Characterization of the mechanisms of HIV-1 Vpr(52-96) internalization in cells

Biochimie

Volumn 93, Issue 10, 2011, Pages 1647-1658

  Greiner, Vanille J ^a   Shvadchak, Volodymyr ^a   Fritz, Joëlle ^a   Arntz, Youri ^a   Didier, Pascal ^a   Frisch, Benoît ^a   Boudier, Christian ^a   Mély, Yves ^a   De Rocquigny, Hugues ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Confocal microscopy; FLIM; Fluorescence; HIV; Vpr

Indexed keywords

CLATHRIN; CYCLODEXTRIN; HEPARIN; LIPOSOME; PROTEOHEPARAN SULFATE; TRANSFERRIN; VPR PROTEIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; BRAIN OXYGEN TENSION; CARBOXY TERMINAL SEQUENCE; CAVEOLA; CELL MEMBRANE PERMEABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; ENDOCYTOSIS; FEMALE; FLUORESCENCE IMAGING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INTRACELLULAR TRANSPORT; ISOTHERMAL TITRATION CALORIMETRY; LIGHT SCATTERING; LIPID BILAYER; LIPID RAFT; NONHUMAN; PROTEIN AGGREGATION; UBIQUITINATION; VIRUS CHARACTERIZATION; VIRUS ENTRY;

BETA-CYCLODEXTRINS; CALORIMETRY; ENDOCYTOSIS; HELA CELLS; HUMANS; LIPID BILAYERS; LIPOSOMES; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, CONFOCAL; TRANSFERRIN; VPR GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 80052079059     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2011.05.033     Document Type: Article

References (75)

1. J.L. Andersen, and V. Planelles The role of Vpr in HIV-1 pathogenesis Curr. HIV Res. 3 2005 43 51 (Pubitemid 40081284)
2. E. Le Rouzic, and S. Benichou The Vpr protein from HIV-1: distinct roles along the viral life cycle Retrovirology 2 2005 11
3. V. Planelles, and S. Benichou Vpr and its interactions with cellular proteins Curr. Top. Microbiol. Immunol. 339 2009 177 200
4. F. Bachand, X.J. Yao, M. Hrimech, N. Rougeau, and E.A. Cohen Incorporation of Vpr into human immunodeficiency virus type 1 requires a direct interaction with the p6 domain of the p55 gag precursor J. Biol. Chem. 274 1999 9083 9091 (Pubitemid 29164715)
5. Y.L. Lu, R.P. Bennett, J.W. Wills, R. Gorelick, and L. Ratner A leucine triplet repeat sequence (LXX)4 in p6gag is important for Vpr incorporation into human immunodeficiency virus type 1 particles J. Virol. 69 1995 6873 6879
6. W. Paxton, R.I. Connor, and N.R. Landau Incorporation of Vpr into human immunodeficiency virus type 1 virions: requirement for the p6 region of gag and mutational analysis J. Virol. 67 1993 7229 7237 (Pubitemid 23343849)
7. E. Le Rouzic, A. Mousnier, C. Rustum, F. Stutz, E. Hallberg, C. Dargemont, and S. Benichou Docking of HIV-1 Vpr to the nuclear envelope is mediated by the interaction with the nucleoporin hCG1 J. Biol. Chem. 277 2002 45091 45098 (Pubitemid 36159110)
8. R.A. Fouchier, B.E. Meyer, J.H. Simon, U. Fischer, A.V. Albright, F. Gonzalez-Scarano, and M.H. Malim Interaction of the human immunodeficiency virus type 1 Vpr protein with the nuclear pore complex J. Virol. 72 1998 6004 6013 (Pubitemid 28283389)
9. M.G. Waldhuber, M. Bateson, J. Tan, A.L. Greenway, and D.A. McPhee Studies with GFP-Vpr fusion proteins: induction of apoptosis but ablation of cell-cycle arrest despite nuclear membrane or nuclear localization Virology 313 2003 91 104 (Pubitemid 37020968)
10. T. Suzuki, N. Yamamoto, M. Nonaka, Y. Hashimoto, G. Matsuda, S.N. Takeshima, M. Matsuyama, T. Igarashi, T. Miura, R. Tanaka, S. Kato, and Y. Aida Inhibition of human immunodeficiency virus type 1 (HIV-1) nuclear import via Vpr-Importin alpha interactions as a novel HIV-1 therapy Biochem. Biophys. Res. Commun. 380 2009 838 843
