Generic placeholder image

Current Protein & Peptide Science

Author(s): Marcella Nunes Melo-Braga, Flávia De Marco Almeida, Daniel Moreira dos Santos, Joaquim Teixeira de Avelar Júnior, Pablo Victor Mendes dos Reis and Maria Elena de Lima*

DOI: 10.2174/1389203721666200116091911

DownloadDownload PDF Flyer Cite As
Antimicrobial Peptides From Lycosidae (Sundevall, 1833) Spiders

Page: [527 - 541] Pages: 15

  • * (Excluding Mailing and Handling)

Abstract

Antimicrobial peptides (AMPs) have been found in all organism taxa and may play an essential role as a host defense system. AMPs are organized in various conformations, such as linear peptides, disulfide bond-linked peptides, backbone-linked peptides and circular peptides. AMPs apparently act primarily on the plasma membrane, although an increasing number of works have shown that they may also target various intracellular sites. Spider venoms are rich sources of biomolecules that show several activities, including modulation or blockage of ion channels, anti-insect, anti-cancer, antihypertensive and antimicrobial activities, among others. In spider venoms from the Lycosidae family there are many linear AMPs with a wide range of activities against several microorganisms. Due to these singular activities, some Lycosidae AMPs have been modified to improve or decrease desirable or undesirable effects, respectively. Such modifications, especially with the aim of increasing their antibiotic activity, have led to the filing of many patent applications. This review explores the abundance of Lycosidae venom AMPs and some of their derivatives, and their use as new drug models.

Keywords: Lycosidae, antimicrobial peptides, AMPs, Lycosa, anticancer peptides, spiders.

Graphical Abstract

[1]
Brogden, K.A. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol., 2005, 3(3), 238-250.
[http://dx.doi.org/10.1038/nrmicro1098] [PMID: 15703760]
[2]
Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature, 2002, 415(6870), 389-395.
[http://dx.doi.org/10.1038/415389a] [PMID: 11807545]
[3]
Bahar, A.A.; Ren, D. Antimicrobial peptides. Pharmaceuticals (Basel), 2013, 6(12), 1543-1575.
[http://dx.doi.org/10.3390/ph6121543] [PMID: 24287494]
[4]
Mahlapuu, M.; Håkansson, J.; Ringstad, L.; Björn, C. Antimicrobial Peptides: An Emerging Category of Therapeutic Agents. Front. Cell. Infect. Microbiol., 2016, 6, 194.
[http://dx.doi.org/10.3389/fcimb.2016.00194] [PMID: 28083516]
[5]
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]
[6]
Park, A.J.; Okhovat, J-P.; Kim, J. Antimicrobial Peptides.Clinical and Basic Immunodermatology; Springer International Publishing: Cham, 2017, pp. 81-95.
[http://dx.doi.org/10.1007/978-3-319-29785-9_6]
[7]
Kwong, W.K.; Mancenido, A.L.; Moran, N.A. Immune system stimulation by the native gut microbiota of honey bees. R. Soc. Open Sci., 2017, 4(2), 170003
[http://dx.doi.org/10.1098/rsos.170003] [PMID: 28386455]
[8]
Franzenburg, S.; Walter, J.; Künzel, S.; Wang, J.; Baines, J.F.; Bosch, T.C.G.; Fraune, S. Distinct antimicrobial peptide expression determines host species-specific bacterial associations. Proc. Natl. Acad. Sci. USA, 2013, 110(39), E3730-E3738.
[http://dx.doi.org/10.1073/pnas.1304960110] [PMID: 24003149]
[9]
Hancock, R.E.W.; Lehrer, R. Cationic peptides: a new source of antibiotics. Trends Biotechnol., 1998, 16(2), 82-88.
[http://dx.doi.org/10.1016/S0167-7799(97)01156-6] [PMID: 9487736]
[10]
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]
[11]
Wang, G. Antimicrobial Peptides: Discovery, Design, and Novel Therapeutic Strategies; CABI Publishing: Oxfordshire, 2010.
[http://dx.doi.org/10.1079/9781845936570.0000]
[12]
Wang, G. Improved Methods for Classification, Prediction, and Design of Antimicrobial Peptides. In: In: Computational Peptidology; , 2015; pp. 43-66.
[13]
Santos, D.M.; Reis, P.V.; Pimenta, A.M.C. Antimicrobial Peptides in Spider Venoms.Spider Venoms; Springer Netherlands: Dordrecht, 2016, pp. 361-377.
