Solid-state nuclear magnetic resonance measurements of HIV fusion peptide 13CO to lipid 31P proximities support similar partially inserted membrane locations of the α helical and β sheet peptide structures

Journal of Physical Chemistry A

Volumn 117, Issue 39, 2013, Pages 9848-9859

  Gabrys, Charles M ^a   Qiang, Wei ^a   Sun, Yan ^a   Xie, Li ^a   Schmick, Scott D ^a   Weliky, David P ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYZED MEMBRANES; HUMAN IMMUNODEFICIENCY VIRUS; INTEGRAL MEMBRANE PROTEINS; MOLECULAR POPULATION; ROTATIONAL ECHO DOUBLE RESONANCE; SOLID-STATE NUCLEAR MAGNETIC RESONANCE; STRUCTURAL MODELING; SUPPORTED MEMBRANE;

ACTIVATION ENERGY; CATALYSIS; CELL MEMBRANES; CYTOLOGY; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDES; VIRUSES;

MEMBRANES;

CARBON; CARBON MONOXIDE; GLYCOPROTEIN GP 41; LIPID; PHOSPHORUS;

AMINO ACID SEQUENCE; ARTICLE; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS; MEMBRANE FUSION; MOLECULAR GENETICS; MUTATION; NUCLEAR MAGNETIC RESONANCE; PROTEIN SECONDARY STRUCTURE; VIRUS ENTRY;

AMINO ACID SEQUENCE; CARBON ISOTOPES; CARBON MONOXIDE; CELL MEMBRANE; HIV; HIV ENVELOPE PROTEIN GP41; LIPIDS; MEMBRANE FUSION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHORUS ISOTOPES; PROTEIN STRUCTURE, SECONDARY; VIRUS INTERNALIZATION;

EID: 84885202727     PISSN: 10895639     EISSN: 15205215     Source Type: Journal    
DOI: 10.1021/jp312845w     Document Type: Article

References (44)

