Micelle-bound structures and dynamics of the hinge deleted analog of melittin and its diastereomer: Implications in cell selective lysis by d-amino acid containing antimicrobial peptides

Biochimica et Biophysica Acta - Biomembranes

Volumn 1798, Issue 2, 2010, Pages 128-139

  Saravanan, Rathi ^a   Bhunia, Anirban ^a   Bhattacharjya, Surajit ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

AMPs; Antibiotic resistance; Antimicrobial peptide; Helical AMPs; Melittin

Indexed keywords

DODECYLPHOSPHORYLCHOLINE; GLUTAMINE; LEUCINE; MELITTIN; MELITTIN H; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG; VALINE;

ANTIBACTERIAL ACTIVITY; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOLYSIS; DIASTEREOISOMER; DRUG CONFORMATION; DRUG SELECTIVITY; DRUG STRUCTURE; ESCHERICHIA COLI; GENE DELETION; HEMOLYSIS; HUMAN; HUMAN CELL; MICELLE; MINIMUM INHIBITORY CONCENTRATION; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS;

ANIMALS; ERYTHROCYTES; HEMOLYSIS; HUMANS; MELITTEN; MICELLES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, SECONDARY; STRUCTURE-ACTIVITY RELATIONSHIP;

APIS MELLIFERA; EUKARYOTA;

EID: 74249119746     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2009.07.014     Document Type: Article

References (62)

