Activity of potent and selective host defense peptide mimetics in mouse models of oral candidiasis

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 7, 2014, Pages 3820-3827

  Ryan, Lisa K ^a,g   Freeman, Katie B ^b   Masso Silva, Jorge A ^c   Falkovsky, Klaudia ^c   Aloyouny, Ashwag ^c   Markowitz, Kenneth ^c   Hise, Amy G ^d,e,f   Fatahzadeh, Mahnaz ^c   Scott, Richard W ^b   Diamond, Gill ^c,h  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b Fox Chase Chemical Diversity Center   (United States)

^c RUTGERS SCHOOL OF DENTAL MEDICINE   (United States)

^d CASE WESTERN RESERVE UNIVERSITY   (United States)

^e CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f DEPARTMENT OF VETERANS AFFAIRS   (United States)

^g UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^h UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; ANTIFUNGAL AGENT; CHLORAMPHENICOL; HOST DEFENSE PEPTIDE; HYDROXYETHYLCELLULOSE; MPE; NYSTATIN; PMX 519; POLYPEPTIDE ANTIBIOTIC AGENT; TETRACYCLINE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BETA DEFENSIN; PEPTIDE;

3T3 CELL LINE; ACTINOMYCES VISCOSUS; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANDIDA ALBICANS; CANDIDA DUBLINIENSIS; CANDIDA GLABRATA; CANDIDA KRUSEI; CANDIDA PARAPSILOSIS; CANDIDA TROPICALIS; CLINICAL ARTICLE; COLONY FORMING UNIT; COMMENSAL; CONTROLLED STUDY; CYTOTOXICITY ASSAY; DRUG CYTOTOXICITY; FLUORESCENCE MICROSCOPY; FUNGAL CELL CULTURE; FUNGICIDAL ACTIVITY; FUNGUS CULTURE; FUNGUS HYPHAE; GENE DELETION; HEPG2 CELL LINE; HIGH THROUGHPUT SCREENING; HOST RESISTANCE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HYDROGEL; IC 50; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; KERATINOCYTE; MALE; MICROBIOME; MINIMUM INHIBITORY CONCENTRATION; MOUSE; NONHUMAN; PATHOGEN LOAD; PRIORITY JOURNAL; STREPTOCOCCUS SALIVARIUS; THRUSH; ANIMAL; ANTIFUNGAL RESISTANCE; BACTERIUM; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; IMMUNOCOMPROMIZED PATIENT; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MOLECULAR MIMICRY;

3T3 CELLS; ANIMALS; ANTI-BACTERIAL AGENTS; ANTIFUNGAL AGENTS; BACTERIA; BETA-DEFENSINS; CANDIDA ALBICANS; CANDIDIASIS, ORAL; CELL SURVIVAL; DRUG RESISTANCE, FUNGAL; HIGH-THROUGHPUT SCREENING ASSAYS; HYPHAE; IMMUNOCOMPROMISED HOST; MALE; MICE; MICROBIAL SENSITIVITY TESTS; MOLECULAR MIMICRY; PEPTIDES;

EID: 84903163434     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02649-13     Document Type: Article

References (47)