[http://dx.doi.org/10.1007/978-94-007-6389-0_19]
[14]
Wang, X.; Wang, G. Insights into Antimicrobial Peptides from Spiders and Scorpions. Protein Pept. Lett., 2016, 23(8), 707-721.
[http://dx.doi.org/10.2174/0929866523666160511151320] [PMID: 27165405]
[15]
Jenssen, H.; Hamill, P.; Hancock, R.E.W. Peptide antimicrobial agents. Clin. Microbiol. Rev., 2006, 19(3), 491-511.
[http://dx.doi.org/10.1128/CMR.00056-05] [PMID: 16847082]
[16]
Wimley, W.C.; Hristova, K. Antimicrobial peptides: successes, challenges and unanswered questions. J. Membr. Biol., 2011, 239(1-2), 27-34.
[http://dx.doi.org/10.1007/s00232-011-9343-0] [PMID: 21225255]
[17]
de Leeuw, E.; Li, C.; Zeng, P.; Li, C.; Diepeveen-de Buin, M.; Lu, W-Y.; Breukink, E.; Lu, W. Functional interaction of human neutrophil peptide-1 with the cell wall precursor lipid II. FEBS Lett., 2010, 584(8), 1543-1548.
[http://dx.doi.org/10.1016/j.febslet.2010.03.004] [PMID: 20214904]
[18]
Yonezawa, A.; Kuwahara, J.; Fujii, N.; Sugiura, Y. Binding of tachyplesin I to DNA revealed by footprinting analysis: significant contribution of secondary structure to DNA binding and implication for biological action. Biochemistry, 1992, 31(11), 2998-3004.
[http://dx.doi.org/10.1021/bi00126a022] [PMID: 1372516]
[19]
Subbalakshmi, C.; Sitaram, N. Mechanism of antimicrobial action of indolicidin. FEMS Microbiol. Lett., 1998, 160(1), 91-96.
[http://dx.doi.org/10.1111/j.1574-6968.1998.tb12896.x] [PMID: 9495018]
[20]
Azim, S.; McDowell, D.; Cartagena, A.; Rodriguez, R.; Laughlin, T.F.; Ahmad, Z. Venom peptides cathelicidin and lycotoxin cause strong inhibition of Escherichia coli ATP synthase. Int. J. Biol. Macromol., 2016, 87, 246-251.
[http://dx.doi.org/10.1016/j.ijbiomac.2016.02.061] [PMID: 26930579]
[21]
Wenzel, M.; Chiriac, A.I.; Otto, A.; Zweytick, D.; May, C.; Schumacher, C.; Gust, R.; Albada, H.B.; Penkova, M.; Krämer, U.; Erdmann, R.; Metzler-Nolte, N.; Straus, S.K.; Bremer, E.; Becher, D.; Brötz-Oesterhelt, H.; Sahl, H.G.; Bandow, J.E. Small cationic antimicrobial peptides delocalize peripheral membrane proteins. Proc. Natl. Acad. Sci. USA, 2014, 111(14), E1409-E1418.
[http://dx.doi.org/10.1073/pnas.1319900111] [PMID: 24706874]
[22]
Yewale, V.N. Antimicrobial resistance--a ticking bomb! Indian Pediatr., 2014, 51(3), 171-172.
[http://dx.doi.org/10.1007/s13312-014-0374-3] [PMID: 24736901]
[23]
Bai, G-H.; Plattner, R.; Desjardins, A.; Kolb, F. Resistance to Fusarium Head Blight and Deoxynivalenol Accumulation in Wheat. Plant Breed., 2001, 120(1), 1-6.
[http://dx.doi.org/10.1046/j.1439-0523.2001.00562.x]
[24]
Balouiri, M.; Sadiki, M.; Ibnsouda, S.K. Methods for in vitro evaluating antimicrobial activity: A review. J. Pharm. Anal., 2016, 6(2), 71-79.
[http://dx.doi.org/10.1016/j.jpha.2015.11.005] [PMID: 29403965]
[25]
Bessa, L.J.; Eaton, P.; Dematei, A.; Plácido, A.; Vale, N.; Gomes, P.; Delerue-Matos, C.; Sa Leite, J.R.; Gameiro, P. Synergistic and antibiofilm properties of ocellatin peptides against multidrug-resistant Pseudomonas aeruginosa. Future Microbiol., 2018, 13(2), 151-163.
