Login Register Cart 0
Generic placeholder image

Current Topics in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1568-0266
ISSN (Online): 1873-4294

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Spotlight on the Selected New Antimicrobial Innate Immune Peptides Discovered During 2015-2019

Author(s): Xiangli Dang and Guangshun Wang*

Volume 20, Issue 32, 2020

Page: [2984 - 2998] Pages: 15

DOI: 10.2174/1568026620666201022143625

Price: $65

Abstract

Background: Antibiotic resistance is a global issue and new anti-microbials are required.

Introduction: Anti-microbial peptides are important players of host innate immune systems that prevent infections. Due to their ability to eliminate drug-resistant pathogens, AMPs are promising candidates for developing the next generation of anti-microbials.

Methods: The anti-microbial peptide database provides a useful tool for searching, predicting, and designing new AMPs. In the period from 2015-2019, ~500 new natural peptides have been registered.

Results: This article highlights a selected set of new AMP members with interesting properties. Teixobactin is a cell wall inhibiting peptide antibiotic, while darobactin inhibits a chaperone and translocator for outer membrane proteins. Remarkably, cOB1, a sex pheromone from commensal enterococci, restricts the growth of multidrug-resistant Enterococcus faecalis in the gut at a picomolar concentration. A novel proline-rich AMP has been found in the plant Brassica napus. A shrimp peptide MjPen- II comprises three different sequence domains: serine-rich, proline-rich, and cysteine-rich regions. Surprisingly, an amphibian peptide urumin specifically inhibits H1 hemagglutinin-bearing influenza A virus. Defensins are abundant and typically consist of three pairs of intramolecular disulfide bonds. However, rat rattusin dimerizes via forming five pairs of intermolecular disulfide bonds. While human LL-37 can be induced by vitamin D, vitamin A induces the expression of resistin-like molecule alpha (RELMα) in mice. The isolation and characterization of an alternative human cathelicidin peptide, TLN-58, substantiates the concept of one gene multiple peptides. The involvement of a fly AMP nemuri in sleep induction may promote the research on the relationship between sleep and infection control.

Conclusion: The functional roles of AMPs continue to grow and the general term “innate immune peptides” becomes useful. These discoveries widen our view on the anti-microbial peptides and may open new opportunities for developing novel peptide therapeutics for different applications.

Keywords: Anti-microbial peptide, Classification, New structure, Pheromone with picomolar antibacterial activity, Sleep and immunity, Vitamin.

