In vitro antifungal potency of the moronecidin-like peptide against Candida albicans, Candida glabrata, and Candida tropicalis
-
Nasrin Amirrajab
,
Seyed Amin Ayatollahi Mousavi
,
Behrooz Taheri
,
Samira Salari
,
Noor Ali Ahmadi Sarsahra
Abstract
Background and Objectives: The aim of this study was to investigate the in vitro antifungal potency of the moronecidin-like peptide against Candida albicans, Candida glabrata, and Candida tropicalis.
Materials and Methods: To evaluate the antifungal effect of moronecidin-like peptide, the protocol presented in CLSI M27-A3 and CLSI M27-S4 was used and the minimum inhibitory concentration was determined.
Results: The minimum inhibitory effect of moronecidin-like peptide composition was 8 µg/ml for Candida tropicalis and Candida albicans and 32 µg/ml for Candida glabrata. The MIC of nystatin was determined to be 1.25 µg/ml for Candida glabrata and Candida albicans and 0.625 µg/ml for Candida tropicalis strains. The MFC composition of the moronecidin-like peptide was determined for Candida tropicalis and Candida albicans strains 8 µg/ml and for Candida glabrata strain 64 µg/ml. The results of cytotoxicity and hemolysis of the moronecidin peptide test on macrophage showed that moronecidin peptide has no cytotoxicity and toxicity properties.
Conclusion: According to the results of the present study, the moronecidin-like peptide could be a new strategy in the treatment of infections caused by Candida strains. The discovery of the exact mechanism of which requires extensive clinical studies in this field.
1. Bongomin F, Gago S, Oladele RO, Denning DW. Global and multi-national prevalence of fungal diseases—estimate precision. J Fungi (Basel) 2017; 3: 57.
2. Köhler JR, Hube B, Puccia R, Casadevall A, Perfect JR. Fungi that infect humans. Microbiol Spectr 2017; 5: 10.1128/microbiolspec.FUNK-0014-2016.
3. Köhler JR, Casadevall A, Perfect J. The spectrum of fungi that infects humans. Cold Spring Harb Perspect Med 2014; 5: a019273.
4. Akeme Yamamoto AC, de Paula CR, Dias LB, Tadano T, Martins ÉR, Amadio JV, et al. Epidemiological and clinical characteristics of nosocomial candidiasis in university hospitals in Cuiabá–Mato Grosso, Brazil. Rev Iberoam Micol 2012; 29: 164-168.
5. McCarty TP, Pappas PG. Invasive candidiasis. Infect Dis Clin North Am 2016; 30: 103-124.
6. Vallabhaneni S, Kallen A, Tsay S, Chow N, Welsh R, Kerins J, et al. Investigation of the first seven reported cases of Candida auris, a globally emerging invasive, multidrug-resistant fungus—United States, May 2013–August 2016. MMWR Morb Mortal Wkly Rep 2016; 65: 1234-1237.
7. Piispanen AE, Hogan DA. PEPped up: induction of Candida albicans virulence by bacterial cell wall fragments. Cell Host Microbe 2008; 4: 1-2.
8. Shao L-C, Sheng C-Q, Zhang W-N. Recent advances in the study of antifungal lead compounds with new chemical scaffolds. Yao Xue Xue Bao 2007; 42: 1129-1136.
9. Negri M, Martins M, Henriques M, Svidzinski TI, Azeredo J, Oliveira R. Examination of potential virulence factors of Candida tropicalis clinical isolates from hospitalized patients. Mycopathologia 2010; 169: 175-182.
10. Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 2004; 39: 309-317.
11. Kullberg BJ, Arendrup MC. Invasive candidiasis. N Engl J Med 2015; 373: 1445-1456.
12. Brandt ME, Lockhart SR. Recent taxonomic developments with Candida and other opportunistic yeasts. Curr Fungal Infect Rep 2012; 6: 170-177.
13. Colombo AL, Nucci M, Park BJ, Nouér SA, Arthington-Skaggs B, da Matta DA, et al. Epidemiology of candidemia in Brazil: a nationwide sentinel surveillance of candidemia in eleven medical centers. J Clin Microbiol 2006; 44: 2816-2823.
14. Pfaller MA, Diekema D, Group IFSP. Twelve years of fluconazole in clinical practice: global trends in species distribution and fluconazole susceptibility of bloodstream isolates of Candida. Clin Microbiol Infect 2004; 10 Suppl 1: 11-23.
15. Rodrigues CF, Silva S, Henriques M. Candida glabrata: a review of its features and resistance. Eur J Clin Microbiol Infect Dis 2014; 33: 673-688.
