Labeling of virus components for advanced, quantitative imaging analyses

FEBS Letters

Volumn , Issue , 2016, Pages 1896-1914

  Sakin, Volkan ^a   Paci, Giulia ^b   Lemke, Edward A ^b   Müller, Barbara ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

amber suppression; click labeling; fluorescence; human immunodeficiency virus; imaging; nanoscopy; single molecule techniques; virus

Indexed keywords

FLUORESCENT DYE;

CHEMICAL LABELING; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR TRANSPORT; NONHUMAN; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; REVIEW; VIRION; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS GENOME; VIRUS INFECTIVITY; VIRUS MORPHOGENESIS; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS UNCOATING;

EID: 84978863028     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1002/1873-3468.12131     Document Type: Review

References (139)

1. Giepmans BN, Adams SR, Ellisman MH and Tsien RY (2006) The fluorescent toolbox for assessing protein location and function. Science 312, 217–224.
2. Nienhaus K and Nienhaus GU (2014) Fluorescent proteins for live-cell imaging with super-resolution. Chem Soc Rev 43, 1088–1106.
3. Machan R and Wohland T (2014) Recent applications of fluorescence correlation spectroscopy in live systems. FEBS Lett 588, 3571–3584.
4. Wiseman PW (2015) Image correlation spectroscopy: principles and applications. Cold Spring Harb Protoc 2015, 336–348.
5. Milles S and Lemke EA (2013) What precision-protein-tuning and nano-resolved single molecule sciences can do for each other. BioEssays 35, 65–74.
6. Hell SW (2007) Far-field optical nanoscopy. Science 316, 1153–1158.
7. Huang B, Bates M and Zhuang X (2009) Super-resolution fluorescence microscopy. Annu Rev Biochem 78, 993–1016.
8. Hanne J, Zila V, Heilemann M, Müller B, Kräusslich HG (2016) Super-resolved insights into human immunodeficiency virus biology. FEBS Lett, doi: 10.1002/1873-3468.
9. Baumgartel V, Muller B and Lamb DC (2012) Quantitative live-cell imaging of human immunodeficiency virus (HIV-1) assembly. Viruses 4, 777–799.
10. Boulant S, Stanifer M and Lozach PY (2015) Dynamics of virus-receptor interactions in virus binding, signaling, and endocytosis. Viruses 7, 2794–2815.
11. Brandenburg B and Zhuang X (2007) Virus trafficking – learning from single-virus tracking. Nat Rev Microbiol 5, 197–208.
12. Rust MJ, Lakadamyali M, Brandenburg B and Zhuang X (2011) Single-virus tracking in live cells. Cold Spring Harb Protoc, doi: 10.1101/pdb.top065623.
13. Fackler OT, Murooka TT, Imle A and Mempel TR (2014) Adding new dimensions: towards an integrative understanding of HIV-1 spread. Nat Rev Microbiol 12, 563–574.
14. Hell SW and Wichmann J (1994) Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt Lett 19, 780–782.
15. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, Bonifacino JS, Davidson MW, Lippincott-Schwartz J and Hess HF (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313, 1642–1645.
16. Hess ST, Girirajan TP and Mason MD (2006) Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys J 91, 4258–4272.
17. Rust MJ, Bates M and Zhuang X (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3, 793–795.
18. Campbell EM and Hope TJ (2008) Live cell imaging of the HIV-1 life cycle. Trends Microbiol 16, 580–587.
19. Chojnacki J and Muller B (2013) Investigation of HIV-1 assembly and release using modern fluorescence imaging techniques. Traffic 14, 15–24.
20. McDonald D, Vodicka MA, Lucero G, Svitkina TM, Borisy GG, Emerman M and Hope TJ (2002) Visualization of the intracellular behavior of HIV in living cells. J Cell Biol 159, 441–452.
21. Albanese A, Arosio D, Terreni M and Cereseto A (2008) HIV-1 pre-integration complexes selectively target decondensed chromatin in the nuclear periphery. PLoS One 3, e2413.
22. Hermida-Matsumoto L and Resh MD (2000) Localization of human immunodeficiency virus type 1 Gag and Env at the plasma membrane by confocal imaging. J Virol 74, 8670–8679.
23. Perrin-Tricaud C, Davoust J and Jones IM (1999) Tagging the human immunodeficiency virus gag protein with green fluorescent protein. Minimal evidence for colocalisation with actin. Virology 255, 20–25.
