Amide side chain amphiphilic polymers disrupt surface established bacterial bio-films and protect mice from chronic Acinetobacter baumannii infection

Biomaterials

Volumn 74, Issue , 2016, Pages 131-143

  Uppu, Divakara S S M ^a   Samaddar, Sandip ^a   Ghosh, Chandradhish ^a   Paramanandham, Krishnamoorthy ^b   Shome, Bibek R ^b   Haldar, Jayanta ^a  

^a JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

^b ICAR NATIONAL INSTITUTE OF VETERINARY EPIDEMIOLOGY AND DISEASE INFORMATICS   (India)

Author keywords

Acinetobacter baumannii; Anti infective biomaterials; Bacterial resistance; Biofilm disruption; In vivo burn wound infection; Membrane active amphiphilic polymer

Indexed keywords

AMIDES; ANTIBIOTICS; BACTERIA; BIOFILMS; BIOMATERIALS; CHAINS; CYTOLOGY; ENZYME INHIBITION; FUNCTIONAL POLYMERS; MAMMALS; TOXICITY;

AMPHIPHILIC POLYMERS; BACTERIAL RESISTANCE; BAUMANNII; MEMBRANE DEPOLARIZATION; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; RESISTANCE TO ANTIBIOTICS; VANCOMYCIN-RESISTANT ENTEROCOCCI; WOUND INFECTIONS;

POLYMERS;

AMIDE; AMPHOPHILE; MALEIC ANHYDRIDE; POLYMER;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL LOAD; BIOFILM; CELL MEMBRANE PERMEABILITY; CHEMICAL STRUCTURE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HYDROPHOBICITY; MEMBRANE DEPOLARIZATION; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; VANCOMYCIN RESISTANT ENTEROCOCCUS; ACINETOBACTER INFECTIONS; ANIMAL; BAGG ALBINO MOUSE; CHEMICAL PHENOMENA; CHEMISTRY; CHRONIC DISEASE; ISOLATION AND PURIFICATION; SURFACE PROPERTY;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTIONS; AMIDES; ANIMALS; BIOFILMS; CHRONIC DISEASE; FEMALE; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MICE; MICE, INBRED BALB C; POLYMERS; SURFACE PROPERTIES;

EID: 84945161553     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.09.042     Document Type: Article

References (63)

