Irregular structure of the HIV fusion peptide in membranes demonstrated by solid-state NMR and MD simulations

European Biophysics Journal

Volumn 40, Issue 4, 2011, Pages 529-543

  Grasnick, Dorit ^a   Sternberg, Ulrich ^a   Strandberg, Erik ^a   Wadhwani, Parvesh ^a   Ulrich, Anne S ^a  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

Stranded secondary structure; All atom MD simulations; Fusogenic peptides; HIV 1 protein gp41; Membrane fusion; Solid state 19F and 2H NMR

Indexed keywords

DIMYRISTOYLPHOSPHATIDYLCHOLINE; GLYCOPROTEIN GP 41; MEMBRANE FUSION PROTEIN;

ARTICLE; CHEMISTRY; GROWTH, DEVELOPMENT AND AGING; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; ISOTOPE LABELING; LIPID BILAYER; METABOLISM; METHODOLOGY; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PATHOLOGY; PROTEIN SECONDARY STRUCTURE;

DIMYRISTOYLPHOSPHATIDYLCHOLINE; HIV ENVELOPE PROTEIN GP41; HIV INFECTIONS; HIV-1; HUMANS; ISOTOPE LABELING; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE FUSION PROTEINS; MOLECULAR DYNAMICS SIMULATION; PROTEIN STRUCTURE, SECONDARY;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 79956041013     PISSN: 01757571     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00249-011-0676-5     Document Type: Article

References (77)

1. 19F-NMR structure analysis of membrane-associated peptides Chembiochem 4 1151 1163 14613106 10.1002/cbic.200300568 1:CAS:528:DC%2BD3sXptFajtrw%3D (Pubitemid 37462816)
2. 19F NMR Magn Reson Chem 42 195 203 14745800 10.1002/mrc.1340 1:CAS:528:DC%2BD2cXhtFKhtrs%3D (Pubitemid 38178089)
3. S Afonin UHN Dürr P Wadhwani JB Salgado AS Ulrich 2008 Solid state NMR structure analysis of the antimicrobial peptide gramicidin S in lipid membranes: concentration-dependent re-alignment and self-assembly as a β-barrel Topics Curr Chem 273 139 154 10.1007/128-2007-20 1:CAS:528:DC%2BD1cXhtlamtrrN
4. 19F-NMR spectroscopy J Am Chem Soc 130 16512 16514 19049452 10.1021/ja803156d 1:CAS:528:DC%2BD1cXhsVWgt7bP
5. FH Allen O Kennard DG Watson L Brammer AG Orpen R Taylor 1987 Tables of bond lengths determined by X-ray and neutron diffraction.1. Bond lengths in organic compounds J Chem Soc Perkin Trans 2 S1 S19
6. B Barz TC Wong I Kosztin 2008 Membrane curvature and surface area per lipid affect the conformation and oligomeric state of HIV-1 fusion peptide: a combined FTIR and MD simulation study Biochim Biophys Acta 1778 945 953 18177732 10.1016/j.bbamem.2007.11.014 1:CAS:528:DC%2BD1cXktVGrtrg%3D
7. ML Bodner CM Gabrys JO Struppe DP Weliky 2008 13C-13C and 15 N-13C correlation spectroscopy of membrane-associated and uniformly labeled human immunodeficiency virus and influenza fusion peptides: amino acid-type assignments and evidence for multiple conformations J Chem Phys 128 052319 18266436 10.1063/1.2829984 (Pubitemid 351598432)
8. GL Buchschacher Jr EO Freed AT Panganiban 1995 Effects of second-site mutations on dominant interference by a human immunodeficiency virus type 1 envelope glycoprotein mutant J Virol 69 1344 1348 7815519 1:CAS:528: DyaK2MXjtlGqu70%3D
9. S Castano B Desbat 2005 Structure and orientation study of fusion peptide FP23 of gp41 from HIV-1 alone or inserted into various lipid membrane models (mono-, bi- and multibi-layers) by FT-IR spectroscopies and Brewster angle microscopy Biochim Biophys Acta 1715 81 95 16126160 10.1016/j.bbamem.2005.07.008 1:CAS:528:DC%2BD2MXpslart7k%3D (Pubitemid 41219696)