16. Wiederhold NP. Antifungal resistance: current trends and future strategies to combat. Infect Drug Resist 2017; 10: 249-259.
17. Choi MJ, Won EJ, Shin JH, Kim SH, Lee W-G, Kim M-N, et al. Resistance mechanisms and clinical features of fluconazole-nonsusceptible Candida tropicalis isolates compared with fluconazole-less-susceptible isolates. Antimicrob Agents Chemother 2016; 60: 3653-3661.
18. Seneviratne CJ, Rajan S, Wong SS, Tsang DN, Lai CK, Samaranayake LP, et al. Antifungal susceptibility in serum and virulence determinants of candida bloodstream isolates from Hong Kong. Front Microbiol 2016; 7: 216.
19. Pfaller MA, Diekema DJ, Gibbs DL, Newell VA, Ellis D, Tullio V, et al. Results from the ARTEMIS DISK Global Antifungal Surveillance Study, 1997 to 2007: a 10.5-year analysis of susceptibilities of Candida Species to fluconazole and voriconazole as determined by CLSI standardized disk diffusion. J Clin Microbiol 2010; 48: 1366-1377.
20. Healey KR, Perlin DS. Fungal resistance to echinocandins and the MDR phenomenon in Candida glabrata. J Fungi (Basel) 2018; 4: 105.
21. Cheng J-W, Yu S-Y, Xiao M, Wang H, Kudinha T, Kong F, et al. Identification and antifungal susceptibility profile of Candida guilliermondii and Candida fermentati from a multicenter study in China. J Clin Microbiol 2016; 54: 2187-2189.
22. Mohammadi M, Taheri B, Momenzadeh N, Salarinia R, Nabipour I, Farshadzadeh Z, et al. Identification and characterization of novel antimicrobial peptide from hippocampus comes by In Silico and experimental studies. Mar Biotechnol (NY) 2018; 20: 718-728.
23. McMillan KAM, Coombs MRP. Investigating potential applications of the fish anti-microbial peptide pleurocidin: a systematic review. Pharmaceuticals (Basel) 2021; 14: 687.
24. Del Gaudio G, Lombardi L, Maisetta G, Esin S, Batoni G, Sanguinetti M, et al. Antifungal activity of the noncytotoxic human peptide hepcidin 20 against fluconazole-resistant Candida glabrata in human vaginal fluid. Antimicrob Agents Chemother 2013; 57: 4314-4321.
25. Gerdol M, Puillandre N, De Moro G, Guarnaccia C, Lucafò M, Benincasa M, et al. Identification and characterization of a novel family of cysteine-rich peptides (MgCRP-I) from Mytilus galloprovincialis. Genome Biol Evol 2015; 7: 2203-2219.
26. Silphaduang U, Noga EJ. Peptide antibiotics in mast cells of fish. Nature 2001; 414: 268-269.
27. Taheri B, Mohammadi M, Nabipour I, Momenzadeh N, Roozbehani M. Identification of novel antimicrobial peptide from Asian sea bass (Lates calcarifer) by in silico and activity characterization. PLoS One 2018; 13(10): e0206578.
28. Lauth X, Shike H, Burns JC, Westerman ME, Ostland VE, Carlberg JM, et al. Discovery and characterization of two isoforms of moronecidin, a novel antimicrobial peptide from hybrid striped bass. J Biol Chem 2002; 277: 5030-5039.
29. Houyvet B, Bouchon-Navaro Y, Bouchon C, Goux D, Bernay B, Corre E, et al. Identification of a moronecidin-like antimicrobial peptide in the venomous fish Pterois volitans: Functional and structural study of pteroicidin-α. Fish Shellfish Immunol 2018; 72: 318-324.
30. Wu Y, Zhang G, Zhou M. Inhibitory and anti‐inflammatory effects of two antimicrobial peptides moronecidin and temporin‐1Dra against Propionibacterium acnes in vitro and in vivo. J Pept Sci 2020; 26(7): e3255.
31. Wayne P. Clinical and Laboratory Standards Institute. Reference method for broth dilution antifungal susceptibility testing of filamentous fungi. CLSI Document M38-A2. Clinical and Laboratory Standards Institute, 2008.
32. Wayne P. Reference method for broth dilution antifungal susceptibility testing of yeasts, approved standard. CLSI document M27-A2. 2002.
33. Santos ERd, Forno CFD, Hernandez MG, Kubiça TF, Venturini TP, Chassot F, et al. Susceptibility of Candida spp. isolated from blood cultures as evaluated using the M27-A3 and new M27-S4 approved breakpoints. Rev Inst Med Trop Sao Paulo 2014; 56: 477-482.
