Advertisement

Monitoring HIV-1 Protein Oligomerization by FLIM FRET Microscopy

  • Ludovic Richert
  • Pascal Didier
  • Hugues de Rocquigny
  • Yves MélyEmail author
Chapter
Part of the Springer Series in Chemical Physics book series (CHEMICAL, volume 111)

Abstract

The majority of the human immunodeficiency virus type 1 (HIV-1) proteins are able to self assemble into oligomers. Since these oligomers generally exhibit functions that differ from those of their monomeric counterpart, the regulation of the monomer-oligomer equilibria plays a central role in the viral cycle. To characterize the oligomerization of these proteins in live cells, the combination of fluorescence lifetime imaging microscopy (FLIM) with Förster resonance energy transfer (FRET) has proven to be very powerful. In this review, we illustrate the application of FRET-FLIM on the characterization of the oligomerization of the Vpr, Vif and Pr55Gag proteins of HIV-1 in fusion with eGFP and mCherry. For Vpr and Pr55Gag proteins, very high levels of FRET leading to strong decreases in eGFP fluorescence lifetime are obtained, as a consequence of the rather small size of the viral proteins, the strong packing of the protomers and the presence of multiple acceptors for one donor. Analyzing the time-resolved decays by a two-component analysis further provides the possibility to discriminate monomers from oligomers and to monitor the spatiotemporal evolution of both populations in the cells. Though FRET-FLIM unambiguously reveals the oligomerization of a given protein, it hardly discloses the oligomer stoichiometry (number of protomers per oligomers). This parameter can be obtained by fluorescence correlation spectroscopy, which allows further interpreting the FRET-FLIM data. FRET-FLIM is also highly useful to identify the determinants of the oligomerization process and to investigate its regulation by other HIV-1 proteins and host proteins.

Keywords

Fluorescence Lifetime Fluorescence Correlation Spectroscopy Fluorescence Lifetime Imaging Microscopy Fluorescence Correlation Spectroscopy Measurement Fast Decay Component 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Salah Edin El Meshri for his technical help. This work was supported by the European Project THINPAD “Targeting the HIV-1 Nucleocapsid Protein to fight Antiretroviral Drug Resistance” (FP7—grant agreement 601969), Agence National Recherche sur le SIDA (ANRS) (2012-14. CSS2), SIDACTION (AI22-1-01963), Centre National Recherche Scientifique (CNRS), Université de Strasbourg and Institut National sur la Santé Et la Recherche Médicale (INSERM).

References

  1. 1.
    C.S. Adamson, E.O. Freed, Human immunodeficiency virus type 1 assembly, release, and maturation, Advances in Pharmacology, vol 55 (Elsevier, San Diego, Calif, 2007), pp. 347–387Google Scholar
  2. 2.
    K. Amari, E. Boutant, C. Hofmann, C. Schmitt-Keichinger, L. Fernandez-Calvino, P. Didier, A. Lerich, J. Mutterer, C.L. Thomas, M. Heinlein, Y. Mely, A.J. Maule, C. Ritzenthaler, A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLoS Pathog. 6, e1001119 (2010)CrossRefGoogle Scholar
  3. 3.
    E. Asante-Appiah, A.M. Skalka, HIV-1 integrase: structural organization, conformational changes, and catalysis. Adv. Virus Res. 52, 351–369 (1999)CrossRefGoogle Scholar
  4. 4.
    J.R. Auclair, K.M. Green, S. Shandilya, J.E. Evans, M. Somasundaran, C.A. Schiffer, Mass spectrometry analysis of HIV-1 Vif reveals an increase in ordered structure upon oligomerization in regions necessary for viral infectivity. Proteins 69, 270–284 (2007)CrossRefGoogle Scholar
  5. 5.
    J. Azoulay, J.P. Clamme, J.L. Darlix, B.P. Roques, Y. Mely, Destabilization of the HIV-1 complementary sequence of TAR by the nucleocapsid protein through activation of conformational fluctuations. J. Mol. Biol. 326, 691–700 (2003)CrossRefGoogle Scholar
  6. 6.
    F. Bachand, X.J. Yao, M. Hrimech, N. Rougeau, 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, 9083–9091 (1999)CrossRefGoogle Scholar
  7. 7.
