
Review Article

Atomic Force Microscopy for Collagen-Based Nanobiomaterials

Cancer Biophysics Laboratory, Department of Mechanical and Manufacturing Engineering, Faculty of Engineering, University of Cyprus, Nicosia 1678, Cyprus

Correspondence should be addressed to Andreas Stylianou

Received 1 August 2016; Revised 28 November 2016; Accepted 23 January 2017; Published 15 February 2017

Academic Editor: Ilaria Armentano

Copyright © 2017 Andreas Stylianou. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. Fratzl, Collagen Structure and Mechanics, Springer, New York, NY, USA, 2008.
  2. G. T. Tihan, I. Rǎu, R. G. Zgârian, and M. V. Ghica, “Collagen-based biomaterials for ibuprofen delivery,” Comptes Rendus Chimie, vol. 19, pp. 389–393, 2016. View at Google Scholar
  3. B. D. Walters and J. P. Stegemann, “Strategies for directing the structure and function of three-dimensional collagen biomaterials across length scales,” Acta Biomaterialia, vol. 10, no. 4, pp. 1488–1501, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Ricard-Blum, “The collagen family,” Cold Spring Harbor Perspectives in Biology, vol. 3, no. 1, pp. 1–19, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. D. J. S. Hulmes, “Collagen diversity, synthesis and assembly,” Collagen: Structure and Mechanics, pp. 15–47, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. V. Hasirci, E. Vrana, P. Zorlutuna et al., “Nanobiomaterials: a review of the existing science and technology, and new approaches,” Journal of Biomaterials Science, Polymer Edition, vol. 17, no. 11, pp. 1241–1268, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. P. Fratzl, “Collagen: structure and mechanics, an introduction,” Collagen: Structure and Mechanics, pp. 1–13, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Stylianou, D. Yova, and K. Politopoulos, “Atomic force microscopy quantitative and qualitative nanoscale characterization of collagen thin films,” in Proceedings of the 5th International Conference on Emerging Technologies in Non-Destructive Testing (NDT '12), pp. 415–420, Ioannina, Greece, February 2012.
  9. S. Ricard-Blum, F. Ruggiero, and M. Van Der Rest, “The collagen superfamily,” Topics in Current Chemistry, vol. 247, pp. 35–84, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. L. Bozec, G. van der Heijden, and M. Horton, “Collagen fibrils: nanoscale ropes,” Biophysical Journal, vol. 92, no. 1, pp. 70–75, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. J. A. Petruska and A. J. Hodge, “A subunit model for the tropocollagen macromolecule,” Proceedings of the National Academy of Sciences of the United States, vol. 51, pp. 871–876, 1964. View at Publisher · View at Google Scholar · View at Scopus
  12. J. M. Wallace, B. G. Orr, J. C. Marini, and M. M. B. Holl, “Nanoscale morphology of Type I collagen is altered in the Brtl mouse model of Osteogenesis Imperfecta,” Journal of Structural Biology, vol. 173, no. 1, pp. 146–152, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. C. A. Grant, M. A. Phillips, and N. H. Thomson, “Dynamic mechanical analysis of collagen fibrils at the nanoscale,” Journal of the Mechanical Behavior of Biomedical Materials, vol. 5, no. 1, pp. 165–170, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Poole, K. Khairy, J. Friedrichs et al., “Molecular-scale topographic cues induce the orientation and directional movement of fibroblasts on two-dimensional collagen surfaces,” Journal of Molecular Biology, vol. 349, no. 2, pp. 380–386, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. D. R. Stamov, A. Müller, Y. Wegrowski, S. Brezillon, and C. M. Franz, “Quantitative analysis of type I collagen fibril regulation by lumican and decorin using AFM,” Journal of Structural Biology, vol. 183, no. 3, pp. 394–403, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. V. P. Ivanova and A. I. Krivchenko, “A current viewpoint on structure and evolution of collagens. I. Fibrillar collagens,” Journal of Evolutionary Biochemistry and Physiology, vol. 48, no. 2, pp. 127–139, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. M. D. Shoulders and R. T. Raines, “Collagen structure and stability,” Annual Review of Biochemistry, vol. 78, pp. 929–958, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. M. K. Gordon and R. A. Hahn, “Collagens,” Cell and Tissue Research, vol. 339, no. 1, pp. 247–257, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Cen, W. Liu, L. Cui, W. Zhang, and Y. Cao, “Collagen tissue engineering: development of novel biomaterials and applications,” Pediatric Research, vol. 63, no. 5, pp. 492–496, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Stylianou and D. Yova, “Surface nanoscale imaging of collagen thin films by Atomic Force Microscopy,” Materials Science and Engineering: C, vol. 33, no. 5, pp. 2947–2957, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Stylianou, D. Yova, and K. Politopoulos, “Atomic force microscopy surface nanocharacterization of UV-irradiated collagen thin films,” in Proceedings of the 12th IEEE International Conference on BioInformatics and BioEngineering (BIBE '12), Larnaca, Cyprus, November 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. V. J. Morris, A. R. Kirby, and A. P. Gunning, Atomic Force Microscopy for Biologists, Imperial College Press, London, UK, 2008.
