Table of Contents Author Guidelines Submit a Manuscript
Biochemistry Research International
Volume 2012, Article ID 979351, 10 pages
http://dx.doi.org/10.1155/2012/979351
Research Article

Fine Structure of Glycosaminoglycans from Fresh and Decellularized Porcine Cardiac Valves and Pericardium

1Dipartimento di Scienze Fisiologiche, Biochimiche e Cellulari, Università di Sassari, Viale Muroni 25, 07100 Sassari, Italy
2Dipartimento di Scienze Cardiologiche, Toraciche e Vascolari, Università di Padova, Viale Giustiniani 2, 35128 Padova, Italy
3Dipartimento di Scienze Biomediche Sperimentali, Università di Padova, Viale G. Colombo 3, 35131 Padova, Italy

Received 30 June 2011; Revised 18 October 2011; Accepted 27 October 2011

Academic Editor: Laura Alaniz

Copyright © 2012 Antonio Cigliano 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. P. Human and P. Zilla, “Inflammatory and immune processes: the neglected villain of bioprosthetic degeneration?” Journal of Long-Term Effects of Medical Implants, vol. 11, no. 3-4, pp. 199–220, 2001. View at Google Scholar · View at Scopus
  2. M. Briand, P. Pibarot, J. P. Després et al., “Metabolic syndrome is associated with faster degeneration of bioprosthetic valves,” Circulation, vol. 114, no. 1, supplement, pp. I512–I517, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. T. C. Flanagan and A. Pandit, “Living artificial heart valve alternatives: a review,” European Cells and Materials, vol. 6, pp. 28–45, 2003. View at Google Scholar · View at Scopus
  4. S. H. Goldbarg, S. Elmariah, M. A. Miller, and V. Fuster, “Insights into degenerative aortic valve disease,” Journal of the American College of Cardiology, vol. 50, no. 13, pp. 1205–1213, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. I. Vesely, “Heart valve tissue engineering,” Circulation Research, vol. 97, no. 8, pp. 743–755, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. M. S. Sacks, F. J. Schoen, and J. E. Mayer, “Bioengineering challenges for heart valve tissue engineering,” Annual Review of Biomedical Engineering, vol. 11, pp. 289–313, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Rothenburger, W. Volker, P. Vischer, B. Glasmacher, H. H. Scheld, and M. Deiwick, “Ultrastructure of proteoglycans in tissue-engineered cardiovascular structures,” Tissue Engineering, vol. 8, no. 6, pp. 1049–1056, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. K. J. Grande-Allen, A. Clabro, V. Gupta, T. N. Wight, V. C. Hascall, and I. Vesely, “Glycosaminoglycans and proteoglycans in normal mitral valve leaflets and chordae: association with regions of tensile and compressive loading,” Glycobiology, vol. 14, no. 7, pp. 621–633, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. E. H. Stephens, C. K. Chu, and K. J. Grande-Allen, “Valve proteoglycan content and glycosaminoglycan fine structure are unique to microstructure, mechanical load and age: relevance to an age-specific tissue-engineered heart valve,” Acta Biomaterialia, vol. 4, no. 5, pp. 1148–1160, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. M. G. Kinsella, S. L. Bressler, and T. N. Wight, “The regulated synthesis of versican, decorin, and biglycan: extracellular matrix proteoglycans that influence cellular phenotype,” Critical Reviews in Eukaryotic Gene Expression, vol. 14, no. 3, pp. 203–234, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. K. R. Taylor and R. L. Gallo, “Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation,” FASEB Journal, vol. 20, no. 1, pp. 9–22, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. F. J. Schoen and R. J. Levy, “Tissue heart valves: current challenges and future research perspectives,” Journal of Biomedical Materials Research, vol. 47, no. 4, pp. 439–465, 1999. View at Publisher · View at Google Scholar · View at Scopus
  13. N. R. Vyavahare, M. Ogle, F. J. Schoen et al., “Mechanisms of bioprosthetic heart valve failure: fatigue causes collagen denaturation and glycosaminoglycan loss,” Journal of Biomedical Materials Research, vol. 46, no. 1, pp. 44–50, 1999. View at Publisher · View at Google Scholar · View at Scopus
  14. J. J. Lovekamp, D. T. Simionescu, J. J. Mercuri, B. Zubiateb, M. S. Sacksb, and N. R. Vyavahare, “Stability and function of glycosaminoglycans in porcine bioprosthetic heart valves,” Biomaterials, vol. 27, no. 8, pp. 1507–1518, 2006. View at Google Scholar