« Previous Next »
Graphical Abstract

[1]
Peschel, A.; Sahl, H.G. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat. Rev. Microbiol., 2006, 4(7), 529-536.
[http://dx.doi.org/10.1038/nrmicro1441] [PMID: 16778838]
[2]
Mishra, B.; Lakshmaiah Narayana, J.; Lushnikova, T.; Wang, X.; Wang, G. Low cationicity is important for systemic in vivo efficacy of database-derived peptides against drug-resistant Gram-positive pathogens. Proc. Natl. Acad. Sci. USA, 2019, 116(27), 13517-13522.
[http://dx.doi.org/10.1073/pnas.1821410116] [PMID: 31209048]
[3]
Wang, Z.; Wang, G. APD: The antimicrobial peptide database. Nucleic Acids Res., 2004, 32(Database issue), D590-D592.
[http://dx.doi.org/10.1093/nar/gkh025] [PMID: 14681488]
[4]
Wang, G.; Li, X.; Wang, Z. APD3: the antimicrobial peptide database as a tool for research and education. Nucleic Acids Res., 2016, 44(D1), D1087-D1093.
[http://dx.doi.org/10.1093/nar/gkv1278] [PMID: 26602694]
[5]
Koehbach, J.; Craik, D.J. The vast structural diversity of antimicrobial peptides. Trends Pharmacol. Sci., 2019, 40(7), 517-528.
[http://dx.doi.org/10.1016/j.tips.2019.04.012] [PMID: 31230616]
[6]
Yasir, M.; Dutta, D.; Willcox, M.D.P. Mode of action of the antimicrobial peptide Mel4 is independent of Staphylococcus aureus cell membrane permeability. PLoS One, 2019, 14(7)e0215703
[http://dx.doi.org/10.1371/journal.pone.0215703] [PMID: 31356627]
[7]
Hancock, R.E.; Sahl, H.G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol., 2006, 24(12), 1551-1557.
[http://dx.doi.org/10.1038/nbt1267] [PMID: 17160061]
[8]
Wang, G.; Mishra, B.; Lau, K.; Lushnikova, T.; Golla, R.; Wang, X. Antimicrobial peptides in 2014. Pharmaceuticals, 2015, 8(1), 123-150.
[http://dx.doi.org/10.3390/ph8010123] [PMID: 25806720]
[9]
Wang, G. The antimicrobial peptide database provides a platform for decoding the design principles of naturally occurring antimicrobial peptides. Protein Sci., 2020, 29(1), 8-18.
[http://dx.doi.org/10.1002/pro.3702] [PMID: 31361941]
[10]
Rončević, T.; Puizina, J.; Tossi, A. Antimicrobial peptides as anti-infective agents in pre-post-antibiotic era? Int. J. Mol. Sci., 2019, 20(22), 5713.
[http://dx.doi.org/10.3390/ijms20225713] [PMID: 31739573]
[11]
Wang, G. Discovery, classification and functional diversity of antimicrobial peptides.Antimicrobial peptides: discovery, design and novel therapeutic strategies, 2nd ed; Wang, G., Ed.; CABI: Wallingford, UK, 2017, pp. 1-19.
[http://dx.doi.org/10.1079/9781786390394.0001]
[12]
Boman, H.G. Antibacterial peptides: basic facts and emerging concepts. J. Intern. Med., 2003, 254(3), 197-215.
[http://dx.doi.org/10.1046/j.1365-2796.2003.01228.x] [PMID: 12930229]
[13]
Wang, G., Ed.; Antimicrobial peptides: discovery, design and novel therapeutic strategies; CABI: Wallingford, 2010.
[http://dx.doi.org/10.1079/9781845936570.0000]
[14]
Cotter, P.D.; Hill, C.; Ross, R.P. Bacteriocins: developing innate immunity for food. Nat. Rev. Microbiol., 2005, 3(10), 777-788.
[http://dx.doi.org/10.1038/nrmicro1273] [PMID: 16205711]
[15]
Egorov, T.A.; Odintsova, T.I.; Pukhalsky, V.A.; Grishin, E.V. Diversity of wheat anti-microbial peptides. Peptides, 2005, 26(11), 2064-2073.
[http://dx.doi.org/10.1016/j.peptides.2005.03.007] [PMID: 16269343]
[16]
Wang, G. Improved methods for classification, prediction, and design of antimicrobial peptides. Methods Mol. Biol., 2015, 1268, 43-66.
[http://dx.doi.org/10.1007/978-1-4939-2285-7_3] [PMID: 25555720]
[17]
Wang, G. Human antimicrobial peptides and proteins. Pharmaceuticals, 2014, 7(5), 545-594.
[http://dx.doi.org/10.3390/ph7050545] [PMID: 24828484]
[18]
Gudmundsson, G.H.; Agerberth, B.; Odeberg, J.; Bergman, T.; Olsson, B.; Salcedo, R. The human gene FALL39 and processing of the cathelin precursor to the antibacterial peptide LL-37 in granulocytes. Eur. J. Biochem., 1996, 238(2), 325-332.
[http://dx.doi.org/10.1111/j.1432-1033.1996.0325z.x] [PMID: 8681941]
[19]
Wang, G. Structures of human host defense cathelicidin LL-37 and its smallest antimicrobial peptide KR-12 in lipid micelles. J. Biol. Chem., 2008, 283(47), 32637-32643.
[http://dx.doi.org/10.1074/jbc.M805533200] [PMID: 18818205]
[20]
Varga, J.F.A.; Bui-Marinos, M.P.; Katzenback, B.A. Frog skin innate immune defences: sensing and surviving pathogens. Front. Immunol., 2019, 9, 3128.
[http://dx.doi.org/10.3389/fimmu.2018.03128] [PMID: 30692997]
[21]
Csordas, A.; Michl, H. Isolation and structural resolution of a haemolytically active polypeptide from the immune secretion of a European toad. Monatsh. Chem., 1970, 101, 182-189.
[22]
Zasloff, M. 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. USA, 1987, 84(15), 5449-5453.
[http://dx.doi.org/10.1073/pnas.84.15.5449] [PMID: 3299384]
[23]
Berkowitz, B.A.; Bevins, C.L.; Zasloff, M.A. Magainins: a new family of membrane-active host defense peptides. Biochem. Pharmacol., 1990, 39(4), 625-629.
[http://dx.doi.org/10.1016/0006-2952(90)90138-B] [PMID: 1689576]
[24]
