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High-resolution structures and orientations of antimicrobial peptides piscidin 1 and piscidin 3 in fluid bilayers reveal tilting, kinking, and bilayer immersion.

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Perrin BS, Tian Y, Fu R, Grant CV, Chekmenev EY, Wieczorek WE, Dao AE, Hayden RM, Burzynski CM, Venable RM, Sharma M, Opella SJ, Pastor RW, Cotten ML
OpenAccess logo J Am Chem Soc 136 3491-504 (2014)
Related entries: 2mcu, 2mcv, 2mcx

Cited: 45 times
EuropePMC logo PMID: 24410116

Abstract

While antimicrobial peptides (AMPs) have been widely investigated as potential therapeutics, high-resolution structures obtained under biologically relevant conditions are lacking. Here, the high-resolution structures of the homologous 22-residue long AMPs piscidin 1 (p1) and piscidin 3 (p3) are determined in fluid-phase 3:1 phosphatidylcholine/phosphatidylglycerol (PC/PG) and 1:1 phosphatidylethanolamine/phosphatidylglycerol (PE/PG) bilayers to identify molecular features important for membrane destabilization in bacterial cell membrane mimics. Structural refinement of (1)H-(15)N dipolar couplings and (15)N chemical shifts measured by oriented sample solid-state NMR and all-atom molecular dynamics (MD) simulations provide structural and orientational information of high precision and accuracy about these interfacially bound α-helical peptides. The tilt of the helical axis, τ, is between 83° and 93° with respect to the bilayer normal for all systems and analysis methods. The average azimuthal rotation, ρ, is 235°, which results in burial of hydrophobic residues in the bilayer. The refined NMR and MD structures reveal a slight kink at G13 that delineates two helical segments characterized by a small difference in their τ angles (<10°) and significant difference in their ρ angles (~25°). Remarkably, the kink, at the end of a G(X)4G motif highly conserved among members of the piscidin family, allows p1 and p3 to adopt ρ angles that maximize their hydrophobic moments. Two structural features differentiate the more potent p1 from p3: p1 has a larger ρ angle and less N-terminal fraying. The peptides have comparable depths of insertion in PC/PG, but p3 is 1.2 Å more deeply inserted than p1 in PE/PG. In contrast to the ideal α-helical structures typically assumed in mechanistic models of AMPs, p1 and p3 adopt disrupted α-helical backbones that correct for differences in the amphipathicity of their N- and C-ends, and their centers of mass lie ~1.2-3.6 Å below the plane defined by the C2 atoms of the lipid acyl chains.

Articles - 2mcw mentioned but not cited (4)

  1. High-resolution structures and orientations of antimicrobial peptides piscidin 1 and piscidin 3 in fluid bilayers reveal tilting, kinking, and bilayer immersion. Perrin BS, Tian Y, Fu R, Grant CV, Chekmenev EY, Wieczorek WE, Dao AE, Hayden RM, Burzynski CM, Venable RM, Sharma M, Opella SJ, Pastor RW, Cotten ML. J. Am. Chem. Soc. 136 3491-3504 (2014)
  2. A Practical Implicit Membrane Potential for NMR Structure Calculations of Membrane Proteins. Tian Y, Schwieters CD, Opella SJ, Marassi FM. Biophys. J. 109 574-585 (2015)
  3. Structure and Function in Antimicrobial Piscidins: Histidine Position, Directionality of Membrane Insertion, and pH-Dependent Permeabilization. Mihailescu M, Sorci M, Seckute J, Silin VI, Hammer J, Perrin BS, Hernandez JI, Smajic N, Shrestha A, Bogardus KA, Greenwood AI, Fu R, Blazyk J, Pastor RW, Nicholson LK, Belfort G, Cotten ML. J Am Chem Soc 141 9837-9853 (2019)
  4. Metal-ion Binding to Host Defense Peptide Piscidin 3 Observed in Phospholipid Bilayers by Magic Angle Spinning Solid-state NMR. Rai RK, De Angelis A, Greenwood A, Opella SJ, Cotten ML. Chemphyschem 20 295-301 (2019)


Reviews citing this publication (10)

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  9. Deuterium Solid State NMR Studies of Intact Bacteria Treated With Antimicrobial Peptides. Booth V. Front Med Technol 2 621572 (2020)
  10. Antimicrobial peptides: biochemical determinants of activity and biophysical techniques of elucidating their functionality. Shagaghi N, Palombo EA, Clayton AHA, Bhave M. World J. Microbiol. Biotechnol. 34 62 (2018)

Articles citing this publication (31)

