Derivatives of the mouse Cathelicidin-Related Antimicrobial Peptide (CRAMP) inhibit fungal and bacterial biofilm formation

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 9, 2014, Pages 5395-5404

  De Brucker, Katrijn ^a   Delattin, Nicolas ^a   Robijns, Stijn ^a   Steenackers, Hans ^a   Verstraeten, Natalie ^a   Landuyt, Bart ^a   Luyten, Walter ^a   Schoofs, Liliane ^a   Dovgan, Barbara ^b   Froḧlich, Mirjam ^b,c   Michiels, Jan ^a   Vanderleyden, Jos ^a   Cammue, Bruno P A ^a,d   Thevissen, Karin ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b Animal Physiology and Neurobiology Section KU Leuven ^*  (Slovenia)

^c JO EF STEFAN INSTITUTE   (Slovenia)

^d DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AS 10; BACTERICIDE; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; FUNGICIDE; P 318; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG; AMPHOTERICIN B; ANTIFUNGAL AGENT; ANTIINFECTIVE AGENT; ANTIMICROBIAL CATIONIC PEPTIDE; CAP18 LIPOPOLYSACCHARIDE-BINDING PROTEIN; CASPOFUNGIN; CATHELICIDIN; CATHELICIDIN ANTIMICROBIAL PEPTIDE; ECHINOCANDIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; BACTERICIDAL ACTIVITY; BIOFILM; BONE REGENERATION; CANDIDA ALBICANS; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; FUNGICIDAL ACTIVITY; FUNGUS GROWTH; GROWTH INHIBITION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PANCREAS ISLET; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; ANIMAL; BACTERIUM; DRUG EFFECTS; MICROBIAL SENSITIVITY TEST; PLANKTON; PROCEDURES;

AMPHOTERICIN B; ANIMALS; ANTI-BACTERIAL AGENTS; ANTIFUNGAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIA; BIOFILMS; CANDIDA ALBICANS; CATHELICIDINS; ECHINOCANDINS; HUMANS; MICE; MICROBIAL SENSITIVITY TESTS; PLANKTON;

EID: 84906085336     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.03045-14     Document Type: Article

References (56)

1. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322. http://dx.doi.org/10.1126/science.284.5418.1318. (Pubitemid 29289651)
2. Douglas LJ. 2003. Candida biofilms and their role in infection. Trends Microbiol. 11:30-36. http://dx.doi.org/10.1016/S0966-842X(02)00002-1. (Pubitemid 36084353)
3. Kojic EM, Darouiche RO. 2004. Candida infections of medical devices. Clin. Microbiol. Rev. 17:255-267. http://dx.doi.org/10.1128/CMR.17.2.255-267. 2004. (Pubitemid 38534029)
4. Ramage G, Martinez JP, Lopez-Ribot JL. 2006. Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res. 6:979-986. http://dx.doi.org/10.1111/j.1567-1364.2006.00117.x.
5. Fanning S, Mitchell AP. 2012. Fungal biofilms. PLoS Pathog. 8:e1002585. http://dx.doi.org/10.1371/journal.ppat.1002585.
6. Seneviratne CJ, Jin L, Samaranayake LP. 2008. Biofilm lifestyle of Candida: a mini review. Oral Dis. 14:582-590. http://dx.doi.org/10.1111/j.1601- 0825.2007.01424.x.
7. Römling U, Balsalobre C. 2012. Biofilm infections, their resilience to therapy and innovative treatment strategies. J. Intern. Med. 272:541-561. http://dx.doi.org/10.1111/joim.12004.
8. Bostanci N, Belibasakis GN. 2012. Porphyromonas gingivalis: an invasive and evasive opportunistic oral pathogen. FEMS Microbiol. Lett. 333:1-9. http://dx.doi.org/10.1111/j.1574-6968.2012.02579.x.
