Protein conformational changes induced by adsorption onto material surfaces: an important issue for biomedical applications of material science

• Autorzy: Ballet T. , Boulange L. , Brechet Y. , Bruckert F. , Weidenhaupt M.
• Języki publikacji: EN

Abstrakty

EN

Protein adsorption on solid surfaces is a widespread phenomenon of large biological and biotechnological significance. Conformational changes are likely to accompany protein adsorption, but are difficult to evidence directly. Nevertheless they have important consequences, since the partial unfolding of protein domains can expose hitherto hidden amino acids. This remodeling of the protein surface can trigger the activation of molecular complexes such as the blood coagulation cascade or the innate immune complement system. In the case of extracellular matrix, it can also change the way cells interact with the material surfaces and result in modified cell behavior. In this review, we present direct and indirect evidences that support the view that some proteins change their conformation upon adsorption. We also show that both physical and chemical methods are needed to study the extent and kinetics of protein conformational changes. In particular, AFM techniques and cryo-electron microscopy provide useful and complementary information. We then review the chemical and topological features of both proteins and material surfaces in relation with protein adsorption. Mutating key amino acids in proteins changes their stability and this is related to material-induced conformational changes, as shown for instance with insulin. In addition, combinatorial methods should provide valuable information about peptide or antibody adsorption on well-defined material surfaces. These techniques could be combined with molecular modeling methods to decipher the rules governing conformational changes associated with protein adsorption.

Słowa kluczowe

EN

protein; conformation; unfolding; aggregation; material surface; nanostructure

• Wydawca: Polska Akademia Nauk, Wydział IV Nauk Technicznych
• Czasopismo: Bulletin of the Polish Academy of Sciences. Technical Sciences
• Rocznik: 2010
• Tom: Vol. 58, nr 2
• Strony: 303--315
• Opis fizyczny: Bibliogr. 139 poz., rys.

Twórcy

autor

Ballet T.

autor

Boulange L.

autor

Brechet Y.

autor

Bruckert F.

autor

Weidenhaupt M.

• Laboratoire des Mat´eriaux et du Genie Physique, Grenoble Institute of Technology Minatec, 3, Parvis Louis Neel, BP 257, 38016 Grenoble Cedex 1, France,

