Cell adhesion and proliferation on RGD-modified recombinant spider silk proteins

Biomaterials

Volumn 33, Issue 28, 2012, Pages 6650-6659

  Wohlrab, Stefanie ^a   Müller, Susanne ^a   Schmidt, Andreas ^a   Neubauer, Stefanie ^b   Kessler, Horst ^b,c   Leal Egaña, Aldo ^a   Scheibel, Thomas ^a  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

Cell adhesion; Cell proliferation; Chemical coupling; Genetic engineering; RGD peptide; Silk

Indexed keywords

ADHESION PROPERTIES; AMINO ACID SEQUENCE; BIOMEDICAL APPLICATIONS; CHEMICAL COUPLING; CHEMICALLY MODIFIED; CYCLIC PEPTIDES; FILM PROPERTIES; INTEGRINS; MOUSE-FIBROBLASTS; RECOGNITION SEQUENCE; RECOMBINANT SPIDER SILK PROTEINS; RGD PEPTIDE; RGD SEQUENCES; SECONDARY STRUCTURES; SILK PROTEINS; SPIDER SILKS; WATER CONTACT ANGLE;

AMINO ACIDS; BIOCOMPATIBILITY; BIODEGRADATION; CELL ADHESION; CELL CULTURE; CELL PROLIFERATION; CONTACT ANGLE; GENETIC ENGINEERING; MECHANICAL PROPERTIES; MEDICAL APPLICATIONS; PEPTIDES; SILK; SURFACE ROUGHNESS;

RECOMBINANT PROTEINS;

ARGINYLGLYCYLASPARTIC ACID; HYBRID PROTEIN; INTEGRIN; RECOMBINANT PROTEIN; RECOMBINANT SPIDER SILK PROTEIN; UNCLASSIFIED DRUG; WATER;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL ADHESION; CELL PROLIFERATION; FIBROBLAST; FILM; GENETIC ENGINEERING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; SILK; SURFACE PROPERTY;

AMINO ACID SEQUENCE; ANIMALS; ARTHROPOD PROTEINS; BALB 3T3 CELLS; BIOCOMPATIBLE MATERIALS; CELL ADHESION; CELL PROLIFERATION; CIRCULAR DICHROISM; MASS SPECTROMETRY; MEMBRANES, ARTIFICIAL; MICE; OLIGOPEPTIDES; PEPTIDES; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SILK; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SPIDERS;

ADHESION; AMINO ACIDS; CHEMICAL BONDS; CONTACT ANGLE; GENETIC ENGINEERING; MECHANICAL PROPERTIES; PROTEINS; ROUGHNESS; SILK;

ARANEAE;

EID: 84864006044     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2012.05.069     Document Type: Article

References (66)