Matsuzaki, K. Magainins as paradigm for the mode of action of pore forming polypeptides. Biochim. Biophys. Acta, 1998, 1376(3), 391-400.
[http://dx.doi.org/10.1016/S0304-4157(98)00014-8] [PMID: 9804997]
[25]
Reddy, K.V.; Shahani, S.K.; Meherji, P.K. Spermicidal activity of Magainins: in vitro and in vivo studies. Contraception, 1996, 53(4), 205-210.
[http://dx.doi.org/10.1016/0010-7824(96)00038-8] [PMID: 8706437]
[26]
Baker, M.A.; Maloy, W.L.; Zasloff, M.; Jacob, L.S. Anticancer efficacy of Magainin2 and analogue peptides. Cancer Res., 1993, 53(13), 3052-3057.
[PMID: 8319212]
[27]
Yang, L.; Harroun, T.A.; Weiss, T.M.; Ding, L.; Huang, H.W. Barrel-stave model or toroidal model? A case study on melittin pores. Biophys. J., 2001, 81(3), 1475-1485.
[http://dx.doi.org/10.1016/S0006-3495(01)75802-X] [PMID: 11509361]
[28]
Rozek, T.; Wegener, K.L.; Bowie, J.H.; Olver, I.N.; Carver, J.A.; Wallace, J.C.; Tyler, M.J. The antibiotic and anticancer active aurein peptides from the Australian Bell Frogs Litoria aurea and Litoria raniformis the solution structure of aurein 1.2. Eur. J. Biochem., 2000, 267(17), 5330-5341.
[http://dx.doi.org/10.1046/j.1432-1327.2000.01536.x] [PMID: 10951191]
[29]
Wang, G.; Li, Y.; Li, X. Correlation of three-dimensional structures with the antibacterial activity of a group of peptides designed based on a nontoxic bacterial membrane anchor. J. Biol. Chem., 2005, 280(7), 5803-5811.
[http://dx.doi.org/10.1074/jbc.M410116200] [PMID: 15572363]
[30]
Li, X.; Li, Y.; Han, H.; Miller, D.W.; Wang, G. Solution structures of human LL-37 fragments and NMR-based identification of a minimal membrane-targeting antimicrobial and anticancer region. J. Am. Chem. Soc., 2006, 128(17), 5776-5785.
[http://dx.doi.org/10.1021/ja0584875] [PMID: 16637646]
[31]
Bulet, P.; Hetru, C.; Dimarcq, J.L.; Hoffmann, D. Antimicrobial peptides in insects; structure and function. Dev. Comp. Immunol., 1999, 23(4-5), 329-344.
[http://dx.doi.org/10.1016/S0145-305X(99)00015-4] [PMID: 10426426]
[32]
Steiner, H.; Hultmark, D.; Engström, A.; Bennich, H.; Boman, H.G. Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature, 1981, 292(5820), 246-248.
[http://dx.doi.org/10.1038/292246a0] [PMID: 7019715]
[33]
Zhu, Y.; Johnson, T.J.; Myers, A.A.; Kanost, M.R. Identification by subtractive suppression hybridization of bacteria-induced genes expressed in Manduca sexta fat body. Insect Biochem. Mol. Biol., 2003, 33(5), 541-559.
[http://dx.doi.org/10.1016/S0965-1748(03)00028-6] [PMID: 12706633]
[34]
Dai, H.; Rayaprolu, S.; Gong, Y.; Huang, R.; Prakash, O.; Jiang, H. Solution structure, antibacterial activity, and expression profile of Manduca sexta moricin. J. Pept. Sci., 2008, 14(7), 855-863.
[http://dx.doi.org/10.1002/psc.1016] [PMID: 18265434]
[35]
Fehlbaum, P.; Bulet, P.; Chernysh, S.; Briand, J.P.; Roussel, J.P.; Letellier, L.; Hetru, C.; Hoffmann, J.A. Structure-activity analysis of thanatin, a 21-residue inducible insect defense peptide with sequence homology to frog skin antimicrobial peptides. Proc. Natl. Acad. Sci. USA, 1996, 93(3), 1221-1225.
[http://dx.doi.org/10.1073/pnas.93.3.1221] [PMID: 8577744]
[36]
Imamura, T.; Yamamoto, N.; Tamura, A.; Murabayashi, S.; Hashimoto, S.; Shimada, H.; Taguchi, S. NMR based structure-activity relationship analysis of an antimicrobial peptide, thanatin, engineered by site-specific chemical modification: Activity improvement and spectrum alteration. Biochem. Biophys. Res. Commun., 2008, 369(2), 609-615.
[http://dx.doi.org/10.1016/j.bbrc.2008.02.057] [PMID: 18294955]
[37]
Monincová, L.; Buděšínský, M.; Čujová, S.; Čeřovský, V.; Veverka, V. Structural basis for antimicrobial activity of lasiocepsin. ChemBioChem, 2014, 15(2), 301-308.
[http://dx.doi.org/10.1002/cbic.201300509] [PMID: 24339323]
[38]
Lay, F.T.; Brugliera, F.; Anderson, M.A. Isolation and properties of floral defensins from ornamental tobacco and petunia. Plant Physiol., 2003, 131(3), 1283-1293.
[http://dx.doi.org/10.1104/pp.102.016626] [PMID: 12644678]
[39]
Essig, A.; Hofmann, D.; Münch, D.; Gayathri, S.; Künzler, M.; Kallio, P.T.; Sahl, H.G.; Wider, G.; Schneider, T.; Aebi, M. Copsin, a novel peptide-based fungal antibiotic interfering with the peptidoglycan synthesis. J. Biol. Chem., 2014, 289(50), 34953-34964.
[http://dx.doi.org/10.1074/jbc.M114.599878] [PMID: 25342741]
[40]
Imai, Y.; Meyer, K.J.; Iinishi, A.; Favre-Godal, Q.; Green, R.; Manuse, S.; Caboni, M.; Mori, M.; Niles, S.; Ghiglieri, M.; Honrao, C.; Ma, X.; Guo, J.J.; Makriyannis, A.; Linares-Otoya, L.; Böhringer, N.; Wuisan, Z.G.; Kaur, H.; Wu, R.; Mateus, A.; Typas, A.; Savitski, M.M.; Espinoza, J.L.; O’Rourke, A.; Nelson, K.E.; Hiller, S.; Noinaj, N.; Schäberle, T.F.; D’Onofrio, A.; Lewis, K. A new antibiotic selectively kills Gram-negative pathogens. Nature, 2019, 576(7787), 459-464.
[http://dx.doi.org/10.1038/s41586-019-1791-1] [PMID: 31747680]
[41]
Field, D.; Cotter, P.D.; Hill, C.; Ross, R.P. Bioengineering lantibiotics for therapeutic success. Front. Microbiol., 2015, 6, 1363.
[http://dx.doi.org/10.3389/fmicb.2015.01363] [PMID: 26640466]
