Structural insights into and activity analysis of the antimicrobial peptide myxinidin

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 9, 2014, Pages 5280-5290

  Cantisani, Marco ^a,b,c   Finamore, Emiliana ^a   Mignogna, Eleonora ^a   Falanga, Annarita ^a,b   Nicoletti, Giovanni Francesco ^a   Pedone, Carlo ^a,b   Morelli, Giancarlo ^a,b   Leone, Marilisa ^b   Galdiero, Massimiliano ^a   Galdiero, Stefania ^a,b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b CNR   (Italy)

^c ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; MYXINIDIN; POLYPEPTIDE ANTIBIOTIC AGENT; TRYPTOPHAN; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; FISH PROTEIN; MYXINIDIN PEPTIDE, MYXINE GLUTINOSA; OLIGOPEPTIDE;

AMINO ACID SEQUENCE; ANTIMICROBIAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG DESIGN; DRUG MECHANISM; DRUG POTENCY; HAGFISH; HUMAN; INFECTION; MYXINE GLUTINOSA; NONHUMAN; PRIORITY JOURNAL; CHEMISTRY; CIRCULAR DICHROISM; DRUG EFFECTS; ESCHERICHIA COLI; KLEBSIELLA PNEUMONIAE; MICROBIAL SENSITIVITY TEST; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PSEUDOMONAS AERUGINOSA; SALMONELLA ENTERICA SEROVAR TYPHI; STAPHYLOCOCCUS AUREUS; STRUCTURE ACTIVITY RELATION; SYNTHESIS;

ANTI-BACTERIAL AGENTS; CIRCULAR DICHROISM; ESCHERICHIA COLI; FISH PROTEINS; KLEBSIELLA PNEUMONIAE; MAGNETIC RESONANCE SPECTROSCOPY; MICROBIAL SENSITIVITY TESTS; OLIGOPEPTIDES; PSEUDOMONAS AERUGINOSA; SALMONELLA TYPHI; STAPHYLOCOCCUS AUREUS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84906077156     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02395-14     Document Type: Article

References (55)