1. Eisenbarth E. Biomaterials for tissue engineering. Adv Eng Mater 2007, 9:1051-1060.
2. Vladkova T.G. Surface engineered polymeric biomaterials with improved biocontact properties. Int J Polym Sci 2010, Article ID 296094.
3. Tamada Y., Ikada Y. Fibroblast growth on polymer surfaces and biosynthesis of collagen. J Biomed Mater Res 1994, 28:783-789.
4. Wei J., Igarashi T., Okumori N., Maetani T., Liu B., Yoshinari M. Influence of surface wettability on competitive protein adsorption and initial attachment of osteoblasts. Biomed Mater 2009, 4:045002.
5. Leal-Egana A., Lang G., Mauerer C., Wickinghoff J., Weber M., Geimer S., et al. Interactions of fibroblasts with different morphologies made of an engineered spider silk protein. Adv Eng Mater 2011, 14:B67-B75.
6. Lensen M.C., Schulte V.A., Salber J., Diez M., Menges F., Moller M. Cellular responses to novel, micropatterned biomaterials. Pure Appl Chem 2008, 80:2479-2487.
7. van Kooten T.G., Spijker H.T., Busscher H.J. Plasma-treated polystyrene surfaces: model surfaces for studying cell-biomaterial interactions. Biomaterials 2004, 25:1735-1747.
8. Elvira C., Yi F., Azevedo M.C., Rebouta L., Cunha A.M., San Roman J., et al. Plasma- and chemical-induced graft polymerization on the surface of starch-based biomaterials aimed at improving cell adhesion and proliferation. J Mater Sci Mater Med 2003, 14:187-194.
9. Yoshihiro I. Tissue engineering by immobilized growth factors. Mater Sci Eng C 1998, 6:267-274.
10. Hwang D.S., Sim S.B., Cha H.J. Cell adhesion biomaterial based on mussel adhesive protein fused with RGD peptide. Biomaterials 2007, 28:4039-4046.
11. Schaffner P., Meyer J., Dard M., Wenz R., Nies B., Verrier S., et al. Induced tissue integration of bone implants by coating with bone selective RGD-peptides in vitro and in vivo studies. J Mater Sci Mater Med 1999, 10:837-839.
12. Kammerer P.W., Heller M., Brieger J., Klein M.O., Al-Nawas B., Gabriel M. Immobilisation of linear and cyclic RGD-peptides on titanium surfaces and their impact on endothelial cell adhesion and proliferation. Eur Cells Mater 2011, 21:364-372.
13. Shu X.Z., Ghosh K., Liu Y., Palumbo F.S., Luo Y., Clark R.A., et al. Attachment and spreading of fibroblasts on an RGD peptide-modified injectable hyaluronan hydrogel. J Biomed Mater Res A 2004, 68:365-375.
14. Li B., Chen J.X., Wang J.H.C. RGD peptide-conjugated poly(dimethylsiloxane) promotes adhesion, proliferation, and collagen secretion of human fibroblasts. J Biomed Mater Res A 2006, 79:989-998.
15. Hersel U., Dahmen C., Kessler H. RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials 2003, 24:4385-4415.
16. Kantlehner M., Finsinger D., Meyer J., Schaffner P., Jonczyk A., Diefenbach B., et al. Selective RGD-mediated adhesion of osteoblasts at surfaces of implants. Angew Chem Int Edit 1999, 38:560-562.
17. Morgan A.W., Roskov K.E., Lin-Gibson S., Kaplan D.L., Becker M.L., Simon C.G. Characterization and optimization of RGD-containing silk blends to support osteoblastic differentiation. Biomaterials 2008, 29:2556-2563.
18. Bini E., Foo C.W., Huang J., Karageorgiou V., Kitchel B., Kaplan D.L. RGD-functionalized bioengineered spider dragline silk biomaterial. Biomacromolecules 2006, 7:3139-3145.
19. Sofia S., McCarthy M.B., Gronowicz G., Kaplan D.L. Functionalized silk-based biomaterials for bone formation. J Biomed Mater Res 2001, 54:139-148.
20. Asakura T., Tanaka C., Yang M., Yao J., Kurokawa M. Production and characterization of a silk-like hybrid protein, based on the polyalanine region of Samia cynthia ricini silk fibroin and a cell adhesive region derived from fibronectin. Biomaterials 2004, 25:617-624.
21. Delforge D., Gillon B., Art M., Dewelle J., Raes M., Remacle J. Design of a synthetic adhesion protein by grafting RGD tailed cyclic peptides on bovine serum albumin. Lett Pept Sci 1998, 5:87-91.
22. Pierschbacher M.D., Ruoslahti E. Influence of stereochemistry of the sequence Arg-Gly-Asp-Xaa on binding specificity in cell adhesion. J Biol Chem 1987, 262:17294-17298.
