Single-particle tracking reveals switching of the HIV fusion peptide between two diffusive modes in membranes

Journal of Physical Chemistry B

Volumn 117, Issue 42, 2013, Pages 13308-13321

  Ott, Maria ^a   Shai, Yechiel ^a   Haran, Gilad ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

DIFFUSION; HIDDEN MARKOV MODELS; LIPID BILAYERS; LIQUID CRYSTALS; MOLECULES; T-CELLS;

DIFFUSIVE MODES; INTERCONVERSIONS; LIQUID CRYSTALLINE; SINGLE PARTICLE TRACKING; SOLUTION VISCOSITY; STOKES-EINSTEIN RELATION; SUPPORTED LIPID BILAYERS; VIRAL INFECTIONS;

PEPTIDES;

GP120 PROTEIN, SIMIAN IMMUNODEFICIENCY VIRUS; MEMBRANE PROTEIN; PEPTIDE; VIRUS ENVELOPE PROTEIN;

ARTICLE; CHEMISTRY; DIFFUSION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; KINETICS; LIPID BILAYER; METABOLISM; PHASE TRANSITION; PROBABILITY; PROTEIN SECONDARY STRUCTURE; TEMPERATURE; VISCOSITY;

DIFFUSION; HIV; HUMANS; KINETICS; LIPID BILAYERS; MARKOV CHAINS; MEMBRANE GLYCOPROTEINS; PEPTIDES; PHASE TRANSITION; PROTEIN STRUCTURE, SECONDARY; TEMPERATURE; VIRAL ENVELOPE PROTEINS; VISCOSITY;

EID: 84886650183     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp4039418     Document Type: Article

References (87)

