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Current Pharmaceutical Biotechnology

Author(s): Houda Haddad, Klinger Antonio da Franca Rodrigues, Houcemeddine Othman, Leiz Maria Costa Veras, Raiza Raianne Luz Rodrigues, Ines Ouahchi, Bouraoui Ouni and Amira Zaϊri*

DOI: 10.2174/0113892010296038240427050421

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In vitro Antileishmanial Activity and In silico Molecular Modeling Studies of Novel Analogs of Dermaseptins S4 and B2

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Abstract

Background: Leishmaniasis is responsible for approximately 65,000 annual deaths. Various Leishmania species are the predominant cause of visceral, cutaneous, or mucocutaneous leishmaniasis, affecting millions worldwide. The lack of a vaccine, emergence of resistance, and undesirable side effects caused by antileishmanial medications have prompted researchers to look for novel therapeutic approaches to treat this disease. Antimicrobial peptides (AMPs) offer an alternative for promoting the discovery of new drugs.

Methods: In this study, we detail the synthesis process and investigate the antileishmanial activity against Leishmania (Viannia) braziliensis for peptides belonging to the dermaseptin (DS) family and their synthetic analogs. The MTT assay was performed to investigate the cytotoxicity of these peptides on the murine macrophage cell line RAW 264.7. Subsequently, we performed molecular modeling analysis to explore the structure-function correlation of the derivatives interacting with the parasitic membrane.

Results: All examined derivatives displayed concentration-dependent antileishmanial effect at low concentrations. Their effectiveness varied according to the peptide's proprieties. Notably, peptides with higher levels of charge demonstrated the most pronounced activities. Cytotoxicity assays showed that all the tested peptides were not cytotoxic compared to the tested conventional drug. The structure-function relationships demonstrated that the charged N-terminus could be responsible for the antileishmanial effect observed on promastigotes.

Conclusion: Collectively, these results propose that dermaseptins (DS) might offer potential as promising candidates for the development of effective antileishmanial therapies.

Keywords: Dermaseptin B2, dermaseptin S4, analogs, Leishmania (Viannia) braziliensis, antileishmanial activity, promastigotes.

Graphical Abstract

[1]
WHO Leishmaniosis 2019. Available from: http://www.who.int/leishmaniasis/en/ (accessed on 01 November 2023).
[2]
Leishmaniasis, W.H.O. WHO Leishmaniosis., 2017. Available from: https://www.who.int/data/gho/data/themes/topics/gho-ntd-leishmaniasis/ (accessed on 23 November 2023).
[3]
Neri, F.S.M.; Júnior, D.B.C.; Froes, T.Q.; da Silva, P.B.G.; do Egito, M.S.; Moreira, P.O.L.; de Pilla Varotti, F.; Castilho, M.S.; Teixeira-Neto, R.G.; de Albuquerque, J.F.C.; Leite, F.H.A. Antileishmanial activity evaluation of thiazolidine-2,4-dione against Leishmania infantum and Leishmania braziliensis. Parasitol. Res., 2020, 119(7), 2263-2274.
[http://dx.doi.org/10.1007/s00436-020-06706-3] [PMID: 32462293]
[4]
Badirzadeh, A.; Heidari-Kharaji, M.; Fallah-Omrani, V.; Dabiri, H.; Araghi, A.; Salimi Chirani, A. Antileishmanial activity of Urtica dioica extract against zoonotic cutaneous leishmaniasis. PLoS Negl. Trop. Dis., 2020, 14(1), e0007843.
[http://dx.doi.org/10.1371/journal.pntd.0007843] [PMID: 31929528]
[5]
Fernando, C. Leishmaniasis. Imported Infectious Diseases; Woodhead; Publishing, 2014, pp. 227-242.
[http://dx.doi.org/10.1533/9781908818737.227]
[6]
Frézard, F.; Demicheli, C.; Ribeiro, R. Pentavalent antimonials: New perspectives for old drugs. Molecules, 2009, 14(7), 2317-2336.
[http://dx.doi.org/10.3390/molecules14072317] [PMID: 19633606]
[7]
Sunyoto, T.; Potet, J.; Boelaert, M. Why miltefosine—a life-saving drug for leishmaniasis—is unavailable to people who need it the most. BMJ Glob. Health, 2018, 3(3), e000709.
