Core–shell magnetic nanoparticles display synergistic antibacterial effects against Pseudomonas aeruginosa and Staphylococcus aureus when combined with cathelicidin LL-37 or selected ceragenins

International Journal of Nanomedicine

Volumn 11, Issue , 2016, Pages 5443-5455

  Niemirowicz, Katarzyna ^a   Piktel, Ewelina ^a   Wilczewska, Agnieszka Z ^b   Markiewicz, Karolina H ^b   Durnaś, Bonita ^c   Wątek, Marzena ^d   Puszkarz, Irena ^c   Wróblewska, Marta ^e,f   Niklińska, Wiesława ^a   Savage, Paul B ^g   Bucki, Robert ^a,c  

^a MEDICAL UNIVERSITY OF BIALYSTOK   (Poland)

^b UNIVERSITY OF BIALYSTOK   (Poland)

^c JAN KOCHANOWSKI UNIVERSITY   (Poland)

^d Center Holy Cross Regional Hospital   (Poland)

^e MEDICAL UNIVERSITY OF WARSAW   (Poland)

^f Central Clinical Hospital in Warsaw   (Poland)

^g Brigham Young University   (United States)

Author keywords

Antibiotic resistant bacteria; Ceragenins; LL 37 peptide; Magnetic nanoparticles; Synergistic activity

Indexed keywords

ANTIBIOTIC AGENT; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; COLISTIN; CORE SHELL MAGNETIC NANOPARTICLE; CRYSTAL VIOLET; CSA 13; CSA 131; MAGNETIC NANOPARTICLE; UNCLASSIFIED DRUG; VANCOMYCIN; ANTIINFECTIVE AGENT; ANTIMICROBIAL CATIONIC PEPTIDE; CAP18 LIPOPOLYSACCHARIDE-BINDING PROTEIN; CERAGENIN CSA-13; MAGNETITE NANOPARTICLE; STEROID;

ARTICLE; BACTERICIDAL ACTIVITY; BIOFILM; CHEMOLUMINESCENCE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG POTENTIATION; FRACTIONAL BACTERICIDAL CONCENTRATION INDEX; FRACTIONAL INHIBITORY CONCENTRATION INDEX; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; PSEUDOMONAS AERUGINOSA; ANTIBIOTIC RESISTANCE; CHEMISTRY; COMBINATION DRUG THERAPY; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MICROBIAL SENSITIVITY TEST; STAPHYLOCOCCUS AUREUS;

ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; DRUG RESISTANCE, BACTERIAL; DRUG SYNERGISM; DRUG THERAPY, COMBINATION; HUMANS; MAGNETITE NANOPARTICLES; MICROBIAL SENSITIVITY TESTS; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS; STEROIDS;

EID: 84994430555     PISSN: 11769114     EISSN: 11782013     Source Type: Journal    
DOI: 10.2147/IJN.S113706     Document Type: Article

References (61)