24. Hubner W, Chen P, Del Portillo A, Liu Y, Gordon RE and Chen BK (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, 12596–12607.
25. Muller B, Daecke J, Fackler OT, Dittmar MT, Zentgraf H and Krausslich HG (2004) Construction and characterization of a fluorescently labeled infectious human immunodeficiency virus type 1 derivative. J Virol 78, 10803–10813.
26. Hendrix J, Baumgärtel V, Schrimpf W, Ivanchenko S, Digman MA, Gratton E, Kräusslich HG, Müller B and Lamb DC (2015) Live-cell observation of cytosolic HIV-1 assembly onset reveals RNA-interacting Gag oligomers. J Cell Biol 210, 629–646.
27. El Meshri SE, Dujardin D, Godet J, Richert L, Boudier C, Darlix JL, Didier P, Mely Y and de Rocquigny H (2015) 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 427, 1480–1494.
28. Jouvenet N, Bieniasz PD and Simon SM (2008) Imaging the biogenesis of individual HIV-1 virions in live cells. Nature 454, 236–240.
29. Ivanchenko S, Godinez WJ, Lampe M, Kräusslich HG, Eils R, Rohr K, Brauchle C, Müller B and Lamb DC (2009) Dynamics of HIV-1 assembly and release. PLoS Pathog 5, e1000652.
30. Baumgärtel V, Ivanchenko S, Dupont A, Sergeev M, Wiseman PW, Kräusslich HG, Brauchle C, Müller B, Lamb DC et al. (2011) Live-cell visualization of dynamics of HIV budding site interactions with an ESCRT component. Nat Cell Biol 13, 469–474.
31. Jouvenet N, Simon SM and Bieniasz PD (2009) Imaging the interaction of HIV-1 genomes and Gag during assembly of individual viral particles. Proc Natl Acad Sci USA 106, 19114–19119.
32. Jouvenet N, Zhadina M, Bieniasz PD and Simon SM (2011) Dynamics of ESCRT protein recruitment during retroviral assembly. Nat Cell Biol 13, 394–401.
33. Miyauchi K, Marin M and Melikyan GB (2011) Visualization of retrovirus uptake and delivery into acidic endosomes. Biochem J 434, 559–569.
34. Herold N, Anders-Osswein M, Glass B, Eckhardt M, Muller B and Krausslich HG (2014) HIV-1 entry in SupT1-R5, CEM-ss, and primary CD4+ T cells occurs at the plasma membrane and does not require endocytosis. J Virol 88, 13956–13970.
35. Izquierdo-Useros N, Lorizate M, Puertas MC, Rodriguez-Plata MT, Zangger N, Erikson E, Pino M, Erkizia I, Glass B, Clotet B et al. (2012) Siglec-1 is a novel dendritic cell receptor that mediates HIV-1 trans-infection through recognition of viral membrane gangliosides. PLoS Biol 10, e1001448.
36. Chen J, Nikolaitchik O, Singh J, Wright A, Bencsics CE, Coffin JM, Ni N, Lockett S, Pathak VK and Hu WS (2009) High efficiency of HIV-1 genomic RNA packaging and heterozygote formation revealed by single virion analysis. Proc Natl Acad Sci USA 106, 13535–13540.
37. Chen J, Rahman SA, Nikolaitchik OA, Grunwald D, Sardo L, Burdick RC, Plisov S, Liang E, Tai S, Pathak VK et al. (2016) HIV-1 RNA genome dimerizes on the plasma membrane in the presence of Gag protein. Proc Natl Acad Sci USA 113, E201–E208.
38. Itano MS, Bleck M, Johnson DS and Simon SM (2016) Readily accessible multiplane microscopy: 3D tracking the HIV-1 genome in living cells. Traffic 17, 179–186.
39. Miyauchi K, Kim Y, Latinovic O, Morozov V and Melikyan GB (2009) HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 137, 433–444.
40. Mamede JI and Hope TJ (2016) Detection and tracking of dual-labeled HIV particles using wide-field live cell imaging to follow viral core integrity. Methods Mol Biol 1354, 49–59.
41. Gunzenhauser J, Olivier N, Pengo T and Manley S (2012) Quantitative super-resolution imaging reveals protein stoichiometry and nanoscale morphology of assembling HIV-Gag virions. Nano Lett 12, 4705–4710.