Bibliografia

• [1] H.K. Kleinman and G.R.Martin, “Matrigel: basement membrane matrix with biological activity”, Semin. Cancer Biol. 15 (5), 378–386 (2005).
• [2] T. Sordel, F. Kermarec-Marcel, S. Garnier-Raveaud, N. Glade, F. Sauter-Starace, C. Pudda, M. Borella, M. Plissonnier, F. Chatelain, F. Bruckert, and N. Picollet- D’hahan, “Influence of glass and polymer coatings on CHO cell morphology and adhesion”, Biomaterials 28 (8), 1572–1584 (2007).
• [3] E.A. Vogler, J.C. Graper, H.W. Sugg, L.M. Lander, and W.J. Brittain, “Contact activation of the plasma coagulation cascade. II. Protein adsorption to procoagulant surfaces”, J. Biomed Mater. Res. 29 (8), 1017–1028 (1995).
• [4] E.A. Vogler, J.C. Graper, G.R. Harper, H.W. Sugg, L.M. Lander, and W.J. Brittain, “Contact activation of the plasma coagulation cascade. I. Procoagulant surface chemistry and energy”, J. Biomed Mater. Res. 29 (8), 1005–1016 (1995).
• [5] J.H. Griffin, “Role of surface in surface-dependent activation of Hageman factor (blood coagulation factor XII)”, Proc. Natl. Acad. Sci. USA 75 (4), 1998–2002 (1978).
• [6] B. Nilsson, K.N. Ekdahl, T.E. Mollnes, and J.D. Lambris, “The role of complement in biomaterial-induced inflammation”, Mol. Immunol. 44 (1–3), 82–94 (2007).
• [7] D.E. Chenoweth, ”Complement activation in extracorporeal circuits”, Ann. NY Acad. Sci. 516, 306–313 (1987).
• [8] C. Gaboriaud, F. Teillet, L.A. Gregory, N.M. Thielens, and G.J. Arlaud, “Assembly of C1 and the MBL- and ficolin- MASP complexes: structural insights”, Immunobiology 212 (4–5), 279–288 (2007).
• [9] C. Gaboriaud, N.M. Thielens, L.A. Gregory, V. Rossi, J.C. Fontecilla-Camps, and G.J. Arlaud, “Structure and activation of the C1 complex of complement: unraveling the puzzle”, Trends Immunol. 25 (7), 368–373 (2004).
• [10] V. Garlatti, L. Martin, E. Gout, J.B. Reiser, T. Fujita, G.J. Arlaud, N.M. Thielens, and C. Gaboriaud, “Structural basis for innate immune sensing by M-ficolin and its control by a pH-dependent conformational switch”, J. Biol. Chem. 282 (49), 35814–35820 (2007).
• [11] T. Vorup-Jensen, S.V. Petersen, A.G. Hansen, K. Poulsen, W. Schwaeble, R.B. Sim, K.B. Reid, S.J. Davis, S. Thiel, and J.C. Jensenius, “Distinct pathways of mannanbinding lectin (MBL)- and C1-complex autoactivation revealed by reconstitution of MBL with recombinant MBL-associated serine protease-2”, J. Immunol. 165 (4), 2093–2100 (2000).
• [12] R. Gref, M. Luck, P. Quellec, M. Marchand, E. Dellacherie, S. Harnisch, T. Blunk, and R.H. Muller, “’Stealth’ coronacore nanoparticles surface modified by polyethylene glycol (PEG): influences of the corona (PEG chain length and surface density) and of the core composition on phagocytic uptake and plasma protein adsorption”, Colloids Surf. B Biointerfaces 18 (3–4), 301–313 (2000).
• [13] D.W. Branch, B.C. Wheeler, G.J. Brewer, and D.E. Leckband, “Long-term stability of grafted polyethylene glycol surfaces for use with microstamped substrates in neuronal cell culture”, Biomaterials 22 (10), 1035–1047 (2001).
• [14] A. Kidane and K. Park, “Complement activation by PEOgrafted glass surfaces”, J. Biomed Mater. Res. 48 (5), 640–647 (1999).
• [15] A. Kidane, G.C. Lantz, S. Jo, and K. Park, “Surface modification with PEO-containing triblock copolymer for improved biocompatibility: in vitro and ex vivo studies”, J. Biomater Sci. Polym. Ed. 10 (10), 1089–1105 (1999).
• [16] S.M. Moghimi, A.C. Hunter, and J.C. Murray, “Longcirculating and target-specific nanoparticles: theory to practice”, Pharmacol Rev. 53 (2), 283–318 (2001).
• [17] P. Broz, S.M. Benito, C. Saw, P. Burger, H. Heider, M. Pfisterer, S. Marsch, W. Meier, and P. Hunziker, “Cell targeting by a generic receptor-targeted polymer nanocontainer platform”, J. Control Release 102 (2), 475–488 (2005).
• [18] S. Stephan, S.G. Ball, M. Williamson, D.V. Bax, A. Lomas, C.A. Shuttleworth, and C.M. Kielty, “Cell-matrix biology in vascular tissue engineering”, J. Anat. 209 (4), 495–502 (2006).
• [19] M.R. Kapadia, D.A. Popowich, and M.R. Kibbe, “Modified prosthetic vascular conduits”, Circulation 117 (14), 1873–1882 (2008).
