1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Virology
  4. Volume 1, 2014
  5. Article

Annual Review of Virology

Volume 1, 2014

Live Cell Imaging of Retroviral Entry

Abstract

Cellular entry of retroviruses is the first critical stage of retroviral replication. Live cell imaging has been utilized to visualize the dynamics, localization, and kinetics of the viral fusion process. Here, we review the different methodologies used for live cell imaging and how the use of these techniques has better elucidated the viral entry process of avian sarcoma and leukosis virus (ASLV) and human immunodeficiency virus type 1 (HIV-1) as well as cell-to-cell transmission of retroviruses. Although some controversies remain, further development of these techniques will provide new insights into the process and dynamics of retroviral fusion in vivo.

Keyword(s): ASLV, cell-to-cell transmission, fluorescence microscopy, HIV-1, viral fusion

Associated Article

There are media items related to this article:
Live Cell Imaging of Retroviral Entry: Video 1
Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-031413-085502
2014-09-29
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/virology/1/1/annurev-virology-031413-085502.html?itemId=/content/journals/10.1146/annurev-virology-031413-085502&mimeType=html&fmt=ahah

Literature Cited

  1. Harrison SC. 1.  2008. Viral membrane fusion. Nat. Struct. Mol. Biol. 15:690–98 [Google Scholar]
  2. Lindemann D, Steffen I, Pöhlmann S. 2.  2013. Cellular entry of retroviruses. Adv. Exp. Med. Biol. 790:128–49 [Google Scholar]
  3. Wilen CB, Tilton JC, Doms RW. 3.  2012. Molecular mechanisms of HIV entry. Adv. Exp. Med. Biol. 726:223–42 [Google Scholar]
  4. Einfeld D, Hunter E. 4.  1988. Oligomeric structure of a prototype retrovirus glycoprotein. Proc. Natl. Acad. Sci. USA 85:8688–92 [Google Scholar]
  5. Barnard RJ, Elleder D, Young JA. 5.  2006. Avian sarcoma and leukosis virus-receptor interactions: from classical genetics to novel insights into virus-cell membrane fusion. Virology 344:25–29 [Google Scholar]
  6. Young JA, Bates P, Varmus HE. 6.  1993. Isolation of a chicken gene that confers susceptibility to infection by subgroup A avian leukosis and sarcoma viruses. J. Virol. 67:1811–16 [Google Scholar]
  7. Bates P, Young JA, Varmus HE. 7.  1993. A receptor for subgroup A Rous sarcoma virus is related to the low density lipoprotein receptor. Cell 74:1043–51 [Google Scholar]
  8. Elleder D, Melder DC, Trejbalova K, Svoboda J, Federspiel MJ. 8.  2004. Two different molecular defects in the Tva receptor gene explain the resistance of two tvar lines of chickens to infection by subgroup A avian sarcoma and leukosis viruses. J. Virol. 78:13489–500 [Google Scholar]
  9. Gilbert JM, Mason D, White JM. 9.  1990. Fusion of Rous sarcoma virus with host cells does not require exposure to low pH. J. Virol. 64:5106–13 [Google Scholar]
  10. Mothes W, Boerger AL, Narayan S, Cunningham JM, Young JAT. 10.  2000. Retroviral entry mediated by receptor priming and low pH triggering of an envelope glycoprotein. Cell 103:679–89 [Google Scholar]
  11. Hallenberger S, Bosch V, Angliker H-D, Shaw E, Klenk HD, Garten W. 11.  1992. Inhibition of furin-mediated cleavage activation of HIV-1 glycoprotein gp160. Nature 360:358–61 [Google Scholar]
  12. Poignard P, Saphire EO, Parren P, Burton DR. 12.  2001. GP120: biologic aspects of structural features. Annu. Rev. Immunol. 19:253–74 [Google Scholar]
  13. Yang P, Ai L-S, Huang S-C, Li H-F, Chan W-E. 13.  et al. 2010. The cytoplasmic domain of human immunodeficiency virus type 1 transmembrane protein gp41 harbors lipid raft association determinants. J. Virol. 84:59–75 [Google Scholar]
  14. Dalgleish AG, Beverley PCL, Clapham PR, Crawford DH, Greaves MF, Weiss RA. 14.  1984. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 312:763–67 [Google Scholar]