  23. D. P. Allison, N. P. Mortensen, C. J. Sullivan, and M. J. Doktycz, “Atomic force microscopy of biological samples,” Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology, vol. 2, no. 6, pp. 618–634, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. D. A. Cisneros, J. Friedrichs, A. Taubenberger, C. M. Franz, and D. J. Muller, “Creating ultrathin nanoscopic collagen matrices for biological and biotechnological applications,” Small, vol. 3, no. 6, pp. 956–963, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Zhuo, X. Zhu, J. Chen, and S. Xie, “Quantitative biomarkers of human skin photoaging based on intrinsic second harmonic generation signal,” Scanning, vol. 35, no. 4, pp. 273–276, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Yokota, J. Kaneshiro, and Y. Uesu, “Optical second harmonic generation microscopy as a tool of material diagnosis,” Physics Research International, vol. 2012, Article ID 704634, 12 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. P. Sowa, J. Rutkowska-Talipska, K. Rutkowski, B. Kosztyła-Hojna, and R. Rutkowski, “Optical radiation in modern medicine,” Advances in Dermatology and Allergology, vol. 30, no. 4, pp. 246–251, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. M. H. Niemz, Laser-Tissue Interactions, Springer, Heidelberg, Germany, 2002. View at Publisher · View at Google Scholar
  29. A. E. Tuer, S. Krouglov, N. Prent et al., “Nonlinear optical properties of type i collagen fibers studied by polarization dependent second harmonic generation microscopy,” Journal of Physical Chemistry B, vol. 115, no. 44, pp. 12759–12769, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. R. M. Williams, W. R. Zipfel, and W. W. Webb, “Interpreting second-harmonic generation images of collagen I fibrils,” Biophysical Journal, vol. 88, no. 2, pp. 1377–1386, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Sionkowska, M. Wisniewski, J. Skopinska et al., “Thermal and mechanical properties of UV irradiated collagen/chitosan thin films,” Polymer Degradation and Stability, vol. 91, no. 12, pp. 3026–3032, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Torikai and H. Shibata, “Effect of ultraviolet radiation on photodegradation of collagen,” Journal of Applied Polymer Science, vol. 73, no. 7, pp. 1259–1265, 1999. View at Publisher · View at Google Scholar · View at Scopus
  33. G. Binnig, C. F. Quate, and C. Gerber, “Atomic force microscope,” Physical Review Letters, vol. 56, no. 9, pp. 930–933, 1986. View at Publisher · View at Google Scholar · View at Scopus
  34. N. Gadegaard, “Atomic force microscopy in biology: technology and techniques,” Biotechnic and Histochemistry, vol. 81, no. 2-3, pp. 87–97, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Stylianou, D. Yova, and E. Alexandratou, “Nanotopography of collagen thin films in correlation with fibroblast response,” Journal of Nanophotonics, vol. 7, no. 1, Article ID 073590, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. A. Stylianou and T. Stylianopoulos, “Atomic force microscopy probing of cancer cells and tumor microenvironment components,” BioNanoScience, vol. 6, no. 1, pp. 33–46, 2016. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Stylianou, K. Politopoulos, and D. Yova, “Atomic force microscopy imaging of the nanoscale assembly of type i collagen on controlled polystyrene particles surfaces,” in Proceedings of the 5th European Conference of the International Federation for Medical and Biological Engineering, pp. 1058–1061, September 2011.
  38. A. Stylianou, S. B. Kontomaris, M. Kyriazi, and D. Yova, “Surface characterization of collagen films by atomic force microscopy,” in Proceedings of the 12th Mediterranean Conference on Medical and Biological Engineering and Computing (MEDICON '10), pp. 612–615, Chalkidiki, Greece, 2010.
  39. S. V. Kontomaris, A. Stylianou, D. Yova, and K. Politopoulos, “Mechanical properties of collagen fibrils on thin films by atomic force microscopy nanoindentation,” in Proceedings of the 12th IEEE International Conference on BioInformatics and BioEngineering (BIBE '12), pp. 608–613, Larnaca, Cyprus, November 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Stylianou, S. V. Kontomaris, D. Yova, and G. Balogiannis, “AFM multimode imaging and nanoindetation method for assessing collagen nanoscale thin films heterogeneity,” in Proceedings of the 13th Mediterranean Conference on Medical and Biological Engineering and Computing, vol. 41, 2014.
  41. S. V. Kontomaris, A. Stylianou, D. Yova, and G. Balogiannis, “The effects of UV irradiation on collagen D-band revealed by atomic force microscopy,” Scanning, vol. 37, no. 2, pp. 101–111, 2015. View at Publisher · View at Google Scholar · View at Scopus
  42. Keysight-Technologies, Keysight 5500 Scanning Probe Microscope-User's Guide, N9410-90001, Keysight Technologies, 2014.