    M. Balasubramaniam, E.O. Freed, New insights into HIV assembly and trafficking. Physiology (Bethesda) 26, 236–251 (2011)CrossRefGoogle Scholar
  8. 8.
    D.S. Banks, C. Fradin, Anomalous diffusion of proteins due to molecular crowding. Biophys. J. 89, 2960–2971 (2005)CrossRefGoogle Scholar
  9. 9.
    J. Batisse, S.X. Guerrero, S. Bernacchi, L. Richert, J. Godet, V. Goldschmidt, Y. Mely, R. Marquet, H. de Rocquigny, J.C. Paillart, APOBEC3G impairs the multimerization of the HIV-1 Vif protein in living cells. J. Virol. 87, 6492–6506 (2013)CrossRefGoogle Scholar
  10. 10.
    W. Becker, A. Bergmann, M.A. Hink, K. König, K. Benndorf, C. Biskup, Fluorescence lifetime imaging by time-correlated single photon counting. Micr. Res. Techn. 63, 58–66 (2004)CrossRefGoogle Scholar
  11. 11.
    W. Becker, K. Benndorf, A. Bergmann, C. Biskup, K. König, U. Tirlapur, T. Zimmer, FRET measurements by TCSPC laser scanning microscopy. Proc. SPIE 4431, 94–98 (2001)CrossRefGoogle Scholar
  12. 12.
    W. Becker, Advanced time-correlated single-photon counting techniques (Springer, Heidelberg, New York, 2005)CrossRefGoogle Scholar
  13. 13.
    W. Becker, The bh TCSPC Handbook, 5th edn. (2012). Printed copies available from Becker&Hickl GmbH, Electronic version available from www.becker-hickl.com
  14. 14.
    W. Becker, Fluorescence lifetime imaging—techniques and applications. J. Microsc. 247, 119–136 (2012)CrossRefGoogle Scholar
  15. 15.
    N.M. Bell, A.M. Lever, HIV Gag polyprotein: processing and early viral particle assembly. Trends Microbiol. 21, 136–144 (2013)CrossRefGoogle Scholar
  16. 16.
    C. Biskup, L. Kelbauskas, T. Zimmer, K. Benndorf, A. Bergmann, W. Becker, J.P. Ruppersberg, C. Stockklausner, N. Klöcker, Interaction of PSD-95 with potassium channels visualized by fluorescence lifetime-based resonance energy transfer imaging. J. Biomed. Opt. 9, 735–759 (2004)CrossRefGoogle Scholar
  17. 17.
    D.L. Bolton, 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, 8878–8890 (2007)CrossRefGoogle Scholar
  18. 18.
    H.P. Bogerd, B.P. Doehle, H.L. Wiegand, B.R. Cullen, A single amino acid difference in the host APOBEC3G protein controls the primate species specificity of HIV type 1 virion infectivity factor. Proc. Natl. Acad. Sci. U.S.A. 101, 3770–3774 (2004)CrossRefGoogle Scholar
  19. 19.
    K. Brandner, A. Sambade, E. Boutant, P. Didier, Y. Mely, C. Ritzenthaler, M. Heinlein, Tobacco mosaic virus movement protein interacts with green fluorescent protein-tagged microtubule end-binding protein 1. Plant Physiol. 147, 611–623 (2008)CrossRefGoogle Scholar
  20. 20.
    K. Bruns, T. Fossen, V. Wray, P. Henklein, U. Tessmer, U. Schubert, Structural characterization of the HIV-1 Vpr N terminus: evidence of cis/trans-proline isomerism. J. Biol. Chem. 278, 43188–43201 (2003)CrossRefGoogle Scholar
  21. 21.
    C.A. Bucherl, A. Bader, A.H. Westphal, S.P. Laptenok, J.W. Borst, FRET-FLIM applications in plant systems. Protoplasma 251, 383–394 (2014)CrossRefGoogle Scholar
  22. 22.
    N.S. Caron, L.N. Munsie, J.W. Keillor, R. Truant, Using FLIM-FRET to measure conformational changes of transglutaminase type 2 in live cells, PloS one 7, e44159 (2012)Google Scholar
  23. 23.
    Chen, A. Periasamy, Characterization of two-photon excitation fluorescence lifetime imaging micros-copy for protein localization, Microsc. Res. Tech. 63, 72–80 (2004)Google Scholar
  24. 24.