[http://dx.doi.org/10.1136/bmjgh-2018-000709] [PMID: 29736277]
[8]
Roatt, B.M.; de Oliveira Cardoso, J.M.; De Brito, R.C.F.; Coura-Vital, W.; de Oliveira Aguiar-Soares, R.D.; Reis, A.B. Recent advances and new strategies on leishmaniasis treatment. Appl. Microbiol. Biotechnol., 2020, 104(21), 8965-8977.
[http://dx.doi.org/10.1007/s00253-020-10856-w] [PMID: 32875362]
[9]
Madusanka, R.K.; Silva, H.; Karunaweera, N.D. Treatment of cutaneous leishmaniasis and insights into species-specific responses: A narrative review. Infect. Dis. Ther., 2022, 11(2), 695-711.
[http://dx.doi.org/10.1007/s40121-022-00602-2] [PMID: 35192172]
[10]
Bahar, A.; Ren, D. Antimicrobial peptides. Pharmaceuticals, 2013, 6(12), 1543-1575.
[http://dx.doi.org/10.3390/ph6121543] [PMID: 24287494]
[11]
Mwangi, J.; Hao, X.; Lai, R.; Zhang, Z.Y. Antimicrobial peptides: New hope in the war against multidrug resistance. Zool. Res., 2019, 40(6), 488-505.
[http://dx.doi.org/10.24272/j.issn.2095-8137.2019.062] [PMID: 31592585]
[12]
El-Dirany, R.; Shahrour, H.; Dirany, Z.; Abdel-Sater, F.; Gonzalez-Gaitano, G.; Brandenburg, K.; Martinez de Tejada, G.; Nguewa, P.A. Activity of anti-microbial peptides (AMPs) against Leishmania and other parasites: An overview. Biomolecules, 2021, 11(7), 984.
[http://dx.doi.org/10.3390/biom11070984] [PMID: 34356608]
[13]
Mor, A.; Delfour, A.; Migliore-Samour, D.; Nicolas, P.; Nicolas, P. Isolation, amino acid sequence and synthesis of dermaseptin, a novel antimicrobial peptide of amphibian skin. Biochemistry, 1991, 30(36), 8824-8830.
[http://dx.doi.org/10.1021/bi00100a014] [PMID: 1909573]
[14]
Amiche, M.; Ladram, A.; Nicolas, P. A consistent nomenclature of antimicrobial peptides isolated from frogs of the subfamily Phyllomedusinae. Peptides, 2008, 29(11), 2074-2082.
[http://dx.doi.org/10.1016/j.peptides.2008.06.017] [PMID: 18644413]
[15]
Nicolas, P.; El Amri, C. The dermaseptin superfamily: A gene-based combinatorial library of antimicrobial peptides. Biochim. Biophys. Acta Biomembr., 2009, 1788(8), 1537-1550.
[http://dx.doi.org/10.1016/j.bbamem.2008.09.006] [PMID: 18929530]
[16]
Shai, Y. Mode of action of membrane active antimicrobial peptides. Biopolymers, 2002, 66(4), 236-248.
[http://dx.doi.org/10.1002/bip.10260] [PMID: 12491537]
[17]
Feder, R.; Dagan, A.; Mor, A. Structure-activity relationship study of antimicrobial dermaseptin S4 showing the consequences of peptide oligomerization on selective cytotoxicity. J. Biol. Chem., 2000, 275(6), 4230-4238.
[http://dx.doi.org/10.1074/jbc.275.6.4230] [PMID: 10660589]
[18]
Efron, L.; Dagan, A.; Gaidukov, L.; Ginsburg, H.; Mor, A. Direct interaction of dermaseptin S4 aminoheptanoyl derivative with intraerythrocytic malaria parasite leading to increased specific antiparasitic activity in culture. J. Biol. Chem., 2002, 277(27), 24067-24072.
[http://dx.doi.org/10.1074/jbc.M202089200] [PMID: 11937508]
[19]
Daly, J.W.; Caceres, J.; Moni, R.W.; Gusovsky, F.; Moos, M., Jr; Seamon, K.B.; Milton, K.; Myers, C.W. Frog secretions and hunting magic in the upper Amazon: Identification of a peptide that interacts with an adenosine receptor. Proc. Natl. Acad. Sci. USA, 1992, 89(22), 10960-10963.