  43. W. Han and F. M. Serry, Force Spectroscopy with the Atomic Force Microscope—Application Note, Agilent Technologies, 2008.
  44. M. Stolz, R. Raiteri, A. U. Daniels, M. R. VanLandingham, W. Baschong, and U. Aebi, “Dynamic elastic modulus of porcine articular cartilage determined at two different levels of tissue organization by indentation-type atomic force microscopy,” Biophysical Journal, vol. 86, no. 5, pp. 3269–3283, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Stolz, R. Gottardi, R. Raiteri et al., “Early detection of aging cartilage and osteoarthritis in mice and patient samples using atomic force microscopy,” Nature Nanotechnology, vol. 4, pp. 186–192, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. W. C. Oliver and G. M. Pharr, “Measurement of hardness and elastic modulus by instrumented indentation: advances in understanding and refinements to methodology,” Journal of Materials Research, vol. 19, no. 1, pp. 3–20, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. E. M. Darling, “Force scanning: a rapid, high-resolution approach for spatial mechanical property mapping,” Nanotechnology, vol. 22, no. 17, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. C. Braunsmann, J. Seifert, J. Rheinlaender, and T. E. Schäffer, “High-speed force mapping on living cells with a small cantilever atomic force microscope,” Review of Scientific Instruments, vol. 85, no. 7, Article ID 073703, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Stylianou, S.-V. Kontomaris, and D. Yova, “Assessing collagen nanoscale thin films heterogeneity by AFM multi-mode imaging and nanoindetation for nanobiomedical applications,” Micro and Nanosystems, vol. 6, no. 2, pp. 95–102, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. S. V. Kontomaris, D. Yova, A. Stylianou, and K. Politopoulos, “The significance of the percentage differences of young’s modulus in the AFM nanoindentation procedure,” Micro and Nanosystems, vol. 7, no. 2, pp. 86–97, 2015. View at Publisher · View at Google Scholar · View at Scopus
  51. H. Hertz, “Ueber die Berührung fester elastischer Körper,” Journal für die Reine und Angewandte Mathematik, vol. 92, pp. 156–171, 1882. View at Google Scholar
  52. J. L. Mackay and S. Kumar, “Measuring the elastic properties of living cells with atomic force microscopy indentation,” Methods in Molecular Biology, vol. 931, pp. 313–329, 2013. View at Google Scholar · View at Scopus
  53. D. J. Müller and Y. F. Dufrêne, “Atomic force microscopy: a nanoscopic window on the cell surface,” Trends in Cell Biology, vol. 21, no. 8, pp. 461–469, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. D. J. Müller and Y. F. Dufrêne, “Atomic force microscopy as a multifunctional molecular toolbox in nanobiotechnology,” Nature Nanotechnology, vol. 3, no. 5, pp. 261–269, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Li, L.-Q. Liu, N. Xi, and Y.-C. Wang, “Nanoscale monitoring of drug actions on cell membrane using atomic force microscopy,” Acta Pharmacologica Sinica, vol. 36, no. 7, pp. 769–782, 2015. View at Publisher · View at Google Scholar · View at Scopus
  56. X. Shi, X. Zhang, T. Xia, and X. Fang, “Living cell study at the single-molecule and single-cell levels by atomic force microscopy,” Nanomedicine, vol. 7, no. 10, pp. 1625–1637, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. F. Variola, “Atomic force microscopy in biomaterials surface science,” Physical Chemistry Chemical Physics, vol. 17, no. 5, pp. 2950–2959, 2015. View at Publisher · View at Google Scholar · View at Scopus
  58. B. Ohler, “Perspectives on over twenty years of life science research with atomic force microscopy and a look toward the future,” Microscopy and Microanalysis, vol. 16, no. 2, pp. 1034–1035, 2010. View at Publisher · View at Google Scholar
  59. D. Kirmizis and S. Logothetidis, “Atomic force microscopy probing in the measurement of cell mechanics,” International Journal of Nanomedicine, vol. 5, no. 1, pp. 137–145, 2010. View at Google Scholar · View at Scopus
