Effect of amphipathic HIV fusion inhibitor peptides on POPC and POPC/Cholesterol membrane properties: A molecular simulation study

International Journal of Molecular Sciences

Volumn 14, Issue 7, 2013, Pages 14724-14743

  Martins do Canto, António M T ^a,b   Palace Carvalho, Alfredo J ^a,b   Prates Ramalho, João P ^a,b   Loura, Luís M S ^c,d  

^a UNIVERSITY OF ÉVORA   (Portugal)

^b Évora Chemistry Center   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

AIDS; Enfuvirtide; HIV fusion inhibitor; Lipid bilayer; Lipid peptide interaction; Molecular dynamics

Indexed keywords

2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; ENFUVIRTIDE; TIFUVIRTIDE;

ARTICLE; BILAYER MEMBRANE; BINDING AFFINITY; CONTROLLED STUDY; DIFFUSION COEFFICIENT; DRUG ADSORPTION; DRUG BINDING; HYDROGEN BOND; LIPID MEMBRANE; MOLECULAR DYNAMICS;

CHOLESTEROL; HIV; HIV ENVELOPE PROTEIN GP41; HIV FUSION INHIBITORS; HUMANS; HYDROGEN BONDING; LIPID BILAYERS; MOLECULAR DYNAMICS SIMULATION; PEPTIDE FRAGMENTS; PEPTIDES; PHOSPHATIDYLCHOLINES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84880214958     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140714724     Document Type: Article

References (45)