1. Livermore DM. 2009. Has the era of untreatable infections arrived? J. Antimicrob. Chemother. 64(Suppl 1):i29 -i36. http://dx.doi.org/10.1093/jac/ dkp255.
2. Hawkey PM. 2008. The growing burden of antimicrobial resistance. J. Antimicrob. Chemother. 62(Suppl 1):i1-i9. http://dx.doi.org/10.1093/jac/dkn241.
3. Choi KY, Chow LN, Mookherjee N. 2012. Cationic host defence peptides: multifaceted role in immune modulation and inflammation. J. Innate Immun. 4:361-370. http://dx.doi.org/10.1159/000336630.
4. Bowdish DM, Davidson DJ, Hancock RE. 2005. A re-evaluation of the role of host defence peptides in mammalian immunity. Curr. Protein Pept. Sci. 6:35-51. http://dx.doi.org/10.2174/1389203053027494. (Pubitemid 40259800)
5. Zhao X, Wu H, Lu H, Li G, Huang Q. 2013. LAMP: a database linking antimicrobial peptides. PLoS One 8:e66557. http://dx.doi.org/10.1371/journal. pone.0066557.
6. Jenssen H, Hamill P, Hancock RE. 2006. Peptide antimicrobial agents. Clin. Microbiol. Rev. 19:491-511. http://dx.doi.org/10.1128/CMR.00056-05. (Pubitemid 44137212)
7. Wiesner J, Vilcinskas A. 2010. Antimicrobial peptides: the ancient arm of the human immune system. Virulence 1:440-464. http://dx.doi.org/10.4161/viru.1. 5.12983.
8. Zasloff M. 2002. Antimicrobial peptides of multicellular organisms. Nature 415:389-395. http://dx.doi.org/10.1038/415389a. (Pubitemid 34100944)
9. Wang Z, Wang G. 2004. APD: the antimicrobial peptide database. Nucleic Acids Res. 32:D590-D592. http://dx.doi.org/10.1093/nar/gkh025. (Pubitemid 38081727)
10. Seshadri Sundararajan V, Gabere MN, Pretorius A, Adam S, Christoffels A, Lehväslaiho M, Archer JA, Bajic VB. 2012. DAMPD: a manually curated antimicrobial peptide database. Nucleic Acids Res. 40:D1108-D1112. http://dx.doi.org/10.1093/nar/gkr1063.
11. Ellis AE. 2001. Innate host defense mechanisms of fish against viruses and bacteria. Dev. Comp. Immunol. 25:827-839. http://dx.doi.org/10.1016/S0145- 305X(01)00038-6. (Pubitemid 32780993)
12. Masso-Silva J, Diamond G. 2014. Antimicrobial peptides from fish. Pharmaceuticals (Basel) 7:265-310. http://dx.doi.org/10.3390/ph7030265.
13. Rakers S, Niklasson L, Steinhagen D, Kruse C, Schauber J, Sundell K, Paus R. 2013. Antimicrobial peptides (AMPs) from fish epidermis: perspectives for investigative dermatology. J. Invest. Dermatol. 133:1140-1149. http://dx.doi.org/10.1038/jid.2012.503.
14. Subramanian S, Ross NW, MacKinnon SL. 2009. Myxinidin, a novel antimicrobial peptide from the epidermal mucus of hagfish, Myxine glutinosa L. Mar. Biotechnol. (NY) 11:748-757. http://dx.doi.org/10.1007/s10126-009-9189-y.
15. Subramanian S, Ross NW, Mackinnon SL. 2008. Comparison of the biochemical composition of normal epidermal mucus and extruded slime of hagfish (Myxine glutinosa L.). Fish Shellfish Immunol. 25:625-632. http://dx.doi.org/10.1016/j. fsi.2008.08.012.
16. Cantisani M, Leone M, Mignogna E, Kampanaraki K, Falanga A, Morelli G, Galdiero M, Galdiero S. 2013. Structure-activity relations of myxinidin, an antibacterial peptide derived from the epidermal mucus of hagfish. Antimicrob. Agents Chemother. 57:5665-5673. http://dx.doi.org/10.1128/AAC.01341-13.
17. Cunningham BC, Wells JA. 1989. High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis. Science 244:1081-1085. http://dx.doi.org/10.1126/science.2471267. (Pubitemid 19152300)
18. Galdiero S, Capasso D, Vitiello M, D'Isanto M, Pedone C, Galdiero M. 2003. Role of surface-exposed loops of Haemophilus influenzae protein P2 in the mitogen-activated protein kinase cascade. Infect. Immun. 71:2798-2809. http://dx.doi.org/10.1128/IAI.71.5.2798-2809.2003. (Pubitemid 36519894)
19. Chakrabartty A, Kortemme T, Baldwin RL. 1994. Helix propensities of the amino acids measured in alanine-based peptides without helixstabilizing side-chain interactions. Protein Sci. 3:843-852. (Pubitemid 24139910)