  15. D. T. Simionescu, J. J. Lovekamp, and N. R. Vyavahare, “Glycosaminoglycan-degrading enzymes in porcine aortic heart valves: implications for bioprosthetic heart valve degeneration,” Journal of Heart Valve Disease, vol. 12, no. 2, pp. 217–225, 2003. View at Google Scholar · View at Scopus
  16. D. T. Simionescu, J. J. Lovekamp, and N. R. Vyavahare, “Degeneration of bioprosthetic heart valve cusp and wall tissues is initiated during tissue preparation: an ultrastructural study,” Journal of Heart Valve Disease, vol. 12, no. 2, pp. 226–234, 2003. View at Google Scholar · View at Scopus
  17. K. J. Grande-Allen, W. J. Mako, A. Calabro, Y. Shi, N. B. Ratliff, and I. Vesely, “Loss of chondroitin 6-sulfate and hyaluronan from failed porcine bioprosthetic valves,” Journal of Biomedical Materials Research A, vol. 65, no. 2, pp. 251–259, 2003. View at Google Scholar · View at Scopus
  18. K. J. Grande-Allen, N. Osman, M. L. Ballinger, H. Dadlani, S. Marasco, and P. J. Little, “Glycosaminoglycan synthesis and structure as targets for the prevention of calcific aortic valve disease,” Cardiovascular Research, vol. 76, no. 1, pp. 19–28, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Dainese, F. Barili, V. K. Topkara et al., “Effect of cryopreservation techniques on aortic valve glycosaminoglycans,” Artificial Organs, vol. 30, no. 4, pp. 259–264, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Torii, R. I. Banshey, and K. Nakao, “Acid Mucopolysaccharide composition of human heart valve,” Biochim Biophys Acta, vol. 101, no. 3, pp. 285–291, 1965. View at Google Scholar
  21. A. Moretti and M. W. Whitehouse, “Changes in the mucopolysaccharide composition of bovine heart valves with age,” Biochemical Journal, vol. 87, no. 2, pp. 396–402, 1963. View at Google Scholar
  22. S. Sell and R. E. Scully, “Aging changes in the aortic and mitral valves: histologic and histochemical studies with observations on calcific aortic stenosis and calcification of the mitral annulus,” The American Journal of Pathology, vol. 46, pp. 345–365, 1965. View at Google Scholar · View at Scopus
  23. G. S. Kuschen, F. Coulin, C. A. Power et al., “Glycosaminoglycans interact selectively with chemokines and modulate receptor binding and cellular responses,” Biochemistry, vol. 38, no. 39, pp. 12959–12968, 1999. View at Publisher · View at Google Scholar · View at Scopus
  24. R. J. Linhardt and T. Toida, “Role of glycosaminoglycans in cellular communication,” Accounts of Chemical Research, vol. 37, no. 7, pp. 431–438, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. I. Wille, A. Rek, E. Krenn, and A. Kungl, “Biophysical investigation of human heparin sulfate D-glucosaminyl 3-O-sulfotransferase-3A: a mutual effect of enzyme oligomerisation and glycosaminoglycan ligand binding,” Biochim Biophys Acta, vol. 1774, no. 11, pp. 1470–1476, 2007. View at Google Scholar
  26. F. Naso, A. Gandaglia, M. Formato et al., “Differential distribution of structural components and hydration in aortic and pulmonary heart valve conduits: impact of detergent-based cell removal,” Acta Biomaterialia, vol. 6, no. 12, pp. 4675–4688, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Spina, F. Ortolani, A. E. Messlemani et al., “Isolation of intact aortic valve scaffolds for heart-valve bioprostheses: extracellular matrix structure, prevention from calcification, and cell repopulation features,” Journal of Biomedical Materials Research A, vol. 67, no. 4, pp. 1338–1350, 2003. View at Google Scholar · View at Scopus
  28. T. Bitter and H. M. Muir, “A modified uronic acid carbazole reaction,” Analytical Biochemistry, vol. 4, no. 4, pp. 330–334, 1962. View at Google Scholar · View at Scopus
  29. A. Calabro, M. Benavides, M. Tammi, V. C. Hascall, and R. J. Midura, “Microanalysis of enzyme digests of hyaluronan and chondroitin/dermatan sulfate by fluorophore-assisted carbohydrate electrophoresis (FACE),” Glycobiology, vol. 10, no. 3, pp. 273–281, 2000. View at Google Scholar · View at Scopus
  30. A. Zinellu, S. Pisanu, E. Zinellu et al., “A novel LIF-CE method for the separation of hyalurnan- and chondroitin sulfate-derived disaccharides: application to structural and quantitative analyses of human plasma low- and high-charged chondroitin sulfate isomers,” Electrophoresis, vol. 28, no. 14, pp. 2439–2447, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. E. G. Karousou, M. Militsopoulou, G. Porta, G. De Luca, V. C. Hascall, and A. Passi, “Polyacrylamide gel electrophoresis of fluorophore-labeled hyaluronan and chondroitin sulfate disaccharides: application to the analysis in cells and tissues,” Electrophoresis, vol. 25, no. 17, pp. 2919–2925, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Iop, V. Renier, F. Naso et al., “The influence of heart valve leaflet matrix characteristics on the interaction between human mesenchymal stem cells and decellularized scaffolds,” Biomaterials, vol. 30, no. 25, pp. 4104–4116, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. S. A. Korossis, C. Booth, H. E. Wilcox et al., “Tissue engineering of cardiac valve prostheses II: biomechanical characterization of decellularized porcine aortic heart valves,” Journal of Heart Valve Disease, vol. 11, no. 4, pp. 463–471, 2002. View at Google Scholar · View at Scopus
