Influence of the bilayer composition on the binding and membrane disrupting effect of polybia-MP1, an antimicrobial mastoparan peptide with leukemic T-lymphocyte cell selectivity

Biochemistry

Volumn 51, Issue 24, 2012, Pages 4898-4908

  Dos Santos Cabrera, Marcia Perez ^a   Arcisio Miranda, Manoel ^b   Gorjão, Renata ^c   Leite, Natália Bueno ^a   De Souza, Bibiana Monson ^a   Curi, Rui ^d   Procopio, Joaquim ^d   Ruggiero Neto, João ^a   Palma, Mario Sérgio ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSIDADE CRUZEIRO DO SUL   (Brazil)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANIONIC LIPIDS; BI-LAYER; BILAYER COMPOSITIONS; BLUE SHIFT; CARDIOLIPINS; CELL-SELECTIVITY; DNA FRAGMENTATION; DOMAIN FORMATION; JURKAT CELL; LIPID CHARGE; MEMBRANE FLUIDITY; MODE OF ACTION; MODEL MEMBRANES; MOLECULAR MECHANISM; PARTITION COEFFICIENT; PEPTIDE BINDING; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLSERINE; SPHINGOMYELIN; STERN-VOLMER CONSTANTS; T-LYMPHOCYTES;

ANISOTROPY; CELL MEMBRANES; CHOLESTEROL; CYTOLOGY; ELECTROPHYSIOLOGY; FLUIDITY; PHOSPHOLIPIDS; TOXICITY;

PEPTIDES;

AMPHOLYTE; CARDIOLIPIN; CHOLESTEROL; MASTOPARAN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLSERINE; POLYBIA MP1; SPHINGOMYELIN; UNCLASSIFIED DRUG;

ANISOTROPY; ARTICLE; BILAYER MEMBRANE; CELL MEMBRANE FLUIDITY; CONTROLLED STUDY; DNA FRAGMENTATION; ELECTROPHYSIOLOGY; HUMAN; HUMAN CELL; LEUKEMIA; LEUKEMIA CELL; LIPID BILAYER; LYMPHOCYTE; MEMBRANE DAMAGE; MEMBRANE FLUIDITY; NECROSIS; PARTITION COEFFICIENT; PRIORITY JOURNAL; T LYMPHOCYTE;

ADSORPTION; AMINO ACID SEQUENCE; ANIMALS; ANTI-INFECTIVE AGENTS; ANTINEOPLASTIC AGENTS; CELL MEMBRANE; CELL SURVIVAL; CHOLESTEROL; HUMANS; JURKAT CELLS; LEUKEMIA; LIPID BILAYERS; MOLECULAR SEQUENCE DATA; PEPTIDES; POROSITY; PROTEIN BINDING; SUBSTRATE SPECIFICITY; SURFACE PROPERTIES; T-LYMPHOCYTES; UNILAMELLAR LIPOSOMES; WASP VENOMS; WASPS;

EID: 84862580384     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201608d     Document Type: Article

References (41)