1. Costerton J.W., Stewart P.S., Greenberg E.P. Bacterial biofilms: a common cause of persistent infections. Science 1999, 284:1318-1322.
2. O'Toole G., Kaplan H.B., Kolter R. Biofilm formation as microbial development. Annu. Rev. Microbiol. 2000, 54:49-79.
3. Hall-Stoodley L., Costerton J.W., Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2004, 2:95-108.
4. Romero D., Aguilar C., Losick R., Kolter R. Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:2230-2234.
5. Wu H., Moser C., Wang H.Z., Hoiby N., Song Z.J. Strategies for combating bacterial biofilm infections. Int. J. Oral Sci. 2015, 7:1-7.
6. Bjarnsholt T., Ciofu O., Molin S., Givskov M., Hoiby N. Applying insights from biofilm biology to drug development - can a new approach be developed?. Nat. Rev. Drug Discov. 2013, 12:791-808.
7. Davies D. Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov. 2003, 2:114-122.
8. Ciofu O., Tolker-Nielsen T., Jensen P.O., Wang H., Hoiby N. Antimicrobial resistance, respiratory tract infections and role of biofilms in lung infections in cystic fibrosis patients. Adv. Drug Deliv. Rev. 2015, 85:7-23.
9. Stewart P.S., Costerton J.W. Antibiotic resistance of bacteria in biofilms. Lancet 2001, 358:135-138.
10. Mah T.F., Pitts B., Pellock B., Walker G.C., Stewart P.S., O'Toole G.A. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 2003, 426:306-310.
11. Hurdle J.G., O'Neill A.J., Chopra I., Lee R.E. Targeting bacterial membrane function: an underexploited mechanism for treating persistent infections. Nat. Rev. Microbiol. 2011, 9:62-75.
12. Chua S.L., Liu Y., Yam J.K., Chen Y., Vejborg R.M., Tan B.G., et al. Dispersed cells represent a distinct stage in the transition from bacterial biofilm to planktonic lifestyles. Nat. Commun. 2014, 5:4462.
13. Hoiby N., Bjarnsholt T., Givskov M., Molin S., Ciofu O. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 2010, 35:322-332.
14. Obst U., Schwartz T., Volkmann H. Antibiotic resistant pathogenic bacteria and their resistance genes in bacterial biofilms. Int. J. Artif. Organs 2006, 29:387-394.
15. Smith A.W. Biofilms and antibiotic therapy: is there a role for combating bacterial resistance by the use of novel drug delivery systems?. Adv. Drug Deliv. Rev. 2005, 57:1539-1550.
16. Stewart P.S. Mechanisms of antibiotic resistance in bacterial biofilms. Int. J. Med. Microbiol. 2002, 292:107-113.
17. Balaban N.Q., Gerdes K., Lewis K., McKinney J.D. A problem of persistence: still more questions than answers?. Nat. Rev. Microbiol. 2013, 11:587-591.
18. O'Loughlin C.T., Miller L.C., Siryaporn A., Drescher K., Semmelhack M.F., Bassler B.L. A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:17981-17986.
19. Chen M., Yu Q., Sun H. Novel strategies for the prevention and treatment of biofilm related infections. Int. J. Mol. Sci. 2013, 14:18488-18501.
20. 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 2011, 23:690-718.
21. Fischer M., Vahdatzadeh M., Konradi R., Friedrichs J., Maitz M.F., Freudenberg U., et al. Multilayer hydrogel coatings to combine hemocompatibility and antimicrobial activity. Biomaterials 2015, 56:198-205.
22. Kazemzadeh-Narbat M., Lai B.F.L., Ding C.F., Kizhakkedathu J.N., Hancock R.E.W., Wang R.Z. Multilayered coating on titanium for controlled release of antimicrobial peptides for the prevention of implant-associated infections. Biomaterials 2013, 34:5969-5977.
23. Mi L., Jiang S.Y. Integrated Antimicrobial and Nonfouling Zwitterionic Polymers. Angew. Chem. Int. Ed. 2014, 53:1746-1754.
24. Statz A.R., Meagher R.J., Barron A.E., Messersmith P.B. New peptidomimetic polymers for antifouling surfaces. J. Am. Chem. Soc. 2005, 127:7972-7973.
