Protein transduction domains of HIV-1 and SIV TAT interact with charged lipid vesicles. Binding mechanism and thermodynamic analysis

Biochemistry

Volumn 42, Issue 30, 2003, Pages 9185-9194

  Ziegler, André ^a   Li Blatter, Xiaochun ^a   Seelig, Anna ^a   Seelig, Joachim ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

INVERTED MICELLES;

AMINO ACIDS; CELL MEMBRANES; CONFORMATIONS; LIPIDS; MICELLES; MONOLAYERS; THERMODYNAMICS; VIRUSES;

PROTEINS;

AMINO ACID; ANION; CELL PROTEIN; DEUTERIUM; DYE; GLYCOSAMINOGLYCAN; MEMBRANE PROTEIN; PHOSPHATIDYLGLYCEROL; PHOSPHORUS 31; TRANSACTIVATOR PROTEIN; VIRUS PROTEIN;

ADSORPTION; ARTICLE; BINDING AFFINITY; CALORIMETRY; CELL CULTURE; CELL MEMBRANE; CHEMICAL REACTION; CONFORMATIONAL TRANSITION; ELECTRICITY; ENERGY; ENTHALPY; FILM; HEAT; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROPHOBICITY; LIGHT SCATTERING; LIPID BILAYER; LIPID VESICLE; MEASUREMENT; MEMBRANE BINDING; MICELLE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SIMIAN IMMUNODEFICIENCY VIRUS; STOICHIOMETRY; THERMODYNAMICS; TITRIMETRY;

ANIMALS; BINDING SITES; CALORIMETRY; DEUTERIUM; ELECTROSTATICS; GENE PRODUCTS, TAT; HIV-1; HUMANS; LIPID BILAYERS; MODELS, CHEMICAL; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLGLYCEROLS; PHOSPHORUS ISOTOPES; PRESSURE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SCATTERING, RADIATION; SIMIAN IMMUNODEFICIENCY VIRUS; SURFACE PROPERTIES; THERMODYNAMICS;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; INSERTION SEQUENCES; SIMIAE; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 0043166977     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0346805     Document Type: Article

References (54)