[http://dx.doi.org/10.2217/fmb-2017-0175] [PMID: 29308671]
[26]
Gordon, Y.J.; Romanowski, E.G.; McDermott, A.M. A review of antimicrobial peptides and their therapeutic potential as anti-infective drugs. Curr. Eye Res., 2005, 30(7), 505-515.
[http://dx.doi.org/10.1080/02713680590968637] [PMID: 16020284]
[27]
Dobson, A.J.; Purves, J.; Kamysz, W.; Rolff, J. Comparing selection on S. aureus between antimicrobial peptides and common antibiotics. PLoS One, 2013, 8(10), e76521
[http://dx.doi.org/10.1371/journal.pone.0076521] [PMID: 24204634]
[28]
Deslouches, B.; Di, Y.P. Antimicrobial peptides with selective antitumor mechanisms: prospect for anticancer applications. Oncotarget, 2017, 8(28), 46635-46651.
[http://dx.doi.org/10.18632/oncotarget.16743] [PMID: 28422728]
[29]
Felício, M.R.; Silva, O.N.; Gonçalves, S.; Santos, N.C.; Franco, O.L. Peptides with Dual Antimicrobial and Anticancer Activities. Front Chem., 2017, 5, 5.
[http://dx.doi.org/10.3389/fchem.2017.00005] [PMID: 28271058]
[30]
Pretzel, J.; Mohring, F.; Rahlfs, S.; Becker, K. Antiparasitic peptides. Advances in biochemical engineering/biotechnology, 2013, 157-192.
[http://dx.doi.org/10.1007/10_2013_191]
[31]
Perumal Samy, R.; Stiles, B.G.; Franco, O.L.; Sethi, G.; Lim, L.H.K. Animal venoms as antimicrobial agents. Biochem. Pharmacol., 2017, 134, 127-138.
[http://dx.doi.org/10.1016/j.bcp.2017.03.005] [PMID: 28288817]
[32]
Primon-Barros, M.; José Macedo, A. Animal Venom Peptides: Potential for New Antimicrobial Agents. Curr. Top. Med. Chem., 2017, 17(10), 1119-1156.
[http://dx.doi.org/10.2174/1568026616666160930151242] [PMID: 27697042]
[33]
Yan, L.; Adams, M.E. Lycotoxins, antimicrobial peptides from venom of the wolf spider Lycosa carolinensis. J. Biol. Chem., 1998, 273(4), 2059-2066.
[http://dx.doi.org/10.1074/jbc.273.4.2059] [PMID: 9442044]
[34]
World Spider Catalog. Nat; Hist. Museum Bern, 2018.
[35]
Campbell, D.S.; Rees, R.S.; King, L.E. Wolf spider bites. Cutis, 1987, 39(2), 113-114.
[PMID: 3829717]
[36]
Ribeiro, L.A.; Jorge, M.T.; Piesco, R.V.; Nishioka, Sde.A. Wolf spider bites in São Paulo, Brazil: a clinical and epidemiological study of 515 cases. Toxicon, 1990, 28(6), 715-717.
[http://dx.doi.org/10.1016/0041-0101(90)90260-E] [PMID: 2402765]
[37]
Isbister, G.K.; Framenau, V.W. Australian wolf spider bites (Lycosidae): clinical effects and influence of species on bite circumstances. J. Toxicol. Clin. Toxicol., 2004, 42(2), 153-161.
[http://dx.doi.org/10.1081/CLT-120030941] [PMID: 15214620]
[38]
Livshits, Z.; Bernstein, B.; Sorkin, L.N.; Smith, S.W.; Hoffman, R.S. Wolf spider envenomation. Wilderness Environ. Med., 2012, 23(1), 49-50.
[http://dx.doi.org/10.1016/j.wem.2011.11.010] [PMID: 22441089]
[39]
Xu, K.; Ji, Y.; Qu, X. Purification and Characterization of an Antibacterial Peptide from Venom of Lycosa Singoriensis. Dong Wu Xue Bao, 1989, 35(3), 300-305.
[40]
Cruz, J.S.; Cotta, G.; Diniz, C.R.; Beirão, P.S. Partial purification and pharmacological characterization of a neurotoxic fraction isolated from the venom of the spider Lycosa erythrognatha. Braz. J. Med. Biol. Res., 1994, 27(11), 2653-2659.
[PMID: 7549989]
[41]
Ferreira, L.A.F.; Alves, W.E.; Lucas, M.S.; Habermehl, G.G. Isolation and characterization of a bradykinin potentiating peptide (BPP-S) isolated from Scaptocosa raptoria venom. Toxicon, 1996, 34(5), 599-603.