1. Boman H.G. Peptide antibiotics and their role in innate immunity. Annu. Rev. Immunol. 13 (1995) 61-92
2. Zelezetsky I., and Tossi A. Alpha-helical antimicrobial peptides-using a sequence template to guide structure-activity relationship studies. Biochim. Biophys. Acta 1758 (2006) 1436-1449
3. Epand R.M., and Vogel H.J. Diversity of antimicrobial peptides and their mechanisms of action. Biochim. Biophys. Acta 1462 (1999) 11-28
4. Hancock R.E. Cationic peptides: effectors in innate immunity and novel antimicrobials. Lancet Infect. Dis. 1 (2001) 156-164
5. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 415 (2002) 389-395
6. Dürr U., Sudheendra U.S., and Ramamoorthy A. LL-37, the only human member of the cathelicidin family of antimicrobial peptides. Biochim. Biophys. Acta 1758 (2006) 1408-1425
7. Dhople V., Krukemeyer A., and Ramamoorthy A. The human beta-defensin-3, an antibacterial peptide with multiple biological functions. Biochim. Biophys. Acta 1758 (2006) 1499-1512
8. Bechinger B., and Lohner K. Detergent-like actions of linear amphipathic cationic antimicrobial peptides. Biochim. Biophys. Acta 1758 (2006) 1529-1539
9. Sato H., and Feix J.B. Peptide-membrane interactions and mechanisms of membrane destruction by amphipathic alpha-helical antimicrobial peptides. Biochim. Biophys. Acta 1758 (2006) 1245-1256
10. Ramamoorthy A. Beyond NMR spectra of antimicrobial peptides: dynamical images at atomic resolution and functional insights. Solid State Nucl. Magn. Reson. 35 4 (2009) 201-207
11. Ramamoorthy A., Lee D., Santos J.S., and Henzler-Wildman K.A. Nitrogen-14 solid-state NMR spectroscopy of aligned phospholipid bilayers to probe peptide-lipid interaction and oligomerization of membrane associated peptides. J. Am. Chem. Soc. 130 (2008) 11023-11029
12. Tossi A., Sandri L., and Giangaspero A. Amphipathic, alpha-helical antimicrobial peptides. Biopolymers 55 (2000) 4-30
13. Jenssen H., Hamill P., and Hancock R.E. Peptide antimicrobial agents. Clin. Microbiol. Rev. 19 (2006) 491-511
14. Shai Y. Mode of action of membrane active antimicrobial peptides. Biopolymers 66 (2002) 236-248
15. Gottler L.M., and Ramamoorthy A. Structure, membrane orientation, mechanism, and function of pexiganan-a highly potent antimicrobial peptide designed from magainin. Biochim. Biophys. Acta 1788 8 (2009) 1680-1686
16. Blondelle S.E., and Lohner K. Combinatorial libraries: a tool to design antimicrobial and antifungal peptide analogues having lytic specificities for structure-activity relationship studies. Biopolymers 55 (2000) 74-87
17. Oh J.E., Hong S.Y., and Lee K.H. Structure-activity relationship study: short antimicrobial peptides. J. Pept. Res. 53 (1999) 41-46
18. Sitaram N., and Nagaraj R. Interaction of antimicrobial peptides with biological and model membranes: structural and charge requirements for activity. Biochim. Biophys. Acta 1462 (1999) 29-54
19. Habermann E. Bee and wasp venoms. Science 177 (1972) 314-322
20. Raghuraman H., and Chattopadhyay A. Melittin: a membrane-active peptide with diverse functions. Biosci. Rep. 27 (2007) 189-223
21. Dempsey C.E. The actions of melittin on membranes. Biochim. Biophys. Acta 1031 (1990) 143-161
22. Matsuzaki K., Yoneyama S., and Miyajima K. Pore formation and translocation of melittin. Biophys. J. 73 (1997) 831-838
23. Rex S., and Schwarz G. Quantitative studies on the melittin-induced leakage mechanism of lipid vesicles. Biochemistry 37 (1998) 2336-2345
24. Lee M.T., Hung W.C., Chen F.Y., and Huang H.W. Mechanism and kinetics of pore formation in membranes by water-soluble amphipathic peptides. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 5087-5092
25. van den Bogaart G., Guzman J.V., Mika J.T., and Poolman B. On the mechanism of pore formation by melittin. J. Biol. Chem. 283 (2008) 33854-33857
26. Ladokhin A.S., and White S.H. Folding of amphipathic alpha-helices on membranes: energetics of helix formation by melittin. J. Mol. Biol. 285 (1999) 1363-1369
27. Blondelle S.E., and Houghten R.A. Hemolytic and antimicrobial activities of the twenty-four individual omission analogues of melittin. Biochemistry 30 (1991) 4671-4678
28. Blondelle S.E., Simpkins L.R., Perez-Paya E., and Houghten R.A. Influence of tryptophan residues on melittin's hemolytic activity. Biochim. Biophys. Acta 1202 (1993) 331-336
29. Subbalakshmi C., Nagaraj R., and Sitaram N. Biological activities of C-terminal 15-residue synthetic fragment of melittin: design of an analog with improved antibacterial activity. FEBS Lett. 448 (1999) 62-66
30. Asthana N., Yadav S.P., and Ghosh J.K. Dissection of antibacterial and toxic activity of melittin: a leucine zipper motif plays a crucial role in determining its hemolytic activity but not antibacterial activity. J. Biol. Chem. 279 (2004) 55042-55050
31. Zhu W.L., Song Y.M., Park Y., Park K.H., Yang S.T., Kim J.I., Park I.S., Hahm K.S., and Shin S.Y. Substitution of the leucine zipper sequence in melittin with peptoid residues affects self-association, cell selectivity, and mode of action. Biochim. Biophys. Acta 1768 (2007) 1506-1517
32. Boman H.G., Wade D., Boman I.A., Wahlin B., and Merrifield R.B. Antibacterial and antimalarial properties of peptides that are cecropin-melittin hybrids. FEBS Lett. 259 (1989) 103-106
33. Friedrich C., Scott M.G., Karunaratne N., Yan H., and Hancock R.E. Salt-resistant alpha-helical cationic antimicrobial peptides. Antimicrob. Agents. Chemother. 43 (1999) 1542-1548
