Interaction of Piscidin-1 with zwitterionic versus anionic membranes: a comparative molecular dynamics study

Plasma membrane of each micro-organism has a unique set of lipid composition as a consequence of the environmental adaptation or a response to exposure to antimicrobial peptides (AMPs) as antibiotic agents. Understanding the relationship between lipid composition and action of antimicrobial peptides or considering how different lipid bilayers respond to AMPs may help us design more effective peptide drugs in the future. In this contribution, we intend to elucidate how two currently used membrane models, namely palmitoyl-oleoyl-phosphtidylglycerol (POPG) and 1-palmitoyl-oleoyl-glycero-phosphocholine (POPC), respond to antimicrobial peptide Piscidin-1 (Pis-1).The computed density profile of the peptide as it moves from the bulk solvent toward the membrane core suggests that Pis-1 penetrates into the POPG bilayer less than the POPC membrane. Furthermore, we showed that the two model membranes used in this study have different behavior in the presence of Pis-1. Hence, we suggest that membrane composition could be an important factor in determining lytic ability of peptide drugs to kill a unique bacterial species. An animated interactive 3D complement (I3DC) is available in Proteopedia at http://proteopedia.org/w/Journal:JBSD:37

[1]  T. Wymore,et al.  Molecular dynamics simulation of the structure and dynamics of a dodecylphosphocholine micelle in aqueous solution , 1999 .

[2]  M. Parrinello,et al.  Polymorphic transitions in single crystals: A new molecular dynamics method , 1981 .

[3]  Hoover,et al.  Canonical dynamics: Equilibrium phase-space distributions. , 1985, Physical review. A, General physics.

[4]  R. Larson,et al.  Effect of salt on the interactions of antimicrobial peptides with zwitterionic lipid bilayers. , 2006, Biochimica et biophysica acta.

[5]  Michael R. Yeaman,et al.  Mechanisms of Antimicrobial Peptide Action and Resistance , 2003, Pharmacological Reviews.

[6]  R. B. Nelson,et al.  Effect of lipid composition on buforin II structure and membrane entry , 2008, Proteins.

[7]  Generalized theory of semiflexible polymers. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[8]  Gerrit Groenhof,et al.  GROMACS: Fast, flexible, and free , 2005, J. Comput. Chem..

[9]  William J. Allen,et al.  GridMAT‐MD: A grid‐based membrane analysis tool for use with molecular dynamics , 2009, J. Comput. Chem..

[10]  Mark S. P. Sansom,et al.  Asymmetric Switching in a Homodimeric ABC Transporter: A Simulation Study , 2010, PLoS Comput. Biol..

[11]  Andreas Kukol,et al.  Lipid Models for United-Atom Molecular Dynamics Simulations of Proteins. , 2009, Journal of chemical theory and computation.

[12]  Y. Shai,et al.  Host defense peptides as new weapons in cancer treatment , 2005, Cellular and Molecular Life Sciences CMLS.

[13]  K. Miller.  Structure of a bacterial photosynthetic membrane. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[14]  K Schulten,et al.  VMD: visual molecular dynamics. , 1996, Journal of molecular graphics.

[15]  G. Molle,et al.  Structure and mechanism of action of the antimicrobial peptide piscidin. , 2007, Biochemistry.

[16]  Robert L. Erwin.  Host-defense peptides , 1996, Nature Biotechnology.

[17]  T. Darden,et al.  A smooth particle mesh Ewald method , 1995 .

[18]  Durba Sengupta,et al.  Toroidal pores formed by antimicrobial peptides show significant disorder. , 2008, Biochimica et biophysica acta.

[19]  A. Waring,et al.  Phosphate-mediated arginine insertion into lipid membranes and pore formation by a cationic membrane peptide from solid-state NMR. , 2007, Journal of the American Chemical Society.

[20]  J. Bradshaw,et al.  Cationic Antimicrobial Peptides , 2012, BioDrugs.

[21]  M. Zasloff.  Antimicrobial peptides of multicellular organisms , 2002, Nature.

[22]  D. van der Spoel,et al.  GROMACS: A message-passing parallel molecular dynamics implementation , 1995 .

[23]  W. Delano.  The PyMOL Molecular Graphics System , 2002 .

[24]  C. Yip,et al.  Molecular dynamics simulations of indolicidin association with model lipid bilayers. , 2007, Biophysical journal.

[25]  R. Hancock,et al.  The relationship between peptide structure and antibacterial activity , 2003, Peptides.

[26]  B. Bechinger.  Structure and Function of Membrane-Lytic Peptides , 2004 .

