How C-Terminal Carboxyamidation Alters the Biological Activity of Peptides from the Venom of the Eumenine Solitary Wasp

Biochemistry

Volumn 43, Issue 19, 2004, Pages 5608-5617

  Sforça, Maurício L ^a   Oyama Jr , Sérgio ^a   Canduri, Fernanda ^c,d   Lorenzi, Carla C B ^c,d   Pertinhez, Thelma A ^a   Konno, Katsuhiro ^b,c   Souza, Bibiana M ^b,c   Palma, Mário S ^b,c   Neto, J Ruggiero ^c,d   Azevedo Jr , Walter F ^c,d   Spisni, Alberto ^a,e  

^a LABORATÓRIO NACIONAL DE LUZ SÍNCROTRON   (Brazil)

^b Institute of Biosciences   (Brazil)

^c INSTITUTO BUTANTAN   (Brazil)

^d SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^e UNIVERSITY OF PARMA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; CELLS; CHEMICAL MODIFICATION; CONFORMATIONS; HYDROGEN BONDS; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PERTURBATION TECHNIQUES;

BIOLOGICAL ACTIVITY; CARBOXYAMIDATION; CIRCULAR DICHROISM; DEGRANULATING PEPTIDES;

BIOCHEMISTRY;

AMIDE; CARBONYL DERIVATIVE; EUMENINE MASTOPARAN AF; ISOLEUCINE; LEUCINE; MAST CELL DEGRANULATING PEPTIDE; PEPTIDE DERIVATIVE; UNCLASSIFIED DRUG; WASP VENOM;

ALPHA HELIX; AMIDATION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CIRCULAR DICHROISM; HYDROGEN BOND; MICELLE; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN PROCESSING; PROTEIN STRUCTURE; SIMULATION;

AMIDES; ANIMALS; CIRCULAR DICHROISM; COMPUTER SIMULATION; INSECT PROTEINS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, SECONDARY; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS; TRIFLUOROETHANOL; WASP VENOMS; WATER;

INVERTEBRATA; MEGASCOLIA FLAVIFRONS; VESPIDAE;

EID: 18844471721     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0360915     Document Type: Article

References (74)