[http://dx.doi.org/10.1073/pnas.89.22.10960] [PMID: 1438301]
[20]
van Zoggel, H.; Carpentier, G.; Dos Santos, C.; Hamma-Kourbali, Y.; Courty, J.; Amiche, M.; Delbé, J. Antitumor and angiostatic activities of the antimicrobial peptide dermaseptin B2. PLoS One, 2012, 7(9), e44351.
[http://dx.doi.org/10.1371/journal.pone.0044351] [PMID: 23028527]
[21]
Mor, A.; Amiche, M.; Nicolas, P. Structure, synthesis, and activity of Dermaseptin b, a novel vertebrate defensive peptide from frog skin: Relationship with adenoregulin. Biochemistry, 1994, 33(21), 6642-6650.
[http://dx.doi.org/10.1021/bi00187a034] [PMID: 8204601]
[22]
Kückelhaus, C.S.; Kückelhaus, S.A.S.; Tosta, C.E.; Muniz-Junqueira, M.I. Pravastatin modulates macrophage functions of Leishmania (L.) amazonensis-infected BALB/c mice. Exp. Parasitol., 2013, 134(1), 18-25.
[http://dx.doi.org/10.1016/j.exppara.2013.01.020] [PMID: 23402845]
[23]
Abdille, A.A.; Kimani, J.; Wamunyokoli, F.; Bulimo, W.; Gavamukulya, Y.; Maina, E.N. Dermaseptin B2’s anti-proliferative activity and down regulation of anti-proliferative, angiogenic and metastatic genes in rhabdomyosarcoma RD cells in vitro. Adv. Biosci. Biotechnol., 2021, 12(10), 337-359.
[http://dx.doi.org/10.4236/abb.2021.1210022]
[24]
Antimicrobial peptide databases. 2016. Available from: http://aps.unmc.edu/AP/ (accessed on 03 July 2023).
[25]
Charpentier, S.; Amiche, M.; Mester, J.; Vouille, V.; Le Caer, J.P.; Nicolas, P.; Delfour, A. Structure, synthesis, and molecular cloning of dermaseptins B, a family of skin peptide antibiotics. J. Biol. Chem., 1998, 273(24), 14690-14697.
[http://dx.doi.org/10.1074/jbc.273.24.14690]
[26]
Auvynet, C.; El Amri, C.; Lacombe, C.; Bruston, F.; Bourdais, J.; Nicolas, P.; Rosenstein, Y. Structural requirements for antimicrobial versus chemoattractant activities for dermaseptin S9. FEBS J., 2008, 275(16), 4134-4151.
[http://dx.doi.org/10.1111/j.1742-4658.2008.06554.x] [PMID: 18637027]
[27]
Gautier, R.; Douguet, D.; Antonny, B.; Drin, G. HELIQUEST: A web server to screen sequences with specific α-helical properties. Bioinformatics, 2008, 24(18), 2101-2102.
[http://dx.doi.org/10.1093/bioinformatics/btn392] [PMID: 18662927]
[28]
Fernández-Escamilla, A.M.; Rousseau, F.; Schymkowitz, J.; Serrano, L. Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins. Nat. Biotechnol., 2004, 22(10), 1302-1306.
[http://dx.doi.org/10.1038/nbt1012] [PMID: 15361882]
[29]
Muñoz, V.; Serrano, L. Elucidating the folding problem of helical peptides using empirical parameters. Nat. Struct. Mol. Biol., 1994, 1(6), 399-409.
[http://dx.doi.org/10.1038/nsb0694-399] [PMID: 7664054]
[30]
Rodrigues, K.A.F.; Amorim, L.V.; Dias, C.N.; Moraes, D.F.C.; Carneiro, S.M.P.; Carvalho, F.A.A. Syzygium cumini (L.) Skeels essential oil and its major constituent α-pinene exhibit anti-Leishmania activity through immunomodulation in vitro. J. Ethnopharmacol., 2015, 160, 32-40.
