Structure of the lipodepsipeptide syringomycin e in phospholipids and sodium dodecylsulphate micelle studied by circular dichroism, NMR spectroscopy and molecular dynamics

Biochimica et Biophysica Acta - Biomembranes

Volumn 1808, Issue 9, 2011, Pages 2102-2110

  Anselmi, Massimiliano ^a   Eliseo, Tommaso ^b   Zanetti Polzi, Laura ^a   Fullone, Maria Rosaria ^a   Fogliano, Vincenzo ^c   Di Nola, Alfredo ^a   Paci, Maurizio ^b   Grgurina, Ingeborg ^a,c  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Antifungal lipodepsipeptide; Molecular dynamics; NMR spectroscopy; Phospholipid; SDS micelle; Syringomycin E conformation

Indexed keywords

DEPSIPEPTIDE; DODECYL SULFATE SODIUM; LIPODEPSIPEPTIDE; OCTANE; SYRINGOMYCIN E; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; MICELLE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHOLIPID BILAYER; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PSEUDOMONAS SYRINGAE;

ANTIFUNGAL AGENTS; CIRCULAR DICHROISM; HEMOLYSIS; HYDROGEN BONDING; ION CHANNELS; LIPIDS; MAGNETIC RESONANCE SPECTROSCOPY; MICELLES; MOLECULAR DYNAMICS SIMULATION; PEPTIDES, CYCLIC; PHOSPHOLIPIDS; PROTEIN CONFORMATION; RIFAMPIN; SODIUM DODECYL SULFATE; WATER;

PSEUDOMONAS SYRINGAE PV. SYRINGAE;

EID: 79960018840     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.04.018     Document Type: Article

References (61)

