Deletion of all cysteines in tachyplesin I abolishes hemolytic activity and retains antimicrobial activity and lipopolysaccharide selective binding

Biochemistry

Volumn 45, Issue 20, 2006, Pages 6529-6540

  Ramamoorthy, Ayyalusamy ^a   Thennarasu, Sathiah ^a,d   Tan, Anmin ^a   Gottipati, Kiran ^b   Sreekumar, Sreeja ^b   Heyl, Deborah L ^b   An, Florence Y P ^c   Shelburne, Charles E ^c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b EASTERN MICHIGAN UNIVERSITY   (United States)

^c UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^d CENTRAL LEATHER RESEARCH INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ENTHALPY; ENZYME INHIBITION; ESCHERICHIA COLI; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHASE TRANSITIONS; PHOSPHOLIPIDS; POLYPEPTIDES;

LIPID MEMBRANES; LIPOPOLYSACCHARIDE SELECTIVE BINDING; TACHYPLESIN I;

POLYSACCHARIDES;

2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; CYSTEINE; DIMYRISTOYLPHOSPHATIDYLCHOLINE; PHOSPHOLIPID; SYNTHETIC PEPTIDE; TACHYPLESIN;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACILLUS SUBTILIS; BACTERIAL OUTER MEMBRANE; BINDING AFFINITY; BLOOD CELL; CIRCULAR DICHROISM; CRAB; DIFFERENTIAL SCANNING CALORIMETRY; ENTEROCOCCUS FAECALIS; ENTHALPY; ESCHERICHIA COLI; HEMOLYSIS; LIPID MEMBRANE; LISTERIA MONOCYTOGENES; MEMBRANE PERMEABILITY; MEMBRANE VESICLE; NONHUMAN; PARTITION COEFFICIENT; PEPTIDE SYNTHESIS; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SALMONELLA ENTERICA; SOLID STATE; TACHYPLEUS TRIDENTATUS; TEMPERATURE;

ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BINDING SITES; CELL MEMBRANE PERMEABILITY; CIRCULAR DICHROISM; CYSTEINE; DNA-BINDING PROTEINS; HEMOLYSIS; LIPID BILAYERS; LIPOPOLYSACCHARIDES; MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDES; PEPTIDES, CYCLIC; PROTEIN STRUCTURE, SECONDARY; THERMODYNAMICS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; TACHYPLEUS TRIDENTATUS;

EID: 33646891071     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052629q     Document Type: Article

References (70)

