Preassembly of membrane-active peptides is an important factor in their selectivity toward target cells

Biochemistry. 2002 Oct 1;41(39):11921-30. doi: 10.1021/bi0260482.

Abstract

Membrane-active peptides comprise a large group of toxins used in the defense and offense systems of all organisms including plants and humans. They act on diverse targets including microorganisms and mammalian cells, but the factors that determine their target cell selectivity are not yet clear. Here, we tested the role of peptide length and preassembly on the ability of diastereomeric cationic antimicrobial peptides to discriminate among bacteria, erythrocytes, and fungal cells, by using peptides with variable lengths (13, 16, and 19 amino acids long) and their covalently linked pentameric bundles. All the bundles expressed similar potent antifungal activity (minimal inhibitory concentration of 0.2-0.3 microM) and high antimicrobial activity. Hemolytic activity was also observed at concentrations higher than those required for antifungal activity. In contrast, all the monomers showed length-dependent antimicrobial activity, were less active toward bacteria and fungi, and were devoid of hemolytic activity. BIAcore biosensor experiments revealed a approximately 300-fold increase in peptide-membrane binding affinity between the 13- and 19-residue monomers toward zwitterionic (egg phosphatidylcholine (PC)/egg spingomyelin (SM)/cholesterol) vesicles. All the monomeric peptides display a similar high affinity to negatively charged (E. coli phosphatidylethanolamine (PE)/egg phosphatidylglycerol (PG)) vesicles regardless of their length. In contrast, irrespective of the size of the monomeric subunit, all the bundles bind irreversibly and strongly disrupt both PC/SM/cholesterol and PE/PG membranes. Attenuated total reflectance Fourier-transform infrared spectroscopy revealed that peptide assembly also affects structure as observed by an increased alpha-helical and beta-sheet content in membranes and enhances acyl chain disruption of PC/cholesterol. The correlation between the antibacterial activity and ability to depolarize the transmembrane potential of E. coli spheroplasts, as well as the ability to induce calcein release from vesicles, suggests that the bacterial membrane is their target. The data demonstrate that preassembly of cationic diastereomeric antimicrobial peptides is an essential factor in their membrane targeting.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acinetobacter baumannii / drug effects
  • Acinetobacter baumannii / growth & development
  • Amino Acid Sequence
  • Anti-Bacterial Agents
  • Anti-Infective Agents / chemical synthesis
  • Anti-Infective Agents / metabolism
  • Anti-Infective Agents / pharmacology
  • Antifungal Agents / chemical synthesis
  • Antifungal Agents / metabolism
  • Antifungal Agents / pharmacology
  • Antimicrobial Cationic Peptides / chemical synthesis
  • Antimicrobial Cationic Peptides / metabolism*
  • Antimicrobial Cationic Peptides / pharmacology
  • Biosensing Techniques
  • Cryptococcus neoformans / drug effects
  • Cryptococcus neoformans / growth & development
  • Enterobacter cloacae / drug effects
  • Enterobacter cloacae / growth & development
  • Escherichia coli / drug effects
  • Escherichia coli / growth & development
  • Fluoresceins / metabolism
  • Hemolysis / drug effects
  • Humans
  • Liposomes / metabolism
  • Membrane Potentials
  • Membrane Proteins / chemical synthesis
  • Membrane Proteins / metabolism*
  • Membrane Proteins / pharmacology
  • Molecular Sequence Data
  • Phosphatidylcholines / chemistry
  • Phosphatidylethanolamines / chemistry
  • Phosphatidylglycerols / chemistry
  • Phospholipids / metabolism*
  • Protein Binding
  • Protein Processing, Post-Translational*
  • Protein Structure, Secondary
  • Spectroscopy, Fourier Transform Infrared / methods
  • Staphylococcus aureus / drug effects
  • Staphylococcus aureus / growth & development
  • Stereoisomerism

Substances

  • Anti-Bacterial Agents
  • Anti-Infective Agents
  • Antifungal Agents
  • Antimicrobial Cationic Peptides
  • Fluoresceins
  • Liposomes
  • Membrane Proteins
  • Phosphatidylcholines
  • Phosphatidylethanolamines
  • Phosphatidylglycerols
  • Phospholipids
  • fluorexon