Abstract
Pericardial tissue has been used to construct bioprostheses employed in the repair of different kinds of injuries, mostly cardiac. However, calcification and mechanical failure have been the main causes of the limited durability of cardiac bioprostheses constructed with bovine pericardium. In the course of this work, a study was conducted on porcine fibrous pericardium, its microscopic structure and biochemical nature. The general morphology and architecture of collagen were studied under conventional light and polarized light microscopy. The biochemical study of the pericardial matrix was conducted according to the following procedures: swelling test, hydroxyproline and collagen dosage, quantification of amino acids in soluble collagen, component extraction of the extracellular matrix of the right and left ventral regions of pericardium with different molarities of guanidine chloride, protein and glycosaminoglycan (GAG) dosage, sodium dodecyl sulfate-polyacrylamide gel electrophoresis and total GAG analysis. Microscopic analysis showed collagen fibers arranged in multidirectionally oriented layers forming a closely knit web, with a larger number of fibers obliquely oriented, initiating at the lower central region toward the upper left lateral relative to the heart. No qualitative differences were found between proteins extracted from the right and left regions. Likewise, no differences were found between fresh and frozen material. Protein dosages from left frontal and right frontal pericardium regions showed no significant differences. The quantities of extracted GAGs were too small for detection by the method used. Enzymatic digestion and electrophoretic analysis showed that the GAG found is possibly dermatan sulfate. The proteoglycan showed a running standard very similar to the small proteoglycan decorin.
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References
Ault NK, Hoffman AH (1992) A composite micromechanical model for connective tissues: Part II. Application to rat tail tendon and joint capsule. J Biomech Eng 114:137–141
Barros PSM, Safatle AMV, Rigueiro M (1999) Experimental lamellar corneal graft in dogs using preserved equine pericardium. Braz J Vet Res Anim Sci 36:71–76
Bashey RI, Bashey HM, Jimenez SA (1978) Characterization of pepsin-solubilized bovine heart-valve collagen. Biochem J 173:885–894
Beeley JG (1985) Glycoprotein and proteoglycan techniques, vol 16. Elsevier, New York, pp 268–270
Blum B, Beier H, Gross HJ (1987) Improved silver staining of plant proteins RNA and DNA in polyacrylamide gels. Electrophoresis 8:93–99
Bradford MM (1976) A rapid sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Ann Biochem 72:248–254
Brown DC, Vogel KG (1989) Characteristics of the in vitro interaction of a small proteoglycan (PGII) of bovine tendon type I collagen. Matrix 9:468–479
Chanda J, Kuribayashi R, Abe T (1997) Use of glutaraldehyde-chitosan treated porcine pericardium as a pericardial substitute. Biomaterials 17:1087–1091
Dietrich CP, Dietrich SM (1976) Electrophoretic behaviour of acidic mucopolysaccharides in diamine buffers. Anal Biochem 70:645–647
Farndale RW, Buttle DJ, Barret AJ (1986) Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochem Biophys Acta 883:173–177
Fentie IH, Allen DJ, Schenck MH, Didio LJA (1986) Comparative electron microscopic study of bovine, porcine and human parietal pericardium, as materials for cardiac valve bioprostheses. J Submicrosc Cytol 18:53–65
Fisher LW (1999) Decorin. In: Kreis T, Vale R (eds) Extracellular matrix, anchor and adhesion proteins. Oxford University Press, New York, pp 241–254
Gathercole LJ, Keller A (1991) Crimp morphology in fibre-forming collagens. Matrix 11:214–234
Grodzinsky AJ (1983) Electrochemical and physicochemical properties of connective tissue. CRC Crit Rev Biomed Eng 9:133–199
Heinegård D, Pimentel ER (1992) Cartilage matrix proteins. In: Kuttner KE, Scheleyerbach R, Peyron JG, Hascall VC (eds) Articular cartilage and osteoarthritis. Raven Press, New York, pp 95–111
Heinegård D, Sommarin Y (1987) Proteoglycan: an overview. Methods Enzymol 144:319–373
Hollinshead WH (1980) O sistema circulatório. In: Hollishead WH (ed) Livro texto de anatomia humana. Harper & Row do Brasil, São Paulo, pp 82–83
Iozzo RV (1997) The family of the small leucine-rich proteoglycans: key regulators of matrix assembly and cellular growth. Crit Rev Biochem Mol Biol 32:141–174
Jorge-Herrero E, Fernandez P, Turnay J, Olmo N, Calero P, Garcia R, Freile I, Castillo-Olivares JL (1999) Influence of different chemical cross-linking treatment on the properties of bovine pericardium and collagen. Biomaterials 20:539–545
Khor E (1997) Methods for the treatment of collagenous tissues for bioprostheses. Biomaterials 18:95–105
Klaus W, Osborn M (1969) The reliability of molecular weight determinations by dodecyl sulfate-polyacrylamide gel electrophoresis. J Biol Chem 244:4406–4412
Koob TJ, Vogel KG (1987) Site-related variations in glycosaminoglycan content and swelling properties of bovine flexor tendon. J Orthop Res 5:414–424