[27]  W. Brey,et al.  Investigating molecular recognition and biological function at interfaces using piscidins, antimicrobial peptides from fish. , 2006, Biochimica et biophysica acta.

[28]  F. Mehrnejad,et al.  Molecular Dynamics Simulation Study of the Interaction of Piscidin 1 with DPPC Bilayers: Structure-Activity Relationship , 2010, Journal of biomolecular structure & dynamics.

[29]  D Peter Tieleman,et al.  Interactions of the designed antimicrobial peptide MB21 and truncated dermaseptin S3 with lipid bilayers: molecular-dynamics simulations. , 2003, The Biochemical journal.

[30]  Yuguang Shi,et al.  Identification and Characterization of a Gene Encoding Human LPGAT1, an Endoplasmic Reticulum-associated Lysophosphatidylglycerol Acyltransferase*[boxs] , 2004, Journal of Biological Chemistry.

[31]  K. Brogden.  Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? , 2005, Nature Reviews Microbiology.

[32]  D P Tieleman,et al.  A computer perspective of membranes: molecular dynamics studies of lipid bilayer systems. , 1997, Biochimica et biophysica acta.

[33]  K. Edwards,et al.  Effect of α-helical peptides on liposome structure: a comparative study of melittin and alamethicin. , 2010, Journal of colloid and interface science.

[34]  S. Singer,et al.  The fluid mosaic model of the structure of cell membranes. , 1972, Science.

[35]  H. Berendsen,et al.  Molecular dynamics with coupling to an external bath , 1984 .

[36]  G. Jürgens,et al.  correction: Peptide antibiotics in mast cells of fish , 2001, Nature.

[37]  T. Darden,et al.  Particle mesh Ewald: An N⋅log(N) method for Ewald sums in large systems , 1993 .

[38]  S. Nosé,et al.  Constant pressure molecular dynamics for molecular systems , 1983 .

[39]  Sushmita Mukherjee,et al.  Membrane domains. , 2004, Annual review of cell and developmental biology.

[40]  L. Bryan,et al.  Inactivation of viruses infecting ectothermic animals by amphibian and piscine antimicrobial peptides. , 2004, Virology.

[41]  K. Hahm,et al.  Solution structure and cell selectivity of piscidin 1 and its analogues. , 2007, Biochemistry.

[42]  W. Dowhan,et al.  Molecular basis for membrane phospholipid diversity: why are there so many lipids? , 1997, Annual review of biochemistry.

[43]  D. Hoskin,et al.  Studies on anticancer activities of antimicrobial peptides. , 2008, Biochimica et biophysica acta.

[44]  M S Sansom,et al.  Lipid properties and the orientation of aromatic residues in OmpF, influenza M2, and alamethicin systems: molecular dynamics simulations. , 1998, Biochemistry.

[45]  Berk Hess,et al.  GROMACS 3.0: a package for molecular simulation and trajectory analysis , 2001 .

[46]  R. Larson,et al.  Binding and insertion of alpha-helical anti-microbial peptides in POPC bilayers studied by molecular dynamics simulations. , 2004, Chemistry and physics of lipids.

[47]  Steven W. Taylor,et al.  Discovery and Characterization of Two Isoforms of Moronecidin, a Novel Antimicrobial Peptide from Hybrid Striped Bass* , 2002, The Journal of Biological Chemistry.

[48]  R. Hancock,et al.  The importance of bacterial membrane composition in the structure and function of aurein 2.2 and selected variants. , 2011, Biochimica et biophysica acta.

[49]  Fang-Yu Chen,et al.  Evidence for membrane thinning effect as the mechanism for peptide-induced pore formation. , 2003, Biophysical journal.

[50]  S. Opella,et al.  Amphipathic antimicrobial piscidin in magnetically aligned lipid bilayers. , 2011, Biophysical journal.

[51]  Berk Hess,et al.  LINCS: A linear constraint solver for molecular simulations , 1997 .

[52]  J. Bradshaw,et al.  Cationic antimicrobial peptides : issues for potential clinical use. , 2003, BioDrugs : clinical immunotherapeutics, biopharmaceuticals and gene therapy.

[53]  E. Lindahl,et al.  The role of lipid composition for insertion and stabilization of amino acids in membranes. , 2009, The Journal of chemical physics.

[54]  E. Dufourc,et al.  Restatement of order parameters in biomembranes: calculation of C-C bond order parameters from C-D quadrupolar splittings. , 1995, Biophysical journal.

[55]  I. Vattulainen,et al.  Atomic-scale structure and electrostatics of anionic palmitoyloleoylphosphatidylglycerol lipid bilayers with Na+ counterions. , 2007, Biophysical journal.