  60. H. Q. Phong, S.-L. Wang, and M.-J. Wang, “Cell behaviors on micro-patterned porous thin films,” Materials Science and Engineering B: Solid-State Materials for Advanced Technology, vol. 169, no. 1-3, pp. 94–100, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. C. Y. Tay, S. A. Irvine, F. Y. C. Boey, L. P. Tan, and S. Venkatraman, “Micro-/nano-engineered cellular responses for soft tissue engineering and biomedical applications,” Small, vol. 7, no. 10, pp. 1361–1378, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. J. T. Elliott, A. Tona, J. T. Woodward, P. L. Jones, and A. L. Plant, “Thin films of collagen affect smooth muscle cell morphology,” Langmuir, vol. 19, no. 5, pp. 1506–1514, 2003. View at Publisher · View at Google Scholar · View at Scopus
  63. F. H. Silver, J. W. Freeman, and G. P. Seehra, “Collagen self-assembly and the development of tendon mechanical properties,” Journal of Biomechanics, vol. 36, no. 10, pp. 1529–1553, 2003. View at Publisher · View at Google Scholar · View at Scopus
  64. F. Jiang, K. Khairy, K. Poole, J. Howard, and D. J. Müller, “Creating nanoscopic collagen matrices using atomic force microscopy,” Microscopy Research and Technique, vol. 64, no. 5-6, pp. 435–440, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. F. Jiang, H. Hörber, J. Howard, and D. J. Müller, “Assembly of collagen into microribbons: effects of pH and electrolytes,” Journal of Structural Biology, vol. 148, no. 3, pp. 268–278, 2004. View at Publisher · View at Google Scholar · View at Scopus
  66. E. K. F. Yim, R. M. Reano, S. W. Pang, A. F. Yee, C. S. Chen, and K. W. Leong, “Nanopattern-induced changes in morphology and motility of smooth muscle cells,” Biomaterials, vol. 26, no. 26, pp. 5405–5413, 2005. View at Publisher · View at Google Scholar · View at Scopus
  67. S. Zhong, W. E. Teo, X. Zhu, R. W. Beuerman, S. Ramakrishna, and L. Y. L. Yung, “An aligned nanofibrous collagen scaffold by electrospinning and its effects on in vitro fibroblast culture,” Journal of Biomedical Materials Research Part A, vol. 79, no. 3, pp. 456–463, 2006. View at Publisher · View at Google Scholar · View at Scopus
  68. J. T. Elliott, J. T. Woodward, A. Umarji, Y. Mei, and A. Tona, “The effect of surface chemistry on the formation of thin films of native fibrillar collagen,” Biomaterials, vol. 28, no. 4, pp. 576–585, 2007. View at Publisher · View at Google Scholar · View at Scopus
  69. C. C. Dupont-Gillain and P. G. Rouxhet, “AFM study of the interaction of collagen with polystyrene and plasma-oxidized polystyrene,” Langmuir, vol. 17, no. 23, pp. 7261–7266, 2001. View at Publisher · View at Google Scholar · View at Scopus
  70. G. G. Biino and P. Gröning, “Cleavage mechanism and surface chemical characterization of phengitic muscovite and muscovite as constrained by X-ray Photoelectron Spectroscopy,” Physics and Chemistry of Minerals, vol. 25, no. 2, pp. 168–181, 1998. View at Publisher · View at Google Scholar · View at Scopus
  71. F. Ostendorf, C. Schmitz, S. Hirth, A. Kühnle, J. J. Kolodziej, and M. Reichling, “How flat is an air-cleaved mica surface?” Nanotechnology, vol. 19, no. 30, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. H. Yang, S.-Y. Fung, M. Pritzker, and P. Chen, “Modification of hydrophilic and hydrophobic surfaced using an ionic-complementary peptide,” PLoS ONE, vol. 2, no. 12, Article ID e1325, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. S. Mulley, “Ordering and manipulation of MoS2 platelets on differently charged micas by atomic force microscopy,” Journal of Materials Chemistry, vol. 6, no. 4, pp. 661–666, 1996. View at Publisher · View at Google Scholar · View at Scopus
  74. M. Sun, A. Stetco, and E. F. Merschrod, “Surface-templated formation of protein microfibril arrays,” Langmuir, vol. 24, no. 10, pp. 5418–5421, 2008. View at Publisher · View at Google Scholar · View at Scopus
  75. J. K. Rainey and M. Cynthia Goh, “A statistically derived parameterization for the collagen triple-helix,” Protein Science, vol. 11, no. 11, pp. 2748–2754, 2002. View at Publisher · View at Google Scholar · View at Scopus
  76. H.-W. Su, M.-S. Ho, and C.-M. Cheng, “Probing characteristics of collagen molecules on various surfaces via atomic force microscopy,” Applied Physics Letters, vol. 100, no. 23, Article ID 233703, 2012. View at Publisher · View at Google Scholar · View at Scopus
  77. P. Lisboa, M.-B. Villiers, C. Brakha et al., “Fabrication of bio-functionalised polypyrrole nanoarrays for bio-molecular recognition,” Micro and Nanosystems, vol. 3, no. 1, pp. 83–89, 2011. View at Publisher · View at Google Scholar · View at Scopus