1. Matthews, T.; Salgo, M.; Greenberg, M.; Chung, J.; DeMasi, R.; Bolognesi, D. Enfuvirtide: The first therapy to inhibit the entry of HIV-1 into host CD4 lymphocytes. Nat. Rev. Drug. Discov. 2004, 3, 215-225.
2. Eron, J.J.; Gulick, R.M.; Bartlett, J.A.; Merigan, T.; Arduino, R.; Kilby, J.M.; Yangco, B.; Diers, A.; Drobnes, C.; DeMasi, R.; et al. Short-term safety and antiretroviral activity of T-1249, a second-generation fusion inhibitor of HIV. J. Infect. Dis. 2004, 189, 1075-1083.
3. Colman, P.M.; Lawrence, M.C. The structural biology of type I viral membrane fusion. Nat. Rev. Mol. Cell Biol. 2003, 4, 309-319.
4. Lawless, M.K.; Barney, S.; Guthrie, K.I.; Bucy, T.B.; Petteway, S.R., Jr.; Merutka, G. HIV-1 membrane fusion mechanism: Structural studies of the interactions between biologically-active peptides from gp41. Biochemistry 1996, 35, 13697-13708.
5. Naider, F.; Anglister, J. Peptides in the treatment of AIDS. Curr. Opin. Struct. Biol. 2009, 19, 473-482.
6. Pan, C.; Liu, S.; Jiang, S. HIV-1 gp41 fusion intermediate: a target for HIV therapeutics. J. Formos. Med. Assoc. 2010, 109, 94-105.
7. Chan, D.C.; Fass, D.; Berger, J.M.; Kim, P.S. Core structure of gp41 from the HIV envelope glycoprotein. Cell 1997, 89, 263-273.
8. Wild, C.T.; Shugars, D.C.; Greenwell, T.K.; McDanal, C.B.; Matthews, T.J. Peptides corresponding to a predictive alpha-helical domain of human immunodeficiency virus type 1 gp41 are potent inhibitors of virus infection. Proc. Natl. Acad. Sci. USA 1994, 91, 9770-9774.
9. Baldwin, C.E.; Sanders, R.W.; Berkhout, B. Inhibiting HIV-1 entry with fusion inhibitors. Curr. Med. Chem. 2003, 10, 1633-1642.
10. Liu, S.; Jing, W.; Cheung, B.; Lu, H.; Sun, J.; Yan, X.; Niu, J.; Farmar, J.; Wu, S.; Jiang, S. HIV gp41 C-terminal heptad repeat contains multifunctional domains. Relation to mechanisms of action of anti-HIV peptides. J. Biol. Chem. 2007, 282, 9612-9620.
11. Kilby, J.M.; Eron, J.J. Novel therapies based on mechanisms of HIV-1 cell entry. N. Engl. J. Med. 2003, 348, 2228-2238.
12. Cooley, L.A.; Lewin, S.R. HIV-1 cell entry and advances in viral entry inhibitor therapy. J. Clin. Virol. 2003, 26, 121-132.
13. Dwyer, J.J.; Wilson, K.L.; Davison, D.K.; Freel, S.A.; Seedorff, J.E.; Wring, S.A.; Tvermoes, N.A.; Matthews, T.J.; Greenberg, M.L.; Delmedico, M.K. Design of helical, oligomeric HIV-1 fusion inhibitor peptides with potent activity against enfuvirtide-resistant virus. Proc. Natl. Acad. Sci. USA 2007, 104, 12772-12777.
14. Otaka, A.; Nakamura, M.; Nameki, D.; Kodama, E.; Uchiyama, S.; Nakamura, S.; Nakano, H.; Tamamura, H.; Kobayashi, Y.; Matsuoka, M.; et al. Remodeling of gp41-C34 peptide leads to highly effective inhibitors of the fusion of HIV-1 with target cells. Angew. Chem. Int. Ed. Engl. 2002, 41, 2937-2940.
15. Veiga, S.; Henriques, S.; Santos, N.C.; Castanho, M. Putative role of membranes in the HIV fusion inhibitor enfuvirtide mode of action at the molecular level. Biochem. J. 2004, 377, 107-110.
16. Nishikawa, H.; Oishi, S.; Fujita, M.; Watanabe, K.; Tokiwa, R.; Ohno, H.; Kodama, E.; Izumi, K.; Kajiwara, K.; Naitoh, T.; et al. Identification of minimal sequence for HIV-1 fusion inhibitors. Bioorg. Med. Chem. 2008, 16, 9184-9187.
17. Veiga, A.S.; Santos, N.C.; Loura, L.M.; Fedorov, A.; Castanho, M.A. HIV fusion inhibitor peptide T-1249 is able to insert or adsorb to lipidic bilayers. Putative correlation with improved efficiency. J. Am. Chem. Soc. 2004, 126, 14758-14763.
18. Martins do Canto, A.M.T.; Carvalho, A.J.P.; Ramalho, J.P.P.; Loura, L.M.S. Structure and conformation of HIV fusion inhibitor peptide T-1249 in presence of model membranes: A molecular dynamics study. J. Mol. Struct. THEOCHEM 2010, 946, 119-124.
19. Martins do Canto, A.M.T.; Carvalho, A.J.; Ramalho, J.P.; Loura, L.M. Molecular dynamics simulations of T-20 HIV fusion inhibitor interacting with model membranes. Biophys. Chem. 2011, 159, 275-286.
20. Martins do Canto, A.M.T.; Palace Carvalho, A.J.; Prates Ramalho, J.P.; Loura, L.M. Molecular dynamics simulation of HIV fusion inhibitor T-1249: Insights on peptide-lipid interaction. Comput. Math. Methods Med. 2012, 2012, doi:10.1155/2012/151854.
21. Matos, P.M.; Castanho, M.A.; Santos, N.C. HIV-1 fusion inhibitor peptides enfuvirtide and T-1249 interact with erythrocyte and lymphocyte membranes. PLoS One 2010, 5, doi:10.1371/journal.pone.0009830.