    Y. Chen, J.D. Muller, Q. Ruan, E. Gratton, Molecular brightness characterization of EGFP in vivo by fluorescence fluctuation spectroscopy, Biophys. J. 82, 133–144 (2002)Google Scholar
  25. 25.
    J.P. Clamme, J. Azoulay, Y. Mely, Monitoring of the formation and dissociation of polyethylenimine/DNA complexes by two photon fluorescence correlation spectroscopy. Biophys. J. 84, 1960–1968 (2003)CrossRefGoogle Scholar
  26. 26.
    B. Corry, D. Jayatilaka, P. Rigby, A flexible approach to the calculation of resonance energy transfer efficiency between multiple donors and acceptors in complex geometries. Biophys. J. 89, 3822–3836 (2005)CrossRefGoogle Scholar
  27. 27.
    S. Dahmane, E. Rubinstein, P.E. Milhiet, Viruses and tetraspanins: lessons from single molecule approaches. Viruses 6, 1992–2011 (2014)CrossRefGoogle Scholar
  28. 28.
    S.A. Datta, L.G. Temeselew, R.M. Crist, F. Soheilian, A. Kamata, J. Mirro, D. Harvin, K. Nagashima, R.E. Cachau, A. Rein, On the role of the SP1 domain in HIV-1 particle assembly: a molecular switch? J. Virol. 85, 4111–4121 (2011)CrossRefGoogle Scholar
  29. 29.
    C. Depienne, P. Roques, C. Creminon, L. Fritsch, R. Casseron, D. Dormont, C. Dargemont, S. Benichou, Cellular distribution and karyophilic properties of matrix, integrase, and Vpr proteins from the human and simian immunodeficiency viruses. Exp. Cell Res. 260, 387–395 (2000)CrossRefGoogle Scholar
  30. 30.
    A. Derdowski, L. Ding, P. Spearman, A novel fluorescence resonance energy transfer assay demonstrates that the human immunodeficiency virus type 1 Pr55Gag I domain mediates Gag-Gag interactions. J. Virol. 78, 1230–1242 (2004)CrossRefGoogle Scholar
  31. 31.
    B.A. Desimmie, K.A. Delviks-Frankenberrry, R.C. Burdick, D. Qi, T. Izumi, V.K. Pathak, Multiple APOBEC3 restriction factors for HIV-1 and one Vif to rule them all. J. Mol. Biol. 426, 1220–1245 (2014)CrossRefGoogle Scholar
  32. 32.
    M.A. Digman, E. Gratton, Fluorescence correlation spectroscopy and fluorescence cross-correlation spectroscopy. Wiley Interdisc. Rev. Syst. Biol. Med. 1, 273–282 (2009)CrossRefGoogle Scholar
  33. 33.
    B.M. Dunn, M.M. Goodenow, A. Gustchina, A. Wlodawer, Retroviral proteases, Genome Biol. 3, REVIEWS3006 (2002)Google Scholar
  34. 34.
    S.E. El Meshri, D. Dujardin, J. Godet, L. Richert, C. Boudier, J.L. Darlix, P. Didier, Y. Mely, H. de Rocquigny, Role of the nucleocapsid domain in HIV-1 Gag oligomerization and trafficking to the plasma membrane: A fluorescence lifetime imaging microscopy investigation. J. Mol. Biol. (2015, in press) Google Scholar
  35. 35.
    S. Engel, S. Scolari, B. Thaa, N. Krebs, T. Korte, A. Herrmann, M. Veit, FLIM-FRET and FRAP reveal association of influenza virus haemagglutinin with membrane rafts. Biochem. J. 425, 567–573 (2010)CrossRefGoogle Scholar
  36. 36.
    A.W. Fjorback, P. Pla, H.K. Muller, O. Wiborg, F. Saudou, J.R. Nyengaard, Serotonin transporter oligomerization documented in RN46A cells and neurons by sensitized acceptor emission FRET and fluorescence lifetime imaging microscopy. Biochem. Biophys. Res. Commun. 380, 724–728 (2009)CrossRefGoogle Scholar
  37. 37.
    Th. Förster, Zwischenmolekulare Energiewanderung und Fluoreszenz, Ann. Phys. (Serie 6) 2, 55–75 (1948)Google Scholar
  38. 38.
    Th. Förster, Energy migration and fluorescence. Translated by Klaus Suhling. J. Biomed. Opt. 17, 011002-1–10 (2012)Google Scholar
  39. 39.