1. Nakamura, T., Furunaka, H., Miyata, T., Tokunaga, F., Muta, T., Iwanaga, S., Niwa, M., Takao, T., and Shimonishi, Y. (1988) Tachyplesin, a class of antimicrobial peptide from the-hemocytes of the horseshoe crab (Tachypleus tridentatus): Isolation and chemical structure, J. Biol. Chem. 263, 16709-16713.
2. Miyata, T., Tokunaga, F., Yoneya, T., Yoshikawa, K., Iwanaga, S., Niwa, M., Takao, T., and Shimonishi, Y. (1989) Antimicrobial peptides, isolated from horseshoe crab hemocytes, tachyplesin II, and polyphemusins I and II: chemical structures and biological activity, J. Biochem. (Tokyo) 106, 663-668.
3. Ohta, M., Ito, H., Masuda, K., Tanaka, S., Arakawa, Y., Wacharotayankun, R., Kato, N. (1992) Mechanisms of antibacterial action of tachyplesins and polyphemusins, a group of antimicrobial peptides isolated from horseshoe crab hemocytes, Antimicrob. Agents Chemother. 36, 1460-1465.
4. Yonezawa, A., Kuwahara, J., Fujii, N., and Sugiura, Y. (1992) Binding of tachyplesin I to DNA revealed by footprinting analysis: Significant contribution of secondary structure to DNA binding and implication for biological action, Biochemistry 31, 2998-3004.
5. Matsuzaki, K., Fukui, M., Fujii, N., and Miyajima, K. (1991) Interactions of an antimicrobial peptide, tachyplesin I, with lipid membranes, Biochim. Biophys. Acta 1070, 259-264.
6. Kawano, K., Yoneya, T., Miyata, T., Yoshikawa, K., Tokunaga, F., Terada, Y., and Iwanaga, S. (1990) Antimicrobial peptide, tachyplesin I, isolated from hemocytes of the horseshoe crab (Tachypleus tridentatus): NMR determination of the beta-sheet structure, J. Biol. Chem. 265, 15365-15367.
7. 7]-polyphemusin II), determined by nuclear magnetic resonance, Biochim. Biophys. Acta 1163, 209-216.
8. Laederach, A., Andreotti, A. H., and Fulton, D. B. (2002) Solution and micelle-bound structures of tachyplesin I and its active aromatic linear derivatives, Biochemistry 41, 12359-12368.
9. Park, N. G., Lee, S., Oishi, O., Aoyagi, H., Iwanaga, S., Yamashita, S., and Ohno, M. (1992) Conformation of tachyplesin I from Tachypleus tridentatus when interacting with lipid matrixes, Biochemistry 31, 12241-12247.
10. Tamamura, H., Ikoma, R., Niwa, M., Funakoshi, S., Murakami, T., and Fujii, N. (1993) Antimicrobial activity and conformation of tachyplesin I and its analogues, Chem. Pharm. Bull. 41, 978-980.
11. Matsuzaki, K., Yoneyama, S., Fujii, N., Miyajima, K., Yamada, K.-I., Kirino, Y., and Anzai, K. (1997) Membrane permeabilization mechanisms of a cyclic antimicrobial peptide, tachyplesin I, and its linear analogue, Biochemistry 36, 9799-9809.
12. Rao, A. G. (1999) Conformation and antimicrobial activity of linear derivatives of tachyplesin lacking disulfide bonds, Arch. Biochem. Biophys. 361, 127-134.
13. Matsuzaki, K., Nakayama, M., Fukui, M., Otaka, A., Funakoshi, S., Fujii, N., Bessho, K., and Miyajima, K. (1993) Role of disulfide linkages in tachyplesin-lipid interactions, Biochemistry 32, 11704-11710.
14. Shai, Y. (2002) From innate immunity to de-novo designed antimicrobial peptides, Curr. Pharm. Des. 8, 715-725.
15. Rapaport, D., and Shai, Y. (1991) Interaction of fluorescently labeled pardaxin and its analogues with lipid bilayers, J. Biol. Chem. 266, 23769-23775.
16. Beshiaschvili, G., and Seelig, J. (1990) Melittin binding to mixed phosphatidylglycerol/phosphatidylcholine membranes, Biochemistry 29, 52-58.
17. Rizzo, V., Stankowsky, S., and Schwarz, G. (1987) Alamethicin incorporation in lipid bilayers: a thermodynamic study, Biochemistry 26, 2751-2759.
18. Hallock, K. J., Wilderman, K. A. H., Lee, D. K., and Ramamoorthy, A. (2002) An innovative procedure using a sublimable solid to align lipid bilayers for solid-state NMR studies, Biophys J. 82, 2499-2503.
19. Washburn, E. W., West, C. J., and Hull, C. (1926) International Critical Tables of Numerical Data, Physics, Chemistry, and Technology, McGraw-Hill, New York.
20. Bennett, A. E., Rienstra, C. M., Auger, M., Lakshmi, K. V., and Griffin, R. G. (1995) Heteronuclear decoupling in rotating solids, J. Chem. Phys. 103, 6951-6958.
21. Slavik, J. (1982) Anilinonaphthalene sulfonate as a probe of membrane composition and function, Biochim. Biophys. Acta 694, 1-25.
22. Thennarasu, S., Lee, D.-K., Tan, A., Prasad Kari, U., and Ramamoorthy, A. (2005) Antimicrobial activity and membrane selective interactions of a synthetic lipopeptide MSI-843, Biochim. Biophys. Acta 1711, 49-58.