[42]
Garg, N.; Tang, W.; Goto, Y.; Nair, S.K.; van der Donk, W.A. Lantibiotics from Geobacillus thermodenitrificans. Proc. Natl. Acad. Sci. USA, 2012, 109(14), 5241-5246.
[http://dx.doi.org/10.1073/pnas.1116815109] [PMID: 22431611]
[43]
Batista, C.V.; Scaloni, A.; Rigden, D.J.; Silva, L.R.; Rodrigues Romero, A.; Dukor, R.; Sebben, A.; Talamo, F.; Bloch, C. A novel heterodimeric antimicrobial peptide from the tree-frog Phyllomedusa distincta. FEBS Lett., 2001, 494(1-2), 85-89.
[http://dx.doi.org/10.1016/S0014-5793(01)02324-9] [PMID: 11297740]
[44]
Martin, N.I.; Sprules, T.; Carpenter, M.R.; Cotter, P.D.; Hill, C.; Ross, R.P.; Vederas, J.C. Structural characterization of lacticin 3147, a two-peptide lantibiotic with synergistic activity. Biochemistry, 2004, 43(11), 3049-3056.
[http://dx.doi.org/10.1021/bi0362065] [PMID: 15023056]
[45]
Wilson, K.A.; Kalkum, M.; Ottesen, J.; Yuzenkova, J.; Chait, B.T.; Landick, R.; Muir, T.; Severinov, K.; Darst, S.A. Structure of microcin J25, a peptide inhibitor of bacterial RNA polymerase, is a lassoed tail. J. Am. Chem. Soc., 2003, 125(41), 12475-12483.
[http://dx.doi.org/10.1021/ja036756q] [PMID: 14531691]
[46]
Kajimura, Y.; Kaneda, M. Fusaricidin A, a new depsipeptide antibiotic produced by Bacillus polymyxa KT-8. Taxonomy, fermentation, isolation, structure elucidation and biological activity. J. Antibiot. (Tokyo), 1996, 49(2), 129-135.
[http://dx.doi.org/10.7164/antibiotics.49.129] [PMID: 8621351]
[47]
Eliopoulos, G.M.; Willey, S.; Reiszner, E.; Spitzer, P.G.; Caputo, G.; Moellering, R.C., Jr In vitro and in vivo activity of LY 146032, a new cyclic lipopeptide antibiotic. Antimicrob. Agents Chemother., 1986, 30(4), 532-535.
[http://dx.doi.org/10.1128/AAC.30.4.532] [PMID: 3024560]
[48]
Guo, Y.; Huang, E.; Yuan, C.; Zhang, L.; Yousef, A.E. Isolation of a Paenibacillus sp. strain and structural elucidation of its broad-spectrum lipopeptide antibiotic. Appl. Environ. Microbiol., 2012, 78(9), 3156-3165.
[http://dx.doi.org/10.1128/AEM.07782-11] [PMID: 22367082]
[49]
Balty, C.; Guillot, A.; Fradale, L.; Brewee, C.; Boulay, M.; Kubiak, X.; Benjdia, A.; Berteau, O. Ruminococcin C, an anti-clostridial sactipeptide produced by a prominent member of the human microbiota Ruminococcus gnavus. J. Biol. Chem., 2019, 294(40), 14512-14525.
[http://dx.doi.org/10.1074/jbc.RA119.009416] [PMID: 31337708]
[50]
Abdalla, M.A.; McGaw, L.J. Natural cyclic peptides as an attractive modality for therapeutics: a mini review. Molecules, 2018, 23(8), 2080.
[http://dx.doi.org/10.3390/molecules23082080] [PMID: 30127265]
[51]
Niggemann, J.; Bozko, P.; Bruns, N.; Wodtke, A.; Gieseler, M.T.; Thomas, K.; Jahns, C.; Nimtz, M.; Reupke, I.; Brüser, T.; Auling, G.; Malek, N.; Kalesse, M. Baceridin, a cyclic hexapeptide from an epiphytic bacillus strain, inhibits the proteasome. ChemBioChem, 2014, 15(7), 1021-1029.
[http://dx.doi.org/10.1002/cbic.201300778] [PMID: 24692199]
[52]
Garcia, A.E.; Osapay, G.; Tran, P.A.; Yuan, J.; Selsted, M.E. Isolation, synthesis, and antimicrobial activities of naturally occurring theta-defensin isoforms from baboon leukocytes. Infect. Immun., 2008, 76(12), 5883-5891.
[http://dx.doi.org/10.1128/IAI.01100-08] [PMID: 18852242]
[53]
Tam, J.P.; Lu, Y.A.; Yang, J.L.; Chiu, K.W. An unusual structural motif of antimicrobial peptides containing end-to-end macrocycle and cystine-knot disulfides. Proc. Natl. Acad. Sci. USA, 1999, 96(16), 8913-8918.
[http://dx.doi.org/10.1073/pnas.96.16.8913] [PMID: 10430870]
[54]
Kawulka, K.E.; Sprules, T.; Diaper, C.M.; Whittal, R.M.; McKay, R.T.; Mercier, P.; Zuber, P.; Vederas, J.C. Structure of subtilosin A, a cyclic antimicrobial peptide from Bacillus subtilis with unusual sulfur to alpha-carbon cross-links: formation and reduction of alpha-thio-alpha-amino acid derivatives. Biochemistry, 2004, 43(12), 3385-3395.
[http://dx.doi.org/10.1021/bi0359527] [PMID: 15035610]
[55]
Hasper, H.E.; Kramer, N.E.; Smith, J.L.; Hillman, J.D.; Zachariah, C.; Kuipers, O.P.; de Kruijff, B.; Breukink, E. An alternative bactericidal mechanism of action for lantibiotic peptides that target lipid II. Science, 2006, 313(5793), 1636-1637.
[http://dx.doi.org/10.1126/science.1129818] [PMID: 16973881]
[56]
Ling, L.L.; Schneider, T.; Peoples, A.J.; Spoering, A.L.; Engels, I.; Conlon, B.P.; Mueller, A.; Schäberle, T.F.; Hughes, D.E.; Epstein, S.; Jones, M.; Lazarides, L.; Steadman, V.A.; Cohen, D.R.; Felix, C.R.; Fetterman, K.A.; Millett, W.P.; Nitti, A.G.; Zullo, A.M.; Chen, C.; Lewis, K. A new antibiotic kills pathogens without detectable resistance. Nature, 2015, 517(7535), 455-459.
[http://dx.doi.org/10.1038/nature14098] [PMID: 25561178]
[57]
Chen, K.H.; Le, S.P.; Han, X.; Frias, J.M.; Nowick, J.S. Alanine scan reveals modifiable residues in teixobactin. Chem. Commun. (Camb.), 2017, 53(82), 11357-11359.
[http://dx.doi.org/10.1039/C7CC03415F] [PMID: 28967925]
[58]
