The lipopeptide toxins anabaenolysin A and B target biological membranes in a cholesterol-dependent manner

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 12, 2012, Pages 3000-3009

  Oftedal, Linn ^a,d   Myhren, Lene ^a   Jokela, Jouni ^b   Gausdal, Gro ^a   Sivonen, Kaarina ^b   Doskeland, Stein Ove ^a   Herfindal, Lars ^a,c  

^a UNIVERSITY OF BERGEN   (Norway)

^b UNIVERSITY OF HELSINKI   (Finland)

^c HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^d STAVANGER UNIVERSITY HOSPITAL   (Norway)

Author keywords

Biodetergent; Cholesterol; Cyanobacteria; Cyclic lipopeptide; Hemolysis; Mitochondria

Indexed keywords

ANABAENOLYSIN A; ANABAENOLYSIN B; BACTERIAL TOXIN; CHOLESTEROL; CYTOCHROME C; DIGITONIN; GLYCOLIPID; HEMOLYSIN; LIPOPEPTIDE; LIPOSOME; NODULARIN; PROPIDIUM IODIDE; SURFACTIN; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL PERMEABILIZATION; CELL TRANSFORMATION; CELL VIABILITY; CHEMICAL STRUCTURE; COMPUTER MODEL; CONTROLLED STUDY; ECHINOCYTE; ENZYME RELEASE; ERYTHROCYTE; HUMAN; HUMAN CELL; INTERNALIZATION; LIVER MITOCHONDRION; LYSIS; MEMBRANE BIOLOGY; MEMBRANE DAMAGE; MEMBRANE POTENTIAL; MITOCHONDRION; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN STRUCTURE; TARGET CELL; TOXIN STRUCTURE; ULTRASTRUCTURE;

ANABAENA; ANIMALS; APOPTOSIS; BACTERIAL TOXINS; CELL LINE, TUMOR; CELL MEMBRANE; CHOLESTEROL; CYTOCHROMES C; DIGITONIN; HEMOLYSIN PROTEINS; LIPOPEPTIDES; LIPOSOMES; LIVER; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MITOCHONDRIA, LIVER; MODELS, MOLECULAR; PEPTIDES, CYCLIC; PROPIDIUM; RATS;

CYANOBACTERIA; EUKARYOTA; MAMMALIA; PROKARYOTA; RATTUS;

EID: 84865317358     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.07.015     Document Type: Article

References (43)

