Rationally designed dual functional block copolymers for bottlebrush-like coatings: In vitro and in vivo antimicrobial, antibiofilm, and antifouling properties

Acta Biomaterialia

Volumn 51, Issue , 2017, Pages 112-124

  Gao, Qiang ^a   Yu, Meng ^a   Su, Yajuan ^a   Xie, Meihua ^a   Zhao, Xin ^a   Li, Peng ^b   Ma, Peter X ^c  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b NANJING TECH UNIVERSITY   (China)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Antibiofilm; Antifouling; Antimicrobial polypeptides; Polymer bottlebrush; Surface coating

Indexed keywords

BLOCK COPOLYMERS; CATIONIC POLYMERIZATION; CHAINS; ESCHERICHIA COLI; MAMMALS; PLASTIC COATINGS; POLYETHYLENE GLYCOLS; POLYPEPTIDES; RING OPENING POLYMERIZATION; SILICONES; SYNTHESIS (CHEMICAL);

ANTI-FOULINGS; ANTI-MICROBIAL ACTIVITY; ANTIBIOFILMS; ANTIMICROBIAL COATINGS; ANTIMICROBIAL POLYPEPTIDE; BIOMEDICAL DEVICES; IN-VITRO; POLYMER BOTTLEBRUSH; SURFACE COATINGS; SYNTHESISED;

BIOCOMPATIBILITY;

AMPHOPHILE; COPOLYMER; MACROGOL; METHACRYLIC ACID; POLYPEPTIDE; POLYPEPTIDE ANTIBIOTIC AGENT; SILASTIC; ANTIMICROBIAL CATIONIC PEPTIDE; BIOCOMPATIBLE COATED MATERIAL;

ADSORPTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIMICROBIAL ACTIVITY; ARTICLE; BIOCOMPATIBILITY; BIOFILM; CONTROLLED STUDY; CYTOTOXICITY TEST; DEVICE INFECTION; ESCHERICHIA COLI; FEMALE; FOULING CONTROL; HEMOLYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFECTION PREVENTION; MAMMAL CELL; MATERIAL COATING; MOUSE; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; RAT; RING OPENING; STAPHYLOCOCCUS AUREUS; SYNTHESIS; THROMBOCYTE ADHESION; ANIMAL; CHEMISTRY; DRUG EFFECTS; MATERIALS TESTING; PHYSIOLOGY;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BIOFILMS; COATED MATERIALS, BIOCOMPATIBLE; ESCHERICHIA COLI; HUMANS; MATERIALS TESTING; MICE; PSEUDOMONAS AERUGINOSA; RATS; STAPHYLOCOCCUS AUREUS;

EID: 85011411914     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2017.01.061     Document Type: Article

References (61)

