Bactericidal activity of ceragenin CSA-13 in cell culture and in an animal model of peritoneal infection

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 10, 2015, Pages 6274-6282

  Bucki, Robert ^a,b,c   Niemirowicz, Katarzyna ^a   Wnorowska, Urszula ^a   Byfield, Fitzroy J ^c   Piktel, Ewelina ^a   Wątek, Marzena ^d   Janmey, Paul A ^c   Savage, Paul B ^e  

^a MEDICAL UNIVERSITY OF BIALYSTOK   (Poland)

^b JAN KOCHANOWSKI UNIVERSITY   (Poland)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d Center of Oncology of Kielce   (Poland)

^e Brigham Young University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL CATIONIC PEPTIDE; BACTERICIDE; BACTERIUM LIPOPOLYSACCHARIDE; BUTYRIC ACID; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CERAGENIN CSA 13; FLUORESCENT DYE; INTERLEUKIN 8; IRDYE 800CW DYE; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; CAP18 LIPOPOLYSACCHARIDE-BINDING PROTEIN; CERAGENIN CSA-13; STEROID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AREA UNDER THE CURVE; ARTICLE; BACTERIAL GROWTH; BACTERIAL PERITONITIS; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; COMPARATIVE EFFECTIVENESS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG CLEARANCE; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG HALF LIFE; DRUG POTENCY; DRUG PROTEIN BINDING; HUMAN; HUMAN CELL; IN VITRO STUDY; KIDNEY; LIVER; LUNG ALVEOLUS EPITHELIUM CELL; MAXIMUM PLASMA CONCENTRATION; MEAN RESIDENCE TIME; MOUSE; NONHUMAN; PERITONEAL CAVITY; PERITONEAL FLUID; PLASMA CONCENTRATION-TIME CURVE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; TIME TO MAXIMUM PLASMA CONCENTRATION; ANIMAL; BIOAVAILABILITY; CELL LINE; CHEMISTRY; DISEASE MODEL; DRUG EFFECTS; EPITHELIUM CELL; FEMALE; GROWTH, DEVELOPMENT AND AGING; INTRAPERITONEAL DRUG ADMINISTRATION; LUNG; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; NUDE MOUSE; PATHOLOGY; PERITONITIS; PSEUDOMONAS INFECTIONS; RESPIRATORY MUCOSA;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BIOLOGICAL AVAILABILITY; BUTYRIC ACID; CELL LINE; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; FEMALE; FLUORESCENT DYES; HUMANS; INJECTIONS, INTRAPERITONEAL; KIDNEY; LIVER; LUNG; MICE; MICE, NUDE; MICROBIAL SENSITIVITY TESTS; PERITONITIS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RESPIRATORY MUCOSA; STEROIDS;

EID: 84942936037     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00653-15     Document Type: Article

References (52)