42. Lehmann M, Rocha S, Mangeat B, Blanchet F, Uji IH, Hofkens J and Piguet V (2011) Quantitative multicolor super-resolution microscopy reveals tetherin HIV-1 interaction. PLoS Pathog 7, e1002456.
43. Muranyi W, Malkusch S, Muller B, Heilemann M and Krausslich HG (2013) Super-resolution microscopy reveals specific recruitment of HIV-1 envelope proteins to viral assembly sites dependent on the envelope C-terminal tail. PLoS Pathog 9, e1003198.
44. Lehmann MJ, Sherer NM, Marks CB, Pypaert M and Mothes W (2005) Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells. J Cell Biol 170, 317–325.
45. Murooka TT, Deruaz M, Marangoni F, Vrbanac VD, Seung E, von Andrian UH, Tager AM, Luster AD and Mempel TR (2012) HIV-infected T cells are migratory vehicles for viral dissemination. Nature 490, 283–287.
46. Sewald X, Gonzalez DG, Haberman AM and Mothes W (2012) In vivo imaging of virological synapses. Nat Commun 3, 1320.
47. Sewald X, Ladinsky MS, Uchil PD, Beloor J, Pi R, Herrmann C, Motamedi N, Murooka TT, Brehm MA, Greiner DL et al. (2015) Retroviruses use CD169-mediated trans-infection of permissive lymphocytes to establish infection. Science 350, 563–567.
48. Mishin AS, Belousov VV, Solntsev KM and Lukyanov KA (2015) Novel uses of fluorescent proteins. Curr Opin Chem Biol 27, 1–9.
49. Craggs TD (2009) Green fluorescent protein: structure, folding and chromophore maturation. Chem Soc Rev 38, 2865–2875.
50. Costantini LM and Snapp EL (2015) Going viral with fluorescent proteins. J Virol 89, 9706–9708.
51. Costantini LM, Fossati M, Francolini M and Snapp EL (2012) Assessing the tendency of fluorescent proteins to oligomerize under physiologic conditions. Traffic 13, 643–649.
52. Keppler A, Gendreizig S, Gronemeyer T, Pick H, Vogel H and Johnsson K (2003) A general method for the covalent labeling of fusion proteins with small molecules in vivo. Nat Biotechnol 21, 86–89.
53. Gautier A, Juillerat A, Heinis C, Correa IR Jr, Kindermann M, Beaufils F and Johnsson K (2008) An engineered protein tag for multiprotein labeling in living cells. Chem Biol 15, 128–136.
54. Los GV, Encell LP, McDougall MG, Hartzell DD, Karassina N, Zimprich C, Wood MG, Learish R, Ohana RF, Urh M et al. (2008) HaloTag: a novel protein labeling technology for cell imaging and protein analysis. ACS Chem Biol 3, 373–382.
55. Wombacher R, Heidbreder M, van de Linde S, Sheetz MP, Heilemann M, Cornish VW and Sauer M (2010) Live-cell super-resolution imaging with trimethoprim conjugates. Nat Methods 7, 717–719.
56. Adams SR, Campbell RE, Gross LA, Martin BR, Walkup GK, Yao Y, Llopis J and Tsien RY (2002) New biarsenical ligands and tetracysteine motifs for protein labeling in vitro and in vivo: synthesis and biological applications. J Am Chem Soc 124, 6063–6076.
57. Popp MW, Antos JM, Grotenbreg GM, Spooner E and Ploegh HL (2007) Sortagging: a versatile method for protein labeling. Nat Chem Biol 3, 707–708.
58. Lin CW and Ting AY (2006) Transglutaminase-catalyzed site-specific conjugation of small-molecule probes to proteins in vitro and on the surface of living cells. J Am Chem Soc 128, 4542–4543.
59. Yin J, Straight PD, McLoughlin SM, Zhou Z, Lin AJ, Golan DE, Kelleher NL, Kolter R and Walsh CT (2005) Genetically encoded short peptide tag for versatile protein labeling by Sfp phosphopantetheinyl transferase. Proc Natl Acad Sci USA 102, 15815–15820.
60. Zhou Z, Koglin A, Wang Y, McMahon AP and Walsh CT (2008) An eight residue fragment of an acyl carrier protein suffices for post-translational introduction of fluorescent pantetheinyl arms in protein modification in vitro and in vivo. J Am Chem Soc 130, 9925–9930.