1. Banks, B. E., and Shipolini, R. A. (1986) Chemistry and pharmacology of honey-bee venom, in Venoms of the Hymenoptera: Biochemical, Pharmacological and Behavioural Aspects (Piek, T., Ed.) pp 327-416, Academic Press, London.
2. Nakajima, T. (1986) Pharmacological biochemistry of vespid venoms, in Venoms of the Hymenoptera: Biochemical, Pharmacological and Behavioural Aspects (Piek, T., Ed.) pp 309-327, Academic Press, London.
3. Konno, K., Hisada, M., Fontana, R., Lorenzi, C. C. B., Naoki, H., Itagaki, Y., Miwa, A., Kawai, N., Nakata, Y., Yasuhara, T., Neto, J. R., de Azevedo, W. F., Palma, M. S., and Nakajima, T. (2001) Anoplin, a novel antimicrobial peptide from the venom of the solitary wasp Anoplius samariensis, Biochim. Biophys. Acta 1550, 70-80.
4. Kreil, G. (1973) Biosynthesis of melittin, a toxic peptide from bee venom. Amino-acid sequence of the precursor, Eur. J. Biochem. 33, 558-566.
5. Andreu, D., Merrifield, R. B., Steiner, H., and Boman, H. G. (1983) Solid-phase synthesis of cecropin A and related peptides, Proc. Natl. Acad. Sci. U.S.A. 80, 6475-6479.
6. Mor, A., Nguyen, V. H., Delfour, A., Migliore-Samour, D., and Nicolas, P. (1991) Isolation, amino acid sequence and synthesis of dermaseptin, a novel antimicrobial peptide of amphibian skin, Biochemistry 30, 8824-8830.
7. Kuchler, K., Kreil, G., and Sures, I. (1989) The genes for the frog skin peptides GLa, xenopsin, levitide and caerulein contain a homologous export exon encoding a signal sequence and part of an amphiphilic peptide, Eur. J. Biochem. 179, 281-285.
8. Lee, I. H., Cho, Y., and Lehrer, R. I. (1997) Effects of pH and salinity on the antimicrobial properties of clavanins, Infect. Immun. 65, 2898-2903.
9. Agerberth, B., Lee, J.-Y., Bergman, T., Carlquist, M., Boman, H. G., Mutt, V., and Jörnvall, H. (1991) Amino acid sequence of PR-39. Isolation from pig intestine of a new member of the family of proline-arginine-rich antibacterial peptides, Eur. J. Biochem. 2002, 849-854.
10. Castells, P., Ampe, C., Jacobs, F., Vaeck, M., and Tempst, P. (1989) Apidaecins: antibacterial peptides from honeybees, EMBO J. 8, 2387-2391.
11. Harwig, S. L. S., Kokryakov, V. N., Swiderek, K. M., Aleshina, G. M., Zhao, C., and Lehrer, R. I. (1995) Prophenin-1, an exceptionally proline-rich antimicrobial peptide from porcine leukocytes, FEBS Lett. 362, 65-69.
12. 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. 106, 663-668.
13. Destoumieux, D., Bulet, P., Loew, D., Van Dorsselaer, A., Rodríguez, J., and Bachère, E. (1997) A new family of antimicrobial peptides in the shrimp Penaeus vannamei (Decapoda), J. Biol. Chem. 272, 28398-28406.
14. Sandvik, A. K., and Dockray, G. J. (1999) Biological activity of carboxy-terminal gastrin analogs, Eur. J. Pharmacol. 364, 199-203.
15. Katayama, H., Ohira, T., Aida, K., and Nagasawa, H. (2002) Significance of a carboxyl-terminal amide moiety in the folding and biological activity of crustacean hyperglycemic hormone, Peptides 23, 1537-1546.
16. Ali, M. F., Soto, A. M., Knoop, F. C., and Conlon, J. M. (2001) Antimicrobial peptides isolated from skin secretions of the diploid frog, Xenopus tropicalis (Pipidae), Biochim. Biophys. Acta 1550, 81-89.
17. Shai, Y. (1999) Mechanism of the binding, insertion and destabilization of phospholipid bilayers membranes by α-helical antimicrobial and cell non-selective lytic peptides, Biochim. Biophys. Acta 1462, 55-70.
18. Shai, Y. (2002) Mode of action of membrane active antimicrobial peptides, Biopolymers 66, 236-248.
19. van't Hof, W., Verrman, E. C. I., Helmerhorst, E. J., and Amerongen, A. V. N. (2001) Antimicrobial peptides: properties and applicability, Biol. Chem. 382, 597-619.
20. Konno, K., Hisada, M., Naoki, H., Itagaki, Y., Kawai, A., Miwa, A., Yasuhara, T., Morimoto, Y., and Nakata, Y. (2000) Structure and biological activity of eunamine mastoparan-AF (EMP-AF), a new mast cell degranulating peptide in the venom of the solitary wasp (Anterhynchium flavomarginatum micado), Toxicon 38, 1505-1515.
21. Canduri, F., Delatorre, P., Fadel, V., Lorenzi, C. C. B., Pereira, J. H., Olivieri, J. R., Neto, J. R., Konno, K., Palma, M. S., Yamane, T., and de Azevedo, W. F. (2000) Crystallization and preliminary X-ray diffraction analysis of a eumedine mastoparan toxin: a new class of mast-cell degranulating peptide in the wasp venom, Acta Crystallogr. D56, 1434-1436.
22. Delatorre, P., Olivieri, J. R., Neto, J. R., Lorenzi, C. C. B., Canduri, F., Fadel, V., Konno, K., Palma, M. S., Yamane, T., and de Azevedo, W. F. (2001) Preliminary cryocrystallography analysis of an eumenine mastoparan toxin isolated from the venom of the wasp Anterhynchium flavomarginatum micado, Biochim. Biophys. Acta 1545, 372-376.