1. Palma, M. S. (2006) Insect venom peptides. In The handbook of biologically active peptides (Kastin, A. J., Ed.) Vol. 56, pp 409-416, Elsevier, Amsterdam.
2. Konno, K., Rangel, M., Oliveira, J. S., Dos Santos Cabrera, M. P., Fontana, R., Hirata, I. Y., Hide, I., Nakata, Y., Mori, K., Kawano, M., Fuchino, H., Sekita, S., and Ruggiero Neto, J. (2007) Decoralin, a novel linear cationic α-helical peptide from the venom of the solitary eumenine wasp Oreumenes decoratus. Peptides 28, 2320-2327.
3. Wang, K. R., Zhang, B. Z., Zhang, W., Yan, J. X., Li, J., and Wang, R. (2008) Antitumor effects, cell selectivity and structure-activity relationship of a novel antimicrobial peptide Polybia-MPI. Peptides 29, 963-968.
4. Hirai, Y., Yasuhara, T., Yoshida, H., Nakajima, T., Fujino, M., and Kitada, C. (1979) A new mast cell degranulating peptide "mastoparan"in the venom of Vespula lewisii. Chem. Pharm. Bull. 27, 1942-1944. (Pubitemid 10223843)
5. Nakajima, T., Uzu, S., Wakamatsu, K., Saito, K., Miyazawa, T., Yasuhara, T., Tsukamoto, Y., and Fujino, M. (1986) Amphiphilic peptides in wasp venom. Biopolymers 25, 115-121.
6. De Souza, B. M., Mendes, M. A., Santos, L. D., Marques, M. R., Cesar, L. M., Almeida, R. N., Pagnocca, F. C., Konno, K., and Palma, M. S. (2005) Structural and functional characterization of two novel peptide toxins isolated from the venom of the social wasp Polybia paulista. Peptides 26, 2157-2164. (Pubitemid 41584079)
7. De Souza, B. M., da Silva, A. V., Resende, V. M., Arcuri, H. A., Dos Santos Cabrera, M. P., Ruggiero Neto, J., and Palma, M. S. (2009) Characterization of two novel polyfunctional mastoparan peptides from the venom of the social wasp Polybia paulista. Peptides 30, 1387-1395.
8. Dos Santos Cabrera, M. P., Costa, S. T., de Souza, B. M., Palma, M. S., Ruggiero, J. R., and Ruggiero Neto, J. (2008) Selectivity in the mechanism of action of antimicrobial mastoparan peptide Polybia-MP-1. Eur. Biophys. J. 37, 879-891.
9. Wang, K. R., Yan, J. X., Zhang, B. Z., Song, J. J., Jia, P. F., and Wang, R. (2009) Novel mode of action of Polybia-MPI, a novel antimicrobial peptide, in multi-drug resistant leukemic cells. Cancer Lett. 278, 65-72.
10. Zhang, W., Li, J., Liu, L. W., Wang, K. R., Song, J. J., Yan, J. X., Li, Z. Y., Zhang, B. Z., and Wang, R. (2010) A novel analog of antimicrobial peptide Polybia-MPI, with thioamide bond substitution, exhibits increased therapeutic efficacy against cancer and diminished toxicity in mice. Peptides 31, 1832-1838.
11. Boyum, A. (1968) Isolation of leucocytes from human blood. Further observations. Methylcellulose, dextran, and ficoll as erythrocytea ggregating agents. Scand. J. Clin. Lab. Invest. 97, 31-50.
12. Nicoletti, I., Migliorati, G., Pagliacci, M. C., Grignani, F., and Riccardi, C. (1991) A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 139, 271-279.
13. Mueller, P., Rudin, H. T., Tien, T., and Wescott, W. C. (1963) Methods for the formation of single bimolecular lipid membranes in aqueous solutions. J. Phys. Chem. 67, 534-535.
14. Dos Santos Cabrera, M. P., Arcisio-Miranda, M., Da Costa, L. C., De Souza, B. M., Broggio Costa, S. T., Palma, M. S., Ruggiero Neto, J., and Procopio, J. (2009) Interactions of mast cell degranulating peptides with model membranes: A comparative biophysical study. Arch. Biochem. Biophys. 486, 1-11.
15. Chattopadhyay, A., Rawat, S. S., Greathouse, D. V., Kelkar, D. A., and Koeppe, R. E., II (2008) Role of tryptophan residues in gramicidin channel organization and function. Biophys. J. 95, 166-175.
16. Ladokhin, A. S., Jayasinghe, S., and White, S. H. (2000) How to measure and analyze tryptophan fluorescence in membranes properly, and why bother? Anal. Biochem. 285, 235-245.
17. Lakowicz, J. R. (1999) Principles of Fluorescence Spectroscopy, Kluwer Academic/Plenum, New York.
18. Castanho, M. A., and Prieto, M. J. (1992) Fluorescence study of the macrolide pentaene antibiotic filipin in aqueous solution and in a model system of membranes. Eur. J. Biochem. 207, 125-134.
19. Matos, P. M., Franquelim, H. G., Castanho, M. A. R. B., and Santos, N. C. (2010) Quantitative assessment of peptide-lipid interactions. Ubiquitous fluorescence methodologies. Biochim. Biophys. Acta 1798, 1999-2012.
20. Kubo, S., Nemani, V. M., Chalkley, R. J., Anthony, M. D., Hattori, N., Mizuno, Y., Edwards, R. H., and Fortin, D. L. (2005) A combinatorial code for the interaction of α-synuclein with membranes. J. Biol. Chem. 280, 31664-31672. (Pubitemid 41291913)