61. Fernandez-Suarez M, Baruah H, Martinez-Hernandez L, Xie KT, Baskin JM, Bertozzi CR and Ting AY (2007) Redirecting lipoic acid ligase for cell surface protein labeling with small-molecule probes. Nat Biotechnol 25, 1483–1487.
62. Uttamapinant C, White KA, Baruah H, Thompson S, Fernández-Suárez M, Puthenveetil S and Ting AY (2010) A fluorophore ligase for site-specific protein labeling inside living cells. Proc Natl Acad Sci U S A 107, 10914–10919.
63. Cohen GN and Munier R (1956) Incorporation of structural analogues of amino acids in bacterial proteins. Biochim Biophys Acta 21, 592–593.
64. Ngo JT and Tirrell DA (2011) Noncanonical amino acids in the interrogation of cellular protein synthesis. Acc Chem Res 44, 677–685.
65. Liu DR and Schultz PG (1999) Progress toward the evolution of an organism with an expanded genetic code. Proc Natl Acad Sci USA 96, 4780–4785.
66. Liu CC and Schultz PG (2010) Adding new chemistries to the genetic code. Annu Rev Biochem 79, 413–444.
67. Elliott TS, Townsley FM, Bianco A, Ernst RJ, Sachdeva A, Elsasser SJ, Davis L, Lang K, Pisa R, Greiss S et al. (2014) Proteome labeling and protein identification in specific tissues and at specific developmental stages in an animal. Nat Biotechnol 32, 465–472.
68. Greiss S and Chin JW (2011) Expanding the genetic code of an animal. J Am Chem Soc 133, 14196–14199.
69. Lemke EA (2014) The exploding genetic code. ChemBioChem 15, 1691–1694.
70. Nikic I and Lemke EA (2015) Genetic code expansion enabled site-specific dual-color protein labeling: superresolution microscopy and beyond. Curr Opin Chem Biol 28, 164–173.
71. Hackenberger CP and Schwarzer D (2008) Chemoselective ligation and modification strategies for peptides and proteins. Angew Chem Int Ed Engl 47, 10030–10074.
72. van Hest JC and van Delft FL (2011) Protein modification by strain-promoted alkyne-azide cycloaddition. ChemBioChem 12, 1309–1312.
73. Sauer J, Mielert A, Lang D and Peter D (1965) Eine Studie der Diels-Alder-Reaktion, III: Umsetzungen von 1.2.4.5-Tetrazinen mit Olefinen. Zur Struktur von Dihydropyridazinen. Chem Ber 98, 1435–1445.
74. Wiessler M, Waldeck W, Kliem C, Pipkorn R and Braun K (2009) The Diels-Alder-reaction with inverse-electron-demand, a very efficient versatile click-reaction concept for proper ligation of variable molecular partners. Int J Med Sci 7, 19–28.
75. Devaraj NK, Weissleder R and Hilderbrand SA (2008) Tetrazine-based cycloadditions: application to pretargeted live cell imaging. Bioconjug Chem 19, 2297–2299.
76. Lin S, Yan H, Li L, Yang M, Peng B, Chen S, Li W and Chen PR (2013) Site-specific engineering of chemical functionalities on the surface of live hepatitis D virus. Angew Chem Int Ed Engl 52, 13970–13974.
77. Nikic I, Plass T, Schraidt O, Szymanski J, Briggs JA, Schultz C and Lemke EA (2014) Minimal tags for rapid dual-color live-cell labeling and super-resolution microscopy. Angew Chem Int Ed Engl 53, 2245–2249.
78. Jao CY and Salic A (2008) Exploring RNA transcription and turnover in vivo by using click chemistry. Proc Natl Acad Sci USA 105, 15779–15784.
79. Salic A and Mitchison TJ (2008) A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc Natl Acad Sci USA 105, 2415–2420.
80. Wang IH, Suomalainen M, Andriasyan V, Kilcher S, Mercer J, Neef A, Luedtke NW and Greber UF (2013) Tracking viral genomes in host cells at single-molecule resolution. Cell Host Microbe 14, 468–480.
81. Xu H, Franks T, Gibson G, Huber K, Rahm N, Strambio De Castillia C, Luban J, Aiken C, Watkins S, Sluis-Cremer N et al. (2013) Evidence for biphasic uncoating during HIV-1 infection from a novel imaging assay. Retrovirology 10, 70.