10. DK Chang SF Cheng WJ Chien 1997 The amino-terminal fusion domain peptide of human immunodeficiency virus type 1 gp41 inserts into the sodium dodecyl sulfate micelle primarily as a helix with a conserved glycine at the micelle-water interface J Virol 71 6593 6602 9261381 1:CAS:528: DyaK2sXlsVKqu7s%3D
11. DK Chang WJ Chien SF Cheng 1997 The FLG motif in the N-terminal region of glucoprotein 41 of human immunodeficiency virus type 1 adopts a type-I beta turn in aqueous solution and serves as the initiation site for helix formation Eur J Biochem 247 896 905 9288913 10.1111/j.1432-1033.1997.00896.x 1:CAS:528:DyaK2sXlsVCmtbg%3D
12. DK Chang SF Cheng VD Trivedi 1999 Biophysical characterization of the structure of the amino-terminal region of gp41 of HIV-1. Implications on viral fusion mechanism J Biol Chem 274 5299 5309 10026137 10.1074/jbc.274.9.5299 1:CAS:528:DyaK1MXhsFamurs%3D (Pubitemid 29109171)
13. MD Delahunty I Rhee EO Freed JS Bonifacino 1996 Mutational analysis of the fusion peptide of the human immunodeficiency virus type 1: identification of critical glycine residues Virology 218 94 102 8615045 10.1006/viro.1996.0169 1:CAS:528:DyaK28XitVCmtLY%3D (Pubitemid 26133090)
14. SR Durell I Martin JM Ruysschaert Y Shai R Blumenthal 1997 What studies of fusion peptides tell us about viral envelope glycoprotein-mediated membrane fusion Mol Membr Biol 14 97 112 9394290 10.3109/09687689709048170 1:CAS:528:DyaK2sXnt1Cgu7o%3D (Pubitemid 27478674)
15. 19F-NMR studies on fluorine-labeled model compounds and biomolecules Biochemistry. Ph D thesis, University of Karlsruhe, Karlsruhe
16. 15N PISEMA NMR spectra of membrane peptides: a theoretical analysis Biophys J 96 3233 3241 19383467 10.1016/j.bpj.2008.12.3950
17. S Esteban-Martín E Strandberg J Salgado AS Ulrich 2010 Solid state NMR analysis of peptides in membranes: influence of dynamics and labeling scheme Biochim Biophys Acta 1798 252 257 19715662 10.1016/j.bbamem.2009.08.010
18. Evans J, Morris GP (1990) Statistical mechanics of nonequilibrium liquids. Academic Press, London
19. CM Gabrys DP Weliky 2007 Chemical shift assignment and structural plasticity of a HIV fusion peptide derivative in dodecylphosphocholine micelles Biochim Biophys Acta 1768 3225 3234 17935693 10.1016/j.bbamem.2007.07.028 1:CAS:528:DC%2BD2sXhsVCktr7P (Pubitemid 350236081)
20. D Gerber M Pritsker S Gunther-Ausborn B Johnson R Blumenthal Y Shai 2004 Inhibition of HIV-1 envelope glycoprotein-mediated cell fusion by a DL-amino acid-containing fusion peptide: possible recognition of the fusion complex J Biol Chem 279 48224 48230 15339935 10.1074/jbc.M403436200 1:CAS:528: DC%2BD2cXptl2ntL8%3D (Pubitemid 39540978)
21. RW Glaser M Grüne C Wandelt AS Ulrich 1999 NMR and CD structural analysis of the fusogenic peptide sequence B18 from the fertilization protein bindin Biochemistry 38 2560 2569 10029551 10.1021/bi982130e 1:CAS:528: DyaK1MXntVyktQ%3D%3D (Pubitemid 29102818)
22. 3-phenylglycine labels J Magn Reson 168 153 163 15082261 10.1016/j.jmr.2004.02.008 1:CAS:528: DC%2BD2cXjtVWit7s%3D