[http://dx.doi.org/10.1016/0041-0101(96)00010-4] [PMID: 8783454]
[42]
Roewer, C.F. Katalog Der Araneae von 1758 Bis 1940, Bzw.. Institut royal des Sciences naturelles de Belgique: Bruxelles; , 1954, pp. 1-1751.
[43]
Roewer, V.C.F. Araneae Lycosaeformia II; Lycosidae, 1959.
[44]
King, G.F.; Gentz, M.C.; Escoubas, P.; Nicholson, G.M. A rational nomenclature for naming peptide toxins from spiders and other venomous animals. Toxicon, 2008, 52(2), 264-276.
[http://dx.doi.org/10.1016/j.toxicon.2008.05.020] [PMID: 18619481]
[45]
Menousek, J.; Mishra, B.; Hanke, M.L.; Heim, C.E.; Kielian, T.; Wang, G. Database screening and in vivo efficacy of antimicrobial peptides against methicillin-resistant Staphylococcus aureus USA300. Int. J. Antimicrob. Agents, 2012, 39(5), 402-406.
[http://dx.doi.org/10.1016/j.ijantimicag.2012.02.003] [PMID: 22445495]
[46]
Budnik, B.A.; Olsen, J.V.; Egorov, T.A.; Anisimova, V.E.; Galkina, T.G.; Musolyamov, A.K.; Grishin, E.V.; Zubarev, R.A. De novo sequencing of antimicrobial peptides isolated from the venom glands of the wolf spider Lycosa singoriensis. J. Mass Spectrom., 2004, 39(2), 193-201.
[http://dx.doi.org/10.1002/jms.577] [PMID: 14991689]
[47]
Liu, Z.; Deng, M.; Xiang, J.; Ma, H.; Hu, W.; Zhao, Y.; Li, D.W-C.; Liang, S. A novel spider peptide toxin suppresses tumor growth through dual signaling pathways. Curr. Mol. Med., 2012, 12(10), 1350-1360.
[http://dx.doi.org/10.2174/156652412803833643] [PMID: 22882120]
[48]
Tan, H.; Ding, X.; Meng, S.; Liu, C.; Wang, H.; Xia, L.; Liu, Z.; Liang, S. Antimicrobial potential of lycosin-I, a cationic and amphiphilic peptide from the venom of the spider Lycosa singorensis. Curr. Mol. Med., 2013, 13(6), 900-910.
[http://dx.doi.org/10.2174/15665240113139990045] [PMID: 23638903]
[49]
Wang, L.; Wang, Y-J.; Liu, Y-Y.; Li, H.; Guo, L-X.; Liu, Z-H.; Shi, X-L.; Hu, M. In vitro potential of Lycosin-I as an alternative antimicrobial drug for treatment of multidrug-resistant Acinetobacter baumannii infections. Antimicrob. Agents Chemother., 2014, 58(11), 6999-7002.
[http://dx.doi.org/10.1128/AAC.03279-14] [PMID: 25199777]
[50]
Wang, Y.; Wang, L.; Yang, H.; Xiao, H.; Farooq, A.; Liu, Z.; Hu, M.; Shi, X. The Spider Venom Peptide Lycosin-II Has Potent Antimicrobial Activity against Clinically Isolated Bacteria. Toxins (Basel), 2016, 8(5), 119.
[http://dx.doi.org/10.3390/toxins8050119] [PMID: 27128941]
[51]
Santos, D.M.; Verly, R.M.; Piló-Veloso, D.; de Maria, M.; de Carvalho, M.A.R.; Cisalpino, P.S.; Soares, B.M.; Diniz, C.G.; Farias, L.M.; Moreira, D.F.F.; Frézard, F.; Bemquerer, M.P.; Pimenta, A.M.; de Lima, M.E. LyeTx I, a potent antimicrobial peptide from the venom of the spider Lycosa erythrognatha. Amino Acids, 2010, 39(1), 135-144.
[http://dx.doi.org/10.1007/s00726-009-0385-x] [PMID: 19946788]
[52]
Consuegra, J.; de Lima, M.E.; Santos, D.; Sinisterra, R.D.; Cortés, M.E. Peptides: β-cyclodextrin inclusion compounds as highly effective antimicrobial and anti-epithelial proliferation agents. J. Periodontol., 2013, 84(12), 1858-1868.