82. Jewett JC and Bertozzi CR (2010) Cu-free click cycloaddition reactions in chemical biology. Chem Soc Rev 39, 1272–1279.
83. Rubino FA, Oum YH, Rajaram L, Chu Y and Carrico IS (2012) Chemoselective modification of viral surfaces via bioorthogonal click chemistry. J Vis Exp 19, e4246.
84. Kuerschner L and Thiele C (2014) Multiple bonds for the lipid interest. Biochim Biophys Acta 1841, 1031–1037.
85. Checkley MA, Luttge BG and Freed EO (2011) HIV-1 envelope glycoprotein biosynthesis, trafficking, and incorporation. J Mol Biol 410, 582–608.
86. Pereira CF, Ellenberg PC, Jones KL, Fernandez TL, Smyth RP, Hawkes DJ, Hijnen M, Vivet-Boudou V, Marquet R, Johnson I et al. (2011) Labeling of multiple HIV-1 proteins with the biarsenical-tetracysteine system. PLoS One 6, e17016.
87. Nakane S, Iwamoto A and Matsuda Z (2015) The V4 and V5 variable loops of HIV-1 envelope glycoprotein are tolerant to insertion of green fluorescent protein and are useful targets for labeling. J Biol Chem 290, 15279–15291.
88. Munro JB, Gorman J, Ma X, Zhou Z, Arthos J, Burton DR, Koff WC, Courter JR, Smith AB, 3rd, Kwong PD et al. (2014) Conformational dynamics of single HIV-1 envelope trimers on the surface of native virions. Science 346, 759–763.
89. Ruthardt N, Lamb DC and Brauchle C (2011) Single-particle tracking as a quantitative microscopy-based approach to unravel cell entry mechanisms of viruses and pharmaceutical nanoparticles. Mol Ther 19, 1199–1211.
90. Matreyek KA and Engelman A (2013) Viral and cellular requirements for the nuclear entry of retroviral preintegration nucleoprotein complexes. Viruses 5, 2483–2511.
91. Ambrose Z and Aiken C (2014) HIV-1 uncoating: connection to nuclear entry and regulation by host proteins. Virology 454–455, 371–379.
92. Campbell EM and Hope TJ (2015) HIV-1 capsid: the multifaceted key player in HIV-1 infection. Nat Rev Microbiol 13, 471–483.
93. Arhel N, Genovesio A, Kim KA, Miko S, Perret E, Olivo-Marin JC, Shorte S and Charneau P (2006) Quantitative four-dimensional tracking of cytoplasmic and nuclear HIV-1 complexes. Nat Methods 3, 817–824.
94. Peng K, Muranyi W, Glass B, Laketa V, Yant SR, Tsai L, Cihlar T, Müller B and Kräusslich HG (2014) Quantitative microscopy of functional HIV post-entry complexes reveals association of replication with the viral capsid. Elife 3, e04114.
95. Campbell EM, Perez O, Anderson JL and Hope TJ (2008) Visualization of a proteasome-independent intermediate during restriction of HIV-1 by rhesus TRIM5alpha. J Cell Biol 180, 549–561.
96. Rihn SJ, Wilson SJ, Loman NJ, Alim M, Bakker SE, Bhella D, Gifford RJ, Rixon FJ and Bieniasz PD (2013) Extreme genetic fragility of the HIV-1 capsid. PLoS Pathog 9, e1003461.
97. von Schwedler UK, Stray KM, Garrus JE and Sundquist WI (2003) Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J Virol 77, 5439–5450.
98. von Appen A, Kosinski J, Sparks L, Ori A, DiGuilio AL, Vollmer B, Mackmull MT, Banterle N, Parca L, Kastritis P et al. (2015) In situ structural analysis of the human nuclear pore complex. Nature 526, 140–143.
99. Ribbeck K and Gorlich D (2001) Kinetic analysis of translocation through nuclear pore complexes. EMBO J 20, 1320–1330.
100. Mettenleiter TC (2015) Breaching the barrier-the nuclear envelope in virus infection. J Mol Biol, doi: 10.1016/j.jmb.2015.10.001.
101. Labokha AA and Fassati A (2013) Viruses challenge selectivity barrier of nuclear pores. Viruses 5, 2410–2423.
102. Naim B, Brumfeld V, Kapon R, Kiss V, Nevo R and Reich Z (2007) Passive and facilitated transport in nuclear pore complexes is largely uncoupled. J Biol Chem 282, 3881–3888.
