Structure and function of a unique pore-forming protein from a pathogenic acanthamoeba

Nature Chemical Biology

Volumn 9, Issue 1, 2013, Pages 37-42

  Michalek, Matthias ^a   Sönnichsen, Frank D ^a   Wechselberger, Rainer ^b   Dingley, Andrew J ^c   Hung, Chien Wen ^a   Kopp, Annika ^d   Wienk, Hans ^b   Simanski, Maren ^a   Herbst, Rosa ^a   Lorenzen, Inken ^a   Marciano Cabral, Francine ^e   Gelhaus, Christoph ^a   Gutsmann, Thomas ^d   Tholey, Andreas ^a   Grötzinger, Joachim ^a   Leippe, Matthias ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

^d RESEARCH CENTER BORSTEL   (Germany)

^e VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACANTHAPORIN; DIMER; PORE FORMING CYTOTOXIC PROTEIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ACANTHAMOEBA; ACANTHAMOEBA CULBERTSONI; ANTIMICROBIAL ACTIVITY; ARTICLE; CHANNEL GATING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CYTOTOXICITY; DIMERIZATION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HUMAN; HUMAN CELL; MEMBRANE PERMEABILITY; MOLECULAR CLONING; MOLECULAR MODEL; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE;

ACANTHAMOEBA; ACANTHAMOEBA CULBERTSONI; ACANTHAMOEBIDAE; BACTERIA (MICROORGANISMS); ENTAMOEBA HISTOLYTICA; PROTOZOA;

EID: 84871269910     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1116     Document Type: Article

References (46)