11. S. Bourbigot, H. Beltz, J. Denis, N. Morellet, B.P. Roques, Y. Mely, and S. Bouaziz The C-terminal domain of the HIV-1 regulatory protein Vpr adopts an antiparallel dimeric structure in solution via its leucine-zipper-like domain Biochem. J. 387 2005 333 341 (Pubitemid 40571219)
12. P. Henklein, K. Bruns, M.P. Sherman, U. Tessmer, K. Licha, J. Kopp, C.M. de Noronha, W.C. Greene, V. Wray, and U. Schubert Functional and structural characterization of synthetic HIV-1 Vpr that transduces cells, localizes to the nucleus, and induces G2 cell cycle arrest J. Biol. Chem. 275 2000 32016 32026
13. W. Schuler, K. Wecker, H. de Rocquigny, Y. Baudat, J. Sire, and B.P. Roques NMR structure of the (52-96) C-terminal domain of the HIV-1 regulatory protein Vpr: molecular insights into its biological functions J. Mol. Biol. 285 1999 2105 2117 (Pubitemid 29078174)
14. K. Wecker, and B.P. Roques NMR structure of the (1-51) N-terminal domain of the HIV-1 regulatory protein Vpr Eur. J. Biochem. 266 1999 359 369
15. N. Morellet, S. Bouaziz, P. Petitjean, and B.P. Roques NMR structure of the HIV-1 regulatory protein VPR J. Mol. Biol. 327 2003 215 227 (Pubitemid 36293314)
16. N. Morellet, B.P. Roques, and S. Bouaziz Structure-function relationship of Vpr: biological implications Curr. HIV Res. 7 2009 184 210
17. G. Jacquot, E. le Rouzic, A. David, J. Mazzolini, J. Bouchet, S. Bouaziz, F. Niedergang, G. Pancino, and S. Benichou Localization of HIV-1 Vpr to the nuclear envelope: Impact on Vpr functions and virus replication in macrophages Retrovirology 4 2007 84
18. D.L. Bolton, and M.J. Lenardo Vpr cytopathicity independent of G2/M cell cycle arrest in human immunodeficiency virus type 1-infected CD4 + T cells J. Virol. 81 2007 8878 8890 (Pubitemid 47311433)
19. J.V. Fritz, P. Didier, J.P. Clamme, E. Schaub, D. Muriaux, C. Cabanne, N. Morellet, S. Bouaziz, J.L. Darlix, Y. Mely, and H. de Rocquigny Direct Vpr-Vpr interaction in cells monitored by two photon fluorescence correlation spectroscopy and fluorescence lifetime imaging Retrovirology 5 2008 87
20. J.V. Fritz, D. Dujardin, J. Godet, P. Didier, J. De Mey, J.L. Darlix, Y. Mely, and H. de Rocquigny HIV-1 Vpr oligomerization but not that of Gag directs the interaction between Vpr and Gag J. Virol. 84 2010 1585 1596
21. J.V. Fritz, L. Briant, Y. Mely, S. Bouaziz, and H. de Rocquigny HIV-1 Viral Protein R: from structure to function Future Virol. 5 2010 607 625
22. C. Arunagiri, I. Macreadie, D. Hewish, and A. Azad A C-terminal domain of HIV-1 accessory protein Vpr is involved in penetration, mitochondrial dysfunction and apoptosis of human CD4+ lymphocytes Apoptosis 2 1997 69 76 (Pubitemid 127508895)
23. E.N. Sabbah, and B.P. Roques Critical implication of the (70-96) domain of human immunodeficiency virus type 1 Vpr protein in apoptosis of primary rat cortical and striatal neurons J. Neurovirol. 11 2005 489 502 (Pubitemid 43123768)
24. A.N. Godet, J. Guergnon, A. Croset, X. Cayla, P.B. Falanga, J.H. Colle, and A. Garcia PP2A1 binding, cell transducing and apoptotic properties of Vpr(77-92): a new functional domain of HIV-1 Vpr proteins PLoS One 5 2010 e13760
25. M.P. Sherman, U. Schubert, S.A. Williams, C.M. de Noronha, J.F. Kreisberg, P. Henklein, and W.C. Greene HIV-1 Vpr displays natural protein-transducing properties: implications for viral pathogenesis Virology 302 2002 95 105 (Pubitemid 35356858)
26. K. Siddiqui, L. Del Valle, N. Morellet, J. Cui, M. Ghafouri, R. Mukerjee, K. Urbanska, S. Fan, C.B. Pattillo, S.L. Deshmane, M.F. Kiani, R. Ansari, K. Khalili, B.P. Roques, K. Reiss, S. Bouaziz, S. Amini, A. Srinivasan, and B.E. Sawaya Molecular mimicry in inducing DNA damage between HIV-1 Vpr and the anticancer agent, cisplatin Oncogene 27 2008 32 43