1. Savage PB, Li C. 2000. Cholic acid derivatives: novel antimicrobials. Expert Opin Investig Drugs 9:263-272. http://dx.doi.org/10.1517/13543784.9.2.263.
2. Savage PB, Li C, Taotafa U, Ding B, Guan Q. 2002. Antibacterial properties of cationic steroid antibiotics. FEMS Microbiol Lett 217:1-7. http://dx.doi.org/10.1111/j.1574-6968.2002.tb11448.x.
3. Leszczynska K, Namiot A, Fein DE, Wen Q, Namiot Z, Savage PB, Diamond S, Janmey PA, Bucki R. 2009. Bactericidal activities of the cationic steroid CSA-13 and the cathelicidin peptide LL-37 against Helicobacter pylori in simulated gastric juice. BMC Microbiol 9:187. http://dx.doi.org/10.1186/1471-2180-9-187.
4. Chin JN, Rybak MJ, Cheung CM, Savage PB. 2007. Antimicrobial activities of ceragenins against clinical isolates of resistant Staphylococcus aureus. Antimicrob Agents Chemother 51:1268-1273. http://dx.doi.org/10.1128/AAC.01325-06.
5. Howell MD, Streib JE, Kim BE, Lesley LJ, Dunlap AP, Geng D, Feng Y, Savage PB, Leung DY. 2009. Ceragenins: a class of antiviral compounds to treat orthopox infections. J Invest Dermatol 129:2668-2675. http://dx.doi.org/10.1038/jid.2009.120.
6. Lara D, Feng Y, Bader J, Savage P, Maldonado R. 2010. Antitrypanosomatid activity of ceragenins. J Parasitol 96:638-642. http://dx.doi.org/10.1645/GE-2329.1.
7. Leszczynska K, Namiot D, Byfield FJ, Cruz K, Zendzian-Piotrowska M, Fein DE, Savage PB, Diamond S, McCulloch CA, Janmey PA, Bucki R. 2013. 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 68:610-618. http://dx.doi.org/10.1093/jac/dks434.
8. Sevgi M, Toklu A, Vecchio D, Hamblin MR. 2013. Topical antimicrobials for burn infections: an update. Recent Pat Antiinfect Drug Discov 8:161-197. http://dx.doi.org/10.2174/15748898113089990001.
9. Sinclair KD, Pham TX, Williams DL, Farnsworth RW, Loc-Carrillo CM, Bloebaum RD. 2013. Model development for determining the efficacy of a combination coating for the prevention of perioperative device related infections: a pilot study. J Biomed Mater Res B Appl Biomater 101:1143-1153. http://dx.doi.org/10.1002/jbm.b.32924.
10. Pollard JE, Snarr J, Chaudhary V, Jennings JD, Shaw H, Christiansen B, Wright J, Jia W, Bishop RE, Savage PB. 2012. In vitro evaluation of the potential for resistance development to ceragenin CSA-13. J Antimicrob Chemother 67:2665-2672. http://dx.doi.org/10.1093/jac/dks276.
11. Moscoso M, Esteban-Torres M, Menendez M, Garcia E. 2014. In vitro bactericidal and bacteriolytic activity of ceragenin CSA-13 against planktonic cultures and biofilms of Streptococcus pneumoniae and other pathogenic streptococci. PLoS One 9:e101037. http://dx.doi.org/10.1371/journal.pone.0101037.
12. Nagant C, Pitts B, Stewart PS, Feng Y, Savage PB, Dehaye JP. 2013. Study of the effect of antimicrobial peptide mimic, CSA-13, on an established biofilm formed by Pseudomonas aeruginosa. Microbiologyopen 2:318-325. http://dx.doi.org/10.1002/mbo3.77.
13. Kuroda K, Fukuda T, Okumura K, Yoneyama H, Isogai H, Savage PB, Isogai E. 2013. Ceragenin CSA-13 induces cell cycle arrest and antiproliferative effects in wild-type and p53 null mutant HCT116 colon cancer cells. Anticancer Drugs 24:826-834. http://dx.doi.org/10.1097/CAD.0b013e3283634dd0.
14. Epand RF, Savage PB, Epand RM. 2007. Bacterial lipid composition and the antimicrobial efficacy of cationic steroid compounds (ceragenins). Biochim Biophys Acta 1768:2500-2509. http://dx.doi.org/10.1016/j.bbamem.2007.05.023.
15. Epand RF, Pollard JE, Wright JO, Savage PB, Epand RM. 2010. Depolarization, bacterial membrane composition, and the antimicrobial action of ceragenins. Antimicrob Agents Chemother 54:3708-3713. http://dx.doi.org/10.1128/AAC.00380-10.
16. Evans SE, Xu Y, Tuvim MJ, Dickey BF. 2010. Inducible innate resistance of lung epithelium to infection. Annu Rev Physiol 72:413-435. http://dx.doi.org/10.1146/annurev-physiol-021909-135909.
17. McCray PB, Jr, Bentley L. 1997. Human airway epithelia express a betadefensin. AmJ Respir Cell Mol Biol 16:343-349. http://dx.doi.org/10.1165/ajrcmb.16.3.9070620.