1. Leippe, M. Antimicrobial and cytolytic polypeptides of amoeboid protozoa - effector molecules of primitive phagocytes. Dev. Comp. Immunol. 23, 267-279 (1999).
2. Herbst, R. et al. Pore-forming polypeptides of the pathogenic protozoon Naegleria fowleri. J. Biol. Chem. 277, 22353-22360 (2002).
3. Herbst, R., Marciano-Cabral, F. & Leippe, M. Antimicrobial and pore-forming peptides of free-living and potentially highly pathogenic Naegleria fowleri are released from the same precursor molecule. J. Biol. Chem. 279, 25955-25958 (2004).
4. Hecht, O. et al. Solution structure of the pore-forming protein of Entamoeba histolytica. J. Biol. Chem. 279, 17834-17841 (2004).
5. Kolter, T., Winau, F., Schaible, U.E., Leippe, M. & Sandhoff, K. Lipid-binding proteins in membrane digestion, antigen presentation, and antimicrobial defense. J. Biol. Chem. 280, 41125-41128 (2005).
6. Liepinsh, E., Andersson, M., Ruysschaert, J.M. & Otting, G. Saposin fold revealed by the NMR structure of NK-lysin. Nat. Struct. Biol. 4, 793-795 (1997).
7. Anderson, D.H. et al. Granulysin crystal structure and a structure-derived lytic mechanism. J. Mol. Biol. 325, 355-365 (2003).
8. Leippe, M., Bruhn, H., Hecht, O. & Grötzinger, J. Ancient weapons: the three-dimensional structure of amoebapore A. Trends Parasitol. 21, 5-7 (2005).
9. Marciano-Cabral, F. & Cabral, G. Acanthamoeba spp. as agents of disease in humans. Clin. Microbiol. Rev. 16, 273-307 (2003).
10. Martinez, A.J. Free-living amebas: infection of the central nervous system. Mt. Sinai J. Med. 60, 271-278 (1993).
11. Visvesvara, G.S. Amebic meningoencephalitides and keratitis: challenges in diagnosis and treatment. Curr. Opin. Infect. Dis. 23, 590-594 (2010).
12. Greub, G. & Raoult, D. Microorganisms resistant to free-living amoebae. Clin. Microbiol. Rev. 17, 413-433 (2004).
13. Ellman, G.L. Tissue sulfhydryl groups. Arch. Biochem. Biophys. 82, 70-77 (1959).
14. Holm, L., Kaariainen, S., Rosenstrom, P. & Schenkel, A. Searching protein structure databases with DaliLite v.3. Bioinformatics 24, 2780-2781 (2008).
15. Madej, T., Gibrat, J.F. & Bryant, S.H. Threading a database of protein cores. Proteins 23, 356-369 (1995).
16. Gibrat, J.F., Madej, T. & Bryant, S.H. Surprising similarities in structure comparison. Curr. Opin. Struct. Biol. 6, 377-385 (1996).
17. Andrä, J., Herbst, R. & Leippe, M. Amoebapores, archaic effector peptides of protozoan origin, are discharged into phagosomes and kill bacteria by permeabilizing their membranes. Dev. Comp. Immunol. 27, 291-304 (2003).
18. Yeaman, M.R. & Yount, N.Y. Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev. 55, 27-55 (2003).
19. Rötzschke, O., Lau, J.M., Hofstatter, M., Falk, K. & Strominger, J.L. A pH-sensitive histidine residue as control element for ligand release from HLA-DR molecules. Proc. Natl. Acad. Sci. USA 99, 16946-16950 (2002).
20. Baumann, G. & Mueller, P. A molecular model of membrane excitability. J. Supramol. Struct. 2, 538-557 (1974).
21. Shai, Y. 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 (1999).
22. Yang, L., Harroun, T.A., Weiss, T.M., Ding, L. & Huang, H.W. Barrel-stave model or toroidal model? A case study on melittin pores. Biophys. J. 81, 1475-1485 (2001).
23. Anderluh, G. & Lakey, J.H. Disparate proteins use similar architectures to damage membranes. Trends Biochem. Sci. 33, 482-490 (2008).
24. Jenssen, H., Hamill, P. & Hancock, R.E. Peptide antimicrobial agents. Clin. Microbiol. Rev. 19, 491-511 (2006).
25. Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature 415, 389-395 (2002).
26. Gutsmann, T. et al. Interaction of amoebapores and NK-lysin with symmetric phospholipid and asymmetric lipopolysaccharide/phospholipid bilayers. Biochemistry 42, 9804-9812 (2003).
27. Leippe, M., Andrä, J., Nickel, R., Tannich, E. & Müller-Eberhard, H.J. Amoebapores, a family of membranolytic peptides from cytoplasmic granules of Entamoeba histolytica: isolation, primary structure, and pore formation in bacterial cytoplasmic membranes. Mol. Microbiol. 14, 895-904 (1994).
28. Schägger, H. & von Jagow, G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368 (1987).
29. Frohman, M.A., Dush, M.K. & Martin, G.R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc. Natl. Acad. Sci. USA 85, 8998-9002 (1988).
30. Scotto-Lavino, E., Du, G. & Frohman, M.A. 3′ end cDNA amplification using classic RACE. Nat. Protoc. 1, 2742-2745 (2006).
31. LaVallie, E.R. et al. A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. coli cytoplasm. Bio/Technology 11, 187-193 (1993).
32. Dingley, A.J., Lorenzen, I. & Grötzinger, J. NMR analysis of viral protein structures. Methods Mol. Biol. 451, 441-462 (2008).
33. Markley, J.L. et al. Recommendations for the presentation of NMR structures of proteins and nucleic acids. J. Mol. Biol. 280, 933-952 (1998).
34. Delaglio, F. et al. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995).
35. Goddard, T. & Kneller, D. SPARKY 3 (University of San Francisco, California, USA.)
36. Johnson, B.A. Using NMR-View to visualize and analyze the NMR spectra of macromolecules. Methods Mol. Biol. 278, 313-352 (2004).
37. Güntert, P. Automated NMR structure calculation with CYANA. Methods Mol. Biol. 278, 353-378 (2004).
38. Schwieters, C.D., Kuszewski, J.J., Tjandra, N. & Clore, G.M. The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson. 160, 65-73 (2003).
39. Linge, J.P., Williams, M.A., Spronk, C.A., Bonvin, A.M. & Nilges, M. Refinement of protein structures in explicit solvent. Proteins 50, 496-506 (2003).
40. Koradi, R., Billeter, M. & Wuthrich, K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14, 51-55, 29-32 (1996).
41. Andrä, J. & Leippe, M. Pore-forming peptide of Entamoeba histolytica. Significance of positively charged amino acid residues for its mode of action. FEBS Lett. 354, 97-102 (1994).
42. Montal, M. & Mueller, P. Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties. Proc. Natl. Acad. Sci. USA 69, 3561-3566 (1972).
43. Dougherty, R.M., Galli, C., Ferro-Luzzi, A. & Iacono, J.M. Lipid and phospholipid fatty acid composition of plasma, red blood cells, and platelets and how they are affected by dietary lipids: a study of normal subjects from Italy, Finland, and the USA. Am. J. Clin. Nutr. 45, 443-455 (1987).
44. Bruhn, H., Riekens, B., Berninghausen, O. & Leippe, M. Amoebapores and NK-lysin, members of a class of structurally distinct antimicrobial and cytolytic peptides from protozoa and mammals: a comparative functional analysis. Biochem. J. 375, 737-744 (2003).
45. Boman, H.G., Nilsson-Faye, I., Paul, K. & Rasmuson, T. Jr. Insect immunity. I. Characteristics of an inducible cell-free antibacterial reaction in hemolymph of Samia cynthia pupae. Infect. Immun. 10, 136-145 (1974).
46. Leippe, M., Ebel, S., Schoenberger, O.L., Horstmann, R.D. & Müller-Eberhard, H.J. Pore-forming peptide of pathogenic Entamoeba histolytica. Proc. Natl. Acad. Sci. USA 88, 7659-7663 (1991).