1. Alkhatib, G.; Combadiere, C.; Broder, C. C.; Feng, Y.; Kennedy, P. E.; Murphy, P. M.; Berger, E. A. CC CKR5: a RANTES, MIP-1alpha, MIP-1beta Receptor as a Fusion Cofactor for Macrophage-Tropic HIV-1 Science 1996, 272, 1955-1958
2. Kowalski, M.; Potz, J.; Basiripour, L.; Dorfman, T.; Goh, W. C.; Terwilliger, E.; Dayton, A.; Rosen, C.; Haseltine, W.; Sodroski, J. Functional Regions of the Envelope Glycoprotein of Human Immunodeficiency Virus Type 1 Science 1987, 237, 1351-1355
3. Wyatt, R.; Kwong, P. D.; Desjardins, E.; Sweet, R. W.; Robinson, J.; Hendrickson, W. A.; Sodroski, J. G. The Antigenic Structure of the HIV gp120 Envelope Glycoprotein Nature 1998, 393, 705-711
4. Suarez, T.; Gallaher, W. R.; Agirre, A.; Goni, F. M.; Nieva, J. L. Membrane Interface-Interacting Sequences within the Ectodomain of the Human Immunodeficiency Virus Type 1 Envelope Glycoprotein: Putative Role during Viral Fusion J. Virol. 2000, 74, 8038-8047
5. Peisajovich, S. G.; Blank, L.; Epand, R. F.; Epand, R. M.; Shai, Y. On the Interaction between gp41 and Membranes: The Immunodominant Loop Stabilizes gp41 Helical Hairpin Conformation J. Mol. Biol. 2003, 326, 1489-1501
6. Chan, D. C.; Kim, P. S. HIV Entry and Its Inhibition Cell 1998, 93, 681-684
7. Weissenhorn, W.; Dessen, A.; Calder, L. J.; Harrison, S. C.; Skehel, J. J.; C., W. D. Structural Basis for Membrane Fusion by Enveloped Viruses Mol. Membr. Biol. 1999, 16, 3-9
8. Gordon, L. M.; Mobley, P. W.; Lee, W.; Eskandari, S.; Kaznessis, Y. N.; Sherman, M. A.; Waring, A. J. Conformational Mapping of the N-Terminal Peptide of HIV-1 gp41 in Lipid Detergent and Aqueous Environments Using 13C-Enhanced Fourier Transform Infrared Spectroscopy Protein Sci. 2004, 13, 1012-1030
9. Gordon, L. M.; Mobley, P. W.; Pilpa, R.; Sherman, M. A.; Waring, A. J. Conformational Mapping of the N-Terminal Peptide of HIV-1 gp41 in Membrane Environments Using 13C-Enhanced Fourier Transform Infrared Spectroscopy Biochim. Biophys. Acta, Biomembr. 2002, 1559, 96-120
10. Curtain, C.; Separovic, F.; Nielsen, K.; Craik, D.; Zhong, Y.; Kirkpatrick, A. The Interactions of the N-Terminal Fusogenic Peptide of HIV-1 gp41 with Neutral Phospholipids Eur. Biophys. J. 1999, 28, 427-436
11. 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
12. Li, Y.; 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. Martin, I.; Defrise-Quertain, F.; Decroly, E.; Vandenbranden, M.; Brasseur, R.; Ruysschaert, J.-M. Orientation and Structure of the NH2-Terminal HIV-1 gp41 Peptide in Fused and Aggregated Liposomes Biochim. Biophys. Acta, Biomembr. 1993, 1145, 124-133
14. 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
15. Sackett, K.; Shai, Y. The HIV Fusion Peptide Adopts Intermolecular Parallel β-Sheet Structure in Membranes When Stabilized by the Adjacent N-Terminal Heptad Repeat: A 13C FTIR Study J. Mol. Biol. 2005, 350, 790-805
16. Cohen, T.; Pevsner-Fischer, M.; Cohen, N.; Cohen, I. R.; Shai, Y. Characterization of the Interacting Domain of the HIV-1 Fusion Peptide with the Transmembrane Domain of the T-Cell Receptor Biochemistry 2008, 47, 4826-4833
17. Mobley, P. W.; Waring, A. J.; Sherman, M. A.; Gordon, L. M. Membrane Interactions of the Synthetic N-Terminal Peptide of HIV-1 gp41 and Its Structural Analogs Biochim. Biophys. Acta, Biomembr. 1999, 1418, 1-18
18. Nieva, J. L.; Nir, S.; Muga, A.; Goni, F. M.; Wilschut, J. Interaction of the HIV-1 Fusion Peptide with Phospholipid Vesicles: Different Structural Requirements for Fusion and Leakage Biochemistry 1994, 33, 3201-3209
19. Rafalski, M.; Lear, J. D.; DeGrado, W. F. Phospholipid Interactions of Synthetic Peptides Representing the N-Terminus of HIV gp41 Biochemistry 1990, 29, 7917-7922
20. MacDonald, R. I. Characteristics of Self-Quenching of the Fluorescence of Lipid-Conjugated Rhodamine in Membranes J. Biol. Chem. 1990, 265, 13533-13539
21. 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