34. Fernández de Ullivarri M, Arbulu S, Garcia-Gutierrez E, Cotter PD. Antifungal peptides as therapeutic agents. Front Cell Infect Microbiol 2020; 10: 105.
35. Ostrosky-Zeichner L, Bazemore S, Paetznick VL, Rodriguez JR, Chen E, Wallace T, et al. Differential antifungal activity of isomeric forms of nystatin. Antimicrob Agents Chemother 2001; 45: 2781-2786.
36. Kebede B, Shibeshi W. In vitro antibacterial and antifungal activities of extracts and fractions of leaves of Ricinus communis Linn against selected pathogens. Vet Med Sci 2022; 8: 1802-1815.
37. Stark M, Liu L-P, Deber CM. Cationic hydrophobic peptides with antimicrobial activity. Antimicrob Agents Chemother 2002; 46: 3585-3590.
38. Cheung GY, Yeh AJ, Kretschmer D, Duong AC, Tuffuor K, Fu C-L, et al. Functional characteristics of the Staphylococcus aureus δ-toxin allelic variant G10S. Sci Rep 2015; 5: 18023.
39. Shin SC, Ahn IH, Ahn DH, Lee YM, Lee J, Lee JH, et al. Characterization of two antimicrobial peptides from antarctic fishes (Notothenia coriiceps and Parachaenichthys charcoti). PLoS One 2017; 12(1): e0170821.
40. Wang K, Yan J, Dang W, Xie J, Yan B, Yan W, et al. Dual antifungal properties of cationic antimicrobial peptides polybia-MPI: membrane integrity disruption and inhibition of biofilm formation. Peptides 2014; 56: 22-29.
41. Kościuczuk EM, Lisowski P, Jarczak J, Strzałkowska N, Jóźwik A, Horbańczuk J, et al. Cathelicidins: family of antimicrobial peptides. A review. Mol Biol Rep 2012; 39: 10957-10970.
42. Burrows LL, Stark M, Chan C, Glukhov E, Sinnadurai S, Deber CM. Activity of novel non-amphipathic cationic antimicrobial peptides against Candida species. J Antimicrob Chemother 2006; 57: 899-907.
43. Benincasa M, Scocchi M, Pacor S, Tossi A, Nobili D, Basaglia G, et al. Fungicidal activity of five cathelicidin peptides against clinically isolated yeasts. J Antimicrob Chemother 2006; 58: 950-959.
44. Strandberg E, Tiltak D, Ieronimo M, Kanithasen N, Wadhwani P, Ulrich AS. Influence of C-terminal amidation on the antimicrobial and hemolytic activities of cationic α-helical peptides. Pure Appl Chem 2007; 79: 717-728.
45. Dini I, De Biasi MG, Mancusi A. An overview of the potentialities of antimicrobial peptides derived from natural sources. Antibiotics (Basel) 2022; 11: 1483.
2. Köhler JR, Hube B, Puccia R, Casadevall A, Perfect JR. Fungi that infect humans. Microbiol Spectr 2017; 5: 10.1128/microbiolspec.FUNK-0014-2016.
3. Köhler JR, Casadevall A, Perfect J. The spectrum of fungi that infects humans. Cold Spring Harb Perspect Med 2014; 5: a019273.
4. Akeme Yamamoto AC, de Paula CR, Dias LB, Tadano T, Martins ÉR, Amadio JV, et al. Epidemiological and clinical characteristics of nosocomial candidiasis in university hospitals in Cuiabá–Mato Grosso, Brazil. Rev Iberoam Micol 2012; 29: 164-168.
5. McCarty TP, Pappas PG. Invasive candidiasis. Infect Dis Clin North Am 2016; 30: 103-124.
6. Vallabhaneni S, Kallen A, Tsay S, Chow N, Welsh R, Kerins J, et al. Investigation of the first seven reported cases of Candida auris, a globally emerging invasive, multidrug-resistant fungus—United States, May 2013–August 2016. MMWR Morb Mortal Wkly Rep 2016; 65: 1234-1237.
7. Piispanen AE, Hogan DA. PEPped up: induction of Candida albicans virulence by bacterial cell wall fragments. Cell Host Microbe 2008; 4: 1-2.
8. Shao L-C, Sheng C-Q, Zhang W-N. Recent advances in the study of antifungal lead compounds with new chemical scaffolds. Yao Xue Xue Bao 2007; 42: 1129-1136.
9. Negri M, Martins M, Henriques M, Svidzinski TI, Azeredo J, Oliveira R. Examination of potential virulence factors of Candida tropicalis clinical isolates from hospitalized patients. Mycopathologia 2010; 169: 175-182.
10. Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 2004; 39: 309-317.
11. Kullberg BJ, Arendrup MC. Invasive candidiasis. N Engl J Med 2015; 373: 1445-1456.
12. Brandt ME, Lockhart SR. Recent taxonomic developments with Candida and other opportunistic yeasts. Curr Fungal Infect Rep 2012; 6: 170-177.
13. Colombo AL, Nucci M, Park BJ, Nouér SA, Arthington-Skaggs B, da Matta DA, et al. Epidemiology of candidemia in Brazil: a nationwide sentinel surveillance of candidemia in eleven medical centers. J Clin Microbiol 2006; 44: 2816-2823.
14. Pfaller MA, Diekema D, Group IFSP. Twelve years of fluconazole in clinical practice: global trends in species distribution and fluconazole susceptibility of bloodstream isolates of Candida. Clin Microbiol Infect 2004; 10 Suppl 1: 11-23.
15. Rodrigues CF, Silva S, Henriques M. Candida glabrata: a review of its features and resistance. Eur J Clin Microbiol Infect Dis 2014; 33: 673-688.
16. Wiederhold NP. Antifungal resistance: current trends and future strategies to combat. Infect Drug Resist 2017; 10: 249-259.
17. Choi MJ, Won EJ, Shin JH, Kim SH, Lee W-G, Kim M-N, et al. Resistance mechanisms and clinical features of fluconazole-nonsusceptible Candida tropicalis isolates compared with fluconazole-less-susceptible isolates. Antimicrob Agents Chemother 2016; 60: 3653-3661.
18. Seneviratne CJ, Rajan S, Wong SS, Tsang DN, Lai CK, Samaranayake LP, et al. Antifungal susceptibility in serum and virulence determinants of candida bloodstream isolates from Hong Kong. Front Microbiol 2016; 7: 216.
19. Pfaller MA, Diekema DJ, Gibbs DL, Newell VA, Ellis D, Tullio V, et al. Results from the ARTEMIS DISK Global Antifungal Surveillance Study, 1997 to 2007: a 10.5-year analysis of susceptibilities of Candida Species to fluconazole and voriconazole as determined by CLSI standardized disk diffusion. J Clin Microbiol 2010; 48: 1366-1377.
20. Healey KR, Perlin DS. Fungal resistance to echinocandins and the MDR phenomenon in Candida glabrata. J Fungi (Basel) 2018; 4: 105.
21. Cheng J-W, Yu S-Y, Xiao M, Wang H, Kudinha T, Kong F, et al. Identification and antifungal susceptibility profile of Candida guilliermondii and Candida fermentati from a multicenter study in China. J Clin Microbiol 2016; 54: 2187-2189.
22. Mohammadi M, Taheri B, Momenzadeh N, Salarinia R, Nabipour I, Farshadzadeh Z, et al. Identification and characterization of novel antimicrobial peptide from hippocampus comes by In Silico and experimental studies. Mar Biotechnol (NY) 2018; 20: 718-728.
23. McMillan KAM, Coombs MRP. Investigating potential applications of the fish anti-microbial peptide pleurocidin: a systematic review. Pharmaceuticals (Basel) 2021; 14: 687.
24. Del Gaudio G, Lombardi L, Maisetta G, Esin S, Batoni G, Sanguinetti M, et al. Antifungal activity of the noncytotoxic human peptide hepcidin 20 against fluconazole-resistant Candida glabrata in human vaginal fluid. Antimicrob Agents Chemother 2013; 57: 4314-4321.
25. Gerdol M, Puillandre N, De Moro G, Guarnaccia C, Lucafò M, Benincasa M, et al. Identification and characterization of a novel family of cysteine-rich peptides (MgCRP-I) from Mytilus galloprovincialis. Genome Biol Evol 2015; 7: 2203-2219.
26. Silphaduang U, Noga EJ. Peptide antibiotics in mast cells of fish. Nature 2001; 414: 268-269.
27. Taheri B, Mohammadi M, Nabipour I, Momenzadeh N, Roozbehani M. Identification of novel antimicrobial peptide from Asian sea bass (Lates calcarifer) by in silico and activity characterization. PLoS One 2018; 13(10): e0206578.
28. Lauth X, Shike H, Burns JC, Westerman ME, Ostland VE, Carlberg JM, et al. Discovery and characterization of two isoforms of moronecidin, a novel antimicrobial peptide from hybrid striped bass. J Biol Chem 2002; 277: 5030-5039.