  15. Klatzmann D, Champagne E, Chamaret S, Gruest J, Guetard D. 15.  et al. 1984. T-lymphocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature 312:767–68 [Google Scholar]
  16. Feng Y, Broder CC, Kennedy PE, Berger EA. 16.  1996. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272:872–77 [Google Scholar]
  17. Alkhatib G, Combadiere C, Broder CC, Feng Y, Kennedy PE. 17.  et al. 1996. CC CKR5: a RANTES, MIP-1α, MIP-1β receptor as a fusion cofactor for macrophage-tropic HIV-1. Science 272:1955–58 [Google Scholar]
  18. Choe H, Farzan M, Sun Y, Sullivan N, Rollins B. 18.  et al. 1996. The β-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85:1135–48 [Google Scholar]
  19. Deng HK, Liu R, Ellmeier W, Choe S, Unutmaz D. 19.  et al. 1996. Identification of a major co-receptor for primary isolates of HIV-1. Nature 381:661–66 [Google Scholar]
  20. Doranz BJ, Rucker J, Yi YJ, Smyth RJ, Samson M. 20.  et al. 1996. A dual-tropic primary HIV-1 isolate that uses fusin and the β-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell 85:1149–58 [Google Scholar]
  21. Dragic T, Litwin V, Allaway GP, Martin SR, Huang Y. 21.  et al. 1996. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 381:667–73 [Google Scholar]
  22. Oberlin E, Amara A, Bachelerie F, Bessia C, Virelizier JL. 22.  et al. 1996. The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1. Nature 382:833–35 [Google Scholar]
  23. Liu R, Paxton WA, Choe S, Ceradini D, Martin SR. 23.  et al. 1996. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86:367–77 [Google Scholar]
  24. Dean M, Carrington M, Winkler C, Huttley GA, Smith MW. 24.  et al. 1996. Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Science 273:1856–62 [Google Scholar]
  25. Samson M, Libert F, Doranz BJ, Rucker J, Liesnard C. 25.  et al. 1996. Resistance to HIV-1 infection in Caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 382:722–25 [Google Scholar]
  26. Connor RI, Sheridan KE, Ceradini D, Choe S, Landau NR. 26.  1997. Change in coreceptor use correlates with disease progression in HIV-1–infected individuals. J. Exp. Med. 185:621–28 [Google Scholar]
  27. Miyauchi K, Kim Y, Latinovic O, Morozov V, Melikyan GB. 27.  2009. HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 137:433–44Identification of endosomal entry route of HIV-1. [Google Scholar]
  28. Melikyan GB, Barnard RJO, Abrahamyan LG, Mothes W, Young JAT. 28.  2005. Imaging individual retroviral fusion events: from hemifusion to pore formation and growth. Proc. Natl. Acad. Sci. USA 102:8728–33Confirmation of two-step pH-dependent process of ASLV fusion. [Google Scholar]
  29. Barnard RJO, Narayan S, Dornadula G, Miller MD, Young JAT. 29.  2004. Low pH is required for avian sarcoma and leukosis virus Env-dependent viral penetration into the cytosol and not for viral uncoating. J. Virol. 78:10433–41 [Google Scholar]
  30. Melikyan GB, Barnard RJO, Markosyan RM, Young JAT, Cohen FS. 30.  2004. Low pH is required for avian sarcoma and leukosis virus Env-induced hemifusion and fusion pore formation but not for pore growth. J. Virol. 78:3753–62 [Google Scholar]
  31. Jha NK, Latinovic O, Martin E, Novitskiy G, Marin M. 31.  et al. 2011. Imaging single retrovirus entry through alternative receptor isoforms and intermediates of virus-endosome fusion. PLoS Pathog. 7:e1001260 [Google Scholar]
  32. Crivat G, Taraska JW. 32.  2012. Imaging proteins inside cells with fluorescent tags. Trends Biotechnol. 30:8–16 [Google Scholar]
  33. Campbell EM, Perez O, Melar M, Hope TJ. 33.  2007. Labeling HIV-1 virions with two fluorescent proteins allows identification of virions that have productively entered the target cell. Virology 360:286–93 [Google Scholar]
  34. McDonald D, Vodicka MA, Lucero G, Svitkina TM, Borisy GG. 34.  et al. 2002. Visualization of the intracellular behavior of HIV in living cells. J. Cell Biol. 159:441–52 [Google Scholar]