103. Dange T, Grunwald D, Grunwald A, Peters R and Kubitscheck U (2008) Autonomy and robustness of translocation through the nuclear pore complex: a single-molecule study. J Cell Biol 183, 77–86.
104. Yang W, Gelles J and Musser SM (2004) Imaging of single-molecule translocation through nuclear pore complexes. Proc Natl Acad Sci USA 101, 12887–12892.
105. Grunwald D and Singer RH (2010) In vivo imaging of labelled endogenous beta-actin mRNA during nucleocytoplasmic transport. Nature 467, 604–607.
106. Lowe AR, Siegel JJ, Kalab P, Siu M, Weis K and Liphardt JT (2010) Selectivity mechanism of the nuclear pore complex characterized by single cargo tracking. Nature 467, 600–603.
107. Loschberger A, van de Linde S, Dabauvalle MC, Rieger B, Heilemann M, Krohne G and Sauer M (2012) Super-resolution imaging visualizes the eightfold symmetry of gp210 proteins around the nuclear pore complex and resolves the central channel with nanometer resolution. J Cell Sci 125, 570–575.
108. Szymborska A, de Marco A, Daigle N, Cordes VC, Briggs JA and Ellenberg J (2013) Nuclear pore scaffold structure analyzed by super-resolution microscopy and particle averaging. Science 341, 655–658.
109. Ori A, Banterle N, Iskar M, Andres-Pons A, Escher C, Khanh Bui H, Sparks L, Solis-Mezarino V, Rinner O, Bork P et al. (2013) Cell type-specific nuclear pores: a case in point for context-dependent stoichiometry of molecular machines. Mol Syst Biol 9, 648.
110. Banterle N, Bui KH, Lemke EA and Beck M (2013) Fourier ring correlation as a resolution criterion for super-resolution microscopy. J Struct Biol 183, 363–367.
111. Hilditch L and Towers GJ (2014) A model for cofactor use during HIV-1 reverse transcription and nuclear entry. Curr Opin Virol 4, 32–36.
112. Forshey BM, von Schwedler U, Sundquist WI and Aiken C (2002) Formation of a human immunodeficiency virus type 1 core of optimal stability is crucial for viral replication. J Virol 76, 5667–5677.
113. Bhattacharya A, Alam SL, Fricke T, Zadrozny K, Sedzicki J, Taylor AB, Demeler B, Pornillos O, Ganser-Pornillos BK, Diaz-Griffero F et al. (2014) Structural basis of HIV-1 capsid recognition by PF74 and CPSF6. Proc Natl Acad Sci USA 111, 18625–18630.
114. Price AJ, Jacques DA, McEwan WA, Fletcher AJ, Essig S, Chin JW, Halambage UD, Aiken C and James LC (2014) Host cofactors and pharmacologic ligands share an essential interface in HIV-1 capsid that is lost upon disassembly. PLoS Pathog 10, e1004459.
115. Briggs JA, Wilk T, Welker R, Krausslich HG and Fuller SD (2003) Structural organization of authentic, mature HIV-1 virions and cores. EMBO J 22, 1707–1715.
116. Sundquist WI and Krausslich HG (2012) HIV-1 assembly, budding, and maturation. Cold Spring Harb Perspect Med 2, a006924.
117. Konvalinka J, Kräusslich HG and Müller B (2015) Retroviral proteases and their roles in virion maturation. Virology 479–480, 403–417.
118. Briggs JA and Krausslich HG (2011) The molecular architecture of HIV. J Mol Biol 410, 491–500.
119. Manley S, Gillette JM, Patterson GH, Shroff H, Hess HF, Betzig E and Lippincott-Schwartz J (2008) High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat Methods 5, 155–157.
120. Van Engelenburg SB, Shtengel G, Sengupta P, Waki K, Jarnik M, Ablan SD, Freed EO, Hess HF and Lippincott-Schwartz J (2014) Distribution of ESCRT machinery at HIV assembly sites reveals virus scaffolding of ESCRT subunits. Science 343, 653–656.
121. Bleck M, Itano MS, Johnson DS, Thomas VK, North AJ, Bieniasz PD and Simon SM (2014) Temporal and spatial organization of ESCRT protein recruitment during HIV-1 budding. Proc Natl Acad Sci USA 111, 12211–12216.