1. A. Segre, R.C. Bachmann, A. Ballio, F. Bossa, I. Grgurina, N.S. Iacobellis, G. Marino, P. Pucci, M. Simmaco, and J.Y. Takemoto The structure of syringomycins A1, E and G FEBS Lett. 255 1989 27 31
2. N. Fukuchi, A. Isogai, J. Nakayama, S. Takayama, S. Yamashita, K. Suyama, J.Y. Takemoto, and A. Suzuki Structure and stereochemistry of three phytotoxins syringomycin, syringostatin and syringotoxin produced by Pseudomonas syringae pv. syringae J. Chem. Perkin. Trans. 1 1992 1149 1157
3. A. Scaloni, R.C. Bachmann, J.Y. Takemoto, D. Barra, M. Simmaco, and A. Ballio Stereochemical structure of syringomycin, a phytotoxic metabolite of Pseudomonas syringae pv. syringae Nat. Prod. Lett. 4 1994 159 164 (Pubitemid 24216227)
4. A. Ballio, F. Bossa, A. Collina, M. Gallo, N.S. Iacobellis, M. Paci, P. Pucci, A. Scaloni, A. Segre, and M. Simmaco Structure of syringotoxin, a bioactive metabolite of Pseudomonas syringae pv. syringae FEBS Lett. 269 1990 377 380 (Pubitemid 20273830)
5. A. Ballio, F. Bossa, D. Di Giorgio, P. Ferranti, M. Paci, P. Pucci, A. Scaloni, A.L. Segre, and G.A. Strobel Novel bioactive lipodepsipeptides from Pseudomonas syringae: the pseudomycins FEBS Lett. 355 1994 96 100 (Pubitemid 24352110)
6. B.K. Scholz-Schroeder, M.L. Hutchison, I. Grgurina, and D.C. Gross The contribution of syringopeptin and syringomycin to virulence of Pseudomonas syringae pv. syringae strain B 301 D on the basis of sypA and syrB1 biosynthesis mutant analysis Mol. Plant Microbe Interact. 14 2001 336 348 (Pubitemid 32176728)
7. N.S. Iacobellis, P. Lavermicocca, I. Grgurina, M. Simmaco, and A. Ballio Phytotoxic properties of Pseudomonas syringae pv. syringae toxins Physiol. Mol. Plant Pathol. 40 1992 107 116
8. I. Grgurina, A. Barca, S. Cervigni, M. Gallo, A. Scaloni, and P. Pucci Relevance of chlorine-substituent for the antifugal activity of syringomycin and syringotoxin, metabolites of the phytopathogenic bacterium Pseudomonas syringae pv. syringae Experientia 50 1994 130 133 (Pubitemid 24086628)
9. C.T. Bull, M.L. Wadsworth, K.M. Sorensen, J.Y. Takemoto, R.K. Austin, and J.L. Smilanick Syringomycin E produced by biological control agents controls green mold on lemons Biol. Control 12 1998 89 95 (Pubitemid 28305679)
10. A.J. De Lucca, T.J. Jacks, J.Y. Takemoto, B. Vinyard, J. Peter, E. Navarro, and T.J. Walsh Fungal lethality, binding, and cytotoxicity of syringomycin-E Antimicrob. Agents Chemother. 43 1999 371 373 (Pubitemid 29079176)
11. A.J. De Lucca, and T.J. Walsh Antifungal peptides: novel therapeutic compounds against emerging pathogens Antimicrob. Agents Chemother. 43 1999 1 11 (Pubitemid 29069190)
12. K.N. Sorensen, A.A. Wangstrom, S.D. Allen, and J.Y. Takemoto Efficacy of syringomycin E in a murine model of vaginal candidiasis J. Antibiot. 51 1998 743 749 (Pubitemid 28432866)
13. M.L. Hutchison, and D.C. Gross Lipopeptide phytotoxin produced by Pseudomonas syringae pv. syringae: comparison of the biosurfactant and ion channel-forming activities of syringopeptin and syringomycin Mol. Plant Microbe Interact. 10 1997 347 354 (Pubitemid 27165137)
14. M. Dalla Serra, G. Fagiuoli, P. Nordera, I. Bernhart, C. Della Volpe, D. Di Giorgio, A. Ballio, and G. Menestrina The interaction of lipodepsipeptide toxins from Pseudomonas syringae pv. syringae with biological membranes: a comparison of syringotoxin, syringomycin, and two syringopeptins Mol. Plant Microbe Interact. 5 1999 391 400 (Pubitemid 29194709)
15. K. Blasko, L.V. Schagina, G. Agner, Y.A. Kaulin, and Y. Takemoto Membrane sterol composition modulates the pore forming activity of syringomycin E in human red blood cells Biochim. Biophys. Acta 1373 1998 163 169 (Pubitemid 28495677)