• [20] B. Sharma, “Immunogenicity of therapeutic proteins. Part 2: impact of container closures”, Biotechnol. Adv. 25 (3), 318–324 (2007).
• [21] L.S. Jones, A. Kaufmann, and C.R. Middaugh, “Silicone oil induced aggregation of proteins”, J. Pharm. Sci. 94 (4), 918–927 (2005).
• [22] L. Sun, H. Alexander, N. Lattarulo, N.C. Blumenthal, J.L. Ricci, and G. Chen, “Protein denaturation induced by cyclic silicone”, Biomaterials 18 (24), 1593–1597 (1997).
• [23] V.T. Oi, T.M. Vuong, R. Hardy, J. Reidler, J. Dangle, L.A. Herzenberg, and L. Stryer, “Correlation between segmental flexibility and effecter function of antibodies”, Nature 307 (5947), 136–140 (1984).
• [24] D.G. Dearborn and D.B. Wetlaufer, “Reversible thermal conformation changes in human serum low-density lipoprotein”, Proc. Nat. Acad. Sci. USA 62 (1), 179–185 (1969).
• [25] V.N. Uversky, “The mysterious unfoldome: structureless, underappreciated, yet vital part of any given proteome”, J. Biomed. Biotechnol. 5, 680–688 (2010).
• [26] W. Norde, “My voyage of discovery to proteins in flatland and beyond”, Colloids Surf. B Biointerfaces 61 (1), 1–9 (2008).
• [27] R. Gabizon, M. Mor, M.M. Rosenberg, L. Britan, Z. Hayouka, M. Kotler, D.E. Shalev, and A. Friedler, “Using peptides to study the interaction between the p53 tetramerization domain and HIV-1 Tat”, Biopolymers 90 (2), 105–116 (2008).
• [28] T. Higashijima, K. Wakamatsu, M. Takemitsu, M. Fujino, T. Nakajima, and T. Miyazawa, “Conformational change of mastoparan from wasp venom on binding with phospholipid membrane”, FEBS Lett. 152 (2), 227–230 (1983).
• [29] J. Brange, S. Havelund, E. Hommel, E. Sorensen, and C. Kuhl, “Neutral insulin solutions physically stabilized by addition of Zn2+”, Diabet. Med. 3 (6), 532–536 (1986).
• [30] C.P. Hill, Z. Dauter, E.J. Dodson, G.G. Dodson, and M.F. Dunn, “X-ray structure of an unusual Ca2+ site and the roles of Zn2+ and Ca2+ in the assembly, stability, and storage of the insulin hexamer”, Biochemistry 30 (4), 917–924 (1991).
• [31] V. Sluzky, J.A. Tamada, A.M. Klibanov, and R. Langer, “Kinetics of insulin aggregation in aqueous solutions upon agitation in the presence of hydrophobic surfaces”, Proc. Natl. Acad. Sci. USA 88 (21), 9377–9381 (1991).
• [32] V. Sluzky, A.M. Klibanov, and R. Langer, “Mechanism of insulin aggregation and stabilization in agitated aqueous solutions”, Biotechnol. Bioeng. 40 (8), 895–903 (1992).
• [33] V. Feingold, A.B. Jenkins, and E.W. Kraegen, “Effect of contact material on vibration-induced insulin aggregation”, Diabetologia 27 (3), 373–378 (1984).
• [34] M. Dathe, K. Gast, D. Zirwer, H. Welfle, and B. Mehlis, “Insulin aggregation in solution”, Int. J. Pept Protein Res. 36 (4), 344–349 (1990).
• [35] S.H. Mollmann, J.T. Bukrinsky, S. Frokjaer, and U. Elofsson, “Adsorption of human insulin and AspB28 insulin on a PTFE-like surface”, J. Colloid Interface Sci. 286 (1), 28–35 (2005).
• [36] I.B. Hirsch, “Insulin analogues”, N. Engl. J. Med. 352 (2), 174–183 (2005).
• [37] A. Wollmer, B. Rannefeld, J. Stahl, and S.G. Melberg, “Structural transition in the metal-free hexamer of proteinengineered [B13 Gln]insulin”, Biol. Chem. Hoppe Seyler 370 (9), 1045–1053 (1989).
• [38] G.A. Bentley, J. Brange, Z. Derewenda, E.J. Dodson, G.G. Dodson, J. Markussen, A.J. Wilkinson, A. Wollmer, and B. Xiao, “Role of B13 Glu in insulin assembly. The hexamer structure of recombinant mutant (B13 Glu!Gln) insulin”, J. Mol. Biol. 228 (4), 1163–1176 (1992).
• [39] H. Noh and E.A. Vogler, “Volumetric interpretation of protein adsorption: competition from mixtures and the Vroman effect”, Biomaterials 28 (3), 405–422 (2007).
• [40] P. Wojciechowski and J.L. Brash, “The Vroman effect in tube geometry: the influence of flow on protein adsorption T. Ballet, L. Boulange, Y. Brechet, F. Bruckert, and M. Weidenhaupt measurements”, J. Biomater Sci. Polym. Ed. 2 (3), 203–216 (1991).
• [41] J.L. Brash, C.F. Scott, P. Hove, P. Wojciechowski, and R.W. Colman, “Mechanism of transient adsorption of fibrinogen from plasma to solid surfaces: role of the contact and fibrinolytic systems”, Blood 71 (4), 932–939 (1988).
• [42] C. Zhou, J.M. Friedt, A. Angelova, K.H. Choi, W. Laureyn, F. Frederix, L.A. Francis, A. Campitelli, Y. Engelborghs, and G. Borghs, “Human immunoglobulin adsorption investigated by means of quartz crystal microbalance dissipation, atomic force microscopy, surface acoustic wave, and surface plasmon resonance techniques”, Langmuir 20 (14), 5870–5878 (2004).
• [43] S.G. Steinemann, “Metal implants and surface reactions”, Injury 27, 16–22 (1996).
• [44] J.A. Disegi and L. Eschbach, “Stainless steel in bone surgery”, Injury 31, 2–6 (2000).
• [45] R.W. Billington, J.A. Williams, and G.J. Pearson, “Ion processes in glass ionomer cements”, J. Dent 34 (8), 544–555 (2006).
• [46] L.L. Hench, I.D. Xynos, and J.M. Polak, “Bioactive glasses for in situ tissue regeneration”, J. Biomater Sci. Polym. Ed. 15 (4), 543–562 (2004).
• [47] S.H. Gehrke, L.H. Uhden, and J.F. McBride, “Enhanced loading and activity retention of bioactive proteins in hydrogel delivery systems”, J. Control Release 55 (1), 21–33 (1998).
• [48] T. Crouzier, K. Ren, C. Nicolas, C. Roy, and C. Picart, “Layer-by-layer films as a biomimetic reservoir for rhBMP-2 delivery: controlled differentiation of myoblasts to osteoblasts”, Small 5 (5), 598–608 (2009).
• [49] Y. Tie, C. Calonder, and P.R. Van Tassel, “Protein adsorption: kinetics and history dependence”, J. Colloid Interface Sci. 268 (1), 1–11 (2003).
• [50] K. Vallieres, P. Chevallier, C. Sarra-Bournet, S. Turgeon, and G. Laroche, “AFM imaging of immobilized fibronectin: does the surface conjugation scheme affect the protein orientation/conformation?”, Langmuir 23 (19), 9745–9751 (2007).
• [51] C.C. Dupont-Guillain and P.G. Rouxhet, “AFM Study of the Interaction of Collagen with Polystyrene and Plasma-Oxidized Polystyrene”, Langmuir 17, 7261–7266 (2001).
• [52] P. Hallett, G. Offer, and M.J. Miles, “Atomic force microscopy of the myosin molecule”, Biophys. J. 68 (4), 1604–1606 (1995).
• [53] T. Ando, N. Kodera, E. Takai, D. Maruyama, K. Saito, and A. Toda, “A high-speed atomic force microscope for studying biological macromolecules”, Proc. Natl. Acad. Sci. USA 98 (22), 12468–12472 (2001).
• [54] N. Kodera, T. Kinoshita, T. Ito, and T. Ando, “Highresolution imaging of myosin motor in action by a highspeed atomic force microscope”, Adv. Exp. Med. Biol. 538, 119–127 (2003).
• [55] M. Taniguchi, O. Matsumoto, S. Suzuki, Y. Nishino, A. Okuda, T. Taga, and T. Yamane, “MgATP-induced conformational changes in a single myosin molecule observed by atomic force microscopy: periodicity of substructures in myosin rods”, Scanning 25 (5), 223–229 (2003).
• [56] R.P. Richter and A.R. Brisson, “Following the formation of supported lipid bilayers on mica: a study combining AFM, QCM-D, and ellipsometry”, Biophys. J. 88 (5), 3422–3433 (2005).
• [57] M. Han, A. Sethuraman, S.T. Kane, and G. Belfort, “Nanometer-scale roughness having little effect on the amount or structure of adsorbed protein”, Langmui 19, 9868–9872 (2003).
• [58] F.A. Denis, P. Hanarp, D.S. Sutherland, J. Gold, C. Mustin, P.G. Rouxhet, and Y.F. Dufrˆene, “Protein adsorption on model surfaces with controlled nanotopography and chemistry”, Langmuir 18, 819–828 (2002).
• [59] T. Hayashi, M. Tanaka, S. Yamamoto, M. Shimomura, and M. Hara, “Direct observation of interaction between proteins and blood-compatible polymer surfaces”, Biointerphases 2, 119–125 (2007).
• [60] C. Gergely, J. Hemmerle, P. Schaaf, J.K. Horber, J.C. Voegel, and B. Senger, “Multibead-and-spring model to interpret protein detachment studied by AFM force spectroscopy”, Biophys. J. 83 (2), 706–722 (2002).
• [61] R. Merkel, P. Nassoy, A. Leung, K. Ritchie, and E. Evans, “Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy”, Nature 397 (6714), 50–53 (1999).
• [62] J. Dubochet, M. Adrian, J.J. Chang, J.C. Homo, J. Lepault, A.W. McDowall, and P. Schultz, “Cryo-electron microscopy of vitrified specimens”, Q Rev.Biophys. 21 (2), 129–228 (1988).
• [63] C.M. Spahn and P.A. Penczek, “Exploring conformational modes of macromolecular assemblies by multiparticle cryo-EM”, Curr. Opin. Struct. Biol. 19 (5), 623–631 (2009).
• [64] J.C. Schuette, F.V.T. Murphy, A.C. Kelley, J.R. Weir, J. Giesebrecht, S.R. Connell, J.Loerke, T. Mielke,W. Zhang, P.A. Penczek, V. Ramakrishnan, and C.M. Spahn, “GTPase activation of elongation factor EF-Tu by the ribosome during decoding”, EMBO J. 28 (6), 755–765 (2009).
• [65] A. Sartori, R. Gatz, F. Beck, A. Rigort, W. Baumeister, and J.M. Plitzko, “Correlative microscopy: bridging the gap between fluorescence light microscopy and cryoelectron tomography”, J. Struct. Biol. 160 (2), 135–145 (2007).
• [66] Z.H. Zhou, “Towards atomic resolution structural determination by single-particle cryo-electron microscopy”, Curr. Opin. Struct. Biol. 18 (2), 218–228 (2008).
• [67] E.V. Orlova and H.R. Saibil, “Structure determination of macromolecular assemblies by single-particle analysis of cryo-electron micrographs”, Curr. Opin. Struct. Biol. 14 (5), 584–590 (2004).
• [68] F. Zenhausern, M. Adrian, and P. Descouts, “Solution structure and direct imaging of fibronectin adsorption to solid surfaces by scanning force microscopy and cryoelectron microscopy”, J. Electron. Microsc. (Tokyo) 42 (6), 378–388 (1993).
• [69] L. Baugh and V. Vogel, “Structural changes of fibronectin adsorbed to model surfaces probed by fluorescence resonance energy transfer”, J. Biomed. Mater. Res. A 69 (3), 525–534 (2004).
• [70] G. Baneyx, L. Baugh, and V. Vogel, “Coexisting conformations of fibronectin in cell culture imaged using fluorescence resonance energy transfer”, Proc. Natl. Acad. Sci. USA 98 (25), 14464–14468 (2001).
• [71] M.L. Smith, D. Gourdon, W.C. Little, K.E. Kubow, R.A. Eguiluz, S. Luna-Morris, and V. Vogel, “Force-induced unfolding of fibronectin in the extracellular matrix of living cells”, PLoS Biol. 5‘ (10), 268 (2007).
• [72] P. Sukumvanich, V. DesMarais, C.V. Sarmiento, Y. Wang, I. Ichetovkin, G. Mouneimne, S. Almo, and J. Condeelis, “Cellular localization of activated N-WASP using a conformation-sensitive antibody”, Cell Motil Cytoskeleton 59 (2), 141–152 (2004).
• [73] M.K. Gorny, C. Williams, B. Volsky, K. Revesz, S. Cohen, V.R. Polonis, W.J. Honnen, S.C. Kayman, C. Krachmarov, A. Pinter, and S. Zolla-Pazner, “Human monoclonal antibodies specific for conformation-sensitive epitopes of V3 neutralize human immunodeficiency virus type 1 primary isolates from various clades”, J. Virol. 76 (18), 9035–9045 (2002).
• [74] N. Moretto, A. Bolchi, C. Rivetti, B.P. Imbimbo, G. Villetti, V. Pietrini, L. Polonelli, S. Del Signore, K.M. Smith, R.J. Ferrante, and S. Ottonello, “Conformation-sensitive antibodies against alzheimer amyloid-beta by immunization with a thioredoxinconstrained B-cell epitope peptide”, J. Biol. Chem. 282 (15), 11436–11445 (2007).
• [75] H. Ueno, O. Murayama, S. Maeda, N. Sahara, J.M. Park, M. Murayama, A. Sanda, K. Iwahashi, M. Matsuda, and A. Takashima, “Novel conformation-sensitive antibodies specific to three- and four-repeat tau”, Biochem. Biophys. Res. Commun. 358 (2), 602–607 (2007).
• [76] U.L. Jayasena, S.K. Gribble, A. McKenzie, K. Beyreuther, C.L. Masters, and J.R. Underwood, “Identification of structural variations in the carboxyl terminus of Alzheimer’s disease-associated beta A4[1-42] amyloid using a monoclonal antibody”, Clin Exp Immunol 124 (2), 297–305 (2001).
• [77] K.R. Murray, M.P. Nair, A.F. Ayyobi, J.S. Hill, P.H. Pritchard, and A.G. Lacko, “Probing the 121-136 domain of lecithin:cholesterol acyltransferase using antibodies”, Arch. Biochem. Biophys. 385 (2), 267–275 (2001).
• [78] G. Andersson, E. Lundgren, and H.P. Ekre, “Application of four anti-human interferon-alpha monoclonal antibodies for immunoassay and comparative analysis of natural interferon-alpha mixtures”, J. Interferon. Res. 11 (1), 53–60 (1991).
• [79] S.A. Darst, C.R. Robertson, and J.A. Berzofsky, “Adsorption of the protein antigen myoglobin affects the binding of conformation-specific monoclonal antibodies”, Biophys. J. 53 (4), 533–539 (1988).
• [80] M.J. Shields, J.N. Siegel, C.R. Clark, K.K. Hines, L.A. Potempa, H. Gewurz, and B. Anderson, “An appraisal of polystyrene-(ELISA) and nitrocellulose-based (ELIFA) enzyme immunoassay systems using monoclonal antibodies reactive toward antigenically distinct forms of human Creactive protein”, J. Immunol. Methods 141 (2), 253–261 (1991).
• [81] D.C. Hocking, R.K. Smith, and P.J. McKeown-Longo, “A novel role for the integrin-binding III-10 module in fibronectin matrix assembly”, J. Cell. Biol. 133 (2), 431–444 (1996).
• [82] M.A. Chernousov, F.J. Fogerty, V.E. Koteliansky, and D.F. Mosher, “Role of the I-9 and III-1 modules of fibronectin in formation of an extracellular fibronectin matrix”, J. Biol. Chem. 266 (17), 10851–10858 (1991).
• [83] P.Y. Meadows and G.C. Walker, “Force microscopy studies of fibronectin adsorption and subsequent cellular adhesion to substrates with well-defined surface chemistries”, Langmuir 21 (9), 4096–4107 (2005).
• [84] R.G. Rodrigues, N. Guo, L. Zhou, J.M. Sipes, S.B. Williams, N.S. Templeton, H.R. Gralnick, and D.D. Roberts, “Conformational regulation of the fibronectin binding and alpha 3beta 1 integrin-mediated adhesive activities of thrombospondin-1”, J. Biol. Chem. 276 (30), 27913–27922 (2001).
• [85] D.J. Iuliano, S.S. Saavedra, and G.A. Truskey, “Effect of the conformation and orientation of adsorbed fibronectin on endothelial cell spreading and the strength of adhesion”, J. Biomed. Mater. Res. 27 (8), 1103–1113 (1993).
• [86] M.M. Martino, M. Mochizuki, D.A. Rothenfluh, S.A. Rempel, J.A. Hubbell, and T.H. Barker, “Controlling integrin specificity and stem cell differentiation in 2D and 3D environments through regulation of fibronectin domain stability”, Biomaterials 30 (6), 1089–1097 (2009).
• [87] S. Bierbaum, U. Hempel, U. Geissler, T. Hanke, D. Scharnweber, K.W. Wenzel, and H. Worch, “Modification of Ti6AL4V surfaces using collagen I, III, and fibronectin. II. Influence on osteoblast responses”, J. Biomed. Mater. Res. A 67 (2), 431–438 (2003).
• [88] S. Bierbaum, R. Beutner, T. Hanke, D. Scharnweber, U. Hempel, and H. Worch, “Modification of Ti6Al4V surfaces using collagen I, III, and fibronectin, Biochemical and morphological characteristics of the adsorbed matrix”, J. Biomed. Mater. Res. A 67 (2), 421–430 (2003).
• [89] R. Jansen,W. Dzwolak, and R.Winter, “Amyloidogenic selfassembly of insulin aggregates probed by high resolution atomic force microscopy”, Biophys. J. 88 (2), 1344-1353 (2005).
• [90] M. Manno, E.F. Craparo, V. Martorana, D. Bulone, and P.L. San Biagio, “Kinetics of insulin aggregation: disentanglement of amyloid fibrillation from large-size cluster formation”, Biophys. J. 90 (12), 4585–4591 (2006).
• [91] M.B. Hovgaard, M. Dong, D.E. Otzen, and F. Besenbacher, “Quartz crystal microbalance studies of multilayer glucagon fibrillation at the solid-liquid interface”, Biophys. J. 93 (6), 2162–2169 (2007).
• [92] C. Goldsbury, J. Kistler, U. Aebi, T. Arvinte, and G.J. Cooper, “Watching amyloid fibrils grow by time-lapse atomic force microscopy”, J. Mol. Biol. 285 (1), 33–39 (1999).
• [93] S.S. Cheng, K.K. Chittur, C.N. Sukenic, L.A. Culp, and K. Lewandowska, “The conformation of fibronectin on selfassembled monolayers with different surface composition: An FTIR/ATR study”, J. Colloid Interface Sci. 162, 135–143 (1994).
• [94] M. Nocentini, R.M. Gendreau, and K.K. Chittur, “Conformational changes of protein adsorbed on polyurethane studied by FTIR-ATR spectroscopy”, Microchimica Acta 94, 343–347 (1988).
• [95] A. Sethuraman and G. Belfort, “Protein structural perturbation and aggregation on homogeneous surfaces”, Biophys. J. 88 (2), 1322–1333 (2005).
• [96] R. Khurana, C. Coleman, C. Ionescu-Zanetti, S.A. Carter, V. Krishna, R.K. Grover, R. Roy, and S. Singh, “Mechanism of thioflavin T binding to amyloid fibrils”, J. Struct. Biol. 151 (3), 229–238 (2005).
• [97] M.R. Krebs, E.H. Bromley, S.S. Rogers, and A.M. Donald, “The mechanism of amyloid spherulite formation by bovine insulin”, Biophys. J. 88 (3), 2013–2021 (2005).
• [98] U.B. Ericsson, B.M. Hallberg, G.T. Detitta, N. Dekker, and P. Nordlund, “Thermofluor-based high-throughput stability optimization of proteins for structural studies”, Anal. Biochem. 357 (2), 289–298 (2006).
• [99] M. Vedadi, F.H. Niesen, A. Allali-Hassani, O.Y. Fedorov, P.J. Finerty, Jr., G.A. Wasney, R. Yeung, C. Arrowsmith, T. Ballet, L. Boulange, Y. Brechet, F. Bruckert, and M. Weidenhaupt L.J. Ball, H. Berglund, R. Hui, B.D. Marsden, P. Nordlund, M. Sundstrom, J. Weigelt, and A.M. Edwards, “Chemical screening methods to identify ligands that promote protein stability, protein crystallization, and structure determination”, Proc. Natl. Acad. Sci. USA 103 (43), 15835–15840 (2006).
• [100] N. Ferraz, B. Nilsson, J. Hong, and M. Karlsson Ott, “Nanopore size affects complement activation”, J. Biomed. Mater. Res. A 87 (3), 575–581 (2008).
• [101] R.Y. Kannan, H.J. Salacinski, J. De Groot, I. Clatworthy, L. Bozec, M. Horton, P.E. Butler, and A.M. Seifalian, “The antithrombogenic potential of a polyhedral oligomeric silsesquioxane (POSS) nanocomposite”, Biomacromolecules 7 (1), 215–223 (2006).
• [102] V.A. Schulte, M. Diez, M. Moller, and M.C. Lensen, “Surface topography induces fibroblast adhesion on intrinsically nonadhesive poly(ethylene glycol) substrates”, Biomacromolecules 10 (10), 2795–2801 (2009).
• [103] S.E. Woodcock, W.C. Johnson, and Z. Chen, “Collagen adsorption and structure on polymer surfaces observed by atomic force microscopy”, J. Colloid Interface Sci. 292 (1), 99–107 (2005).
• [104] F. Luthen, R. Lange, P. Becker, J. Rychly, U. Beck, and J.G. Nebe, “The influence of surface roughness of titanium on beta1- and beta3-integrin adhesion and the organization of fibronectin in human osteoblastic cells”, Biomaterials 26 (15), 2423–2440 (2005).
• [105] T.J. Webster, C. Ergun, R.H. Doremus, R.W. Siegel, and R. Bizios, “Specific proteins mediate enhanced osteoblast adhesion on nanophase ceramics”, J. Biomed. Mater. Res. 51 (3), 475–483 (2000).
• [106] S.R. Whaley, D.S. English, E.L. Hu, P.F. Barbara, and A.M. Belcher, “Selection of peptides with semiconductor binding specificity for directed nanocrystal assembly”, Nature 405 (6787), 665–668 (2000).
• [107] C. Mao, C.E. Flynn, A. Hayhurst, R. Sweeney, J. Qi, G. Georgiou, B. Iverson, and A.M. Belcher, “Viral assembly of oriented quantum dot nanowires”, Proc. Natl. Acad. Sci. USA 100 (12), 6946–6951 (2003).
• [108] A.B. Sanghvi, K.P. Miller, A.M. Belcher, and C.E. Schmidt, “Biomaterials functionalization using a novel peptide that selectively binds to a conducting polymer”, Nat. Mater. 4 (6), 496–502 (2005).
• [109] G.L. Devlin, T.P. Knowles, A. Squires, M.G. McCammon, S.L. Gras, M.R. Nilsson, C.V. Robinson, C.M. Dobson, and C.E. MacPhee, “The component polypeptide chains of bovine insulin nucleate or inhibit aggregation of the parent protein in a conformation-dependent manner”, J. Mol. Biol. 360 (2), 497–509 (2006).
• [110] M.I. Ivanova, M.J. Thompson, and D. Eisenberg, “A systematic screen of beta(2)-microglobulin and insulin for amyloidlike segments”, Proc. Natl. Acad. Sci. USA 103 (11), 4079–4082 (2006).
• [111] P. Tito, E.J. Nettleton, and C.V. Robinson, “Dissecting the hydrogen exchange properties of insulin under amyloid fibril forming conditions: a site-specific investigation by mass spectrometry”, J. Mol. Biol. 303 (2), 267–278 (2000).
• [112] M.I. Ivanova, S.A. Sievers, M.R. Sawaya, J.S. Wall, and D. Eisenberg, “Molecular basis for insulin fibril assembly”, Proc. Natl. Acad. Sci. USA 106 (45), 18990–18995 (2009).
• [113] S. Gunther, P. May, A. Hoppe, C. Frommel, and R. Preissner, “Docking without docking: ISEARCH–prediction of interactions using known interfaces”, Proteins 69 (4), 839–844 (2007).
• [114] S.R. Comeau, D.W. Gatchell, S. Vajda, and C.J. Camacho, “ClusPro: an automated docking and discrimination method for the prediction of protein complexes”, Bioinformatics 20 (1), 45–50 (2004).
• [115] S.S. Negi, C.H. Schein, N. Oezguen, T.D. Power, and W. Braun, “InterProSurf: a web server for predicting interacting sites on protein surfaces”, Bioinformatics 23 (24), 3397–3399 (2007).
• [116] S.J. de Vries and A.M. Bonvin, “Intramolecular surface contacts contain information about protein-protein interface regions”, Bioinformatics 22 (17), 2094–2098 (2006).
• [117] H. Neuvirth, R. Raz, and G. Schreiber, “ProMate: a structure based prediction program to identify the location of protein-protein binding sites”, J. Mol. Biol. 338 (1), 181–199 (2004).