Abdel Monaim, S.A.H.; Ramchuran, E.J.; El-Faham, A.; Albericio, F.; de la Torre, B.G. Converting teixobactin into a cationic antimicrobial peptide (AMP). J. Med. Chem., 2017, 60(17), 7476-7482.
[http://dx.doi.org/10.1021/acs.jmedchem.7b00834] [PMID: 28795806]
[59]
Giltrap, A.M.; Dowman, L.J.; Nagalingam, G.; Ochoa, J.L.; Linington, R.G.; Britton, W.J.; Payne, R.J. Total synthesis of teixobactin. Org. Lett., 2016, 18(11), 2788-2791.
[http://dx.doi.org/10.1021/acs.orglett.6b01324] [PMID: 27191730]
[60]
Zong, Y.; Fang, F.; Meyer, K.J.; Wang, L.; Ni, Z.; Gao, H.; Lewis, K.; Zhang, J.; Rao, Y. Gram-scale total synthesis of teixobactin promoting binding mode study and discovery of more potent antibiotics. Nat. Commun., 2019, 10(1), 3268.
[http://dx.doi.org/10.1038/s41467-019-11211-y] [PMID: 31332172]
[61]
Gilmore, M.S.; Rauch, M.; Ramsey, M.M.; Himes, P.R.; Varahan, S.; Manson, J.M.; Lebreton, F.; Hancock, L.E. Pheromone killing of multidrug-resistant Enterococcus faecalis V583 by native commensal strains. Proc. Natl. Acad. Sci. USA, 2015, 112(23), 7273-7278.
[http://dx.doi.org/10.1073/pnas.1500553112] [PMID: 26039987]
[62]
Bulet, P.; Dimarcq, J.L.; Hetru, C.; Lagueux, M.; Charlet, M.; Hegy, G.; Van Dorsselaer, A.; Hoffmann, J.A. A novel inducible antibacterial peptide of Drosophila carries an O-glycosylated substitution. J. Biol. Chem., 1993, 268(20), 14893-14897.
[PMID: 8325867]
[63]
Cao, H.; Ke, T.; Liu, R.; Yu, J.; Dong, C.; Cheng, M.; Huang, J.; Liu, S. Identification of a novel proline-rich antimicrobial peptide from Brassica napus. PLoS One, 2015, 10(9)e0137414
[http://dx.doi.org/10.1371/journal.pone.0137414] [PMID: 26383098]
[64]
Mardirossian, M.; Pérébaskine, N.; Benincasa, M.; Gambato, S.; Hofmann, S.; Huter, P.; Müller, C.; Hilpert, K.; Innis, C.A.; Tossi, A.; Wilson, D.N. The Dolphin proline-rich antimicrobial peptide tur1A inhibits protein synthesis by targeting the bacterial ribosome. Cell Chem. Biol., 2018, 25(5), 530-539.e7.
[http://dx.doi.org/10.1016/j.chembiol.2018.02.004] [PMID: 29526712]
[65]
Tassanakajon, A.; Amparyup, P.; Somboonwiwat, K.; Supungul, P. Cationic antimicrobial peptides in penaeid shrimp. Mar. Biotechnol., 2010, 12, 487-505.
[http://dx.doi.org/10.1007/s10126-010-9288-9]
[66]
An, M.Y.; Gao, J.; Zhao, X.F.; Wang, J.X. A new subfamily of penaeidin with an additional serine-rich region from kuruma shrimp (Marsupenaeus japonicus) contributes to antimicrobial and phagocytic activities. Dev. Comp. Immunol., 2016, 59, 186-198.
[http://dx.doi.org/10.1016/j.dci.2016.02.001] [PMID: 26855016]
[67]
Crowe, J.E., Jr Treating flu with skin of frog. Immunity, 2017, 46(4), 517-518.
[http://dx.doi.org/10.1016/j.immuni.2017.04.007] [PMID: 28423328]
[68]
Kumar, V.T.; Holthausen, D.; Jacob, J.; George, S. Host defense peptides from Asian frogs as potential clinical therapies. Antibiotics (Basel), 2015, 4(2), 136-159.
[http://dx.doi.org/10.3390/antibiotics4020136] [PMID: 27025618]
[69]
Holthausen, D.J.; Lee, S.H.; Kumar, V.T.; Bouvier, N.M.; Krammer, F.; Ellebedy, A.H.; Wrammert, J.; Lowen, A.C.; George, S.; Pillai, M.R.; Jacob, J. An amphibian host defense peptide is virucidal for human H1 hemagglutinin-bearing influenza viruses. Immunity, 2017, 46(4), 587-595.
[http://dx.doi.org/10.1016/j.immuni.2017.03.018] [PMID: 28423338]
[70]
Ji, S.; Yun, H.; Park, G.; Min, H.J.; Lee, C.W. Expression and characterization of recombinant rattusin, an α-defensin-related peptide with a homodimeric scaffold formed by intermolecular disulfide exchanges. Protein Expr. Purif., 2018, 147, 17-21.
[http://dx.doi.org/10.1016/j.pep.2018.02.006] [PMID: 29454031]
[71]
Min, H.J.; Yun, H.; Ji, S.; Rajasekaran, G.; Kim, J.I.; Kim, J.S.; Shin, S.Y.; Lee, C.W. Rattusin structure reveals a novel defensin scaffold formed by intermolecular disulfide exchanges. Sci. Rep., 2017, 7, 45282.
[http://dx.doi.org/10.1038/srep45282] [PMID: 28345637]
[72]
Selsted, M.E.; Ouellette, A.J. Mammalian defensins in the antimicrobial immune response. Nat. Immunol., 2005, 6(6), 551-557.
[http://dx.doi.org/10.1038/ni1206] [PMID: 15908936]
[73]
Schroeder, B.O.; Wu, Z.; Nuding, S.; Groscurth, S.; Marcinowski, M.; Beisner, J.; Buchner, J.; Schaller, M.; Stange, E.F.; Wehkamp, J. Reduction of disulphide bonds unmasks potent antimicrobial activity of human β-defensin 1. Nature, 2011, 469(7330), 419-423.
[http://dx.doi.org/10.1038/nature09674] [PMID: 21248850]
[74]
Méndez-Samperio, P. The human cathelicidin hCAP18/LL-37: a multifunctional peptide involved in mycobacterial infections. Peptides, 2010, 31(9), 1791-1798.
[http://dx.doi.org/10.1016/j.peptides.2010.06.016] [PMID: 20600427]
[75]
Xhindoli, D.; Pacor, S.; Benincasa, M.; Scocchi, M.; Gennaro, R.; Tossi, A. The human cathelicidin LL-37--A pore-forming antibacterial peptide and host-cell modulator. Biochim. Biophys. Acta, 2016, 1858(3), 546-566.
[http://dx.doi.org/10.1016/j.bbamem.2015.11.003] [PMID: 26556394]
[76]
Sørensen, O.E.; Follin, P.; Johnsen, A.H.; Calafat, J.; Tjabringa, G.S.; Hiemstra, P.S.; Borregaard, N. Human cathelicidin, hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with proteinase 3. Blood, 2001, 97(12), 3951-3959.
