Skip to main content
SpringerLink
Log in

RGD-modified acellular bovine pericardium as a bioprosthetic scaffold for tissue engineering

  • Published:
Journal of Materials Science: Materials in Medicine Aims and scope Submit manuscript

Abstract

Acellular biological tissues, including bovine pericardia (BP), have been proposed as natural biomaterials for tissue engineering. However, small pore size, low porosity and lack of extra cellular matrix (ECM) after native cell extraction directly restrict the seed cell adhesion, migration and proliferation and which is a vital problem for ABP’s application in the tissue engineered heart valve (TEHV). In the present study, we treated acellular BP with acetic acid, which increased the scaffold pore size and porosity and conjugated RGD polypeptides to ABP scaffolds. After 10 days of culture in vitro, the human mesenchymal stem cells (hMSCs) attached the best and proliferated the fastest on RGD-modified acellular scaffolds, and the cell has grown deep into the scaffold. In contrast, a low density of cells attached to the unmodified scaffolds, with few infiltrating into the acellular tissues. These findings support the potential use of modified acellular BP as a scaffold for tissue engineered heart valves.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Lai PH, Chang Y, Chen SC, Wang CC, Liang HC, Chang WC, et al. Acellular biological tissues containing inherent glycosaminoglycans for loading basic fibroblast growth factor promote angiogenesis and tissue regeneration. Tissue Eng. 2006;12(9):2499–508. doi:10.1089/ten.2006.12.2499.

    Article  CAS  PubMed  Google Scholar 

  2. Schmidt CE, Baier JM. Acellular vascular tissues: natural biomaterials for tissue repair and tissue engineering. Biomaterials. 2000;21(22):2215–31. doi:10.1016/S0142-9612(00)00148-4.

    Article  CAS  PubMed  Google Scholar 

  3. Guldner NW, Jasmund I, Zimmermann H, Heinlein M, Girndt B, Meier V, et al. Detoxification and endothelialization of glutaraldehyde-fixed bovine pericardium with titanium coating: a new technology for cardiovascular tissue engineering. Circulation. 2009;119(12):1653–60. doi:10.1161/CIRCULATIONAHA.108.823948.

    Article  CAS  PubMed  Google Scholar 

  4. Chang Y, Tsai CC, Liang HC, Sung HW. In vivo evaluation of cellular and acellular bovine pericardia fixed with a naturally occurring crosslinking agent (genipin). Biomaterials. 2002;23(12):2447–57. doi:10.1016/S0142-9612(01)00379-9.

    Article  CAS  PubMed  Google Scholar 

  5. Courtman DW, Pereira CA, Kashef V, McComb D, Lee JM, Wilson GJ. Development of a pericardial acellular matrix biomaterial: biochemical and mechanical effects of cell extraction. J Biomed Mater Res. 1994;28(6):655–66. doi:10.1002/jbm.820280602.

    Article  CAS  PubMed  Google Scholar 

  6. Hodde J. Naturally occurring scaffolds for soft tissue repair and regeneration. Tissue Eng. 2002;8(2):295–308. doi:10.1089/107632702753725058.

    Article  CAS  PubMed  Google Scholar 

  7. Elizabeth DH. Cell biology of extracellular matrix. New York: Plenum Press; 1991.

    Google Scholar 

  8. Stringer SE, Gallagher JT. Heparan sulphate. Int J Biochem Cell Biol. 1997;29(5):709–14. doi:10.1016/S1357-2725(96)00170-7.

    Article  CAS  PubMed  Google Scholar 

  9. Wei HJ, Liang HC, Lee MH, Huang YC, Chang Y, Sung HW. Construction of varying porous structures in acellular bovine pericardia as a tissue-engineering extracellular matrix. Biomaterials. 2005;26(14):1905–13. doi:10.1016/j.biomaterials.2004.06.014.

    Article  CAS  PubMed  Google Scholar 

  10. Li J, Mak AFT. Transfer of collagen coating from porogen to scaffold: Collagen coating within poly(DL-lactic-co-glycolic acid) scaffold. Compos. B. 2007;38:317–23. doi:10.1016/j.compositesb.2006.06.009.

    Article  Google Scholar 

  11. Pierschbacher MD, Ruoslahti E. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature. 1984;309:30–3. doi:10.1038/309030a0.

    Article  CAS  PubMed  ADS  Google Scholar 

  12. Cutler SM, Garcia AJ. Engineering cell adhesive surfaces that direct integrin alpha5beta1 binding using a recombinant fragment of fibronectin. Biomaterials. 2003;24(10):1759–70. doi:10.1016/S0142-9612(02)00570-7.

