Antimicrobial peptide coatings for hydroxyapatite: Electrostatic and covalent attachment of antimicrobial peptides to surfaces

Journal of the Royal Society Interface

Volumn 14, Issue 126, 2017, Pages

  Townsend, Leigh ^a   Williams, Richard L ^a,c   Anuforom, Olachi ^a   Berwick, Matthew R ^a   Halstead, Fenella ^b,c   Hughes, Erik ^a   Stamboulis, Artemis ^a   Oppenheim, Beryl ^b,c   Gough, Julie ^d   Grover, Liam ^a,c   Scott, Robert A H ^c   Webber, Mark ^a,c   Peacock, Anna F A ^a   Belli, Antonio ^a,c   Logan, Ann ^a,c   De Cogan, Felicity ^a,c  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY HOSPITALS BIRMINGHAM NHS FOUNDATION TRUST   (United Kingdom)

^c QUEEN ELIZABETH HOSPITAL   (United Kingdom)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Antimicrobial; Device tissue interface; Surface engineering

Indexed keywords

BACTERIA; CELL ADHESION; ELECTROSTATIC COATINGS; HYDROXYAPATITE; INTERFACES (MATERIALS); MICROORGANISMS; PEPTIDES; POLYPEPTIDES; TISSUE; TISSUE ENGINEERING;

ANTIMICROBIAL; ANTIMICROBIAL PEPTIDE; BACTERIAL COLONIZATION; COVALENT ATTACHMENT; COVALENTLY BONDED; GRAM-NEGATIVE BACTERIA; SURFACE ENGINEERING; TISSUE INTERFACE;

COATINGS;

HYDROXYAPATITE; POLYPEPTIDE ANTIBIOTIC AGENT; ANTIMICROBIAL CATIONIC PEPTIDE; BIOCOMPATIBLE COATED MATERIAL;

ANIMAL CELL; ARTICLE; BACTERIUM ISOLATE; CELL ADHESION; CONTROLLED STUDY; COVALENT BOND; NONHUMAN; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; SURFACE PROPERTY; ANIMAL; CELL LINE; CHEMISTRY; CYTOLOGY; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; GROWTH, DEVELOPMENT AND AGING; MATERIALS TESTING; METABOLISM; MOUSE; OSTEOBLAST; STATIC ELECTRICITY;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL LINE; COATED MATERIALS, BIOCOMPATIBLE; DURAPATITE; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; MATERIALS TESTING; MICE; OSTEOBLASTS; STATIC ELECTRICITY;

EID: 85011586753     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2016.0657     Document Type: Article

References (56)

