Table of Contents
International Journal of Tissue Engineering
Volume 2015 (2015), Article ID 586493, 10 pages
http://dx.doi.org/10.1155/2015/586493
Research Article

The Use of a Green Fluorescent Protein Porcine Model to Evaluate Host Tissue Integration into Extracellular Matrix Derived Bionanocomposite Scaffolds

1Department of Bioengineering, University of Missouri, 254 Agricultural Engineering, Columbia, MO 65211, USA
2Department of Orthopaedic Surgery, University of Missouri, Missouri Orthopaedic Institute, 1100 Virginia Avenue Columbia, MO 65212, USA

Received 30 September 2014; Accepted 10 December 2014

Academic Editor: Kimimasa Tobita

Copyright © 2015 S. E. Smith et al. 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. S. F. Badylak, D. O. Freytes, and T. W. Gilbert, “Extracellular matrix as a biological scaffold material: structure and function,” Acta Biomaterialia, vol. 5, no. 1, pp. 1–13, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. S. F. Badylak, “Decellularized allogeneic and xenogeneic tissue as a bioscaffold for regenerative medicine: factors that influence the host response,” Annals of Biomedical Engineering, vol. 42, no. 7, pp. 1517–1527, 2014. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. N. L. Leong, F. A. Petrigliano, and D. R. McAllister, “Current tissue engineering strategies in anterior cruciate ligament reconstruction,” Journal of Biomedical Materials Research Part A, vol. 102, no. 5, pp. 1614–1624, 2014. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. L. Melman, E. D. Jenkins, N. A. Hamilton et al., “Early biocompatibility of crosslinked and non-crosslinked biologic meshes in a porcine model of ventral hernia repair,” Hernia, vol. 15, no. 2, pp. 157–164, 2011. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. S. P. Zhong, Y. Z. Zhang, and C. T. Lim, “Tissue scaffolds for skin wound healing and dermal reconstruction,” WIREs Nanomed Nanobi, vol. 2, pp. 510–525, 2010. View at Publisher · View at Google Scholar · View at PubMed
  6. B. N. Brown and S. F. Badylak, “Extracellular matrix as an inductive scaffold for functional tissue reconstruction,” Translational Research, vol. 163, no. 4, pp. 268–285, 2014. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. X. Jiang, Z. Kalajzic, P. Maye et al., “Histological analysis of GFP expression in murine bone,” Journal of Histochemistry & Cytochemistry, vol. 53, no. 5, pp. 593–602, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  8. N. Tamamaki, Y. Yanagawa, R. Tomioka, J.-I. Miyazaki, K. Obata, and T. Kaneko, “Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse,” Journal of Comparative Neurology, vol. 467, no. 1, pp. 60–79, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. V. V. Artym and K. Matsumoto, “Imaging cells in three-dimensional collagen matrix,” Current Protocols in Cell Biology, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  10. N. Billinton and A. W. Knight, “Seeing the wood through the trees: a review of techniques for distinguishing green fluorescent protein from endogenous autofluorescence,” Analytical Biochemistry, vol. 291, no. 2, pp. 175–197, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. W. Baschong, R. Suetterlin, and R. Hubert Laeng, “Control of autofluorescence of archival formaldehyde-fixed, paraffin-embedded tissue in confocal laser scanning microscopy (CLSM),” Journal of Histochemistry and Cytochemistry, vol. 49, no. 12, pp. 1565–1571, 2001. View at Publisher · View at Google Scholar · View at Scopus
  12. N. Zhu, D. Chapman, D. Cooper, D. J. Schreyer, and X. Chen, “X-ray diffraction enhanced imaging as a novel method to visualize low-density scaffolds in soft tissue engineering,” Tissue Engineering Part C: Methods, vol. 17, no. 11, pp. 1071–1080, 2011. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. E. T. Curtis, S. Zhang, V. Khalilzad-Sharghi, T. Boulet, and S. F. Othman, “Magnetic resonance elastography methodology for the evaluation of tissue engineered construct growth,” Journal of Visualized Experiments, no. 60, article no. e3618, 2012. View at Publisher · View at Google Scholar · View at PubMed