[http://dx.doi.org/10.1182/blood.V97.12.3951] [PMID: 11389039]
[77]
Sørensen, O.E.; Gram, L.; Johnsen, A.H.; Andersson, E.; Bangsbøll, S.; Tjabringa, G.S.; Hiemstra, P.S.; Malm, J.; Egesten, A.; Borregaard, N. Processing of seminal plasma hCAP-18 to ALL-38 by gastricsin: a novel mechanism of generating antimicrobial peptides in vagina. J. Biol. Chem., 2003, 278(31), 28540-28546.
[http://dx.doi.org/10.1074/jbc.M301608200] [PMID: 12759353]
[78]
Murakami, M.; Kameda, K.; Tsumoto, H.; Tsuda, T.; Masuda, K.; Utsunomiya, R.; Mori, H.; Miura, Y.; Sayama, K. TLN-58, an additional hCAP18 processing form, found in the lesion vesicle of palmoplantar pustulosis in the skin. J. Invest. Dermatol., 2017, 137(2), 322-331.
[http://dx.doi.org/10.1016/j.jid.2016.07.044] [PMID: 27771329]
[79]
Toda, H.; Williams, J.A.; Gulledge, M.; Sehgal, A. A sleep-inducing gene, nemuri, links sleep and immune function in Drosophila. Science, 2019, 363(6426), 509-515.
[http://dx.doi.org/10.1126/science.aat1650] [PMID: 30705188]
[80]
Kuo, T.H.; Williams, J.A. Increased sleep promotes survival during a bacterial infection in Drosophila. Sleep (Basel),, 2014, 37(6), 1077-1086. 1086A-1086D
[http://dx.doi.org/10.5665/sleep.3764] [PMID: 24882902]
[81]
Schröder, J.M. Seeing is believing: Vitamin A promotes skin health through a host-derived antibiotic. Cell Host Microbe, 2019, 25(6), 769-770.
[http://dx.doi.org/10.1016/j.chom.2019.05.011] [PMID: 31194936]
[82]
Gallo, R.L.; Hooper, L.V. Epithelial antimicrobial defence of the skin and intestine. Nat. Rev. Immunol., 2012, 12(7), 503-516.
[http://dx.doi.org/10.1038/nri3228] [PMID: 22728527]
[83]
Russell, R.M.; Suter, P.M. Vitamin and trace mineral deficiency and excess.Harrison’s Principles of internal medicine; Longo, D.L.; Fauci, A.S.; Kasper, D.L.; Hauser, S.L.; Jameson, J.L; Loscalzo, J., Ed.; McGraw-Hill, 2012.
[84]
Harris, T.A.; Gattu, S.; Propheter, D.C.; Kuang, Z.; Bel, S.; Ruhn, K.A.; Chara, A.L.; Edwards, M.; Zhang, C.; Jo, J.H.; Raj, P.; Zouboulis, C.C.; Kong, H.H.; Segre, J.A.; Hooper, L.V. Resistin-like molecule α provides vitamin-A-dependent antimicrobial protection in the skin. Cell Host Microbe, 2019, 25(6), 777-788.e8.
[http://dx.doi.org/10.1016/j.chom.2019.04.004] [PMID: 31101494]
[85]
Karlsson, J.; Carlsson, G.; Larne, O.; Andersson, M.; Pütsep, K. Vitamin D3 induces pro-LL-37 expression in myeloid precursors from patients with severe congenital neutropenia. J. Leukoc. Biol., 2008, 84(5), 1279-1286.
[http://dx.doi.org/10.1189/jlb.0607437] [PMID: 18703682]
[86]
Huang, H.W. Action of antimicrobial peptides: two-state model. Biochemistry, 2000, 39(29), 8347-8352.
[http://dx.doi.org/10.1021/bi000946l] [PMID: 10913240]
[87]
Hansen, P.R., Ed.; Antimicrobial peptides: methods and protocols; Springer Nature: Switzerland, 2017.
[http://dx.doi.org/10.1007/978-1-4939-6737-7]
[88]
Chen, F.Y.; Lee, M.T.; Huang, H.W. Sigmoidal concentration dependence of antimicrobial peptide activities: a case study on alamethicin. Biophys. J., 2002, 82(2), 908-914.
[http://dx.doi.org/10.1016/S0006-3495(02)75452-0] [PMID: 11806932]
[89]
Su, Z.; Shodiev, M.; Leitch, J.J.; Abbasi, F.; Lipkowski, J. Role of transmembrane potential and defects on the permeabilization of lipid bilayers by alamethicin, an ion-channel-forming peptide. Langmuir, 2018, 34(21), 6249-6260.
[http://dx.doi.org/10.1021/acs.langmuir.8b00928] [PMID: 29722994]
[90]
Song, C.; Weichbrodt, C.; Salnikov, E.S.; Dynowski, M.; Forsberg, B.O.; Bechinger, B.; Steinem, C.; de Groot, B.L.; Zachariae, U.; Zeth, K. Crystal structure and functional mechanism of a human antimicrobial membrane channel. Proc. Natl. Acad. Sci. USA, 2013, 110(12), 4586-4591.
[http://dx.doi.org/10.1073/pnas.1214739110] [PMID: 23426625]
[91]
Henzler Wildman, K.A.; Lee, D.K.; Ramamoorthy, A. Mechanism of lipid bilayer disruption by the human antimicrobial peptide, LL-37. Biochemistry, 2003, 42(21), 6545-6558.
[http://dx.doi.org/10.1021/bi0273563] [PMID: 12767238]
[92]
Tang, M.; Hong, M. Structure and mechanism of beta-hairpin antimicrobial peptides in lipid bilayers from solid-state NMR spectroscopy. Mol. Biosyst., 2009, 5(4), 317-322.
[http://dx.doi.org/10.1039/b820398a] [PMID: 19396367]
[93]
Lei, J.; Sun, L.; Huang, S.; Zhu, C.; Li, P.; He, J.; Mackey, V.; Coy, D.H.; He, Q. The antimicrobial peptides and their potential clinical applications. Am. J. Transl. Res., 2019, 11(7), 3919-3931.
[PMID: 31396309]
[94]
Järvå, M.; Lay, F.T.; Phan, T.K.; Humble, C.; Poon, I.K.H.; Bleackley, M.R.; Anderson, M.A.; Hulett, M.D.; Kvansakul, M. X-ray structure of a carpet-like antimicrobial defensin-phospholipid membrane disruption complex. Nat. Commun., 2018, 9(1), 1962.
[http://dx.doi.org/10.1038/s41467-018-04434-y] [PMID: 29773800]
[95]
Gazit, E.; Miller, I.R.; Biggin, P.C.; Sansom, M.S.; Shai, Y. Structure and orientation of the mammalian antibacterial peptide cecropin P1 within phospholipid membranes. J. Mol. Biol., 1996, 258(5), 860-870.