  1. Anti-inflammatory activities of cecropin A and its mechanism of action. Lee E, Shin A, Kim Y. Arch. Insect Biochem. Physiol. 88 31-44 (2015)
  2. Dynamic Nuclear Polarization as an Enabling Technology for Solid State Nuclear Magnetic Resonance Spectroscopy. Smith AN, Long JR. Anal. Chem. 88 122-132 (2016)
  3. Role of phenylalanine and valine10 residues in the antimicrobial activity and cytotoxicity of piscidin-1. Lee E, Shin A, Jeong KW, Jin B, Jnawali HN, Shin S, Shin SY, Kim Y. PLoS ONE 9 e114453 (2014)
  4. A polyalanine peptide derived from polar fish with anti-infectious activities. Cardoso MH, Ribeiro SM, Nolasco DO, de la Fuente-Núñez C, Felício MR, Gonçalves S, Matos CO, Liao LM, Santos NC, Hancock RE, Franco OL, Migliolo L. Sci Rep 6 21385 (2016)
  5. Membrane interactions of phylloseptin-1, -2, and -3 peptides by oriented solid-state NMR spectroscopy. Resende JM, Verly RM, Aisenbrey C, Cesar A, Bertani P, Piló-Veloso D, Bechinger B. Biophys. J. 107 901-911 (2014)
  6. Antimicrobial Peptides Share a Common Interaction Driven by Membrane Line Tension Reduction. Henderson JM, Waring AJ, Separovic F, Lee KYC. Biophys. J. 111 2176-2189 (2016)
  7. Engineering monolayer poration for rapid exfoliation of microbial membranes. Pyne A, Pfeil MP, Bennett I, Ravi J, Iavicoli P, Lamarre B, Roethke A, Ray S, Jiang H, Bella A, Reisinger B, Yin D, Little B, Muñoz-García JC, Cerasoli E, Judge PJ, Faruqui N, Calzolai L, Henrion A, Martyna GJ, Grovenor CRM, Crain J, Hoogenboom BW, Watts A, Ryadnov MG. Chem Sci 8 1105-1115 (2017)
  8. Solid-state NMR and membrane proteins. Opella SJ. J. Magn. Reson. 253 129-137 (2015)
  9. The Curvature Induction of Surface-Bound Antimicrobial Peptides Piscidin 1 and Piscidin 3 Varies with Lipid Chain Length. Perrin BS, Sodt AJ, Cotten ML, Pastor RW. J. Membr. Biol. 248 455-467 (2015)
  10. The cooperative behaviour of antimicrobial peptides in model membranes. Wang J, Mura M, Zhou Y, Pinna M, Zvelindovsky AV, Dennison SR, Phoenix DA. Biochim. Biophys. Acta 1838 2870-2881 (2014)
  11. Piscidin-1-analogs with double L- and D-lysine residues exhibited different conformations in lipopolysaccharide but comparable anti-endotoxin activities. Kumar A, Mahajan M, Awasthi B, Tandon A, Harioudh MK, Shree S, Singh P, Shukla PK, Ramachandran R, Mitra K, Bhattacharjya S, Ghosh JK. Sci Rep 7 39925 (2017)
  12. Cosolvent, ions, and temperature effects on the structural properties of Cecropin A-Magainin 2 hybrid peptide in solutions. Sarukhanyan E, Milano G, Roccatano D. Biopolymers 103 1-14 (2015)
  13. Expression, purification, and micelle reconstitution of antimicrobial piscidin 1 and piscidin 3 for NMR studies. Chen W, Cotten ML. Protein Expr. Purif. 102 63-68 (2014)
  14. Influence of membrane composition on the binding and folding of a membrane lytic peptide from the non-enveloped flock house virus. Nangia S, May ER. Biochim Biophys Acta Biomembr 1859 1190-1199 (2017)
  15. Nuclease activity gives an edge to host-defense peptide piscidin 3 over piscidin 1, rendering it more effective against persisters and biofilms. Libardo MDJ, Bahar AA, Ma B, Fu R, McCormick LE, Zhao J, McCallum SA, Nussinov R, Ren D, Angeles-Boza AM, Cotten ML. FEBS J. 284 3662-3683 (2017)
  16. Switching Cytolytic Nanopores into Antimicrobial Fractal Ruptures by a Single Side Chain Mutation. Hammond K, Cipcigan F, Al Nahas K, Losasso V, Lewis H, Cama J, Martelli F, Simcock PW, Fletcher M, Ravi J, Stansfeld PJ, Pagliara S, Hoogenboom BW, Keyser UF, Sansom MSP, Crain J, Ryadnov MG. ACS Nano 15 9679-9689 (2021)