1. Whitehouse JD, Friedman ND, Kirkland KB, Richardson WJ, Sexton DJ. 2002 The impact of surgical-site infections following orthopaedic surgery at a community hospital and a university hospital: adverse quality of life, excess length of stay and extra cost. Infect. Control Hosp. Epidimiol. 23, 183-189. (doi:10.1086/502033)
2. Noroozi H, Kazemi A, Fadee R, Alavi S, Mohammadzadeh M. 2010 Microbiological assessment of nonsurgical traumatic wound infections and surgical site infections in hospitalised patients. Iran. J. Clin. Infect. Disease 5, 80-83.
3. Philips JE, Crane TP, Noy M, Elliott TSJ, Grimer RJ. 2006 The incidence of deep prosthetic infections in a specialist orthopaedic hospital. J. Bone Joint Surg. 88-B, 943-948. (doi:10.1302/0301-620X.88B7.17150)
4. Song Z, Borgwardt L, Hoiby N, Wu H, Sorensen TS, Borgwardt A. 2013 Prosthesis infections after orthopaedic joint replacement: the possible role of bacterial biofilms. Orthop. Rev. 5, e14. (doi:10.4081/or.2013.e14)
5. Funao H et al. 2016 A novel hydroxyapatite film coated with ionic silver via inositol hexaphosphate chelation prevents implant-associated infection. Sci. Rep. 6, 23238. (doi:10.1038/srep23238)
6. Zapotoczna M, O'Neill E, O'Gara JP. 2016 Untangling the diverse and redundant mechanisms of Staphylococcus aureus biofilm formation. PLoS Pathog. 12, e1005671. (doi:10.1371/journal.ppat.1005671)
7. Moran E, Byren I, Atkins BL. 2010 The diagnosis and management of prosthetic joint infections. J. Antimicrob. Chemother. 65, 45-54. (doi:10.1093/jac/dkq305)
8. Uesenko M, Windhager R, Kontekakis A, Hanstein T, Kuehn K-D. 2016 Risk factors for periprosthetic joint infections following primary total hip arthroplasty. Univ. J. Med. Sci. 4, 38-44. (doi:10.13189/ujmsj. 2016.040105)
9. Geetha M, Singh AK, Asokamani R, Gogia AK. 2009 Ti based biomaterials, the ultimate choice for orthopaedic implants-a review. Prog. Mater Sci. 54, 397-425. (doi:10.1016/j.pmatsci.2008.06.004)
10. l-Sanabani JS, Madfa AA, Al-Sanabani FA. 2013 Application of calcium phosphate materials in dentistry. Int. J. Biomater. 2013, 876132.
11. Shamsul JB, Nurhidayah AZ, Ruzaidi CM. 2007 Characterization of cobalt-chromium-HAP biomaterial for biomedical application. J. Appl. Sci. Res. 3, 1544-1553.
12. Vahabzadeh S, Roy M, Bandyopadhyay A, Bose S. 2015 Phase stability and biological property evaluation of plasma sprayed hydroxyapatite coatings for orthopaedic and dental applications. Acta Biomater. 17, 47-55. (doi:10.1016/j.actbio. 2015.01.022)
13. Chambers B, St Clair SF, Froimson MI. 2007 Hydroxyapatite-coated tapered cementless femoral components in total hip arthroplasty. J. Arthroplasty 22(4 Suppl. 1), 71-74. (doi:10.1016/j.arth.2007.01.019)
14. Ferreira A, Aslanian T, Dalin T, Picaud J. 2016 Ceramic bearings with bilayer coating in cementless total hip arthroplasty. A safe solution. A retrospective study of one hundred and twenty six cases with more than ten years follow-up. Int. Orthop. 1, 1-7. (doi:10.1007/s00264-016-3271-7)
15. Xu Q, Zhang W, Dong C, Sreeprassad TS, Xia Z. 2016 Biomimetic self-cleaning surfaces: synthesis, mechanism and application. J. R. Soc. Interface 13, 1-12. (doi:10.1098/rsif.2016.0300)
16. Nithyanandan A, Suntharavathanan M, Huang J, Rehman S, Draper E, Edirisinghe M. 2015 Bioinspired electrohydrodynamic ceramic patterning of curved metallic substrates. Bioinsp. Biomim. Nanobiomater. 4, 59-67. (doi:10.1680/bbn.14. 00020)
17. Boccaccini AR, Keim S, Ma R, Li Y, Zhitomirsky I. 2010 Electrophoretic deposition of biomaterials. J. R. Soc. Interface 7, 581-613. (doi:10.1098/rsif. 2010.0156.focus)
18. Zhang S, Karaca BT, VanOosten SK, Yuca E, Mahalingam S, Edirisinghe M, Tamerler C. 2015 Coupling infusion and gyration for the nanoscale assembly of functional polymer nanofibers integrated with genetically engineered proteins. Macromol. Rapid Commun. 36, 1322-1328. (doi:10. 1002/marc.201500174)
19. Xu Z, Mahalingam S, Rohn JL, Ren G, Edirisinghe M. 2015 Physico-chemical and antibacterial characteristics of pressure spun nylon nanofibers embedded with functional silver nanoparticles. Mater. Sci. Eng. C 56, 195-204. (doi:10.1016/j. msec.2015.06.003)