[http://dx.doi.org/10.1902/jop.2013.120679] [PMID: 23510146]
[53]
Cruz Olivo, E.A.; Santos, D.; de Lima, M.E.; Dos Santos, V.L.; Sinisterra, R.D.; Cortés, M.E. Antibacterial Effect of Synthetic Peptide LyeTxI and LyeTxI/β-Cyclodextrin Association Compound Against Planktonic and Multispecies Biofilms of Periodontal Pathogens. J. Periodontol., 2017, 88(6), e88-e96.
[http://dx.doi.org/10.1902/jop.2016.160438] [PMID: 27989223]
[54]
Nuding, S.; Frasch, T.; Schaller, M.; Stange, E.F.; Zabel, L.T. Synergistic effects of antimicrobial peptides and antibiotics against Clostridium difficile. Antimicrob. Agents Chemother., 2014, 58(10), 5719-5725.
[http://dx.doi.org/10.1128/AAC.02542-14] [PMID: 25022581]
[55]
Tan, H.; Huang, Y.; Xu, J.; Chen, B.; Zhang, P.; Ye, Z.; Liang, S.; Xiao, L.; Liu, Z. Spider Toxin Peptide Lycosin-I Functionalized Gold Nanoparticles for in vivo Tumor Targeting and Therapy. Theranostics, 2017, 7(12), 3168-3178.
[http://dx.doi.org/10.7150/thno.19780] [PMID: 28839471]
[56]
Huth, H.W.; Santos, D.M.; Gravina, H.D.; Resende, J.M.; Goes, A.M.; de Lima, M.E.; Ropert, C. Upregulation of p38 pathway accelerates proliferation and migration of MDA-MB-231 breast cancer cells. Oncol. Rep., 2017, 37(4), 2497-2505.
[http://dx.doi.org/10.3892/or.2017.5452] [PMID: 28260101]
[57]
Ma, B.; Xi, Z.; Li, J.; Gao, T.; Liao, R.; Wang, S.; Li, X.; Tang, Y.; Wang, Z.; Hou, S.; Jiang, J.; Deng, M.; Duan, Z.; Tang, X.; Jiang, L. Vasodilator and hypotensive effects of the spider peptide Lycosin-I in vitro and in vivo. Peptides, 2018, 99, 108-114.
[http://dx.doi.org/10.1016/j.peptides.2017.12.011] [PMID: 29248696]
[58]
Moreira, C.K.; Rodrigues, F.G.; Ghosh, A.; Varotti, F. de P.; Miranda, A.; Daffre, S.; Jacobs-Lorena, M.; Moreira, L.A. Effect of the antimicrobial peptide gomesin against different life stages of Plasmodium spp. Exp. Parasitol., 2007, 116(4), 346-353.
[http://dx.doi.org/10.1016/j.exppara.2007.01.022] [PMID: 17376436]
[59]
Tang, Y.; Hou, S.; Li, X.; Wu, M.; Ma, B.; Wang, Z.; Jiang, J.; Deng, M.; Duan, Z.; Tang, X.; Liu, Y.; Wang, W.; Han, X.; Jiang, L. Anti-parasitic effect on Toxoplasma gondii induced by a spider peptide lycosin-I. Exp. Parasitol., 2019, 198, 17-25.
[http://dx.doi.org/10.1016/j.exppara.2019.01.009] [PMID: 30682337]
[60]
Rothan, H.A.; Bahrani, H.; Rahman, N.A.; Yusof, R. Identification of natural antimicrobial agents to treat dengue infection: In vitro analysis of latarcin peptide activity against dengue virus. BMC Microbiol., 2014, 14(1), 140.
[http://dx.doi.org/10.1186/1471-2180-14-140] [PMID: 24885331]
[61]
Bulet, P.; Stöcklin, R.; Menin, L. Anti-microbial peptides: from invertebrates to vertebrates. Immunol. Rev., 2004, 198, 169-184.
[http://dx.doi.org/10.1111/j.0105-2896.2004.0124.x] [PMID: 15199962]
[62]
Kondejewski, L.H.; Jelokhani-Niaraki, M.; Farmer, S.W.; Lix, B.; Kay, C.M.; Sykes, B.D.; Hancock, R.E.W.; Hodges, R.S. Dissociation of antimicrobial and hemolytic activities in cyclic peptide diastereomers by systematic alterations in amphipathicity. J. Biol. Chem., 1999, 274(19), 13181-13192.