1. Altarawneh S, Bencharit S, Mendoza L, Curran A, Barrow D, Barros S, Preisser J, Loewy ZG, Gendreau L, Offenbacher S. 2013. Clinical and histological findings of denture stomatitis as related to intraoral colonization patterns of Candida albicans, salivary flow, and dry mouth. J. Prosthodont. 22: 13-22. http://dx.doi.org/10.1111/j.1532-849X.2012.00906.x.
2. Akpan A, Morgan R. 2002. Oral candidiasis. Postgrad. Med. J. 78:455-459. http://dx.doi.org/10.1136/pmj.78.922.455. (Pubitemid 34948150)
3. Rodu B, Carpenter JT, Jones MR. 1988. The pathogenesis and clinical significance of cytologically detectable oral Candida in acute leukemia. Cancer 62:2042-2046. http://dx.doi.org/10.1002/1097-0142(19881101)62:9〈2042::AID- CNCR2820620928〉3.0.CO;2-D.
4. Dupont B, Graybill JR, Armstrong D, Laroche R, Touze JE, Wheat LJ. 1992. Fungal infections in AIDS patients. J. Med. Vet. Mycol. 30(Suppl 1):19-28. http://dx.doi.org/10.1080/02681219280000731. (Pubitemid 23055885)
5. Dongari-Bagtzoglou A, Fidel PL, Jr. 2005. The host cytokine responses and protective immunity in oropharyngeal candidiasis. J. Dent. Res. 84: 966-977. http://dx.doi.org/10.1177/154405910508401101. (Pubitemid 43828140)
6. Gupta KL, Ghosh AK, Kochhar R, Jha V, Chakrabarti A, Sakhuja V. 1994. Esophageal candidiasis after renal transplantation: comparative study in patients on different immunosuppressive protocols. Am. J. Gastroenterol. 89:1062-1065. (Pubitemid 24201845)
7. Walsh TJ, Gonzalez CE, Piscitelli S, Bacher JD, Peter J, Torres R, Shetti D, Katsov V, Kligys K, Lyman CA. 2000. Correlation between in vitro and in vivo antifungal activities in experimental fluconazole-resistant oropharyngeal and esophageal candidiasis. J. Clin. Microbiol. 38:2369-2373. (Pubitemid 30414367)
8. Sheft DJ, Shrago G. 1970. Esophageal moniliasis. The spectrum of the disease. JAMA 213:1859-1862.
9. Thom K, Forrest G. 2006. Gastrointestinal infections in immunocompromised hosts. Curr. Opin. Gastroenterol. 22:18-23. (Pubitemid 44124278)
10. Lortholary O, Petrikkos G, Akova M, Arendrup MC, Arikan-Akdagli S, Bassetti M, Bille J, Calandra T, Castagnola E, Cornely OA, Cuenca-Estrella M, Donnelly JP, Garbino J, Groll AH, Herbrecht R, Hope WW, Jensen HE, Kullberg BJ, Lass-Florl C, Meersseman W, Richardson MD, Roilides E, Verweij PE, Viscoli C, Ullmann AJ, ESMID Fungal Infection Study Group. 2012. ESCMID*guideline for the diagnosis and management of Candida diseases 2012: patients with HIV infection or AIDS. Clin. Microbiol. Infect. 18(Suppl 7):68-77. http://dx.doi.org/10.1111/1469-0691.12042.
11. Ghannoum MA, Rice LB. 1999. Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin. Microbiol. Rev. 12:501-517. (Pubitemid 29484744)
12. Diamond G, Beckloff N, Weinberg A, Kisich KO. 2009. The roles of antimicrobial peptides in innate host defense. Curr. Pharm. Des. 15:2377-2392. http://dx.doi.org/10.2174/138161209788682325.
13. Strom MB, Haug BE, Skar ML, Stensen W, Stiberg T, Svendsen JS. 2003. The pharmacophore of short cationic antibacterial peptides. J. Med. Chem. 46:1567-1570. http://dx.doi.org/10.1021/jm0340039. (Pubitemid 36444211)
14. Mensa B, Kim YH, Choi S, Scott R, Caputo GA, DeGrado WF. 2011. Antibacterial mechanism of action of arylamide foldamers. Antimicrob. Agents Chemother. 55:5043-5053. http://dx.doi.org/10.1128/AAC.05009-11.
15. Tew GN, Scott RW, Klein ML, DeGrado WF. 2010. De novo design of antimicrobial polymers, foldamers and small molecules: from discovery to practical applications. Acc. Chem. Res. 43:30-39. http://dx.doi.org/10.1021/ ar900036b.
16. Choi S, Isaacs A, Clements D, Liu D, Kim H, Scott RW, Winkler JD, DeGrado WF. 2009. De novo design and in vivo activity of conformationally restrained antimicrobial arylamide foldamers. Proc. Natl. Acad. Sci. U. S. A. 106:6968-6973. http://dx.doi.org/10.1073/pnas.0811818106.