122. Pornillos O, Higginson DS, Stray KM, Fisher RD, Garrus JE, Payne M, He GP, Wang HE, Morham SG and Sundquist WI (2003) HIV Gag mimics the Tsg101-recruiting activity of the human Hrs protein. J Cell Biol 162, 425–434.
123. Eckhardt M, Anders M, Muranyi W, Heilemann M, Krijnse-Locker J and Muller B (2011) A SNAP-tagged derivative of HIV-1–a versatile tool to study virus-cell interactions. PLoS One 6, e22007.
124. Malkusch S, Muranyi W, Muller B, Krausslich HG and Heilemann M (2013) Single-molecule coordinate-based analysis of the morphology of HIV-1 assembly sites with near-molecular spatial resolution. Histochem Cell Biol 139, 173–179.
125. Gousset K, Ablan SD, Coren LV, Ono A, Soheilian F, Nagashima K, Ott DE and Freed EO (2008) Real-time visualization of HIV-1 GAG trafficking in infected macrophages. PLoS Pathog 4, e1000015.
126. Turville SG, Aravantinou M, Stossel H, Romani N and Robbiani M (2008) Resolution of de novo HIV production and trafficking in immature dendritic cells. Nat Methods 5, 75–85.
127. Lelek M, Di Nunzio F, Henriques R, Charneau P, Arhel N and Zimmer C (2012) Superresolution imaging of HIV in infected cells with FlAsH-PALM. Proc Natl Acad Sci USA 109, 8564–8569.
128. Popp MW, Karssemeijer RA and Ploegh HL (2012) Chemoenzymatic site-specific labeling of influenza glycoproteins as a tool to observe virus budding in real time. PLoS Pathog 8, e1002604.
129. Jullien L and Gautier A (2015) Fluorogen-based reporters for fluorescence imaging: a review. Methods Appl Fluoresc 3, e042007.
130. Bruchez MP (2015) Dark dyes-bright complexes: fluorogenic protein labeling. Curr Opin Chem Biol 27, 18–23.
131. Lukinavicius G, Umezawa K, Olivier N, Honigmann A, Yang G, Plass T, Mueller V, Reymond L, Correa IR Jr, Luo ZG et al. (2013) A near-infrared fluorophore for live-cell super-resolution microscopy of cellular proteins. Nat Chem 5, 132–139.
132. Lukinavicius G, Blaukopf C, Pershagen E, Schena A, Reymond L, Derivery E, Gonzalez-Gaitan M, D'Este E, Hell SW, Gerlich DW et al. (2015) SiR-Hoechst is a far-red DNA stain for live-cell nanoscopy. Nat Commun 6, 8497.
133. Herner A, Estrada Girona G, Nikic I, Kallay M, Lemke EA and Kele P (2014) New generation of bioorthogonally applicable fluorogenic dyes with visible excitations and large Stokes shifts. Bioconjug Chem 25, 1370–1374.
134. Mukai T, Hayashi A, Iraha F, Sato A, Ohtake K, Yokoyama S and Sakamoto K (2010) Codon reassignment in the Escherichia coli genetic code. Nucleic Acids Res 38, 8188–8195.
135. Johnson DB, Xu J, Shen Z, Takimoto JK, Schultz MD, Schmitz RJ, Xiang Z, Ecker JR, Briggs SP and Wang L (2011) RF1 knockout allows ribosomal incorporation of unnatural amino acids at multiple sites. Nat Chem Biol 7, 779–786.
136. Neumann H, Wang KH, Davis L, Garcia-Alai M and Chin JW (2010) Encoding multiple unnatural amino acids via evolution of a quadruplet-decoding ribosome. Nature 464, 441–444.
137. Schmied WH, Elsasser SJ, Uttamapinant C and Chin JW (2014) Efficient multisite unnatural amino acid incorporation in mammalian cells via optimized pyrrolysyl tRNA synthetase/tRNA expression and engineered eRF1. J Am Chem Soc 136, 15577–15583.
138. Tcherkasskaya O, Davidson EA and Uversky VN (2003) Biophysical constraints for protein structure prediction. J Proteome Res 2, 37–42.
139. Flatt JW and Greber UF (2015) Misdelivery at the nuclear pore complex-stopping a virus dead in its tracks. Cells 4, 277–296.