Application of cellulose-based biomaterials in vascular tissue engineering - a review and our experience

• Autorzy: Bacakova L. , Novotna K. , Parizek M. , Havelka P. , Sopuch T.
• Języki publikacji: EN

Abstrakty

EN

Artificial vascular replacements used in current clinical practice are fabricated from polyethylene terephthalate (PET, e.g. Dacron) orpolyterafluoroethylene (PTFE, e.g. Teflon). Older materials used earlier for constructing vascular prostheses are polyamide (Nylon), polyvinyl alcohol (Ivalon) and polyacrylonitrile (Orlon). New promising materials include polyurethane and a wide range of biodegradable synthetic or nature-derived polymers, which are usually designed as temporary scaffolds for vascular cells forming a new regenerated blood vessel wall (for a review, see [1]). One of the nature-derived polymers is cellulose and its derivatives and composites with other materials. Cellulose is the most abundant biopolymer on Earth. It is a polysaccharide consisting of a linear chain of several hundred to over ten thousand ß(1\to 4) linked D-glucose units [2,3]. Cellulose is the structural component of the primary cell wall of green plants, many forms of algae and the oomycetes. In plant cells, cellulose microfibrils are synthesized at the plasma membrane by hexameric protein complexes, also known as cellulose synthase complexes [4]. Some species of bacteria secrete cellulose to form biofilms. For industrial use, cellulose is mainly obtained from wood pulp and cotton. For tissue engineering applications, bacterial cellulose has been predominantly used, mainly that synthesized by Acetobacterxylinum. Bacterial cellulose is identical to plant cellulose in chemical structure, but it can be produced without contaminant molecules, such as lignin and hemicelluloses, and does not require intensive purification processes. In addition, it is remarkable for its mechanical strength, its ability to be engineered structurally and chemically at nano-, micro-, and macroscales, its biocompatibility and chemical and morphologic controllability [5]. Bacterial cellulose has been used for experimental engineering of bone tissue [6], cartilage [7], skin [8], heart valve [9], and also for urinary reconstruction and diversion [10]. One of the first attempts at vascular tissue engineering was made with cellulose fibers, which were used for constructing three-dimensional vascularized tissue in vitro. These fibers were immobilized with fibronectin in order to improve cell adhesion, and were seeded with bovine coronary artery smooth muscle cells. These cells proliferated on the scaffolds and, after they formed multilayers on the fibers, the fibers were removed by enzymatic digestion using cellulase. The remaining smooth muscle cell aggregates maintained lumens after this procedure, and thus mimicked newly-formed blood vessels [11]. Similarly, three-dimensional nanofibrous scaffolds with micropores made of bacterial cellulose allowed attachment and proliferation of human saphenous vein smooth muscle cells on the surface and also in the inside of the scaffolds [12]. In addition, the mechanical properties of nanofibrous bacterial cellulose scaffolds, evaluated by the shape of the stress-strain response, were reminiscent of the properties of the carotid artery, most probably due to the similarity in architecture of the nanofibril network [13]. The adhesion and growth of vascular endothelial cells was also supported by cellulose-based scaffolds, namely by nanofibrous bacterial cellulose or cellulose acetate scaffolds, especially if these scaffolds were functionalized with RGD-containing oligopeptides, i.e. ligands for integrin adhesion receptors on cells [14, 15], or if they were combined with chitosan [16]. The angiogenic response to bacterial cellulose was also observed under in vivo conditions, i.e. after implantation of these scaffolds in the form of dorsal skinfold chambers into Syrian golden hamsters [17]. Cellulose has also been used for creating tubular structures designed for replacing small-caliber vessels. Hollow-shaped segments of bacterial cellulose were created with a length of 10 mm, an inner diameter of 3.0-3.7 mm and a wall thickness of 0.6 -1.0 mm. These grafts were used to replace the carotid arteries of eight pigs. After a follow-up period of 3 months, seven grafts (87.5%) remained patent, whereas one graft was found to be occluded. All patent grafts developed a single inner layer of endothelium with a basement membrane and a thin layer of collagen, followed by a concentric medial layer containing smooth muscle cells and cellulose, and an outer layer of fibrous cells [18]. Similarly, bacterial cellulose grafts 4 cm in length and 4 mm in internal diameter were implanted bilaterally in the carotid arteries of eight sheep. Although 50% of the grafts occluded within 2 weeks, all patent grafts developed a confluent inner layer of endothelial- like cells [19]. In addition, the mechanical properties of tubular structures created from bacterial cellulose seemed to be advantageous for vascular tissue engineering. For example, these structures exhibited a compliance response similar to that of human saphenous vein [20]. In our experiments, we have concentrated on cellulose-based materials modified with oxidation and/or functionalization with biomolecules. We have prepared fibrous scaffolds made of non-oxidized viscose, dialdehyde cellulose and 6-carboxycellulose with 2.1 wt.% or 6.6 wt.% of -COOH groups. In addition, all these material types were functionalized with arginine, i.e. an amino acid with a basic side chain, or with chitosan, in order to balance (compensate) the relatively acid character of oxidized cellulose molecules. Two groups of samples with and without functionalization were then seeded with vascular smooth muscle cells (VSMC) derived from the rat thoracic aorta by an explantation method [21]. We found that the oxidized cellulose with 2.1 wt.% of-COOH groups was the most appropriate of all the tested materials for colonization with VSMC. The cells on this material achieved an elongated shape, while they were spherical in shape on the other materials. In addition, the numbers of cells obtained in one week after seeding and the concentration of alpha-actin and SM1 and SM2 myosins, measured per mg of protein, were significantly higher on oxidized cellulose with 2.1 wt.% of -COOH groups. Functionalization with arginine and chitosan improved the cell adhesion, but usually only slightly. The most apparent increase in cell number after functionalization was observed on oxidized cellulose with 2.1 wt.% of -COOH groups functionalized with chitosan, and on viscose functionalized with chitosan or arginin. However, the cells on all samples proliferated slowly and with a non-significant increase in cell population densities from day 1 to 7 after seeding. This suggests that cellulose-based materials can be used in applications where high proliferation activity of vascular smooth muscle cells is not desirable. They can therefore be used on vascular prostheses, where excessive VSMC proliferation can lead to the restenosis of the graft. Alternatively, cell proliferation might be enhanced by some other more efficient modification. This would require further research.