22. Hofsass, C.; Lindahl, E.; Edholm, O. Molecular dynamics simulations of phospholipid bilayers with cholesterol. Biophys. J. 2003, 84, 2192-2206.
23. Dai, J.; Alwarawrah, M.; Huang, J. Instability of cholesterol clusters in lipid bilayers and the cholesterol's Umbrella effect. J. Phys. Chem. B 2010, 114, 840-848.
24. GROMACS Version 3.3 User Manual. Available online: ftp://ftp.gromacs.org/pub/manual/ manual-3.3.pdf (accessed on 1 June 2013).
25. Anezo, C.; de Vries, A.H.; Holtje, H.D.; Tieleman, D.P.; Marrink, S.J. Methodological issues in lipid bilayer simulations. J. Phys. Chem. B 2003, 107, 9424-9433.
26. Lindahl, E.; Edholm, O. Molecular dynamics simulation of NMR relaxation rates and slow dynamics in lipid bilayers. J. Chem. Phys. 2001, 115, 4938-4950.
27. Loura, L.M.; Ramalho, J.P. Location and dynamics of acyl chain NBD-labeled phosphatidylcholine (NBD-PC) in DPPC bilayers. A molecular dynamics and time-resolved fluorescence anisotropy study. Biochim. Biophys. Acta 2007, 1768, 467-478.
28. Pandit, S.A.; Jakobsson, E.; Scott, H.L. Simulation of the early stages of nano-domain formation in mixed bilayers of sphingomyelin, cholesterol, and dioleylphosphatidylcholine. Biophys. J. 2004, 87, 3312-3322.
29. Arguslab, version 4.0.1.; software for molecular modeling; Medio Systems Inc.: Seattle, WA, USA, 2004.
30. Berendsen, H.J.C.; Postma, J.P.M.; van Gunsteren, W.F.; Hermans, J. Interaction Models for Water in Relation to Protein Hydration. In Intermolecular Forces; Pullman, B., Ed.; D. Models Publishing Company: Dordrecht, The Netherlands, 1981; pp. 331-342.
31. Biocomputing Group, University of Calgary. Available online: http://wcm.ucalgary.ca/ tieleman/downloads (accessed on 1 June 2013).
32. Holtje, M.; Forster, T.; Brandt, B.; Engels, T.; von Rybinski, W.; Holtje, H.D. Molecular dynamics simulations of stratum corneum lipid models: fatty acids and cholesterol. Biochim. Biophys. Acta 2001, 1511, 156-167.
33. GROMACS Molecule topologies. Available online: http://www.gromacs.org/index.php?title= Download_%26_Installation/User_contributions/Molecule_topologies (accessed on 1 June 2013).
34. Bekker, H.; Berendsen, H.J.C.; Dijkstra, E.J.; Achterop, S.; Vondrumen, R.; Vanderspoel, D.; Sijbers, A.; Keegstra, H.; Reitsma, B.; Renardus, M.K.R. GROMACS: A parallel computer for molecular dynamics simulations. In Physics Computing 92; Groot, R.A.D., Nadrchal, J., Eds.; World Scientific: Singapore, 1993.
35. Van der Spoel, D.; Lindahl, E.; Hess, B.; Groenhof, G.; Mark, A.E.; Berendsen, H.J. GROMACS: Fast, flexible, and free. J. Comput. Chem. 2005, 26, 1701-1718.
36. Berendsen, H.J.C.; Postma, J.P.M.; Vangunsteren, W.F.; Dinola, A.; Haak, J.R. Molecular-Dynamics with Coupling to an External Bath. J. Chem. Phys. 1984, 81, 3684-3690.
37. Miyamoto, S.; Kollman, P.A. Settle-An Analytical Version of the Shake and Rattle for Rigid Water Models. J. Comput. Chem. 1992, 13, 952-962.
38. Hess, B.; Bekker, H.; Berendsen, H.J.C.; Fraaije, J.G.E.M. LINCS: A linear constraint solver for molecular simulations. J. Comput. Chem. 1997, 18, 1463-1472.
39. Essmann, U.; Perera, L.; Berkowitz, M.L.; Darden, T.; Lee, H.; Pedersen, L.G.A. Smooth particle mesh ewald method. J. Chem. Phys. 1995, 103, 8577-8593.
40. Flyvbjerg, H.; Petersen, H.G. Error estimates on averages of correlated data. J. Chem. Phys. 1989, 91, 461-466.
41. Franquelim, H.G.; Gaspar, D.; Veiga, A.S.; Santos, N.C.; Castanho, M.A. Decoding distinct membrane interactions of HIV-1 fusion inhibitors using a combined atomic force and fluorescence microscopy approach. Biochim. Biophys. Acta 2013, 1828, 1777-1785.
42. Pan, C.; Lu, H.; Qi, Z.; Jiang, S. Synergistic efficacy of combination of enfuvirtide and sifuvirtide, the first-and next-generation HIV-fusion inhibitors. AIDS 2009, 23, 639-641.
43. Pan, C.; Cai, L.; Lu, H.; Qi, Z.; Jiang, S. Combinations of the first and next generations of human immunodeficiency virus (HIV) fusion inhibitors exhibit a highly potent synergistic effect against enfuvirtide-sensitive and-resistant HIV type 1 strains. J. Virol. 2009, 83, 7862-7872.
44. Liu, S.; Lu, H.; Zhao, Q.; He, Y.; Niu, J.; Debnath, A.K.; Wu, S.; Jiang, S. Theaflavin derivatives in black tea and catechin derivatives in green tea inhibit HIV-1 entry by targeting gp41. Biochim. Biophys. Acta 2005, 1723, 270-281.
45. Sirk, T.W.; Friedman, M.; Brown, E.F. Molecular binding of black tea theaflavins to biological membranes: relationship to bioactivities. J. Agric. Food Chem. 2011, 59, 3780-3787.