9. Folkesson A, Jelsbak L, Yang L, Johansen HK, Ciofu O, Hoiby N, Molin S. 2012. Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective. Nat. Rev. Microbiol. 10:841-851. http://dx.doi.org/10. 1038/nrmicro2907.
10. Livermore DM. 2012. Current epidemiology and growing resistance of gram-negative pathogens. Korean J. Intern. Med. 27:128-142. http://dx.doi.org/ 10.3904/kjim.2012.27.2.128.
11. Bink A, Kucharikova S, Neirinck B, Vleugels J, Van Dijck P, Cammue BP, Thevissen K. 2012. The nonsteroidal antiinflammatory drug diclofenac potentiates the in vivo activity of caspofungin against Candida albicans biofilms. J. Infect. Dis. 206:1790-1797. http://dx.doi.org/10.1093/infdis/jis594.
12. Bonez PC, Dos Santos Alves CF, Dalmolin TV, Agertt VA, Mizdal CR, Flores Vda C, Marques JB, Santos RC, Anraku de Campos MM. 2013. Chlorhexidine activity against bacterial biofilms. Am. J. Infect. Control 41:e119-e122. http://dx.doi.org/10.1016/j.ajic.2013.05.002.
13. Danscher G, Locht LJ. 2010. In vivo liberation of silver ions from metallic silver surfaces. Histochem. Cell Biol. 133:359-366. http://dx.doi.org/10.1007/s00418-009-0670-5.
14. Bowdish DM, Davidson DJ, Scott MG, Hancock RE. 2005. Immunomodulatory activities of small host defense peptides. Antimicrob. Agents Chemother. 49:1727-1732. http://dx.doi.org/10.1128/AAC.49.5.1727-1732.2005. (Pubitemid 40631581)
15. Brown KL, Hancock RE. 2006. Cationic host defense (antimicrobial) peptides. Curr. Opin. Immunol. 18:24-30. http://dx.doi.org/10.1016/j.coi.2005. 11.004. (Pubitemid 43049644)
16. Overhage J, Campisano A, Bains M, Torfs EC, Rehm BH, Hancock RE. 2008. Human host defense peptide LL-37 prevents bacterial biofilm formation. Infect. Immun. 76:4176-4182. http://dx.doi.org/10.1128/IAI.00318-08.
17. Lohan S, Bisht GS. 2013. Recent approaches in design of peptidomimetics for antimicrobial drug discovery research. Mini Rev. Med. Chem. 13: 1073-1088. http://dx.doi.org/10.2174/1389557511313070010.
18. Kanthawong S, Bolscher JG, Veerman EC, van Marle J, de Soet HJ, Nazmi K, Wongratanacheewin S, Taweechaisupapong S. 2012. Antimicrobial and antibiofilm activity of LL-37 and its truncated variants against Burkholderia pseudomallei. Int. J. Antimicrob. Agents 39:39-44. http://dx.doi.org/10.1016/j.ijantimicag. 2011.09.010.
19. Nagant C, Pitts B, Nazmi K, Vandenbranden M, Bolscher JG, Stewart PS, Dehaye JP. 2012. Identification of peptides derived from the human antimicrobial peptide LL-37 active against biofilms formed by Pseudomonas aeruginosa using a library of truncated fragments. Antimicrob. Agents Chemother. 56:5698-5708. http://dx.doi.org/10.1128/AAC.00918-12.
20. Wong JH, Ng TB, Legowska A, Rolka K, Hui M, Cho CH. 2011. Antifungal action of human cathelicidin fragment (LL13-37) on Candida albicans. Peptides 32:1996-2002. http://dx.doi.org/10.1016/j.peptides.2011.08.018.
21. Feng X, Sambanthamoorthy K, Palys T, Paranavitana C. 2013. The human antimicrobial peptide LL-37 and its fragments possess both antimicrobial and antibiofilm activities against multidrug-resistant Acinetobacter baumannii. Peptides 49:131-137. http://dx.doi.org/10.1016/j.peptides.2013.09.007.