[http://dx.doi.org/10.1074/jbc.274.19.13181] [PMID: 10224074]
[63]
Dathe, M.; Wieprecht, T.; Nikolenko, H.; Handel, L.; Maloy, W.L.; MacDonald, D.L.; Beyermann, M.; Bienert, M. Hydrophobicity, hydrophobic moment and angle subtended by charged residues modulate antibacterial and haemolytic activity of amphipathic helical peptides. FEBS Lett., 1997, 403(2), 208-212.
[http://dx.doi.org/10.1016/S0014-5793(97)00055-0] [PMID: 9042968]
[64]
Edwards, I.A.; Elliott, A.G.; Kavanagh, A.M.; Zuegg, J.; Blaskovich, M.A.T.; Cooper, M.A. Contribution of Amphipathicity and Hydrophobicity to the Antimicrobial Activity and Cytotoxicity of β-Hairpin Peptides. ACS Infect. Dis., 2016, 2(6), 442-450.
[http://dx.doi.org/10.1021/acsinfecdis.6b00045] [PMID: 27331141]
[65]
Dennison, S.R.; Phoenix, D.A. Susceptibility of sheep, human, and pig erythrocytes to haemolysis by the antimicrobial peptide Modelin 5. Eur. Biophys. J., 2014, 43(8-9), 423-432.
[http://dx.doi.org/10.1007/s00249-014-0974-9] [PMID: 25030320]
[66]
Belokoneva, O.S.; Villegas, E.; Corzo, G.; Dai, L.; Nakajima, T. The hemolytic activity of six arachnid cationic peptides is affected by the phosphatidylcholine-to-sphingomyelin ratio in lipid bilayers. Biochim. Biophys. Acta, 2003, 1617(1-2), 22-30.
[http://dx.doi.org/10.1016/j.bbamem.2003.08.010] [PMID: 14637016]
[67]
Helmerhorst, E.J.; Reijnders, I.M.; van ’t Hof, W.; Veerman, E.C.I.; Nieuw Amerongen, A.V. A critical comparison of the hemolytic and fungicidal activities of cationic antimicrobial peptides. FEBS Lett., 1999, 449(2-3), 105-110.
[http://dx.doi.org/10.1016/S0014-5793(99)00411-1] [PMID: 10338113]
[68]
Ohsaki, Y.; Gazdar, A.F.; Chen, H.C.; Johnson, B.E. Antitumor activity of magainin analogues against human lung cancer cell lines. Cancer Res., 1992, 52(13), 3534-3538.
[PMID: 1319823]
[69]
Hoskin, D.W.; Ramamoorthy, A. Studies on anticancer activities of antimicrobial peptides. Biochim. Biophys. Acta, 2008, 1778(2), 357-375.
[http://dx.doi.org/10.1016/j.bbamem.2007.11.008] [PMID: 18078805]
[70]
Gaspar, D.; Veiga, A.S.; Castanho, M.A.R.B. From antimicrobial to anticancer peptides. A review. Front. Microbiol., 2013, 4, 294.
[http://dx.doi.org/10.3389/fmicb.2013.00294] [PMID: 24101917]
[71]
Hancock, R.E.W.; 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]
[72]
Afacan, N.J.; Yeung, A.T.Y.; Pena, O.M.; Hancock, R.E.W. Therapeutic potential of host defense peptides in antibiotic-resistant infections. Curr. Pharm. Des., 2012, 18(6), 807-819.
[http://dx.doi.org/10.2174/138161212799277617] [PMID: 22236127]
[73]
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]
[74]
Nizet, V. Antimicrobial peptide resistance mechanisms of human bacterial pathogens. Curr. Issues Mol. Biol., 2006, 8(1), 11-26.
[PMID: 16450883]
[75]
Andersson, D.I.; Hughes, D.; Kubicek-Sutherland, J.Z. Mechanisms and consequences of bacterial resistance to antimicrobial peptides. Drug Resist. Updat., 2016, 26, 43-57.
[http://dx.doi.org/10.1016/j.drup.2016.04.002] [PMID: 27180309]
[76]
Baguley, B.C. Multiple drug resistance mechanisms in cancer. Mol. Biotechnol., 2010, 46(3), 308-316.
[http://dx.doi.org/10.1007/s12033-010-9321-2] [PMID: 20717753]
[77]
Lau, J.L.; Dunn, M.K. Therapeutic peptides: Historical perspectives, current development trends, and future directions. Bioorg. Med. Chem., 2018, 26(10), 2700-2707.