27. K. Muthumani, V.M. Lambert, M. Shanmugam, K.P. Thieu, A.Y. Choo, J.C. Chung, A. Satishchandran, J.J. Kim, D.B. Weiner, and K.E. Ugen Anti-tumor activity mediated by protein and peptide transduction of HIV viral protein R (Vpr) Cancer Biol. Therapy 8 2009 180 187
28. M. Cadene, C. Boudier, G.D. de Marcillac, and J.G. Bieth Influence of low molecular mass heparin on the kinetics of neutrophil elastase inhibition by mucus proteinase inhibitor J. Biol. Chem. 270 1995 13204 13209
29. H. de Rocquigny, A. Caneparo, T. Delaunay, J. Bischerour, J.F. Mouscadet, and B.P. Roques Interactions of the C-terminus of viral protein R with nucleic acids are modulated by its N-terminus Eur. J. Biochem. 267 2000 3654 3660 (Pubitemid 30423027)
30. R. Zidovetzki, and I. Levitan Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies Biochim. Biophys. Acta 1768 2007 1311 1324 (Pubitemid 46782714)
31. F. Gabor, U. Klausegger, and M. Wirth The interaction between wheat germ agglutinin and other plant lectins with prostate cancer cells Du-145 Int. J. Pharm. 221 2001 35 47 (Pubitemid 32524033)
32. J. Azoulay, J.P. Clamme, J.L. Darlix, B.P. Roques, and Y. Mely Destabilization of the HIV-1 complementary sequence of TAR by the nucleocapsid protein through activation of conformational fluctuations J. Mol. Biol. 326 2003 691 700 (Pubitemid 36279312)
33. J.P. Clamme, J. Azoulay, and Y. Mely Monitoring of the formation and dissociation of polyethylenimine/DNA complexes by two photon fluorescence correlation spectroscopy Biophys. J. 84 2003 1960 1968 (Pubitemid 36322958)
34. T.D. Madden, M.B. Bally, M.J. Hope, P.R. Cullis, H.P. Schieren, and A.S. Janoff Protection of large unilamellar vesicles by trehalose during dehydration: retention of vesicle contents Biochim. Biophys. Acta 817 1985 67 74 (Pubitemid 15011680)
35. S. Bernacchi, and Y. Mely Exciton interaction in molecular beacons: a sensitive sensor for short range modifications of the nucleic acid structure Nucleic Acids Res. 29 2001 E62 62
36. M. Kasha Energy transfer, charge transfer, and proton transfer in molecular composite systems Basic Life Sci. 58 1991 231 251 (discussion 251-235)
37. B.Z. Packard, D.D. Toptygin, A. Komoriya, and L. Brand Profluorescent protease substrates: intramolecular dimers described by the exciton model Proc. Natl. Acad. Sci. U.S.A. 93 1996 11640 11645 (Pubitemid 26347175)
38. J.P. Richard, K. Melikov, E. Vives, C. Ramos, B. Verbeure, M.J. Gait, L.V. Chernomordik, and B. Lebleu Cell-penetrating peptides. A reevaluation of the mechanism of cellular uptake J. Biol. Chem. 278 2003 585 590 (Pubitemid 36043612)
39. F. Duchardt, M. Fotin-Mleczek, H. Schwarz, R. Fischer, and R. Brock A comprehensive model for the cellular uptake of cationic cell-penetrating peptides Traffic (Copenhagen, Denmark) 8 2007 848 866 (Pubitemid 46971632)
40. L.N. Patel, J.L. Zaro, and W.C. Shen Cell penetrating peptides: intracellular pathways and pharmaceutical perspectives Pharm. Res. 24 2007 1977 1992 (Pubitemid 47493563)
41. M. Rusnati, D. Coltrini, P. Oreste, G. Zoppetti, A. Albini, D. Noonan, F. d'Adda di Fagagna, M. Giacca, and M. Presta Interaction of HIV-1 Tat protein with heparin. Role of the backbone structure, sulfation, and size J. Biol. Chem. 272 1997 11313 11320 (Pubitemid 27184133)
42. S.L. Schmid Clathrin-coated vesicle formation and protein sorting: an integrated process Annu. Rev. Biochem. 66 1997 511 548 (Pubitemid 27274666)