16. G. Agner, Y.A. Kaulin, P.A. Gurnev, Z. Szabo, L.V. Schagina, J.Y. Takemoto, and K. Blasko Membrane-permeabilizing activities of cyclic lipodepsipeptides, syringopeptin 22A and syringomycin E from Pseudomonas syringae pv. syringae in human red blood cells and in bilayer lipid membranes Bioelectrochemistry 52 2000 161 167
17. D. Di Giorgio, P. Lavermicocca, C. Marchiafava, L. Camoni, G. Surico, and A. Ballio Effect of syringomycin E and syringopeptins on isolated plant mitochondria Physiol. Mol. Plant Pathol. 48 1996 325 334 (Pubitemid 126746006)
18. P. Cliften, Y. Wang, D. Mochizuchi, T. Miyakawa, R. Wangspa, J. Hughes, and J.Y. Takemoto Syr2, a gene necessary for syringomycin growth inhibition of Saccharomyces cerevisiae Microbiology 142 1996 477 484 (Pubitemid 26093633)
19. M.M. Grilley, S.D. Stock, R.C. Dickson, R.L. Lester, and J.Y. Takemoto Syringomycin action gene SYR2 is essential for sphingolipid 4-hydroxylation in Saccharomyces cerevisiae J. Biol. Chem. 273 1998 11062 11068 (Pubitemid 28204951)
20. H. Hama, D.A. Young, J.A. Radding, D. Ma, J. Tang, S.D. Stock, and J.Y. Takemoto Requirement of sphingolipid β-hydroxylation for fungicidal action of syringomycin E FEBS Lett. 478 2000 26 28 (Pubitemid 30462252)
21. S.D. Stock, H. Hama, J.A. Radding, D.A. Young, and J.Y. Takemoto Syringomycin E inhibition of Saccharomyces cerevisiae: requirement for biosynthesis of sphingolipids with very-long-chain fatty acids and mannose- and phosphoinositol-containing head groups Antimicrob. Agents Chemother. 44 2000 1174 1180 (Pubitemid 30228291)
22. N. Taguchi, Y. Takano, C. Julmanop, Y. Wang, S.D. Stock, J.Y. Takemoto, and T. Miyakawa Identification and analysis of the Saccharomyces cerevisiae SYR1 gene reveals that ergosterol is involved in the action of syringomycin Microbiology 140 1994 353 359 (Pubitemid 24090602)
23. J.Y. Takemoto, Y. Yu, S.D. Stock, and T. Miyakawa Yeast genes involved in growth inhibition by Pseudomonas syringae pv. syringae syringomycin family lipodepsipeptides FEMS Microbiol. Lett. 114 1993 339 342 (Pubitemid 23360621)
24. 2+ transport J. Gen. Microbiol. 137 1991 653 659
25. A.M. Feigin, L.V. Schagina, J.Y. Takemoto, J.H. Teeter, and J.G. Brand The effect of sterol on the sensitivity of membranes to the channel-forming antifungal antibiotic, syringomycin E Biochim. Biophys. Acta 1324 1997 102 110 (Pubitemid 27076766)
26. Y.A. Kaulin, J.Y. Takemoto, L.V. Schagina, O.S. Ostroumova, R. Wangspa, J.H. Teeter, and J.G. Brand Sphingolipids influence the sensitivity of lipid bilayers to fungicide, syringomycin E J. Bioenerg. Biomembr. 37 2005 339 348 (Pubitemid 41778773)
27. A.M. Feigin, J.Y. Takemoto, R. Wangspa, J.H. Teeter, and J.G. Brand Properties of voltage-gated ion channels formed by syringomycin E in planar lipid bilayers J. Membr. Biol. 149 1996 41 47 (Pubitemid 26048769)
28. V.V. Malev, L.V. Schagina, P.A. Gurnev, J.Y. Takemoto, E.M. Nestorovich, and S.M. Bezrukov Syringomycin E channel: a lipidic pore stabilized by lipopeptide? Biophys. J. 2002 1985 1994 (Pubitemid 34280813)
29. O.S. Ostroumova, P.A. Gurnev, L.V. Schagina, and S.M. Bezrukov Asymmetry of syringomycin E channel studied by polymer partitioning FEBS Lett. 581 2007 804 808
30. O.S. Ostroumova, Y.A. Kaulin, and L.V. Schagina Effect of agents modifying the membrane dipole potential on properties of syringomycin E channels Langmuir 23 2007 6889 6892 (Pubitemid 47143204)