    K.H. Fogarty, Y. Chen, I.F. Grigsby, P.J. Macdonald, E.M. Smith, J.L. Johnson, J.M. Rawson, L.M. Mansky, J.D. Mueller, Characterization of cytoplasmic Gag-gag interactions by dual-color z-scan fluorescence fluctuation spectroscopy. Biophys. J. 100, 1587–1595 (2011)CrossRefGoogle Scholar
  40. 40.
    J.V. Fritz, P. Didier, J.P. Clamme, E. Schaub, D. Muriaux, C. Cabanne, N. Morellet, S. Bouaziz, J.L. Darlix, Y. Mely, H. de Rocquigny, Direct Vpr-Vpr interaction in cells monitored by two photon fluorescence correlation spectroscopy and fluorescence lifetime imaging. Retrovirology 5, 87 (2008)CrossRefGoogle Scholar
  41. 41.
    J.V. Fritz, L. Briant, Y. Mely, S. Bouaziz, H. de Rocquigny, HIV-1 Viral Protein R: from structure to function. Future Virol. 5, 607–625 (2010)CrossRefGoogle Scholar
  42. 42.
    J.V. Fritz, D. Dujardin, J. Godet, P. Didier, J. De Mey, J.L. Darlix, Y. Mely, H. de Rocquigny, HIV-1 Vpr oligomerization but not that of Gag directs the interaction between Vpr and Gag. J. Virol. 84, 1585–1596 (2010)CrossRefGoogle Scholar
  43. 43.
    T.W. Gadella Jr, T.M. Jovin, Oligomerization of epidermal growth factor receptors on A431 cells studied by time-resolved fluorescence imaging microscopy. A stereochemical model for tyrosine kinase receptor activation. J. Cell Biol. 129, 1543–1558 (1995)CrossRefGoogle Scholar
  44. 44.
    T.R. Gamble, S. Yoo, F.F. Vajdos, U.K. von Schwedler, D.K. Worthylake, H. Wang, J.P. McCutcheon, W.I. Sundquist, C.P. Hill, Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein. Science 278, 849–853 (1997)CrossRefGoogle Scholar
  45. 45.
    B.K. Ganser-Pornillos, M. Yeager, W.I. Sundquist, The structural biology of HIV assembly. Curr. Opin. Struct. Biol. 18, 203–217 (2008)CrossRefGoogle Scholar
  46. 46.
    J. He, S. Choe, R. Walker, P. Di Marzio, D.O. Morgan, N.R. Landau, Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity. J. Virol. 69, 6705–6711 (1995)Google Scholar
  47. 47.
    N.K. Heinzinger, M.I. Bukinsky, S.A. Haggerty, A.M. Ragland, V. Kewalramani, M.A. Lee, H.E. Gendelman, L. Ratner, M. Stevenson, M. Emerman, The Vpr protein of human immunodeficiency virus type 1 influences nuclear localization of viral nucleic acids in nondividing host cells. Proc. Natl. Acad. Sci. U.S.A. 91, 7311–7315 (1994)CrossRefGoogle Scholar
  48. 48.
    P. Henklein, K. Bruns, M.P. Sherman, U. Tessmer, K. Licha, J. Kopp, C.M. de Noronha, W.C. Greene, V. Wray, 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, 32016–32026 (2000)CrossRefGoogle Scholar
  49. 49.
    B. Herman, G. Gordon, N. Mahajan, V. Centonze, in Methods of Cellular Imaging, ed. by A. Periasamy. Measurement of fluorescence resonance energy transfer in the optical microscpe (Oxford University Press, New York, 2001)Google Scholar
  50. 50.
    L. Hermida-Matsumoto, M.D. Resh, Localization of human immunodeficiency virus type 1 Gag and Env at the plasma membrane by confocal imaging. J. Virol. 74, 8670–8679 (2000)CrossRefGoogle Scholar
  51. 51.
    C.P. Hill, D. Worthylake, D.P. Bancroft, A.M. Christensen, W.I. Sundquist, Crystal structures of the trimeric human immunodeficiency virus type 1 matrix protein: implications for membrane association and assembly. Proc. Natl. Acad. Sci. U.S.A. 93, 3099–3104 (1996)CrossRefGoogle Scholar
  52. 52.