  35. Sherer NM, Lehmann MJ, Jimenez-Soto LF, Ingmundson A, Horner SM. 35.  et al. 2003. Visualization of retroviral replication in living cells reveals budding into multivesicular bodies. Traffic 4:785–801 [Google Scholar]
  36. Hübner W, Chen P, Del Portillo A, Liu Y, Gordon RE, Chen BK. 36.  2007. 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. 81:12596–607 [Google Scholar]
  37. Yu Z, Dobro MJ, Woodward CL, Levandovsky A, Danielson CM. 37.  et al. 2013. Unclosed HIV-1 capsids suggest a curled sheet model of assembly. J. Mol. Biol. 425:112–23 [Google Scholar]
  38. Padilla-Parra S, Marin M, Kondo N, Melikyan GB. 38.  2012. Synchronized retrovirus fusion in cells expressing alternative receptor isoforms releases the viral core into distinct sub-cellular compartments. PLoS Pathog. 8:e1002694 [Google Scholar]
  39. Rudner L, Nydegger S, Coren LV, Nagashima K, Thali M, Ott DE. 39.  2005. Dynamic fluorescent imaging of human immunodeficiency virus type 1 Gag in live cells by biarsenical labeling. J. Virol. 79:4055–65 [Google Scholar]
  40. Campbell EM, Perez O, Anderson JL, Hope TJ. 40.  2008. Visualization of a proteasome-independent intermediate during restriction of HIV-1 by rhesus TRIM5α. J. Cell Biol. 180:549–61 [Google Scholar]
  41. Eckhardt M, Anders M, Muranyi W, Heilemann M, Krijnse-Locker J, Müller B. 41.  2011. A SNAP-tagged derivative of HIV-1—a versatile tool to study virus-cell interactions. PLoS ONE 6:e22007 [Google Scholar]
  42. Day RN. 42.  2005. Imaging protein behavior inside the living cell. Mol. Cell. Endocrinol. 230:1–6 [Google Scholar]
  43. Piston DW, Kremers GJ. 43.  2007. Fluorescent protein FRET: the good, the bad and the ugly. Trends Biochem. Sci. 32:407–14 [Google Scholar]
  44. Narayan S, Barnard RJO, Young JAT. 44.  2003. Two retroviral entry pathways distinguished by lipid raft association of the viral receptor and differences in viral infectivity. J. Virol. 77:1977–83 [Google Scholar]
  45. Padilla-Parra S, Matos PM, Kondo N, Marin M, Santos NC, Melikyan GB. 45.  2012. Quantitative imaging of endosome acidification and single retrovirus fusion with distinct pools of early endosomes. Proc. Natl. Acad. Sci. USA 109:17627–32 [Google Scholar]
  46. Markosyan RM, Cohen FS, Melikyan GB. 46.  2005. Time-resolved imaging of HIV-1 Env-mediated lipid and content mixing between a single virion and cell membrane. Mol. Biol. Cell 16:5502–13 [Google Scholar]
  47. Vega M, Marin M, Kondo N, Miyauchi K, Kim Y. 47.  de la et al. 2011. Inhibition of HIV-1 endocytosis allows lipid mixing at the plasma membrane, but not complete fusion. Retrovirology 8:99 [Google Scholar]
  48. Miyauchi K, Marin M, Melikyan GB. 48.  2011. Visualization of retrovirus uptake and delivery into acidic endosomes. Biochem. J. 434:559–69 [Google Scholar]
  49. Lakadamyali M, Rust MJ, Zhuang X. 49.  2006. Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 124:997–1009 [Google Scholar]
  50. Lakadamyali M, Rust MJ, Babcock HP, Zhuang X. 50.  2003. Visualizing infection of individual influenza viruses. Proc. Natl. Acad. Sci. USA 100:9280–85 [Google Scholar]
  51. Kielian MC, Marsh M, Helenius A. 51.  1986. Kinetics of endosome acidification detected by mutant and wild-type Semliki Forest virus. EMBO J. 5:3103–9 [Google Scholar]
  52. Zhong P, Agosto LM, Munro JB, Mothes W. 52.  2013. Cell-to-cell transmission of viruses. Curr. Opin. Virol. 3:44–50 [Google Scholar]
  53. Phillips DM. 53.  1994. The role of cell-to-cell transmission in HIV-infection. AIDS 8:719–31 [Google Scholar]
  54. Sattentau Q. 54.  2008. Avoiding the void: cell-to-cell spread of human viruses. Nat. Rev. Microbiol. 6:815–26 [Google Scholar]
  55. Zhong P, Agosto LM, Ilinskaya A, Dorjbal B, Truong R. 55.  et al. 2013. Cell-to-cell transmission can overcome multiple donor and target cell barriers imposed on cell-free HIV. PLoS ONE 8:e53138 [Google Scholar]
