Binding of oligoarginine to membrane lipids and heparan sulfate: Structural and thermodynamic characterization of a cell-penetrating peptide

Biochemistry

Volumn 44, Issue 7, 2005, Pages 2692-2702

  Gonçalves, Elisabete ^a   Kitas, Eric ^b   Seelig, Joachim ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CALORIMETERS; ENTHALPY; HYDROPHOBICITY; NUCLEAR MAGNETIC RESONANCE; POSITIVE IONS; PROTEINS;

ASSOCIATION CONSTANT; BINDING SITES; CELL-PENETRATING PEPTIDES (CPP); HEPARAN SULFATE (HS);

LIPIDS;

2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; ARGININE; DEUTERIUM; HEPARAN SULFATE; MEMBRANE LIPID; PROTEOHEPARAN SULFATE;

ARTICLE; CALORIMETRY; CELL SURFACE; ELECTRICITY; ELECTROPHORETIC MOBILITY; ENTHALPY; ENTROPY; ISOTHERMAL TITRATION CALORIMETRY; LIPID BILAYER; LIPID VESICLE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; THERMODYNAMICS;

ANIMALS; ANIONS; ARGININE; CALORIMETRY; CELL MEMBRANE PERMEABILITY; DEUTERIUM EXCHANGE MEASUREMENT; ELECTROSTATICS; HEPARITIN SULFATE; LIGHT; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, CHEMICAL; OLIGOPEPTIDES; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLGLYCEROLS; PHOSPHORUS ISOTOPES; PROTEIN BINDING; SCATTERING, RADIATION; SWINE; THERMODYNAMICS;

EID: 14044270161     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048046i     Document Type: Article

References (80)