    B. Hoffmann, T. Zimmer, N. Klöcker, L. Kelbauskas, K. König, K. Benndorf, C. Biskup, Prolonged irradiation of enhanced cyan fluorescent protein or Cerulean can invalidate Förster resonance energy transfer measurements. J. Biomed. Opt. 13(3), 031250-1 to -9 (2008)Google Scholar
  53. 53.
    I.B. Hogue, A. Hoppe, A. Ono, Quantitative fluorescence resonance energy transfer microscopy analysis of the human immunodeficiency virus type 1 Gag-Gag interaction: relative contributions of the CA and NC domains and membrane binding. J. Virol. 83, 7322–7336 (2009)CrossRefGoogle Scholar
  54. 54.
    W. Hubner, P. Chen, A. Del Portillo, Y. Liu, R.E. Gordon, B.K. Chen, Sequence of human immunodeficiency virus type 1 (HIV-1) Gag localization and oligomerization monitored with live confocal imaging of a replication-competent, fluorescently tagged HIV-1. J. Virol. 81, 12596–12607 (2007)CrossRefGoogle Scholar
  55. 55.
    W. Hubner, G.P. McNerney, P. Chen, B.M. Dale, R.E. Gordon, F.Y. Chuang, X.D. Li, D.M. Asmuth, T. Huser, B.K. Chen, Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 323, 1743–1747 (2009)CrossRefGoogle Scholar
  56. 56.
    A. Jacobo-Molina, J. Ding, R.G. Nanni, A.D. Clark, Jr., X. Lu, C. Tantillo, R.L. Williams, G. Kamer, A.L. Ferris, P. Clark et al., Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 A resolution shows bent DNA, Proc. Natl. Acad. Sci. USA 90, 6320–6324 (1993)Google Scholar
  57. 57.
    E. Jacotot, K.F. Ferri, C. El Hamel, C. Brenner, S. Druillennec, J. Hoebeke, P. Rustin, D. Metivier, C. Lenoir, M. Geuskens, H.L. Vieira, M. Loeffler, A.S. Belzacq, J.P. Briand, N. Zamzami, L. Edelman, Z.H. Xie, J.C. Reed, B.P. Roques, G. Kroemer, Control of mitochondrial membrane permeabilization by adenine nucleotide translocator interacting with HIV-1 viral protein rR and Bcl-2. J. Exp. Med. 193, 509–519 (2001)CrossRefGoogle Scholar
  58. 58.
    J.B. Jowett, V. Planelles, B. Poon, N.P. Shah, M.L. Chen, I.S. Chen, The human immunodeficiency virus type 1 vpr gene arrests infected T cells in the G2+M phase of the cell cycle. J. Virol. 69, 6304–6313 (1995)Google Scholar
  59. 59.
    L.A. Kohlstaedt, J. Wang, J.M. Friedman, P.A. Rice, T.A. Steitz, Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science 256, 1783–1790 (1992)CrossRefGoogle Scholar
  60. 60.
    E. Kondo, F. Mammano, E.A. Cohen, H.G. Gottlinger, The p6gag domain of human immunodeficiency virus type 1 is sufficient for the incorporation of Vpr into heterologous viral particles. J. Virol. 69, 2759–2764 (1995)Google Scholar
  61. 61.
    S.B. Kutluay, P.D. Bieniasz, Analysis of the initiating events in HIV-1 particle assembly and genome packaging. PLoS Pathog. 6, e1001200 (2010)CrossRefGoogle Scholar
  62. 62.
    A.J. Lam, F. St-Pierre, Y. Gong, J.D. Marshall, P.J. Cranfill, M.A. Baird, M.R. McKeown, J. Wiedenmann, M.W. Davidson, M.J. Schnitzer, R.Y. Tsien, M.Z. Lin, Improving FRET dynamic range with bright green and red fluorescent proteins. Nat. Methods 9, 1005–1012 (2012)CrossRefGoogle Scholar
  63. 63.
    D.R. Larson, M.C. Johnson, W.W. Webb, V.M. Vogt, Visualization of retrovirus budding with correlated light and electron microscopy. Proc. Natl. Acad. Sci. U.S.A. 102, 15453–15458 (2005)CrossRefGoogle Scholar
  64. 64.