18. Goldman MJ, Anderson GM, Stolzenberg ED, Kari UP, Zasloff M, Wilson JM. 1997. Human β-defensin-1 is a salt-sensitive antibiotic in lung that is inactivated in cystic fibrosis. Cell 88:553-560. http://dx.doi.org/10.1016/S0092-8674 (00) 81895-4.
19. Chen CI, Schaller-Bals S, Paul KP, Wahn U, Bals R. 2004. β-Defensins and LL-37 in bronchoalveolar lavage fluid of patients with cystic fibrosis. J Cyst Fibros 3:45-50. http://dx.doi.org/10.1016/j.jcf.2003.12.008.
20. Bucki R, Leszczynska K, Namiot A, Sokolowski W. 2010. Cathelicidin LL-37: a multitask antimicrobial peptide. Arch Immunol Ther Exp (Warsz) 58:15-25. http://dx.doi.org/10.1007/s00005-009-0057-2.
21. 3 induces pro-LL-37 expression in myeloid precursors from patients with severe congenital neutropenia. J Leukoc Biol 84:1279-1286. http://dx.doi.org/10.1189/jlb.0607437.
22. 3 in various tissues. J Steroid Biochem Mol Biol 103:552-557. http://dx.doi.org/10.1016/j.jsbmb.2006.12.095.
23. Maiti S, Patro S, Purohit S, Jain S, Senapati S, Dey N. 2014. Effective control of Salmonella infections by employing combinations of recombinant antimicrobial human β-defensins hBD-1 and hBD-2. Antimicrob Agents Chemother 58:6896-6903. http://dx.doi.org/10.1128/AAC.03628-14.
24. Cavanagh JP, Granslo HN, Fredheim EA, Christophersen L, Jensen PO, Thomsen K, Van Gennip M, Klingenberg C, Flaegstad T, Moser C. 2013. Efficacy of a synthetic antimicrobial peptidomimetic versus vancomycin in a Staphylococcus epidermidis device-related murine peritonitis model. J Antimicrob Chemother 68:2106-2110. http://dx.doi.org/10.1093/jac/dkt161.
25. Hase K, Eckmann L, Leopard JD, Varki N, Kagnoff MF. 2002. Cell differentiation is a key determinant of cathelicidin LL-37/human cationic antimicrobial protein 18 expression by human colon epithelium. Infect Immun 70:953-963. http://dx.doi.org/10.1128/IAI.70.2.953-963.2002.
26. Schwab M, Reynders V, Shastri Y, Loitsch S, Stein J, Schroder O. 2007. Role of nuclear hormone receptors in butyrate-mediated upregulation of the antimicrobial peptide cathelicidin in epithelial colorectal cells. Mol Immunol 44:2107-2114. http://dx.doi.org/10.1016/j.molimm.2006.09.016.
27. Nanda JS, Lorsch JR. 2014. Labeling a protein with fluorophores using NHS ester derivitization. Methods Enzymol 536:87-94. http://dx.doi.org/10.1016/B978-0-12-420070-8.00008-8.
28. Gootz TD, Subashi TA, Lindner DL. 1988. Simple spectrophotometric assay for measuring protein binding of penem antibiotics to human serum. Antimicrob Agents Chemother 32:159-163. http://dx.doi.org/10.1128/AAC.32.2.159.
29. Plotkowski MC, de Bentzmann S, Pereira SH, Zahm JM, Bajolet-Laudinat O, Roger P, Puchelle E. 1999. Pseudomonas aeruginosa internalization by human epithelial respiratory cells depends on cell differentiation, polarity, and junctional complex integrity. Am J Respir Cell Mol Biol 20:880-890. http://dx.doi.org/10.1165/ajrcmb.20.5.3408.
30. Lee A, Chow D, Haus B, Tseng W, Evans D, Fleiszig S, Chandy G, Machen T. 1999. Airway epithelial tight junctions and binding and cytotoxicity of Pseudomonas aeruginosa. Am J Physiol 277:L204-L217.
31. Chin JN, Jones RN, Sader HS, Savage PB, Rybak MJ. 2008. Potential synergy activity of the novel ceragenin, CSA-13, against clinical isolates of Pseudomonas aeruginosa, including multidrug-resistant P. aeruginosa. J Antimicrob Chemother 61:365-370.
32. Leszczynska K, Namiot A, Cruz K, Byfield FJ, Won E, Mendez G, Sokolowski W, Savage PB, Bucki R, Janmey PA. 2011. Potential of ceragenin CSA-13 and its mixture with pluronic F-127 as treatment of topical bacterial infections. J Appl Microbiol 110:229-238. http://dx.doi.org/10.1111/j.1365-2672.2010.04874.x.
33. Surel U, Niemirowicz K, Marzec M, Savage P, Bucki R. 2014. Ceragenins: a new weapon to fight multidrug resistant bacterial infections. Studia Med 30:207-213.
34. Bozkurt-Guzel C, Savage PB, Akcali A, Ozbek-Celik B. 2014. Potential synergy activity of the novel ceragenin, CSA-13, against carbapenemresistant Acinetobacter baumannii strains isolated from bacteremia patients. Biomed Res Int 2014:710273.