1. Lundberg, P., and Langel, U. (2003) A brief introduction to cell-penetrating peptides, J. Mol. Recognit. 16, 227-233.
2. Jarver, P., and Langel, U. (2004) The use of cell-penetrating peptides as a tool for gene regulation, Drug Discovery Today 9, 395-402.
3. Zhao, M., and Weissleder, R. (2004) Intracellular cargo delivery using tat peptide and derivatives, Med. Res. Rev. 24, 1-12.
4. Fawell, S., Seery, J., Daikh, Y., Moore, C., Chen, L., Pepinsky, B., and Barsoum, J. (1994) Tat-mediated delivery of heterologous proteins into cells, Proc. Natl. Acad. Sci. U.S.A. 91, 664-668.
5. Schwarze, S. R., Ho, A., Vocero-Akbani, A., and Dowdy, S. F. (1999) In vivo protein transduction: Delivery of a biologically active protein into the mouse, Science 285, 1569-1572.
6. Astriab-Fisher, A., Sergueev, D., Fisher, M., Shaw, B. R., and Juliano, R. L. (2002) Conjugates of antisense oligonucleotides with the Tat and antennapedia cell-penetrating peptides: Effects on cellular uptake, binding to target sequences, and biologic actions, Pharm. Res. 19, 744-754.
7. Torchilin, V. P., Levchenko, T. S., Rammohan, R., Volodina, N., Papahadjopoulos-Sternberg, B., and D'Souza, G. G. M. (2003) Cell transfection in vitro and in vivo with nontoxic TAT peptide-liposome-DNA complexes, Proc. Natl. Acad. Sci. U.S.A. 100, 1972-1977.
8. Nori, A., Jensen, K. D., Tijerina, M., Kopeckova, P., and Kopecek, J. (2003) Tat-conjugated synthetic macromolecules facilitate cytoplasmic drug delivery to human ovarian carcinoma cells, Bioconjugate Chem. 14, 44-50.
9. Vives, E., Brodin, P., and Lebleu, B. (1997) A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus, J. Biol. Chem. 272, 16010-16017.
10. Derossi, D., Joliot, A., Chassaing, G., and Prochiantz, A. (1994) The third helix of the Antennapedia homeodomain translocates through biological membranes, J. Biol. Chem. 269, 10444-10450.
11. Wender, P. A., Mitchell, D. J., Pattabiraman, K., Pelkey, E. T., Steinman, L., and Rothbard, J. B. (2000) The design, synthesis, and evaluation of molecules that enable or enhance cellular uptake: Peptoid molecular transporters, Proc. Natl. Acad. Sci. U.S.A. 97, 13003-13008.
12. 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, 318-325.
13. Futaki, S., Suzuki, T., Ohashi, W., Yagami, T., Tanaka, S., Ueda, K., and Sugiura, Y. (2001) Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery, J. Biol. Chem. 276, 5836-5840.
14. Wender, P. A., Rothbard, J. B., Jessop, T. C., Kreider, E. L., and Wylie, B. L. (2002) Oligocarbamate molecular transporters: Design, synthesis, and biological evaluation of a new class of transporters for drug delivery, J. Am. Chem. Soc. 124, 13382-13383.
15. Futaki, S., Nakase, I., Suzuki, T., Youjun, Z., and Sugiura, Y. (2002) Translocation of branched-chain arginine peptides through cell membranes: Flexibility in the spatial disposition of positive charges in membrane-permeable peptides, Biochemistry 41, 7925-7930.
16. Suzuki, T., Futaki, S., Niwa, M., Tanaka, S., Ueda, K., and Sugiura, Y. (2002) Possible existence of common internalization mechanisms among arginine-rich peptides, J. Biol. Chem. 277, 2437-2443.
17. Lundberg, M., and Johansson, M. (2002) Positively charged DNA-binding proteins cause apparent cell membrane translocation, Biochem. Biophys. Res. Commun. 291, 367-371.
18. Richard, J. P., Melikov, K., Vives, E., Ramos, C., Verbeure, B., Gait, M. J., Chernomordik, L. V., and Lebleu, B. (2003) Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake, J. Biol. Chem. 278, 585-590.
19. Drin, G., Cottin, S., Blanc, E., Rees, A. R., and Temsamani, J. (2003) Studies on the internalization mechanism of cationic cell-penetrating peptides, J. Biol. Chem. 278, 31192-31201.
20. Console, S., Marty, C., Garcia-Echeverria, C., Schwendener, R., and Ballmer-Hofer, K. (2003) Antennapedia and HIV transactivator of transcription (TAT) "Protein transduction domains" promote endocytosis of high molecular weight cargo upon binding to cell surface glycosaminoglycans, J. Biol. Chem. 278, 35109-35114.
21. Fittipaldi, A., Ferrari, A., Zoppe, M., Arcangeli, C., Pellegrini, V., Beltram, F., and Giacca, M. (2003) Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 Tat fusion proteins, J. Biol. Chem. 278, 34141-34149.
22. Fuchs, S. M., and Raines, R. T. (2004) Pathway for polyarginine entry into mammalian cells, Biochemistry 43, 2438-2444.
23. Fischer, R., Kohler, K., Fotin-Mleczek, M., and Brock, R. (2004) A stepwise dissection of the intracellular fate of cationic cell-penetrating peptides, J. Biol. Chem. 279, 12625-12635.
24. Thoren, P. E., Persson, D., Isakson, P., Goksor, M., Onfelt, A., and Norden, B. (2003) Uptake of analogs of penetratin, Tat(48-60) and oligoarginine in live cells, Biochem. Biophys. Res. Commun. 307, 100-107.