23. Haubner R., Finsinger D., Kessler H. Stereoisomeric peptide libraries and peptidomimetics for designing selective inhibitors of the alpha(V)beta(3) integrin for a new cancer therapy. Angew Chem Int Edit 1997, 36:1375-1389.
24. Aumailley M., Gurrath M., Muller G., Calvete J., Timpl R., Kessler H. Arg-Gly-Asp constrained within cyclic pentapeptides. Strong and selective inhibitors of cell adhesion to vitronectin and laminin fragment P1. FEBS Lett 1991, 291:50-54.
25. Meyer A., Auernheimer J., Modlinger A., Kessler H. Targeting RGD recognizing integrins: drug development, biomaterial research, tumor imaging and targeting. Curr Pharm Design 2006, 12:2723-2747.
26. Humenik M., Smith A.M., Scheibel T. Recombinant spider silks-biopolymers with potential for future applications. Polymers 2011, 3:640-661.
27. Forrest R.D. Early history of wound treatment. J Roy Soc Med 1982, 75:198-205.
28. Huemmerich D., Helsen C.W., Quedzuweit S., Oschmann J., Rudolph R., Scheibel T. Primary structure elements of spider dragline silks and their contribution to protein solubility. Biochemistry 2004, 43:13604-13612.
29. Rising A., Widhe M., Johansson J., Hedhammar M. Spider silk proteins: recent advances in recombinant production, structure-function relationships and biomedical applications. Cell Mol Life Sci 2011, 68:169-184.
30. Vendrely C., Scheibel T. Biotechnological production of spider-silk proteins enables new applications. Macromol Biosci 2007, 7:401-409.
31. Xia X.X., Qian Z.G., Ki C.S., Park Y.H., Kaplan D.L., Lee S.Y. Native-sized recombinant spider silk protein produced in metabolically engineered Escherichia coli results in a strong fiber. Proc Natl Acad Sci USA 2010, 107:14059-14063.
32. Slotta U., Tammer M., Kremer F., Koelsch P., Scheibel T. Structural analysis of spider silk films. Supramol Chem 2006, 18:465-471.
33. Spiess K., Wohlrab S., Scheibel T. Structural characterization and functionalization of engineered spider silk films. Soft Matter 2010, 6:4168-4174.
34. Lammel A., Schwab M., Slotta U., Winter G., Scheibel T. Processing conditions for the formation of spider silk microspheres. ChemSusChem 2008, 1:413-416.
35. Slotta U.K., Rammensee S., Gorb S., Scheibel T. An engineered spider silk protein forms microspheres. Angew Chem Int Edit 2008, 47:4592-4594.
36. Hermanson K.D., Huemmerich D., Scheibel T., Bausch A.R. Engineered microcapsules fabricated from reconstituted spider silk. Adv Mater 2007, 19:1810-1815.
37. Schacht K., Scheibel T. Controlled hydrogel formation of a recombinant spider silk protein. Biomacromolecules 2011, 12:2488-2495.
38. Spiess K., Lammel A., Scheibel T. Recombinant spider silk proteins for applications in biomaterials. Macromol Biosci 2010, 10:998-1007.
39. Acharya C., Ghosh S.K., Kundu S.C. Silk fibroin protein from mulberry and non-mulberry silkworms: cytotoxicity, biocompatibility and kinetics of L929 murine fibroblast adhesion. J Mater Sci Mater Med 2008, 19:2827-2836.
40. Seo Y.K., Yoon H.H., Park Y.S., Song K.Y., Lee W.S., Park J.K. Correlation between scaffold in vivo biocompatibility and in vitro cell compatibility using mesenchymal and mononuclear cell cultures. Cell Biol Toxicol 2009, 25:513-522.
41. Hu X., Kaplan D., Cebe P. Determining beta-sheet crystallinity in fibrous proteins by thermal analysis and infrared spectroscopy. Macromolecules 2006, 39:6161-6170.
42. Goncalves R., da Silva C.L., Ferreira B.S., Lemos M.A., Lemos F., Almeida-Porada G., et al. Kinetic analysis of the ex vivo expansion of human hematopoietic stem/progenitor cells. Biotechnol Lett 2006, 28:335-340.
43. Meinnel T., Mechulam Y., Blanquet S. Methionine as translation start signal - a review of the enzymes of the pathway in Escherichia coli. Biochimie 1993, 75:1061-1075.
44. Spiess K., Ene R., Keenan C.D., Senker J., Kremer F., Scheibel T. Impact of initial solvent on thermal stability and mechanical properties of recombinant spider silk films. J Mater Chem 2011, 21:13594-13604.
45. Cao H., Chen X., Huang L., Shao Z.Z. Electrospinning of reconstituted silk fiber from aqueous silk fibroin solution. Mat Sci Eng C-Mater 2009, 29:2270-2274.