29. Houyvet B, Bouchon-Navaro Y, Bouchon C, Goux D, Bernay B, Corre E, et al. Identification of a moronecidin-like antimicrobial peptide in the venomous fish Pterois volitans: Functional and structural study of pteroicidin-α. Fish Shellfish Immunol 2018; 72: 318-324.
30. Wu Y, Zhang G, Zhou M. Inhibitory and anti‐inflammatory effects of two antimicrobial peptides moronecidin and temporin‐1Dra against Propionibacterium acnes in vitro and in vivo. J Pept Sci 2020; 26(7): e3255.
31. Wayne P. Clinical and Laboratory Standards Institute. Reference method for broth dilution antifungal susceptibility testing of filamentous fungi. CLSI Document M38-A2. Clinical and Laboratory Standards Institute, 2008.
32. Wayne P. Reference method for broth dilution antifungal susceptibility testing of yeasts, approved standard. CLSI document M27-A2. 2002.
33. Santos ERd, Forno CFD, Hernandez MG, Kubiça TF, Venturini TP, Chassot F, et al. Susceptibility of Candida spp. isolated from blood cultures as evaluated using the M27-A3 and new M27-S4 approved breakpoints. Rev Inst Med Trop Sao Paulo 2014; 56: 477-482.
34. Fernández de Ullivarri M, Arbulu S, Garcia-Gutierrez E, Cotter PD. Antifungal peptides as therapeutic agents. Front Cell Infect Microbiol 2020; 10: 105.
35. Ostrosky-Zeichner L, Bazemore S, Paetznick VL, Rodriguez JR, Chen E, Wallace T, et al. Differential antifungal activity of isomeric forms of nystatin. Antimicrob Agents Chemother 2001; 45: 2781-2786.
36. Kebede B, Shibeshi W. In vitro antibacterial and antifungal activities of extracts and fractions of leaves of Ricinus communis Linn against selected pathogens. Vet Med Sci 2022; 8: 1802-1815.
37. Stark M, Liu L-P, Deber CM. Cationic hydrophobic peptides with antimicrobial activity. Antimicrob Agents Chemother 2002; 46: 3585-3590.
38. Cheung GY, Yeh AJ, Kretschmer D, Duong AC, Tuffuor K, Fu C-L, et al. Functional characteristics of the Staphylococcus aureus δ-toxin allelic variant G10S. Sci Rep 2015; 5: 18023.
39. Shin SC, Ahn IH, Ahn DH, Lee YM, Lee J, Lee JH, et al. Characterization of two antimicrobial peptides from antarctic fishes (Notothenia coriiceps and Parachaenichthys charcoti). PLoS One 2017; 12(1): e0170821.
40. Wang K, Yan J, Dang W, Xie J, Yan B, Yan W, et al. Dual antifungal properties of cationic antimicrobial peptides polybia-MPI: membrane integrity disruption and inhibition of biofilm formation. Peptides 2014; 56: 22-29.
41. Kościuczuk EM, Lisowski P, Jarczak J, Strzałkowska N, Jóźwik A, Horbańczuk J, et al. Cathelicidins: family of antimicrobial peptides. A review. Mol Biol Rep 2012; 39: 10957-10970.
42. Burrows LL, Stark M, Chan C, Glukhov E, Sinnadurai S, Deber CM. Activity of novel non-amphipathic cationic antimicrobial peptides against Candida species. J Antimicrob Chemother 2006; 57: 899-907.
43. Benincasa M, Scocchi M, Pacor S, Tossi A, Nobili D, Basaglia G, et al. Fungicidal activity of five cathelicidin peptides against clinically isolated yeasts. J Antimicrob Chemother 2006; 58: 950-959.
44. Strandberg E, Tiltak D, Ieronimo M, Kanithasen N, Wadhwani P, Ulrich AS. Influence of C-terminal amidation on the antimicrobial and hemolytic activities of cationic α-helical peptides. Pure Appl Chem 2007; 79: 717-728.
45. Dini I, De Biasi MG, Mancusi A. An overview of the potentialities of antimicrobial peptides derived from natural sources. Antibiotics (Basel) 2022; 11: 1483.
| Files | ||
| Issue | Vol 15 No 3 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v15i3.12907 | |
| Keywords | ||
| In vitro; Fungi; Antimicrobial peptides; Cytotoxicity | ||
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How to Cite
1.
Amirrajab N, Ayatollahi Mousavi SA, Taheri B, Salari S, Ahmadi Sarsahra NA. In vitro antifungal potency of the moronecidin-like peptide against Candida albicans, Candida glabrata, and Candida tropicalis. Iran J Microbiol. 2023;15(3):456-461.
