The peculiar N- and C-termini of trichogin GA IV are needed for membrane interaction and human cell death induction at doses lacking antibiotic activity

Biochimica et Biophysica Acta - Biomembranes

Volumn 1848, Issue 1, 2015, Pages 134-144

  Tavano, Regina ^a   Malachin, Giulia ^a   De Zotti, Marta ^a   Peggion, Cristina ^a   Biondi, Barbara ^a   Formaggio, Fernando ^a   Papini, Emanuele ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

Cytotoxicity; Lipopeptaibol; Membrane active peptide; Trichogin

Indexed keywords

GLYCINE; LYSINE; POLYPEPTIDE ANTIBIOTIC AGENT; TRICHOGIN GLYCYLALANINE IV; UNCLASSIFIED DRUG; 1,2-DIOLEOYL-GLYCERO-3-PHOSPHATIDYL ETHANOLAMINE; 1,2-DIOLEOYL-SN-GLYCERO-3-PHOSPHOGLYCEROL; 1,2-OLEOYLPHOSPHATIDYLCHOLINE; ANTIINFECTIVE AGENT; CHOLESTEROL; LIPOPEPTIDE; LIPOSOME; MEMBRANE LIPID; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLGLYCEROL; TRICHOGIN GA IV;

AMINO TERMINAL SEQUENCE; ANTIBACTERIAL ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DEATH; CONTROLLED STUDY; CYTOTOXICITY; EC50; ENDOCYTOSIS; ESCHERICHIA COLI; ESTERIFICATION; EUKARYOTIC CELL; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HUMAN; HUMAN CELL; MINIMUM INHIBITORY CONCENTRATION; PHOSPHOLIPID BILAYER; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; TRICHODERMA LONGIBRACHIATUM; TUMOR CELL; AMINO ACID SEQUENCE; BINDING COMPETITION; CELL CULTURE; CELL LINE; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL SURVIVAL; CHEMISTRY; CONFOCAL MICROSCOPY; DOSE RESPONSE; DRUG EFFECTS; HELA CELL LINE; HEMOLYSIS; HL 60 CELL LINE; METABOLISM; MICROBIAL SENSITIVITY TEST; TUMOR CELL LINE;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; BINDING, COMPETITIVE; CELL LINE; CELL LINE, TUMOR; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL SURVIVAL; CELLS, CULTURED; CHOLESTEROL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCYTOSIS; HELA CELLS; HEMOLYSIS; HL-60 CELLS; HUMANS; LIPOPEPTIDES; MEMBRANE LIPIDS; MICROBIAL SENSITIVITY TESTS; MICROSCOPY, CONFOCAL; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLETHANOLAMINES; PHOSPHATIDYLGLYCEROLS; UNILAMELLAR LIPOSOMES;

EID: 84908389334     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2014.10.005     Document Type: Article

References (35)