  14. O. Morin, A. Gillis, J. Chen et al., “Megavoltage cone-beam CT: system description and clinical applications,” Medical Dosimetry, vol. 31, no. 1, pp. 51–61, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  15. E. Brown, J. Mantell, D. Carter, G. Tilly, and P. Verkade, “Studying intracellular transport using high-pressure freezing and correlative light electron microscopy,” Seminars in Cell & Developmental Biology, vol. 20, no. 8, pp. 910–919, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  16. T. Murakami and E. Kobayashi, “GFP-transgenic animals for in vivo imaging: rats, rabbits, and pigs,” in In Vivo Cellular Imaging Using Fluorescent Proteins, R. M. Hoffman, Ed., Methods in Molecular Biology, pp. 177–189, 2012. View at Google Scholar
  17. Z. Liu, J. Song, Z. Wang et al., “Green fluorescent protein (GFP) transgenic pig produced by somatic cell nuclear transfer,” Chinese Science Bulletin, vol. 53, no. 7, pp. 1035–1039, 2008. View at Publisher · View at Google Scholar
  18. X. Yu, L. Wang, Z. Xia et al., “Modulation of host osseointegration during bone regeneration by controlling exogenous stem cell differentiation using a material approach,” Biomaterials Science, vol. 2, no. 2, pp. 242–251, 2014. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. T. Zantop, T. W. Gilbert, M. C. Yoder, and S. F. Badylak, “Extracellular matrix scaffolds are repopulated by bone marrow-derived cells in a mouse model of achilles tendon reconstruction,” Journal of Orthopaedic Research, vol. 24, no. 6, pp. 1299–1309, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. Y. Bai, P.-F. Lee, H. C. Gibbs, K. J. Bayless, and A. T. Yeh, “Dynamic multicomponent engineered tissue reorganization and matrix deposition measured with an integrated nonlinear optical microscopy-optical coherence microscopy system,” Journal of Biomedical Optics, vol. 19, no. 3, Article ID 036014, 2014. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  21. A. E. Loiselle, L. Wei, M. Faryad et al., “Specific biomimetic hydroxyapatite nanotopographies enhance osteoblastic differentiation and bone graft osteointegration,” Tissue Engineering: Part A, vol. 19, no. 15-16, pp. 1704–1712, 2013. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. A. A. Sawyer, K. M. Hennessy, and S. L. Bellis, “Regulation of mesenchymal stem cell attachment and spreading on hydroxyapatite by RGD peptides and adsorbed serum proteins,” Biomaterials, vol. 26, no. 13, pp. 1467–1475, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  23. S. A. Grant, C. S. Spradling, D. N. Grant et al., “Assessment of the biocompatibility and stability of a gold nanoparticle collagen bioscaffold,” Journal of Biomedical Materials Research Part A, vol. 102, no. 2, pp. 332–339, 2014. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. Y. Zhou, Y. Kong, S. Kundu, J. D. Cirillo, and H. Liang, “Antibacterial activities of gold and silver nanoparticles against Escherichia coli and bacillus Calmette-Guérin,” Journal of Nanobiotechnology, vol. 10, article 19, 2012. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. Ö. A. Kalaycı, F. B. Cömert, B. Hazer, T. Atalay, K. A. Cavicchi, and M. Cakmak, “Synthesis, characterization, and antibacterial activity of metal nanoparticles embedded into amphiphilic comb-type graft copolymers,” Polymer Bulletin, vol. 65, no. 3, pp. 215–226, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. J. Siegel, K. Kolářová, V. Vosmanská, S. Rimpelová, J. Leitner, and V. Švorčík, “Antibacterial properties of green-synthesized noble metal nanoparticles,” Materials Letters, vol. 113, pp. 59–62, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. P. Dauthal and M. Mukhopadhyay, “In-vitro free radical scavenging activity of biosynthesized gold and silver nanoparticles using Prunus armeniaca (apricot) fruit extract,” Journal of Nanoparticle Research, vol. 15, article 1366, 2012. View at Publisher · View at Google Scholar