  78. K. M. Brouwer, P. van Rensch, V. E. M. Harbers et al., “Evaluation of methods for the construction of collagenous scaffolds with a radial pore structure for tissue engineering,” Journal of Tissue Engineering and Regenerative Medicine, vol. 5, no. 6, pp. 501–504, 2011. View at Publisher · View at Google Scholar · View at Scopus
  79. A. L. Plant, K. Bhadriraju, T. A. Spurlin, and J. T. Elliott, “Cell response to matrix mechanics: focus on collagen,” Biochimica et Biophysica Acta - Molecular Cell Research, vol. 1793, no. 5, pp. 893–902, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. X. F. Walboomers and J. A. Jansen, “Cell and tissue behavior on micro-grooved surfaces,” Odontology, vol. 89, no. 1, pp. 2–11, 2001. View at Publisher · View at Google Scholar
  81. W. A. Loesberg, J. te Riet, F. C. M. J. M. van Delft et al., “The threshold at which substrate nanogroove dimensions may influence fibroblast alignment and adhesion,” Biomaterials, vol. 28, no. 27, pp. 3944–3951, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Hou, X.-X. Li, X.-Y. Li et al., “Patterning of 293T fibroblasts on a mica surface,” Analytical and Bioanalytical Chemistry, vol. 394, no. 8, pp. 2111–2117, 2009. View at Publisher · View at Google Scholar · View at Scopus
  83. S. Vanharanta and J. Massagué, “Field cancerization: something new under the sun,” Cell, vol. 149, no. 6, pp. 1179–1181, 2012. View at Publisher · View at Google Scholar · View at Scopus
  84. T. T. Lu, Y. Z. Chen, T. Lu, and Y. Y. Zhang, “Mechanism of UV damage and the protective effect of natral products against UV damage,” Chinese Pharmacological Bulletin, pp. 1655–1659, 2012. View at Google Scholar
  85. H. Ryssel, G. Germann, and E. Koellensperger, “An overview of current biomaterials in aesthetic soft tissue augmentation,” European Journal of Plastic Surgery, vol. 35, no. 2, pp. 121–133, 2012. View at Publisher · View at Google Scholar · View at Scopus
  86. H. Suh and J.-C. Park, “Evaluation of calcification in porcine valves treated by ultraviolet ray and glutaraldehyde,” Materials Science and Engineering C, vol. 13, no. 1-2, pp. 65–73, 2000. View at Publisher · View at Google Scholar · View at Scopus
  87. G. Fessel, J. Wernli, Y. Li, C. Gerber, and J. G. Snedeker, “Exogenous collagen cross-linking recovers tendon functional integrity in an experimental model of partial tear,” Journal of Orthopaedic Research, vol. 30, no. 6, pp. 973–981, 2012. View at Publisher · View at Google Scholar · View at Scopus
  88. A. Gaspar, L. Moldovan, D. Constantin, A. M. Stanciuc, P. M. Sarbu Boeti, and I. C. Efrimescu, “Collagen-based scaffolds for skin tissue engineering,” Journal of Medicine and Life, vol. 4, no. 2, pp. 172–177, 2011. View at Google Scholar · View at Scopus
  89. N. N. Fathima, R. Suresh, J. R. Rao, B. U. Nair, and T. Ramasami, “Effect of UV irradiation on stabilized collagen: role of chromium(III),” Colloids and Surfaces B: Biointerfaces, vol. 62, no. 1, pp. 11–16, 2008. View at Publisher · View at Google Scholar · View at Scopus
  90. N. N. Fathima, R. Suresh, J. R. Rao, and B. U. Nair, “Effect of UV irradiation on the physicochemical properties of collagen stabilized using aldehydes,” Journal of Applied Polymer Science, vol. 104, no. 6, pp. 3642–3648, 2007. View at Publisher · View at Google Scholar · View at Scopus
  91. K. Jariashvili, B. Madhan, B. Brodsky, A. Kuchava, L. Namicheishvili, and N. Metreveli, “Uv damage of collagen: insights from model collagen peptides,” Biopolymers, vol. 97, no. 3, pp. 189–198, 2012. View at Publisher · View at Google Scholar · View at Scopus
  92. N. O. Metreveli, K. K. Jariashvili, L. O. Namicheishvili et al., “UV-vis and FT-IR spectra of ultraviolet irradiated collagen in the presence of antioxidant ascorbic acid,” Ecotoxicology and Environmental Safety, vol. 73, no. 3, pp. 448–455, 2010. View at Publisher · View at Google Scholar · View at Scopus
  93. J. Skopinska-Wisniewska, A. Sionkowska, A. Kaminska, A. Kaznica, R. Jachimiak, and T. Drewa, “Surface characterization of collagen/elastin based biomaterials for tissue regeneration,” Applied Surface Science, vol. 255, no. 19, pp. 8286–8292, 2009. View at Publisher · View at Google Scholar · View at Scopus