46. Jin H.J., Chen J.S., Karageorgiou V., Altman G.H., Kaplan D.L. Human bone marrow stromal cell responses on electrospun silk fibroin mats. Biomaterials 2004, 25:1039-1047.
47. Wenk E., Wandrey A.J., Merkle H.P., Meinel L. Silk fibroin spheres as a platform for controlled drug delivery. J Control Release 2008, 132:26-34.
48. Kluge J.A., Rabotyagova O., Leisk G.G., Kaplan D.L. Spider silks and their applications. Trends Biotechnol 2008, 26:244-251.
49. O'Brien F.J., Harley B.A., Yannas I.V., Gibson L.J. The effect of pore size on cell adhesion in collagen-GAG scaffolds. Biomaterials 2005, 26:433-441.
50. Chung T.W., Liu D.Z., Wang S.Y., Wang S.S. Enhancement of the growth of human endothelial cells by surface roughness at nanometer scale. Biomaterials 2003, 24:4655-4661.
51. Lydon M.J., Minett T.W., Tighe B.J. Cellular interactions with synthetic polymer surfaces in culture. Biomaterials 1985, 6:396-402.
52. Kunzler T.P., Drobek T., Schuler M., Spencer N.D. Systematic study of osteoblast and fibroblast response to roughness by means of surface-morphology gradients. Biomaterials 2007, 28:2175-2182.
53. Wang R.C.C., Hsieh M.C., Lee T.M. Effects of nanometric roughness on surface properties and fibroblast's initial cytocompatibilities of Ti6Al4V. Biointerphases 2011, 6:87-97.
54. Lin H.B., Sun W., Mosher D.F., Garciaecheverria C., Schaufelberger K., Lelkes P.I., et al. Synthesis, surface, and cell-adhesion properties of polyurethanes containing covalently grafted RGD-peptides. J Biomed Mater Res 1994, 28:329-342.
55. Kato M., Mrksich M. Using model substrates to study the dependence of focal adhesion formation on the affinity of integrin-ligand complexes. Biochemistry 2004, 43:2699-2707.
56. Xiao Y., Truskey G.A. Effect of receptor-ligand affinity on the strength of endothelial cell adhesion. Biophys J 1996, 71:2869-2884.
57. Kaufmann D., Fiedler A., Junger A., Auernheimer J., Kessler H., Weberskirch R. Chemical conjugation of linear and cyclic RGD moieties to a recombinant elastin-mimetic polypeptide - a versatile approach towards bioactive protein hydrogels. Macromol Biosci 2008, 8:577-588.
58. Kantlehner M., Schaffner P., Finsinger D., Meyer J., Jonczyk A., Diefenbach B., et al. Surface coating with cyclic RGD peptides stimulates osteoblast adhesion and proliferation as well as bone formation. Chembiochem 2000, 1:107-114.
59. Haubner R., Gratias R., Diefenbach B., Goodman S.L., Jonczyk A., Kessler H. Structural and functional aspects of RGD-containing cyclic pentapeptides as highly potent and selective integrin alpha(v)beta(3) antagonists. J Am Chem Soc 1996, 118:7461-7472.
60. Massia S.P., Hubbell J.A. An RGD spacing of 440 nm is sufficient for integrin alpha-V-beta-3-mediated fibroblast spreading and 140 nm for focal contact and stress fiber formation. J Cell Biol 1991, 114:1089-1100.
61. Cavalcanti-Adam E.A., Micoulet A., Blummel J., Auernheimer J., Kessler H., Spatz J.P. Lateral spacing of integrin ligands influences cell spreading and focal adhesion assembly. Eur J Cell Biol 2006, 85:219-224.
62. Huang J., Grater S.V., Corbellini F., Rinck S., Bock E., Kemkemer R., et al. Impact of order and disorder in RGD nanopatterns on cell adhesion. Nano Lett 2009, 9:1111-1116.
63. Bellahcene A., Bonjean K., Fohr B., Fedarko N.S., Robey F.A., Young M.F., et al. Bone sialoprotein mediates human endothelial cell attachment and migration and promotes angiogenesis. Circ Res 2000, 86:885-891.
64. Kalinina S., Gliemann H., Lopez-Garcia M., Petershans A., Auernheimer J., Schimmel T., et al. Isothiocyanate-functionalized RGD peptides for tailoring cell-adhesive surface patterns. Biomaterials 2008, 29:3004-3013.
65. Gao Z., Wang S., Zhu H.S., Su C.N., Xu G.L., Lian X.J. Using selected uniform cells in round shape with a micropipette to measure cell adhesion strength on silk fibroin-based materials. Mat Sci Eng C-Bio S 2008, 28:1227-1235.
66. Wang Q., Parrish A.R., Wang L. Expanding the genetic code for biological studies. Chem Biol 2009, 16:323-336.