23. 19F-NMR Biophys J 88 3392 3397 15695635 10.1529/biophysj.104.056424 1:CAS:528:DC%2BD2MXktFShurY%3D (Pubitemid 40586589)
24. 13C-enhanced Fourier transform infrared spectroscopy Biochim Biophys Acta 1559 96 120 11853678 10.1016/S0005-2736(01)00443-6 1:CAS:528: DC%2BD38XisVWrsrg%3D (Pubitemid 34164420)
25. 13C-enhanced Fourier transform infrared spectroscopy Protein Sci 13 1012 1030 15044732 10.1110/ps.03407704 1:CAS:528:DC%2BD2cXivFaktb8%3D (Pubitemid 38429224)
26. LM Gordon A Nisthal AB Lee S Eskandari P Ruchala CL Jung AJ Waring PW Mobley 2008 Structural and functional properties of peptides based on the N-terminus of HIV-1 gp41 and the C-terminus of the amyloid-beta protein Biochim Biophys Acta 1778 2127 2137 18515070 10.1016/j.bbamem.2008.05.002 1:CAS:528:DC%2BD1cXhtFCktbzM
27. SL Grage S Afonin AS Ulrich 2010 Dynamic transitions of membrane active peptides Meth Mol Biol 618 183 207 10.1007/978-1-60761-594-1-13 1:CAS:528:DC%2BC3cXhtVSlu7rF
28. ME Haque V Koppaka PH Axelsen BR Lentz 2005 Properties and structures of the influenza and HIV fusion peptides on lipid membranes: implications for a role in fusion Biophys J 89 3183 3194 16183890 10.1529/biophysj.105.063032 1:CAS:528:DC%2BD2MXht1Wnt73K (Pubitemid 41636073)
29. CP Jaroniec JD Kaufman SJ Stahl M Viard R Blumenthal PT Wingfield A Bax 2005 Structure and dynamics of micelle-associated human immunodeficiency virus gp41 fusion domain Biochemistry 44 16167 16180 16331977 10.1021/bi051672a 1:CAS:528:DC%2BD2MXht1WisbzN (Pubitemid 41785815)
30. M Kanyalkar S Srivastava A Saran E Coutinho 2004 Conformational study of fragments of envelope proteins (gp120: 254-274 and gp41: 519-541) of HIV-1 by NMR and MD simulations J Pept Sci 10 363 380 15214441 10.1002/psc.530 1:CAS:528:DC%2BD2cXltFCisr4%3D (Pubitemid 38801619)
31. Y Kliger A Aharoni D Rapaport P Jones R Blumenthal Y Shai 1997 Fusion peptides derived from the HIV type 1 glycoprotein 41 associate within phospholipid membranes and inhibit cell-cell fusion. Structure-function study J Biol Chem 272 13496 13505 9153194 10.1074/jbc.272.21.13496 1:CAS:528: DyaK2sXjsFWhsro%3D (Pubitemid 27224777)
32. Y Li LK Tamm 2007 Structure and plasticity of the human immunodeficiency virus gp41 fusion domain in lipid micelles and bilayers Biophys J 93 876 885 17513369 10.1529/biophysj.106.102335 1:CAS:528:DC%2BD2sXotV2itb4%3D (Pubitemid 47219779)
33. MW Maddox ML Longo 2002 Conformational partitioning of the fusion peptide of HIV-1 gp41 and its structural analogs in bilayer membranes Biophys J 83 3088 3096 12496080 10.1016/S0006-3495(02)75313-7 1:CAS:528:DC%2BD3sXislSgsA%3D%3D (Pubitemid 36041931)
34. 19F-NMR analysis of peptaibols in membranes J Am Chem Soc 131 15596 15597 19827760 10.1021/ja9067595 1:CAS:528:DC%2BD1MXht1KjtL3N
35. MP Marsan I Muller C Ramos F Rodriguez EJ Dufourc J Czaplicki A Milon 1999 Cholesterol orientation and dynamics in dimyristoylphosphatidylcholine bilayers: a solid state deuterium NMR analysis Biophys J 76 351 359 9876147 10.1016/S0006-3495(99)77202-4 1:CAS:528:DyaK1MXjs1SltA%3D%3D (Pubitemid 29202462)
36. PW Mobley AJ Waring MA Sherman LM Gordon 1999 Membrane interactions of the synthetic N-terminal peptide of HIV-1 gp41 and its structural analogs Biochim Biophys Acta 1418 1 18 10209206 10.1016/S0005-2736(99)00014-0 1:CAS:528:DyaK1MXjtVWhuro%3D (Pubitemid 29182742)