1. Lindgren, M., Hallbrink, M., Prochiantz, A., and Langel, U. (2000) Cell-penetrating peptides, Trends Pharmacol. Sci. 21, 99-103.
2. Frankel, A. D., and Pabo, C. O. (1988) Cellular uptake of the tat protein from human immunodeficiency virus, Cell 55, 1189-93.
3. Green, M., and Loewenstein, P. M. (1988) Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein, Cell 55, 1179-88.
4. Thorén, P. E., Persson, D., Karlsson, M., and Norden, B. (2000) The antennapedia peptide penetratin translocates across lipid bilayers-the first direct observation, FEBS Lett. 482, 265-8.
5. Drin, G., Demene, H., Temsamani, J., and Brasseur, R. (2001) Translocation of the pAntp peptide and its amphipathic analogue AP-2AL, Biochemistry 40, 1824-34.
6. Tyagi, M., Rusnati, M., Presta, M., and Giacca, M. (2001) Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans, J. Biol. Chem. 276, 3254-61.
7. Prochiantz, A. (2000) Messenger proteins: homeoproteins, TAT, and others, Curr. Opin. Cell Biol. 12, 400-6.
8. von Heijne, G. (2000) Membrane permeability-Transport of peptides and proteins through membranes-Editorial overview, Curr. Opin. Cell Biol. 12, 399.
9. Gally, H. U., Niederberger, W., and Seelig, J. (1975) Conformation and motion of the choline headgroup in bilayers of dipalmitoyl-3-sn-phosphatidylcholine, Biochemistry 14, 3647-52.
10. Wohlgemuth, R., Waespe-Sarcevic, N., and Seelig, J. (1980) Bilayers of phosphatidylglycerol. A deuterium and phosphorus nuclear magnetic resonance study of the headgroup region, Biochemistry 19, 3315-21.
11. Buser, C. A., and McLaughlin, S. (1998) Ultracentrifugation technique for measuring the binding of peptides and proteins to sucrose-loaded phospholipid vesicles, Methods Mol. Biol. 84, 267-81.
12. Seelig, A., Alt, T., Lotz, S., and Holzemann, G. (1996) Binding of substance P agonists to lipid membranes and to the neurokinin-1 receptor, Biochemistry 35, 4365-74.
13. Seelig, A. (1987) Local anesthetics and pressure a comparison of dibucaine binding to lipid monolayers and bilayers, Biochim. Biophys. Acta 899, 196-204.
14. Seelig, A. (1992) Interaction of a substance P agonist and of substance P antagonists with lipid membranes. A thermodynamic analysis, Biochemistry 31, 2897-904.
15. Boguslavsky, V., Rebecchi, M., Morris, A. J., Jhon, D. Y., Rhee, S. G., and McLaughlin, S. (1994) Effect of monolayer surface pressure on the activities of phosphoinositide-specific phospholipase C-β1, -γ 1, and -δ 1, Biochemistry 33, 3032-7.
16. Wieprecht, T., Beyermann, M., and Seelig, J. (1999) Binding of antibacterial magainin peptides to electrically neutral membranes: thermodynamics and structure, Biochemistry 38, 10377-87.
17. van Holde, K. E., Johnson, W. C., and Ho, S. P. (1998) Principles of Physical Biochemistry, p 605, Prentice Hall, Upper Saddle River, New Jersey.
18. Seelig, J. (1997) Titration calorimetry of lipid-peptide interactions, Biochim. Biophys. Acta 1331, 103-16.
19. Wiseman, T., Williston, S., Brandts, J. F., and Lin, L. N. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter, Anal. Biochem. 179, 131-7.
20. Michaelson, D. M., Horwitz, A. F., and Klein, M. P. (1973) Transbilayer asymmetry and surface homogeneity of mixed phospholipids in cosonicated vesicles, Biochemistry 12, 2637-45.
21. Aveyard, R., and Haydon, D. A. (1973) An introduction to the principles of surface chemistry, Cambridge University Press, London.
22. McLaughlin, S. (1977) Electrostatic potentials at membrane-solution interfaces, Curr. Top. Membr. Transp. 9, 71-144.
23. Beschiaschvili, G., and Seelig, J. (1990) Peptide binding to lipid bilayers. Binding isotherms and ζ-potential of a cyclic somatostafin analogue, Biochemistry 29, 10995-1000.
24. Seelig, J., Nebel, S., Ganz, P., and Bruns, C. (1993) Electrostatic and nonpolar peptide-membrane interactions. Lipid binding and functional properties of somatostatin analogues of charge z = +1 to z = +3, Biochemistry 32, 9714-21.
25. 31P nuclear magnetic resonance and the headgroup structure of phospholipids in membranes, Biochim. Biophys. Acta 515, 105-40.
26. Seelig, J., Macdonald, P. M., and Scherer, P. G. (1987) Phospholipid headgroups as sensors of electric charge in membranes, Biochemistry 26, 7535-41.
27. Niederberger, W., and Seelig, J. (1974) Deuterium magnetische Resonanzspektroskopie an spezifisch deuterierten flüssigen Kristallen, Ber. Bunsen-Ges. Physik. Chem. 78, 947-9.
28. Macdonald, P. M., and Seelig, J. (1987) Calcium binding to mixed phosphatidylglycerol-phosphatidylcholine bilayers as studied by deuterium nuclear magnetic resonance, Biochemistry 26, 1231-40.
29. Akutsu, H., and Seelig, J. (1981) Interaction of metal ions with phosphatidylcholine bilayer membranes, Biochemistry 20, 7366-73.
30. 2+ complex with two phospholipid molecules, Biochemistry 23, 3913-20.