[http://dx.doi.org/10.1016/j.jep.2014.11.024] [PMID: 25460590]
[31]
Lamiable, A.; Thévenet, P.; Rey, J.; Vavrusa, M.; Derreumaux, P.; Tufféry, P. PEP-FOLD3: Faster de novo structure prediction for linear peptides in solution and in complex. Nucleic Acids Res., 2016, 44(W1), W449-W454.
[http://dx.doi.org/10.1093/nar/gkw329] [PMID: 27131374]
[32]
Du, Z.; Su, H.; Wang, W.; Ye, L.; Wei, H.; Peng, Z.; Anishchenko, I.; Baker, D.; Yang, J. The trRosetta server for fast and accurate protein structure prediction. Nat. Protoc., 2021, 16(12), 5634-5651.
[http://dx.doi.org/10.1038/s41596-021-00628-9] [PMID: 34759384]
[33]
Jurrus, E.; Engel, D.; Star, K.; Monson, K.; Brandi, J.; Felberg, L.E.; Brookes, D.H.; Wilson, L.; Chen, J.; Liles, K.; Chun, M.; Li, P.; Gohara, D.W.; Dolinsky, T.; Konecny, R.; Koes, D.R.; Nielsen, J.E.; Head-Gordon, T.; Geng, W.; Krasny, R.; Wei, G.W.; Holst, M.J.; McCammon, J.A.; Baker, N.A. Improvements to the APBS biomolecular solvation software suite. Protein Sci., 2018, 27(1), 112-128.
[http://dx.doi.org/10.1002/pro.3280] [PMID: 28836357]
[34]
Kustanovich, I.; Shalev, D.E.; Mikhlin, M.; Gaidukov, L.; Mor, A. Structural requirements for potent versus selective cytotoxicity for antimicrobial dermaseptin S4 derivatives. J. Biol. Chem., 2002, 277(19), 16941-16951.
[http://dx.doi.org/10.1074/jbc.M111071200] [PMID: 11847217]
[35]
Ong, Z.Y.; Wiradharma, N.; Yang, Y.Y. Strategies employed in the design and optimization of synthetic antimicrobial peptide amphiphiles with enhanced therapeutic potentials. Adv. Drug Deliv. Rev., 2014, 78, 28-45.
[http://dx.doi.org/10.1016/j.addr.2014.10.013] [PMID: 25453271]
[36]
Ma, Z.; Wei, D.; Yan, P.; Zhu, X.; Shan, A.; Bi, Z. Characterization of cell selectivity, physiological stability and endotoxin neutralization capabilities of α-helix-based peptide amphiphiles. Biomaterials, 2015, 52, 517-530.
[http://dx.doi.org/10.1016/j.biomaterials.2015.02.063] [PMID: 25818457]
[37]
Lyu, Y.; Yang, Y.; Lyu, X.; Dong, N.; Shan, A. Antimicrobial activity, improved cell selectivity and mode of action of short PMAP-36-derived peptides against bacteria and Candida. Sci. Rep., 2016, 6(1), 27258.
[http://dx.doi.org/10.1038/srep27258] [PMID: 27251456]
[38]
Dong, N.; Zhu, X.; Chou, S.; Shan, A.; Li, W.; Jiang, J. Antimicrobial potency and selectivity of simplified symmetric-end peptides. Biomaterials, 2014, 35(27), 8028-8039.
[http://dx.doi.org/10.1016/j.biomaterials.2014.06.005] [PMID: 24952979]
[39]
Irazazabal, L.N.; Porto, W.F.; Ribeiro, S.M.; Casale, S.; Humblot, V.; Ladram, A.; Franco, O.L. Selective amino acid substitution reduces cytotoxicity of the antimicrobial peptide mastoparan. Biochim. Biophys. Acta Biomembr., 2016, 1858(11), 2699-2708.
[http://dx.doi.org/10.1016/j.bbamem.2016.07.001] [PMID: 27423268]
[40]
Navon-Venezia, S.; Feder, R.; Gaidukov, L.; Carmeli, Y.; Mor, A. Antibacterial properties of dermaseptin S4 derivatives with in vivo activity. Antimicrob. Agents Chemother., 2002, 46(3), 689-694.