43. R.G. Anderson The caveolae membrane system Annu. Rev. Biochem. 67 1998 199 225 (Pubitemid 28411129)
44. A. Fittipaldi, A. Ferrari, M. Zoppe, C. Arcangeli, V. Pellegrini, F. Beltram, and M. Giacca Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 Tat fusion proteins J. Biol. Chem. 278 2003 34141 34149 (Pubitemid 37553255)
45. E. Coeytaux, D. Coulaud, E. Le Cam, O. Danos, and A. Kichler The cationic amphipathic alpha-helix of HIV-1 viral protein R (Vpr) binds to nucleic acids, permeabilizes membranes, and efficiently transfects cells J. Biol. Chem. 278 2003 18110 18116 (Pubitemid 36799424)
46. J.A. Swanson, and C. Watts Macropinocytosis Trends Cell Biol. 5 1995 424 428
47. N.Q. Liu, A.S. Lossinsky, W. Popik, X. Li, C. Gujuluva, B. Kriederman, J. Roberts, T. Pushkarsky, M. Bukrinsky, M. Witte, M. Weinand, and M. Fiala Human immunodeficiency virus type 1 enters brain microvascular endothelia by macropinocytosis dependent on lipid rafts and the mitogen-activated protein kinase signaling pathway J. Virol. 76 2002 6689 6700 (Pubitemid 34633535)
48. N. Schmidt, A. Mishra, G.H. Lai, and G.C. Wong Arginine-rich cell-penetrating peptides FEBS Lett. 584 2010 1806 1813
49. Z.V. Leonenko, E. Finot, H. Ma, T.E. Dahms, and D.T. Cramb Investigation of temperature-induced phase transitions in DOPC and DPPC phospholipid bilayers using temperature-controlled scanning force microscopy Biophys. J. 86 2004 3783 3793 (Pubitemid 38780255)
50. I. Vergne, P. Constant, and G. Laneelle Phagosomal pH determination by dual fluorescence flow cytometry Anal. Biochem. 255 1998 127 132 (Pubitemid 28047628)
51. A. Dinter, and E.G. Berger Golgi-disturbing agents Histochem. Cell Biol. 109 1998 571 590 (Pubitemid 28289231)
52. S. Aubry, B. Aussedat, D. Delaroche, C.Y. Jiao, G. Bolbach, S. Lavielle, G. Chassaing, S. Sagan, and F. Burlina MALDI-TOF mass spectrometry: a powerful tool to study the internalization of cell-penetrating peptides Biochim. Biophys. Acta 2009
53. G. Krishnamoorthy, G. Duportail, and Y. Mely Structure and dynamics of condensed DNA probed by 1,1′-(4,4,8,8-tetramethyl-4,8- diazaundecamethylene)bis[4-[[3- methylbenz-1,3-oxazol-2-yl]methylidine]-1,4- dihydroquinolinium] tetraiodide fluorescence Biochemistry 41 2002 15277 15287 (Pubitemid 36008137)
54. J.R. Lakowicz Fluorescence spectroscopic investigations of the dynamic properties of proteins, membranes and nucleic acids J. Biochem. Biophys. Methods 2 1980 91 119 (Pubitemid 10142969)
55. R.Y. Zhao, D. Liang, G. Li, C.W. Larrimore, and B.L. Mirkin Anti-cancer effect of HIV-1 viral protein R on doxorubicin resistant neuroblastoma PLoS One 5 2010 e11466
56. T. Taguchi, M. Shimura, Y. Osawa, Y. Suzuki, I. Mizoguchi, K. Niino, F. Takaku, and Y. Ishizaka Nuclear trafficking of macromolecules by an oligopeptide derived from Vpr of human immunodeficiency virus type-1 Biochem. Biophys. Res. Commun. 320 2004 18 26 (Pubitemid 38781779)
57. V. Tiriveedhi, and P. Butko A fluorescence spectroscopy study on the interactions of the TAT-PTD peptide with model lipid membranes Biochemistry 46 2007 3888 3895 (Pubitemid 46493489)
58. C.M. de Noronha, M.P. Sherman, H.W. Lin, M.V. Cavrois, R.D. Moir, R.D. Goldman, and W.C. Greene Dynamic disruptions in nuclear envelope architecture and integrity induced by HIV-1 Vpr Science 294 2001 1105 1108 (Pubitemid 33041866)
59. S.C. Piller, P. Jans, P.W. Gage, and D.A. Jans Extracellular HIV-1 virus protein R causes a large inward current and cell death in cultured hippocampal neurons: implications for AIDS pathology Proc. Natl. Acad. Sci. U.S.A. 95 1998 4595 4600 (Pubitemid 28207958)