  34. P. M. Crapo, T. W. Gilbert, and S. F. Badylak, “An overview of tissue and whole organ decellularization processes,” Biomaterials, vol. 32, no. 12, pp. 3233–3243, 2011. View at Google Scholar
  35. F. Naso, A. Gandaglia, L. Iop, M. Spina, and G. Gerosa, “First quantitative assay of alpha-Gal in soft tissues: presence and distribution of the epitope before and after cell removal from xenogeneic heart valves,” Acta Biomaterialia, vol. 7, no. 4, pp. 1728–1434, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Bartolucci, L. Cellai, M. A. Iannelli et al., “Inhibition of human leukocyte elastase by chemically and naturally oversulfated galactosaminoglycans,” Carbohydrate Research, vol. 276, no. 2, pp. 401–408, 1995. View at Publisher · View at Google Scholar · View at Scopus
  37. E. O. Kozlowski, P. C. Lima, C. P. Vicente et al., “Dermatan sulfate in tunicate phylogeny: order-specific sulfation pattern and the effect of ?4IdoA(2-Sulfate)ß-1?3GalNAc(4-Sulfate)ß-1?] motifs in dermatan sulfate on heparin cofactor II activity,” BMC Biochemistry, vol. 12, article 29, 2011. View at Publisher · View at Google Scholar
  38. J. B. Garcia-Bengoecbea, J. R. Gonzilez-Juanatey, J. Rubio, D. DurHn, and J. Sierra, “Thromboembolism in patients with pericardial valves in the absence of chronic anticoagulation: 12 years’ experience,” European Journal of Cardio-Thoracic Surgery, vol. 5, no. 11, pp. 592–597, 1991. View at Google Scholar
  39. D. Simionescu, R. V. Iozzo, and N. A. Kefalides, “Bovine pericardial proteoglycan: biochemical, immunochemical and ultrastructural studies,” Matrix, vol. 9, no. 4, pp. 301–310, 1989. View at Google Scholar · View at Scopus
  40. J. Liao, E. M. Joyce, and M. S. Sacks, “Effects of decellularization on the mechanical and structural properties of the porcine aortic valve leaflet,” Biomaterials, vol. 29, no. 8, pp. 1065–1074, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. V. Gupta, J. A. Werdenberg, B. D. Lawrence, J. S. Mendez, E. H. Stephens, and K. J. Grande-Allen, “Reversible secretion of glycosaminoglycans and proteoglycans by cyclically stretched valvular cells in 3D culture,” Annals of Biomedical Engineering, vol. 36, no. 7, pp. 1092–1103, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. S. R. Shah and N. R. Vyavahare, “The effect of glycosaminoglycan stabilization on tissue buckling in bioprosthetic heart valves,” Biomaterials, vol. 29, no. 11, pp. 1645–1653, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. V. Gupta, J. E. Barzilla, J. S. Mendez et al., “Abundance and location of proteoglycans and hyaluronan within normal and myxomatous mitral valves,” Cardiovascular Pathology, vol. 18, no. 4, pp. 191–197, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. L. E. M. Cardoso and P. A. S. Mourao, “Glycosaminoglycan fractions from human arteries presenting diverse susceptibilities to atherosclerosis have different binding affinities to plasma LDL,” Arteriosclerosis and Thrombosis, vol. 14, no. 1, pp. 115–124, 1994. View at Google Scholar · View at Scopus
  45. O. M. S. Toledo and P. A. S. Mourao, “Sulfated glycosaminoglycans of human aorta: chondroitin 6-sulfate increase with age,” Biochemical and Biophysical Research Communications, vol. 89, no. 1, pp. 50–55, 1979. View at Google Scholar · View at Scopus
  46. K. Murata and Y. Yokoyama, “Acidic glycosaminoglycans in human atherosclerotic cerebral arterial tissues,” Atherosclerosis, vol. 78, no. 1, pp. 69–79, 1989. View at Google Scholar · View at Scopus
  47. A. D. Theocharis, D. A. Theocharis, G. De Luca, A. Hjerpe, and N. K. Karamanos, “Compositional and structural alterations of chondroitin and dermatan sulfates during the progression of atherosclerosis and aneurysmal dilatation of the human abdominal aorta,” Biochimie, vol. 84, no. 7, pp. 667–674, 2002. View at Publisher · View at Google Scholar · View at Scopus