34. Porcelli F., Buck-Koehntop B.A., Thennarasu S., Ramamoorthy A., and Veglia G. Structures of the dimeric and monomeric variants of magainin antimicrobial peptides (MSI-78 and MSI-594) in micelles and bilayers, determined by NMR spectroscopy. Biochemistry 45 (2006) 5793-5799
35. Ramamoorthy A., Thennarasu S., Lee D.K., Tan A., and Maloy L. Solid-state NMR investigation of the membrane-disrupting mechanism of antimicrobial peptides MSI-78 and MSI-594 derived from magainin 2 and melittin. Biophys. J. 91 (2006) 206-216
36. Oren Z., Hong J., and Shai Y. A repertoire of novel antibacterial diastereomeric peptides with selective cytolytic activity. J. Biol. Chem. 272 (1997) 14643-14649
37. Oren Z., and Shai Y. Selective lysis of bacteria but not mammalian cells by diastereomers of melittin: structure-function study. Biochemistry 36 (1997) 1826-1835
38. Papo N., and Shai Y. Exploring peptide membrane interaction using surface plasmon resonance: differentiation between pore formation versus membrane disruption by lytic peptides. Biochemistry 42 (2003) 458-466
39. Sharon M., Oren Z., Shai Y., and Anglister J. 2D-NMR and ATR-FTIR study of the structure of a cell-selective diastereomer of melittin and its orientation in phospholipids. Biochemistry 38 (1999) 15305-15316
40. Kondejewski L.H., Jelokhani-Niaraki M., Farmer S.W., Lix B., Kay C.M., Sykes B.D., Hancock R.E., and Hodges R.S. Dissociation of antimicrobial and hemolytic activities in cyclic peptide diastereomers by systematic alterations in amphipathicity. J. Biol. Chem. 274 (1999) 13181-13192
41. Shai Y., and Oren Z. Diastereoisomers of cytolysins, a novel class of potent antibacterial peptides. J. Biol. Chem. 271 (1996) 7305-7308
42. Wang G. Determination of solution structure and lipid micelle location of an engineered membrane peptide by using one NMR experiment and one sample. Biochim. Biophys. Acta 1768 (2007) 3271-3281
43. Terwilliger T.C., and Eisenberg D. The structure of melittin. I. Structure determination and partial refinement. J. Biol. Chem. 257 (1982) 6010-6015
44. Inagaki F., Shimada I., Kawaguchi K., Hirano M., Terasawa I., Ikura T., and Go N. Structure of melittin bound to perdeuterated dodecylphosphocholine micelles as studied by two-dimensional NMR and distance geometry calculations. Biochemistry 28 (1989) 5985-5991
45. Bechinger B. The structure, dynamics and orientation of antimicrobial peptides in membranes by multidimensional solid-state NMR spectroscopy. Biochim. Biophys. Acta 1462 (1999) 157-183
46. 13C NMR spectroscopy. Biophys. J. 78 (2000) 2405-2417
47. Bazzo R., Tappin M.J., Pastore A., Harvey T.S., Carver J.A., and Campbell I.D. The structure of melittin. A 1H-NMR study in methanol. Eur. J. Biochem. 173 (1988) 139-146
48. Bhattacharjya S., Venkatraman J., Kumar A., and Balaram P. Fluoroalcohols as structure modifiers in peptides and proteins: hexafluoroacetone hydrate stabilizes a helical conformation of melittin at low pH. J. Pept. Res. 54 (1999) 100-111
49. Bhunia A., Domadia P.N., and Bhattacharjya S. Structural and thermodynamic analyses of the interaction between melittin and lipopolysaccharide. Biochim. Biophys. Acta 1768 (2007) 3282-3291
50. Porcelli F., Buck B., Lee D.K., Hallock K.J., Ramamoorthy A., and Veglia G. Structure and orientation of pardaxin determined by NMR experiments in model membranes. J. Biol. Chem. 279 (2004) 45815-45823
51. Porcelli F., Verardi R., Shi L., Henzler-Wildman K.A., Ramamoorthy A., and Veglia G. NMR structure of the cathelicidin-derived human antimicrobial peptide LL-37 in dodecylphosphocholine micelles. Biochemistry 47 (2008) 5565-5572
52. Traaseth N.J., Verardi R., Torgersen K.D., Karim C.B., Thomas D.D., and Veglia G. Spectroscopic validation of the pentameric structure of phospholamban. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 14676-14681
53. Ferre R., Badosa E., Feliu L., Planas M., Montesinos E., and Bardaji E. Inhibition of plant-pathogenic bacteria by short synthetic cecropin A-melittin hybrid peptides. Appl. Environ. Microbiol. 72 (2006) 3302-3308
54. Bhunia A., Domadia P.N., Mohanram H., and Bhattacharjya S. NMR structural studies of the Ste11 SAM domain in the dodecyl phosphocholine micelle. Proteins 74 (2009) 328-343
55. Bhattacharjya S., Xu P., Xiang H., Chretien M., Seidah N.G., and Ni F., pH-induced conformational transitions of a molten-globule-like state of the inhibitory prodomain of furin: implications for zymogen activation. Protein Sci. 10 (2001) 934-942
56. Guntert P., Mumenthaler C., and Wuthrich K. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273 (1997) 283-298
57. Cornilescu G., Delaglio F., and Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13 (1999) 289-302
58. K Wuthrich, NMR of proteins and nucleic acids (1986).
59. Wishart D.S., Sykes B.D., and Richards F.M. Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J. Mol. Biol. 222 (1991) 311-333
60. Dempsey C.E., Bazzo R., Harvey T.S., Syperek I., Boheim G., and Campbell I.D. Contribution of proline-14 to the structure and actions of melittin. FEBS Lett. 281 (1991) 240-244
61. Dempsey C.E., and Sternberg B. Reversible disc-micellization of dimyristoylphosphatidylcholine bilayers induced by melittin and [Ala-14]melittin. Biochim. Biophys. Acta 1061 (1991) 175-184
62. Rex S. A Pro->Ala substitution in melittin affects self-association, membrane binding and pore-formation kinetics due to changes in structural and electrostatic properties. Biophys. Chem. 85 (2000) 209-228