1. White, J. M.; Delos, S. E.; Brecher, M.; Schornberg, K. Structures and Mechanisms of Viral Membrane Fusion Proteins: Multiple Variations on a Common Theme Crit. Rev. Biochem. Mol. Biol. 2008, 43, 189-219
2. Vogel, E. P.; Curtis-Fisk, J.; Young, K. M.; Weliky, D. P. Solid-State Nuclear Magnetic Resonance (NMR) Spectroscopy of Human Immunodeficiency Virus gp41 Protein That Includes the Fusion Peptide: NMR Detection of Recombinant Fgp41 in Inclusion Bodies in Whole Bacterial Cells and Structural Characterization of Purified and Membrane-Associated Fgp41 Biochemistry 2011, 50, 10013-10026
3. Durell, S. R.; Martin, I.; Ruysschaert, J. M.; Shai, Y.; Blumenthal, R. What Studies of Fusion Peptides Tell Us About Viral Envelope Glycoprotein-Mediated Membrane Fusion Mol. Membr. Biol. 1997, 14, 97-112
4. Nieva, J. L.; Agirre, A. Are Fusion Peptides a Good Model to Study Viral Cell Fusion? Biochim. Biophys. Acta 2003, 1614, 104-115
5. Yang, J.; Prorok, M.; Castellino, F. J.; Weliky, D. P. Oligomeric β-Structure of the Membrane-Bound HIV-1 Fusion Peptide Formed from Soluble Monomers Biophys. J. 2004, 87, 1951-1963
6. Yang, R.; Prorok, M.; Castellino, F. J.; Weliky, D. P. 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. 2004, 126, 14722-14723
7. Chang, D. K.; Cheng, S. F.; Chien, W. J. 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. 1997, 71, 6593-6602
8. Chang, D. K.; Cheng, S. F. Determination of the Equilibrium Micelle-Inserting Position of the Fusion Peptide of gp41 of Human Immunodeficiency Virus Type 1 at Amino Acid Resolution by Exchange Broadening of Amide Proton Resonances J. Biomol. NMR 1998, 12, 549-552
9. Morris, K. F.; Gao, X. F.; Wong, T. C. The Interactions of the HIV gp41 Fusion Peptides with Zwitterionic Membrane Mimics Determined by NMR Spectroscopy Biochim. Biophys. Acta 2004, 1667, 67-81
10. Jaroniec, C. P.; Kaufman, J. D.; Stahl, S. J.; Viard, M.; Blumenthal, R.; Wingfield, P. T.; Bax, A. Structure and Dynamics of Micelle-Associated Human Immunodeficiency Virus gp41 Fusion Domain Biochemistry 2005, 44, 16167-16180
11. Gabrys, C. M.; Weliky, D. P. Chemical Shift Assignment and Structural Plasticity of a HIV Fusion Peptide Derivative in Dodecylphosphocholine Micelles Biochim. Biophys. Acta 2007, 1768, 3225-3234
12. Li, Y. L.; Tamm, L. K. Structure and Plasticity of the Human Immunodeficiency Virus gp41 Fusion Domain in Lipid Micelles and Bilayers Biophys. J. 2007, 93, 876-885
13. Qiang, W.; Bodner, M. L.; Weliky, D. P. 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. 2008, 130, 5459-5471
14. Qiang, W.; Weliky, D. P. HIV Fusion Peptide and Its Cross-Linked Oligomers: Efficient Syntheses, Significance of the Trimer in Fusion Activity, Correlation of β Strand Conformation with Membrane Cholesterol, and Proximity to Lipid Headgroups Biochemistry 2009, 48, 289-301
15. Qiang, W.; Sun, Y.; Weliky, D. P. A Strong Correlation between Fusogenicity and Membrane Insertion Depth of the HIV Fusion Peptide Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 15314-15319
16. Qiang, W.; Yang, J.; Weliky, D. P. 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 2007, 46, 4997-5008 PMCID: 2631438.
17. Zheng, Z.; Yang, R.; Bodner, M. L.; Weliky, D. P. Conformational Flexibility and Strand Arrangements of the Membrane-Associated HIV Fusion Peptide Trimer Probed by Solid-State NMR Spectroscopy Biochemistry 2006, 45, 12960-12975
18. Zheng, Z.; Qiang, W.; Weliky, D. P. Investigation of Finite-Pulse Radiofrequency-Driven Recoupling Methods for Measurement of Intercarbonyl Distances in Polycrystalline and Membrane-Associated HIV Fusion Peptide Samples Magn. Reson. Chem. 2007, 245, S247-S260
19. Pereira, F. B.; Goni, F. M.; Nieva, J. L. Liposome Destabilization Induced by the HIV-1 Fusion Peptide Effect of a Single Amino Acid Substitution FEBS Lett. 1995, 362, 243-246
20. Schmick, S. D.; Weliky, D. P. Major Antiparallel and Minor Parallel Beta Sheet Populations Detected in the Membrane-Associated Human Immunodeficiency Virus Fusion Peptide Biochemistry 2010, 49, 10623-10635
21. Lai, A. L.; Moorthy, A. E.; Li, Y. L.; Tamm, L. K. Fusion Activity of HIV gp41 Fusion Domain Is Related to Its Secondary Structure and Depth of Membrane Insertion in a Cholesterol-Dependent Fashion J. Mol. Biol. 2012, 418, 3-15