[http://dx.doi.org/10.1006/jmbi.1996.0293] [PMID: 8637016]
[96]
Manzini, M.C.; Perez, K.R.; Riske, K.A.; Bozelli, J.C., Jr; Santos, T.L.; da Silva, M.A.; Saraiva, G.K.; Politi, M.J.; Valente, A.P.; Almeida, F.C.; Chaimovich, H.; Rodrigues, M.A.; Bemquerer, M.P.; Schreier, S.; Cuccovia, I.M. Peptide:lipid ratio and membrane surface charge determine the mechanism of action of the antimicrobial peptide BP100. Conformational and functional studies. Biochim. Biophys. Acta, 2014, 1838(7), 1985-1999.
[http://dx.doi.org/10.1016/j.bbamem.2014.04.004] [PMID: 24743023]
[97]
Phoenix, D.A.; Harris, F.; Mura, M.; Dennison, S.R. The increasing role of phosphatidylethanolamine as a lipid receptor in the action of host defence peptides. Prog. Lipid Res., 2015, 59, 26-37.
[http://dx.doi.org/10.1016/j.plipres.2015.02.003] [PMID: 25936689]
[98]
Burman, R.; Strömstedt, A.A.; Malmsten, M.; Göransson, U. Cyclotide-membrane interactions: defining factors of membrane binding, depletion and disruption. Biochim. Biophys. Acta, 2011, 1808(11), 2665-2673.
[http://dx.doi.org/10.1016/j.bbamem.2011.07.004] [PMID: 21787745]
[99]
Henriques, S.T.; Huang, Y.H.; Rosengren, K.J.; Franquelim, H.G.; Carvalho, F.A.; Johnson, A.; Sonza, S.; Tachedjian, G.; Castanho, M.A.; Daly, N.L.; Craik, D.J. Decoding the membrane activity of the cyclotide kalata B1: the importance of phosphatidylethanolamine phospholipids and lipid organization on hemolytic and anti-HIV activities. J. Biol. Chem., 2011, 286(27), 24231-24241.
[http://dx.doi.org/10.1074/jbc.M111.253393] [PMID: 21576247]
[100]
Sass, V.; Schneider, T.; Wilmes, M.; Körner, C.; Tossi, A.; Novikova, N.; Shamova, O.; Sahl, H.G. Human beta-defensin 3 inhibits cell wall biosynthesis in Staphylococci. Infect. Immun., 2010, 78(6), 2793-2800.
[http://dx.doi.org/10.1128/IAI.00688-09] [PMID: 20385753]
[101]
Breukink, E.; Wiedemann, I.; van Kraaij, C.; Kuipers, O.P.; Sahl, H.G.; de Kruijff, B. Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic. Science, 1999, 286(5448), 2361-2364.
[http://dx.doi.org/10.1126/science.286.5448.2361] [PMID: 10600751]
[102]
Kjos, M.; Oppegård, C.; Diep, D.B.; Nes, I.F.; Veening, J.W.; Nissen-Meyer, J.; Kristensen, T. Sensitivity to the two-peptide bacteriocin lactococcin G is dependent on UppP, an enzyme involved in cell-wall synthesis. Mol. Microbiol., 2014, 92(6), 1177-1187.
[http://dx.doi.org/10.1111/mmi.12632] [PMID: 24779486]
[103]
Lin, Y.M.; Wu, S.J.; Chang, T.W.; Wang, C.F.; Suen, C.S.; Hwang, M.J.; Chang, M.D.; Chen, Y.T.; Liao, Y.D. Outer membrane protein I of Pseudomonas aeruginosa is a target of cationic antimicrobial peptide/protein. J. Biol. Chem., 2010, 285(12), 8985-8994.
[http://dx.doi.org/10.1074/jbc.M109.078725] [PMID: 20100832]
[104]
Heeney, D.D.; Yarov-Yarovoy, V.; Marco, M.L. Sensitivity to the two peptide bacteriocin plantaricin EF is dependent on CorC, a membrane-bound, magnesium/cobalt efflux protein. MicrobiologyOpen, 2019, 8(11)e827
[http://dx.doi.org/10.1002/mbo3.827] [PMID: 30891921]
[105]
Nagarajan, D.; Roy, N.; Kulkarni, O.; Nanajkar, N.; Datey, A.; Ravichandran, S.; Thakur, C.Ω. 76: A designed antimicrobial peptide to combat carbapenem- and tigecycline-resistant Acinetobacter baumannii. Sci. Adv., 2019, 5(7)
[106]
Scocchi, M.; Mardirossian, M.; Runti, G.; Benincasa, M. Non-membrane permeabilizing modes of action of antimicrobial peptides on bacteria. Curr. Top. Med. Chem., 2016, 16(1), 76-88.
[http://dx.doi.org/10.2174/1568026615666150703121009] [PMID: 26139115]
[107]
Park, C.B.; Kim, H.S.; Kim, S.C. Mechanism of action of the antimicrobial peptide buforin II: buforin II kills microorganisms by penetrating the cell membrane and inhibiting cellular functions. Biochem. Biophys. Res. Commun., 1998, 244(1), 253-257.
[http://dx.doi.org/10.1006/bbrc.1998.8159] [PMID: 9514864]
[108]
Nam, J.; Yun, H.; Rajasekaran, G.; Kumar, S.D.; Kim, J.I.; Min, H.J.; Shin, S.Y.; Lee, C.W. Structural and functional assessment of mBjAMP1, an antimicrobial peptide from Branchiostoma japonicum, revealed a novel α-hairpinin-like scaffold with membrane permeable and DNA binding activity. J. Med. Chem., 2018, 61(24), 11101-11113.
[http://dx.doi.org/10.1021/acs.jmedchem.8b01135] [PMID: 30475621]
[109]
Lu, X.; Shen, J.; Jin, X.; Ma, Y.; Huang, Y.; Mei, H.; Chu, F.; Zhu, J. Bactericidal activity of Musca domestica cecropin (Mdc) on multidrug-resistant clinical isolate of Escherichia coli. Appl. Microbiol. Biotechnol., 2012, 95(4), 939-945.
[http://dx.doi.org/10.1007/s00253-011-3793-2] [PMID: 22202966]
[110]
Peng, J.; Long, H.; Liu, W.; Wu, Z.; Wang, T.; Zeng, Z.; Guo, G.; Wu, J. Antibacterial mechanism of peptide Cec4 against Acinetobacter baumannii. Infect. Drug Resist., 2019, 12, 2417-2428.
[http://dx.doi.org/10.2147/IDR.S214057] [PMID: 31496754]
[111]
Bandyopadhyay, S.; Lee, M.; Sivaraman, J.; Chatterjee, C. Model membrane interaction and DNA-binding of antimicrobial peptide Lasioglossin II derived from bee venom. Biochem. Biophys. Res. Commun., 2013, 430(1), 1-6.