31. Z. Szabó, M. Budai, K. Blasko, and P. Grof Molecular dynamics of the cyclic lipodepsipeptides' action on model membranes: effects of syringopeptin 22A, syringomycin E, and syringotoxin studied by EPR technique Biochim. Biophys. Acta 1660 1-2 2004 118 130 (Pubitemid 38125238)
32. E. Matyus, L. Monticelli, K.E. Kover, Z. Xu, K. Blasko, J. Fidy, and D.P. Tieleman Structural investigation of syringomycin-E using molecular dynamics simulation and NMR Eur. Biophys. J. 35 2006 459 467 (Pubitemid 44043062)
33. F. Abbassi, C. Galanth, M. Amiche, K. Saito, C. Piesse, L. Zargarian, K. Hani, P. Nicolas, O. Lequin, and A. Ladram Solution structure and model membrane interactions of temporins-SH, antimicrobial peptides from amphibian skin-a NMR spectroscopy and differential scanning calorimetry study Biochemistry 47 2008 10513 10525
34. L.T. Nguyen, D.J. Schibli, and H.J. Vogel Structural studies and model membrane interaction of two peptides derived from bovine lacoferrine J. Pept. Sci. 11 2005 379 389 (Pubitemid 40959938)
35. D.J. Schibli, L.T. Nguyen, S.D. Kernagan, O. Redkal, and H.J. Vogel Structure-function analysis of tripticin analogues: relationships between antimicrobial activities, model membrane interactions, and their micelle-bound NMR structures Biophys. J. 91 2006 4413 4426 (Pubitemid 44904228)
36. A. Rozek, C.L. Friedrich, and R.E.W. Hancock Structure of bovine antimicrobial peptide indolicin bound to dodecylphosphocoline and sodium dodecylsulfate micelles Biochemistry 39 2000 15765 15774 (Pubitemid 32040945)
37. I. Grgurina, and F. Mariotti Biosynthetic origin of syringomycin and syringopeptin 22, toxic secondary metabolites of the phytopathogenic bacterium Pseudomonas syringae pv. syringae FEBS Lett. 462 1999 151 154
38. L. Rigaud, A. Bluzat, and S. Buschlen Incorporation of bacteriorhodopsin into large unilamellar liposomes by reverse phase evaporation Biochem. Biophys. Res. Commun. 111 1983 373 382
39. 1HNMR study Biochemistry 34 1995 11617 11624
40. W.F. van Gunsteren, S. Billeter, A. Eising, P. Hunenberger, P. Kruger, A.E. Mark, W. Scott, and I. Tironi Biomolecular simulations: The GROMOS 96 Manual and user guide 1996 BIOMOS bv Zurich, Groningen
41. B. Hess, H. Bekker, H.J.C. Berendsen, and J.G.E.M. Fraaije LINCS: a linear constraint solver for molecular simulations J. Comput. Chem. 18 1997 1463 1472 (Pubitemid 127637344)
42. D. Van der Spoel, R. Van Drunen and H.J.C. Berendsen, GROningen Machine for chemical simulation. Department of Biophysical Chemistry, BIOSON Research Institute, Nijeborgh 4 NL-9717 AG, Groningen.
43. T. Darden, D. York, and L. Pedersen Particle Mesh Ewald: an N Log (N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
44. D. Brown, and J.H.L. Clark A comparison of constant energy, constant temperature and constant pressure ensembles in molecular dynamics simulations of atomic liquids Mol. Phys. 51 1984 1243 1252
45. A. Ballio, A. Collina, A. Di Nola, C. Manetti, M. Paci, and A.L. Segre Determination of structure and conformation in solution of syringotoxin, a lipodepsipeptide from Pseudomonas syringae pv. syringae by 2D NMR and molecular dynamics Struct. Chem. 5 1994 43 50
46. A. Ballio, F. Bossa, D. Di Giorgio, A. Di Nola, C. Manetti, M. Paci, A. Scaloni, and A.L. Segre Solution conformation of the Pseudomonas syringae pv. syringae phytotoxic lipodepsipeptide SP25A: 2D NMR, distance geometry and molecular dynamics Eur. J. Biochem. 234 1995 747 758 (Pubitemid 26024331)