22. Agirre, A.; Flach, C.; Goni, F. M.; Mendelsohn, R.; Valpuesta, J. M.; Wu, F. J.; Nieva, J. L. Interactions of the HIV-1 Fusion Peptide with Large Unilamellar Vesicles and Monolayers. A Cryo-Tem and Spectroscopic Study Biochim. Biophys. Acta 2000, 1467, 153-164
23. Haque, M. E.; Koppaka, V.; Axelsen, P. H.; Lentz, B. R. Properties and Structures of the Influenza and HIV Fusion Peptides on Lipid Membranes: Implications for a Role in Fusion Biophys. J. 2005, 89, 3183-3194
24. Gullion, T. Introduction to Rotational-Echo, Double-Resonance NMR Concepts Magn. Reson. 1998, 10, 277-289
25. Toke, O.; Maloy, W. L.; Kim, S. J.; Blazyk, J.; Schaefer, J. Secondary Structure and Lipid Contact of a Peptide Antibiotic in Phospholipid Bilayers by REDOR Biophys. J. 2004, 87, 662-674
26. Doherty, T.; Waring, A.; Hong, M. Membrane-Bound Conformation and Topology of the Antimicrobial Peptide Tachyplesin I by Solid-State NMR Biochemistry 2006, 45, 13323-13330
27. Murphy, O. J., 3rd; Kovacs, F. A.; Sicard, E. L.; Thompson, L. K. Site-Directed Solid-State NMR Measurement of a Ligand-Induced Conformational Change in the Serine Bacterial Chemoreceptor Biochemistry 2001, 40, 1358-1366
28. 19F-Dephased Redor Shift (Fresh) Spectroscopy Magn. Reson. Chem. 2007, 45, S129-S134
29. Tristram-Nagle, S.; Nagle, J. F. Lipid Bilayers: Thermodynamics, Structure, Fluctuations, and Interactions Chem. Phys. Lipids 2004, 127, 3-14
30. 2H Rotational-Echo Double-Resonance Solid-State NMR J. Biomol. NMR 2013, 55, 11-17
31. Freed, E. O.; Delwart, E. L.; Buchschacher, G. L., Jr.; Panganiban, A. T. A Mutation in the Human Immunodeficiency Virus Type 1 Transmembrane Glycoprotein gp41 Dominantly Interferes with Fusion and Infectivity Proc. Natl. Acad. Sci. U. S. A. 1992, 89, 70-74
32. Sackett, K.; Nethercott, M. J.; Epand, R. F.; Epand, R. M.; Kindra, D. R.; Shai, Y.; Weliky, D. P. 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. 2010, 397, 301-315
33. Gabrys, C. M.; Yang, R.; Wasniewski, C. M.; Yang, J.; Canlas, C. G.; Qiang, W.; Sun, Y.; Weliky, D. P. Nuclear Magnetic Resonance Evidence for Retention of a Lamellar Membrane Phase with Curvature in the Presence of Large Quantities of the HIV Fusion Peptide Biochim. Biophys. Acta 2010, 1798, 194-201
34. Tristram-Nagle, S.; Chan, R.; Kooijman, E.; Uppamoochikkal, P.; Qiang, W.; Weliky, D. P.; Nagle, J. F. HIV Fusion Peptide Penetrates, Disorders, and Softens T-Cell Membrane Mimics J. Mol. Biol. 2010, 402, 139-153
35. Reichert, J.; Grasnick, D.; Afonin, S.; Buerck, J.; Wadhwani, P.; Ulrich, A. S. A Critical Evaluation of the Conformational Requirements of Fusogenic Peptides in Membranes Eur. Biophys. J. 2007, 36, 405-413
36. Wadhwani, P.; Reichert, J.; Burck, J.; Ulrich, A. S. Antimicrobial and Cell-Penetrating Peptides Induce Lipid Vesicle Fusion by Folding and Aggregation Eur. Biophys. J. 2012, 41, 177-187
37. Kamath, S.; Wong, T. C. Membrane Structure of the Human Immunodeficiency Virus gp41 Fusion Domain by Molecular Dynamics Simulation Biophys. J. 2002, 83, 135-143
38. Maddox, M. W.; Longo, M. L. Conformational Partitioning of the Fusion Peptide of HIV-1 gp41 and Its Structural Analogs in Bilayer Membranes Biophys. J. 2002, 83, 3088-3096
39. Promsri, S.; Ullmann, G. M.; Hannongbua, S. Molecular Dynamics Simulation of HIV-1 Fusion Domain-Membrane Complexes: Insight into the N-Terminal gp41 Fusion Mechanism Biophys. Chem. 2012, 170, 9-16
40. Munoz-Barroso, I.; Durell, S.; Sakaguchi, K.; Appella, E.; Blumenthal, R. Dilation of the Human Immunodeficiency Virus-1 Envelope Glycoprotein Fusion Pore Revealed by the Inhibitory Action of a Synthetic Peptide from gp41 J. Cell Biol. 1998, 140, 315-323
41. Brugger, B.; Glass, B.; Haberkant, P.; Leibrecht, I.; Wieland, F. T.; Krasslich, H. G. The HIV Lipidome: A Raft with an Unusual Composition Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 2641-2646
42. Bloom, M.; Evans, E.; Mouritsen, O. G. Physical Properties of the Fluid Lipid-Bilayer Component of Cell Membranes: A Perspective Q. Rev. Biophys. 1991, 24, 293-397
43. Buzon, V.; Padros, E.; Cladera, J. Interaction of Fusion Peptides from HIV gp41 with Membranes: A Time-Resolved Membrane Binding, Lipid Mixing, and Structural Study Biochemistry 2005, 44, 13354-13364
44. Sackett, K.; Wexler-Cohen, Y.; Shai, Y. Characterization of the HIV N-Terminal Fusion Peptide-Containing Region in Context of Key gp41 Fusion Conformations J. Biol. Chem. 2006, 281, 21755-21762-21762