22. Butts A, Krysan DJ. 2012. Antifungal drug discovery: something old and something new. PLoS Pathog. 8:e1002870. http://dx.doi.org/10.1371/journal.ppat. 1002870.
23. Bowdish DM, Davidson DJ, Lau YE, Lee K, Scott MG, Hancock RE. 2005. Impact of LL-37 on anti-infective immunity. J. Leukoc. Biol. 77: 451-459. http://dx.doi.org/10.1189/jlb.0704380. (Pubitemid 40489520)
24. Hell E, Giske CG, Nelson A, Romling U, Marchini G. 2010. Human cathelicidin peptide LL37 inhibits both attachment capability and biofilm formation of Staphylococcus epidermidis. Lett. Appl. Microbiol. 50:211-215. http://dx.doi.org/10.1111/j.1472-765X.2009.02778.x.
25. Kanthawong S, Nazmi K, Wongratanacheewin S, Bolscher JG, Wuthiekanun V, Taweechaisupapong S. 2009. In vitro susceptibility of Burkholderia pseudomallei to antimicrobial peptides. Int. J. Antimicrob. Agents 34:309-314. http://dx.doi.org/10.1016/j.ijantimicag.2009.05.012.
26. Tsai PW, Yang CY, Chang HT, Lan CY. 2011. Human antimicrobial peptide LL-37 inhibits adhesion of Candida albicans by interacting with yeast cell-wall carbohydrates. PLoS One 6:e17755. http://dx.doi.org/10.1371/journal.pone. 0017755.
27. Chang HT, Tsai PW, Huang HH, Liu YS, Chien TS, Lan CY. 2012. LL37 and hBD-3 elevate the beta-1,3-exoglucanase activity of Candida albicans Xog1p, resulting in reduced fungal adhesion to plastic. Biochem. J. 441:963-970. http://dx.doi.org/10.1042/BJ20111454.
28. Fonzi WA, Irwin MY. 1993. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134:717-728. (Pubitemid 23193572)
29. Plaine A, Walker L, Da Costa G, Mora-Montes HM, McKinnon A, Gow NA, Gaillardin C, Munro CA, Richard ML. 2008. Functional analysis of Candida albicans GPI-anchored proteins: roles in cell wall integrity and caspofungin sensitivity. Fungal Genet. Biol. 45:1404-1414. http://dx.doi.org/10.1016/j.fgb. 2008.08.003.
30. Kaur R, Ma B, Cormack BP. 2007. A family of glycosylphosphatidyli- nositol-linked aspartyl proteases is required for virulence of Candida glabrata. Proc. Natl. Acad. Sci. U. S. A. 104:7628-7633. http://dx.doi.org/10.1073/pnas. 0611195104. (Pubitemid 47185957)
31. Sullivan DJ, Westerneng TJ, Haynes KA, Bennett DE, Coleman DC. 1995. Candida dubliniensis sp. nov.: phenotypic and molecular characterization of a novel species associated with oral candidosis in HIV-infected individuals. Microbiology 141(Pt 7):1507-1521. http://dx.doi.org/10.1099/13500872-141-7-1507.
32. Thevissen K, Pellens K, De Brucker K, Francois IE, Chow KK, Meert EM, Meert W, Van Minnebruggen G, Borgers M, Vroome V, Levin J, De Vos D, Maes L, Cos P, Cammue BP. 2011. Novel fungicidal benzylsulfanyl-phenylguanidines. Bioorg. Med. Chem. Lett. 21:3686-3692. http://dx.doi.org/10.1016/j.bmcl.2011.04.075.
33. Sambrook JF, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
34. Liberati NT, Urbach JM, Miyata S, Lee DG, Drenkard E, Wu G, Villanueva J, Wei T, Ausubel FM. 2006. An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc. Natl. Acad. Sci. U. S. A. 103:2833-2838. http://dx.doi.org/10.1073/pnas.0511100103.
