Biotechnology and Bioprocess Engineering:BBE

The Korean Society for Biotechnology and Bioengineering (한국생물공학회)
권호 표지

Anti-calcification of Bovine Pericardium for Bioprosthetic Heart Valves after Surface Modification with Hyaluronic Acid Derivatives

  • Hahn Sei Kwang (Department of Bioengineering, Box 352255, University of Washington) ;
  • Ohri Rachit (Department of Bioengineering, Box 352255, University of Washington) ;
  • Giachelli Cecilia M. (Department of Bioengineering, Box 352255, University of Washington)
  • Published : 2005.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

Surface modification of glutaraldehyde fixed bovine pericardium (GFBP) was success­fully carried out with hyaluronic acid (HA) derivatives. At first, HA was chemically modified with adipic dihydrazide (ADH) to introduce hydrazide functional group into the carboxyl group of HA backbone. Then, GFBP was surface modified by grafting HA-ADH to the free aldehyde groups on the tissue and the subsequent HA-ADH hydrogel coating. HA-ADH hydrogels could be prepared through selective crosslinking at low pH between hydrazide groups of HA-ADH and crosslinkers containing succinimmidyl moieties with minimized protein denaturation. When HA­ADH hydrogels were prepared at low pH of 4.8 in the presence of erythropoietin (EPO) as a model protein, EPO release was continued up to $85\%$ of total amount of loaded EPO for 4 days. To the contrary, only $30\%$ of EPO was released from HA-ADH hydrogels prepared at pH=7.4, which might be due to the denaturation of EPO during the crosslinking reaction. Because the carboxyl groups on the glucuronic acid residues are recognition sites for HA degradation by hyaluronidase, the HA-ADH hydrogels degraded more slowly than HA hydrogels prepared by the crosslinking reaction of divinyl sulfone with hydroxyl groups of HA. Following a two-week subcutaneous implantation in osteopontin-null mice, clinically significant levels of calcification were observed for the positive controls without any surface modification. However, the calcification of surface modified GFBP with HA-ADH and HA-ADH hydrogels was drastically reduced by more than $85\%$ of the positive controls. The anti-calcification effect of HA surface modification was also confirmed by microscopic analysis of explanted tissue after staining with Alizarin Red S for calcium, which followed the trend as observed with calcium quantification.