35. Bucki R, Namiot DB, Namiot Z, Savage PB, Janmey PA. 2008. Salivary mucins inhibit antibacterial activity of the cathelicidin-derived LL-37 peptide but not the cationic steroid CSA-13. J Antimicrob Chemother 62:329-335. http://dx.doi.org/10.1093/jac/dkn176.
36. Bucki R, Sostarecz AG, Byfield FJ, Savage PB, Janmey PA. 2007. 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 60:535-545. http://dx.doi.org/10.1093/jac/dkm218.
37. Sinclair KD, Pham TX, Farnsworth RW, Williams DL, Loc-Carrillo C, Horne LA, Ingebretsen SH, Bloebaum RD. 2012. Development of a broad spectrum polymer-released antimicrobial coating for the prevention of resistant strain bacterial infections. J Biomed Mater Res A 100:2732-2738. http://dx.doi.org/10.1002/jbm.a.34209.
38. Williams DL, Sinclair KD, Jeyapalina S, Bloebaum RD. 2013. Characterization of a novel active release coating to prevent biofilm implantrelated infections. J Biomed Mater Res B Appl Biomater 101:1078-1089. http://dx.doi.org/10.1002/jbm.b.32918.
39. Perry EL, Beck JP, Williams DL, Bloebaum RD. 2010. Assessing periimplant tissue infection prevention in a percutaneous model. J Biomed Mater Res B Appl Biomater 92:397-408.
40. Saha S, Savage PB, Bal M. 2008. Enhancement of the efficacy of erythromycin in multiple antibiotic-resistant Gram-negative bacterial pathogens. J Appl Microbiol 105:822-828. http://dx.doi.org/10.1111/j.1365-2672.2008.03820.x.
41. Nagant C, Savage PB, Dehaye JP. 2012. Effect of pluronic acid F-127 on the toxicity towards eukaryotic cells of CSA-13, a cationic steroid analogue of antimicrobial peptides. J Appl Microbiol 112:1173-1183. http://dx.doi.org/10.1111/j.1365-2672.2012.05297.x.
42. Bucki R, Pastore JJ, Randhawa P, Vegners R, Weiner DJ, Janmey PA. 2004. 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 48:1526-1533. http://dx.doi.org/10.1128/AAC.48.5.1526-1533.2004.
43. Guillard T, Cambau E, Chau F, Massias L, de Champs C, Fantin B. 2013. Ciprofloxacin treatment failure in a murine model of pyelonephritis due to an AAC (6=)-Ib-cr-producing Escherichia coli strain susceptible to ciprofloxacin in vitro. Antimicrob Agents Chemother 57:5830-5835. http://dx.doi.org/10.1128/AAC.01489-13.
44. Fahmy S, Abu-Gharbieh E. 2014. In vitro dissolution and in vivo bioavailability of six brands of ciprofloxacin tablets administered in rabbits and their pharmacokinetic modeling. Biomed Res Int 2014:590848.
45. Stott WT, Dryzga MD, Ramsey JC. 1983. Blood-flow distribution in the mouse. J Appl Toxicol 3:310-312. http://dx.doi.org/10.1002/jat.2550030607.
46. Krishnan K, Crouse LC, Bazar MA, Major MA, Reddy G. 2009. Physiologically based pharmacokinetic modeling of cyclotrimethylenetrinitramine in male rats. J Appl Toxicol 29:629-637. http://dx.doi.org/10.1002/jat.1455.
47. 18F]fleroxacin in healthy human subjects studied by using positron emission tomography. Antimicrob Agents Chemother 37:2144-2152. http://dx.doi.org/10.1128/AAC.37.10.2144.
48. Gremse F, Theek B, Kunjachan S, Lederle W, Pardo A, Barth S, Lammers T, Naumann U, Kiessling F. 2014. Absorption reconstruction improves biodistribution assessment of fluorescent nanoprobes using hybrid fluorescence-mediated tomography. Theranostics 4:960-971. http://dx.doi.org/10.7150/thno. 9293.
49. Baker M. 2010. Whole-animal imaging: the whole picture. Nature 463:977-980. http://dx.doi.org/10.1038/463977a.
50. Ntziachristos V, Ripoll J, Wang LV, Weissleder R. 2005. Looking and listening to light: the evolution of whole-body photonic imaging. Nat Biotechnol 23:313-320. http://dx.doi.org/10.1038/nbt1074.
51. Nagant C, Feng Y, Lucas B, Braeckmans K, Savage P, Dehaye JP. 2011. Effect of a low concentration of a cationic steroid antibiotic (CSA-13) on the formation of a biofilm by Pseudomonas aeruginosa. J Appl Microbiol 111:763-772. http://dx.doi.org/10.1111/j.1365-2672.2011.05085.x.
52. Saar-Dover R, Bitler A, Nezer R, Shmuel-Galia L, Firon A, Shimoni E, Trieu-Cuot P, Shai Y. 2012. D-Alanylation of lipoteichoic acids confers resistance to cationic peptides in group B streptococcus by increasing the cell wall density. PLoS Pathog 8:e1002891. http://dx.doi.org/10.1371/journal.ppat.1002891.