20. Galdiero S, Falanga A, Vitiello M, D'Isanto M, Cantisani M, Kampanaraki A, Benedetti E, Browne H, Galdiero M. 2008. Peptides containing membrane-interacting motifs inhibit herpes simplex virus type 1 infectivity. Peptides 29:1461-1471. http://dx.doi.org/10.1016/j.peptides.2008.04.022.
21. Dalvit C. 1998. Efficient multiple-solvent suppression for the study of the interactions of organic solvents with biomolecules. J. Biomol. NMR 11:437-444. http://dx.doi.org/10.1023/A:1008272928075. (Pubitemid 128512224)
22. Wüthrich K. 1986. NMR of proteins and nucleic acids. John Wiley & Sons, New York, NY.
23. Griesinger C, Otting G, Wüthrich K, Ernst RR. 1988. Clean TOCSY for proton spin system identification in macromolecules. J. Am. Chem. Soc. 110:7870-7872. http://dx.doi.org/10.1021/ja00231a044.
24. Kumar A, Ernst RR, Wüthrich K. 1980. A two-dimensional nuclear Overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules. Biochem. Biophys. Res. Commun. 95:1-6. http://dx.doi.org/10.1016/0006-291X(80)90695-6.
25. Piantini U, Sorensen OW, Ernst RR. 1982. Multiple quantum filters for elucidating NMR coupling networks. J. Am. Chem. Soc. 104:6800-6801. http://dx.doi.org/10.1021/ja00388a062.
26. Bartels C, Xia TH, Billeter M, Güntert P, Wüthrich K. 1995. The program XEASY for computer-supported NMR spectral analysis of biological macromolecules. J. Biomol. NMR 6:1-10. http://dx.doi.org/10.1007/BF00417486.
27. Herrmann T, Güntert P, Wüthrich K. 2002. Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol. 319:209-227. http://dx.doi.org/10.1016/S0022-2836(02)00241-3. (Pubitemid 34729497)
28. Koradi R, Billeter M, Wüthrich K. 1996. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:51-55, 29-32.
29. Doreleijers JF, Sousa da Silva AW, Krieger E, Nabuurs SB, Spronk CA, Stevens TJ, Vranken WF, Vriend G, Vuister GW. 2012. CING: an integrated residue-based structure validation program suite. J. Biomol. NMR 54:267-283. http://dx.doi.org/10.1007/s10858-012-9669-7.
30. Doreleijers JF, Vranken WF, Schulte C, Markley JL, Ulrich EL, Vriend G, Vuister GW. 2012. NRG-CING: integrated validation reports of remediated experimental biomolecular NMR data and coordinates in wwPDB. Nucleic Acids Res. 40:D519-D524. http://dx.doi.org/10.1093/nar/gkr1134.
31. Mosmann T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65:55-63. http://dx.doi.org/10.1016/0022-1759(83)90303-4. (Pubitemid 14203433)
32. Ames GF. 1968. Lipids of Salmonella Typhimurium and Escherichia coli: structure and metabolism. J. Bacteriol. 95:833-843.
33. Buck M. 1998. Trifluoroethanol and colleagues: cosolvents come of age. Recent studies with peptides and proteins. Q. Rev. Biophys. 31:297-355. (Pubitemid 29213772)
34. Wishart DS, Sykes BD, Richards FM. 1991. Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J. Mol. Biol. 222:311-333. http://dx.doi.org/10.1016/0022-2836(91)90214-Q. (Pubitemid 121004009)
35. Jiang Z, Vasil AI, Gera L, Vasil ML, Hodges RS. 2011. Rational design of α-helical antimicrobial peptides to target Gram-negative pathogens, Acinetobacter baumannii and Pseudomonas aeruginosa: utilization of charge, 'specificity determinants,' total hydrophobicity, hydrophobe type and location as design parameters to improve the therapeutic ratio. Chem. Biol. Drug Des. 77:225-240. http://dx.doi.org/10.1111/j.1747-0285.2011.01086.x.
36. Hawrani A, Howe RA, Walsh TR, Dempsey CE. 2008. Origin of low mammalian cell toxicity in a class of highly active antimicrobial amphipathic helical peptides. J. Biol. Chem. 283:18636-18645. http://dx.doi.org/10.1074/jbc. M709154200.
37. Juretić D, Vukičević D, Ilić N, Antcheva N, Tossi A. 2009. Computational design of highly selective antimicrobial peptides. J. Chem. Infect. Model. 49:2873-2882. http://dx.doi.org/10.1021/ci900327a.
38. Giangaspero A, Sandri L, Tossi A. 2001. Amphipathic alpha-helical antimicrobial peptides. Eur. J. Biochem. 268:5589-5600. http://dx.doi.org/10. 1046/j.1432-1033.2001.02494.x.
39. Tossi A, Sandri L, Giangaspero A. 2000. Amphipathic, alpha-helical antimicrobial peptides. Biopolymers 55:4-30. http://dx.doi.org/10.1002/1097- 0282(2000)55:1〈4::AID-BIP30〉3.0.CO;2-M.