37. 19F NMR spectroscopy Angew Chem Int Ed Engl 45 5659 5661 10.1002/anie.200600346 (Pubitemid 44366771)
38. 19F NMR labels for peptides in the polyproline II conformation Angew Chem Int Ed Engl 47 5765 5767 18576439 10.1002/anie.200801022 1:CAS:528:DC%2BD1cXpsFKrsrw%3D
39. SG Peisajovich RF Epand M Pritsker Y Shai RM Epand 2000 The polar region consecutive to the HIV fusion peptide participates in membrane fusion Biochemistry 39 1826 1833 10677233 10.1021/bi991887i 1:CAS:528: DC%2BD3cXmvV2jsQ%3D%3D (Pubitemid 30108975)
40. FB Pereira FM Goni A Muga JL Nieva 1997 Permeabilization and fusion of uncharged lipid vesicles induced by the HIV-1 fusion peptide adopting an extended conformation: dose and sequence effects Biophys J 73 1977 1986 9336193 10.1016/S0006-3495(97)78228-6 1:CAS:528:DyaK2sXmsFCntL4%3D (Pubitemid 27425728)
41. J Peuvot A Schanck L Lins R Brasseur 1999 Are the fusion processes involved in birth, life and death of the cell depending on tilted insertion of peptides into membranes? J Theor Biol 198 173 181 10339392 10.1006/jtbi.1999. 0908 1:CAS:528:DyaK1MXjt1Knsro%3D (Pubitemid 29259736)
42. M Pritsker P Jones R Blumenthal Y Shai 1998 A synthetic all D-amino acid peptide corresponding to the N-terminal sequence of HIV-1 gp41 recognizes the wild-type fusion peptide in the membrane and inhibits HIV-1 envelope glycoprotein-mediated cell fusion Proc Natl Acad Sci U S A 95 7287 7292 9636141 10.1073/pnas.95.13.7287 1:CAS:528:DyaK1cXktFChtrw%3D (Pubitemid 28293244)
43. M Pritsker J Rucker TL Hoffman RW Doms Y Shai 1999 Effect of nonpolar substitutions of the conserved Phe11 in the fusion peptide of HIV-1 gp41 on its function, structure, and organization in membranes Biochemistry 38 11359 11371 10471286 10.1021/bi990232e 1:CAS:528:DyaK1MXkvFOgt74%3D (Pubitemid 29420956)
44. W Qiang DP Weliky 2009 HIV fusion peptide and its cross-linked oligomers: efficient syntheses, significance of the trimer in fusion activity, correlation of beta strand conformation with membrane cholesterol, and proximity to lipid headgroups Biochemistry 48 289 301 19093835 10.1021/bi8015668 1:CAS:528:DC%2BD1cXhsFais77J
45. W Qiang J Yang DP Weliky 2007 Solid-state nuclear magnetic resonance measurements of HIV fusion peptide to lipid distances reveal the intimate contact of beta strand peptide with membranes and the proximity of the Ala-14-Gly-16 region with lipid headgroups Biochemistry 46 4997 5008 17417873 10.1021/bi6024808 1:CAS:528:DC%2BD2sXjvVOlsr4%3D (Pubitemid 46682998)
46. W Qiang ML Bodner DP Weliky 2008 Solid-state NMR spectroscopy of human immunodeficiency virus fusion peptides associated with host-cell-like membranes: 2D correlation spectra and distance measurements support a fully extended conformation and models for specific antiparallel strand registries J Am Chem Soc 130 5459 5471 18370385 10.1021/ja077302m 1:CAS:528:DC%2BD1cXjvFejtLc%3D (Pubitemid 351612954)
47. W Qiang Y Sun DP Weliky 2009 A strong correlation between fusogenicity and membrane insertion depth of the HIV fusion peptide Proc Natl Acad Sci U S A 106 15314 15319 19706388 10.1073/pnas.0907360106 1:CAS:528:DC%2BD1MXhtFGgtr%2FP