    D.R. Larson, Y.M. Ma, V.M. Vogt, W.W. Webb, Direct measurement of Gag-Gag interaction during retrovirus assembly with FRET and fluorescence correlation spectroscopy. J. Cell Biol. 162, 1233–1244 (2003)CrossRefGoogle Scholar
  65. 65.
    C. Lavallee, X.J. Yao, A. Ladha, H. Gottlinger, W.A. Haseltine, E.A. Cohen, Requirement of the Pr55gag precursor for incorporation of the Vpr product into human immunodeficiency virus type 1 viral particles, J. Virol. 68, 1926–1934 (1994)Google Scholar
  66. 66.
    J. Liu, A. Bartesaghi, M.J. Borgnia, G. Sapiro, S. Subramaniam, Molecular architecture of native HIV-1 gp120 trimers. Nature 455, 109–113 (2008)CrossRefGoogle Scholar
  67. 67.
    D. McDonald, M.A. Vodicka, G. Lucero, T.M. Svitkina, G.G. Borisy, M. Emerman, T.J. Hope, Visualization of the intracellular behavior of HIV in living cells. J. Cell Biol. 159, 441–452 (2002)CrossRefGoogle Scholar
  68. 68.
    A. Merk, S. Subramaniam, HIV-1 envelope glycoprotein structure. Curr. Opin. Struct. Biol. 23, 268–276 (2013)CrossRefGoogle Scholar
  69. 69.
    E.M. Merzlyak, J. Goedhart, D. Shcherbo, M.E. Bulina, A.S. Shcheglov, A.F. Fradkov, A. Gaintzeva, K.A. Lukyanov, S. Lukyanov, T.W. Gadella, D.M. Chudakov, Bright monomeric red fluorescent protein with an extended fluorescence lifetime. Nat. Methods 2007(4), 555–557 (2007)CrossRefGoogle Scholar
  70. 70.
    F. Michel, C. Crucifix, F. Granger, S. Eiler, J.F. Mouscadet, S. Korolev, J. Agapkina, R. Ziganshin, M. Gottikh, A. Nazabal, S. Emiliani, R. Benarous, D. Moras, P. Schultz, M. Ruff, Structural basis for HIV-1 DNA integration in the human genome, role of the LEDGF/P75 cofactor, EMBO J. 28, 980–991 (2009)Google Scholar
  71. 71.
    G. Mirambeau, S. Lyonnais, R.J. Gorelick, Features, processing states, and heterologous protein interactions in the modulation of the retroviral nucleocapsid protein function. RNA Biol. 7, 724–734 (2010)CrossRefGoogle Scholar
  72. 72.
    N. Morellet, S. Bouaziz, P. Petitjean, B.P. Roques, NMR structure of the HIV-1 regulatory protein VPR. J. Mol. Biol. 327, 215–227 (2003)CrossRefGoogle Scholar
  73. 73.
    N. Morellet, S. Druillennec, C. Lenoir, S. Bouaziz, B.P. Roques, Helical structure determined by NMR of the HIV-1 (345-392) Gag sequence, surrounding p2: implications for particle assembly and RNA packaging. Protein Sci. 14, 375–386 (2005)CrossRefGoogle Scholar
  74. 74.
    N. Morellet, B.P. Roques, S. Bouaziz, Structure-function relationship of Vpr: biological implications. Curr. HIV Res. 7, 184–210 (2009)CrossRefGoogle Scholar
  75. 75.
    B. Muller, J. Daecke, O.T. Fackler, M.T. Dittmar, H. Zentgraf, H.G. Krausslich, Construction and characterization of a fluorescently labeled infectious human immunodeficiency virus type 1 derivative. J. Virol. 78, 10803–10813 (2004)CrossRefGoogle Scholar
  76. 76.
    A. Niehl, K. Amari, D. Gereige, K. Brandner, Y. Mely, M. Heinlein, Control of tobacco mosaic virus movement protein fate by CELL-DIVISION-CYCLE protein48. Plant Physiol. 160, 2093–2108 (2012)CrossRefGoogle Scholar
  77. 77.
    I.P. O’Carroll, F. Soheilian, A. Kamata, K. Nagashima, A. Rein, Elements in HIV-1 Gag contributing to virus particle assembly. Virus Res. 171, 341–345 (2013)CrossRefGoogle Scholar
  78. 78.