  28. P. Ionita, F. Spafiu, and C. Ghica, “Dual behavior of gold nanoparticles, as generators and scavengers for free radicals,” Journal of Materials Science, vol. 43, no. 19, pp. 6571–6574, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Zhang, H. He, W.-J. Gao, S.-Y. Lu, Y. Liu, and H.-Y. Gu, “Rapid adhesion and proliferation of keratinocytes on the gold colloid/chitosan film scaffold,” Materials Science and Engineering: C, vol. 29, pp. 908–912, 2009. View at Google Scholar
  30. S. A. Grant, C. R. Deeken, S. R. Hamilton, D. A. Grant, S. L. Bachman, and B. J. Ramshaw, “A comparative study of the remodeling and integration of a novel AuNP-tissue scaffold and commercial tissue scaffolds in a porcine model,” Journal of Biomedical Materials Research Part A, vol. 101, no. 10, pp. 2778–2787, 2013. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  31. C. R. Deeken, M. Esebua, S. L. Bachman, B. J. Ramshaw, and S. A. Grant, “Assessment of the biocompatibility of two novel, bionanocomposite scaffolds in a rodent model,” Journal of Biomedical Materials Research Part B: Applied Biomaterials, vol. 96, no. 2, pp. 351–359, 2011. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  32. C. R. Deeken, M. J. Cozad, S. L. Bachman, B. J. Ramshaw, and S. A. Grant, “Characterization of bionanocomposite scaffolds comprised of amine-functionalized single-walled carbon nanotubes crosslinked to an acellular porcine tendon,” Journal of Biomedical Materials Research: Part A, vol. 96, no. 3, pp. 584–594, 2011. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. C. R. Deeken, S. L. Bachman, B. J. Ramshaw, and S. A. Grant, “Characterization of bionanocomposite scaffolds comprised of mercaptoethylamine-functionalized gold nanoparticles crosslinked to acellular porcine tissue,” Journal of Materials Science: Materials in Medicine, vol. 23, no. 2, pp. 537–546, 2012. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  34. C. R. Deeken, D. B. Fox, S. L. Bachman, B. J. Ramshaw, and S. A. Grant, “Characterization of bionanocomposite scaffolds comprised of amine-functionalized gold nanoparticles and silicon carbide nanowires crosslinked to an acellular porcine tendon,” Journal of Biomedical Materials Research Part B: Applied Biomaterials, vol. 97, no. 2, pp. 334–344, 2011. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  35. M. J. Cozad, S. L. Bachman, and S. A. Grant, “Assessment of decellularized porcine diaphragm conjugated with gold nanomaterials as a tissue scaffold for wound healing,” Journal of Biomedical Materials Research Part A, vol. 99, no. 3, pp. 426–434, 2011. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. J. E. Valentin, J. S. Badylak, G. P. McCabe, and S. F. Badylak, “Extracellular matrix bioscaffolds for orthopaedic applications: a comparative histologic study,” Journal of Bone and Joint Surgery: Series A, vol. 88, no. 12, pp. 2673–2686, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. L. Pauzenberger, S. Syré, and M. Schurz, “‘Ligamentization’ in hamstring tendon grafts after anterior cruciate ligament reconstruction: a systematic review of the literature and a glimpse into the future,” Arthroscopy, vol. 29, no. 10, pp. 1712–1721, 2013. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. J. M. Anderson, A. Rodriguez, and D. T. Chang, “Foreign body reaction to biomaterials,” Seminars in Immunology, vol. 20, no. 2, pp. 86–100, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. G. Golomb, F. J. Schoen, M. S. Smith, J. Linden, M. Dixon, and R. J. Levy, “The role of glutaraldehyde-induced cross-links in calcification of bovine pericardium used in cardiac valve bioprostheses,” The American Journal of Pathology, vol. 127, no. 1, pp. 122–130, 1987. View at Google Scholar · View at Scopus