  94. A. Stylianou, D. Yova, E. Alexandratou, and A. Petri, “Atomic force imaging microscopy investigation of the interaction of ultraviolet radiation with collagen thin films,” in Nanoscale Imaging, Sensing, and Actuation for Biomedical Applications X, vol. 8594 of Proceedings of SPIE, February 2013. View at Publisher · View at Google Scholar
  95. A. Stylianou, D. Yova, and E. Alexandratou, “Investigation of the influence of UV irradiation on collagen thin films by AFM imaging,” Materials Science and Engineering C, vol. 45, pp. 455–468, 2014. View at Publisher · View at Google Scholar · View at Scopus
  96. C. Zink, H. Hall, D. M. Brunette, and N. D. Spencer, “Orthogonal nanometer-micrometer roughness gradients probe morphological influences on cell behavior,” Biomaterials, vol. 33, no. 32, pp. 8055–8061, 2012. View at Publisher · View at Google Scholar · View at Scopus
  97. K. Anselme, A. Ponche, and M. Bigerelle, “Relative influence of surface topography and surface chemistry on cell response to bone implant materials. Part 2: biological aspects,” Proceedings of the Institution of Mechanical Engineers, Part H: Journal of Engineering in Medicine, vol. 224, no. 12, pp. 1487–1507, 2010. View at Publisher · View at Google Scholar · View at Scopus
  98. U. Covani, L. Giacomelli, A. Krajewski et al., “Biomaterials for orthopedics: a roughness analysis by atomic force microscopy,” Journal of Biomedical Materials Research—Part A, vol. 82, no. 3, pp. 723–730, 2007. View at Publisher · View at Google Scholar · View at Scopus
  99. A. Sionkowska, A. Płanecka, J. Kozłowska, and J. Skopińska-Wiśniewska, “Surface properties of UV-irradiated poly(vinyl alcohol) films containing small amount of collagen,” Applied Surface Science, vol. 255, no. 7, pp. 4135–4139, 2009. View at Publisher · View at Google Scholar · View at Scopus
  100. A. Sionkowska, J. Kozłowska, A. Płanecka, and J. Skopińska-Wiśniewska, “Collagen fibrils in UV irradiated poly(vinyl pyrrolidone) films,” Applied Surface Science, vol. 255, no. 5, pp. 2030–2039, 2008. View at Publisher · View at Google Scholar · View at Scopus
  101. Z. Cheng and S.-H. Teoh, “Surface modification of ultra thin poly (ε-caprolactone) films using acrylic acid and collagen,” Biomaterials, vol. 25, no. 11, pp. 1991–2001, 2004. View at Publisher · View at Google Scholar · View at Scopus
  102. M. Achilli, J. Lagueux, and D. Mantovani, “On the effects of UV-C and pH on the mechanical behavior, molecular conformation and cell viability of collagen-based scaffold for vascular tissue engineering,” Macromolecular Bioscience, vol. 10, no. 3, pp. 307–316, 2010. View at Publisher · View at Google Scholar · View at Scopus
  103. A. B. Caruso and M. G. Dunn, “Changes in mechanical properties and cellularity during long-term culture of collagen fiber ACL reconstruction scaffolds,” Journal of Biomedical Materials Research Part A, vol. 73, no. 4, pp. 388–397, 2005. View at Publisher · View at Google Scholar · View at Scopus
  104. N. Rajan, J. Lagueux, F. Couet, W. Pennock, D. Mantovani, and A. Sionkowska, “Low doses of ultraviolet radiation stimulate cell activity in collagen-based scaffolds,” Biotechnology Progress, vol. 24, no. 4, pp. 884–889, 2008. View at Publisher · View at Google Scholar · View at Scopus
  105. S. J. Kew, J. H. Gwynne, D. Enea et al., “Regeneration and repair of tendon and ligament tissue using collagen fibre biomaterials,” Acta Biomaterialia, vol. 7, no. 9, pp. 3237–3247, 2011. View at Publisher · View at Google Scholar · View at Scopus
  106. A. Sionkowska and T. Wess, “Mechanical properties of UV irradiated rat tail tendon (RTT) collagen,” International Journal of Biological Macromolecules, vol. 34, no. 1-2, pp. 9–12, 2004. View at Publisher · View at Google Scholar · View at Scopus
  107. S. Anastase-Ravion, M. P. Carreno, C. Blondin et al., “Synergistic effects of glucose and ultraviolet irradiation on the physical properties of collagen,” Journal of Biomedical Materials Research, vol. 60, no. 3, pp. 384–391, 2002. View at Publisher · View at Google Scholar · View at Scopus
  108. A. Stylianou and D. Yova, “Atomic force microscopy investigation of the interaction of low-level laser irradiation of collagen thin films in correlation with fibroblast response,” Lasers in Medical Science, vol. 30, no. 9, pp. 2369–2379, 2015. View at Publisher · View at Google Scholar · View at Scopus
  109. R. W. Boyd, Nonlinear Optics, Academic Press, The Institute of Optics University of Rochester, New York, NY, USA, 1992.
