In vitro characterization of a collagen scaffold enzymatically cross-linked with a tailored elastin-like polymer

Tissue Engineering - Part A

Volumn 15, Issue 4, 2009, Pages 887-899

  Garcia, Yolanda ^a   Hemantkumar, Naik ^a   Collighan, Russell ^b   Griffin, Martin ^c   Rodriguez Cabello, Jose Carlos ^d   Pandit, Abhay ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b ASTON UNIVERSITY   (United Kingdom)

^c NOTTINGHAM TRENT UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF VALLADOLID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION; BIOMECHANICS; BLOOD VESSEL PROSTHESES; CELL ADHESION; CELL CULTURE; CELL MEMBRANES; COLLAGEN; DNA; DNA SEQUENCES; DRUG DELIVERY; ELECTRIC DISCHARGE MACHINING; ENDOTHELIAL CELLS; FRACTURE MECHANICS; FUNCTIONAL POLYMERS; GENETIC ENGINEERING; GLYCOPROTEINS; MECHANICAL PROPERTIES; NUCLEIC ACIDS; SELF ASSEMBLY; STIFFNESS MATRIX; THERMODYNAMIC PROPERTIES; TISSUE;

COLLAGEN SCAFFOLDS; COLLAGEN TISSUE; COLLAGEN-BASED SCAFFOLDS; DIFFERENT STRUCTURE; DOSE-DEPENDENT MANNER; ELASTIC ELEMENT; ELASTIN-LIKE POLYMERS; EXTRACELLULAR MATRICES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; IN-VITRO; IRREVERSIBLE DEFORMATION; MECHANICAL STRENGTH; MICROBIAL TRANSGLUTAMINASE; PHYSICOCHEMICAL PROPERTY; PROTEOLYTIC RESISTANCE; RECOMBINANT DNA; SMOOTH MUSCLE CELLS; SPECIFIC SEQUENCES; STRUCTURAL COMPONENT; TENSILE STIFFNESS; THERMAL BEHAVIORS; THERMAL PROPERTIES;

SCAFFOLDS;

COLLAGEN; ELASTIN; ENZYME; POLYMER; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; RECOMBINANT DNA; BIOMATERIAL; TISSUE SCAFFOLD;

ANIMAL CELL; ARTICLE; CELL ADHESION; COMPARATIVE STUDY; CONTROLLED STUDY; COVALENT BOND; CROSS LINKING; DOSE RESPONSE; DRUG DELIVERY SYSTEM; EMBRYO; ENDOTHELIUM CELL; EVALUATION; FIBROBLAST; HUMAN; HUMAN CELL; IN VITRO STUDY; METHODOLOGY; MOUSE; NONHUMAN; PHYSICAL CHEMISTRY; POROSITY; PRIORITY JOURNAL; PROTEIN DEGRADATION; SMOOTH MUSCLE FIBER; STRENGTH; SYNTHESIS; UMBILICAL VEIN; AMINO ACID SEQUENCE; ANIMAL; ATOMIC FORCE MICROSCOPY; BIOMECHANICS; CELL STRAIN 3T3; CELL SURVIVAL; CHEMISTRY; DRUG EFFECT; INFRARED SPECTROSCOPY; METABOLISM; MOLECULAR GENETICS; THERMODYNAMICS; TISSUE ENGINEERING;

3T3 CELLS; AMINO ACID SEQUENCE; ANIMALS; BIOCOMPATIBLE MATERIALS; BIOMECHANICS; CELL SURVIVAL; COLLAGEN; ELASTIN; HUMANS; MICE; MICROSCOPY, ATOMIC FORCE; MOLECULAR SEQUENCE DATA; POLYMERS; POROSITY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; THERMODYNAMICS; TISSUE ENGINEERING; TISSUE SCAFFOLDS; TRANSGLUTAMINASES;

EID: 67049165509     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2008.0104     Document Type: Article

References (54)