1. [1] Scott, R.D., The Direct Medical Costs of Healthcare-associated Infections in U.S. Hospitals and the Benefits of Prevention. 2009, Centers for Disease Control and Prevention.
2. [2] Calfee, D.P., Crisis in hospital-acquired, healthcare-associated infections. Annu. Rev. Med. 63 (2012), 359–371.
3. [3] Davies, D., Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug. Discov. 2 (2003), 114–122.
4. [4] Costerton, J.W., Stewart, P.S., Greenberg, E.P., Bacterial biofilms: a common cause of persistent infections. Science 284 (1999), 1318–1322.
5. [5] Król, J.E., Nguyen, H.D., Rogers, L.M., Beyenal, H., Krone, S.M., Top, E.M., Increased transfer of a multidrug resistance plasmid in Escherichia coli biofilms at the air-liquid interface. Appl. Environ. Microbiol. 77 (2011), 5079–5088.
6. [6] Gasik, M., Van Mellaert, L., Pierron, D., Braem, A., Hofmans, D., De Waelheyns, E., Anné, J., Harmand, M.F., Vleugels, J., Reduction of biofilm infection risks and promotion of osteointegration for optimized surfaces of titanium implants. Adv. Healthcare Mater. 1 (2012), 117–127.
7. [7] Lu, Y., Yue, Z.G., Wang, W., Cao, Z.Q., Strategies on designing multifunctional surfaces to prevent biofilm formation. Front. Chem. Sci. Eng. 9 (2015), 324–335.
8. [8] Siedenbiedel, F., Tiller, J.C., Antimicrobial polymers in solution and on surfaces: overview and functional principles. Polymers 4 (2012), 46–71.
9. [9] Hetrick, E.M., Schoenfisch, M.H., Reducing implant-related infections: active release strategies. Chem. Soc. Rev. 35 (2006), 780–789.
10. [10] Yatvin, J., Gao, J., Locklin, J., Durable defense: robust and varied attachment of non-leaching poly“-onium” bactericidal coatings to reactive and inert surfaces. Chem. Commu. 50 (2014), 9433–9442.
11. [11] Muñoz-Bonilla, A., Fernández-García, M., The roadmap of antimicrobial polymeric materials in macromolecular nanotechnology. Eur. Polym. J. 65 (2015), 46–62.
12. [12] Bonilla, A.M., García, M.F., Polymeric materials with antimicrobial activity. Prog. Polym. Sci. 37 (2012), 281–339.
13. [13] Weber, D.J., Rutala, W.A., Self-disinfecting surfaces: review of current methodologies and future prospects. Am. J. Infect. Control 41 (2013), S31–S35.
14. [14] Yang, C., Ding, X., Ono, R.J., Lee, H., Hsu, L.Y., Tong, Y.W., Hedrick, J., Yang, Y.Y., Brush-like polycarbonates containing dopamine, cations, and PEG providing a broad-spectrum, antibacterial, and antifouling surface via one-step coating. Adv. Mater. 26 (2014), 7346–7351.
15. [15] Lau, K.H.A., Ren, C.L., Sileika, T.S., Park, S.H., Szleife, I., Messersmith, P.B., Surface-grafted polysarcosine as a peptoid antifouling polymer brush. Langmuir 28 (2012), 16099–16107.
16. [16] Zhu, Y.H., Sundaram, H.S., Liu, S.J., Zhang, L., Xu, X.W., Yu, Q.M., Xu, J.Q., Jiang, S.Y., A robust graft-to strategy to form multifunctional and stealth zwitterionic polymer-coated mesoporous silica nanoparticles. Biomacromolecules 15 (2014), 1845–1851.
17. [17] Hartleb, W., Saar, J.S., Zou, P., Lienkamp, K., Just antimicrobial is not enough: toward bifunctional polymer surfaces with dual antimicrobial and protein-repellent functionality. Macromol. Chem. Phys. 217 (2016), 225–231.