  110. B.-M. Kim, J. Eichler, K. M. Reiser, A. M. Rubenchik, and L. B. Da Silva, “Collagen structure and nonlinear susceptibility: effects of heat, glycation, and enzymatic cleavage on second harmonic signal intensity,” Lasers in Surgery and Medicine, vol. 27, no. 4, pp. 329–335, 2000. View at Publisher · View at Google Scholar · View at Scopus
  111. T. Theodossiou, G. S. Rapti, V. Hovhannisyan, E. Georgiou, K. Politopoulos, and D. Yova, “Thermally induced irreversible conformational changes in collagen probed by optical second harmonic generation and laser-induced fluorescence,” Lasers in Medical Science, vol. 17, no. 1, pp. 34–41, 2002. View at Publisher · View at Google Scholar · View at Scopus
  112. E. Brown, T. McKee, E. DiTomaso et al., “Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation,” Nature Medicine, vol. 9, no. 6, pp. 796–800, 2003. View at Publisher · View at Google Scholar · View at Scopus
  113. S.-J. Lin, W. Lo, H.-Y. Tan et al., “Prediction of heat-induced Collagen shrinkage by use of second harmonic generation microscopy,” Journal of Biomedical Optics, vol. 11, no. 3, Article ID 034020, 2006. View at Publisher · View at Google Scholar · View at Scopus
  114. P. J. Campagnola and L. M. Loew, “Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms,” Nature Biotechnology, vol. 21, no. 11, pp. 1356–1360, 2003. View at Publisher · View at Google Scholar · View at Scopus
  115. P. J. Campagnola and C.-Y. Dong, “Second harmonic generation microscopy: principles and applications to disease diagnosis,” Laser and Photonics Reviews, vol. 5, no. 1, pp. 13–26, 2011. View at Publisher · View at Google Scholar · View at Scopus
  116. A. Stylianou, K. Politopoulos, M. Kyriazi, and D. Yova, “Combined information from AFM imaging and SHG signal analysis of collagen thin films,” Biomedical Signal Processing and Control, vol. 6, no. 3, pp. 307–313, 2011. View at Publisher · View at Google Scholar · View at Scopus
  117. A. Stylianou, M. Kyriazi, K. Politopoulos, and D. Yova, “Combined SHG signal information with AFM imaging to assess conformational changes in collagen,” in Proceedings of the 9th International Conference on Information Technology and Applications in Biomedicine (ITAB '09), Larnaka, Cyprus, November 2009. View at Publisher · View at Google Scholar · View at Scopus
  118. J. Myllyharju and K. I. Kivirikko, “Collagens and collagen-related diseases,” Annals of Medicine, vol. 33, no. 1, pp. 7–21, 2001. View at Publisher · View at Google Scholar · View at Scopus
  119. O. Maller, K. C. Hansen, T. R. Lyons et al., “Collagen architecture in pregnancy-induced protection from breast cancer,” Journal of Cell Science, vol. 126, no. 18, pp. 4108–4120, 2013. View at Publisher · View at Google Scholar · View at Scopus
  120. J. G. Goetz, S. Minguet, I. Navarro-Lérida et al., “Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis,” Cell, vol. 146, no. 1, pp. 148–163, 2011. View at Publisher · View at Google Scholar · View at Scopus
  121. M. W. Pickup, H. Laklai, I. Acerbi et al., “Stromally derived lysyl oxidase promotes metastasis of transforming growth factor-β-deficient mouse mammary carcinomas,” Cancer Research, vol. 73, no. 17, pp. 5336–5346, 2013. View at Publisher · View at Google Scholar · View at Scopus
  122. R. Navab, D. Strumpf, C. To et al., “Integrin α11β1 regulates cancer stromal stiffness and promotes tumorigenicity and metastasis in non-small cell lung cancer,” Oncogene, vol. 35, no. 15, pp. 1899–1908, 2016. View at Publisher · View at Google Scholar · View at Scopus
  123. M. Ferrarini, G. Mazzoleni, N. Steimberg, D. Belloni, and E. Ferrero, “Innovative models to assess multiple myeloma biology and the impact of drugs,” in Multiple Myeloma—A Quick Reflection on the Fast Progress, R. Hajek, Ed., chapter 3, InTech, Rijeka, Croatia, 2013. View at Publisher · View at Google Scholar
  124. B. Weigelt, C. M. Ghajar, and M. J. Bissell, “The need for complex 3D culture models to unravel novel pathways and identify accurate biomarkers in breast cancer,” Advanced Drug Delivery Reviews, vol. 69-70, pp. 42–51, 2014. View at Publisher · View at Google Scholar · View at Scopus
  125. V. Gkretsi, A. Stylianou, P. Papageorgis, C. Polydorou, and T. Stylianopoulos, “Remodeling components of the tumor microenvironment to enhance cancer therapy,” Frontiers in Oncology, vol. 5, article 214, 2015. View at Publisher · View at Google Scholar · View at Scopus
  126. S. Gehler, M. Baldassarre, Y. Lad et al., “Filamin A-β1 integrin complex tunes epithelial cell response to matrix tension,” Molecular Biology of the Cell, vol. 20, no. 14, pp. 3224–3238, 2009. View at Publisher · View at Google Scholar · View at Scopus
  127. C. S. Szot, C. F. Buchanan, J. W. Freeman, and M. N. Rylander, “3D in vitro bioengineered tumors based on collagen I hydrogels,” Biomaterials, vol. 32, no. 31, pp. 7905–7912, 2011. View at Publisher · View at Google Scholar · View at Scopus