1. Bell BG, Schellevis F, Stobberingh E, Goossens H, Pringle M. A systematic review and meta-analysis of the effects of antibiotic consumption on antibiotic resistance. BMC Infect Dis. 2014;14:13.
2. Ozer B, Ozbakıs Akkurt BC, Duran N, Onlen Y, Savas L, Turhanoglu S. Evaluation of nosocomial infections and risk factors in critically ill patients. Med Sci Monit. 2011;17(3):H17–H22.
3. Bereket W, Hemalatha K, Getenet B, et al. Update on bacterial nosocomial infections. Eur Rev Med Pharmacol Sci. 2012;16(8):1039–1044.
4. Ray GT, Suaya JA, Baxter R. Incidence, microbiology, and patient characteristics of skin and soft-tissue infections in a U.S. population: a retrospective population-based study. BMC Infect Dis. 2013; 13:252.
5. Watkins RR, David MZ, Salata RA. Current concepts on the virulence mechanisms of meticillin-resistant Staphylococcus aureus. J Med Microbiol. 2012;61(pt 9):1179–1193.
6. van Belkum A, Melles DC, Nouwen J, et al. Co-evolutionary aspects of human colonisation and infection by Staphylococcus aureus. Infect Genet Evol. 2009;9(1):32–47.
7. Monecke S, Coombs G, Shore AC, et al. A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS One. 2011;6(4):e17936.
8. Jones AM, Dodd ME, Morris J, Doherty C, Govan JR, Webb AK. Clinical outcome for cystic fibrosis patients infected with transmissible Pseudomonas aeruginosa: an 8-year prospective study. Chest. 2010; 137(6):1405–1409.
9. Gang RK, Bang RL, Sanyal SC, Mokaddas E, Lari AR. Pseudomonas aeruginosa septicaemia in burns. Burns. 1999;25(7):611–616.
10. Kluytmans JA, Mouton JW, Ijzerman EP, et al. Nasal carriage of Staphylococcus aureus as a major risk factor for wound infections after cardiac surgery. J Infect Dis. 1995;171(1):216–219.
11. Mulcahy LR, Isabella VM, Lewis K. Pseudomonas aeruginosa biofilms in disease. Microb Ecol. 2014;68(1):1–12.
12. Huh AJ, Kwon YJ. “Nanoantibiotics”: a new paradigm for treating infectious diseases using nanomaterials in the antibiotics resistant era. J Control Release. 2011;156(2):128–145.
13. Niemirowicz K, Markiewicz KH, Wilczewska AZ, Car H. Magnetic nanoparticles as new diagnostic tools in medicine. Adv Med Sci. 2012; 57(2):196–207.
14. Wilczewska AZ, Niemirowicz K, Markiewicz KH, Car H. Nanoparticles as drug delivery systems. Pharmacol Rep. 2012;64(5):1020–1037.
15. Chomoucka J, Drbohlavova J, Huska D, Adam V, Kizek R, Hubalek J. Magnetic nanoparticles and targeted drug delivering. Pharmacol Res. 2010;62(2):144–149.
16. Laurent S, Dutz S, Häfeli UO, Mahmoudi M. Magnetic fluid hyperthermia: focus on superparamagnetic iron oxide nanoparticles. Adv Colloid Interface Sci. 2011;166(1–2):8–23.
17. Niemirowicz K, Swiecicka I, Wilczewska AZ, et al. Gold-functionalized magnetic nanoparticles restrict growth of Pseudomonas aeruginosa. Int J Nanomedicine. 2014;9:2217–2224.
18. Niemirowicz K, Swiecicka I, Wilczewska AZ, et al. Growth arrest and rapid capture of select pathogens following magnetic nanoparticle treatment. Colloids Surf B Biointerfaces. 2015;131:29–38.
19. Ghosh IN, Patil SD, Sharma TK, Srivastava SK, Pathania R, Navani NK. Synergistic action of cinnamaldehyde with silver nanoparticles against spore-forming bacteria: a case for judicious use of silver nanoparticles for antibacterial applications. Int J Nanomedicine. 2013;8:4721–4731.
20. Brown AN, Smith K, Samuels TA, Lu J, Obare SO, Scott ME. Nanoparticles functionalized with ampicillin destroy multiple-antibiotic-resistant isolates of Pseudomonas aeruginosa and Enterobacter aerogenes and methicillin-resistant Staphylococcus aureus. Appl Environ Microbiol. 2012;78(8):2768–2774.
21. Li LH, Yen MY, Ho CC, et al. Non-cytotoxic nanomaterials enhance antimicrobial activities of cefmetazole against multidrug-resistant Neisseria gonorrhoeae. PLoS One. 2013;8(5):e64794.
22. Jena P, Mohanty S, Mallick R, Jacob B, Sonawane A. Toxicity and antibacterial assessment of chitosan-coated silver nanoparticles on human pathogens and macrophage cells. Int J Nanomedicine. 2012;7: 1805–1818.