  17. A Potent Host Defense Peptide Triggers DNA Damage and Is Active against Multidrug-Resistant Gram-Negative Pathogens. Juliano SA, Serafim LF, Duay SS, Heredia Chavez M, Sharma G, Rooney M, Comert F, Pierce S, Radulescu A, Cotten ML, Mihailescu M, May ER, Greenwood AI, Prabhakar R, Angeles-Boza AM. ACS Infect Dis 6 1250-1263 (2020)
  18. Copper regulates the interactions of antimicrobial piscidin peptides from fish mast cells with formyl peptide receptors and heparin. Kim SY, Zhang F, Gong W, Chen K, Xia K, Liu F, Gross R, Wang JM, Linhardt RJ, Cotten ML. J. Biol. Chem. 293 15381-15396 (2018)
  19. Histidine-Mediated Ion Specific Effects Enable Salt Tolerance of a Pore-Forming Marine Antimicrobial Peptide. Xian W, Hennefarth MR, Lee MW, Do T, Lee EY, Alexandrova AN, Wong GCL. Angew Chem Int Ed Engl 61 e202108501 (2022)
  20. Folding a viral peptide in different membrane environments: pathway and sampling analyses. Nangia S, Pattis JG, May ER. J Biol Phys 44 195-209 (2018)
  21. Lipid-Mediated Interactions between the Antimicrobial Peptides Magainin 2 and PGLa in Bilayers. Harmouche N, Bechinger B. Biophys. J. 115 1033-1044 (2018)
  22. The host-defense peptide piscidin P1 reorganizes lipid domains in membranes and decreases activation energies in mechanosensitive ion channels. Comert F, Greenwood A, Maramba J, Acevedo R, Lucas L, Kulasinghe T, Cairns LS, Wen Y, Fu R, Hammer J, Blazyk J, Sukharev S, Cotten ML, Mihailescu M. J. Biol. Chem. 294 18557-18570 (2019)
  23. Tuneable poration: host defense peptides as sequence probes for antimicrobial mechanisms. Pfeil MP, Pyne ALB, Losasso V, Ravi J, Lamarre B, Faruqui N, Alkassem H, Hammond K, Judge PJ, Winn M, Martyna GJ, Crain J, Watts A, Hoogenboom BW, Ryadnov MG. Sci Rep 8 14926 (2018)
  24. An optimized antimicrobial peptide analog acts as an antibiotic adjuvant to reverse methicillin-resistant Staphylococcus aureus. Chen X, Wu X, Wang S. NPJ Sci Food 6 57 (2022)
  25. Antimicrobial Activity and Action Mechanisms of Arg-Rich Short Analog Peptides Designed from the C-Terminal Loop Region of American Oyster Defensin (AOD). Seo JK, Kim DG, Lee JE, Park KS, Lee IA, Lee KY, Kim YO, Nam BH. Mar Drugs 19 451 (2021)
  26. Copper-binding anticancer peptides from the piscidin family: an expanded mechanism that encompasses physical and chemical bilayer disruption. Comert F, Heinrich F, Chowdhury A, Schoeneck M, Darling C, Anderson KW, Libardo MDJ, Angeles-Boza AM, Silin V, Cotten ML, Mihailescu M. Sci Rep 11 12620 (2021)
  27. Host Defense Peptide Piscidin and Yeast-Derived Glycolipid Exhibit Synergistic Antimicrobial Action through Concerted Interactions with Membranes. Liu F, Greenwood AI, Xiong Y, Miceli RT, Fu R, Anderson KW, McCallum SA, Mihailescu M, Gross R, Cotten ML. JACS Au 3 3345-3365 (2023)
  28. How Oxygen Availability Affects the Antimicrobial Efficacy of Host Defense Peptides: Lessons Learned from Studying the Copper-Binding Peptides Piscidins 1 and 3. Oludiran A, Courson DS, Stuart MD, Radwan AR, Poutsma JC, Cotten ML, Purcell EB. Int J Mol Sci 20 (2019)
  29. Mechanistic Insight into the Early Stages of Toroidal Pore Formation by the Antimicrobial Peptide Smp24. Bertelsen M, Lacey MM, Nichol T, Miller K. Pharmaceutics 15 2399 (2023)
  30. Revealing weak histidine 15N homonuclear scalar couplings using Solid-State Magic-Angle-Spinning NMR spectroscopy. Tan C, Chen Y, Peng X, Chen Z, Cai S, Cross TA, Fu R. J Magn Reson 316 106757 (2020)
  31. The effect of metalation on antimicrobial piscidins imbedded in normal and oxidized lipid bilayers. Dreab A, Bayse CA. RSC Chem Biol 4 573-586 (2023)


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