48. M Rafalski JD Lear WF DeGrado 1990 Phospholipid interactions of synthetic peptides representing the N-terminus of HIV gp41 Biochemistry 29 7917 7922 2261447 10.1021/bi00486a020 1:CAS:528:DyaK3cXltFelsr4%3D (Pubitemid 20281241)
49. J Reichert D Grasnick S Afonin J Buerck P Wadhwani AS Ulrich 2007 A critical evaluation of the conformational requirements of fusogenic peptides in membranes Eur Biophys J 36 405 413 17089152 10.1007/s00249-006-0106-2 1:CAS:528:DC%2BD2sXktlWjt70%3D (Pubitemid 46626198)
50. K Sackett Y Shai 2002 The HIV-1 gp41 N-terminal heptad repeat plays an essential role in membrane fusion Biochemistry 41 4678 4685 11926830 10.1021/bi0255322 1:CAS:528:DC%2BD38XhslGhtrg%3D (Pubitemid 34275669)
51. K Sackett Y Shai 2003 How structure correlates to function for membrane associated HIV-1 gp41 constructs corresponding to the N-terminal half of the ectodomain J Mol Biol 333 47 58 14516742 10.1016/j.jmb.2003.07.008 1:CAS:528:DC%2BD3sXnsVWrt7c%3D (Pubitemid 37153264)
52. K Sackett M Nethercott Y Shai D Weliky 2009 Hairpin folding of HIV gp41 abrogates lipid mixing function at physiologic pH and inhibits lipid mixing by exposed gp41 constructs Biochemistry 48 2714 2722 19222185 10.1021/bi8019492 1:CAS:528:DC%2BD1MXjtVSjs7w%3D
53. K Sackett MJ Nethercott RF Epand RM Epand DR Kindra Y Shai DP Weliky 2010 Comparative analysis of membrane-associated fusion peptide secondary structure and lipid mixing function of HIV gp41 constructs that model the early pre-hairpin intermediate and final hairpin conformations J Mol Biol 397 301 315 20080102 10.1016/j.jmb.2010.01.018 1:CAS:528:DC%2BC3cXis1aiu70%3D
54. 19F-NMR J Biomol NMR 21 191 208 11775737 10.1023/A:1012946026231 1:CAS:528:DC%2BD3MXptlKrs7w%3D (Pubitemid 33133421)
55. Sternberg U, Koch F-T, Losso P (2006) COSMOS program. COSMOS Software, Jena
56. U Sternberg R Witter AS Ulrich 2007 All-atom molecular dynamics simulations using orientational constraints from anisotropic NMR samples J Biomol NMR 38 23 39 17334824 10.1007/s10858-007-9142-1 1:CAS:528: DC%2BD2sXmtl2jurk%3D (Pubitemid 46745439)
57. E Strandberg AS Ulrich 2004 NMR methods for studying membrane-active antimicrobial peptides Concepts Magn Reson A 23A 89 120 10.1002/cmr.a.20024 1:CAS:528:DC%2BD2MXht1Oj (Pubitemid 40646213)
58. 2H solid state NMR. Biophys J 86:3709-3721 (Pubitemid 38780249)
59. 19F-NMR Biophys J 90 1676 1686 16339890 10.1529/biophysj.105.073858 1:CAS:528:DC%2BD28XitVahtbg%3D
60. E Strandberg N Kanithasen D Tiltak J Bürck P Wadhwani O Zwernemann AS Ulrich 2008 Solid-state NMR analysis comparing the designer-made antibiotic MSI-103 with its parent peptide PGLa in lipid bilayers Biochemistry 47 2601 2616 18220419 10.1021/bi701944r 1:CAS:528:DC%2BD1cXhtVyitbY%3D (Pubitemid 351304566)
61. 2H-NMR data Biophys J 96 3223 3232 19383466 10.1016/j.bpj.2009.02.040 1:CAS:528: DC%2BD1MXnvVeltL0%3D
62. 2H-NMR Biochim Biophys Acta 1758 1330 1342 16716250 10.1016/j.bbamem.2006.02.029 1:CAS:528:DC%2BD28XhtVanu7jE (Pubitemid 44436073)
63. P Tremouilhac E Strandberg P Wadhwani AS Ulrich 2006 Synergistic transmembrane alignment of the antimicrobial heterodimer PGLa/magainin J Biol Chem 281 32089 32094 16877761 10.1074/jbc.M604759200 1:CAS:528: DC%2BD28XhtFSrsbjK (Pubitemid 46036763)