[http://dx.doi.org/10.1128/AAC.46.3.689-694.2002] [PMID: 11850249]
[41]
Krugliak, M.; Feder, R.; Zolotarev, V.Y.; Gaidukov, L.; Dagan, A.; Ginsburg, H.; Mor, A. Antimalarial activities of dermaseptin S4 derivatives. Antimicrob. Agents Chemother., 2000, 44(9), 2442-2451.
[http://dx.doi.org/10.1128/AAC.44.9.2442-2451.2000] [PMID: 10952593]
[42]
Galanth, C.; Abbassi, F.; Lequin, O.; Ayala-Sanmartin, J.; Ladram, A.; Nicolas, P.; Amiche, M. Mechanism of antibacterial action of dermaseptin B2: Interplay between helix-hinge-helix structure and membrane curvature strain. Biochemistry, 2009, 48(2), 313-327.
[http://dx.doi.org/10.1021/bi802025a] [PMID: 19113844]
[43]
Hazime, N.; Belguesmia, Y.; Barras, A.; Amiche, M.; Boukherroub, R.; Drider, D. Enhanced antibacterial activity of dermaseptin through its immobilization on alginate nanoparticles—effects of menthol and lactic acid on its potentialization. Antibiotics, 2022, 11(6), 787.
[http://dx.doi.org/10.3390/antibiotics11060787] [PMID: 35740193]
[44]
Walter, R.; Neidle, A.; Marks, N. Significant differences in the degradation of pro-leu-gly-nH2 by human serum and that of other species (38484). Exp. Biol. Med., 1975, 148(1), 98-103.
[http://dx.doi.org/10.3181/00379727-148-38484] [PMID: 1168915]
[45]
Hong, S.Y.; Oh, J.E.; Lee, K.H. Effect of d-amino acid substitution on the stability, the secondary structure, and the activity of membrane-active peptide. Biochem. Pharmacol., 1999, 58(11), 1775-1780.
[http://dx.doi.org/10.1016/S0006-2952(99)00259-2] [PMID: 10571252]
[46]
Braunstein, A.; Papo, N.; Shai, Y. In vitro activity and potency of an intravenously injected antimicrobial peptide and its DL amino acid analog in mice infected with bacteria. Antimicrob. Agents Chemother., 2004, 48(8), 3127-3129.
[http://dx.doi.org/10.1128/AAC.48.8.3127-3129.2004] [PMID: 15273131]
[47]
Zhao, Y.; Zhang, M.; Qiu, S.; Wang, J.; Peng, J.; Zhao, P.; Zhu, R.; Wang, H.; Li, Y.; Wang, K.; Yan, W.; Wang, R. Antimicrobial activity and stability of the d-amino acid substituted derivatives of antimicrobial peptide polybia-MPI. AMB Express, 2016, 6(1), 122.
[http://dx.doi.org/10.1186/s13568-016-0295-8] [PMID: 27900727]
[48]
Vaezi, Z.; Bortolotti, A.; Luca, V.; Perilli, G.; Mangoni, M.L.; Khosravi-Far, R.; Bobone, S.; Stella, L. Aggregation determines the selectivity of membrane-active anticancer and antimicrobial peptides: The case of killerFLIP. Biochim. Biophys. Acta Biomembr., 2020, 1862(2), 183107.
[http://dx.doi.org/10.1016/j.bbamem.2019.183107] [PMID: 31678022]
[49]
Al Musaimi, O.; Valenzo, O.M.M.; Williams, D.R. Prediction of peptides retention behavior in reversed‐phase liquid chromatography based on their hydrophobicity. J. Sep. Sci., 2023, 46(2), 2200743.
[http://dx.doi.org/10.1002/jssc.202200743] [PMID: 36349538]
[50]
Eisenberg, D.; Weiss, R.M.; Terwilliger, T.C. The hydrophobic moment detects periodicity in protein hydrophobicity. Proc. Natl. Acad. Sci. USA, 1984, 81(1), 140-144.
[http://dx.doi.org/10.1073/pnas.81.1.140] [PMID: 6582470]
[51]
Eisenberg, D.; Weiss, R.M.; Terwilliger, T.C. The helical hydrophobic moment: A measure of the amphiphilicity of a helix. Nature, 1982, 299(5881), 371-374.