Kuc IM, Scott PG (1997) Increased diameters of collagen fibrils precipitated in vitro in the presence of decorin from various connective tissues. Connect Tissue Res 36:287–296
Laemmli VK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage Ty. Nature 227:680–685
Langdon SE, Chernecky R, Pereira DA, Lee JM (1999) Biaxial mechanical/structural effects of biaxial strain during crosslinking of bovine pericardial xenograft materials. Biomaterials 20:137–153
Loke WK, Khor E, Wee A, Teoh SH, Chian KS (1996) Hybrid biomaterials based on the interaction of polyurethane oligomers with porcine pericardium. Biomaterials 17:2163–2172
Michelacci YM, Horton DSPQ (1989) Proteoglycans from the cartilage of young hammerhead shark Sphyrna lewini. Comp Biochem Physiol 92:651–658
Moore KL, Dalley AF (2001) Torax. In: Moore KL, Dalley AF (eds) Anatomia orientada para a clínica, 4th ed. Rio de Janeiro, Guanabara Koogan, pp 52–151
Olmos ZR, Jasso VR, Sotres VA, Cedillo LI, Arreola RJL, Gaxiola GM (1997) Utilidad del pericárdio bovino tratado com glutaraldeido em lãs resecciones pulmonares no anatômicas em perros. Ver Inst Nal Enf Resp Mex 10:155–159
Petite H, Duval J, Frei V, Abdul-Malak N, Sigot-Luizard M, Herbage D (1995) Cytocompatibility of calf pericardium treated by glutaraldehyde and by the acyl azide methods in an organotypic culture model. Biomaterials 16:1003–1008
Pires AC, Saporito WF, Leao LEV (1997) Pericárdio bovino utilizado como remendo no sistema cardiovascular. Ver Brás Cir Cardivasc 12:176–187
Reddy GK, Gum S, Stehno-Bittel L, Enwemeka CS (1998) Biochemistry and biomechanics of healing tendon: Part I. Effects of rigid plaster casts and functional casts. Med Sci Sports Exerc 30:794–800
Riley GP, Harrall RL, Constant CR, Chard MD, Cawston TE, Hazleman BL (1994) Tendon degeneration and chronic shoulder pain: changes in the collagen composition of the human rotator cuff tendons in rotator cuff tendinitis. Ann Rheum Dis 53:359–366
Sacks MS, Chuong CJC, More R (1994) Collagen fiber architeture of bovine pericardium. ASAIO J 40:M632–M637
Scott JE (1996) Proteodermatan and proteokeratan sulfate (decorin, lumican/ fibromodulin) proteins are horse shoe shaped. Implications for their interactions with collagen. Biochemistry 35:8795–8799
Simionescu D, Iozzo R, Kefalides NA (1989) Bovine pericardial proteoglycan: biochemical, immunochemical and ultrastructural studies. Matrix 9:301–310
Slack C, Flint MH, Thompson BM (1984) The effect of tensional load on isolated embryonic chick tendons in organ culture. Connect Tissue Res 12:229–247
Stegemann H, Stalder K (1967) Determination of hydroxyproline. Clin Chim Acta 18:267–273
Stehno-Bittel L, Reddy GK, Gum S, Enwemeka CS (1998) Biochemistry and biomechanics of healing tendon: Part I. Effects of rigid plaster casts and functional casts. Med Sci Sports Exerc 30:788–793
Urban JPG, Maroudas A, Bayliss MT, Dillon MT (1979) Swelling pressures of proteoglycans at concentrations found in cartilaginous tissues. Biorheology 16:447–464
Vidal BC (1966) Macromolecular disorientation in detached tendons. Protoplasma Bd 62:121–131
Vidal BC (1980) The part played by proteoglycans and structural glycoproteins in the macromolecular orientation of collagen bundles. Cell Mol Biol 26:415–421
Vidal BC (1984) Ordem molecular y haces de colageno. Trab Inst Cajal 75:19–27
Vidal BC (1987) Métodos em Biologia Celular. In: Vidal BC, Mello MLS (eds) Biologia Celular. São Paulo, Atheneu, pp 5–34
Vidal BC (1995) From collagen type I solution to fibers with a helical pattern: a self-assembly phenomenon. C R Acad Sci Paris 318:831–836
Vidal BC (2003) Image analysis of tendon helical superstructure using interference and polarized light microscopy. Micron 34:423–432
Vidal BC, Mello MLS (1972) Anisotropic properties of toluidine blue-stained collagen. Ann Histochim 18:106–122
Viswanadham RK, Agrawd DC, Kramer E (1976) Environmental effects on the mechanical properties of reconstituted collagen hollow fiber membranes. J Poly Sci Phys 14:2195–2209
Whittaker P, Boughner DR, Perkins DG, Canham PB (1987) Quantitative structural analysis of collagen in chordae tendineae and its relation to floppy mitral valves and proteoglycan infiltration. Br Heart 57:264–269
Yannas IV, Grodzinsky AJ (1973) Electromechanical energy conversion with collagen fibers in an aqueous medium. J Mechanochem Cell Motility 2:113–125
Zingales B (1984) Analysis of protein sodium dodecyl sulphate-polyacrylamide gel electrophoresis. In: Genes and antigens of parasites. Rio de Janeiro, Fiocruz, pp 357–363
Acknowledgement
This study was financially supported by CAPES: Coordenação de Aperfeiçoamento de Pessoal do Ensino Superior, FAPESP: Fundação de Amparo à Pesquisa de São Paulo and FAPEMIG: Fundação de Apoio à Pesquisa de Minas Gerais, Brazil.
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Braga-Vilela, A.S., Pimentel, E.R., Marangoni, S. et al. Extracellular Matrix of Porcine Pericardium: Biochemistry and Collagen Architecture. J Membrane Biol 221, 15–25 (2008). https://doi.org/10.1007/s00232-007-9081-5
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DOI: https://doi.org/10.1007/s00232-007-9081-5