20. Taha M, Chai F, Blanchemain N, Neut C, Goube M, Maton M, Martel B, Hildebrand HF. 2014 Evaluation of sorption capacity of antibiotic and antibacterial properties of a cyclodextrin-polymer functionalised hydroxyapatite-coated titanium hip prosthesis. Int. J. Pharm. 477, 380-389. (doi:10.1016/j. ijpharm.2014.10.026)
21. He S, Zhou P, Wang L, Xiong X, Zhang Y, Deng Y, Wei S. 2014 Antibiotic-decorated titanium with enhanced antibacterial activity through adhesive polydopamine for dental/bone implant. J. R. Soc. Interface 11, 20140169. (doi:10.1098/rsif. 2014.0169)
22. Lischer S, Korner E, Balaza DJ, Shen D, Wick P, Grieder K, Haas D, Heuberger M, Hegemann D. 2011 Antibacterial burst-release from minimal Agcontaining plasma polymer coatings. J. R. Soc. Interface 8, 1019-1030. (doi:10.1098/rsif. 2010.0596)
23. Cattalini JP, Hoppe A, Pishbin F, Roether J, Boccaccini AR, Lucangioli S, Mourino V. 2015 Novel nanocomposite biomaterials with controlled copper/calcium release capability for bone tissue engineering multifunctional scaffolds. J. R. Soc. Interface 12, 20150509. (doi:10.1098/rsif.2015.0509)
24. Nowlin K, Boseman A, Covell A, LaJeunesse D. 2015 Adhesion-dependent rupturing of Saccharomyces cerevisiae on biological antimicrobial nanostructured surfaces. J. R. Soc. Interface 12, 20140999. (doi:10. 1098/rsif.2014.0999)
25. Díaz M, Barba F, Miranda M, Guitian F, Torrecillas R, Moya JS. 2009 Synthesis and antimicrobial activity of a silver-hydroxyapatite nanocomposite. J. Nanomater. 2009, 498505. (doi:10.1155/2009/498505)
26. Lu X et al. 2011 Nano-Ag-loaded hydroxyapatite coatings on titanium surfaces by electrochemical deposition. J. R. Soc. Interface 8, 529-539. (doi:10. 1098/rsif.2010.0366)
27. Behra R, Sigg L, Clift MJD, Herzog F, Minghetti M, Johnston B, Petri-Fink A, Rothen-Rutishauser B. 2013 Bioavailability of silver nanoparticles and ions: from a chemical and biochemical perspective. J. R. Soc. Interface 10, 20130396. (doi:10.1098/rsif. 2013.0396)
28. Hsueh P-R, Chen W-H, Luh K-T. 2005 Relationships between antimicrobial use and antimicrobial resistance in gram-negative bacteria causing nosocomial infections from 1991-2003 at a university hospital in Taiwan. Int. J. Antimicrob. Agents 26, 463-472. (doi:10.1016/j.ijantimicag. 2005.08.016)
29. Nguyen TL, Haney EF, Vogel HJ. 2011 The expanding scope of antimicrobial peptide structures and their modes of action. Trends Biotechnol. 29, 464-472. (doi:10.1016/j.tibtech.2011.05.001)
30. Wimley WC, Hristova K. 2011 Antimicrobial peptides; successes, challenges and unanswered questions. J. Membr. Biol. 239, 27-34. (doi:10. 1007/s00232-011-9343-0)
31. Zhang BG, Myers DE, Wallace GG, Brandt M, Choong P. 2014 Bioactive coatings for orthopaedic implants-recent trends in development of implant coatings. Int. J. Mol. Sci. 15, 11 878-11 892. (doi:10.3390/ijms150711878)
32. Mishra B, Basu A, Chua RRY, Saravanan R, Tambyah PA, Ho B, Chang MW, Leong SSJ. 2014 Site specific immobilization of a potent antimicrobial peptide onto silicone catheters: evaluation against urinary tract infection pathogens. J. Mater. Chem. B 2, 1706-1716. (doi:10.1039/c3tb21300e)
33. Veldhuizen EJA, Schneider VAF, Agustiandari H, van Dijk A, Tjeerdsma-van Bokhoven JLM, Bikker FJ, Haagsman HP. 2014 Antimicrobial and immunomodulatory activities of PR-39 derived peptides. PLoS ONE 9, 1-7. (doi:10.1371/journal. pone.0095939)
34. Steinstraesser L, Kraneburg U, Jacobsen F, Al-Benna S. 2011 Host defence peptides and their antimicrobial-immunomodulatory duality. Immunobiology 216, 322-333. (doi:10.1016/j. imbio.2010.07.003)
35. Huby RDJ, Dearman RJ, Kimber I. 2000 Why are some proteins allergens? Toxicol. Sci. 55, 235-246. (doi:10.1093/toxsci/55.2.235)
36. Chairatana P, Chu H, Castillo PA, Shen B, Bevins CL, Nolan EM. 2016 Proteolysis triggers self-assembly and unmasks innate immune function of a human defensin peptide. Chem. Sci. 7, 1738-1752. (doi:10. 1039/C5SC04194E)