[http://dx.doi.org/10.1038/299371a0] [PMID: 7110359]
[52]
Dennison, S.R.; Phoenix, D.A. Influence of C-terminal amidation on the efficacy of modelin-5. Biochemistry, 2011, 50(9), 1514-1523.
[http://dx.doi.org/10.1021/bi101687t] [PMID: 21241054]
[53]
Sánchez-Acosta, Y.A.; Castillo Vargas, J.A.; Ramírez Quintero, K.J.; Orduz Peralta, S.; Camargo Rodríguez, D.O. Peptide derivatives of dermaseptin S4 in fresh bovine semen for bacterial contamination control: Physicochemical and structural characterization, antibacterial potency, and effects on red blood and sperm cells. Reprod. Domest. Anim., 2020, 55(8), 905-914.
[http://dx.doi.org/10.1111/rda.13701] [PMID: 32406577]
[54]
Bartels, E.J.H.; Dekker, D.; Amiche, M. Dermaseptins, multifunctional antimicrobial peptides: A review of their pharmacology, effectivity, mechanism of action, and possible future directions. Front. Pharmacol., 2019, 10, 1421.
[http://dx.doi.org/10.3389/fphar.2019.01421] [PMID: 31849670]
[55]
Zou, R.; Zhu, X.; Tu, Y.; Wu, J.; Landry, M.P. Activity of antimicrobial peptide aggregates decreases with increased cell membrane embedding free energy cost. Biochemistry, 2018, 57(18), 2606-2610.
[http://dx.doi.org/10.1021/acs.biochem.8b00052] [PMID: 29638118]
[56]
Torres, M.D.T.; Sothiselvam, S.; Lu, T.K.; de la Fuente-Nunez, C. Peptide design principles for antimicrobial applications. J. Mol. Biol., 2019, 431(18), 3547-3567.
[http://dx.doi.org/10.1016/j.jmb.2018.12.015] [PMID: 30611750]
[57]
Huang, Y.; He, L.; Li, G.; Zhai, N.; Jiang, H.; Chen, Y. Role of helicity of α-helical antimicrobial peptides to improve specificity. Protein Cell, 2014, 5(8), 631-642.
[http://dx.doi.org/10.1007/s13238-014-0061-0] [PMID: 24805306]
[58]
Zelezetsky, I.; Tossi, A. Alpha-helical antimicrobial peptides—Using a sequence template to guide structure–activity relationship studies. Biochim. Biophys. Acta Biomembr., 2006, 1758(9), 1436-1449.
[http://dx.doi.org/10.1016/j.bbamem.2006.03.021] [PMID: 16678118]
[59]
Bern, C.; Adler-Moore, J.; Berenguer, J.; Boelaert, M.; Boer, M.; Davidson, R.N.; Figueras, C.; Gradoni, L.; Kafetzis, D.A.; Ritmeijer, K.; Rosenthal, E.; Royce, C.; Russo, R.; Sundar, S.; Alvar, J. Liposomal amphotericin B for the treatment of visceral leishmaniasis. Clin. Infect. Dis., 2006, 43(7), 917-924.
[http://dx.doi.org/10.1086/507530] [PMID: 16941377]
[60]
Palma, E.; Pasqua, A.; Gagliardi, A.; Britti, D.; Fresta, M.; Cosco, D. Antileishmanial activity of amphotericin B-loaded-PLGA nanoparticles: An overview. Materials, 2018, 11(7), 1167.
[http://dx.doi.org/10.3390/ma11071167] [PMID: 29987206]
[61]
Williamson, P.; Schlegel, R.A. Back and forth. Mol. Membr. Biol., 1994, 11(4), 199-216.
[http://dx.doi.org/10.3109/09687689409160430] [PMID: 7711830]
[62]
Pinto, E.G.; Pimenta, D.C.; Antoniazzi, M.M.; Jared, C.; Tempone, A.G. Antimicrobial peptides isolated from Phyllomedusa nordestina (Amphibia) alter the permeability of plasma membrane of Leishmania and Trypanosoma cruzi. Exp. Parasitol., 2013, 135(4), 655-660.