    S. Padilla-Parra, N. Auduge, H. Lalucque, J.C. Mevel, M. Coppey-Moisan, M. Tramier, Quantitative comparison of different fluorescent protein couples for fast FRET-FLIM acquisition. Biophys. J. 97, 2368–2376 (2009)CrossRefGoogle Scholar
  79. 79.
    R. Pepperkok, A. Squire, S. Geley, P.I. Bastiaens, Simultaneous detection of multiple green fluorescent proteins in live cells by fluorescence lifetime imaging microscopy. Curr. Biol. 9, 269–272 (1999)CrossRefGoogle Scholar
  80. 80.
    V. Planelles, S. Benichou, Vpr and its interactions with cellular proteins. Curr. Top. Microbiol. Immunol. 339, 177–200 (2009)Google Scholar
  81. 81.
    A. Periasamy, Methods in Cellular Imaging (Oxford University Press, Oxford New York, 2001)CrossRefGoogle Scholar
  82. 82.
    C. Perrin-Tricaud, J. Davoust, I.M. Jones, Tagging the human immunodeficiency virus gag protein with green fluorescent protein. Minimal evidence for colocalisation with actin. Virology 255, 20–25 (1999)CrossRefGoogle Scholar
  83. 83.
    O. Pornillos, B.K. Ganser-Pornillos, B.N. Kelly, Y. Hua, F.G. Whitby, C.D. Stout, W.I. Sundquist, C.P. Hill, M. Yeager, X-ray structures of the hexameric building block of the HIV capsid. Cell 137, 1282–1292 (2009)CrossRefGoogle Scholar
  84. 84.
    O. Pornillos, B.K. Ganser-Pornillos, M. Yeager, Atomic-level modelling of the HIV capsid. Nature 469, 424–427 (2011)CrossRefGoogle Scholar
  85. 85.
    A.S. Rinaldi, G. Freund, D. Desplancq, A.P. Sibler, M. Baltzinger, N. Rochel, Y. Mely, P. Didier, E. Weiss, The use of fluorescent intrabodies to detect endogenous gankyrin in living cancer cells. Exp. Cell Res. 319, 838–849 (2013)CrossRefGoogle Scholar
  86. 86.
    V. Raicu, D.R. Singh, FRET spectrometry: a new tool for the determination of protein quaternary structure in living cells. Biophys. J. 105, 1937–1945 (2013)CrossRefGoogle Scholar
  87. 87.
    J. Ries, P. Schwille, Fluorescence correlation spectroscopy, bioessays: news and reviews in molecular. Cell. Dev. Biol. 34, 361–368 (2012)Google Scholar
  88. 88.
    H. de Rocquigny, S.E. El Meshri, L. Richert, P. Didier, J.L. Darlix, Y. Mely, Role of the nucleocapsid region in HIV-1 Gag assembly as investigated by quantitative fluorescence-based microscopy, Virus. Res. 193, 78−88 (2014)Google Scholar
  89. 89.
    B. Schrofelbauer, D. Chen, N.R. Landau, A single amino acid of APOBEC3G controls its species-specific interaction with virion infectivity factor (Vif). Proc. Natl. Acad. Sci. U.S.A. 101, 3927–3932 (2004)CrossRefGoogle Scholar
  90. 90.
    W. Schuler, K. Wecker, H. de Rocquigny, Y. Baudat, J. Sire, 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, 2105–2117 (1999)CrossRefGoogle Scholar
  91. 91.
    W.I. Sundquist, H.G. Krausslich, HIV-1 assembly, budding, and maturation. Cold Spring Harb. Perspect. Med. 2, a006924 (2012)CrossRefGoogle Scholar
  92. 92.
    J.H. Simon, R.A. Fouchier, T.E. Southerling, C.B. Guerra, C.K. Grant, M.H. Malim, The Vif and Gag proteins of human immunodeficiency virus type 1 colocalize in infected human T cells. J. Virol. 71, 5259–5267 (1997)Google Scholar
  93. 93.
    P.R. Tedbury, S.D. Ablan, E.O. Freed, Global rescue of defects in HIV-1 envelope glycoprotein incorporation: implications for matrix structure. PLoS Pathog. 9, e1003739 (2013)CrossRefGoogle Scholar
  94. 94.
    B. Thaa, A. Herrmann, M. Veit, Intrinsic cytoskeleton-dependent clustering of influenza virus M2 protein with hemagglutinin assessed by FLIM-FRET. J. Virol. 84, 12445–12449 (2010)CrossRefGoogle Scholar
  95. 95.
