Structural and Thermodynamic Insight into Spontaneous Membrane-Translocating Peptides Across Model PC/PG Lipid Bilayers

Journal of Membrane Biology

Volumn 248, Issue 3, 2015, Pages 505-515

  Hu, Yuan ^a   Patel, Sandeep ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

Anionic lipid; Cell penetrating peptides; Lipid bilayer; Molecular dynamics simulations; Nano arginine; Spontaneous membrane translocating peptides; Umbrella sampling

Indexed keywords

CELL PENETRATING PEPTIDE; PEPTIDE; SPONTANEOUS MEMBRANE TRANSLOCATING PEPTIDE; UNCLASSIFIED DRUG; WATER; 1-PALMITOYL-2-OLEOYLGLYCERO-3-PHOSPHOGLYCEROL; 1-PALMITOYL-2-OLEOYLPHOSPHATIDYLCHOLINE; LIPID BILAYER; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLGLYCEROL;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; ELECTROCHEMICAL IMPEDANCE SPECTROSCOPY; ENTHALPY; ENTROPY; LIPID BILAYER; MEMBRANE COMPONENT; MEMBRANE MODEL; MOLECULAR DYNAMICS; PROTEIN BINDING; PROTEIN LIPID INTERACTION; PROTEIN MOTIF; PROTEIN STRUCTURE; STATIC ELECTRICITY; THERMODYNAMICS; CELL MEMBRANE; CHEMICAL PHENOMENA; CHEMISTRY; KINETICS; PROTEIN STABILITY;

CELL MEMBRANE; CELL-PENETRATING PEPTIDES; ENTROPY; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KINETICS; LIPID BILAYERS; MOLECULAR DYNAMICS SIMULATION; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLGLYCEROLS; PROTEIN STABILITY; THERMODYNAMICS; WATER;

EID: 84914155758     PISSN: 00222631     EISSN: 14321424     Source Type: Journal    
DOI: 10.1007/s00232-014-9702-8     Document Type: Article

References (34)