40. Galdiero S, Russo L, Falanga A, Cantisani M, Vitiello M, Fattorusso R, Malgieri G, Galdiero M, Isernia C. 2012. Structure and orientation of the gH625-644 membrane interacting region of herpes simplex virus type 1 in a membrane mimetic system. Biochemistry 51:3121-3128. http://dx.doi.org/10.1021/ bi201589m.
41. Falanga A, Tarallo R, Vitiello G, Vitiello M, Perillo E, Cantisani M, D'Errico G, Galdiero M, Galdiero S. 2012. Biophysical characterization and membrane interaction of the two fusion loops of glycoprotein B from herpes simplex type I virus. PLoS One 7:e32186. http://dx.doi.org/10.1371/journal.pone. 0032186.
42. Falanga A, Cantisani M, Pedone C, Galdiero S. 2009. Membrane fusion and fission: enveloped viruses. Protein Pept. Lett. 16:751-759. http://dx.doi.org/ 10.2174/092986609788681760.
43. Dempsey CE, Hawrani A, Howe RA, Walsh TR. 2010. Amphipathic antimicrobial peptides-from biophysics to therapeutics? Protein Pept. Lett. 17:1334-1344. http://dx.doi.org/10.2174/0929866511009011334.
44. Matsuzaki K. 2009. Control of cell selectivity of antimicrobial peptides. Biochim. Biophys. Acta 1788:1687-1692. http://dx.doi.org/10.1016/j.bbamem.2008. 09.013.
45. Bhargava K, Feix JB. 2004. Membrane binding, structure, and localization of cecropin-mellitin hybrid peptides: a site-directed spin-labeling study. Biophys. J. 86:329-336. http://dx.doi.org/10.1016/S0006-3495(04)74108-9. (Pubitemid 38067460)
46. Turner J, Cho Y, Dinh NN, Waring AJ, Lehrer RI. 1998. Activities of LL-37, a cathelin-associated antimicrobial peptide of human neutrophils. Antimicrob. Agents Chemother. 42:2206-2214. (Pubitemid 28420351)
47. Ladokhin AS, White SH. 1999. Folding of amphipathic α-helices on membranes: energetics of helix formation by melittin. J. Mol. Biol. 285:1363-1369. http://dx.doi.org/10.1006/jmbi.1998.2346. (Pubitemid 29060439)
48. Matsuzaki K, Nakamura A, Murase O, Sugishita K, Fujii N, Miyajima K. 1997. Modulation of magainin 2-lipid bilayer interactions by peptide charge. Biochemistry 36:2104-2111. http://dx.doi.org/10.1021/bi961870p.
49. Ma QQ, Shan AS, Dong N, Gu Y, Sun WY, Hu WN, Feng XJ. 2011. Cell selectivity and interaction with model membranes of Val/Arg-rich peptides. J. Pept. Sci. 17:520-526. http://dx.doi.org/10.1002/psc.1360.
50. Wilman RH, Jiye S, Deane MC. 2014. Helix kinks are equally prevalent in soluble and membrane proteins. Proteins Struct. Funct. Bioinform., in press. http://dx.doi.org/10.1002/prot.24550.
51. Scudiero O, Galdiero S, Cantisani M, Di Noto R, Vitiello M, Galdiero M, Naclerio G, Cassiman JJ, Pedone C, Castaldo G. 2010. Novel synthetic, salt-resistant analogs of human beta-defensins 1 and 3 endowed with enhanced antimicrobial activity. Antimicrob. Agents Chemother. 54:2312-2322. http://dx.doi.org/10.1128/AAC.01550-09.
52. Pasupuleti M, Walse B, Svensson B, Malmsten M, Schmidtchen A. 2008. Rational design of antimicrobial C3a analogues with enhanced effects against staphylococci using an integrated structure and function-based approach. Biochemistry 47:9057-9070. http://dx.doi.org/10.1021/bi800991e.
53. Scudiero O, Galdiero S, Nigro E, Del Vecchio L, Di Noto R, Cantisani M, Colavita I, Galdiero M, Cassiman JJ, Daniele A, Pedone C, Salvatore F. 2013. Chimeric beta-defensin analogs, including the novel 3NI analog, display salt-resistant antimicrobial activity and lack toxicity in human epithelial cell lines. Antimicrob. Agents Chemother. 57:1701-1708. http://dx.doi.org/10.1128/ AAC.00934-12.
54. Harder J. 2001. Isolation and characterization of human beta-defensin3, a novel human inducible peptide antibiotic. J. Biol. Chem. 276:5707-5713. http://dx.doi.org/10.1074/jbc.M008557200.
55. Epand RF, Pollard JE, Wright JO, Savage PB, Epand RM. 2010. Depolarization, bacterial membrane composition, and the antimicrobial action of ceragenins. Antimicrob. Agents Chemother. 54:3708-3713. http://dx.doi.org/10. 1128/AAC.00380-10. della Ricerca