22. Gabrys, C. M.; Qiang, W.; Sun, Y.; Xie, L.; Schmick, S. D.; Weliky, D. P. 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. J. Phys. Chem. A 2013, DOI: 10.1021/jp312845w.
23. Tanaka, M.; Sackmann, E. Polymer-Supported Membranes as Models of the Cell Surface Nature 2005, 437, 656-663
24. Elson, E. L.; Magde, D. Fluorescence Correlation Spectroscopy. I. Conceptual Basis and Theory Biopolymers 1974, 13, 1-27
25. Axelrod, D.; Koppel, D.; Schlessinger, J.; Elson, E.; Webb, W. Mobility Measurement by Analysis of Fluorescence Photobleaching Recovery Kinetics Biophys. J. 1976, 16, 1055-1069
26. Saxton, M. Lateral Diffusion in an Archipelago. Single-Particle Diffusion Biophys. J. 1993, 64, 1766-1780
27. Grünwald, D.; Martin, R. M.; Buschmann, V.; Bazett-Jones, D. P.; Leonhardt, H.; Kubitscheck, U.; Cardoso, M. C. Probing Intranuclear Environments at the Single-Molecule Level Biophys. J. 2008, 94, 2847-2858
28. Schütz, G.; Schindler, H.; Schmidt, T. Single-Molecule Microscopy on Model Membranes Reveals Anomalous Diffusion Biophys. J. 1997, 73, 1073-1080
29. Thompson, R. E.; Larson, D. R.; Webb, W. W. Precise Nanometer Localization Analysis for Individual Fluorescent Probes Biophys. J. 2002, 82, 2775-2783
30. Widengren, J.; Rigler, R. Mechanisms of Photobleaching Investigated by Fluorescence Correlation Spectroscopy Bioimaging 1996, 4, 149-157
31. Sharonov, A.; Bandichhor, R.; Burgess, K.; Petrescu, A. D.; Schroeder, F.; Kier, A. B.; Hochstrasser, R. M. Lipid Diffusion from Single Molecules of a Labeled Protein Undergoing Dynamic Association with Giant Unilamellar Vesicles and Supported Bilayers Langmuir 2008, 24, 844-850
32. Scomparin, C.; Lecuyer, S.; Ferreira, M.; Charitat, T.; Tinland, B. Diffusion in Supported Lipid Bilayers: Influence of Substrate and Preparation Technique on the Internal Dynamics Eur. Phys. J. E 2009, 28, 211-220
33. Chiantia, S.; Kahya, N.; Schwille, P. Raft Domain Reorganization Driven by Short- and Long-Chain Ceramide: A Combined AFM and FCS Study Langmuir 2007, 23, 7659-7665
34. Dertinger, T.; von der Hocht, I.; Benda, A.; Hof, M.; Enderlein, J. Surface Sticking and Lateral Diffusion of Lipids in Supported Bilayers Langmuir 2006, 22, 9339-9344
35. Kubitscheck, U.; Wedekind, P.; Peters, R. Lateral Diffusion Measurement at High Spatial Resolution by Scanning Microphotolysis in a Confocal Microscope Biophys. J. 1994, 67, 948-956
36. Burns, A.; Frankel, D.; Buranda, T. Local Mobility in Lipid Domains of Supported Bilayers Characterized by Atomic Force Microscopy and Fluorescence Correlation Spectroscopy Biophys. J. 2005, 89, 1081-1093
37. Wang, T.; Ingram, C.; Weisshaar, J. C. Model Lipid Bilayer with Facile Diffusion of Lipids and Integral Membrane Proteins Langmuir 2010, 26, 11157-11164
38. Murray, D. H.; Tamm, L. K.; Kiessling, V. Supported Double Membranes J. Struct. Biol. 2009, 168, 183-189
39. Sonnleitner, A.; Schütz, G.; Schmidt, T. Free Brownian Motion of Individual Lipid Molecules in Biomembranes Biophys. J. 1999, 77, 2638-2642
40. Rabiner, L. A Tutorial on Hidden Markov Models and Selected Applications in Speech Recognition Proc. IEEE 1989, 77, 257-286
41. Montiel, D.; Cang, H.; Yang, H. Quantitative Characterization of Changes in Dynamical Behavior for Single-Particle Tracking Studies J. Phys. Chem. B 2006, 110, 19763-19770
42. Elliott, L. C. C.; Barhoum, M.; Harris, J. M.; Bohn, P. W. Trajectory Analysis of Single Molecules Exhibiting Non-Brownian Motion Phys. Chem. Chem. Phys. 2011, 13, 4326-4334
43. Das, R.; Cairo, C. W.; Coombs, D. A Hidden Markov Model for Single Particle Tracks Quantifies Dynamic Interactions between LFA-1 and the Actin Cytoskeleton PLoS Comput. Biol. 2009, 5, e1000556
44. Persson, F.; Linden, M.; Unoson, C.; Elf, J. Extracting Intracellular Diffusive States and Transition Rates From Single-Molecule Tracking Data Nat. Methods 2013, 10, 265-269