1. Bangel U (ed) (2006) Handbook of cell penetrating peptides, 2nd edn. CRC, Boca Raton
2. Bechara C, Sagan S (2013) Cell-penetrating peptides: 20 years later, where do we stand? FEBS Lett 587:1693–1702
3. Berendsen HJC, Postma JPM, Gunsteren WFV, DiNola A, Haak JR (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81:3684–3690
4. Cruz J, Mihailescu M, Wiedman G, Herman K, Searson P, Wimley K, Hristova William (2013) A membrane-translocating peptide penetrates into bilayers without significant bilayer perturbations. Biophys J 104(11):2419–2428
5. DeJong DH, Singh G, Bennett WFD, Arnarez C, Wassenaar TA, Schäfer LV, Periole X, Tieleman DP, Marrink SJ (2013) Improved parameters for the martini coarse-grained protein force field. J Chem Theory Comput 9(1):687–697
6. Freites JA, Tobias DJ, White SH (2006) A voltage-sensor water pore. Biophys J 91(11):L90–L92
7. Green M, Loewenstein PM (1988) Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell 55:1179–1188
8. He J, Hristova K, Wimley WC (2012) A highly charged voltage-sensor helix spontaneously translocates across membranes. Angew Chem Int Ed Engl 51(29):7150–7153
9. He J, Kauffman WB, Fuselier T, Naveen SK, Voss TG, Hristova K, Wimley WC (2013) Direct cytosolic delivery of polar cargo to cells by spontaneous membrane-translocating peptides. J Biol Chem. doi:10.1074/Jbc.M113.488312
10. Hess B, Bekker H, JCBerendsen H, GEMFraaije J (1997) LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18(12):1463–1472
11. Hu Y, Ou S, Patel S (2013) Free energetics of arginine permeation into model dmpc lipid bilayers: coupling of effective counterion concentration and lateral bilayer dimensions. J Phys Chem B 117:11641–11653
12. Hu Y, Liu X, Sinha SK, Patel S (2014) Translocation thermodynamics of linear and cyclic nonaarginine into model dppc bilayer via coarse-grained molecular dynamics simulation: Implications of pore formation and nonadditivity. J Phys Chem B 118(10):2670–2682
13. Huang K, García AE (2013) Free energy of translocating an arginine-rich cell-penetrating peptide across a lipid bilayer suggests pore formation. Biophys J 104(2):412–420
14. Järver P, Langel Ü (2006) Cell-penetrating peptides—a brief introduction. Biochim Biophys Acta 1758:260–263
15. Jiao CY, Delaroche D, Burlina F, Alves ID, Chassaing G, Sagan S (2009) Translocation and endocytosis for cell-penetrating peptide internalization. J Biol Chem 284(49):33957–33965
16. Kosuge M, Takeuchi T, Nakase I, Jones AT, Futaki S (2008) Cellular internalization and distribution of arginine-rich peptides as a function of extracellular peptide concentration, serum, and plasma membrane associated proteoglycans. Bioconjug Chem 19(3):656–664
17. Kumar S, Rosenberg JM, Bouzida D, Swendsen RH, Kollman PA (1992) The weighted histogram analysis method for free-energy calculation s on biomolecules. i. The method. J Comp Chem 13(8):1011–1021
18. Laettig-Tuennemann G, Prinz M, Hoffmann D, Behlke J, Palm-Apergi C, Morano I, Herce HD, Cardoso MC (2011) Backbone rigidity and static presentation of guanidinium groups increases cellular uptake of arginine-rich cell-penetrating peptides. Nature Commun 2:1–6
19. Lazaridis T, III JML, PeBenito L (2014) Implicit membrane treatment of buried charged groups: application to peptide translocation across lipid bilayers. Biochim Biophys Acta. http://dx.doi.org/10.1016/j.bbamem.2014.01.015
20. Lin J, Motylinski J, Krauson AJ, Wimley WC, Searson PC, Hristova K (2012) Interactions of membrane active peptides with planar supported bilayers: an impedance spectroscopy study. Langmuir 28(14):6088–6096
21. Lundberg P, Langel Ü (2003) A brief introduction to cell-penetrating peptides. J Mol Recognit 16:227–233
22. Marks JR, Placone J, Hristova K, Wimley WC (2011) Spontaneous membrane-translocating peptides by orthogonal high-throughput screening. J Am Chem Soc 133(23):8995–9004
23. Marrink SJ, Vries AHD, Mark AE (2004) Coarse grained model for semiquantitative lipid simulations. J Phys Chem B 108(2):750–760
24. Monticelli L, Kandasamy SK, Periole X, Larson RG, Tieleman DP, Marrink SJ (2008) The martini coarse-grained force field: extension to proteins. J Chem Theory Comput 4(5):819–834
25. Notman R, Anwar J, Briels W, Noro MG, den Otter W (2008) Simulations of skin barrier function: free energies of hydrophobic and hydrophilic transmembrane pores in ceramide bilayers. Biophys J 95(10):4763
26. Pavan S, Berti F (2011) Short peptides as biosensor transducers. Anal Bioanal Chem 402:3055–3070
27. Saalik P, Niinep A, Pae J, Hansen M, Lubenets D, Langel U, Pooga M (2011) Penetration without cells: membrane translocation of cell-penetrating peptides in the model giant plasma membrane vesicles. J Control Release 153(2):117–125
28. Schmidta N, Mishrab A, Laia GH, Wong GC (2010) Arginine-rich cell-penetrating peptides. FEBS Lett 584:1806–1813
29. Schow EV, Freites JA, Cheng P, Bernsel A, von Heijne G, White SH, Tobias DJ (2011) Arginine in membranes: the connection between molecular dynamics simulations and translocon-mediated insertion experiments. J Membr Biol 239(1–2):35–48
30. Shin MC, Zhang J, Min KA, Lee K, Byun Y, David AE, H He VCY (2013) Cell-penetrating peptides: achievements and challenges in application for cancer treatment. J Biomed Mater Res A 00:00–00
31. Tunnemann G, Ter-Avetisyan G, Martin RM, Stockl M, Herrmann A, Cardoso MC (2009) Live-cell analysis of cell penetration ability and toxicity of oligo-arginines. J Biol Chem 14(4):469–476
32. Walrant A, Matheron L, Cribier S, Chaignepain S, Jobin ML, Sagan S, Alves ID (2013) Direct translocation of cell-penetrating peptides in liposomes: a combined mass spectrometry quantification and fluorescence detection study. Anal Biochem 438(1):1–10
33. Yesylevskyy SO, Schäfer LV, Sengupta D, Marrink SJ (2010) Polarizable water model for the coarse-grained martini force field. PLoS Comput Biol 6(6):e1000810
34. Zorko M, Langel U (2005) Cell-penetrating peptides: mechanism and kinetics of cargo delivery. J Mol Recognit 57:529–545