35. Coykendall AL, Kaczmarek FS, Slots J. 1980. Genetic-heterogeneity in bacteroides-asaccharolyticus (holdeman and moore 1970) finegold and barnes 1977 (approved lists, 1980) and proposal of bacteroides-gingivalis sp-nov and bacteroides-macacae (slots and genco) comb-nov. Int. J. Syst. Bacteriol. 30:559-564. http://dx.doi.org/10.1099/00207713-30-3-559. (Pubitemid 10013529)
36. O'Brien J, Wilson I, Orton T, Pognan F. 2000. Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur. J. Biochem. 267:5421-5426. http://dx.doi.org/10.1046/j.1432- 1327.2000.01606.x.
37. Tellier R, Krajden M, Grigoriew GA, Campbell I. 1992. Innovative endpoint determination system for antifungal susceptibility testing of yeasts. Antimicrob. Agents Chemother. 36:1619-1625. http://dx.doi.org/10.1128/AAC.36.8. 1619.
38. Delattin N, De Brucker K, Vandamme K, Meert E, Marchand A, Chaltin P, Cammue BP, Thevissen K. 2014. Repurposing as a means to increase the activity of amphotericin B and caspofungin against Candida albicans biofilms. J. Antimicrob. Chemother. 69:1035-1044. http://dx.doi.org/10.1093/jac/dkt449.
39. Delattin N, De Brucker K, Craik DJ, Cheneval O, Frohlich M, Veber M, Girandon L, Davis TR, Weeks AE, Kumamoto CA, Cos P, Coenye T, De Coninck B, Cammue BP, Thevissen K. 2014. Plant-derived decapeptide OSIP108 interferes with Candida albicans biofilm formation without affecting cell viability. Antimicrob. Agents Chemother. 58:2647-2656. http://dx.doi.org/10.1128/AAC.01274-13.
40. Janssens JC, Steenackers H, Robijns S, Gellens E, Levin J, Zhao H, Hermans K, De Coster D, Verhoeven TL, Marchal K, Vanderleyden J, De Vos DE, De Keersmaecker SC. 2008. Brominated furanones inhibit biofilm formation by Salmonella enterica serovar Typhimurium. Appl. Environ. Microbiol. 74:6639-6648. http://dx.doi.org/10.1128/AEM.01262-08.
41. Steenackers HP, Ermolat'ev DS, Savaliya B, Weerdt AD, Coster DD, Shah A, Van der Eycken EV, De Vos DE, Vanderleyden J, De Keersmaecker SC. 2011. Structure-activity relationship of 2-hydroxy-2-aryl-2,3-dihydro-imidazo[1,2-a] pyrimidinium salts and 2N-substituted 4(5)- aryl-2-amino-1H-imidazoles as inhibitors of biofilm formation by Salmonella Typhimurium and Pseudomonas aeruginosa. Bioorg. Med. Chem. 19:3462-3473. http://dx.doi.org/10.1016/j.bmc. 2011.04.026.
42. Odds FC. 2003. Synergy, antagonism, and what the chequerboard puts between them. J. Antimicrob. Chemother. 52:1. http://dx.doi.org/10.1093/jac/ dkg301. (Pubitemid 36850074)
43. Boonen K, Baggerman G, D'Hertog W, Husson SJ, Overbergh L, Mathieu C, Schoofs L. 2007. Neuropeptides of the islets of Langerhans: a peptidomics study. Gen. Comp. Endocrinol. 152:231-241. http://dx.doi.org/10.1016/j.ygcen.2007.05. 002. (Pubitemid 46950889)
44. Shin SY, Kang SW, Lee DG, Eom SH, Song WK, Kim JI. 2000. CRAMP analogues having potent antibiotic activity against bacterial, fungal, and tumor cells without hemolytic activity. Biochem. Biophys. Res. Commun. 275:904-909. http://dx.doi.org/10.1006/bbrc.2000.3269.