  40. M. T. Bailey, S. Pillarisetti, H. Xiao, and N. R. Vyavahare, “Role of elastin in pathologic calcification of xenograft heart valves,” Journal of Biomedical Materials Research Part A, vol. 66, no. 1, pp. 93–102, 2003. View at Google Scholar · View at Scopus
  41. A. Singla and C. H. Lee, “Effect of elastin on the calcification rate of collagen-elastin matrix systems,” Journal of Biomedical Materials Research, vol. 60, no. 3, pp. 368–374, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  42. W. F. Daamen, S. T. M. Nillesen, T. Hafmans, J. H. Veerkamp, M. J. A. van Luyn, and T. H. van Kuppevelt, “Tissue response of defined collagen-elastin scaffolds in young and adult rats with special attention to calcification,” Biomaterials, vol. 26, no. 1, pp. 81–92, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. S. E. P. New and E. Aikawa, “Role of extracellular vesicles in de novo mineralization: an additional novel mechanism of cardiovascular calcification,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 33, no. 8, pp. 1753–1758, 2013. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  44. K. Shino, B. W. Oakes, S. Horibe, K. Nakata, N. Nakamura, and P. A. Indelicato, “Collagen fibril populations in human anterior cruciate ligament allografts. Electron microscopic analysis,” The American Journal of Sports Medicine, vol. 23, no. 2, pp. 203–209, 1995. View at Publisher · View at Google Scholar · View at Scopus
  45. D. W. Jackson, J. Corsetti, and T. M. Simon, “Biologic incorporation of allograft anterior cruciate ligament replacements,” Clinical Orthopaedics and Related Research, no. 324, pp. 126–133, 1996. View at Google Scholar · View at Scopus
  46. U. Bosch, B. Decker, H. D. Moller, W. J. Kasperczyk, and H. J. Oestern, “Collagen fibril organization in the patellar tendon autograft after posterior cruciate ligament reconstruction. A quantitative evaluation in a sheep model,” The American Journal of Sports Medicine, vol. 23, no. 2, pp. 196–202, 1995. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Higuchi, K. Kawai, M. Yamamoto et al., “A novel enhanced green fluorescent protein-expressing NOG mouse for analyzing the microenvironment of xenograft tissues,” Experimental Animals, vol. 63, no. 1, pp. 55–62, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Jockusch, S. Voigt, and D. Eberhard, “Localization of GFP in frozen sections from unfixed mouse tissues: immobilization of a highly soluble marker protein by formaldehyde vapor,” Journal of Histochemistry & Cytochemistry, vol. 51, no. 3, pp. 401–404, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. J. J. Whyte and R. S. Prather, “Genetic modifications of pigs for medicine and agriculture,” Molecular Reproduction and Development, vol. 78, no. 10-11, pp. 879–891, 2011. View at Publisher · View at Google Scholar · View at PubMed
  50. Y. Lu, J.-D. Kang, S. Li et al., “Generation of transgenic Wuzhishan miniature pigs expressing monomeric red fluorescent protein by somatic cell nuclear transfer,” Genesis, vol. 51, no. 8, pp. 575–586, 2013. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  51. H. Matsunari, M. Onodera, N. Tada et al., “Transgenic-cloned pigs systemically expressing red fluorescent protein, Kusabira-Orange,” Cloning and Stem Cells, vol. 10, no. 3, pp. 313–323, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  52. N. L. Webster, M. Forni, M. L. Bacci et al., “Multi-transgenic pigs expressing three fluorescent proteins produced with high efficiency by sperm mediated gene transfer,” Molecular Reproduction and Development, vol. 72, no. 1, pp. 68–76, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus