Covalent immobilization of hLf1-11 peptide on a titanium surface reduces bacterial adhesion and biofilm formation

Acta Biomaterialia

Volumn 10, Issue 8, 2014, Pages 3522-3534

  Godoy Gallardo, Maria ^a,b   Mas Moruno, Carlos ^a,b   Fernández Calderón, María C ^b,c   Pérez Giraldo, Ciro ^b,c   Manero, José M ^a,b   Albericio, Fernando ^d,e,f   Gil, Francisco J ^a,b   Rodríguez, Daniel ^a,b  

^a UNIVERSITAT POLITÈCNICA DE CATALUNYA   (Spain)

^b BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^c UNIVERSITY OF EXTREMADURA   (Spain)

^d INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^e UNIVERSITY OF BARCELONA   (Spain)

^f UNIVERSITY OF KWAZULU NATAL   (South Africa)

Author keywords

Antimicrobial peptide; Bacterial adhesion; Biofunctionalization; Lactoferrin peptide; Titanium

Indexed keywords

ADHESION; BACTERIA; BIOFILMS; CELL CULTURE; TITANIUM; X RAY PHOTOELECTRON SPECTROSCOPY;

ADHESION FORMATIONS; ANTIMICROBIAL PEPTIDE; BACTERIAL ADHESION; BACTERIAL BIOFILM; BIOFILM FORMATION; BIOFUNCTIONALIZATION; COVALENT IMMOBILIZATION; LACTOFERRIN; LACTOFERRIN PEPTIDE; TITANIA SURFACES;

PEPTIDES;

HUMAN LACTOFERRIN 1-11; LACTATE DEHYDROGENASE; LACTOFERRIN; POLYPEPTIDE ANTIBIOTIC AGENT; TITANIUM; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BIOMATERIAL; LACTOFERRIN (1-11), HUMAN; PEPTIDE FRAGMENT; PROTEIN BINDING;

ADSORPTION; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIUM ADHERENCE; BIOFILM; CELL VIABILITY; CONTACT ANGLE; CONTROLLED STUDY; COVALENT BOND; ENZYME ASSAY; FIBROBLAST; GROWTH INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; LACTOBACILLUS SALIVARIUS; MORPHOLOGY; NONHUMAN; PLANKTON; PRIORITY JOURNAL; PROTEIN IMMOBILIZATION; STREPTOCOCCUS SANGUINIS; SURFACE PROPERTY; X RAY PHOTOELECTRON SPECTROSCOPY; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; MATERIALS TESTING; PHYSIOLOGY; SYNTHESIS;

BACTERIA (MICROORGANISMS); LACTOBACILLUS SALIVARIUS; STREPTOCOCCUS SANGUINIS;

ADSORPTION; ANTI-INFECTIVE AGENTS; BACTERIAL ADHESION; BIOFILMS; CELL SURVIVAL; COATED MATERIALS, BIOCOMPATIBLE; LACTOFERRIN; MATERIALS TESTING; PEPTIDE FRAGMENTS; PROTEIN BINDING; SURFACE PROPERTIES; TITANIUM;

EID: 84903708326     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.03.026     Document Type: Article

References (71)

1. W. Ahmed, and K. Subramani Emerging Nanotechnologies in Dentistry: Materials, Processes, and Applications 2012 William Andrew New York
2. S. Bauer, P. Schmuki, K. von der Mark, and J. Park Engineering biocompatible implant surfaces: Part I: materials and surfaces Prog Mater Sci 58 2013 261 326
3. H. Algraffee, F. Borumandi, and L. Cascarini Peri-implantitis Br J Oral Maxillofac Surg 50 2012 689 694
4. Z.H. Baqain, W.Y. Moqbel, and F.A. Sawair Early dental implant failure: risk factors Br J Oral Maxillofac Surg 50 2012 239 243
5. A. Piattelli, A. Scarano, and M. Piattelli Microscopical aspects of failure in osseointegrated dental implants: a report of five cases Biomaterials 17 1996 1235 1241
6. A.D. Pye, D.E.A. Lockhart, M.P. Dawson, C.A. Murray, and A.J. Smith A review of dental implants and infection J Hosp Infect 72 2009 104 110
7. P.E. Kolenbrander, R.N. Andersen, and L.V. Moore Intrageneric coaggregation among strains of human oral bacteria: potential role in primary colonization of the tooth surface Appl Environ Microbiol 56 1990 3890 3894
8. P.E. Kolenbrander, and J. London Adhere today, here tomorrow: oral bacterial adherence J Bacteriol 175 1993 3247 3252
9. K. Hori, and S. Matsumoto Bacterial adhesion: from mechanism to control Biochem Eng J 48 2010 424 434
10. G. Mayanagi, T. Sato, H. Shimauchi, and N. Takahashi Microflora profiling of subgingival and supragingival plaque of healthy and periodontitis subjects by nested PCR Int Congr Ser 1284 2005 195 196
11. L.C. Pham, R.J.M. van Spanning, W.F.M. Röling, A.C. Prosperi, Z. Terefework, and J.M. Ten Cate et al. Effects of probiotic Lactobacillus salivarius W24 on the compositional stability of oral microbial communities Arch Oral Biol 54 2009 132 137
12. S.P. Galanakos, S.A. Papadakis, K. Kateros, I. Papakostas, and G. Macheras Biofilm and orthopaedic practice: the world of microbes in a world of implants Orthop Trauma 23 2009 175 179
13. B. Klinge, M. Hultin, and T. Berglundh Peri-implantitis Dent Clin North Am 49 2005 661 676 vii-viii
14. M.M. Fürst, G.E. Salvi, N.P. Lang, and G.R. Persson Bacterial colonization immediately after installation on oral titanium implants Clin Oral Implants Res 18 2007 501 508
15. Z. Artzi, H. Tal, O. Moses, and A. Kozlovsky Mucosal considerations for osseointegrated implants J Prosthet Dent 70 1993 427 432
16. K. Glinel, P. Thebault, V. Humblot, C.M. Pradier, and T. Jouenne Antibacterial surfaces developed from bio-inspired approaches Acta Biomater 8 2012 1670 1684
17. I. Banerjee, R.C. Pangule, and R.S. Kane Antifouling coatings: recent developments in the design of surfaces that prevent fouling by proteins, bacteria, and marine organisms Adv Mater 23 2011 690 718
18. L. Zhao, P.K. Chu, Y. Zhang, and Z. Wu Antibacterial coatings on titanium implants J Biomed Mater Res B Appl Biomater 91B 2009 470 480
19. J. Hasan, R.J. Crawford, and E.P. Ivanova Antibacterial surfaces: the quest for a new generation of biomaterials Trends Biotechnol 31 2013 295 304
20. F. Costa, I.F. Carvalho, R.C. Montelaro, P. Gomes, and M.C.L. Martins Covalent immobilization of antimicrobial peptides (AMPs) onto biomaterial surfaces Acta Biomater 7 2011 1431 1440
21. S.A. Onaizi, and S.S.J. Leong Tethering antimicrobial peptides: current status and potential challenges Biotechnol Adv 29 2011 67 74
22. K.V. Holmberg, M. Abdolhosseini, Y. Li, X. Chen, S.-U. Gorr, and C. Aparicio Bio-inspired stable antimicrobial peptide coatings for dental applications Acta Biomater 9 2013 8224 8231
23. R. Chen, M.D.P. Willcox, N. Cole, K.K.K. Ho, R. Rasul, and J.A. Denman et al. Characterization of chemoselective surface attachment of the cationic peptide melimine and its effects on antimicrobial activity Acta Biomater 8 2012 4371 4379
24. H. Jenssen, and R.E.W. Hancock Antimicrobial properties of lactoferrin Biochimie 91 2009 19 29
25. K.V.R. Reddy, R.D. Yedery, and C. Aranha Antimicrobial peptides: premises and promises Int J Antimicrob Agents 24 2004 536 547
26. M. Pasupuleti, A. Schmidtchen, and M. Malmsten Antimicrobial peptides: key components of the innate immune system Crit Rev Biotechnol 32 2012 143 171
27. A.M. Bouchet, N.B. Iannucci, M.B. Pastrian, O. Cascone, N.C. Santos, and E.A. Disalvo et al. Biological activity of antibacterial peptides matches synergism between electrostatic and non electrostatic forces Colloids Surf B Biointerfaces 114 2014 363 371
28. R.R. Arnold, M.F. Cole, and J.R. McGhee A bactericidal effect for human lactoferrin Science 197 1977 263 265
29. F. Berlutti, F. Pantanella, T. Natalizi, A. Frioni, R. Paesano, and A. Polimeni et al. Antiviral properties of lactoferrin - a natural immunity molecule Molecules 16 2011 6992 7018
30. C.H. Kirkpatrick, I. Green, R.R. Rich, and A.L. Schade Inhibition of growth of Candida albicans by iron-unsaturated lactoferrin: relation to host-defense mechanisms in chronic mucocutaneous candidiasis J Infect Dis 124 1971 539 544
31. T. Soukka, J. Tenovuo, and M. Lenander-Lumikari Fungicidal effect of human lactoferrin against Candida albicans FEMS Microbiol Lett 69 1992 223 228
32. G.A. Weinberg Iron chelators as therapeutic agents against Pneumocystis carinii Antimicrob Agents Chemother 38 1994 997 1003
33. W. Bellamy, M. Takase, H. Wakabayashi, K. Kawase, and M. Tomita Antibacterial spectrum of lactoferricin B, a potent bactericidal peptide derived from the N-terminal region of bovine lactoferrin J Appl Bacteriol 73 1992 472 479
34. C.-C. Yen, C.-J. Shen, W.-H. Hsu, Y.-H. Chang, H.-T. Lin, and H.-L. Chen et al. Lactoferrin: an iron-binding antimicrobial protein against Escherichia coli infection BioMetals 24 2011 585 594
35. H. Ulvatne, H.H. Haukland, Ø. Olsvik, and L.H. Vorland Lactoferricin B causes depolarization of the cytoplasmic membrane of Escherichia coli ATCC 25922 and fusion of negatively charged liposomes FEBS Lett 492 2001 62 65
36. L.H. Vorland, H. Ulvatne, O. Rekdal, and J.S. Svendsen Initial binding sites of antimicrobial peptides in Staphylococcus aureus and Escherichia coli Scand J Infect Dis 31 1999 467 473
37. C.P.J.M. Brouwer, M. Rahman, and M.M. Welling Discovery and development of a synthetic peptide derived from lactoferrin for clinical use Peptides 32 2011 1953 1963
38. W.J. van der Velden, T.M. van Iersel, N.M. Blijlevens, and J.P. Donnelly Safety and tolerability of the antimicrobial peptide human lactoferrin 1-11 (hLF1-11) BMC Med 7 2009 44
39. C. Mas-Moruno, P.M. Dorfner, F. Manzenrieder, S. Neubauer, U. Reuning, and R. Burgkart et al. Behavior of primary human osteoblasts on trimmed and sandblasted Ti6Al4V surfaces functionalized with integrin αvβ3- selective cyclic RGD peptides J Biomed Mater Res A 101A 2013 87 97
40. H.M. Kim, F. Miyaji, T. Kokubo, and T. Nakamura Effect of heat treatment on apatite-forming ability of Ti metal induced by alkali treatment J Mater Sci Mater Med 8 1997 341 347
41. X. Chen, P. Sevilla, and C. Aparicio Surface biofunctionalization by covalent co-immobilization of oligopeptides Colloids Surf B Biointerfaces 107 2013 189 197
42. S.J. Xiao, M. Textor, N.D. Spencer, M. Wieland, B. Keller, and H. Sigrist Immobilization of the cell-adhesive peptide Arg-Gly-Asp-Cys (RGDC) on titanium surfaces by covalent chemical attachment J Mater Sci Mater Med 8 1997 867 872
43. S.-J. Xiao, M. Textor, N.D. Spencer, and H. Sigrist Covalent attachment of cell-adhesive, (Arg-Gly-Asp)-containing peptides to titanium surfaces Langmuir 14 1998 5507 5516
44. J. Peltonen, M. Järn, S. Areva, M. Linden, and J.B. Rosenholm Topographical parameters for specifying a three-dimensional surface Langmuir 20 2004 9428 9431
45. E.S. Gadelmawla, M.M. Koura, T.M.A. Maksoud, I.M. Elewa, and H.H. Soliman Roughness parameters J Mater Process Technol 123 2002 133 145
46. D.K. Owens, and R.C. Wendt Estimation of the surface free energy of polymers J Appl Polym Sci 13 1969 1741 1747
47. S.D. Puckett, E. Taylor, T. Raimondo, and T.J. Webster The relationship between the nanostructure of titanium surfaces and bacterial attachment Biomaterials 31 2010 706 713
48. A. Lupetti, M.M. Welling, E.K. Pauwels, and P.H. Nibbering Radiolabelled antimicrobial peptides for infection detection Lancet Infect Dis 3 2003 223 229
49. R. Müller, J. Abke, E. Schnell, D. Scharnweber, R. Kujat, and C. Englert et al. Influence of surface pretreatment of titanium- and cobalt-based biomaterials on covalent immobilization of fibrillar collagen Biomaterials 27 2006 4059 4068
50. Guha Thakurta S, Subramanian A. Fabrication of dense, uniform aminosilane monolayers: a platform for protein or ligand immobilization. Colloids Surf Physicochem Eng Asp 2012;414:384-92.
51. N.J. Hickok, and I.M. Shapiro Immobilized antibiotics to prevent orthopaedic implant infections Adv Drug Deliv Rev 64 2012 1165 1176
52. S.-H. Yoon, and M.R.K. Mofrad Cell adhesion and detachment on gold surfaces modified with a thiol-functionalized RGD peptide Biomaterials 32 2011 7286 7296
53. Y. Ding, Y.-Y. Zhou, H. Chen, D.-D. Geng, D.-Y. Wu, and J. Hong et al. The performance of thiol-terminated PEG-paclitaxel-conjugated gold nanoparticles Biomaterials 34 2013 10217 10227
54. Y. Han, D. Mayer, A. Offenhäusser, and S. Ingebrandt Surface activation of thin silicon oxides by wet cleaning and silanization Thin Solid Films 510 2006 175 180
55. A. Rodríguez-Hernández, E. Espinar, J.M. Llamas, J.M. Barrera, and F.J. Gil Alumina shot-blasted particles on commercially pure titanium surfaces prevent bacterial attachment Mater Lett 92 2013 42 44
56. M.E. Barbour, D.J. O'Sullivan, H.F. Jenkinson, and D.C. Jagger The effects of polishing methods on surface morphology, roughness and bacterial colonisation of titanium abutments J Mater Sci Mater Med 18 2007 1439 1447
57. M. Grivet, J.J. Morrier, G. Benay, and O. Barsotti Effect of hydrophobicity on in vitro streptococcal adhesion to dental alloys J Mater Sci Mater Med 11 2000 637 642
58. K.A. Strevett, and G. Chen Microbial surface thermodynamics and applications Res Microbiol 154 2003 329 335
59. E.M. Harnett, J. Alderman, and T. Wood The surface energy of various biomaterials coated with adhesion molecules used in cell culture Colloids Surf B Biointerfaces 55 2007 90 97
60. L. Bacakova, E. Filova, M. Parizek, T. Ruml, and V. Svorcik Modulation of cell adhesion, proliferation and differentiation on materials designed for body implants Biotechnol Adv 29 2011 739 767
61. M. Pegueroles, F.J. Gil, J.A. Planell, and C. Aparicio The influence of blasting and sterilization on static and time-related wettability and surface-energy properties of titanium surfaces Surf Coat Technol 202 2008 3470 3479
62. S.D. Techane, L.J. Gamble, and D.G. Castner X-ray photoelectron spectroscopy characterization of gold nanoparticles functionalized with amine-terminated alkanethiols Biointerphases 6 2011 98
63. D.G. Castner, and K. Hinds Graigner DW.X-ray Photoelectron spectroscopy sulfur 2p study of organic thiol and disulfide binding interactions with gold surfaces Langmuir 12 1996 5083 5086
64. C. Vahlberg, M. Linares, S. Villaume, P. Norman, and K. Uvdal Noradrenaline and a thiol analogue on gold surfaces: an infrared reflection-absorption spectroscopy, X-ray photoelectron spectroscopy, and near-edge X-ray absorption fine structure spectroscopy study J Phys Chem C 115 2011 165 175
65. P.M. Dietrich, T. Horlacher, P.-L. Girard-Lauriault, T. Gross, A. Lippitz, and H. Min et al. Adlayers of dimannoside thiols on gold: surface chemical analysis Langmuir ACS J Surf Colloids 27 2011 4808 4815
66. K. Jans, K. Bonroy, R. De Palma, G. Reekmans, H. Jans, and W. Laureyn et al. Stability of mixed PEO-thiol SAMs for biosensing applications Langmuir ACS J Surf Colloids 24 2008 3949 3954
67. A.H. Rickard, A.J. McBain, R.G. Ledder, P.S. Handley, and P. Gilbert Coaggregation between freshwater bacteria within biofilm and planktonic communities FEMS Microbiol Lett 220 2003 133 140
68. J.D. Bryers, and B.D. Ratner Biomaterials approaches to combating oral biofilms and dental disease BMC Oral Health 6 2006 S15
69. M. Shafahi, and K. Vafai Synthesis of biofilm resistance characteristics against antibiotics Int J Heat Mass Transf 53 2010 2943 2950
70. H.P. Stallmann, C. Faber, A.L.J.J. Bronckers, J.M.A. de Blieck-Hogervorst, C.P.J.M. Brouwer, and A.V.N. Amerongen et al. Histatin and lactoferrin derived peptides: antimicrobial properties and effects on mammalian cells Peptides 26 2005 2355 2359
71. L.T. Eliassen, G. Berge, A. Leknessund, M. Wikman, I. Lindin, and C. Løkke et al. The antimicrobial peptide, lactoferricin B, is cytotoxic to neuroblastoma cells in vitro and inhibits xenograft growth in vivo Int J Cancer J Int Cancer 119 2006 493 500