1. Garcia, Y., Collighan, R., Griffin, M., and Pandit, A. Assessment of cell viability in a three-dimensional enzymatically cross-linked collagen scaffold. J Mater Sci Mater Med 18(10), 1991, 2007.
2. Chau, D.Y., Collighan, R.J., Verderio, E.A., Addy, V.L., and Griffin, M. The cellular response to transglutaminase-crosslinked collagen. Biomaterials 26(33), 6518, 2005.
3. Garcia, Y., Wilkins, B., Collighan, R.J., Griffin, M., and Pandit, A. Towards development of a dermal rudiment for enhanced wound healing response. Biomaterials 29(7), 857, 2008.
4. Kloeters, O., Tandara, A., and Mustoe, T.A. Hypertrophic scar model in the rabbit ear: a reproducible model for studying scar tissue behavior with new observations on silicone gel sheeting for scar reduction. Wound Repair Regen 15(s1), S40, 2007.
5. Lenhoff, H.M. The nature of elastin. 2006. Available at http:==www.wsf.org=medical=literature=layreader=elastin .htm.
6. Rodgers, U.R., and Weiss, A.S. Cellular interactions with elastin. Pathol Biol (Paris). 53(7), 390, 2005.
7. Czirok, A., Zach, J., Kozel, B.A., Mecham, R.P., Davis, E.C., and Rongish, B.J. Elastic fiber macro-assembly is a hierarchical, cell motion-mediated process. J Cell Physiol 207(1), 97, 2006.
8. Daamen, W.F., Veerkamp, J.H., van Hest, J.C.M., and van Kuppevelt, T.H. Elastin as a biomaterial for tissue engineering. Biomaterials 28(30), 4378, 2007.
9. Urry, D.W., Hugel, T., Seitz, M., Gaub, H.E., Sheiba, L., Dea, J., Xu, J., and Parker, T. Elastin: a representative ideal protein elastomer. Philos Trans R Soc Lond B Biol Sci 357(1418), 169, 2002.
10. Bellingham, C.M., Woodhouse, K.A., Robson, P., Rothstein, S.J., and Keeley, F.W. Self-aggregation characteristics of recombinantly expressed human elastin polypeptides. Biochimica et Biophysica Acta (BBA)-Protein Struct Mol Enzymol 1550(1), 6, 2001.
11. Keeley, F.W., Bellingham, C.M., andWoodhouse, K.A. Elastin as a self-organizing biomaterial: use of recombinantly expressed human elastin polypeptides as a model for investigations of structure and self-assembly of elastin. Philos Trans R Soc Lond B Biol Sci 357(1418), 185, 2002.
12. Rodriguez-Cabello, J.C., Reguera, J., Girotti, A., Alonso, M., and Testera, A.M. Developing functionality in elastin-like polymers by increasing their molecular complexity: the power of the genetic engineering approach. Prog Polym Sci 30(11), 1119, 2005.
13. Narayanan, A.S., Page, R.C., Kuzan, F., and Cooper, C.G. Elastin cross-linking in vitro. Studies on factors influencing the formation of desmosines by lysyl oxidase action on tropoelastin. Biochem J 173(3), 857, 1978.
14. Debelle, L., Alix, A.J., Jacob, M.P., Huvenne, J.P., Berjot, M., Sombret, B., and Legrand, P. Bovine elastin and kappa-elastin secondary structure determination by optical spectroscopies. J Biol Chem 270(44), 26099, 1995.
15. Robert, L. Cell-elastin interaction and signaling. Pathologie Biologie 53(7), 399, 2005.
16. Mizuno, T., Yau, T.M., Weisel, R.D., Kiani, C.G., and Li, R.K. Elastin stabilizes an infarct and preserves ventricular function. Circulation 112(9 Suppl), 181, 2005.
17. Berglund, J.D., Nerem, R.M., and Sambanis, A. Incorporation of intact elastin scaffolds in tissue-engineered collagenbased vascular grafts. Tissue Eng 10(9-10), 1526, 2004.
18. Buttafoco, L., Engbers-Buijtenhuijs, P., Poot, A.A., Dijkstra, P.J., Vermes, I., and Feijen, J. Physical characterization of vascular grafts cultured in a bioreactor. Biomaterials 27(11), 2380, 2006.
19. Engbers-Buijtenhuijs, P., Buttafoco, L., Poot, A.A., Dijkstra, P.J., de Vos, R.A., Sterk, L.M., Geelkerken, R.H., Vermes, I., and Feijen, J. Biological characterisation of vascular grafts cultured in a bioreactor. Biomaterials 27(11), 2390, 2006.