45. Bloch, I.; Quintana, F. J.; Gerber, D.; Cohen, T.; Cohen, I. R.; Shai, Y. T-Cell Inactivation and Immunosuppressive Activity Induced by HIV gp41 via Novel Interacting Motif FASEB J. 2007, 21, 393-401
46. Boukobza, E.; Sonnenfeld, A.; Haran, G. Immobilization in Surface-Tethered Lipid Vesicles as a New Tool for Single Biomolecule Spectroscopy J. Phys. Chem. B 2001, 105, 12165-12170
47. Ruprecht, V.; Brameshuber, M.; Schutz, G. J. Two-Color Single Molecule Tracking Combined with Photobleaching for the Detection of Rare Molecular Interactions in Fluid Biomembranes Soft Matter 2010, 6, 568-581
48. Widengren, J.; Chmyrov, A.; Eggeling, C.; Löfdahl, P.-A.; Seidel, C. A. M. Strategies to Improve Photostabilities in Ultrasensitive Fluorescence Spectroscopy J. Phys. Chem. A 2007, 111, 429-440
49. Serge, A.; Bertaux, N.; Rigneault, H.; Marguet, D. Dynamic Multiple-Target Tracing to Probe Spatiotemporal Cartography of Cell Membranes Nat. Methods 2008, 5, 687-694
50. Jaqaman, K.; Loerke, D.; Mettlen, M.; Kuwata, H.; Grinstein, S.; Schmid, S. L.; Danuser, G. Robust Single-Particle Tracking in Live-Cell Time-Lapse Sequences Nat. Methods 2008, 5, 695-702
51. Saxton, M. Single-Particle Tracking: the Distribution of Diffusion Coefficients Biophys. J. 1997, 72, 1744-1753
52. Murphy, K. Hidden Markov Model (HMM) Toolbox for Matlab, 1998, http://www.cs.ubc.ca/murphyk/Software/HMM/hmm.html.
53. Gambin, Y.; Lopez-Esparza, R.; Reffay, M.; Sierecki, E.; Gov, N. S.; Genest, M.; Hodges, R. S.; Urbach, W. Lateral Mobility of Proteins in Liquid Membranes Revisited Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 2098-2102
54. Ramadurai, S.; Holt, A.; Krasnikov, V.; van den Bogaart, G.; Killian, J. A.; Poolman, B. Lateral Diffusion of Membrane Proteins J. Am. Chem. Soc. 2009, 131, 12650-12656
55. Saffman, P. G. Brownian Motion in Thin Sheets of Viscous Fluid J. Fluid Mech. 1976, 73, 593
56. Cicuta, P.; Keller, S. L.; Veatch, S. L. Diffusion of Liquid Domains in Lipid Bilayer Membranes J. Phys. Chem. B 2007, 111, 3328-3331
57. Evans, E.; Sackmann, E. Translational and Rotational Drag Coefficients for a Disk Moving in a Liquid Membrane Associated with a Rigid Substrate J. Fluid Mech. 1988, 194, 553-561
58. Stone, H.; Armand Ajdar, I. Hydrodynamics of Particles Embedded in a Flat Surfactant Layer Overlying a Subphase of Finite Depth J. Fluid Mech. 1998, 369, 151-173
59. Peters, R.; Cherry, R. J. Lateral and Rotational Diffusion of Bacteriorhodopsin in Lipid Bilayers-Experimental Test of the Saffman-Delbruck Equations Proc. Natl. Acad. Sci. U.S.A. 1982, 79, 4317-4321
60. Vaz, W. L. C.; Clegg, R. M.; Hallmann, D. Translational Diffusion of Lipids in Liquid Crystalline Phase Phosphatidylcholine Multibilayers. A Comparison of Experiment with Theory Biochemistry 1985, 24, 781-786
61. Korson, L.; Drost-Hansen, W.; Millero, F. J. Viscosity of Water at Various Temperatures J. Phys. Chem. 1969, 73, 34-39
62. Cogan, U.; Shinitzky, M.; Weber, G.; Nishida, T. Microviscosity and Order in the Hydrocarbon Region of Phospholipid and Phospholipid-Cholesterol Dispersions Determined with Fluorescent Probes Biochemistry 1973, 12, 521-528
63. Glasstone, S.; Laidler, K. J.; Eyring, H. The Theory of Rate Processes: the Kinetics of Chemical Rreactions, Viscosity, Diffusion and Electrochemical Phenomena; McGraw-Hill Book Co.: New York, London, 1941; Chapter IX.
64. Cohen, M. H.; Turnbull, D. Molecular Transport in Liquids and Glasses J. Chem. Phys. 1959, 31, 1164
65. Galla, H. J.; Hartmann, W.; Theilen, U.; Sackmann, E. On Two-Dimensional Passive Random Walk in Lipid Bilayers and Fluid Pathways in Biomembranes J. Membr. Biol. 1979, 48, 215-236
66. Gaede, H. C.; Gawrisch, K. Lateral Diffusion Rates of Lipid, Water, and a Hydrophobic Drug in a Multilamellar Liposome Biophys. J. 2003, 85, 1734-1740
67. Vaz, W. L. C.; Criado, M.; Madeira, V. M. C.; Schoellmann, G.; Jovin, T. M. Size Dependence of the Translational Diffusion of Large Integral Membrane Proteins in Liquid-Crystalline Phase Lipid Bilayers. A Study Using Fluorescence Recovery after Photobleaching Biochemistry 1982, 21, 5608-5612