37. Chileveru HR, Lim SA, Chairatana P, Wommack AJ, Chiang I-L, Nolan EM. 2015 Visualising attack of Escherichia coli by the antimicrobial peptide human defensin 5. Biochemistry 54, 1767-1777. (doi:10. 1021/bi501483q)
38. Rigano MM et al. 2012 A novel synthetic peptide from a tomato defensin exhibits antibacterial activities against Helicobacter pylori. J. Pept. Sci. 18, 755-762. (doi:10.1002/psc.2462)
39. Scudiero O et al. 2010 Novel synthetic, salt-resistant analogs of human beta-defensins 1 and 3 endowed with enhanced antimicrobial activity. Antimicrob. Agents Chemother. 54, 2312-2322. (doi:10.1128/AAC.01550-09)
40. Marques MRC, Loebenberg R, Almukainzi M. 2011 Simulated biological fluids with possible application in dissolution testing. Dissolution Technol. 18, 9-23. (doi:10.14227/DT180311P15)
41. Kelly M et al. 2015 Peptide aptamers: novel coatings for orthopaedic implants. Mater. Sci. Eng. C 54, 84-93. (doi:10.1016/j.msec.2015.04.021)
42. Andrews JM. 2001 Determination of minimum inhibitory concentrations. J. Antimicrob. Chemother. 48, 5-16. (doi:10.1093/jac/48.suppl-1.5)
43. Ciapetti G et al. 2003 Osteoblast growth and function in porous poly-e-caprolactone matrices for bone repair: a preliminary study. Biomaterials 24, 3815-3824. (doi:10.1016/S0142-9612(03)00263-1)
44. Yang CC, Lin CC, Liao JW, Yen SK. 2013 Vancomycinchitosan composite deposited on post-porous hydroxyapatite coated Ti6Al4 V. Mater. Sci. Eng. C 33, 2203-2212. (doi:10.1016/j.msec.2013.01.038)
45. Dhople V, Krukemeyer A, Ramamoorthy A. 2006 The human beta-defensin-3, an antibacterial peptide with multiple biological functions. Biochim. Biophys. Acta Biomembr. 158, 1499-1512. (doi:10.1016/j. bbamem.2006.07.007)
46. Brogden KA. 2005 Antimicrobial peptides: pore formers of metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3, 238-250. (doi:10.1038/nrmicro1098)
47. Bechinger B, Lohner K. 2006 Detergent-like actions of linear amphipathic cationic antimicrobial peptides. Biochem. Biophys. Acta Biomembr. 1758, 1529-1539. (doi:10.1016/j.bbamem.2006.07.001)
48. Hancock REW. 2001 Cationic peptides: effectors in innate immunity and novel antimicrobials. Lancet Infect. Dis. 1, 156-164. (doi:10.1016/S1473-3099(01)00092-5)
49. Kilgus DJ, Howe DJ, Strang A. 2002 Results of periprosthetic hip and knee infections caused by resistant bacteria. Clin. Orthop. Relat. Res. 404, 116-124. (doi:10.1097/00003086-200211000-00021)
50. Berbari EF, Hanssen AD, Duffy MC, Steckelberg JM, Ilstrup DM, Harmsen WS, Osmon DR. 1998 Risk factors for prosthetic joint infection: case-control study. Clin. Infect. Dis. 27, 1247-1254. (doi:10.1086/514991)
51. Murphy MB, Hartgerink JD, Goepferich A, Mikos AG. 2007 Synthesis and in vitro hydroxyapatite binding of peptides conjugated to calcium-binding moieties. Biomacromolecules 8, 2237-2243. (doi:10.1021/bm070121s)
52. Williams RL, Hadley MJ, Jiang PJ, Mendes PM, Rappoport JZ, Grover LM. 2013 Thiol modification of silicon-substituted hydroxyapatite nanocrystals facilitates fluorescent labelling and visualization of cellular internalization. J. Mater. Chem. B 1, 4370-4378. (doi:10.1039/c3tb20775g)
53. Tang S, Tian B, Ke QF, Zhu Z-A, Guo YP. 2014 Gentamicin-loaded carbonated hydroxyapatite coatings with hierarchically porous structures: drug delivery properties, bactericidial properties and biocompatibility. RSC Adv. 4, 41500. (doi:10.1039/C4RA05493H)
54. Neut D, de Belt H, van Horn JR, van der Mei HC, Busscher HJ. 2003 Residual gentamicin-release from antiobiotic loaded polymethylmethacrylate beads after 5 years of implantation. Biomaterials 24, 1829-1831. (doi:10.1016/S0142-9612(02) 00614-2)
55. Kim HW, Knowles JC, Kim HE. 2005 Porous scaffolds of gelatin-hydroxyapatite nanocomposites obtained by biomimetic approach: characterization and antibiotic drug release. J. Biomed. Mater. Res. B Appl. Biomater. 74B, 686-699. (doi:10.1002/jbm. b.30236)
56. Stigter M, de Groot K, Layrolle P. 2002 Incorporation of tobramycin into biomimetic hydroxyapatite coating on titanium. Biomaterials 23, 4143-4153. (doi:10.1016/S0142-9612(02)00157-6)