18. [18] Gallardo, M.G., Moruno, C.M., Yu, K., Manero, J.M., Gil, F.J., Kizhakkedathu, J.N., Rodriguez, D., Antibacterial properties of hLf1-11 peptide onto titanium surfaces: a comparison study between silanization and surface initiated polymerization. Biomacromolecules 16 (2015), 483–496.
19. [19] Yu, K., Lo, J.C.Y., Mei, Y., Haney, E.F., Siren, E., Kalathottukaren, M.T., Hancock, R.E.W., Lange, D., Kizhakkedathu, J.N., Toward infection-resistant surfaces: achieving high antimicrobial peptide potency by modulating the functionality of polymer brush and peptide. ACS Appl. Mater. Interfaces 7 (2015), 28591–28605.
20. [20] Zasloff, M., Antimicrobial peptides of multicellular or ganisms. Nature 415 (2002), 389–395.
21. [21] Li, P., Li, X., Saravanan, R., Li, C.M., Leong, S.S.J., Antimicrobial macromolecules: synthesis methods and future applications. RSC Adv. 2 (2012), 4031–4044.
22. [22] Engler, A.C., Shukla, A., Puranam, S., Buss, H.G., Jreige, N., Hammond, P.T., Effects of side group functionality and molecular weight on the activity of synthetic antimicrobial polypeptides. Biomacromolecules 12 (2011), 1666–1674.
23. [23] Cheng, J.J., Deming, T.J., Synthesis of polypeptides by ring-opening polymerization of alpha-amino acid N-carboxyanhydrides. Deming, T.J., (eds.) Peptide-Based Materials, Vol. 310, 2012, Springer Berlin Heidelberg, 1–26.
24. [24] Zhou, C.C., Qi, X.B., Li, P., Chen, W.N., Mouad, L., Chang, M.W., Leong, S.S.J., Chan-Park, M.B., High potency and broad-spectrum antimicrobial peptides synthesized via ring-opening polymerization of alpha-aminoacid-N-carboxyanhydrides. Biomacromolecules 11 (2010), 60–67.
25. [25] Ratner, B.D., Bryant, S.J., Biomaterials: where we have been and where we are going. Annu. Rev. Biomed. Eng. 6 (2004), 41–75.
26. [26] Li, P., Poon, Y.F., Li, W., Zhu, H.-Y., Yeap, S.H., Cao, Y., Qi, X., Zhou, C.C., Lamrani, M., Beuerman, R.W., Kang, E.T., Mu, Y., Li, C.M., Chang, M.W., Leong, S.S.J., Chan-Park, M.B., A polycationic antimicrobial and biocompatible hydrogel with microbe membrane suctioning ability. Nat. Mater. 10 (2011), 149–156.
27. [27] Zhou, C.C., Li, P., Qi, X.B., Sharif, A.R.M., Poon, Y.F., Cao, Y., Chang, M.W., Leong, S.S.J., Chan-Park, M.B., A photopolymerized antimicrobial hydrogel coating derived from epsilon-poly-ι-lysine. Biomaterials 32 (2011), 2704–2712.
28. [28] Wang, Y.L., El-Deen, A.G., Li, P., Oh, B.H.L., Guo, Z.R., Khin, M.M., Vikhe, Y.S., Wang, J., Hu, R.G., Boom, R.M., Kline, K.A., Becker, D.L., Duan, H.W., Chan-Park, M.B., High-performance capacitive deionization disinfection of water with graphene oxide-graft-quaternized chitosan nanohybrid electrode coating. ACS Nano 9 (2015), 10142–10157.
29. [29] Gu, J., Su, Y.J., Liu, P., Li, P., Yang, P., An environmentally benign antimicrobial coating based on a protein supramolecular assembly. ACS Appl. Mater. Interfaces 9 (2017), 198–210.
30. [30] Qi, X.B., Zhou, C.C., Li, P., Xu, W.X., Cao, Y., Ling, H., Chen, W.N., Li, C.M., Xu, R., Lamrani, M., Mu, Y., Leong, S.S.J., Chang, M.W., Chan-Park, M.B., Novel short antibacterial and antifungal peptides with low cytotoxicity: efficacy and action mechanisms. Biochem. Biophs. Res. Commun. 398 (2010), 594–600.
31. [31] Liu, R.H., Chen, X.Y., Chakraborty, S., Lemke, J.J., Hayouka, Z., Chow, C., Welch, R.A., Weisblum, B., Masters, K.S., Gellman, S.H., Tuning the biological activity profile of antibacterial polymers via subunit substitution pattern. J. Am. Chem. Soc. 136 (2014), 4410–4418.