    Article  CAS  PubMed  Google Scholar 

  13. Jang JH, Hwang JH, Chung CP. Production of recombinant human tenascin-C module containing a cell adhesion recognition motif of RGD. Biotechnol Lett. 2004;26(24):1831–5. doi:10.1007/s10529-004-6031-5.

    Article  CAS  PubMed  Google Scholar 

  14. Chen CS, Alonso JL, Ostuni E, Whitesides GM, Ingber DE. Cell shape provides global control of focal adhesion assembly. Biochem Biophys Res Commun. 2003;307(2):355–61. doi:10.1016/S0006-291X(03)01165-3.

    Article  CAS  PubMed  Google Scholar 

  15. Hersel U, Dahmen C, Kessler H. RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials. 2003;24(24):4385–415. doi:10.1016/S0142-9612(03)00343-0.

    Article  CAS  PubMed  Google Scholar 

  16. Rammelt S, Illert T, Bierbaum S, Scharnweber D, Zwipp H, Schneiders W. Coating of titanium implants with collagen, RGD peptide and chondroitin sulfate. Biomaterials. 2006;27(32):5561–71. doi:10.1016/j.biomaterials.2006.06.034.

    Article  CAS  PubMed  Google Scholar 

  17. Sutherland FW, Perry TE, Yu Y, Sherwood MC, Rabkin E, Masuda Y, et al. From stem cells to viable autologous semilunar heart valve. Circulation. 2005;111(21):2783–91. doi:10.1161/CIRCULATIONAHA.104.498378.

    Article  PubMed  Google Scholar 

  18. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005;105(4):1815–22. doi:10.1182/blood-2004-04-1559.

    Article  CAS  PubMed  Google Scholar 

  19. Young B HJ. Wheater’s functional histology. New York: Churchill Livingstone; 2000.

    Google Scholar 

  20. Sandberg LB, Soskel NT, Leslie JG. Elastin structure, biosynthesis, and relation to disease states. N Engl J Med. 1981;304(10):566–79.

    CAS  PubMed  Google Scholar 

  21. Martin I, Shastri VP, Padera RF, Yang J, Mackay AJ, Langer R, et al. Selective differentiation of mammalian bone marrow stromal cells cultured on three-dimensional polymer foams. J Biomed Mater Res. 2001;55(2):229–35. doi:10.1002/1097-4636(200105)55:2<229::AID-JBM1009>3.0.CO;2-Q.

    Article  CAS  PubMed  Google Scholar 

  22. Wayne JS, McDowell CL, Willis MC. Long-term survival of regenerated cartilage on a large joint surface. J Rehabil Res Dev. 2001;38(2):191–200.

    CAS  PubMed  Google Scholar 

  23. Farndale RW, Buttle DJ, Barrett AJ. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta. 1986;883(2):173–7.

    CAS  PubMed  Google Scholar 

  24. Lee JM, Haberer SA, Boughner DR. The bovine pericardial xenograft: I. Effect of fixation in aldehydes without constraint on the tensile viscoelastic properties of bovine pericardium. J Biomed Mater Res. 1989;23(5):457–75. doi:10.1002/jbm.820230502.

    Article  CAS  PubMed  Google Scholar 

  25. Simionescu D, Simionescu A, Deac R. Mapping of glutaraldehyde-treated bovine pericardium and tissue selection for bioprosthetic heart valves. J Biomed Mater Res. 1993;27(6):697–704. doi:10.1002/jbm.820270602.

    Article  CAS  PubMed  Google Scholar 

  26. Sung HW, Chang Y, Chiu CT, Chen CN, Liang HC. Crosslinking characteristics and mechanical properties of a bovine pericardium fixed with a naturally occurring crosslinking agent. J Biomed Mater Res. 1999;47(2):116–26. doi:10.1002/(SICI)1097-4636(199911)47:2<116::AID-JBM2>3.0.CO;2-J.

    Article  CAS  PubMed  Google Scholar 

  27. Chen J, Altman GH, Karageorgiou V, Horan R, Collette A, Volloch V, et al. Human bone marrow stromal cell and ligament fibroblast responses on RGD-modified silk fibers. J Biomed Mater Res A. 2003;67(2):559–70. doi:10.1002/jbm.a.10120.

    Article  PubMed  Google Scholar 

  28. Krupnick AS, Kreisel D, Engels FH, Szeto WY, Plappert T, Popma SH, et al. A novel small animal model of left ventricular tissue engineering. J Heart Lung Transplant. 2002;21(2):233–43. doi:10.1016/S1053-2498(01)00349-7.