68. Vaz, W. L.; Dieter, H. Experimental Evidence against the Applicability of the Saffman-Delbrück Model to the Translational Diffusion of Lipids in Phosphatidylcholine Bilayer Membranes FEBS Lett. 1983, 152, 287-290
69. Needham, D.; Evans, E. Structure and Mechanical Properties of Giant Lipid (DMPC) Vesicle Bilayers from 20 C below to 10 C above the Liquid Crystal-Crystalline Phase Transition at 24.degree.C Biochemistry 1988, 27, 8261-8269
70. Machán, R.; Hof, M. Lipid Diffusion in Planar Membranes Investigated by Fluorescence Correlation Spectroscopy Biochim. Biophys. Acta, Biomembr. 2010, 1798, 1377-1391
71. Seu, K. J.; Cambrea, L. R.; Everly, R. M.; Hovis, J. S. Influence of Lipid Chemistry on Membrane Fluidity: Tail and Headgroup Interactions Biophys. J. 2006, 91, 3727-3735
72. Takeshima, K.; Chikushi, A.; Lee, K.-K.; Yonehara, S.; Matsuzaki, K. Translocation of Analogues of the Antimicrobial Peptides Magainin and Buforin across Human Cell Membranes J. Biol. Chem. 2003, 278, 1310-1315
73. Stella, L.; Burattini, M.; Mazzuca, C.; Palleschi, A.; Venanzi, M.; Coin, I.; Peggion, C.; Toniolo, C.; Pispisa, B. Alamethicin Interaction with Lipid Membranes: A Spectroscopic Study on Synthetic Analogues Chem. Biodiversity 2007, 4, 1299-1312
74. Wassall, S. Pulsed Field Gradient-Spin Echo NMR Studies of Water Diffusion in a Phospholipid Model Membrane Biophys. J. 1996, 71, 2724-2732
75. Tampe, R.; Von Lukas, A.; Galla, H. J. Glycophorin-Induced Cholesterol-Phospholipid Domains in Dimyristoylphosphatidylcholine Bilayer Vesicles Biochemistry 1991, 30, 4909-4916
76. Sheynis, T.; Sykora, J.; Benda, A.; Kolusheva, S.; Hof, M.; Jelinek, R. Bilayer Localization of Membrane-Active Peptides Studied in Biomimetic Vesicles by Visible and Fluorescence Spectroscopies Eur. J. Biochem. 2003, 270, 4478-4487
77. Guo, L.; Smith-Dupont, K. B.; Gai, F. Diffusion as a Probe of Peptide-Induced Membrane Domain Formation Biochemistry 2011, 50, 2291-2297
78. Smith-Dupont, K. B.; Guo, L.; Gai, F. Diffusion as a Probe of the Heterogeneity of Antimicrobial Peptide-Membrane Interactions Biochemistry 2010, 49, 4672-4678
79. Niemela, P. S.; Miettinen, M. S.; Monticelli, L.; Hammaren, H.; Bjelkmar, P.; Murtola, T.; Lindahl, E.; Vattulainen, I. Membrane Proteins Diffuse as Dynamic Complexes with Lipids J. Am. Chem. Soc. 2010, 132, 7574-7575
80. Tokumasu, F.; Jin, A. J.; Feigenson, G. W.; Dvorak, J. A. Atomic Force Microscopy of Nanometric Liposome Adsorption and Nanoscopic Membrane Domain Formation Ultramicroscopy 2003, 97, 217-227
81. Petrache, H. I.; Tristram-Nagle, S.; Nagle, J. F. Fluid Phase Structure of EPC and DMPC Bilayers Chem. Phys. Lipids 1998, 95, 83-94
82. Shchelokovskyy, P.; Tristram-Nagle, S.; Dimova, R. Effect of the HIV-1 Fusion Peptide on the Mechanical Properties and Leaflet Coupling of Lipid Bilayers New J. Phys. 2011, 13, 025004
83. Martens, S.; McMahon, H. T. Mechanisms of Membrane Fusion: Disparate Players and Common Principles Nat. Rev. Mol. Cell Biol. 2008, 9, 543-556
84. Naji, A.; Levine, A. J.; Pincus, P. Corrections to the Saffman-Delbrück Mobility for Membrane Bound Proteins Biophys. J. 2007, 93, L49-L51
85. Naji, A.; Atzberger, P. J.; Brown, F. L. H. Hybrid Elastic and Discrete-Particle Approach to Biomembrane Dynamics with Application to the Mobility of Curved Integral Membrane Proteins Phys. Rev. Lett. 2009, 102, 138102
86. Lecuyer, S.; Charitat, T. From Supported Membranes to Tethered Vesicles: Lipid Bilayers Destabilisation at the Main Transition Europhys. Lett. 2006, 75, 652
87. Goldberg, R.; Schroeder, A.; Silbert, G.; Turjeman, K.; Barenholz, Y.; Klein, J. Boundary Lubricants with Exceptionally Low Friction Coefficients Based on 2D Close-Packed Phosphatidylcholine Liposomes Adv. Mater. 2011, 23, 3517-3521