32. [32] Li, P., Zhou, C.C., Rayatpisheh, S., Ye, K., Poon, Y.F., Hammond, P.T., Duan, H., Chan-Park, M.B., Cationic peptidopolysaccharides show excellent broad-spectrum antimicrobial activities and high selectivity. Adv. Mater. 24 (2012), 4130–4137.
33. [33] Banerjee, I., Pangule, R.C., Kane, R.S., Antifouling coatings: recent developments in the design of surfaces that prevent fouling by proteins, bacteria, and marine organisms. Adv. Mater. 23 (2011), 690–718.
34. [34] Jin, J., Jiang, W., Yin, J.H., Ji, X.L., Stagnaro, P., Plasma proteins adsorption mechanism on polyethylene-grafted poly(ethylene glycol) surface by quartz crystal microbalance with dissipation. Langmuir 29 (2013), 6624–6633.
35. [35] Zhang, Q., Neoh, K.G., Xu, L., Lu, S., Kang, E.T., Mahendran, R., Chiong, E., Functionalized mesoporous silica nanoparticles with mucoadhesive and sustained drug release properties for potential bladder cancer therapy. Langmuir 30 (2014), 6151–6161.
36. [36] Han, E., Lee, H., Effects of PEGylation on the binding interaction of magainin 2 and tachyplesin I with lipid bilayer surface. Langmuir 29 (2013), 14214–14221.
37. [37] Khantamat, O., Li, C.H., Yu, F., Jamison, A.C., Shih, W.C., Cai, C., Lee, T.R., Gold nanoshell-decorated silicone surfaces for the near-infrared (NIR) photothermal destruction of the pathogenic bacterium E. faecalis. ACS Appl. Mater. Interfaces 7 (2015), 3981–3993.
38. [38] Sahin, E., Kiick, K.L., Macromolecule-induced assembly of coiled-coils in alternating multiblock polymers. Biomacromolecules 10 (2009), 2740–2749.
39. [39] Chen, R., Willcox, M.D., Cole, N., Ho, K.K., Rasul, R., Denman, J.A., Kumar, N., Characterization of chemoselective surface attachment of the cationic peptide melimine and its effects on antimicrobial activity. Acta Biomater. 8 (2012), 4371–4379.
40. [40] Yuan, S.J., Wan, D., Liang, B., Pehkonen, S.O., Ting, Y.P., Neoh, K.G., Kang, E.T., Lysozyme-coupled poly(poly(ethylene glycol) methacrylate)-stainless steel hybrids and their antifouling and antibacterial surfaces. Langmuir 27 (2011), 2761–2774.
41. 2 surface: tests of antifouling and antibacterial activities. J. Phys. Chem. B 116 (2012), 13839–13847.
42. [42] Chen, Y.W., Chang, Y., Lee, R.H., Li, W.T., Chinnathambi, A., Alharbi, S.A., Hsiue, G.H., Adjustable bioadhesive control of PEGylated hyperbranch brushes on polystyrene microplate interface for the improved sensitivity of human blood typing. Langmuir 30 (2014), 9139–9146.
43. [43] Shai, Y., Mode of action of membrane active antimicrobial peptides. Biopolymers 66 (2002), 236–248.
44. [44] Tiller, J.C., Liao, C.J., Lewis, K., Klibanov, A.M., Designing surfaces that kill bacteria on contact. Proc. Natl. Acad. Sci. U.S.A. 98 (2001), 5981–5985.
45. [45] Lee, S.B., Koepsel, R.R., Morley, S.W., Matyjaszewski, K., Sun, Y.J., Russell, A.J., Permanent, nonleaching antibacterial surfaces. 1. Synthesis by atom transfer radical polymerization. Biomacromolecules 5 (2004), 877–882.
46. [46] Gabriel, M., Nazmi, K., Veerman, E.C., Nieuw Amerongen, A.V., Zentner, A., Preparation of LL-37-grafted titanium surfaces with bactericidal activity. Bioconjugate Chem. 17 (2006), 548–550.