1. C. Toniolo, and H. Bruckner Fungal Peptides Containing α-Dialkyl α-Amino Acids 2009 Zurich and Wiley-VCH Weinheim
2. E. Benedetti, A. Bavoso, B. Di Blasio, V. Pavone, C. Pedone, C. Toniolo, and G.M. Bonora Peptaibol antibiotics: a study on the helical structure of the 2-9 sequence of emerimicins III and IV Proc. Natl. Acad. Sci. 79 1982 7951 7954
3. A. Wiest, D. Grzegorski, B.W. Xu, C. Goulard, S. Rebuffat, D.J. Ebbole, B. Bodo, and C. Kenerley Identification of peptaibols from Trichoderma virens and cloning of a peptaibol synthetase J. Biol. Chem. 277 2002 20862 20868
4. P.K. Mukherjee, A. Wiest, N. Ruiz, A. Keightley, M.E. Moran-Diez, K. McCluskey, Y.F. Pouchus, and C.M. Kenerley Two classes of new peptaibols are synthesized by a single non-ribosomal peptide synthetase of Trichoderma virens J. Biol. Chem. 286 2011 4544 4554
5. T. Degenkolb, A. Berg, W. Gams, B. Schlegel, and U. Grafe The occurrence of peptaibols and structurally related peptaibiotics in fungi and their mass spectrometric identification via diagnostic fragment ions J. Pept. Sci. 9 2003 666 678
6. J. Peltola, A. Ritieni, R. Mikkola, P.A. Grigoriev, G. Pocsfalvi, M.A. Andersson, and M.S. Salkinoja-Salonen Biological effects of Trichoderma harzianum peptaibols on mammalian cells Appl. Environ. Microbiol. 70 2004 4996 5004
7. M. Shi, H.N. Wang, S.T. Xie, Y. Luo, C.Y. Sun, X.L. Chen, and Y.Z. Zhang Antimicrobial peptaibols, novel suppressors of tumor cells, targeted calcium-mediated apoptosis and autophagy in human hepatocellular carcinoma cells Mol. Cancer 9-26 2010
8. M.K. Mathew, R. Nagaraj, and P. Balaram Membrane channel-forming polypeptides. Aqueous phase aggregation and membrane-modifying activity of synthetic fluorescent alamethicin fragments J. Biol. Chem. 257 1982 2170 2176
9. L.R. Jones, S.W. Maddock, and H.R. Besch Jr. Unmasking effect of alamethicin on the (Na +, K +)-ATPase, beta-adrenergic receptor-coupled adenylate cyclase, and cAMP-dependent protein kinase activities of cardiac sarcolemmal vesicles J. Biol. Chem. 255 1980 9971 9980
10. N. Ruiz, K. Petit, M. Vansteelandt, I. Kerzaon, J. Baudet, Z. Amzil, J.F. Biard, O. Grovel, and Y.F. Pouchus Enhancement of domoic acid neurotoxicity on Diptera larvae bioassay by marine fungal metabolites Toxicon 55 2010 805 810
11. C.U. Hjorringgaard, J.M. Pedersen, T. Vosegaard, N.C. Nielsen, and T. Skrydstrup An automatic solid-phase synthesis of peptaibols J. Org. Chem. 74 2009 1329 1332
12. M. De Zotti, B. Biondi, C. Peggion, Y. Park, K.S. Hahm, F. Formaggio, and C. Toniolo Synthesis, preferred conformation, protease stability, and membrane activity of heptaibin, a medium-length peptaibiotic J. Pept. Sci. 17 2011 585 594
13. C. Auvin-Guette, S. Rebuffat, Y. Prigent, and B. Bodo Trichogin A IV, an 11-residue lipopeptaibol from Trichoderma longibrachiatum J. Am. Chem. Soc. 114 1992 2170 2174
14. C. Peggion, F. Formaggio, M. Crisma, R.F. Epand, R.M. Epand, and C. Toniolo Trichogin: a paradigm for lipopeptaibols J. Pept. Sci. 9 2003 679 689
15. M. De Zotti, B. Biondi, Y. Park, K.S. Hahm, M. Crisma, C. Toniolo, and F. Formaggio Antimicrobial lipopeptaibol trichogin GA IV: role of the three Aib residues on conformation and bioactivity Amino Acids 43 2012 1761 1777
16. M. De Zotti, B. Biondi, F. Formaggio, C. Toniolo, L. Stella, Y. Park, and K.S. Hahm Trichogin GA IV: an antibacterial and protease-resistant peptide J. Pept. Sci. 15 2009 615 619
17. S. Richter, M.G. Cormican, M.A. Pfaller, C.K. Lee, R. Gingrich, M.G. Rinaldi, and D.A. Sutton Fatal disseminated Trichoderma longibrachiatum infection in an adult bone marrow transplant patient: species identification and review of the literature J. Clin. Microbiol. 37 1999 1154 1160