• [118] N.J. Burgoyne and R.M. Jackson, “Predicting protein interaction sites: binding hotspots in protein-protein and proteinligand interfaces”, Bioinformatics 22 (11), 1335–1342 (2006).
• [119] D.W. Ritchie, “Recent progress and future directions in protein-protein docking”, Curr. Protein Pept. Sci. 9 (1), 1–15 (2008).
• [120] P. Han, X. Zhang, R.S. Norton, and Z.P. Feng, “Large-scale prediction of long disordered regions in proteins using random forests”, BMC Bioinformatics 10, 8 (2009).
• [121] C.T. Su, C.Y. Chen, and C.M. Hsu, “iPDA: integrated protein disorder analyzer”, Nucleic Acids Res. 35, W465–472 (2007).
• [122] O.V. Galzitskaya, S.O. Garbuzynskiy, and M.Y. Lobanov, “FoldUnfold: web server for the prediction of disordered regions in protein chain”, Bioinformatics 22 (23), 2948–2949 (2006).
• [123] C.T. Su, C.Y. Chen, and Y.Y. Ou, “Protein disorder prediction by condensed PSSM considering propensity for order or disorder”, BMC Bioinformatics 7, 319 (2006).
• [124] J. Cheng, A.Z. Randall, M.J. Sweredoski, and P. Baldi, “SCRATCH: a protein structure and structural feature prediction server”, Nucleic Acids Res. 33 (Web Server issue), W72–76 (2005).
• [125] Z. Dosztanyi, V. Csizmok, P. Tompa, and I. Simon, “IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content”, Bioinformatics 21 (16), 3433–3434 (2005).
• [126] Z.R. Yang, R. Thomson, P. McNeil, and R.M. Esnouf, “RONN: the bio-basis function neural network technique applied to the detection of natively disordered regions in proteins”, Bioinformatics 21 (16), 3369–3376 (2005).
• [127] F. Ferron, S. Longhi, B. Canard, and D. Karlin, “A practical overview of protein disorder prediction methods”, Proteins 65 (1), 1–14 (2006).
• [128] A. Trovato, F. Seno, and S.C. Tosatto, “The PASTA server for protein aggregation prediction”, Protein Eng. Des Sel 20 (10), 521–523 (2007).
• [129] A.M. Fernandez-Escamilla, F. Rousseau, J. Schymkowitz, and L. Serrano, “Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins”, Nat. Biotechnol. 22 (10), 1302–1306 (2004).
• [130] G.G. Tartaglia and M. Vendruscolo, “The Zyggregator method for predicting protein aggregation propensities”, Chem. Soc. Rev. 37 (7), 1395–1401 (2008).
• [131] F. Rousseau, J. Schymkowitz, and L. Serrano, “Protein aggregation and amyloidosis: confusion of the kinds?”, Curr. Opin. Struct. Biol. 16 (1), 118–126 (2006).
• [132] E. Monsellier, M. Ramazzotti, P.P. de Laureto, G.G. Tartaglia, N. Taddei, A. Fontana, M. Vendruscolo, and F. Chiti, “The distribution of residues in a polypeptide sequence is a determinant of aggregation optimized by evolution”, Biophys. J. 93 (12), 4382–4391(2007).
• [133] G.D. Smith, W.A. Pangborn, and R.H. Blessing, “The structure of T6 bovine insulin”, Acta Crystallogr D Biol. Crystallogr. 61 (Pt 11), 1476–1482 (2005).
• [134] G.D. Smith, W.A. Pangborn, and R.H. Blessing, “Phase changes in T(3)R(3)(f) human insulin: temperature or pressure induced?”, Acta Crystallogr. D Biol Crystallogr. 57 (Pt 8), 1091–1100 (2001).
• [135] G.D. Smith, E. Ciszak, L.A. Magrum, W.A. Pangborn, and R.H. Blessing, “R6 hexameric insulin complexed with mcresol or resorcinol”, Acta Crystallogr. D Biol. Crystallogr. 56 (Pt 12), 1541–1548 (2000).
• [136] Z.P. Yao, Z.H. Zeng, H.M. Li, Y. Zhang, Y.M. Feng, and D.C. Wang, “Structure of an insulin dimer in an orthorhombic crystal: the structure analysis of a human insulin mutant (B9 Ser–¿Glu)”, Acta Crystallogr. D Biol. Crystallogr. 55 (Pt 9), 1524–1532 (1999).
• [137] J.L. Whittingham, D.J. Scott, K. Chance, A. Wilson, J. Finch, J. Brange, and G. Guy Dodson, “Insulin at pH 2: structural analysis of the conditions promoting insulin fibre formation”, J. Mol. Biol. 318 (2), 479–490 (2002).
• [138] H.B. Olsen, S. Ludvigsen, and N.C. Kaarsholm, “Solution structure of an engineered insulin monomer at neutral pH”, Biochemistry 35 (27), 8836–8845 (1996).
• [139] J.L. Moreland, A. Gramada, O.V. Buzko, Q. Zhang, and P.E. Bourne, “The Molecular Biology Toolkit (MBT): a modular platform for developing molecular visualization applications”, BMC Bioinformatics 6, 21 (2005).