  56. Dimitrov DS, Willey RL, Sato H, Chang LJ, Blumenthal R, Martin MA. 56.  1993. Quantitation of human immunodeficiency virus type 1 infection kinetics. J. Virol. 67:2182–90 [Google Scholar]
  57. Carr JM, Hocking H, Li P, Burrell CJ. 57.  1999. Rapid and efficient cell-to-cell transmission of human immunodeficiency virus infection from monocyte-derived macrophages to peripheral blood lymphocytes. Virology 265:319–29 [Google Scholar]
  58. Chen P, Hübner W, Spinelli MA, Chen BK. 58.  2007. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J. Virol. 81:12582–95 [Google Scholar]
  59. Geijtenbeek TBH, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GCF. 59.  et al. 2000. DC-SIGN, a dendritic cell–specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100:587–97 [Google Scholar]
  60. Kwon DS, Gregorio G, Bitton N, Hendrickson WA, Littman DR. 60.  2002. DC-SIGN-mediated internalization of HIV is required for trans-enhancement of T cell infection. Immunity 16:135–44 [Google Scholar]
  61. McDonald D, Wu L, Bohks SM, KewalRamani VN, Unutmaz D, Hope TJ. 61.  2003. Recruitment of HIV and its receptors to dendritic cell-T cell junctions. Science 300:1295–97First direct visualization of cell-to-cell transfer of HIV-1. [Google Scholar]
  62. Yu HJ, Reuter MA, McDonald D. 62.  2008. HIV traffics through a specialized, surface-accessible intracellular compartment during trans-infection of T cells by mature dendritic cells. PLoS Pathog. 4:e1000134 [Google Scholar]
  63. Jolly C, Kashefi K, Hollinshead M, Sattentau QJ. 63.  2004. HIV-1 cell to cell transfer across an Env-induced, actin-dependent synapse. J. Exp. Med. 199:283–93 [Google Scholar]
  64. Hübner W, McNerney GP, Chen P, Dale BM, Gordon RE. 64.  et al. 2009. Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 323:1743–47 [Google Scholar]
  65. Dale BM, McNerney GP, Thompson DL, Hübner W, de los Reyes K. 65.  et al. 2011. Cell-to-cell transfer of HIV-1 via virological synapses leads to endosomal virion maturation that activates viral membrane fusion. Cell Host Microbe 10:551–62 [Google Scholar]
  66. Sherer NM, Lehmann MJ, Jimenez-Soto LF, Horensavitz C, Pypaert M, Mothes W. 66.  2007. Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nat. Cell Biol. 9:310–15 [Google Scholar]
  67. Sowinski S, Jolly C, Berninghausen O, Purbhoo MA, Chauveau A. 67.  et al. 2008. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat. Cell Biol. 10:211–19 [Google Scholar]
  68. Sewald X, Gonzalez DG, Haberman AM, Mothes W. 68.  2012. In vivo imaging of virological synapses. Nat. Commun. 3:1320Intravital imaging of Friend MuLV-infected cells in mice. [Google Scholar]
  69. Murooka TT, Deruaz M, Marangoni F, Vrbanac VD, Seung E. 69.  et al. 2012. HIV-infected T cells are migratory vehicles for viral dissemination. Nature 490:283–87Intravital imaging of HIV-1-infected cells in mice. [Google Scholar]
/content/journals/10.1146/annurev-virology-031413-085502
Loading
Live Cell Imaging of Retroviral Entry
Annual Review of Virology 1, 501 (2014); https://doi.org/10.1146/annurev-virology-031413-085502
/content/journals/10.1146/annurev-virology-031413-085502
/content/journals/10.1146/annurev-virology-031413-085502
Loading

Data & Media loading...

Supplemental Material

    Detection of viral fusion with live cell imaging. The fusion of Tomato-Vpr/iGFP-labeled HIV-1 with CHO cells was imaged at 37°C under a blood/gas mixture of CO on a DeltaVision OMX microscope. The experiment was imaged for 44 min with a Z series of images taken every 45 s. Viral fusion was observed as a decrease in GFP fluorescence after 37.5 min due to release of the fluid phase GFP marker into the cytoplasm of the cell. The Tomato-Vpr-labeled virus retained a lower amount of GFP fluorescence after fusion due to GFP localization to the interior of the capsid (Figure 1). See for further details.

file format download
  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error