1. K. Sivonen, and T. Börner Bioactive compounds produced by cyanobacteria A. Herrero, E. Flores, The Cyanobacteria. Molecular Biology, Genomics and Evolution 2008 Caister Academic Press Norfolk, UK 159 197
2. L. Herfindal, L. Oftedal, F. Selheim, M. Wahlsten, K. Sivonen, and S.O. Doskeland A high proportion of Baltic Sea benthic cyanobacterial isolates contain apoptogens able to induce rapid death of isolated rat hepatocytes Toxicon 46 2005 252 260
3. L. Oftedal, K.H. Skjærven, R.T. Coyne, B. Edvardsen, T. Rohrlack, O.M. Skulberg, S.O. Doskeland, and L. Herfindal The apoptosis-inducing activity towards leukemia and lymphoma cells in a cyanobacterial culture collection is not associated with mouse bioassay toxicity J Ind Microbiol Biotechnol. 38 2011 489 501
4. J. Jokela, L. Oftedal, L. Herfindal, P. Permi, M. Wahlsten, S.O. Doskeland, and K. Sivonen Anabaenolysins, novel cytolytic lipopeptides from benthic Anabaena cyanobacteria PLoS ONE 7 2012 e41222
5. A.M. Burja, B. Banaigs, E. Abou-Mansour, J.G. Burgess, and P.C. Wright Marine cyanobacteria - a prolific source of natural compounds Tetrahedron 57 2001 9347 9377
6. M. Dalla Serra, and G. Menestrina Liposomes in the study of pore-forming toxins Methods Enzymol. 372 2003 99 124
7. G.E. Rowe, and R.A. Welch Assays of hemolytic toxins Methods Enzymol. 235 1994 657 667
8. G. Menestrina, and M. Dalla Serra Pore-forming toxins Encyclopedia of Life Sciences 2001 Wiley 10.1038/npg.els.0002655
9. M. Nishikawa, S. Nojima, T. Akiyama, U. Sankawa, and K. Inoue Interaction of digitonin and its analogs with membrane cholesterol J. Biochem. 96 1984 1231 1239
10. G. Seydlova, and J. Svobodova Review of surfactin chemical properties and the potential biomedical applications Cent. Eur. J. Med. 3 2008 123 133
11. B. Bechinger, and K. Lohner Detergent-like actions of linear amphipathic cationic antimicrobial peptides Biochim. Biophys. Acta 1758 2006 1529 1539
12. M.P. Sheetz, and S.J. Singer Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions Proc. Natl. Acad. Sci. U. S. A. 71 1974 4457 4461
13. H. Heerklotz, and J. Seelig Leakage and lysis of lipid membranes induced by the lipopeptide surfactin Eur. Biophys. J. 36 2007 305 314
14. N. Lacaze, G. Gombaud-Saintonge, and M. Lanotte Conditions controlling long-term proliferation of Brown Norway rat promyelocytic leukemia in vitro: primary growth stimulation by microenvironment and establishment of an autonomous Brown Norway 'leukemic stem cell line' Leuk. Res. 7 1983 145 154
15. M. Lanotte, V. Martin-Thouvenin, S. Najman, P. Balerini, F. Valensi, and R. Berger NB4, a maturation inducible cell line with t(15;17) marker isolated from a human acute promyelocytic leukemia (M3) Blood 77 1991 1080 1086
16. C. Krakstad, L. Herfindal, B.T. Gjertsen, R. Boe, O.K. Vintermyr, K.E. Fladmark, and S.O. Doskeland CaM-kinaseII dependent commitment to microcystin-induced apoptosis is coupled to cell budding, but not to shrinkage or chromatin hypercondensation Cell Death Differ. 13 2006 1191 1202
17. P.O. Seglen Preparation of isolated rat liver cells Methods Cell Biol. 13 1976 29 83
18. G. Mellgren, O.K. Vintermyr, and S.O. Doskeland Okadaic acid, cAMP, and selected nutrients inhibit hepatocyte proliferation at different stages in G1: modulation of the cAMP effect by phosphatase inhibitors and nutrients J. Cell. Physiol. 163 1995 232 240
19. J.C. Reed, J.M. Jurgensmeier, and S. Matsuyama Bcl-2 family proteins and mitochondria Biochim. Biophys. Acta 1366 1998 127 137
20. L. Herfindal, F. Kasprzykowski, F. Schwede, L. Lankiewicz, K.E. Fladmark, J. Lukomska, M. Wahlsten, K. Sivonen, Z. Grzonka, B. Jastorff, and S.O. Doskeland Acyloxymethyl esterification of nodularin-R and microcystin-LA produces inactive protoxins that become reactivated and produce apoptosis inside intact cells J. Med. Chem. 52 2009 5758 5762
21. K.E. Fladmark, O.T. Brustugun, G. Mellgren, C. Krakstad, R. Boe, O.K. Vintermyr, H. Schulman, and S.O. Doskeland Ca2 +/calmodulin-dependent protein kinase II is required for microcystin-induced apoptosis J. Biol. Chem. 277 2002 2804 2811