17. Jorgensen D, Scott RW, Korczak B. 2012. A phase 2 randomized double-blinded dose-ranging active controlled efficacy and safety evaluation of PMX-30063 for the treatment of acute skin and skin structure infections (ABSSSI) caused by Staphylococcus aureus (SA). Abstr. 52nd Intersci. Conf. Antimicrob. Agents Chemother, p L1-1662.
18. Hua J, Yamarthy R, Felsenstein S, Scott RW, Markowitz K, Diamond G. 2010. Activity of antimicrobial peptide mimetics in the oral cavity. I. Activity against biofilms of Candida albicans. Mol. Oral Microbiol. 25:418-425. http://dx.doi.org/10.1111/j.2041-1014.2010.00590.x.
19. Beckloff N, Laube D, Castro T, Furgang D, Park S, Perlin D, Clements D, Tang H, Scott RW, Tew GN, Diamond G. 2007. Activity of an antimicrobial peptide mimetic against planktonic and biofilm cultures of oral pathogens. Antimicrob. Agents Chemother. 51:4125-4132. http://dx.doi.org/10.1128/AAC.00208-07. (Pubitemid 350057814)
20. National Committee for Clinical Laboratory Standards. 2002. Reference method for broth dilution antifungal susceptibility testing of yeasts; approved standard. National Committee for Clinical Laboratory Standards, Wayne, PA.
21. Chambers RS, Sullivan PA. 1993. Expression of the exoglucanase gene in yeast and hyphal forms of Candida albicans. FEMS Microbiol. Lett. 111: 63-67. http://dx.doi.org/10.1111/j.1574-6968.1993.tb06362.x. (Pubitemid 23220971)
22. Dowell SJ, Brown AJ. 2009. Yeast assays for G protein-coupled receptors. Methods Mol. Biol. 552:213-229. http://dx.doi.org/10.1007/978-1-60327-317-6-15.
23. Kuhn DM, Balkis M, Chandra J, Mukherjee PK, Ghannoum MA. 2003. Uses and limitations of the XTT assay in studies of Candida growth and metabolism. J. Clin. Microbiol. 41:506-508. http://dx.doi.org/10.1128/JCM.41.1.506-508.2003. (Pubitemid 36098635)
24. Espinel-Ingroff A, Canton E. 2007. Antifungal susceptibility testing of filamentous fungi, p 209-242. In Schwalbe R, Steele-Moore L, Goodwin AC (ed), Antimicrobial susceptibility testing protocols. CRC Press, Boca Raton, FL.
25. McMahon L, Schwartz K, Yilmaz O, Brown E, Ryan LK, Diamond G. 2011. Vitamin D-mediated induction of innate immunity in gingival epithelial cells. Infect. Immun. 79:2250-2256. http://dx.doi.org/10.1128/IAI.00099-11.
26. Solis NV, Filler SG. 2012. Mouse model of oropharyngeal candidiasis. Nat. Protoc. 7:637-642. http://dx.doi.org/10.1038/nprot.2012.011.
27. Moser C, Weiner DJ, Lysenko E, Bals R, Weiser JN, Wilson JM. 2002. beta-Defensin 1 contributes to pulmonary innate immunity in mice. Infect. Immun. 70: 3068-3072. http://dx.doi.org/10.1128/IAI.70.6.3068-3072.2002. (Pubitemid 34564168)
28. Hise AG, Tomalka J, Ganesan S, Patel K, Hall BA, Brown GD, Fitzgerald KA. 2009. An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe 5:487-497. http://dx.doi.org/10.1016/j.chom.2009.05.002.
29. Avery CW, Som A, Xu Y, Tew GN, Chen Z. 2009. Dependence of antimicrobial selectivity and potency on oligomer structure investigated using substrate supported lipid bilayers and sum frequency generation vibrational spectroscopy. Anal. Chem. 81:8365-8372. http://dx.doi.org/10.1021/ac901271f.
30. Benincasa M, Scocchi M, Pacor S, Tossi A, Nobili D, Basaglia G, Busetti M, Gennaro R. 2006. Fungicidal activity of five cathelicidin peptides against clinically isolated yeasts. J. Antimicrob. Chemother. 58:950-959. http://dx.doi.org/10.1093/jac/dkl382.
31. Oppenheim FG, Xu T, McMillian FM, Levitz SM, Diamond RD, Offner GD, Troxler RF. 1988. Histatins, a novel family of histidine-rich proteins in human parotid secretion. Isolation, characterization, primary structure, and fungistatic effects on Candida albicans. J. Biol. Chem. 263:7472-7477.
32. Vylkova S, Jang WS, Li W, Nayyar N, Edgerton M. 2007. Histatin 5 initiates osmotic stress response in Candida albicans via activation of the Hog1 mitogen-activated protein kinase pathway. Eukaryot. Cell 6:1876-1888. http://dx.doi.org/10.1128/EC.00039-07. (Pubitemid 47585576)