Słowa kluczowe

EN

biomaterials; tissue engineering; vascular

• Wydawca: Polish Society for Biomaterials in Cracow
• Czasopismo: Engineering of Biomaterials
• Rocznik: 2012
• Tom: Vol. 15, no. 116-117 spec. iss.
• Strony: 128--130
• Opis fizyczny: Bibliogr. 21 poz.

Twórcy

autor

Bacakova L.

• Dept. of Biomaterials and Tissue Engineering, Institute of Physiology, Academy of Sciences of the Czech Republic, Videnska 1083, 14220 Prague 4 - Krc, Czech Republic

autor

Novotna K.

• Dept. of Biomaterials and Tissue Engineering, Institute of Physiology, Academy of Sciences of the Czech Republic, Videnska 1083, 14220 Prague 4 - Krc, Czech Republic

autor

Parizek M.

• Dept. of Biomaterials and Tissue Engineering, Institute of Physiology, Academy of Sciences of the Czech Republic, Videnska 1083, 14220 Prague 4 - Krc, Czech Republic

autor

Havelka P.

• VUOS a.s., Rybitvi 296, 533 54 Rybitvi, Czech Republic

autor

Sopuch T.

• SBU Nitroceluloza, Synthesia a.s., Pardubice-Semtin, Czech Republic

Bibliografia

• [1] Chlupac J, Filova E, Bacakova L: Physiol Res 58 Suppl 2: S119-139, 2009.
• [2] Mutwil M, Debolt S, Persson S: Curr Opin Plant Biol 11: 252-257, 2008.
• [3] Pooyan P, Tannenbaum R, Garmestani H: J Mech Behav Biomed Mater 7: 50-59, 2012.
• [4] Gu Y, Somerville C: Plant Signal Behav 5: 1571-1574, 2010.
• [5] Petersen N, Gatenholm P: Appl Microbiol Biotechnol 91: 1277-1286, 2011.
• [6] Zaborowska M, Bodin A, Bäckdahl H, Popp J, Goldstein A, Gatenholm P: Acta Biomater 6: 2540-2547, 2010.
• [7] Andersson J, Stenhamre H, Bäckdahl H, Gatenholm P: J Biomed Mater Res A 94: 1124-1132, 2010.
• [8] Kingkaew J, Jatupaiboon N, Sanchavanakit N, Pavasant P, Phisalaphong M: J Biomater Sci Polym Ed 21: 1009-1021, 2010.
• [9] Mohammadi H: Proc Inst Mech Eng H 225: 718-722, 2011.
• [10] Bodin A, Bharadwaj S, Wu S, Gatenholm P, Atala A, Zhang Y: Biomaterials 31: 8889-8901, 2010.
• [11] Ko IK, Iwata H: Ann N Y Acad Sci 944: 443-455, 2001.
• [12] Backdahl H, Esguerra M, Delbro D, Risberg B, Gatenholm P: J Tissue Eng Regen Med 2: 320-330, 2008.
• [13] Backdahl H, Helenius G, Bodin A, Nannmark U, Johansson BR, Risberg B, Gatenholm P: Biomaterials 27: 2141-2149, 2006.
• [14] Bodin A, Ahrenstedt L, Fink H, Brumer H, Risberg B, Gatenholm P: Biomacromolecules 8: 3697-3704, 2007.
• [15] Fink H, Ahrenstedt L, Bodin A, Brumer H, Gatenholm P, Krettek A, Risberg B: J Tissue Eng Regen Med 5: 454-463, 2011.
• [16] Rubenstein D, Han D, Goldgraben S, El-Gendi H, Gouma PI, Frame MD: Microcirculation 14: 723-737, 2007.
• [17] Esguerra M, Fink H, Laschke MW, Jeppsson A, Delbro D, Gatenholm P, Menger MD, Risberg B: J Biomed Mater Res A 93: 140-149, 2010.
• [18] Wippermann J, Schumann D, Klemm D, Kosmehl H, Salehi- Gelani S, Wählers T. Eur J Vasc Endovasc Surg 37: 592-596, 2009.
• [19] Malm CJ, Risberg B, Bodin A, Bäckdahl H, Johansson BR, Gatenholm P, Jeppsson A. Scand Cardiovasc J 46: 57-62, 2012
• [20] Zahedmanesh H, Mackle JN, Sellborn A, Drotz K, Bodin A, Gatenholm P, Lally C: J Biomed Mater Res B Appl Biomater 97: 105-113, 2011.
• [21] Bacakova L, Lisa V, Pellicciari C, Mares V, Bottone MG, Kocourek F: In Vitro Cell Dev Biol Anim 33: 410-413, 1997.

Uwagi

EN

Supported by the Ministry of Industry and Trade of the Czech Republic (grant No. 2A-1TP1/073) and by the Grant Agency of the Czech Republic (grant No. 305/08/0108). Mr. Robin Healey (Czech Technical University, Prague, Czech Republic) is gratefully acknowledged for his language revision of the text.