20. Patel, A., Fine, B., Sandig, M., and Mequanint, K. Elastin biosynthesis: the missing link in tissue-engineered blood vessels. Cardiovasc Res 71(1), 40, 2006.
21. Woodhouse, K.A., Klement, P., Chen, V., Gorbet,M.B., Keeley, F.W., Stahl, R., Fromstein, J.D., and Bellingham, C.M. Investigation of recombinant human elastin polypeptides as non-thrombogenic coatings. Biomaterials 25(19), 4543, 2004.
22. Daamen, W.F., Nillesen, S.T.M., Hafmans, T., Veerkamp, J.H., van Luyn, M.J.A., and van Kuppevelt, T.H. Tissue response of defined collagen-elastin scaffolds in young and adult rats with special attention to calcification. Biomaterials 26(1), 81, 2005.
23. Urry, D.W. Neutral sites for calcium ion binding to elastin and collagen: a charge neutralization theory for calcification and its relationship to atherosclerosis. Proc Natl Acad Sci USA 68(4), 810, 1971.
24. Lee, J.S., Basalyga, D.M., Simionescu, A., Isenburg, J.C., Simionescu, D.T., and Vyavahare, N.R. Elastin calcification in the rat subdermal model is accompanied by up-regulation of degradative and osteogenic cellular responses. Am J Pathol 168(2), 490, 2006.
25. Daamen, W.F., Hafmans, T., Veerkamp, J.H., and van Kuppevelt, T.H. Isolation of intact elastin fibers devoid of microfibrils. Tissue Eng 11(7-8), 1168, 2005.
26. Bellingham, C.M., Lillie, M.A., Gosline, J.M., Wright, G.M., Starcher, B.C., Bailey, A.J., Woodhouse, K.A., and Keeley, F.W. Recombinant human elastin polypeptides self-assemble into biomaterials with elastin-like properties. Biopolymers 70(4), 445, 2003.
27. Debelle, L., and Tamburro, A.M. Elastin: molecular description and function. Int J Biochem Cell Biol 31(2), 261, 1999.
28. Schmelzer, C.E., Getie, M., and Neubert, R.H. Mass spectrometric characterization of human skin elastin peptides produced by proteolytic digestion with pepsin and thermitase. J Chromatogr A 1083(1-2), 120, 2005.
29. Mecham, R.P., and Davis, E.C. Elastic fiber structure and assembly. In: Yurchenco, P.D., Birk, D.E., and Mecham, R.P., eds. Extracellular Matrix Assembly and Structure, Vol. 1. San Diego, CA: Academic Press, 1994, pp. 281-314.
30. Tamburro, A.M. The physical chemistry of elastin: a historical overview. 2002. Available at http:==www.unibas.it =utenti=tamburro=elastin2002.htm.
31. Debelle, L., Alix, A.J., Wei, S.M., Jacob, M.P., Huvenne, J.P., Berjot, M., and Legrand, P. The secondary structure and architecture of human elastin. Eur J Biochem 258(2), 533, 1998.
32. Urry, D.W., Pattanaik, A., Xu, J., Woods, T.C., McPherson, D.T., and Parker, T.M. Elastic protein-based polymers in soft tissue augmentation and generation. J Biomater Sci Polym Ed 9(10), 1015, 1998.
33. Lee, J., Macosko, C.W., and Urry, D.W. Elastomeric polypentapeptides cross-linked into matrixes and fibers. Biomacromolecules 2(1), 170, 2001.
34. Lee, J., Macosko, C.W., and Urry, D.W. Mechanical properties of cross-linked synthetic elastomeric polypentapeptides. Macromolecules 34(17), 5968, 2001.
35. Wood, S.A., Lemons, J.E., Prasad, K.U., and Urry, D.W. In vitro calcification and in vivo biocompatibility of the crosslinked polypentapeptide of elastin. J Biomed Mater Res 20(3), 315, 1986.
36. Trabbic-Carlson, K., Liu, L., Kim, B., and Chilkoti, A. Expression and purification of recombinant proteins from Escherichia coli: comparison of an elastin-like polypeptide fusion with an oligohistidine fusion. Protein Sci 13(12), 3274, 2004.
37. Herrero-Vanrell, R., Rincon, A.C., Alonso, M., Reboto, V., Molina-Martinez, I.T., and Rodriguez-Cabello, J.C. Selfassembled particles of an elastin-like polymer as vehicles for controlled drug release. J Control Release 102(1), 113, 2005.