22. Y. Yawata Cell Membrane: The Red Blood Cell as a Model 2003 Wiley-VCH Weinheim
23. M. Sanchez, F.J. Aranda, J.A. Teruel, M.J. Espuny, A. Marques, A. Manresa, and A. Ortiz Permeabilization of biological and artificial membranes by a bacterial dirhamnolipid produced by Pseudomonas aeruginosa J. Colloid Interface Sci. 341 2010 240 247
24. A. Zaragoza, F.J. Aranda, M.J. Espuny, J.A. Teruel, A. Marques, A. Manresa, and A. Ortiz Hemolytic activity of a bacterial trehalose lipid biosurfactant produced by Rhodococcus sp.: evidence for a colloid-osmotic mechanism Langmuir 26 2010 8567 8572
25. H. Hagerstrand, and B. Isomaa Morphological characterization of exovesicles and endovesicles released from human erythrocytes following treatment with amphiphiles Biochim. Biophys. Acta 1109 1992 117 126
26. P. Wong A basis of echinocytosis and stomatocytosis in the disc-sphere transformations of the erythrocyte J. Theor. Biol. 196 1999 343 361
27. M. Bessis The erythrocytic series M. Bessis, Living Blood Cells and Their Ultrastructure 1973 Springer Berlin 85 284
28. V. Gogvadze, S. Orrenius, and B. Zhivotovsky Multiple pathways of cytochrome c release from mitochondria in apoptosis Biochim. Biophys. Acta 1757 2006 639 647
29. G. Zubay Biochemistry 1993 Wm. C. Brown publishers Dubuque, Iowa
30. M.P. Besenicar, A. Bavdek, A. Kladnik, P. Macek, and G. Anderluh Kinetics of cholesterol extraction from lipid membranes by methyl-beta-cyclodextrin - a surface plasmon resonance approach Biochim. Biophys. Acta 1778 2008 175 184
31. P. Singh, and S.S. Cameotra Potential applications of microbial surfactants in biomedical sciences Trends Biotechnol. 22 2004 142 146
32. A. Zaragoza, F.J. Aranda, M.J. Espuny, J.A. Teruel, A. Marques, A. Manresa, and A. Ortiz Mechanism of membrane permeabilization by a bacterial trehalose lipid biosurfactant produced by Rhodococcus sp Langmuir 25 2009 7892 7898
33. R. Maget-Dana, and M. Ptak Interactions of surfactin with membrane models Biophys. J. 68 1995 1937 1943
34. C. Carrillo, J.A. Teruel, F.J. Aranda, and A. Ortiz Molecular mechanism of membrane permeabilization by the peptide antibiotic surfactin Biochim. Biophys. Acta 1611 2003 91 97
35. A. Beck, A.D. Tsamaloukas, P. Jurcevic, and H. Heerklotz Additive action of two or more solutes on lipid membranes Langmuir 24 2008 8833 8840
36. M. Nazari, M. Kurdi, and H. Heerklotz Classifying surfactants with respect to their effect on lipid membrane order Biophys. J. 102 2012 498 506
37. H.L. Huaust, A. Kuksis, and J.M. Beveridge Quantitative precipitation of various 3-beta-hydroxysterols with digitonin Can. J. Biochem. 44 1966 119 128
38. S. Buchoux, J. Lai-Kee-Him, M. Garnier, P. Tsan, F. Besson, A. Brisson, and E.J. Dufourc Surfactin-triggered small vesicle formation of negatively charged membranes: a novel membrane-lysis mechanism Biophys. J. 95 2008 3840 3849
39. A. Rantala, D.P. Fewer, M. Hisbergues, L. Rouhiainen, J. Vaitomaa, T. Börner, and K. Sivonen Phylogenetic evidence for the early evolution of microcystin synthesis Proc. Natl. Acad. Sci. U. S. A. 101 2004 568 573
40. C. MacKintosh, K.A. Beattie, S. Klumpp, P. Cohen, and G.A. Codd Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants FEBS Lett. 264 1990 187 192
41. T. Rohrlack, K. Christoffersen, P.E. Hansen, W. Zhang, O. Czarnecki, M. Henning, J. Fastner, M. Erhard, B.A. Neilan, and M. Kaebernick Isolation, characterization, and quantitative analysis of Microviridin J, a new Microcystis metabolite toxic to Daphnia J. Chem. Ecol. 29 2003 1757 1770
42. J. Jokela, L. Herfindal, M. Wahlsten, P. Permi, F. Selheim, V. Vasconcelos, S.O. Doskeland, and K. Sivonen A novel cyanobacterial nostocyclopeptide is a potent antitoxin against microcystin Chembiochem 11 2010 1594 1599
43. L. Herfindal, L.E. Myhren, R. Kleppe, C. Krakstad, F. Selheim, J. Jokela, K. Sivonen, and S.O. Doskeland Nostocyclopeptide-M1: a potent, nontoxic inhibitor of the hepatocyte drug transporters OATP1B3 and 1B1 Mol. Pharm. 8 2011 360 367