18. C.F. Santillan Salas, A.Y. Joshi, N. Dhiman, R. Banerjee, W.C. Huskins, N.L. Wengenack, and N.K. Henry Fatal post-operative Trichoderma longibrachiatum mediastinitis and peritonitis in a paediatric patient with complex congenital cardiac disease on peritoneal dialysis J. Med. Microbiol. 60 2011 1869 1871
19. I.S. Druzhinina, M. Komon-Zelazowska, L. Kredics, L. Hatvani, Z. Antal, T. Belayneh, and C.P. Kubicek Alternative reproductive strategies of Hypocrea orientalis and genetically close but clonal Trichoderma longibrachiatum, both capable of causing invasive mycoses of humans Microbiology 154 2008 3447 3459
20. P. Tang, S. Mohan, L. Sigler, I. Witterick, R. Summerbell, I. Campbell, and T. Mazzulli Allergic fungal sinusitis associated with Trichoderma longibrachiatum J. Clin. Microbiol. 41 2003 5333 5336
21. E. Molnar-Gabor, I. Doczi, L. Hatvani, C. Vagvolgyi, and L. Kredics Isolated sinusitis sphenoidalis caused by Trichoderma longibrachiatum in an immunocompetent patient with headache J. Med. Microbiol. 62 2013 1249 1252
22. R.F. Epand, R.M. Epand, V. Monaco, S. Stoia, F. Formaggio, M. Crisma, and C. Toniolo The antimicrobial peptide trichogin and its interaction with phospholipid membranes Eur. J. Biochem. 266 1999 1021 1028
23. C. Toniolo, C. Peggion, M. Crisma, F. Formaggio, X. Shui, and D.S. Eggleston Structure determination of racemic trichogin A IV using centrosymmetric crystals Nat. Struct. Biol. 1 1994 908 914
24. C. Mazzuca, L. Stella, M. Venanzi, F. Formaggio, C. Toniolo, and B. Pispisa Mechanism of Membrane Activity of the Antibiotic Trichogin GA IV: A Two-State Transition Controlled by Peptide Concentration Biophys. J. 88 2005 3411 3421
25. α-acyl chain length on the membrane-modifying properties of synthetic analogs of the lipopeptaibol trichogin GA IV J. Am. Chem. Soc. 118 1996 4952 4958
26. S. Smeazzetto, M. De Zotti, and M.R. Moncelli A new approach to detect and study ion channel formation in microBLMs Electrochem. Commun. 13 2011 834 836
27. V.N. Syryamina, M. De Zotti, C. Peggion, F. Formaggio, C. Toniolo, J. Raap, and S.A. Dzuba A molecular view on the role of cholesterol upon membrane insertion, aggregation, and water accessibility of the antibiotic lipopeptide trichogin GA IV as revealed by EPR J. Phys. Chem. B 116 2012 5653 5660
28. M. De Zotti, B. Biondi, C. Peggion, F. Formaggio, Y. Park, K.S. Hahm, and C. Toniolo Trichogin GA IV: a versatile template for the synthesis of novel peptaibiotics Org. Biomol. Chem. 10 2012 1285 1299
29. M. De Zotti, F. Formaggio, B. Kaptein, Q.B. Broxterman, P.J. Felock, D.J. Hazuda, S.B. Singh, H. Bruckner, and C. Toniolo Complete absolute configuration of integramide A, a natural, 16-mer peptide inhibitor of HIV-1 integrase, elucidated by total synthesis Chembiochem 10 2009 87 90
30. S. Beychock Circular dichroism of poly-α-amino acids and proteins G.D. Fasman, Poly-α-amino Acids: Protein Models for Conformational Studies 1967 Dekker New York, NY 293 337
31. V. Monaco, E. Locardi, F. Formaggio, M. Crisma, S. Mammi, E. Peggion, C. Toniolo, S. Rebuffat, and B. Bodo Solution conformational analysis of amphiphilic helical, synthetic analogs of the lipopeptaibol trichogin GA IV J. Pept. Res. 52 1998 261 272
32. 2 nanoparticles on monocytes and macrophages in serum Nanomedicine Mar 24 2014 10.2217/nnm.14.22
33. J.P. Richard, K. Melikov, H. Brooks, P. Prevot, B. Lebleu, and L.V. Chernomordik Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors J. Biol. Chem. 280 15 2005 15300 15306
34. S. Bobone, Y. Gerelli, M. De Zotti, G. Bocchinfuso, A. Farrotti, B. Orioni, F. Sebastiani, E. Latter, J. Penfold, R. Senesi, F. Formaggio, A. Palleschi, C. Toniolo, G. Fragneto, and L. Stella Membrane thickness and the mechanism of action of the short peptaibol trichogin GA IV BBA 1828 3 2013 1013 1024
35. T.N. Kropacheva, and J. Raap Ion transport across a phospholipid membrane mediated by the peptide trichogin GA IV Biochim. Biophys. Acta Biomembr. 1567 2002 193 203