38. Daamen, W.F., van Moerkerk, H.T., Hafmans, T., Buttafoco, L., Poot, A.A., Veerkamp, J.H., and van Kuppevelt, T.H. Preparation and evaluation of molecularly-defined collagenelastin- glycosaminoglycan scaffolds for tissue engineering. Biomaterials 24(22), 4001, 2003.
39. Girotti, A., Reguera, J., Rodriguez-Cabello, J.C., Arias, F.J., Alonso, M., and Matestera, A. Design and bioproduction of a recombinant multi(bio)functional elastin-like protein polymer containing cell adhesion sequences for tissue engineering purposes. J Mater Sci Mater Med 15(4), 479, 2004.
40. Prestwich, G.D., and Matthew, H. Hybrid, composite, and complex biomaterials. Ann NY Acad Sci 961, 106, 2002.
41. McHale, M.K., Setton, L.A., and Chilkoti, A. Synthesis and in vitro evaluation of enzymatically cross-linked elastin-like polypeptide gels for cartilaginous tissue repair. Tissue Eng 11(11-12), 1768, 2005.
42. Balklava, Z., Verderio E., Collighan R., Gross S., Adams J., and Griffin M. Analysis of tissue transglutaminase function in the migration of Swiss 3T3 fibroblasts: the active-state conformation of the enzyme does not affect cell motility but is important for its secretion. J Biol Chem 277(19), 16567, 2002.
43. Garcia, Y., Breen, A., Burugapalli, K., Dockery, P., and Pandit, A. Stereological methods to assess tissue response for tissue-engineered scaffolds. Biomaterials 28(2), 175, 2007.
44. Ohtsuki, C. How to prepare the simulated body fluids (SBF) and its related solutions. 2007. Available at http:==mswebs .aist-nara.ac.jp=LABs= tanihara=ohtsuki=SBF=index.html.
45. O'Halloran, D., Collighan, R.J., Griffin, M., and Pandit, A.S. Characterization of a microbial transglutaminase crosslinked type II collagen scaffold. Tissue Eng 12(6), 1467, 2006.
46. Bidwell, G.L., 3rd, Davis, A.N., Fokt, I., Priebe, W., and Raucher, D. A thermally targeted elastin-like polypeptidedoxorubicin conjugate overcomes drug resistance. Invest New Drugs 25(4), 313, 2007.
47. Kumar, A., Srivastava, A., Galaev, I.Y., and Mattiasson, B., Smart polymers: physical forms and bioengineering applications. Prog Polym Sci 32(10), 1205, 2007.
48. Long,M.M., King, V.J., Prasad, K.U., Freeman, B.A., and Urry, D.W. Elastin repeat peptides as chemoattractants for bovine aortic endothelial cells. J Cell Physiol 140(3), 512, 1989.
49. Tajima, S., Wachi, H., Uemura, Y., and Okamoto, K. Modulation by elastin peptide VGVAPG of cell proliferation and elastin expression in human skin fibroblasts. Arch Dermatol Res 289(8), 489, 1997.
50. Groult, V., Hornebeck, W., Ferrari, P., Tixier, J.M., Robert, L., and Jacob, M.P. Mechanisms of interaction between human skin fibroblasts and elastin: differences between elastin fibres and derived peptides. Cell Biochem Funct 9(3), 171, 1991.
51. Hashimoto, T., Suzuki, Y., Tanihara, M., Kakimaru, Y., and Suzuki, K. Development of alginate wound dressings linked with hybrid peptides derived from laminin and elastin. Biomaterials 25(7-8), 1407, 2004.
52. Aoyagi, M., Yamamoto, M., Azuma, H., Niimi, Y., Tajima, S., Hirakawa, K., and Yamamoto, K. Smooth muscle cell proliferation, elastin formation, and tropoelastin transcripts during the development of intimal thickening in rabbit carotid arteries after endothelial denudation. Histochem Cell Biol 107(1), 11, 1997.
53. Hoban, L.D., Pierce, M., Quance, J., Hayward, I., McKee, A., Gowda, D.C., Urry, D.W., and Williams, T. Use of polypentapeptides of elastin to prevent postoperative adhesions: efficacy in a contaminated peritoneal model. J Surg Res 56(2), 179, 1994.
54. Urry, D.W., Nicol, A., Gowda, D.C., Hoban, L.D., McKee, A., Williams, T., Olsen, D.B., and Cox, B.A. Medical applications of bioelastic materials. In: Gebelein, C., ed. Biotechnological Polymers: Medical, Pharmaceutical and Industrial Applications. Lancaster, PA: Technomic Pub. Co., p. 82, 1993.