[http://dx.doi.org/10.1016/j.exppara.2013.09.016] [PMID: 24113627]
[63]
Chaves, R.X.; Quelemes, P.V.; Leite, L.M.; Aquino, D.S.A.; Amorim, L.V.; Rodrigues, K.A.F.; Campelo, Y.D.M.; Veras, L.M.C.; Bemquerer, M.P.; Ramos-Jesus, J.; Arcanjo, D.D.R.; Carvalho, F.A.A.; Kückelhaus, S.A.S.; Leite, J.R.S.A. Antileishmanial and immunomodulatory effects of Dermaseptin-01, A promising peptide against leishmania amazonensis. Curr. Bioact. Compd., 2017, 13(4), 305-311.
[http://dx.doi.org/10.2174/1573407212666161014131415]
[64]
Belaid, A.; Braiek, A.; Alibi, S.; Hassen, W.; Beltifa, A.; Nefzi, A.; Mansour, H.B. Evaluating the effect of dermaseptin S4 and its derivatives on multidrug-resistant bacterial strains and on the colon cancer cell line SW620. Environ. Sci. Pollut. Res. Int., 2021, 28(30), 40908-40916.
[http://dx.doi.org/10.1007/s11356-021-13683-2] [PMID: 33774792]
[65]
Brand, G.; Santos, R.; Arake, L.; Silva, V.; Veras, L.; Costa, V.; Costa, C.; Kuckelhaus, S.; Alexandre, J.; Feio, M.; Leite, J. The skin secretion of the amphibian Phyllomedusa nordestina: A source of antimicrobial and antiprotozoal peptides. Molecules, 2013, 18(6), 7058-7070.
[http://dx.doi.org/10.3390/molecules18067058] [PMID: 23774944]
[66]
Sundar, S.; Singh, B. Emerging therapeutic targets for treatment of leishmaniasis. Expert Opin. Ther. Targets, 2018, 22(6), 467-486.
[http://dx.doi.org/10.1080/14728222.2018.1472241] [PMID: 29718739]
[67]
Pérez-Cordero, J.J.; Lozano, J.M.; Cortés, J.; Delgado, G. Leishmanicidal activity of synthetic antimicrobial peptides in an infection model with human dendritic cells. Peptides, 2011, 32(4), 683-690.
[http://dx.doi.org/10.1016/j.peptides.2011.01.011] [PMID: 21262294]
[68]
Dabirian, S.; Taslimi, Y.; Zahedifard, F.; Gholami, E.; Doustdari, F.; Motamedirad, M.; Khatami, S.; Azadmanesh, K.; Nylen, S.; Rafati, S. Human neutrophil peptide-1 (HNP-1): A new anti-leishmanial drug candidate. PLoS Negl. Trop. Dis., 2013, 7(10), e2491.
[http://dx.doi.org/10.1371/journal.pntd.0002491] [PMID: 24147170]
[69]
Pereira, A.V.; de Barros, G.; Pinto, E.G.; Tempone, A.G.; Orsi, R.O.; dos Santos, L.D.; Calvi, S.; Ferreira, R.S., Jr; Pimenta, D.C.; Barraviera, B. Melittin induces in vitro death of Leishmania (Leishmania) infantum by triggering the cellular innate immune response. J. Venom. Anim. Toxins Incl. Trop. Dis., 2016, 22(1), 1.
[http://dx.doi.org/10.1186/s40409-016-0055-x] [PMID: 26752985]
[70]
Katz, S.; Barbiéri, C.L.; Soler, F.P.M.; Soares, A.M.; Chavantes, M.C.; Zamuner, S.R. Effect of isolated proteins from crotalus durissus terrificus venom on Leishmania (Leishmania) amazonensis-infected macrophages. Protein Pept. Lett., 2020, 27(8), 718-724.
[http://dx.doi.org/10.2174/0929866527666200129152954] [PMID: 31994997]
[71]
Lequin, O.; Ladram, A.; Chabbert, L.; Bruston, F.; Convert, O.; Vanhoye, D.; Chassaing, G.; Nicolas, P.; Amiche, M. Dermaseptin S9, an alpha-helical antimicrobial peptide with a hydrophobic core and cationic termini. Biochemistry, 2006, 45(2), 468-480.