33. Wakabayashi H, Abe S, Okutomi T, Tansho S, Kawase K, Yamaguchi H. 1996. Cooperative anti-Candida effects of lactoferrin or its peptides in combination with azole antifungal agents. Microbiol. Immunol. 40:821-825. http://dx.doi.org/10.1111/j.1348-0421.1996.tb01147.x. (Pubitemid 27034132)
34. Zasloff M. 1987. 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. 84:5449-5453. http://dx.doi.org/10.1073/pnas.84.15.5449. (Pubitemid 17129018)
35. Burrows LL, Stark M, Chan C, Glukhov E, Sinnadurai S, Deber CM. 2006. Activity of novel non-amphipathic cationic antimicrobial peptides against Candida species. J. Antimicrob. Chemother. 57:899-907. http://dx.doi.org/10. 1093/jac/dkl056.
36. Nikawa H, Fukushima H, Makihira S, Hamada T, Samaranayake LP. 2004. Fungicidal effect of three new synthetic cationic peptides against Candida albicans. Oral Dis. 10:221-228. http://dx.doi.org/10.1111/j.1601-0825.2004. 01010.x. (Pubitemid 38868575)
37. Takakura N, Wakabayashi H, Ishibashi H, Teraguchi S, Tamura Y, Yamaguchi H, Abe S. 2003. Oral lactoferrin treatment of experimental oral candidiasis in mice. Antimicrob. Agents Chemother. 47:2619-2623. http://dx.doi.org/10.1128/AAC. 47.8.2619-2623.2003. (Pubitemid 36919468)
38. Meiller TF, Hube B, Schild L, Shirtliff ME, Scheper MA, Winkler R, Ton A, Jabra-Rizk MA. 2009. A novel immune evasion strategy of candida albicans: proteolytic cleavage of a salivary antimicrobial peptide. PLoS One 4:e5039. http://dx.doi.org/10.1371/journal.pone.0005039.
39. Espinel-Ingroff A, Pfaller MA, Bustamante B, Canton E, Fothergill A, Fuller J, Gonzalez GM, Lass-Florl C, Lockhart SR, Martin-Mazuelos E, Meis JF, Melhem MS, Ostrosky-Zeichner L, Pelaez T, Szeszs MW, St- Germain G, Bonfietti LX, Guarro J, Turnidge J. 2014. Multilaboratory study of epidemiological cutoff values for detection of resistance in eight Candida species to fluconazole, posaconazole, and voriconazole. Antimicrob. Agents Chemother. 58:2006-2012. http://dx.doi.org/10.1128/AAC.02615-13.
40. Canton E, Peman J, Gobernado M, Viudes A, Espinel-Ingroff A. 2004. Patterns of amphotericin B killing kinetics against seven Candida species. Antimicrob. Agents Chemother. 48:2477-2482. http://dx.doi.org/10.1128/AAC.48.7. 2477-2482.2004. (Pubitemid 38823413)
41. Venisse N, Gregoire N, Marliat M, Couet W. 2008. Mechanism-based pharmacokinetic-pharmacodynamic models of in vitro fungistatic and fungicidal effects against Candida albicans. Antimicrob. Agents Chemother. 52:937-943. http://dx.doi.org/10.1128/AAC.01030-07. (Pubitemid 351358373)
42. Costa AC, Pereira CA, Junqueira JC, Jorge AO. 2013. Recent mouse and rat methods for the study of experimental oral candidiasis. Virulence 4:391-399. http://dx.doi.org/10.4161/viru.25199.
43. Samaranayake YH, Samaranayake LP. 2001. Experimental oral candidiasis in animal models. Clin. Microbiol. Rev. 14:398-429. http://dx.doi.org/10.1128/CMR. 14.2.398-429.2001. (Pubitemid 32294677)
44. Matsubara VH, Silva EG, Paula CR, Ishikawa KH, Nakamae AE. 2012. Treatment with probiotics in experimental oral colonization by Candida albicans in murine model (DBA/2). Oral Dis. 18:260-264. http://dx.doi.org/10.1111/j.1601- 0825.2011.01868.x.
45. Wong SS, Kao RY, Yuen KY, Wang Y, Yang D, Samaranayake LP, Seneviratne CJ. 2014. In vitro and in vivo activity of a novel antifungal small molecule against Candida infections. PLoS One 9:e85836. http://dx.doi.org/10.1371/ journal.pone.0085836.
46. Som A, Navasa N, Percher A, Scott RW, Tew GN, Anguita J. 2012. Identification of synthetic host defense peptide mimics that exert dual antimicrobial and anti-inflammatory activities. Clin. Vaccine Immunol. 19:1784-1791. http://dx.doi.org/10.1128/CVI.00291-12.
47. Thaker HD, Som A, Ayaz F, Lui D, Pan W, Scott RW, Anguita J, Tew GN. 2012. Synthetic mimics of antimicrobial peptides with immunomodulatory responses. J. Am. Chem. Soc. 134:11088-11091. http://dx.doi.org/10.1021/ ja303304j.