23. Oren, Z., and Shai, Y. (1997) Selective lysis of bacteria but non mammalian cells by diastereomers of mellitin: Structure-function study, Biochemistry 36, 1826-1835.
24. Kustanovich, I., Shalev, D. E., Mikhlin, M., Gaidukov, L., and Mor, A. (2002) Structural requirements for potent versus selective cytotoxicity for antimicrobial dermaseptin S4 derivatives, J. Biol. Chem. 277, 16941-16951.
25. Hirota, N., Mizuno, K., and Goto, Y. (1998) Group additive contributions to the alcohol-induced α-helix formation of melittin: implication for the mechanism of the alcohol effects on proteins, J. Mol. Biol. 275, 365-378.
26. Sonnichsen, F. D., Van Eyk, J. E., Hodges, R. S., and Sykes, B. D. (1992) Effect of trifluoroethanol on protein secondary structure: an NMR and CD study using a synthetic actin peptide, Biochemistry 31, 8790-8798.
27. Chen, Y. H., Yang, J. T., and Chau, K. H. (1974) Determination of the helix and β form of proteins in aqueous solution by circular dichroism, Biochemistry 13, 3350-3359.
28. Piantini, U., Sorensen, O. W., Bodenhausen, G., and Ernest, R. R. (1982) Multiple quantum filters for elucidating NMR coupling networks, J. Am. Chem. Soc. 104, 6800-6801.
29. Braunschweiler, L., and Ernest, R. R. (1983) Coherence transfer by isotropic mixing: application to proton correlation spectroscopy, J. Magn. Reson. 53, 521-528.
30. Kumar, A., Ernst, R. R., and 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.
31. Macura, S., and Ernst, R. R. (1980) Elucidation of cross relaxation in liquids by two-dimensional NMR spectroscopy, Mol. Phys. 41, 95-117.
32. States, D. J., Haberkorn, R. A., and Ruben, D. J. (1982) A Two-Dimensional Nuclear Overhauser Experiment with Pure Absorption Phase in Four Quadrants, J. Magn. Reson. 48, 286-292.
33. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR 6, 277-293.
34. Johnson, B., and Blevins, R. A. (1994) NMRView: A computer program for the visualization and analysis of NMR data, J. Biomol. NMR 4, 603-614.
35. Güntert, P., Mumenthaler, C., and Wüthrich, K. (1997) Torsion Angle Dynamics for NMR Structure Calculation with the New Program Dyana, J. Mol. Biol. 273, 283-298.
36. Pristovšek, P., Rüterjans, H., and Jerala, R. (2002) Semiautomatic sequence-specific assignment of proteins based on the tertiary structure: The program st2 NMR, J. Comput. Chem. 23, 335-340.
37. Dauber-Osguthorpe, P., Osguthorpe, V. A., Wolff, D. J., Genest, M., and Hagler, A. T. (1988) Structure and energetics of ligand binding to proteins: E. coli dihydrofolate reductase-trimethoprim, a drug-receptor system, Proteins: Struct., Funct., Genet. 4, 31-47.
38. INSIGHT II User Guide, version 95 (1995) Accelrys Inc., San Diego.
39. Laskowsky, R. A., Rullmann, J. A., MacArthur, M. W., Kaptein, R., and Thorton, J. M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR, J. Biomol. NMR 8, 477-486.
40. Brunger, A. T., Adams, P. D., Clore, G. M., Delano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J.-S., Kuszewski, J., Nilges, N., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography and NMR system (CNS): a new software system for macromolecular structure determination, Acta Crystallogr. D54, 905-921.
41. Lindahl, E., Hess, B., and van der Spoel, D. (2001) Gromacs 3.0: a package for molecular simulation and trajectory analysis, J. Mol. Model. 7, 306-317.
42. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., and Hermans, J. (1981) Interaction models for water in relation to protein hydration, in Intermolecular Forces (Pullman, B., Ed.) pp 331-342, Reidel Publishing Co., Dordrecht, The Netherlands.
43. Fioroni, M., Burger, K., Mark, A. E., and Roccatano, D. (2000) A new 2,2,2-trifluoroethanol model for molecular dynamics simulations, J. Phys. Chem. B 104, 12347-12354.
44. Darden, T., York, D., and Pedersen, L. (1993) Particle Mesh Ewald: An N-log(N) method for Ewald sums in large systems, J. Chem. Phys. 98, 10089-10092.
45. Cheatham, T. E., III, Miller, J. L., Fox, T., Darden, T. A., and Kollman, P. A. (1995) Molecular dynamics simulations on solvated biomolecular systems: The Particle Mesh Ewald method leads to stable trajectories of DNA, RNA, and proteins, J. Am. Chem. Soc. 117, 4193-4194.
46. Hess, B., Bekker, H., Berendsen, H. J. C., and Fraaije, J. G. E. M. (1997) LINCS: A linear constraint solver for molecular simulations, J. Comput. Chem. 18, 1463-1472.
47. Miyamoto, S., and Kollman, P. A. (1992) SETTLE: An analytical version of the SHAKE and RATTLE algorithm for rigid water models, J. Comput. Chem. 13, 952-962.
48. van Aalten, D. M. F., de Groot, B. L., Findlay, J. B. C., Berendsen, H. J. C., and Amadei, A. (1997) A comparison of techniques for calculating protein essential dynamics, J. Comput. Chem. 18, 169-181.
49. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, John Wiley & Sons, New York.
50. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1992) The Chemical Shift Index: A fast and simple method for the assignment of protein secondary structure through NMR spectroscopy, Biochemistry 31, 1647-1651.
51. Levy, Y., Hanan, E., Solomon, B., and Becker, O. M. (2001) Helx-coil transition of Pr106-126: Molecular dynamic study, Proteins: Struct., Funct., Genet. 45, 382-396.
52. Amadei, A., Linssen, A. B. M., and Berendsen, H. J. C. (1993) Essential dynamics of proteins, Proteins: Struct., Funct., Genet. 17, 412-425.
53. de Groot, B. L., van Aalten, D. M. F., Amadei, A., and Berendsen, H. J. C. (1996) The consistency of large concerted motions in proteins in molecular dynamics simulations, Biophys. J. 71, 1707-1713.
54. Lee, I. H., Zhao, C., Cho, Y., Harwig, S. S., Cooper, E. L., and Lehrer, R. I. (1997) Clavanins, α-helical antimicrobial peptides from tunicate hemocytes, FEBS Lett. 400, 158-162.
55. Yasin, B., Lehrer, R. I., Harwig, S. S., and Wagar, E. A. (1996) Protegrins: structural requirements for inactivating elementary bodies of Chlamydia trachomatis, Infect. Immun. 64, 4863-4866.
56. Nakajima, Y., Qu, X.-M., and Natori, S. (1987) Interaction between liposomes and sarcotoxin IA, a potent antibacterial protein of Sarcophaga peregrina (flesh fly), J. Biol. Chem. 262, 1665-1669.
57. 2-terminal α-helical domain 1-18 of dermaseptin is responsible for antimicrobial activity, J. Biol. Chem. 269, 1934-1939.
58. Fernández, R. C., and Weiss, A. A. (1996) Susceptibilities of Bordetella pertussis strains to antimicrobial peptides, Antimicrob. Agents Chemother. 40, 1041-1043.
59. Shalev, D. E., Mor, A., and Kustanovich, I. (2002) Structural consequences of carboxyamidation of dermaseptin S3, Biochemistry 41, 7312-7317.
60. de Chiara, C., Nicastro, G., Spisni, A., Zanotti, F., Cocco, T., and Papa, S. (2002) Activity and NMR structure of synthetic peptides of the bovine ATPase inhibitor protein, IF1, Peptides 23, 2127-2141.
61. Smith, L., Zachariah, C., Thirumoorthy, R., Rocca, J., Novák, J., Hillman, J. D., and Edison, A. S. (2003) Structure and dynamics of the lantbiotic mutacin 1140, Biochemistry 42, 10372-10384.
62. van Aalten, D. M. F., Findlay, J. B. C., Amadei, A., and Berendsen, H. J. C (1995) Essential dynamics of the cellular retinol-binding protein: Evidence for ligand induced conformational changes, Protein Eng. 8, 1129-1135.
63. de Groot, B. L., Daura, X., Mark, A. E., and Grubmüller, H. (2001) Essential dynamics of reversible peptide folding: Memory-free conformational dynamics governed by internal hydrogen bonds, J. Mol. Biol. 309, 299-313.
64. + channel blocker: Tcl toxin from Tityus cambridgei, FEBS Lett. 535, 29-33.
65. Simmaco, M., Mignona, G., and Barra, D. (1998) Antimicrobial peptides from amphibian skin: What do they tell us? Biopolymers 47, 435-450.
66. Prates, M. V., Sforça, M. L., Regis, W. C. B., Leite, J. R. S. A., Silva, L. P., Pertinhez, T. A., Araújo, A. L. T., Azevedo, R. B., Spisni, A., and Bloch, C., Jr. (2004) The NMR-derived solution structure of a new cationic antimicrobial peptide from the skin secretion of the anuran Hyla punctata, J. Biol. Chem. 279, 13018-13026.
67. Chuang, C.-C., Huang, W.-C., Yu, H.-M., Wang, K.-T., and Wu, S.-H. (1996) Conformation of Vespa basalis Mastoparan-B in trifluoroethanol-containing aqueous solution, Biochim. Biophys. Acta 1292, 1-8.
68. Ho, C. L., Lin, Y. L., Chen, L. L., Hwang, H., Yu, M., and Wang, K. T. (1996) Structural requirements for the edema-inducing and haemolytic activities of mastoparan B isolated from the hornet (Vespa basalis) venom, Toxicon 34, 1027-1035.
69. Wakamatsu, K., Okada, A., Miyazawa, T., Ohya, M., and Higashijima, T. (1992) Membrane-bound confirmation of mastoparan-X, a G-protein-activating peptide, Biochemistry 31, 5654-5660.
70. Pouny, Y., Rapaport, D., Mor, A., Nicolas, P., and Shai, Y. (1992) Interactions of antimicrobial dermaseptin and its fluorescently labeled analogues with phospholipid membranes, Biochemistry 31, 12416-12423.
71. Cociancich, S., Ghazi, A., Hetru, C., Hoffmann, J. A., and Letellier, L. (1993) Insect defensin, an inducible antibacterial peptide, forms voltage-dependent channels in Micrococcus luteus, J. Biol. Chem. 268, 19239-19245.
72. Ludtke, S., He, K., and Huang, H. (1995) Antimicrobial peptide pores in membranes detected by neutron in-plane scattering, Biochemistry 34, 16764-16769.
73. Steiner, H., Andreu, D., and Merrifield, R. B. (1988) Binding and action of cecropin and cecropin analogues: antibacterial peptides from insects, Biochim. Biophys. Acta 939, 260-266.
74. Tossi, A., Sandri, L., and Giangaspero, A. (2000) Amphipathic, α-helical antimicrobial peptides, Biopolymers 55, 4-30.