25. Brugidou, J., Legrand, C., Mery, J., and Rabie, A. (1995) The retro-inverso form of a homeobox-derived short peptide is rapidly internalised by cultured neurones: A new basis for an efficient intracellular delivery system, Biochem. Biophys. Res. Commun. 214, 685-693.
26. 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, 18188-18193.
27. Shieh, M., WuDunn, D., Montgomery, R., Esko, J., and Spear, P. (1992) Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans, J. Cell Biol. 116, 1273-1281.
28. Love, D., Esko, J., and Mosser, D. (1993) A heparin-binding activity on Leishmania amastigotes which mediates adhesion to cellular proteoglycans, J. Cell Biol. 123, 759-766.
29. Dehio, C., Freissler, E., Lanz, C., Gomez-Duarte, O. G., David, G., and Meyer, T. F. (1998) Ligation of cell surface heparan sulfate proteoglycans by antibody-coated beads stimulates phagocytic uptake into epithelial cells: A model for cellular invasion by Neisseria gonorrhoeas, Exp. Cell Res. 242, 528-539.
30. Rusnati, M., Coltrini, D., Oreste, P., Zoppetti, G., Albini, A., Noonan, D., d'Adda di Fagagna, F., Giacca, M., and Presta, M. (1997) Interaction of HIV-1 Tat protein with heparin. Role of the backbone structure, sulfation, and size, J. Biol. Chem. 272, 11313-11320.
31. 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, 3254-3261.
32. Silhol, M., Tyagi, M., Giacca, M., Lebleu, B., and Vives, E. (2002) Different mechanisms for cellular internalization of the HIV-1 Tat-derived cell penetrating peptide and recombinant proteins fused to Tat, Eur. J. Biochem. 269, 494-501.
33. Violini, S., Sharma, V., Prior, J. L., Dyszlewski, M., and Piwnica-Worms, D. (2002) Evidence for a plasma membrane-mediated permeability barrier to Tat basic domain in well-differentiated epithelial cells: Lack of correlation with heparan sulfate, Biochemistry 41, 12652-12661.
34. Berlose, J. P., Convert, O., Derossi, D., Brunissen, A., and Chassaing, G. (1996) Conformational and associative behaviours of the third helix of antennapedia homeodomain in membrane-mimetic environments, Eur. J. Biochem. 242, 372-386.
35. Xu, Y., and Szoka, F. C., Jr. (1996) Mechanism of DNA release from cationic liposome/DNA complexes used in cell transfection, Biochemistry 35, 5616-5623.
36. Deshayes, S., Heitz, A., Morris, M. C., Charnet, P., Divita, G., and Heitz, F. (2004) Insight into the mechanism of internalization of the cell-penetrating carrier peptide Pep-1 through conformational analysis, Biochemistry 43, 1449-1457.
37. Atherton, E., and Sheppard, R. C. (1989) Solid-Phase Peptide Synthesis: A Practical Approach, IRL Press, Oxford, U.K.
38. Ziegler, A., and Seelig, J. (2004) Interaction of the protein transduction domain of HIV-1 TAT with heparan sulfate: Binding mechanism and thermodynamic parameters, Biophys. J. 86, 254-263.
39. Hunter, R. J. (1981) ζ Potential in Colloid Science. Principles and Applications, Academic Press, London, U.K.
40. Seelig, J. (1997) Titration calorimetry of lipid-peptide interactions, Biochim. Biophys. Acta 1331, 103-116.
41. Wieprecht, T., and Seelig, J. (2002) in Current Topics in Membranes, pp 31-56, Elsevier Science, New York.
42. Cantor, C. R., and Shimmel, P. R. (1980) in The Behavior of Biological Macromolecules, pp 849-885, W. H. Freeman and Company, San Francisco, CA.
43. van Holde, K. E., Johnson, W. C., and Ho, P. S. (1998) in Principles of Physical Biochemistry, pp 587-637, Upper Sadle River, NJ.
44. Connors, K. A. (1987) Binding Constants, Wiley-Interscience, New York.
45. Mason, J. T., and Huang, C. (1978) Hydrodynamic analysis of egg phosphatidylcholine vesicles, Ann. N.Y. Acad. Sci. 308, 29-49.
46. 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, 131-137.
47. 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, 9714-9721.
48. Terzi, E., Holzemann, G., and Seelig, J. (1994) Alzheimer β-amyloid peptide 25-35: Electrostatic interactions with phospholipid membranes, Biochemistry 33, 7434-7441.
49. Terzi, E., Holzemann, G., and Seelig, J. (1995) Self-association of β-amyloid peptide (1-40) in solution and binding to lipid membranes, J. Mol. Biol. 252, 633-642.
50. Wenk, M. R., and Seelig, J. (1998) Magainin 2 amide interaction with lipid membranes: Calorimetric detection of peptide binding and pore formation, Biochemistry 37, 3909-3916.
51. Ziegler, A., Blatter, X. L., Seelig, A., and Seelig, J. (2003) Protein transduction domains of HTV-1 and SIV TAT interact with charged lipid vesicles. Binding mechanism and thermodynamic analysis, Biochemistry 42, 9185-9194.
52. Hiemenz, P. C., and Rajagopalan, R. (1997) Principles of Colloid and Surface Chemistry, 3rd ed., Marcel Dekker, Inc., New York.
53. Nebel, S., Ganz, P., and Seelig, J. (1997) Heat changes in lipid membranes under sudden osmotic stress, Biochemistry 36, 2853-2859.
54. Beschiaschvili, G., and Seelig, J. (1990) Peptide binding to lipid bilayers. Binding isotherms and ζ-potential of a cyclic somatostatin analogue, Biochemistry 29, 10995-11000.