25. Tasso M., Pettitt M.E., Cordeiro A.L., Callow M.E., Callow J.A., Werner C. Antifouling potential of Subtilisin A immobilized onto maleic anhydride copolymer thin films. Biofouling 2009, 25:505-516.
26. 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. 2001, 98:5981-5985.
27. Taglietti A., Arciola C.R., D'Agostino A., Dacarro G., Montanaro L., Campoccia D., et al. Antibiofilm activity of a monolayer of silver nanoparticles anchored to an amino-silanized glass surface. Biomaterials 2014, 35:1779-1788.
28. Kumar A., Vemula P.K., Ajayan P.M., John G. Silver-nanoparticle-embedded antimicrobial paints based on vegetable oil. Nat. Mater 2008, 7:236-241.
29. Kalaycl O.A., Comert F.B., Hazer B., Atalay T., Cavicchi K.A., Cakmak M. Synthesis, characterization, and antibacterial activity of metal nanoparticles embedded into amphiphilic comb-type graft copolymers. Polym. Bull. 2010, 65:215-226.
30. Hazer D.B., Mut M., Dincer N., Saribas Z., Hazer B., Ozgen T. The efficacy of silver-embedded polypropylene-grafted polyethylene glycol-coated ventricular catheters on prevention of shunt catheter infection in rats. Childs Nerv. Syst. 2012, 28:839-846.
31. Campoccia D., Montanaro L., Arciola C.R. A review of the biomaterials technologies for infection-resistant surfaces. Biomaterials 2013, 34:8533-8554.
32. Ganewatta M.S., Tang C.B. Controlling macromolecular structures towards effective antimicrobial polymers. Polymer 2015, 63:A1-A29.
33. Hoque J., Akkapeddi P., Yadav V., Manjunath G.B., Uppu D.S., Konai M.M., et al. Broad spectrum antibacterial and antifungal polymeric paint materials: synthesis, structure-activity relationship, and membrane-active mode of action. ACS Appl. Mater Interfaces 2015, 7:1804-1815.
34. Sharma A., Pohane A.A., Bansal S., Bajaj A., Jain V., Srivastava A. Cell Penetrating Synthetic Antimicrobial Peptides (SAMPs) Exhibiting Potent and Selective Killing of Mycobacterium by Targeting Its DNA. Chem. Eur. J. 2015, 21:3540-3545.
35. Strassburg A., Kracke F., Wenners J., Jemeljanova A., Kuepper J., Petersen H., et al. Nontoxic, Hydrophilic Cationic Polymers-Identified as Class of Antimicrobial Polymers. Macromol. Biosci. 2015, published online. 10.1002/mabi.201500207.
36. Peng L., DeSousa J., Su Z., Novak B.M., Nevzorov A.A., Garland E.R., et al. Inhibition of Acinetobacter baumannii biofilm formation on a methacrylate polymer containing a 2-aminoimidazole subunit. Chem. Commun. 2011, 47:4896-4898.
37. Li Y., Fukushima K., Coady D.J., Engler A.C., Liu S., Huang Y., et al. Broad-spectrum antimicrobial and biofilm-disrupting hydrogels: stereocomplex-driven supramolecular assemblies. Angew. Chem. Int. Ed. Engl. 2013, 52:674-678.
38. Liu R., Chen X., Falk S.P., Masters K.S., Weisblum B., Gellman S.H. Nylon-3 polymers active against drug-resistant Candida albicans biofilms. J. Am. Chem. Soc. 2015, 137:2183-2186.
39. Dijkshoorn L., Nemec A., Seifert H. An increasing threat in hospitals: multidrug-resistant Acinetobacter baumannii. Nat. Rev. Microbiol. 2007, 5:939-951.
40. Rodriguez-Bano J., Marti S., Soto S., Fernandez-Cuenca F., Cisneros J.M., Pachon J., et al. Biofilm formation in Acinetobacter baumannii: associated features and clinical implications. Clin. Microbiol. Infect. 2008, 14:276-278.
41. Pour N.K., Dusane D.H., Dhakephalkar P.K., Zamin F.R., Zinjarde S.S., Chopade B.A. Biofilm formation by Acinetobacter baumannii strains isolated from urinary tract infection and urinary catheters. FEMS Immunol. Med. Microbiol. 2011, 62:328-338.
42. McConnell M.J., Actis L., Pachon J. Acinetobacter baumannii: human infections, factors contributing to pathogenesis and animal models. FEMS Microbiol. Rev. 2013, 37:130-155.
43. Longo F., Vuotto C., Donelli G. Biofilm formation in Acinetobacter baumannii. New Microbiol. 2014, 37:119-127.