    M. Tramier, M. Zahid, J.C. Mevel, M.J. Masse, M. Coppey-Moisan, Sensitivity of CFP/YFP and GFP/mCherry pairs to donor photobleaching on FRET determination by fluorescence lifetime imaging microscopy in living cells. Microsc. Res. Tech. 69, 933–939 (2006)CrossRefGoogle Scholar
  96. 96.
    R.Y. Tsien, The green fluorescent protein. Annu. Rev. Biochem. 67, 509–544 (1998)CrossRefGoogle Scholar
  97. 97.
    B.G. Turner, M.F. Summers, Structural biology of HIV. J. Mol. Biol. 285, 1–32 (1999)CrossRefGoogle Scholar
  98. 98.
    Y. Ueda, S. Kwok, Y. Hayashi, Application of FRET probes in the analysis of neuronal plasticity. Frontiers in neural circuits 7, 163 (2013)CrossRefGoogle Scholar
  99. 99.
    E.B. van Munster, T.W. Gadella, Fluorescence lifetime imaging microscopy (FLIM). Adv. Biochem. Eng. Biotechnol. 95, 143–175 (2005)Google Scholar
  100. 100.
    S.S. Vogel, B.W. van der Meer, P.S. Blank, Estimating the distance separating fluorescent protein FRET pairs. Methods 66, 131–138 (2014)CrossRefGoogle Scholar
  101. 101.
    U.K. von Schwedler, K.M. Stray, J.E. Garrus, W.I. Sundquist, Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J. Virol. 77, 5439–5450 (2003)CrossRefGoogle Scholar
  102. 102.
    T.C. Voss, I.A. Demarco, R.N. Day, Quantitative imaging of protein interactions in the cell nucleus. Biotechniques 38, 413–424 (2005)CrossRefGoogle Scholar
  103. 103.
    K. Wecker, N. Morellet, S. Bouaziz, B.P. Roques, NMR structure of the HIV-1 regulatory protein Vpr in H2O/trifluoroethanol. Comparison with the Vpr N-terminal (1–51) and C-terminal (52–96) domains. Eur. J. Biochem. 269, 3779–3788 (2002)CrossRefGoogle Scholar
  104. 104.
    H. Xu, E.S. Svarovskaia, R. Barr, Y. Zhang, M.A. Khan, K. Strebel, V.K. Pathak, A single amino acid substitution in human APOBEC3G antiretroviral enzyme confers resistance to HIV-1 virion infectivity factor-induced depletion. Proc. Natl. Acad. Sci. U.S.A. 101, 5652–5657 (2004)CrossRefGoogle Scholar
  105. 105.
    X.J. Yao, A.J. Mouland, R.A. Subbramanian, J. Forget, N. Rougeau, D. Bergeron, E.A. Cohen, Vpr stimulates viral expression and induces cell killing in human immunodeficiency virus type 1-infected dividing Jurkat T cells. J. Virol. 72, 4686–4693 (1998)Google Scholar
  106. 106.
    S. Yang, Y. Sun, H. Zhang, The multimerization of human immunodeficiency virus type I Vif protein: a requirement for Vif function in the viral life cycle. J. Biol. Chem. 276, 4889–4893 (2001)CrossRefGoogle Scholar
  107. 107.
    B. Yang, L. Gao, L. Li, Z. Lu, X. Fan, C.A. Patel, R.J. Pomerantz, G.C. DuBois, H. Zhang, Potent suppression of viral infectivity by the peptides that inhibit multimerization of human immunodeficiency virus type 1 (HIV-1) Vif proteins. J. Biol. Chem. 278, 6596–6602 (2003)CrossRefGoogle Scholar
  108. 108.
    G. Zanetti, J.A. Briggs, K. Grunewald, Q.J. Sattentau, S.D. Fuller, Cryo-electron tomographic structure of an immunodeficiency virus envelope complex in situ. PLoS Pathog. 2, e83 (2006)CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Ludovic Richert
    • 1
  • Pascal Didier
    • 1
  • Hugues de Rocquigny
    • 1
  • Yves Mély
    • 1
    Email author
  1. 1.UMR 7213 CNRS, Laboratoire de Biophotonique et PharmacologieFaculté de PharmacieIllkirchFrance

Personalised recommendations