31. Seelig, A., Allegrini, P. R., and Seelig, J. (1988) Partitioning of local anesthetics into membranes: surface charge effects monitored by the phospholipid headgroup, Biochim. Biophys. Acta 939, 267-76.
32. Boulanger, Y., Schreier, S., and Smith, I. C. (1981) Molecular details of anesthetic-lipid interaction as seen by deuterium and phosphorus-31 nuclear magnetic resonance, Biochemistry 20, 6824-30.
33. Schote, U., and Seelig, J. (1998) Interaction of the neuronal marker dye FM1-43 with lipid membranes. Thermodynamics and lipid ordering, Biochim. Biophys. Acta 1415, 135-46.
34. Bäuerle, H. D., and Seelig, J. (1991) Interaction of charged and uncharged calcium channel antagonists with phospholipid membranes. Binding equilibrium, binding enthalpy, and membrane location, Biochemistry 30, 7203-11.
35. Thomas, P. G., and Seelig, J. (1993) Binding of the calcium antagonist flunarizine to phosphatidylcholine bilayers: charge effects and thermodynamics, Biochem. J. 291, 397-402.
36. Kuchinka, E., and Seelig, J. (1989) Interaction of melittin with phosphatidylcholine membranes. Binding isotherm and lipid headgroup conformation, Biochemistry 28, 4216-21.
37. Beschiaschvili, G., and Seelig, J. (1991) Peptide binding to lipid membranes. Spectroscopic studies on the insertion of a cyclic somatostatin analogue into phospholipid bilayers, Biochim. Biophys. Acta 1061, 78-84.
38. Spuhler, P., Anantharamaiah, G. M., Segrest, J. P., and Seelig, J. (1994) Binding of apolipoprotein A-I model peptides to lipid bilayers. Measurement of binding isotherms and peptide-lipid headgroup interactions, J. Biol. Chem. 269, 23904-10.
39. 31P NMR study of pentalysine interaction with headgroup deuterated phosphatidylcholine and phosphatidylserine, Eur. Biophys. J. 16, 267-73.
40. Franzin, C. M., and Macdonald, P. M. (2001) Polylysine-induced H-2 NMR-observable domains in phosphatidylserine/phosphatidylcholine lipid bilayers, Biophys. J. 81, 3346-62.
41. May, S., Harries, D., and Ben-Shaul, A. (2000) Lipid demixing and protein-protein interactions in the adsorption of charged proteins on mixed membranes, Biophys. J. 79, 1747-60.
42. Ziegler, A., and Seelig, J. Interaction of protein transduction domain of HIV-1 TAT with heparan sulfate. Binding mechanism and thermodynamic parameters, submitted.
43. Bratton, D. L., Fadok, V. A., Richter, D. A., Kailey, J. M., Guthrie, L. A., and Henson, P. M. (1997) Appearance of phosphatidylserine on apoptotic cells requires calcium-mediated nonspecific flip-flop and is enhanced by loss of the aminophospholipid translocase, J. Biol. Chem. 272, 26159-65.
44. Cantor, C. R., and Schimmel, P. R. (1980) Biophysical Chemistry, Vol. 1, p 283 Freeman, San Francisco.
45. Murray, D., Arbuzova, A., Hangyas-Mihalyne, G., Gambhir, A., Ben-Tal, N., Honig, B., and McLaughlin, S. (1999) Electrostatic properties of membranes containing acidic lipids and adsorbed basic peptides: theory and experiment, Biophys. J. 77, 3176-88.
46. Derossi, D., Joliot, A. H., Chassaing, G., and Prochiantz, A, (1994) The third helix of the Antennapedia homeodomain translocates through biological membranes, J. Biol. Chem. 269, 10444-50.
47. Scheller, A., Oehlke, J., Wiesner, B., Dathe, M., Krause, E., Beyermann, M., Melzig, M., and Bienert, M. (1999) Structural requirements for cellular uptake of α-helical amphipathic peptides, J. Pept. Sci. 5, 185-94.
48. Derossi, D., Calvet, S., Trembleau, A., Brunissen, A., Chassaing, G., and Prochiantz, A. (1996) Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent, J. Biol. Chem. 271, 18188-93.
49. Brugidou, J., Legrand, C., Mery, J., and Rabie, A. (1995) The retro-inverso form of a homeobox-derived short peptide is rapidly internalized by cultured neurones: a new basis for an efficient intracellular delivery system, Biochem. Biophys. Res. Commun. 214, 685-93.
50. Fischer, P. M., Zhelev, N. Z., Wang, S., Melville, J. E., Fahraeus, R., and Lane, D. P. (2000) Structure-activity relationship of truncated and substituted analogues of the intracellular delivery vector Penetratin, J. Pept. Res. 55, 163-72.
51. Thoren, P. E., Persson, D., Karlsson, M., and Norden, B. (2000) The antennapedia peptide penetratin translocates across lipid bilayers-the first direct observation, FEBS Lett 482, 265-8.
52. Persson, D., Thoren, P. E., Herner, M., Lincoln, P., and Norden, B. (2003) Application of a novel analysis to measure the binding of the membrane-translocating peptide penetratin to negatively charged liposomes, Biochemistry 42, 421-9.
53. Wieprecht, T., Apostolov, O., Beyermann, M., and Seelig, J. (1999) Thermodynamics of the α-helix-coil transition of amphipathic peptides in a membrane environment: implications for the peptide-membrane binding equilibrium, J. Mol. Biol. 294, 785-94.
54. Mitchell, D. J., Kim, D. T., Steinman, L., Fathman, C. G., and Rothbard, J. B. (2000) Polyarginine enters cells more efficiently than other polycationic homopolymers, J. Pept. Res. 56, 318-25.