21. Marsh, D. (2009) Cholesterol-induced fluid membrane domains: A compendium of lipid-raft ternary phase diagrams. Biochim. Biophys. Acta 1788, 2114-2123.
22. Goñi, F. M., Alonso, A., Bagatolli, L. A., Brown, R. E., Marsh, D., Prieto, M., and Thewalt, J. L. (2008) Phase diagrams of lipid mixtures relevant to the study of membrane rafts. Biochim. Biophys. Acta 1781, 665-684.
23. Lewis, R. N., and McElhaney, R. N. (2009) The physicochemical properties of cardiolipin bilayers and cardiolipin-containing lipid membranes. Biochim. Biophys. Acta 1788, 2069-2079.
24. Sood, R., Domanov, Y., and Kinnunen, P. K. (2007) Fluorescent temporin B derivative and its binding to liposomes. J. Fluoresc. 17, 223-234. (Pubitemid 46355030)
25. Melo, M. N., Ferre, R., and Castanho, M. A. (2009) Antimicrobial peptides: Linking partition, activity and high membrane-bound concentrations. Nat. Rev. Microbiol. 7, 245-250.
26. Schwarz, G., and Reiter, R. (2001) Negative cooperativity and aggregation in biphasic binding of mastoparan X peptide to membranes with acidic lipids. Biophys. Chem. 90, 269-277. (Pubitemid 32448098)
27. Arbuzova, A., and Schwarz, G. (1999) Pore-forming action of mastoparan peptides on liposomes: A quantitative analysis. Biochim. Biophys. Acta 1420, 139-152. (Pubitemid 29369026)
28. Schwarz, G., and Blochmann, U. (1993) Association of the wasp venom peptide mastoparan with electrically neutral lipid vesicles. Salt effects on partitioning and conformational state. FEBS Lett. 318, 172-176. (Pubitemid 23065947)
29. De Kroon, A. I., Soekarjo, M. W., De Gier, J., and De Kruijff, B. (1990) The role of charge and hydrophobicity in peptide-lipid interaction: A comparative study based on tryptophan fluorescence measurements combined with the use of aqueous and hydrophobic quenchers. Biochemistry 29, 8229-8240. (Pubitemid 20307796)
30. Eftink, M. R., and Ghiron, C. A. (1976) Exposure of tryptophanyl residues in proteins. Quantitative determination by fluorescence quenching studies. Biochemistry 15, 672-680.
31. Haines, T. H., and Dencher, N. A. (2002) Cardiolipin: A proton trap for oxidative phosphorylation. FEBS Lett. 528, 35-39. (Pubitemid 35257995)
32. Cummings, J. E., and Vanderlick, T. K. (2007) Aggregation and hemi-fusion of anionic vesicles induced by the antimicrobial peptide cryptdin-4. Biochim. Biophys. Acta 1768, 1796-1804. (Pubitemid 46890805)
33. Sood, R., Domanov, Y., Pietiainen, M., Kontinen, V. P., and Kinnunen, P. K. (2008) Binding of LL-37 to model biomembranes: Insight into target vs host cell recognition. Biochim. Biophys. Acta 1778, 983-996.
34. Fuller, N., Benatti, C. R., and Rand, R. P. (2003) Curvature and bending constants for phosphatidylserine-containing membranes. Biophys. J. 85, 1667-1674. (Pubitemid 37052249)
35. Dos Santos Cabrera, M. P., Alvares, D. S., Leite, N. B., De Souza, B. M., Palma, M. S., Riske, K. A., and Ruggiero Neto, J. (2011) New insight into the mechanism of action of wasp mastoparan peptides: Lytic activity and clustering observed with giant vesicles. Langmuir 27, 10805-10813.
36. Hasper, H. E., Kramer, N. E., Smith, J. L., Hillman, J. D., Zachariah, C., Kuipers, O. P., de Kruijff, B., and Breukink, E. (2006) An Alternative Bactericidal Mechanism of Action for Lantibiotic Peptides That Target Lipid II. Science 313, 1636-1637. (Pubitemid 44414037)
37. Zhao, H., Mattila, J. P., Holopainen, J. M., and Kinnunen, P. K. (2001) Comparison of the membrane association of two antimicrobial peptides, magainin 2 and indolicidin. Biophys. J. 81, 2979-2991. (Pubitemid 33020082)
38. Zhao, H., Tuominen, E. K., and Kinnunen, P. K. (2004) Formation of amyloid fibers triggered by phosphatidylserine-containing membranes. Biochemistry 43, 10302-10307. (Pubitemid 39079303)
39. Gottfried, E. L. (1967) Lipids of human leukocytes: Relation to cell type. J. Lipid Res. 8, 321-327.
40. 31P MRS analysis of the phospholipid composition of the peripheral blood mononuclear cells (PBMC) and bone marrow mononuclear cells (BMMC) of patients with acute leukemia (AL). Cell. Mol. Biol. Lett. 14, 35-45.
41. Bechinger, B., and Lohner, K. (2006) Detergent-like actions of linear amphipathic cationic antimicrobial peptides. Biochim. Biophys. Acta 1758, 1529-1539. (Pubitemid 44436087)