55. 31P nuclear magnetic resonance and the head group structure of phospholipids in membranes, Biochim. Biophys. Acta 515, 105-140.
56. Wohlgemuth, R., Waespe-Sarcevic, N., and Seelig, J. (1980) Bilayers of phosphatidylglycerol. A deuterium and phosphorus nuclear magnetic resonance study of the head group region, Biochemistry 19, 3315-3321.
57. Seelig, A., Allegrini, P. R., and Seelig, J. (1988) Partitioning of local anesthetics into membranes: Surface charge effects monitored by the phospholipid head group, Biochim. Biophys. Acta 939, 267-276.
58. Lewis, G. N., Randall, M., Pitzer, K. S., and Brewer, L. (1961) Thermodynamics, 2nd ed., McGraw-Hill, New York.
59. Murphy, K. P., and Gill, S. J. (1991) Solid model compounds and the thermodynamics of protein unfolding, J. Mol. Biol. 222, 699-709.
60. Gelman, R. A., Glaser, D. N., and Blackwell, J. (1973) Interaction between chondroitin-6-sulfate and poly-L-arginine in aqueous solution, Biopolymers 12, 1223-1232.
61. Gelman, R. A., and Blackwell, J. (1973) Interactions between mucopolysaccharides and cationic polypeptides in aqueous solution: Chondroitin 4-sulfate and dermatan sulfate, Biopolymers 12, 1959-1974.
62. Gelman, R. A., and Blackwell, J. (1974) Interactions between mucopolysaccharides and cationic polypeptides in aqueous solution: Hyaluronic acid, heparitin sulfate, and keratan sulfate, Biopolymers 13, 139-156.
63. Hileman, R. E., Jennings, R. N., and Linhardt, R. J. (1998) Thermodynamic analysis of the heparin interaction with a basic cyclic peptide using isothermal titration calorimetry, Biochemistry 37, 15231-15237.
64. Fromm, J. R., Hileman, R. E., Caldwell, E. E. O., Weiler, J, M., and Linhardt, R. J. (1997) Pattern and spacing of basic amino acids in heparin binding sites, Arch. Biochem. Biophys, 343, 92-100.
65. Griffin, C. C., Linhardt, R. J., van Gorp, C. L., Toida, T., Hileman, R. E., Schubert, I., Robert L., and Brown, S. E. (1995) Isolation and characterization of heparan sulfate from crude porcine intestinal mucosal peptidoglycan heparin, Carbohydr. Res. 276, 183-197.
66. Sakai, N., and Matile, S. (2003) Anion-mediated transfer of polyarginine across liquid and bilayer membranes, J. Am. Chem. Soc. 125, 14348-14356.
67. Record, M. T., Jr., Anderson, C. F., and Lohman, T. M. (1978) Thermodynamic analysis of ion effects on the binding and conformational equilibria of proteins and nucleic acids: The roles of ion association or release, screening, and ion effects on water activity, Q. Rev. Biophys. 11, 103-178.
68. Ziegler, A., Nervi, P., Dürrenberger, M., and Seelig, J. (2004) The cationic cell-penetrating pep tide CPPTAT derived from the HIV-1 protein TAT is rapidly transported into living fibroblasts: Optical, biophysical, and metabolic evidences, Biochemistry, in press.
69. Rothbard, J. B., Jessop, T. C., Lewis, R. S., Murray, B. A., and Wender, P. A. (2004) Role of membrane potential and hydrogen bonding in the mechanism of translocation of guanidinium-rich peptides into cells, J. Am. Chem. Soc. 126, 9506-9507.
70. Kim, J., Mosior, M., Chung, L. A., Wu, H., and McLaughlin, S. (1991) Binding of peptides with basic residues to membranes containing acidic phospholipids, Biophys. J. 60, 135-148.
71. Thoren, P. E., Persson, D., Esbjorner, E. K., Goksor, M., Lincoln, P., and Norden, B. (2004) Membrane binding and translocation of cell-penetrating peptides, Biochemistry 43, 3471-3489.
72. Seelig, J., Macdonald, P. M., and Scherer, P. G. (1987) Phospholipid head groups as sensors of electric charge in membranes, Biochemistry 26, 7535-7541.
73. Akutsu, H., and Seelig, J. (1981) Interaction of metal ions with phosphatidylcholine bilayer membranes, Biochemistry 20, 7366-7373.
74. Kuchinka, E., and Seelig, J. (1989) Interaction of melittin with phosphatidylcholine membranes. Binding isotherm and lipid head group conformation, Biochemistry 28, 4216-4221.
75. Beschiaschvili, G., and Seelig, J. (1991) Peptide binding to lipid membranes. Spectroscopic studies on the insertion of a cyclic somatostatin analog into phospholipid bilayers, Biochim. Biophys. Acta 1061, 78-84.
76. 31P NMR study of pentalysine interaction with headgroup deuterated phosphatidylcholine and phosphatidylserine, Eur. Biophys. J. 16, 267-273.
77. Beschiaschvili, G., and Seelig, J. (1990) Melittin binding to mixed phosphatidylglycerol/phosphatidylcholine membranes, Biochemistry 29, 52-58.
78. Rand, R. P., and Parsegian, V. A. (1989) Hydration forces between phospholipid bilayers, Biochim. Biophys. Acta 988, 351-376.
79. Scherer, P. G., and Seelig, J. (1987) Structure and dynamics of the phosphatidylcholine and the phosphatidylethanolamine head group in L-M fibroblasts as studied by deuterium nuclear magnetic resonance, EMBO J. 6, 2915-2922.
80. David, G. (1993) Integral membrane heparan sulfate proteoglycans, FASEB J. 7, 1023-1030.