60. A. Ziegler Thermodynamic studies and binding mechanisms of cell-penetrating peptides with lipids and glycosaminoglycans Advan. Drug Delivery Rev. 60 2008 580 597 (Pubitemid 351215575)
61. S.C. Piller, G.D. Ewart, A. Premkumar, G.B. Cox, and P.W. Gage Vpr protein of human immunodeficiency virus type 1 forms cation-selective channels in planar lipid bilayers Proc. Natl. Acad. Sci. U.S.A. 93 1996 111 115 (Pubitemid 26038112)
62. S. Sandgren, F. Cheng, and M. Belting Nuclear targeting of macromolecular polyanions by an HIV-Tat derived peptide. Role for cell-surface proteoglycans J. Biol. Chem. 277 2002 38877 38883 (Pubitemid 35157770)
63. E. Goncalves, E. Kitas, and J. Seelig Binding of oligoarginine to membrane lipids and heparan sulfate: structural and thermodynamic characterization of a cell-penetrating peptide Biochemistry 44 2005 2692 2702 (Pubitemid 40279574)
64. A. Ziegler, and J. Seelig Interaction of the protein transduction domain of HIV-1 TAT with heparan sulfate: binding mechanism and thermodynamic parameters Biophys. J. 86 2004 254 263 (Pubitemid 38067453)
65. A. Ziegler, X.L. Blatter, A. Seelig, and J. Seelig Protein transduction domains of HIV-1 and SIV TAT interact with charged lipid vesicles. Binding mechanism and thermodynamic analysis Biochemistry 42 2003 9185 9194 (Pubitemid 36935428)
66. R. Fischer, K. Kohler, M. Fotin-Mleczek, and R. Brock A stepwise dissection of the intracellular fate of cationic cell-penetrating peptides J. Biol. Chem. 279 2004 12625 12635 (Pubitemid 38445834)
67. A. Vendeville, F. Rayne, A. Bonhoure, N. Bettache, P. Montcourrier, and B. Beaumelle HIV-1 Tat enters T cells using coated pits before translocating from acidified endosomes and eliciting biological responses Mol. Biol. Cell 15 2004 2347 2360 (Pubitemid 38580651)
68. T.B. Potocky, A.K. Menon, and S.H. Gellman Cytoplasmic and nuclear delivery of a TAT-derived peptide and a beta-peptide after endocytic uptake into HeLa cells J. Biol. Chem. 278 2003 50188 50194 (Pubitemid 37548858)
69. R. Trehin, H.M. Nielsen, H.G. Jahnke, U. Krauss, A.G. Beck-Sickinger, and H.P. Merkle Metabolic cleavage of cell-penetrating peptides in contact with epithelial models: human calcitonin (hCT)-derived peptides, Tat(47-57) and penetratin(43-58) Biochem. J. 382 2004 945 956 (Pubitemid 39312909)
70. H. Binder, and G. Lindblom Charge-dependent translocation of the Trojan peptide penetratin across lipid membranes Biophys. J. 85 2003 982 995 (Pubitemid 36909662)
71. D. Persson, P.E. Thoren, M. Herner, P. Lincoln, and B. Norden Application of a novel analysis to measure the binding of the membrane-translocating peptide penetratin to negatively charged liposomes Biochemistry 42 2003 421 429 (Pubitemid 36105760)
72. A. Lamaziere, C. Wolf, O. Lambert, G. Chassaing, G. Trugnan, and J. Ayala-Sanmartin The homeodomain derived peptide Penetratin induces curvature of fluid membrane domains PLoS One 3 2008 e1938
73. D. Terrone, S.L. Sang, L. Roudaia, and J.R. Silvius Penetratin and related cell-penetrating cationic peptides can translocate across lipid bilayers in the presence of a transbilayer potential Biochemistry 42 2003 13787 13799 (Pubitemid 37466604)
74. H.D. Herce, and A.E. Garcia Molecular dynamics simulations suggest a mechanism for translocation of the HIV-1 TAT peptide across lipid membranes Proc. Natl. Acad. Sci. U.S.A. 104 2007 20805 20810
75. R. Rothe, L. Liguori, A. Villegas-Mendez, B. Marques, D. Grunwald, E. Drouet, and J.L. Lenormand Characterization of the cell-penetrating properties of the Epstein-Barr virus ZEBRA trans-activator J. Biol. Chem. 285 2010 20224 20233