Keywords

References

  1. Ohri, R., S. K. Hahn, P. S. Stayton, A. S. Hoffman, and M. Giachelli (2004) Hyaluronic acid grafting mitigates calcification of glutaraldhyde-fixed bovine pericardium. J. Biomed. Mater. Res. 70A: 159-165 https://doi.org/10.1002/jbm.a.30053
  2. Golomb, G., F. J. Schoen, M. S. Smith, J. Linden, M. Dixon, and R. J. Levy (1987) The role of glutaraldehydeinduced cross-links in calcification of bovine pericardium used in cardiac valve bioprostheses. Am. J. Pathol. 127: 122-130
  3. Kim, K. M. (1995) Apoptosis and calcification. Scanning Microscopy 9: 1137-1175
  4. Schoen, F. J. and R. J. Levy (1999) Tissue heart valves: Current challenges and future research perspectives. J. Biomed. Mater. Res. 47: 439-465 https://doi.org/10.1002/(SICI)1097-4636(19991215)47:4<439::AID-JBM1>3.0.CO;2-O
  5. Vyavahare, N., M. Ogle, F. J. Schoen, et al. (1999) Mechanisms of bioprosthetic heart valve failure: Fatigue causes collagen denaturation and glycosaminoglycan loss. J. Biomed. Mater. Res. 46: 44-50 https://doi.org/10.1002/(SICI)1097-4636(199907)46:1<44::AID-JBM5>3.0.CO;2-D
  6. Lovekamp, J. and N. Vyavahare (2001) Periodatemediated glycosaminoglycan stabilization in bioprosthetic heart valves. J. Biomed. Mater. Res. 56: 478-486 https://doi.org/10.1002/1097-4636(20010915)56:4<478::AID-JBM1119>3.0.CO;2-C
  7. Hunter, G. K., K. S. Wong, and J. J. Kim (1988) Binding of calcium to glycosaminoglycans: An equilibrium dialysis study. Arch. Biochem. Biophys. 260: 161-167 https://doi.org/10.1016/0003-9861(88)90437-7
  8. Adrian-Scotto, M., M. Guibbolini, G. Mallet, M. Gaysinski, and D. Vasilescu (2002) $^{23}Na$ NMR study of the interaction between hyaluronan and the bications Ca(++), Mg(++) and Cu(++). J. Biomol. Struct. Dyn. 19: 715-724 https://doi.org/10.1080/07391102.2002.10506778
  9. Chang, N. S. and R. J. Boackle (1985) Hyaluronic acidcomplement interactions-II. Role of divalent cations and gelatin. Mol. Immunol. 22: 843-848 https://doi.org/10.1016/0161-5890(85)90068-9
  10. Vercruysse, K. P., M. R. Ziebell, and G. D. Prestwich (1999) Control of enzymatic degradation of hyaluronan by divalent cations. Carbohydr. Res. 318: 26-37 https://doi.org/10.1016/S0008-6215(99)00087-7
  11. Laurent, T. C. (1998) The Chemistry, Biology and Medical Applications of Hyaluronan and its Derivatives. Wenner- Gren International Series, Vol 72. Portland Press, London, UK
  12. Fraser, J. R., T. C. Laurent, and U. B. Laurent (1997) Hyaluronan: Its nature, distribution, functions and turnover. J. Intern. Med. 242: 27-33 https://doi.org/10.1046/j.1365-2796.1997.00170.x
  13. Fukuda, K., H. Dan, M. Takayama, F. Kumano, M. Saitoh, and S. Tanaka (1996) Hyaluronic acid increases proteoglycan synthesis in bovine articular cartilage in the presence of interleukin-1. J. Pharmacol. Exp. Ther. 277: 1672-1675
  14. Goa, K. L. and P. Benfield (1994) Hyaluronic acid. A review of its pharmacology and use as a surgical aid in ophthalmology, and its therapeutic potential in joint disease and wound healing. Drugs 47: 536-566 https://doi.org/10.2165/00003495-199447030-00009
  15. Balazs, E. A. and J. L. Denlinger (1993) Viscosupplementation: A new concept in the treatment of osteoarthritis. J. Rheumatol. Suppl. 39: 3-9
  16. Balazs, E. A. (1983) Sodium hyaluronate and viscosurgery. pp. 5-28. In: D. Miller and R. Stegmann (eds.). Healon (Sodium Hyaluronate). A Guide to Its Use in Ophthalmic Surgery. Wiley, NY, USA
  17. Balazs, E. A. and A. Leshchiner (1986) Cross-linked gels of hyaluronic acid and products containing such gels. US Patent 4,582,865
  18. Kuo, J. W., D. A. Swann, and G. D. Prestwich (1991) Chemical modification of hyaluronic acid by carbodiimides. Bioconjug. Chem. 2: 232-241 https://doi.org/10.1021/bc00010a007
  19. Illum, L., N. F. Farraj, A. N. Fisher, I. Gill, M. Miglietta, and L. M. Benedetti (1994) Hyaluronic acid ester microspheres as a nasal delivery system. J. Control. Rel. 29: 133-141 https://doi.org/10.1016/0168-3659(94)90129-5
  20. Hahn, K. K. and A. S. Hoffman (2004) Characterization of biocompatible polyelectrolyte complex multiplayer of hyaluronic acid and poly-L-lysin. Biotechnol. Bioprocess Eng. 9: 179-183 https://doi.org/10.1007/BF02942289
  21. Yeo, Y., N. Bae, and K. Park (2001) Microencapsulation methods for delivery of protein drugs. Biotechnol. Bioprocess Eng. 4: 205-212
  22. Shu, X. Z., Y. Liu, F. Palumbo, and G. D. Prestwich (2003) Disulfide-crosslinked hyaluronan-gelatin hydrogel films: A covalent mimic of the extracellular matrix for in vitro cell growth. Biomaterials 24: 3825-3834 https://doi.org/10.1016/S0142-9612(03)00267-9
  23. Hahn, S. K., S. Jelacic, R. V. Maier, P. S. Stayton, and A. S. Hoffman (2004) Anti-inflammatory drug delivery from hyaluronic acid hydrogels. J. Biomat. Sci. Polym. Ed. 15: 1111-1119 https://doi.org/10.1163/1568562041753115
  24. Steitz, S. A., M. Y. Speer, M. D. McKee, et al. (2002) Osteopontin inhibits mineral deposition and promotes regression of ectopic calcification. Am. J. Pathol. 161: 2035-2046 https://doi.org/10.1016/S0002-9440(10)64482-3
  25. Pouyani, T. and G. D. Prestwich (1994) Functionalized derivatives of hyaluronic acid oligosaccharides: Drug carriers and novel biomaterials. Bioconjug. Chem. 5: 339-347 https://doi.org/10.1021/bc00028a010
  26. Bitter, T. and H. Muir (1962) A modified uronic acid carbazole reaction. Anal. Biochem. 4: 330-334 https://doi.org/10.1016/0003-2697(62)90095-7
  27. Liaw, L., D. E. Birk, C. B. Ballas, J. S. Whitsitt, J. M. Davidson, and B. L. Hogan (1998) Altered wound healing in mice lacking a functional osteopontin gene (spp1). J. Clin. Invest. 101: 1468-1478 https://doi.org/10.1172/JCI2131
  28. Bulpitt, P. and D. Aeschlimann (1999) New strategy for chemical modification of hyaluronic acid: Preparation of functionalized derivatives and their use in the formation of novel biocompatible hydrogels. J. Biomed. Mater. Res. 47: 152-169 https://doi.org/10.1002/(SICI)1097-4636(199911)47:2<152::AID-JBM5>3.0.CO;2-I
  29. Hermanson, G. T. (1996) Bioconjugate Techniques. pp. 121. Academic Press, San Diego, USA
  30. Giachelli, C. M. and S. Steitz (2000) Osteopontin: A versatile regulator of inflammation and biomineralization. Matr. Biol. 19: 615-622 https://doi.org/10.1016/S0945-053X(00)00108-6
  31. Lee, W. K., K. D. Park, D. K. Han, H. Suh, J. C. Park, and Y. H. Kim (2000) Heparinized bovine pericardium as a novel cardiovascular bioprosthesis. Biomaterials 21: 2323-2330 https://doi.org/10.1016/S0142-9612(00)00159-9