23. Mao, D., and Wallace, B. A. (1984) Differential light scattering and absorption flattening optical effects are minimal in the circular dichroism spectra of small unilamellar vesicles, Biochemistry 23, 2667-2673.
24. 2 bound to micelles and its interactions with phospholipid bilayers, J. Pept. Res. 61, 219-229.
25. Rinia, H. A., Boots, J. W., Rijkers, D. T., Kik, R. A., Snel, M. M., Demel, R. A., Killian, J. A., Der Eerden, J. P., and de Kruijff, B. (2002) Domain formation in phosphotidylcholine bilayers containing transmembrane peptides: specific effects of flanking residues, Biochemistry 41, 2814-2824.
26. Rojo, N., Gómara, M. J., Busquets, M. A., Alsina, M. A., and Haro, I. (2003) Interaction of E2 and NS3 synthetic peptides of GB virus C/hepatitis G virus with model membranes, Talanta 60, 395-404.
27. Poon, A., Thennarasu, S., Lee, D.-K., Kawulka, K. E., Vederas, J. C., and Ramamoorthy, A. (2005) Membrane permeabilization, orientation, and antimicrobial mechanism of subtilisin A, Chem. Phys. Lipids (in press).
28. Henzler-Wildman, K. A., Martinez, G. V., Brown, M. F., and Ramamoorthy, A. (2004) Perturbation of the hydrophobic core of lipid bilayers by the human antimicrobial peptide LL-37, Biochemistry 43, 8459-8469.
29. Blanco, F., Ramirez-Alvendo, M., and Serrano, L. (1998) Formation and stability of β-hairpin structures in polypeptides, Curr. Opin. Struct. Biol. 8, 107-111.
30. n copolymer in aqueous solution, Polymer 16, 9-15.
31. Hirakura, Y., Kobayashi, S., and Matsuzaki, K. (2002) Specific interactions of the antimicrobial peptide cyclic β-sheet tachyplesin I with lipopolysaccharides, Biochim. Biophys. Acta 1562, 32-36.
32. Scherer, P. G., and Seelig, J. (1989) Electric charge effects on phospholipids headgroups. Phosphatidylcholine in mixtures with cationic and anionic amphiphiles, Biochemistry 28, 7720-7728.
33. Seelig, J., and Seelig, A. (1980) Lipid conformation in model membrane and biological membranes, Q. Rev. Biophys. 13, 19-61.
34. 31P NMR first spectral moment study of the partial magnetic orientation of phospholipid membranes, Biophys. J. 77, 888-902.
35. Santos, J. S., Lee, D. K., and Ramamoorthy, A. (2004) Effects of antidepressants on the conformation of phospholipid headgroups studied by solid-state NMR, Magn. Reson. Chem. 42, 105-114.
36. 31P MAS NMR spectroscopy: Nociceptin-lipid association, J. Am. Chem. Soc. 127, 6610-6618.
37. Lu, J. X., Damodaran, K., Blazyk, J., and Lorigan, G. A. (2005) Solid-state nuclear magnetic resonance relaxation studies of the interaction mechanism of antimicrobial peptides with phospholipid bilayer membranes, Biochemistry 44, 10208-10217.
38. Satoh, K., Okuda, H., Horimoto, H., Kodama, H., and Kondo, M. (1990) Synthesis and properties of a heterodetic cyclic peptide: Gramicidin S analog containing disulfide bond, Bull. Chem. Soc. Jpn. 63, 3467-3472.
39. Tamamura, H., Ikoma, R., Niwa, M., Funakoshi, S., Murakami, T., and Fujii, N. (1993) Antimicrobial activity and conformation of tachyplesin I and its analogs, Chem. Pharm. Bull. 41, 978-980.
40. Shai, Y. (1999) Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by α-helical antimicrobial and cell non-selective membrane-lytic peptides, Biochim. Biophys. Acta 1462, 55-70.
41. Brandenburg, K., and Wiese, A. (2004) Endotoxins: Relationships between structure, function, and activity, Curr. Top. Med. Chem. 11, 1127-1146.
42. Jerala, R., and Porro, M. (2004) Endotoxin neutralizing peptides, Curr. Top. Med. Chem. 11, 1173-1184.
43. Scott, M. G., Gold, M. R., and Hancock, R. E. W. (1999) Interaction of cationic peptides with lipoteichoic acid and gram-positive bacteria, Infect. Immun. 67, 6445-6453.
44. Anderson, R. C., Hancock, R. E. W., and Yu, P.-L. (2004) Antimicrobial activity and bacterial-membrane interaction of ovine-derived cathelicidins, Antimicrob. Agents Chemother. 48, 673-676.
45. Matsuzaki, K. (1999) Why and how-are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes, Biochim. Biophys. Acta 1462, 1-10.
46. Wildman, K. A. H., Lee, D. K., and Ramamoorthy, A. (2003) Mechanism of lipid bilayer disruption by the human antimicrobial peptide, LL-37, Biochemistry 42, 6545-6558.
47. Oren, Z., Hong, J., and Shai, Y. (1997) A repertoire of novel antibacterial diastereomeric peptides with selective cytolytic activity, J. Biol. Chem. 272, 14643-14649.
48. Matsuzaki, M., Sugishita, K., Fujii, N., and Miyajima, K. (1995) Molecular basis for membrane selectivity of an antimicrobial peptide, magainin 2, Biochemistry 34, 3423-3429.