47. V.M. Coiro, A.L. Segre, A. Di Nola, M. Paci, A. Grottesi, G. Veglia, and A. Ballio Solution conformation of the Pseudomonas syringae MSU 16H phytotoxic lipodepsipeptide pseudomycin A determined by computer simulations using distance geometry and molecular dynamics from NMR data Eur. J. Biochem. 257 1998 449 456 (Pubitemid 28489492)
48. S. Baré, V. Coiro, A. Scaloni, A. Di Nola, M. Paci, A. Segre, and A. Ballio Conformations in solution of the fuscopeptins, phytotoxic metabolites of Pseudomonas fuscovaginae Eur. J. Biochem. 266 1999 1 10
49. A. Scaloni, M. Dalla Serra, P. Amodeo, L. Mannina, R.M. Vitale, A.L. Segre, O. Cruciani, F. Lodovichetti, M.L. Greco, A. Fiore, M. Gallo, C. D'Ambrosio, M. Coraiola, G. Menestrina, A. Graniti, and V. Fogliano Structure, conformation and biological activity of a novel lipodepsipeptide from Pseudomonas corrugata: cormycin A Biochem. J. 384 2004 25 36 (Pubitemid 39564158)
50. E. Matyus, K. Blasko, J. Fidy, and D.P. Tielman Structure and dynamics of the antifungal molecules syringotoxin-B and syringopeptin-25A from molecular dynamics simulation Eur. Biophys. J. 37 2008 495 502
51. C.A.G. Hassnoot, F.A.A.M. Leeuw, and A. Altona The relationship between proton-proton NMR coupling constants and substituent electronegativities: an empirical generalization of the Karplus equation Tetrahedron 36 1998 2783 2792
52. E. Vaillo, A. Ballio, P.L. Luisi, and R.M. Thomas The spectroscopic properties of the lipodepsipeptide syringomycin E Biopolymers 32 1992 1317 1326
53. R.J. Mortishire-Smith, J.C. Nutkins, L.C. Packman, C.L. Brodey, P.B. Rainey, K. Johnstone, and D.H. Williams Determination of the structure of an extracellular peptide produced by mushroom saprotroph Pseudomonas reactans Tetrahedron 47 1991 3647 3654
54. A. Carotenuto, S. Malfi, M.R. Saviello, P. Campiglia, I. Gomez-Monterrey, M.L. Mangoni, L. Marcellini Ercolani Gaddi, E. Novellino, and P. Grieco A different molecular mechanism underlying antimicrobial and haemolytic actions of temporins A and L J. Med. Chem. 51 2008 2354 2362 (Pubitemid 351628497)
55. E.F. Haney, F. Lau, and H.J. Vogel Solution structures and model membrane interactions of lactoferrampin, an antimicrobial peptide derived from bovine lactoferrin Biochem. Biophys. Acta 1768 2007 2355 2364 (Pubitemid 47532018)
56. M.R. Saviello, S. Malfi, P. Campiglia, A. Cavalli, P. Grieco, E. Novellino, and A. Carotenuto New insight into the mechanism of action of the temporin antimicrobial peptides Biochemistry 49 2010 1477 1485
57. N. Papo, Z. Orent, U. Pag, H.G. Sahl, and Y. Shai The consequence of sequence alteration of an amphipathic α-helical antimicrobial peptide and its diastereomers J. Biol. Chem. 277 2002 33913 33921
58. L.H. Kondejewski, M. Jelokhani-Niaraki, S.W. Farmer, B. Lix, C.M. Kay, B.D. Sykes, R.E.W. Hancock, and R.S. Hodges Dissociation of antimicrobial and hemolytic activities in cyclic peptide diastereoisomers by systematic alteration in amphipathicity J. Biol. Chem. 274 1999 13181 13192
59. M. Jelokhani-Niaraki, L.H. Kondejewski, S.W. Farmer, R.E.W. Hancock, C.M. Kay, and R.S. Hodges Diastereoisomeric analogues of gramicidin S: structure, biological activity and interaction with lipid bilayers Biochem. J. 349 2000 747 755 (Pubitemid 30609405)
60. N. Papo, and Y. Shai Effect of drastic sequence alteration and D-amino acid incorporation on the membrane binding behavior of lytic peptides Biochemistry 42 2004 6393 6403 (Pubitemid 38697539)
61. M.L. Mangoni, N. Papo, J.M. Saugar, D. Barra, Y. Shai, M. Simmaco, and L. Rivas Effect of natural L- to D-amino acid conversion on the organization, membrane binding and biological function of the antimicrobial peptides bombinins H Biochemistry 45 2006 4266 4276