[http://dx.doi.org/10.1016/j.bmc.2017.06.052] [PMID: 28720325]
[78]
Blondelle, S.E.; Houghten, R.A. Design of model amphipathic peptides having potent antimicrobial activities. Biochemistry, 1992, 31(50), 12688-12694.
[http://dx.doi.org/10.1021/bi00165a020] [PMID: 1472506]
[79]
Deslouches, B.; Phadke, S.M.; Lazarevic, V.; Cascio, M.; Islam, K.; Montelaro, R.C.; Mietzner, T.A. De novo generation of cationic antimicrobial peptides: influence of length and tryptophan substitution on antimicrobial activity. Antimicrob. Agents Chemother., 2005, 49(1), 316-322.
[http://dx.doi.org/10.1128/AAC.49.1.316-322.2005] [PMID: 15616311]
[80]
Deslouches, B.; Steckbeck, J.D.; Craigo, J.K.; Doi, Y.; Mietzner, T.A.; Montelaro, R.C. Rational design of engineered cationic antimicrobial peptides consisting exclusively of arginine and tryptophan, and their activity against multidrug-resistant pathogens. Antimicrob. Agents Chemother., 2013, 57(6), 2511-2521.
[http://dx.doi.org/10.1128/AAC.02218-12] [PMID: 23507278]
[81]
Ge, Y.; MacDonald, D.L.; Holroyd, K.J.; Thornsberry, C.; Wexler, H.; Zasloff, M. In vitro antibacterial properties of pexiganan, an analog of magainin. Antimicrob. Agents Chemother., 1999, 43(4), 782-788.
[http://dx.doi.org/10.1128/AAC.43.4.782] [PMID: 10103181]
[82]
Nagarajan, D.; Nagarajan, T.; Roy, N.; Kulkarni, O.; Ravichandran, S.; Mishra, M.; Chakravortty, D.; Chandra, N. Computational antimicrobial peptide design and evaluation against multidrug-resistant clinical isolates of bacteria. J. Biol. Chem., 2018, 293(10), 3492-3509.
[http://dx.doi.org/10.1074/jbc.M117.805499] [PMID: 29259134]
[83]
Lee, E.Y.; Lee, M.W.; Fulan, B.M.; Ferguson, A.L.; Wong, G.C.L. What can machine learning do for antimicrobial peptides, and what can antimicrobial peptides do for machine learning? Interface Focus, 2017, 7(6), 20160153
[http://dx.doi.org/10.1098/rsfs.2016.0153] [PMID: 29147555]
[84]
Lee, E.Y.; Fulan, B.M.; Wong, G.C.L.; Ferguson, A.L. Mapping membrane activity in undiscovered peptide sequence space using machine learning. Proc. Natl. Acad. Sci. USA, 2016, 113(48), 13588-13593.
[http://dx.doi.org/10.1073/pnas.1609893113] [PMID: 27849600]
[85]
Tucker, A.T.; Leonard, S.P.; DuBois, C.D.; Knauf, G.A.; Cunningham, A.L.; Wilke, C.O.; Trent, M.S.; Davies, B.W. Discovery of Next-Generation Antimicrobials through Bacterial Self-Screening of Surface-Displayed Peptide Libraries. Cell, 2018, 172(3), 618-628.e13.
[http://dx.doi.org/10.1016/j.cell.2017.12.009] [PMID: 29307492]
[86]
Hallock, K.J.; Lee, D-K.; Ramamoorthy, A. MSI-78, an analogue of the magainin antimicrobial peptides, disrupts lipid bilayer structure via positive curvature strain. Biophys. J., 2003, 84(5), 3052-3060.
[http://dx.doi.org/10.1016/S0006-3495(03)70031-9] [PMID: 12719236]
[87]
Adão, R.; Seixas, R.; Gomes, P.; Pessoa, J.C.; Bastos, M. Membrane structure and interactions of a short Lycotoxin I analogue. J. Pept. Sci., 2008, 14(4), 528-534.
[http://dx.doi.org/10.1002/psc.993] [PMID: 18098329]
[88]
Hughes, S.R.; Dowd, P.F.; Hector, R.E.; Panavas, T.; Sterner, D.E.; Qureshi, N.; Bischoff, K.M.; Bang, S.S.; Mertens, J.A.; Johnson, E.T.; Li, X.L.; Jackson, J.S.; Caughey, R.J.; Riedmuller, S.B.; Bartolett, S.; Liu, S.; Rich, J.O.; Farrelly, P.J.; Butt, T.R.; Labaer, J.; Cotta, M.A. Lycotoxin-1 insecticidal peptide optimized by amino acid scanning mutagenesis and expressed as a coproduct in an ethanologenic Saccharomyces cerevisiae strain. J. Pept. Sci., 2008, 14(9), 1039-1050.