[http://dx.doi.org/10.1016/j.bbrc.2012.11.015] [PMID: 23159628]
[112]
Hou, X.; Feng, C.; Li, S.; Luo, Q.; Shen, G.; Wu, H.; Li, M.; Liu, X.; Chen, A.; Ye, M.; Zhang, Z. Mechanism of antimicrobial peptide NP-6 from Sichuan pepper seeds against E. coli and effects of different environmental factors on its activity. Appl. Microbiol. Biotechnol., 2019, 103(16), 6593-6604.
[http://dx.doi.org/10.1007/s00253-019-09981-y] [PMID: 31286166]
[113]
Bellomio, A.; Vincent, P.A.; de Arcuri, B.F.; Farías, R.N.; Morero, R.D. Microcin J25 has dual and independent mechanisms of action in Escherichia coli: RNA polymerase inhibition and increased superoxide production. J. Bacteriol., 2007, 189(11), 4180-4186.
[http://dx.doi.org/10.1128/JB.00206-07] [PMID: 17400747]
[114]
Niklison-Chirou, M.V.; Dupuy, F.; Saavedra, L.; Hebert, E.; Banchio, C.; Minahk, C.; Morero, R.D. Microcin J25-Ga induces apoptosis in mammalian cells by inhibiting mitochondrial RNA-polymerase. Peptides, 2011, 32(4), 832-834.
[http://dx.doi.org/10.1016/j.peptides.2011.01.003] [PMID: 21256173]
[115]
Otvos, L., Jr The short proline-rich antibacterial peptide family. Cell. Mol. Life Sci., 2002, 59, 1138-1150.
[116]
Scocchi, M.; Lüthy, C.; Decarli, P.; Mignogna, G.; Christen, P.; Gennaro, R. The proline-rich antimicrobial peptide Bac7 binds to and inhibits in vitro the molecular chaperon DnaK. Int. J. Pept. Res. Ther., 2009, 15, 147-155.
[117]
Mardirossian, M.; Grzela, R.; Giglione, C.; Meinnel, T.; Gennaro, R.; Mergaert, P.; Scocchi, M. The host antimicrobial peptide Bac71-35 binds to bacterial ribosomal proteins and inhibits protein synthesis. Chem. Biol., 2014, 21(12), 1639-1647.
[http://dx.doi.org/10.1016/j.chembiol.2014.10.009] [PMID: 25455857]
[118]
Krizsan, A.; Volke, D.; Weinert, S.; Sträter, N.; Knappe, D.; Hoffmann, R. Insect-derived proline-rich antimicrobial peptides kill bacteria by inhibiting bacterial protein translation at the 70S ribosome. Angew. Chem. Int. Ed. Engl., 2014, 53(45), 12236-12239.
[http://dx.doi.org/10.1002/anie.201407145] [PMID: 25220491]
[119]
Taniguchi, M.; Ochiai, A.; Kondo, H.; Fukuda, S.; Ishiyama, Y.; Saitoh, E.; Kato, T.; Tanaka, T. Pyrrhocoricin, a proline-rich antimicrobial peptide derived from insect, inhibits the translation process in the cell-free Escherichia coli protein synthesis system. J. Biosci. Bioeng., 2016, 121(5), 591-598.
[http://dx.doi.org/10.1016/j.jbiosc.2015.09.002] [PMID: 26472128]
[120]
Laughlin, T.F.; Ahmad, Z. Inhibition of Escherichia coli ATP synthase by amphibian antimicrobial peptides. Int. J. Biol. Macromol., 2010, 46(3), 367-374.
[http://dx.doi.org/10.1016/j.ijbiomac.2010.01.015] [PMID: 20100509]
[121]
Ma, B.; Fang, C.; Lu, L.; Wang, M.; Xue, X.; Zhou, Y.; Li, M.; Hu, Y.; Luo, X.; Hou, Z. The antimicrobial peptide thanatin disrupts the bacterial outer membrane and inactivates the NDM-1 metallo-β-lactamase. Nat. Commun., 2019, 10(1), 3517.
[http://dx.doi.org/10.1038/s41467-019-11503-3] [PMID: 31388008]
[122]
Galván, A.E.; Chalón, M.C.; Ríos Colombo, N.S.; Schurig-Briccio, L.A.; Sosa-Padilla, B.; Gennis, R.B.; Bellomio, A. Microcin J25 inhibits ubiquinol oxidase activity of purified cytochrome bd-I from Escherichia coli. Biochimie, 2019, 160, 141-147.
[http://dx.doi.org/10.1016/j.biochi.2019.02.007] [PMID: 30790617]
[123]
Zhang, L.J.; Gallo, R.L. Antimicrobial peptides. Curr. Biol., 2016, 26(1), R14-R19.
[http://dx.doi.org/10.1016/j.cub.2015.11.017] [PMID: 26766224]
[124]
Lakshmaiah Narayana, J.; Mishra, B.; Lushnikova, T.; Wu, Q.; Chhonker, Y.S.; Zhang, Y.; Zarena, D.; Salnikov, E.S.; Dang, X.; Wang, F.; Murphy, C.; Foster, K.W.; Gorantla, S.; Bechinger, B.; Murry, D.J.; Wang, G. Two distinct amphipathic peptide antibiotics with systemic efficacy. Proc. Natl. Acad. Sci. USA, 2020, 117(32), 19446-19454.
[http://dx.doi.org/10.1073/pnas.2005540117] [PMID: 32723829]
[125]
Dartois, V.; Sanchez-Quesada, J.; Cabezas, E.; Chi, E.; Dubbelde, C.; Dunn, C.; Granja, J.; Gritzen, C.; Weinberger, D.; Ghadiri, M.R.; Parr, T.R., Jr Systemic antibacterial activity of novel synthetic cyclic peptides. Antimicrob. Agents Chemother., 2005, 49(8), 3302-3310.
[http://dx.doi.org/10.1128/AAC.49.8.3302-3310.2005] [PMID: 16048940]
[126]
Ostorhazi, E.; Holub, M.C.; Rozgonyi, F.; Harmos, F.; Cassone, M.; Wade, J.D.; Otvos, L. Jr Broad-spectrum antimicrobial efficacy of peptide A3-APO in mouse models of multidrug-resistant wound and lung infections cannot be explained by in vitro activity against the pathogens involved. Int. J. Antimicrob. Agents, 2011, 37(5), 480-484.
[http://dx.doi.org/10.1016/j.ijantimicag.2011.01.003] [PMID: 21353493]
[127]
Mishra, B.; Reiling, S.; Zarena, D.; Wang, G. Host defense antimicrobial peptides as antibiotics: design and application strategies. Curr. Opin. Chem. Biol., 2017, 38, 87-96.
[http://dx.doi.org/10.1016/j.cbpa.2017.03.014] [PMID: 28399505]

Rights & Permissions Print Cite
Article Metrics
55
© 2024 Bentham Science Publishers | Privacy Policy