49. Kondejewski, L. H., Farmer, S. W., Wishart, D. S., Kay, C. M., Hancock, R. E. W., and Hodges, R. S. (1996) Modulation of structure and antibacterial and hemolytic activity by ring size in cyclic gramicidin S analogs, J. Biol. Chem. 271, 25261-25268.
50. Hong, J., Oren, Z., and Shai, Y. (1999) Structure and organization of hemolytic and nonhemolytic diastereomers of antimicrobial peptides in membranes, Biochemistry 38, 16963-16973.
51. 31P NMR and differential scanning calorimetry study, Biochim. Biophys. Acta 513, 21-30.
52. Hallock, K. J., Lee, D.-K., Omnaas, J., Mosberg, H. I., and Ramamoorthy, A. (2002) Membrane composition determines pardaxin's mechanism of lipid bilayer disruption, Biophys. J. 83, 1004-1013.
53. Epand, R. M., Sayer, B. G., and Epand, R. F. (2003) Peptide-induced formation of cholesterol-rich domains, Biochemistry 42, 14677-14689.
54. Brown, M. F., and Seelig, J. (1977) Nature 269, 721-723.
55. Dave, P. C., Billington, E., Pan, Y. L., and Straus, S. K. (2005) Interaction of alamethicin with ether-linked phospholipid bilayers: Oriented circular dichroism, P-31 solid-state NMR, and differential scanning calorimetry studies, Biophys. J. 89, 2434-2442.
56. Strandberg, E., and Ulrich, A. S. (2004) NMR methods for studying membrane-active antimicrobial peptides, Concepts Magn. Reson. 23, 89-120.
57. Powers, J. P. S., Tan, A., Ramamoorthy, A., and Hancock, R. E. W. (2005) Solution structure and interaction of the antimicrobial polyphemusins with lipid membranes, Biochemistry 44, 15504-15513.
58. Hallock, K. J., Lee, D. K., and Ramamoorthy, A. (2003) MSI-78, an analogue of the magainin antimicrobial peptides, disrupts lipid bilayer structure via positive curvature strain, Biophys. J. 84, 3052-3060.
59. Marcotte, I., Wegener, K. L., Lam, Y. H., Chia, B. C. S., de Planque, M. R. R., Bowie, J. H., Auger, M., and Separovic, F. (2003) Interaction of antimicrobial peptides from Australian amphibians with lipid membranes, Chem. Phys. Lipids 122, 107-120.
60. Mani, R., Buffy, J. J., Waring, A. J., Lehrer, R. I., and Hong, M. (2004) Solid-state NMR investigation of the selective disruption of lipid membranes by protegrin-1, Biochemistry 43, 13839-13848.
61. Mani, R., Waring, A. J., Lehrer, R. I., and Hong, M. (2005) Membrane-disruptive abilities of beta-hairpin antimicrobial peptides correlate with conformation and activity: A P-31 and H-1 NMR study, Biochim. Biophys. Acta 1716, 11-18.
62. Abu-Baker, S., Qi, X. Y., Newstadt, J., and Lorigan, G. A. (2005) Structural changes in a binary mixed phospholipid bilayer of DOPG and DOPS upon saposin C interaction at acidic pH utilizing P-31 and H-2 solid-state NMR spectroscopy, Biochim. Biophys. Acta 1717, 58-66.
63. Porcelli, F., Buck, B., Lee, D. K., Hallock, K. J., Ramamoorthy, A., and Veglia, G. (2004) Structure and orientation of pardaxin determined by NMR experiments in model membranes, J. Biol. Chem. 279, 45815-45823.
64. Mecke, A., Lee, D. K., Ramamoorthy, A., Orr, B. G., and Holl, M. M. B. (2005) Membrane thinning due to antimicrobial peptide binding: An atomic force microscopy study of MSI-78 in lipid bilayers, Biophys. J. 99, 4043-4050.
65. Dempsey, C. E., Ueno, S., and Avison, M. B. (2003) Enhanced membrane permeabilization and antibacterial activity of a disulfide-dimerized magainin analogue, Biochemistry 42, 402-409.
66. Epand, R. F., Ramamoorthy, A., and Epand, R. M. (2006) Membrane lipid composition and the interaction with pardaxin: the role of cholesterol, Protein Pept. Lett. 13, 1-5.
67. Zwaal, R. F., and Schroit, A. J. (1997) Pathophysiologic implications of membrane phospholipid asymmetry in blood cells, Blood 89, 1121-1132.
68. Tachi, T., Epand, R. F., Epand, R. M., and Matsuzaki, K. (2002) Position-dependent hydrophobicity of the antimicrobial magainin peptide affects the mode of peptide-lipid interactions and selective toxicity, Biochemistry 41, 10723-10731.
69. Dathe, M., Wieprecht, T., Nikolenko, H., Handel, L., Maloy, W. L., MacDonald, D. L., Beyermann, M., and Bienert, M. (1997) Hydrophobicity, hydrophobic moment and angle subtended by charged residues modulate antibacterial and haemolytic activity of amphipathic helical peptides, FEBS Lett. 403, 208-212.
70. Maloy, W. L., and Kari, U. P. (1995) Structure-activity studies on magainins and other host defense peptides, Biopolymers 37, 105-122.