  128. B. N. Mason, A. Starchenko, R. M. Williams, L. J. Bonassar, and C. A. Reinhart-King, “Tuning three-dimensional collagen matrix stiffness independently of collagen concentration modulates endothelial cell behavior,” Acta Biomaterialia, vol. 9, no. 1, pp. 4635–4644, 2013. View at Publisher · View at Google Scholar · View at Scopus
  129. L. J. Kaufman, C. P. Brangwynne, K. E. Kasza et al., “Glioma expansion in collagen I matrices: analyzing collagen concentration-dependent growth and motility patterns,” Biophysical Journal, vol. 89, no. 1, pp. 635–650, 2005. View at Publisher · View at Google Scholar · View at Scopus
  130. M. Delarue, F. Montel, D. Vignjevic, J. Prost, J.-F. Joanny, and G. Cappello, “Compressive stress inhibits proliferation in tumor spheroids through a volume limitation,” Biophysical Journal, vol. 107, no. 8, pp. 1821–1828, 2014. View at Publisher · View at Google Scholar · View at Scopus
  131. K. R. Levental, H. Yu, L. Kass et al., “Matrix crosslinking forces tumor progression by enhancing integrin signaling,” Cell, vol. 139, no. 5, pp. 891–906, 2009. View at Publisher · View at Google Scholar · View at Scopus
  132. W. Tan, R. Krishnaraj, and T. A. Desai, “Influence of chitosan on cell viability and proliferation in three dimensional collage gels,” in Proceedings of the 22nd Annual International Conference of the IEEE Engineering in Medicine and Biology Society, vol. 1502, pp. 1509–1524, Chicago, Ill, USA, July 2000. View at Scopus
  133. V. Vicens-Zygmunt, S. Estany, A. Colom et al., “Fibroblast viability and phenotypic changes within glycated stiffened three-dimensional collagen matrices,” Respiratory Research, vol. 16, article 82, 2015. View at Publisher · View at Google Scholar
  134. S. Nam, K. H. Hu, M. J. Butte, and O. Chaudhuri, “Strain-enhanced stress relaxation impacts nonlinear elasticity in collagen gels,” Proceedings of the National Academy of Sciences of the United States of America, vol. 113, no. 20, pp. 5492–5497, 2016. View at Publisher · View at Google Scholar · View at Scopus
  135. S. van Helvert and P. Friedl, “Strain stiffening of fibrillar collagen during individual and collective cell migration identified by AFM nanoindentation,” ACS Applied Materials & Interfaces, vol. 8, no. 34, pp. 21946–21955, 2016. View at Publisher · View at Google Scholar
  136. R. Garcia and R. Proksch, “Nanomechanical mapping of soft matter by bimodal force microscopy,” European Polymer Journal, vol. 49, no. 8, pp. 1897–1906, 2013. View at Publisher · View at Google Scholar · View at Scopus
  137. R. García and R. Pérez, “Dynamic atomic force microscopy methods,” Surface Science Reports, vol. 47, no. 6-8, pp. 197–301, 2002. View at Publisher · View at Google Scholar · View at Scopus
  138. G. Chawla and S. D. Solares, “Mapping of conservative and dissipative interactions in bimodal atomic force microscopy using open-loop and phase-locked-loop control of the higher eigenmode,” Applied Physics Letters, vol. 99, no. 7, Article ID 074103, 2011. View at Publisher · View at Google Scholar · View at Scopus
  139. R. A. B. Crabb, E. P. Chau, D. M. Decoteau, and A. Hubel, “Microstructural characteristics of extracellular matrix produced by stromal fibroblasts,” Annals of Biomedical Engineering, vol. 34, no. 10, pp. 1615–1627, 2006. View at Publisher · View at Google Scholar · View at Scopus
  140. G. Lamour, C. K. Yip, H. Li, and J. Gsponer, “High intrinsic mechanical flexibility of mouse prion nanofibrils revealed by measurements of axial and radial young's moduli,” ACS Nano, vol. 8, no. 4, pp. 3851–3861, 2014. View at Publisher · View at Google Scholar · View at Scopus
  141. R. Kassies, K. O. Van der Werf, A. Lenferink et al., “Combined AFM and confocal fluorescence microscope for applications in bio-nanotechnology,” Journal of Microscopy, vol. 217, no. 1, pp. 109–116, 2005. View at Publisher · View at Google Scholar · View at MathSciNet · View at Scopus
  142. T. Ludwig, R. Kirmse, and K. Poole, “Challenges and approaches—probing tumor cell invasion by atomic force microscopy,” in Modern Research and Educational Topics in Microscopy, A. Méndez-Vilas and J. Díaz, Eds., pp. 11–22, Formatex, 2007. View at Google Scholar
  143. I. Sokolov, “Chapter 1: atomic force microscopy in cancer cell research,” in Cancer Nanotechnology, H. S. Nalwa and T. Webster, Eds., American Scientific, Valencia, Calif, USA, 2007. View at Google Scholar
  144. L. Cassereau, Y. A. Miroshnikova, G. Ou, J. Lakins, and V. M. Weaver, “A 3D tension bioreactor platform to study the interplay between ECM stiffness and tumor phenotype,” Journal of Biotechnology, vol. 193, pp. 66–69, 2015. View at Publisher · View at Google Scholar · View at Scopus