[http://dx.doi.org/10.1021/bi051711i] [PMID: 16401077]
[72]
Hernandez, C.; Mor, A.; Dagger, F.; Nicolas, P.; Hernandez, A.; Benedetti, E.L.; Dunia, I. Functional and structural damage in Leishmania mexicana exposed to the cationic peptide dermaseptin. Eur. J. Cell Biol., 1992, 59(2), 414-424.
[PMID: 1493807]
[73]
Gaidukov, L.; Fish, A.; Mor, A. Analysis of membrane-binding properties of dermaseptin analogues: Relationships between binding and cytotoxicity. Biochemistry, 2003, 42(44), 12866-12874.
[http://dx.doi.org/10.1021/bi034514x] [PMID: 14596600]
[74]
Savoia, D.; Guerrini, R.; Marzola, E.; Salvadori, S. Synthesis and antimicrobial activity of dermaseptin S1 analogues. Bioorg. Med. Chem., 2008, 16(17), 8205-8209.
[http://dx.doi.org/10.1016/j.bmc.2008.07.032] [PMID: 18676150]
[75]
Eaton, P.; Bittencourt, C.R.; Costa Silva, V.; Véras, L.M.C.; Costa, C.H.N.; Feio, M.J.; Leite, J.R.S.A. Anti-leishmanial activity of the antimicrobial peptide DRS 01 observed in Leishmania infantum (syn. Leishmania chagasi) cells. Nanomedicine , 2014, 10(2), 483-490.
[http://dx.doi.org/10.1016/j.nano.2013.09.003] [PMID: 24096030]
[76]
Yeaman, M.R.; Yount, N.Y. Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev., 2003, 55(1), 27-55.
[http://dx.doi.org/10.1124/pr.55.1.2] [PMID: 12615953]
[77]
Huang, H.W. Molecular mechanism of antimicrobial peptides: The origin of cooperativity. Biochim. Biophys. Acta Biomembr., 2006, 1758(9), 1292-1302.
[http://dx.doi.org/10.1016/j.bbamem.2006.02.001] [PMID: 16542637]
[78]
Routier, F.H.; Higson, A.P.; Ivanova, I.A.; Ross, A.J.; Tsvetkov, Y.E.; Yashunsky, D.V.; Bates, P.A.; Nikolaev, A.V.; Ferguson, M.A.J. Characterization of the elongating alpha-D-mannosyl phosphate transferase from three species of Leishmania using synthetic acceptor substrate analogues. Biochemistry, 2000, 39(27), 8017-8025.
[http://dx.doi.org/10.1021/bi000371s] [PMID: 10891083]
[79]
Mangoni, M.L.; Shai, Y. Short native antimicrobial peptides and engineered ultrashort lipopeptides: Similarities and differences in cell specificities and modes of action. Cell. Mol. Life Sci., 2011, 68(13), 2267-2280.
[http://dx.doi.org/10.1007/s00018-011-0718-2] [PMID: 21573781]
[80]
André, S.; Raja, Z.; Humblot, V.; Piesse, C.; Foulon, T.; Sereno, D.; Oury, B.; Ladram, A. Functional characterization of Temporin-SHe, a new broad-spectrum antibacterial and leishmanicidal temporin-SH paralog from the sahara frog (pelophylax saharicus). Int. J. Mol. Sci., 2020, 21(18), 6713.
[http://dx.doi.org/10.3390/ijms21186713] [PMID: 32933215]
[81]
Leroux, M.; Luquain-Costaz, C.; Lawton, P.; Azzouz-Maache, S.; Delton, I. Fatty acid composition and metabolism in Leishmania parasite species: Potential biomarkers or drug targets for leishmaniasis? Int. J. Mol. Sci., 2023, 24(5), 4702.
[http://dx.doi.org/10.3390/ijms24054702] [PMID: 36902138]
[82]
Waghu, F.H.; Barai, R.S.; Gurung, P.; Idicula-Thomas, S. CAMPR3: A database on sequences, structures and signatures of antimicrobial peptides: Table 1. Nucleic Acids Res., 2016, 44(D1), D1094-D1097.
[http://dx.doi.org/10.1093/nar/gkv1051] [PMID: 26467475]