Crystal structure and functional mechanism of a human antimicrobial membrane channel

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 12, 2013, Pages 4586-4591

  Song, Chen ^a   Weichbrodt, Conrad ^b   Salnikov, Evgeniy S ^c   Dynowski, Marek ^d,e   Forsberg, Björn O ^a   Bechinger, Burkhard ^c   Steinem, Claudia ^b   De Groot, Bert L ^a   Zachariae, Ulrich ^f   Zeth, Kornelius ^e,g  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c CNRS   (France)

^d UNIVERSITY OF FREIBURG   (Germany)

^e MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

^g CSIC UPV Unidad de Biofisica UBF   (Spain)

Author keywords

Crystallography; Electrophysiology; Ion conduction; Molecular dynamics

Indexed keywords

DERMCIDIN; ZINC;

ARTICLE; BACTERIAL GROWTH; CRYSTAL STRUCTURE; ELECTROPHYSIOLOGY; EPIDERMIS; HOST RESISTANCE; HUMAN; MEMBRANE CHANNEL; MEMBRANE DAMAGE; MEMBRANE PERMEABILITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; X RAY CRYSTALLOGRAPHY;

ANTI-INFECTIVE AGENTS; CRYSTALLOGRAPHY, X-RAY; HUMANS; ION CHANNELS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; PEPTIDES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY;

EID: 84875272220     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1214739110     Document Type: Article

References (55)

1. Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415(6870): 389-395.
2. Hancock RE, Diamond G (2000) The role of cationic antimicrobial peptides in innate host defences. Trends Microbiol 8(9):402-410.
3. Peschel A, Sahl H-G (2006) The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat Rev Microbiol 4(7):529-536.
4. Fjell CD, Hiss JA, Hancock REW, Schneider G (2012) Designing antimicrobial peptides: Form follows function. Nat Rev Drug Discovery 11(1):37-51.
5. Hancock REW, Sahl H-G (2006) Antimicrobial and host-defense peptides as new antiinfective therapeutic strategies. Nat Biotechnol 24(12):1551-1557.
6. Spellberg B, et al.; Infectious Diseases Society of America (2008) The epidemic of antibiotic-resistant infections: A call to action for the medical community from the Infectious Diseases Society of America. Clin Infect Dis 46(2):155-164.
7. Bush K, et al. (2011) Tackling antibiotic resistance. Nat Rev Microbiol 9(12):894-896.
8. Hersh AL, Chambers HF, Maselli JH, Gonzales R (2008) National trends in ambulatory visits and antibiotic prescribing for skin and soft-tissue infections. Arch Intern Med 168(14):1585-1591.
9. Brogden KA (2005) Antimicrobial peptides: Pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3(3):238-250.
10. Melo MN, Ferre R, Castanho MA (2009) Antimicrobial peptides: Linking partition, activity and high membrane-bound concentrations. Nat Rev Microbiol 7(3):245-250.
11. Arouri A, Dathe M, Blume A (2009) Peptide induced demixing in PG/PE lipid mixtures: A mechanism for the specificity of antimicrobial peptides towards bacterial membranes? Biochim Biophys Acta 1788(3):650-659.
12. Gläser R, et al. (2005) Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection. Nat Immunol 6(1):57-64.
13. Schittek B, et al. (2001) Dermcidin: A novel human antibiotic peptide secreted by sweat glands. Nat Immunol 2(12):1133-1137.
14. Ganz T (2003) Defensins: Antimicrobial peptides of innate immunity. Nat Rev Immunol 3(9):710-720.
15. Bardan A, Nizet V, Gallo RL (2004) Antimicrobial peptides and the skin. Expert Opin Biol Ther 4(4):543-549.
16. Paulmann M, et al. (2012) Structure-activity analysis of the dermcidin-derived peptide DCD-1L, an anionic antimicrobial peptide present in human sweat. J Biol Chem 287 (11):8434-8443.
17. Cipáková I, Gasperík J, Hostinová E (2006) Expression and purification of human antimicrobial peptide, dermcidin, in Escherichia coli. Protein Expr Purif 45(2):269-274.
18. Brogden KA, De Lucca AJ, Bland J, Elliott S (1996) Isolation of an ovine pulmonary surfactant-associated anionic peptide bactericidal for Pasteurella haemolytica. Proc Natl Acad Sci USA 93(1):412-416.
19. Eissa A, Amodeo V, Smith CR, Diamandis EP (2011) Kallikrein-related peptidase-8 (KLK8) is an active serine protease in human epidermis and sweat and is involved in a skin barrier proteolytic cascade. J Biol Chem 286(1):687-706.
20. Hessa T, et al. (2005) Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433(7024):377-381.
21. Hessa T, et al. (2007) Molecular code for transmembrane-helix recognition by the Sec61 translocon. Nature 450(7172):1026-1030.
22. Bechinger B, Sizun C (2003) Alignment and structural analysis of membrane polypeptides by15N and31P solid-state NMR spectroscopy. Concepts Magn Reson 18A: 130-145.
23. Bechinger B, Resende JM, Aisenbrey C (2011) The structural and topological analysis of membrane-associated polypeptides by oriented solid-state NMR spectroscopy: Established concepts and novel developments. Biophys Chem 153(2-3):115-125.
24. Murzyn K, Róg T, Pasenkiewicz-Gierula M (2005) Phosphatidylethanolamine-phosphatidylglycerol bilayer as a model of the inner bacterial membrane. Biophys J 88(2): 1091-1103.
25. Yang B, Verkman AS (1997) Water and glycerol permeabilities of aquaporins 1-5 and MIP determined quantitatively by expression of epitope-tagged constructs in Xenopus oocytes. J Biol Chem 272(26):16140-16146.
26. Kutzner C, Grubmüller H, de Groot BL, Zachariae U (2011) Computational electrophysiology: The molecular dynamics of ion channel permeation and selectivity in atomistic detail. Biophys J 101(4):809-817.
27. Hill CP, Yee J, Selsted ME, Eisenberg D (1991) Crystal structure of defensin HNP-3, an amphiphilic dimer: Mechanisms of membrane permeabilization. Science 251(5000): 1481-1485.
28. Terwilliger TC, Weissman L, Eisenberg D (1982) The structure of melittin in the form I crystals and its implication for melittin's lytic and surface activities. Biophys J 37(1): 353-361.
29. Langs DA (1988) Three-dimensional structure at 0.86 A of the uncomplexed form of the transmembrane ion channel peptide gramicidin A. Science 241(4862):188-191.
30. Bechinger B (1997) Structure and functions of channel-forming peptides: Magainins, cecropins, melittin and alamethicin. J Membr Biol 156(3):197-211.
31. Fox RO, Jr., Richards FM (1982) A voltage-gated ion channel model inferred from the crystal structure of alamethicin at 1.5-A resolution. Nature 300(5890):325-330.
32. Roux B (2002) Theoretical and computational models of ion channels. Curr Opin Struct Biol 12(2):182-189.
33. Christensen B, Fink J, Merrifield RB, Mauzerall D (1988) Channel-forming properties of cecropins and related model compounds incorporated into planar lipid membranes. Proc Natl Acad Sci USA 85(14):5072-5076.
34. Kagan BL, Selsted ME, Ganz T, Lehrer RI (1990) Antimicrobial defensin peptides form voltage-dependent ion-permeable channels in planar lipid bilayer membranes. Proc Natl Acad Sci USA 87(1):210-214.
35. Bechinger B (2011) Insights into the mechanisms of action of host defence peptides from biophysical and structural investigations. J Pept Sci 17(5):306-314.
36. Bechinger B, Lohner K (2006) Detergent-like actions of linear amphipathic cationic antimicrobial peptides. Biochim Biophys Acta 1758(9):1529-1539.
37. Kralj JM, Hochbaum DR, Douglass AD, Cohen AE (2011) Electrical spiking in Escherichia coli probed with a fluorescent voltage-indicating protein. Science 333(6040): 345-348.
38. Kabsch W (2010) Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr D Biol Crystallogr 66(Pt 2):133-144.
39. Adams PD, et al. (2011) The Phenix software for automated determination of macromolecular structures. Methods 55(1):94-106.
40. Zwart PH, et al. (2008) Automated structure solution with the PHENIX suite. Methods Mol Biol 426:419-435.
41. Winn MD, et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67(Pt 4):235-242.
42. Cowtan K (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr 62(Pt 9):1002-1011.
43. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66(Pt 4):486-501.
44. Murshudov GN, et al. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr 67(Pt 4):355-367.
45. Aisenbrey C, Bertani P, Bechinger B (2010) Solid-state NMR investigations of membrane- associated antimicrobial peptides. Methods Mol Biol 618:209-233.
46. Michalek M, Salnikov ES, Werten S, Bechinger B (2013) Membrane interactions of the amphipathic amino-terminus of huntingtin. Biochemistry 52(5):847-858.
47. Angelova MI, Dimitrov DS (1986) Liposome electroformation. Faraday Discuss Chem Soc 81:303-311.
48. Angelova M, Dimitrov D (1988) A mechanism of liposome electroformation. Trends in Colloid and Interface Science II, ed Degiorgio V (Springer, Berlin), pp 59-67.
49. Angelova M (2000) Giant vesicles. Perspectives in Supramolecular Chemistry, eds Luisi PL, Walde P (Wiley-Interscience, Chichester, UK), 1st Ed, pp 27-36.
50. Hess B, Kutzner C, Van der Spoel D, Lindahl E (2008) GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Comput 4:435-447.
51. Klauda JB, et al. (2010) Update of the CHARMM all-atom additive force field for lipids: Validation on six lipid types. J Phys Chem B 114(23):7830-7843.
52. Bussi G, Donadio D, Parrinello M (2007) Canonical sampling through velocity rescaling. J Chem Phys 126(1):014101.
53. Essmann U, et al. (1995) A smooth particle mesh Ewald method. J Chem Phys 103: 8577-8593.
54. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM (1997) LINCS: A linear constraint solver for molecular simulations. J Comput Chem 18:1463-1472.
55. Feenstra KA, Hess B, Berendsen HJC (1999) Improving efficiency of large time-scale molecular dynamics simulations of hydrogen-rich systems. J Comput Chem 20: 786-798.