47. [47] Lin, J., Qiu, S.Y., Lewis, K., Klibanov, A.M., Mechanism of bactericidal and fungicidal activities of textiles covalently modified with alkylated polyethylenimine. Biotechnol. Bioeng. 83 (2003), 168–172.
48. [48] Bieser, A.M., Tiller, J.C., Mechanistic considerations on contact-active antimicrobial surfaces with controlled functional group densities. Macromol. Biosci. 11 (2011), 526–534.
49. [49] Li, M., Neoh, K.G., Xu, L.Q., Wang, R., Kang, E.T., Lau, T., Olszyna, D.P., Chiong, E., Surface modification of silicone for biomedical applications requiring long-term antibacterial, antifouling, and hemocompatible properties. Langmuir 28 (2012), 16408–16422.
50. [50] Harris, L.G., Tosatti, S., Wieland, M., Textor, M., Richards, R.G., Staphylococcus aureus adhesion to titanium oxide surfaces coated with non-functionalized and peptide-functionalized poly(L-lysine)-grafted-poly(ethylene glycol) copolymers. Biomaterials 25 (2004), 4135–4148.
51. [51] Maddikeri, R.R., Tosatti, S., Schuler, M., Chessari, S., Textor, M., Richards, R.G., Harris, L.G., Reduced medical infection related bacterial strains adhesion on bioactive RGD modified titanium surfaces: A first step toward cell selective surfaces. J. Biomed. Mater. Res. A 84A (2008), 425–435.
52. [52] Voo, Z.X., Khan, M., Xu, Q.X., Narayanan, K., Ng, B.W.J., Ahmad, R.B., Hedrick, J.L., Yang, Y.Y., Antimicrobial coatings against biofilm formation: the unexpected balance between antifouling and bactericidal behavior. Polym. Chem. 7 (2016), 656–668.
53. [53] Xu, L.Q., Pranantyo, D., Neoh, K.G., Kang, E.T., Teo, S.L.M., Fu, G.D., Synthesis of catechol and zwitterion-bifunctionalized poly(ethylene glycol) for the construction of antifouling surfaces. Polym. Chem. 7 (2016), 493–501.
54. [54] Li, M., Neoh, K.G., Kang, E.T., Lau, T., Chiong, E., Surface modification of silicone with covalently immobilized and crosslinked agarose for potential application in the inhibition of infection and omental wrapping. Adv. Funct. Mater. 24 (2014), 1631–1643.
55. [55] Colak, S., Tew, G.N., Dual-functional ROMP-based betaines: effect of hydrophilicity and backbone structure on nonfouling properties. Langmuir 28 (2012), 666–675.
56. [56] Vörös, J., The density and refractive index of adsorbing protein layers. Biophys. J. 87 (2004), 553–561.
57. [57] Fang, Y., Xu, W., Meng, X.L., Ye, X.Y., Wu, J., Xu, Z.K., Poly(2-hydroxyethyl methacrylate) brush surface for specific and oriented adsorption of glycosidases. Langmuir 28 (2012), 13318–13324.
58. [58] Yu, K., Lai, B.F., Kizhakkedathu, J.N., Carbohydrate structure dependent hemocompatibility of biomimetic functional polymer brushes on surfaces. Adv. Healthcare Mater. 1 (2012), 199–213.
59. [59] Voo, Z.X., Khan, M., Narayanan, K., Seah, D., Hedrick, J.L., Yang, Y.Y., Antimicrobial/antifouling polycarbonate coatings: role of block copolymer architecture. Macromolecules 48 (2015), 1055–1064.
60. [60] Chen, R.X., Willcox, M.D.P., Ho, K.K.K., Smyth, D., Kumar, N., Antimicrobial peptide melimine coating for titanium and its in vivo antibacterial activity in rodent subcutaneous infection models. Biomaterials 85 (2016), 142–151.
61. [61] Riool, M., de Boer, L., Jaspers, V., van der Loos, C.M., van Wamel, W.J.B., Wu, G., Kwakman, P.H.S., Zaat, S.A.J., Staphylococcus epidermidis originating from titanium implants infects surrounding tissue and immune cells. Acta Biomater. 10 (2014), 5202–5212.