23. Ruden S, Hilpert K, Berditsch M, Wadhwani P, Ulrich AS. Synergistic interaction between silver nanoparticles and membrane-permeabilizing antimicrobial peptides. Antimicrob Agents Chemother. 2009;53(8): 3538–3540.
24. Naqvi SZ, Kiran U, Ali MI, et al. Combined efficacy of biologically synthesized silver nanoparticles and different antibiotics against multidrug-resistant bacteria. Int J Nanomedicine. 2013;8: 3187–3195.
25. Rai MK, Deshmukh SD, Ingle AP, Gade AK. Silver nanoparticles: the powerful nanoweapon against multidrug-resistant bacteria. J Appl Microbiol. 2012;112(5):841–852.
26. Fayaz AM, Balaji K, Girilal M, Yadav R, Kalaichelvan PT, Venketesan R. Biogenic synthesis of silver nanoparticles and their synergistic effect with antibiotics: a study against gram-positive and gram-negative bacteria. Nanomedicine. 2010;6(1):103–109.
27. Gurunathan S, Han JW, Kwon DN, Kim JH. Enhanced antibacterial and anti-biofilm activities of silver nanoparticles against Gram-negative and Gram-positive bacteria. Nanoscale Res Lett. 2014;9(1):373.
28. Massart R. Preparation of aqueous magnetic liquids in alkaline and acidic media. IEEE Trans Magn. 1981;17(2):1247–1248.
29. Wilczewska A, Markiewicz K. Surface-initiated RAFT/MADIX polymerization on Xanthate-coated iron oxide nanoparticles. Macromol Chem Phys. 2014;215(2):190–197.
30. Timurkaynak F, Can F, Azap OK, Demirbilek M, Arslan H, Karaman SO. In vitro activities of non-traditional antimicrobials alone or in combination against multidrug-resistant strains of Pseudomonas aeruginosa and Acinetobacter baumannii isolated from intensive care units. Int J Antimicrob Agents. 2006;27(3):224–228.
31. Kah JCY, Phonthammachai N, Wan RCY, et al. Synthesis of gold nano-shells based on the deposition-precipitation process. Gold Bull. 2008; 41(1):23–36.
32. Hussein-Al-Ali SH, El Zowalaty ME, Hussein MZ, Ismail M, Webster TJ. Synthesis, characterization, controlled release, and antibacterial studies of a novel streptomycin chitosan magnetic nanoantibiotic. Int J Nanomedicine. 2014;9:549–557.
33. Reddy AJ, Kokila MK, Nagabhushana H, et al. Combustion synthesis, characterization and Raman studies of ZnO nanopowders. Spectrochim Acta A Mol Biomol Spectrosc. 2011;81(1):53–58.
34. Kadurugamuwa JL, Sin L, Albert E, et al. Direct continuous method for monitoring biofilm infection in a mouse model. Infect Immun. 2003; 71(2):882–890.
35. Wnorowska U, Wątek M, Durnaś B, et al. Extracellular DNA as an essential component and therapeutic target of microbial biofilm. Stud Med. 2015;31(2):132–138.
36. Bucki R, Leszczynska K, Namiot A, Sokolowski W. Cathelicidin LL-37: a multitask antimicrobial peptide. Arch Immunol Ther Exp (Warsz). 2010; 58(1):15–25.
37. Zasloff M. Magainins, a class of antimicrobial peptides from Xenopus skin: isolation, characterization of two active forms, and partial cDNA sequence of a precursor. Proc Natl Acad Sci U S A. 1987;84(15):5449–5453.
38. Bucki R, Pastore JJ, Randhawa P, Vegners R, Weiner DJ, Janmey PA. Antibacterial activities of rhodamine B-conjugated gelsolin-derived peptides compared to those of the antimicrobial peptides cathelicidin LL37, magainin II, and melittin. Antimicrob Agents Chemother. 2004; 48(5):1526–1533.
39. Moore KS, Wehrli S, Roder H, et al. Squalamine: an aminosterol antibiotic from the shark. Proc Natl Acad Sci U S A. 1993;90(4):1354–1358.
40. Isogai E, Isogai H, Takahashi K, Okumura K, Savage PB. Ceragenin CSA-13 exhibits antimicrobial activity against cariogenic and perio-dontopathic bacteria. Oral Microbiol Immunol. 2009;24(2):170–172.
41. Bozkurt-Guzel C, Savage PB, Akcali A, Ozbek-Celik B. Potential synergy activity of the novel ceragenin, CSA-13, against carbapenem-resistant Acinetobacter baumannii strains isolated from bacteremia patients. Biomed Res Int. 2014;2014:710273.