45. Harriott MM, Noverr MC. 2011. Importance of Candida-bacterial polymicrobial biofilms in disease. Trends Microbiol. 19:557-563. http://dx.doi.org/10.1016/j.tim.2011.07.004.
46. Harriott MM, Noverr MC. 2009. Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob. Agents Chemother. 53:3914-3922. http://dx.doi.org/10.1128/AAC.00657-09.
47. Harriott MM, Noverr MC. 2010. Ability of Candida albicans mutants to induce Staphylococcus aureus vancomycin resistance during polymicrobial biofilm formation. Antimicrob. Agents Chemother. 54:3746-3755. http://dx.doi.org/10. 1128/AAC.00573-10.
48. Adam B, Baillie GS, Douglas LJ. 2002. Mixed species biofilms of Candida albicans and Staphylococcus epidermidis. J. Med. Microbiol. 51:344-349. (Pubitemid 34252657)
49. Marr KA. 2004. Invasive Candida infections: the changing epidemiology. Oncology (Williston Park) 18(Suppl 13):9-14.
50. Pfaller MA, Diekema DJ. 2010. Epidemiology of invasive mycoses in North America. Crit. Rev. Microbiol. 36:1-53. http://dx.doi.org/10.3109/ 10408410903241444.
51. Pfaller MA, Messer SA, Moet GJ, Jones RN, Castanheira M. 2011. Candida bloodstream infections: comparison of species distribution and resistance to echinocandin and azole antifungal agents in Intensive Care Unit (ICU) and non-ICU settings in the SENTRY Antimicrobial Surveillance Program (2008-2009). Int. J. Antimicrob. Agents 38:65-69. http://dx.doi.org/10.1016/j.ijantimicag. 2011.02.016.
52. Pfaller M, Neofytos D, Diekema D, Azie N, Meier-Kriesche HU, Quan SP, Horn D. 2012. Epidemiology and outcomes of candidemia in 3648 patients: data from the Prospective Antifungal Therapy (PATH Alliance(R)) registry, 2004-2008. Diagn. Microbiol. Infect. Dis. 74:323-331. http://dx.doi.org/10.1016/j. diagmicrobio.2012.10.003.
53. Diekema D, Arbefeville S, Boyken L, Kroeger J, Pfaller M. 2012. The changing epidemiology of healthcare-associated candidemia over three decades. Diagn. Microbiol. Infect. Dis. 73:45-48. http://dx.doi.org/10.1016/j. diagmicrobio.2012.02.001.
54. Wisplinghoff H, Ebbers J, Geurtz L, Stefanik D, Major Y, Edmond MB, Wenzel RP, Seifert H. 2014. Nosocomial bloodstream infections due to Candida spp. in the U. S. A.: species distribution, clinical features and antifungal susceptibilities. Int. J. Antimicrob. Agents 43:78-81.
55. Kaufman DA, Brown AT, Eisenhuth KK, Yue J, Grossman LB, Hazen KC. 2014. More serious infectious morbidity and mortality associated with simultaneous candidemia and coagulase-negative staphylococcal bacteremia in neonates and in vitro adherence studies between Candida albicans and Staphylococcus epidermidis. Early Hum. Dev. 90(Suppl 1): S66 -S70. http://dx.doi.org/10.1016/S0378-3782(14) 70021-0.
56. Venkatesh MP, Pham D, Fein M, Kong L, Weisman LE. 2007. Neonatal coinfection model of coagulase-negative Staphylococcus (Staphylococcus epidermidis) and Candida albicans: fluconazole prophylaxis enhances survival and growth. Antimicrob. Agents Chemother. 51:1240-1245. http://dx.doi.org/10.1128/ AAC.01298-06. (Pubitemid 46586800)