64. 19F-NMR methods for studying biomembranes Progr Nucl Magn Reson Spectrosc 46 1 21 10.1016/j.pnmrs.2004.11.001 1:CAS:528:DC%2BD2MXisFahtrk%3D (Pubitemid 40357060)
65. 19F-NMR analysis of oriented biomembranes. In: Webb GA (ed) Modern magnetic resonance, vol 1. Springer, Dordrecht, pp 261-267
66. AS Ulrich W Tichelaar G Förster O Zschörnig S Weinkauf HW Meyer 1999 Ultrastructural characterization of peptide-induced membrane fusion and peptide self-assembly in the bilayer Biophys J 77 829 841 10423429 10.1016/S0006-3495(99)76935-3 1:CAS:528:DyaK1MXltVyjurs%3D (Pubitemid 29362455)
67. 19F-nuclear magnetic resonance analysis of membrane-active peptides. In: Ramamoorthy A (ed) NMR spectroscopy of biological solids. CRC Press, Boca Raton, pp 215-236
68. 19F-NMR label to monitor and control peptide aggregation in membranes J Am Chem Soc 130 16515 16517 19554688 10.1021/ja804928q 1:CAS:528:DC%2BD1cXhtlOrs77F
69. Wadhwani P, Reichert J, Bürck J, Ulrich AS (2010) Antimicrobial and cell penetrating peptides can trigger membrane fusion by folding and aggregation (submitted)
70. CM Wasniewski PD Parkanzky ML Bodner DP Weliky 2004 Solid-state nuclear magnetic resonance studies of HIV and influenza fusion peptide orientations in membrane bilayers using stacked glass plate samples Chem Phys Lipids 132 89 100 15530451 10.1016/j.chemphyslip.2004.09.008 1:CAS:528:DC%2BD2cXpsFSktbc%3D (Pubitemid 39458323)
71. JM White SE Delos M Brecher K Schornberg 2008 Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme Crit Rev Biochem Mol Biol 43 189 219 18568847 10.1080/10409230802058320 1:CAS:528:DC%2BD1cXnsFaqurk%3D (Pubitemid 351883153)
72. TC Wong 2003 Membrane structure of the human immunodeficiency virus gp41 fusion peptide by molecular dynamics simulation. II. The glycine mutants Biochim Biophys Acta 1609 45 54 12507757 10.1016/S0005-2736(02)00652-1 1:CAS:528:DC%2BD38XpvVaisL4%3D (Pubitemid 36044064)
73. J Yang DP Weliky 2003 Solid-state nuclear magnetic resonance evidence for parallel and antiparallel strand arrangements in the membrane-associated HIV-1 fusion peptide Biochemistry 42 11879 11890 14529300 10.1021/bi0348157 1:CAS:528:DC%2BD3sXnsVOisrs%3D (Pubitemid 37243649)
74. J Yang CM Gabrys DP Weliky 2001 Solid-state nuclear magnetic resonance evidence for an extended β strand conformation of the membrane-bound HIV-1 fusion peptide Biochemistry 40 8126 8137 11434782 10.1021/bi0100283 1:CAS:528:DC%2BD3MXkt1Wktr0%3D (Pubitemid 32641210)
75. R Yang J Yang DP Weliky 2003 Synthesis, enhanced fusogenicity, and solid state NMR measurements of cross-linked HIV-1 fusion peptides Biochemistry 42 3527 3535 12653557 10.1021/bi027052g 1:CAS:528:DC%2BD3sXhvVygsLc%3D (Pubitemid 36368647)
76. R Yang M Prorok FJ Castellino DP Weliky 2004 A trimeric HIV-1 fusion peptide construct which does not self-associate in aqueous solution and which has 15-fold higher membrane fusion rate J Am Chem Soc 126 14722 14723 15535688 10.1021/ja045612o 1:CAS:528:DC%2BD2cXovFSlsr4%3D (Pubitemid 39532144)
77. Z Zheng R Yang ML Bodner DP Weliky 2006 Conformational flexibility and strand arrangements of the membrane-associated HIV fusion peptide trimer probed by solid-state NMR spectroscopy Biochemistry 45 12960 12975 17059213 10.1021/bi0615902 1:CAS:528:DC%2BD28XhtVGmsb7I (Pubitemid 44763419)