42. Nagant C, Pitts B, Stewart PS, Feng Y, Savage PB, Dehaye JP. Study of the effect of antimicrobial peptide mimic, CSA-13, on an established biofilm formed by Pseudomonas aeruginosa. Microbiologyopen. 2013; 2(2):318–325.
43. Leszczynska K, Namiot D, Byfield FJ, et al. Antibacterial activity of the human host defence peptide LL-37 and selected synthetic cationic lipids against bacteria associated with oral and upper respiratory tract infections. J Antimicrob Chemother. 2013;68(3):610–618.
44. Savage PB, Li C, Taotafa U, Ding B, Guan Q. Antibacterial properties of cationic steroid antibiotics. FEMS Microbiol Lett. 2002;217(1):1–7.
45. Chin JN, Rybak MJ, Cheung CM, Savage PB. Antimicrobial activities of ceragenins against clinical isolates of resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2007;51(4):1268–1273.
46. Chin JN, Jones RN, Sader HS, Savage PB, Rybak MJ. Potential synergy activity of the novel ceragenin, CSA-13, against clinical isolates of Pseudomonas aeruginosa, including multidrug-resistant P. aeruginosa. J Antimicrob Chemother. 2008;61(2):365–370.
47. Lai XZ, Feng Y, Pollard J, et al. Ceragenins: cholic acid-based mimics of antimicrobial peptides. Acc Chem Res. 2008;41(10):1233–1240.
48. Istrate CM, Holban AM, Grumezescu AM, et al. Iron oxide nanoparticles modulate the interaction of different antibiotics with cellular membranes. Rom J Morphol Embryol. 2014;55(3):849–856.
49. Grumezescu AM, Gestal MC, Holban AM, et al. Biocompatible Fe3O4 increases the efficacy of amoxicillin delivery against Gram-positive and Gram-negative bacteria. Molecules. 2014;19(4):5013–5027.
50. Gu H, Ho PL, Tong E, Wang L, Xu B. Presenting vancomycin on nanoparticles to enhance antimicrobial activities. Nano Lett. 2003;3(9):1261–1263.
51. Malone ME, Corrigan OI, Kavanagh PV, Gowing C, Donnelly M, D’Arcy DM. Pharmacokinetics of amphotericin B lipid complex in critically ill patients undergoing continuous venovenous haemodiafiltra-tion. Int J Antimicrob Agents. 2013;42(4):335–342.
52. Leuba KD, Durmus NG, Taylor EN, Webster TJ. Short communication: carboxylate functionalized superparamagnetic iron oxide nanoparticles (SPION) for the reduction of S. aureus growth post biofilm formation. Int J Nanomedicine. 2013;8:731–736.
53. Kuroda K, Fukuda T, Okumura K, et al. Ceragenin CSA-13 induces cell cycle arrest and antiproliferative effects in wild-type and p53 null mutant HCT116 colon cancer cells. Anticancer Drugs. 2013;24(8):826–834.
54. Bucki R, Sostarecz AG, Byfield FJ, Savage PB, Janmey PA. Resistance of the antibacterial agent ceragenin CSA-13 to inactivation by DNA or F-actin and its activity in cystic fibrosis sputum. J Antimicrob Chemother. 2007;60(3):535–545.
55. Bucki R, Niemirowicz K, Wnorowska U, et al. Polyelectrolyte-mediated increase of biofilm mass formation. BMC Microbiol. 2015;15:117.
56. Chatterjee S, Maiti P, Dey R, Kundu A. Biofilms on indwelling urologic devices: microbes and antimicrobial management prospect. Ann Med Health Sci Res. 2014;4(1):100–104.
57. Olsen I. Biofilm-specific antibiotic tolerance and resistance. Eur J Clin Microbiol Infect Dis. 2015;34(5):877–886.
58. Poletaev A, Boura P. The immune system, natural autoantibodies and general homeostasis in health and disease. Hippokratia. 2011; 15(4):295–298.
59. Leszczyńska K, Namiot A, Cruz K, et al. Potential of ceragenin CSA-13 and its mixture with pluronic F-127 as treatment of topical bacterial infections. J Appl Microbiol. 2011;110(1):229–238.
60. Singh PK, Tack BF, McCray PB, Welsh MJ. Synergistic and additive killing by antimicrobial factors found in human airway surface liquid. Am J Physiol Lung Cell Mol Physiol. 2000;279(5):L799–L805.
61. Bozkurt-Guzel C, Savage PB, Gerceker AA. In vitro activities of the novel ceragenin CSA-13, alone or in combination with colistin, tobramy-cin, and ciprofloxacin, against Pseudomonas aeruginosa strains isolated from cystic fibrosis patients. Chemotherapy. 2011;57(6):505–510.