    Article  PubMed  Google Scholar 

  29. Matsuda T, Nakayama Y. Surface microarchitectural design in biomedical applications: in vitro transmural endothelialization on microporous segmented polyurethane films fabricated using an excimer laser. J Biomed Mater Res. 1996;31(2):235–42. doi:10.1002/(SICI)1097-4636(199606)31:2<235::AID-JBM10>3.0.CO;2-K.

    Article  CAS  PubMed  Google Scholar 

  30. Nehrer S, Breinan HA, Ramappa A, Young G, Shortkroff S, Louie LK, et al. Matrix collagen type and pore size influence behaviour of seeded canine chondrocytes. Biomaterials. 1997;18(11):769–76. doi:10.1016/S0142-9612(97)00001-X.

    Article  CAS  PubMed  Google Scholar 

  31. Kim BS, Baez CE, Atala A. Biomaterials for tissue engineering. World J Urol. 2000;18(1):2–9. doi:10.1007/s003450050002.

    Article  CAS  PubMed  Google Scholar 

  32. Mirani RD, Pratt J, Iyer P, Madihally SV. The stress relaxation characteristics of composite matrices etched to produce nanoscale surface features. Biomaterials. 2009;30(5):703–10. doi:10.1016/j.biomaterials.2008.10.023.

    Article  CAS  PubMed  Google Scholar 

  33. Ruoslahti E, Pierschbacher MD. New perspectives in cell adhesion: RGD and integrins. Science. 1987;238(4826):491–7. doi:10.1126/science.2821619.

    Article  CAS  PubMed  ADS  Google Scholar 

  34. Burdick JA, Anseth KS. Photoencapsulation of osteoblasts in injectable RGD-modified PEG hydrogels for bone tissue engineering. Biomaterials. 2002;23(22):4315–23. doi:10.1016/S0142-9612(02)00176-X.

    Article  CAS  PubMed  Google Scholar 

  35. Massia SP, Hubbell JA. Human endothelial cell interactions with surface-coupled adhesion peptides on a nonadhesive glass substrate and two polymeric biomaterials. J Biomed Mater Res. 1991;25(2):223–42. doi:10.1002/jbm.820250209.

    Article  CAS  PubMed  Google Scholar 

  36. Beuvelot J, Portet D, Lecollinet G, Moreau MF, Basle MF, Chappard D, et al. In vitro kinetic study of growth and mineralization of osteoblast-like cells (Saos-2) on titanium surface coated with a RGD functionalized bisphosphonate. J Biomed Mater Res B Appl Biomater. 2009.

  37. Lin YC, Brayfield CA, Gerlach JC, Rubin JP, Marra KG. Peptide modification of polyethersulfone surfaces to improve adipose-derived stem cell adhesion. Acta Biomater. 2009;5(5):1416–24. doi:10.1016/j.actbio.2008.11.031.

    Article  CAS  PubMed  Google Scholar 

  38. Chichester CO, Fernandez M, Minguell JJ. Extracellular matrix gene expression by human bone marrow stroma and by marrow fibroblasts. Cell Adhes Commun. 1993;1(2):93–9. doi:10.3109/15419069309095685.

    Article  CAS  PubMed  Google Scholar 

  39. Bashey RI, Torii S, Angrist A. Age-related collagen and elastin content of human heart valves. J Gerontol. 1967;22(2):203–8.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant from National Natural Science Foundation of China (No. 30672086, NO. 30600137) and National High-tech Research and Development Program (863 Program) of China (No. 2006AA02A138).

Author information

Authors and Affiliations

  1. Institute of Cardiovascular Surgery, Xijing Hospital, The Fourth Military Medical University, 17 Changle Western Road, Xi’an, Shaanxi Province, 710032, People’s Republic of China

    Xiaochao Dong, Xufeng Wei, Wei Yi, Chunhu Gu, Xiaojun Kang, Yang Liu, Qiang Li & Dinghua Yi

Authors
  1. Xiaochao Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xufeng Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wei Yi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chunhu Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiaojun Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Qiang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Dinghua Yi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dinghua Yi.

Additional information

Xiaochao Dong and Xufeng Wei contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dong, X., Wei, X., Yi, W. et al. RGD-modified acellular bovine pericardium as a bioprosthetic scaffold for tissue engineering. J Mater Sci: Mater Med 20, 2327–2336 (2009). https://doi.org/10.1007/s10856-009-3791-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10856-009-3791-4

Keywords

Search

Navigation