[http://dx.doi.org/10.1002/psc.1040] [PMID: 18465835]
[89]
Johnson, E.T.; Dowd, P.F.; Hughes, S.R. Expression of a wolf spider toxin in tobacco inhibits the growth of microbes and insects. Biotechnol. Lett., 2014, 36(8), 1735-1742.
[http://dx.doi.org/10.1007/s10529-014-1536-z] [PMID: 24770871]
[90]
Hughes, S.R.; Dowd, P.F.; Johnson, E.T. Cell-penetrating recombinant peptides for potential use in agricultural pest control applications. Pharmaceuticals (Basel), 2012, 5(10), 1054-1063.
[http://dx.doi.org/10.3390/ph5101054] [PMID: 24281256]
[91]
Zhang, P.; Ma, J.; Yan, Y.; Chen, B.; Liu, B.; Jian, C.; Zhu, B.; Liang, S.; Zeng, Y.; Liu, Z. Arginine modification of lycosin-I to improve inhibitory activity against cancer cells. Org. Biomol. Chem., 2017, 15(44), 9379-9388.
[http://dx.doi.org/10.1039/C7OB02233F] [PMID: 29090725]
[92]
Jian, C.; Zhang, P.; Ma, J.; Jian, S.; Zhang, Q.; Liu, B.; Liang, S.; Liu, M.; Zeng, Y.; Liu, Z. The Roles of Fatty-Acid Modification in the Activity of the Anticancer Peptide R-Lycosin-I. Mol. Pharm., 2018, 15(10), 4612-4620.
[http://dx.doi.org/10.1021/acs.molpharmaceut.8b00605] [PMID: 30183307]
[93]
Reis, P.V.M.; Boff, D.; Verly, R.M.; Melo-Braga, M.N.; Cortés, M.E.; Santos, D.M.; Pimenta, A.M.C.; Amaral, F.A.; Resende, J.M.; de Lima, M.E. LyeTxI-b, a Synthetic Peptide Derived From Lycosa erythrognatha Spider Venom, Shows Potent Antibiotic Activity in Vitro and in Vivo. Front. Microbiol., 2018, 9, 667.
[http://dx.doi.org/10.3389/fmicb.2018.00667] [PMID: 29681894]
[94]
Abdel-Salam, M.A.L.; Carvalho-Tavares, J.; Gomes, K.S.; Teixeira-Carvalho, A.; Kitten, G.T.; Nyffeler, J.; Dias, F.F.; Dos Reis, P.V.M.; Pimenta, A.M.C.; Leist, M.; de Lima, M.E.; de Souza-Fagundes, E.M. The synthetic peptide LyeTxI-b derived from Lycosa erythrognatha spider venom is cytotoxic to U-87 MG glioblastoma cells. Amino Acids, 2019, 51(3), 433-449.
[http://dx.doi.org/10.1007/s00726-018-2678-4] [PMID: 30449002]
[95]
Silva, F.R.D.; Paiva, M.R.B.; Dourado, L.F.N.; Silva, R.O.; Silva, C.N.D.; Costa, B.L.D.; Toledo, C.R.; de Lima, M.E.; Silva-Cunha, A.D. Intravitreal injection of the synthetic peptide LyeTx I b, derived from a spider toxin, into the rabbit eye is safe and prevents neovascularization in a chorio-allantoic membrane model. J. Venom. Anim. Toxins Incl. Trop. Dis., 2018, 24(1), 31.
[http://dx.doi.org/10.1186/s40409-018-0168-5] [PMID: 30479614]
[96]
Silva, C.N.D.; Silva, F.R.D.; Dourado, L.F.N.; Reis, P.V.M.D.; Silva, R.O.; Costa, B.L.D.; Nunes, P.S.; Amaral, F.A.; Santos, V.L.D.; de Lima, M.E.; Silva Cunha Júnior, A.D. A new topical eye drop containing LyeTxI-b, a synthetic peptide designed from a lycosa erithrognata venom toxin, was effective to treat resistant bacterial keraTITIS. Toxins (Basel), 2019, 11(4), 203.
[http://dx.doi.org/10.3390/toxins11040203] [PMID: 30987317]