44. Espinal P., Marti S., Vila J. Effect of biofilm formation on the survival of Acinetobacter baumannii on dry surfaces. J. Hosp. Infect. 2012, 80:56-60.
45. Deng M., Zhu M.H., Li J.J., Bi S., Sheng Z.K., Hu F.S., et al. Molecular Epidemiology and Mechanisms of Tigecycline Resistance in Clinical Isolates of Acinetobacter baumannii from a Chinese University Hospital. Antimicrob. Agents Chemother. 2014, 58:297-303.
46. Harris T.L., Worthington R.J., Hittle L.E., Zurawski D.V., Ernst R.K., Melander C. Small molecule downregulation of PmrAB reverses lipid A modification and breaks colistin resistance. ACS Chem. Biol. 2014, 9:122-127.
47. O'Shea M.K. Acinetobacter in modern warfare. Int. J. Antimicrob. Agents 2012, 39:363-375.
48. Murray C.K. Epidemiology of infections associated with combat-related injuries in Iraq and Afghanistan. J. Trauma 2008, 64:S232-S238.
49. Jones A., Morgan D., Walsh A., Turton J., Livermore D., Pitt T., et al. Importation of multidrug-resistant Acinetobacter spp infections with casualties from Iraq. Lancet Infect. Dis. 2006, 6:317-318.
50. Popescu I., Suflet D.M., Pelin I.M., Chitanu G.C. Biomedical Applications of Maleic Anhydride Copolymers. Rev. Roum. Chim. 2011, 56:173-188.
51. Duncan R. The dawning era of polymer therapeutics. Nat. Rev. Drug Discov. 2003, 2:347-360.
52. Krumm C., Harmuth S., Hijazi M., Neugebauer B., Kampmann A.L., Geltenpoth H., et al. Antimicrobial Poly( 2-methyloxazoline) s with Bioswitchable Activity through Satellite Group Modification. Angew. Chem. Int. Ed. 2014, 53:3830-3834.
53. Hussain M., Hastings J.G., White P.J. A chemically defined medium for slime production by coagulase-negative staphylococci. J. Med. Microbiol. 1991, 34:143-147.
54. Uppu D.S., Akkapeddi P., Manjunath G.B., Yarlagadda V., Hoque J., Haldar J. Polymers with tunable side-chain amphiphilicity as non-hemolytic antibacterial agents. Chem. Commun. 2013, 49:9389-9391.
55. Uppu D.S., Manjunath G.B., Yarlagadda V., Kaviyil J.E., Ravikumar R., Paramanandham K., et al. Membrane-Active Macromolecules Resensitize NDM-1 Gram-Negative Clinical Isolates to Tetracycline Antibiotics. PLoS One 2015, 10. e0119422.
56. Choi H., Chakraborty S., Liu R., Gellman S.H., Weisshaar J.C. Medium effects on minimum inhibitory concentrations of nylon-3 polymers against E. coli. PLoS One 2014, 9. e104500.
57. Conlon B.P., Nakayasu E.S., Fleck L.E., LaFleur M.D., Isabella V.M., Coleman K., et al. Activated ClpP kills persisters and eradicates a chronic biofilm infection. Nature 2013, 503:365-370.
58. Allison K.R., Brynildsen M.P., Collins J.J. Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature 2011, 473:216-220.
59. Chakraborty S., Liu R., Lemke J.J., Hayouka Z., Welch R.A., Weisblum B., et al. Effects of Cyclic vs. Acyclic Hydrophobic Subunits on the Chemical Structure and Biological Properties of Nylon-3 Co-Polymers. ACS Macro Lett. 2013, 2.
60. Liu R.H., Chen X.Y., Chakraborty S., Lemke J.J., Hayouka Z., Chow C., et al. Tuning the Biological Activity Profile of Antibacterial Polymers via Subunit Substitution Pattern. J. Am. Chem. Soc. 2014, 136:4410-4418.
61. Hoffman L.R., D'Argenio D.A., MacCoss M.J., Zhang Z., Jones R.A., Miller S.I. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 2005, 436:1171-1175.
62. de la Fuente-Nunez C., Reffuveille F., Mansour S.C., Reckseidler-Zenteno S.L., Hernandez D., Brackman G., et al. D-Enantiomeric Peptides that Eradicate Wild-Type and Multidrug-Resistant Biofilms and Protect against Lethal Pseudomonas aeruginosa Infections. Chem. Biol. 2015, 22:196-205.
63. Nait Chabane Y., Mlouka M.B., Alexandre S., Nicol M., Marti S., Pestel-Caron M., et al. Virstatin inhibits biofilm formation and motility of Acinetobacter baumannii. BMC Microbiol. 2014, 14:62.