The host RNAs in retroviral particles

Viruses

Volumn 8, Issue 8, 2016, Pages

  Telesnitsky, Alice ^a   Wolin, Sandra L ^b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

HIV 1 2; Non coding RNA 1; Retroviral assembly

Indexed keywords

7SL RNA; ALPHA INTERFERON; DNA DIRECTED RNA POLYMERASE III; HEAT SHOCK COGNATE PROTEIN 70; MESSENGER RNA; RETINOIC ACID INDUCIBLE PROTEIN I; RIBONUCLEASE; RIBONUCLEOPROTEIN; SMALL NUCLEAR RNA; TOLL LIKE RECEPTOR 7; TRANSFER RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

BIOGENESIS; CELL MIGRATION; DNA PACKAGING; GENE EXPRESSION REGULATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOPRECIPITATION; INNATE IMMUNITY; LONG INTERSPERSED REPEAT; MEMBRANE FORMATION; MURINE LEUKEMIA VIRUS; NUCLEAR IMPORT; PROTEIN RNA BINDING; RETROPOSON; RETROVIRIDAE; RETROVIRUS INFECTION; REVERSE TRANSCRIPTION; REVIEW; RNA SEQUENCE; VIRION; VIRUS ASSEMBLY; VIRUS GENOME; HOST PATHOGEN INTERACTION; PHYSIOLOGY;

HOST-PATHOGEN INTERACTIONS; HUMANS; RETROVIRIDAE; RNA, UNTRANSLATED; VIRUS ASSEMBLY;

EID: 84983315955     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v8080235     Document Type: Review

References (125)

1. Bishop, J.M.; Levinson, W.E.; Quintrell, N.; Sullivan, D.; Fanshier, L.; Jackson, J. The low molecular weight RNAs of Rous sarcoma virus. I. The 4 S RNA. Virology 1970, 42, 182–195.
2. Eckwahl, M.J.; Telesnitsky, A.; Wolin, S.L. Host RNA packaging by retroviruses: A newly synthesized story. mBio 2016, 7, e02025–e02015.
3. Eckwahl, M.J.; Arnion, H.; Kharytonchyk, S.; Zang, T.; Bieniasz, P.D.; Telesnitsky, A.; Wolin, S.L. Analysis of the human immunodeficiency virus-1 RNA packageome. RNA 2016.
4. Linial, M.L.; Miller, A.D. Retroviral RNA packaging: Sequence requirements and implications. Curr. Top. Microbiol. Immunol. 1990, 157, 125–152.
5. Berkowitz, R.; Fisher, J.; Goff, S.P. RNA packaging. Curr. Top. Microbiol. Immunol. 1996, 214, 177–218.
6. Wang, S.W.; Aldovini, A. RNA incorporation is critical for retroviral particle integrity after cell membrane assembly of Gag complexes. J. Virol. 2002, 76, 11853–11865.
7. Rulli, S.J., Jr.; Hibbert, C.S.; Mirro, J.; Pederson, T.; Biswal, S.; Rein, A. Selective and nonselective packaging of cellular RNAs in retrovirus particles. J. Virol. 2007, 81, 6623–6631.
8. Onafuwa-Nuga, A.A.; King, S.R.; Telesnitsky, A. Nonrandom packaging of host RNAs in Moloney murine leukemia virus. J. Virol. 2005, 79, 13528–13537.
9. Eckwahl, M.J.; Sim, S.; Smith, D.; Telesnitsky, A.; Wolin, S.L. A retrovirus packages nascent host noncoding RNAs from a novel surveillance pathway. Genes Dev. 2015, 29, 646–657.
10. Onafuwa-Nuga, A.A.; Telesnitsky, A.; King, S.R. 7SL RNA, but not the 54-kD signal recognition particle protein, is an abundant component of both infectious HIV-1 and minimal virus-like particles. RNA 2006, 12, 542–546.
11. Mak, J.; Kleiman, L. Primer tRNAs for reverse transcription. J. Virol. 1997, 71, 8087–8095.
12. Dahlberg, J.E.; Sawyer, R.C.; Taylor, J.M.; Faras, A.J.; Levinson, W.E.; Goodman, H.M.; Bishop, J.M. Transcription of DNA from the 70S RNA of Rous sarcoma virus. I. Identification of a specific 4S RNA which serves as primer. J. Virol.1974, 13, 1126–1133.
13. Bonar, R.A.; Sverak, L.; Bolognesi, D.P.; Langlois, A.J.; Beard, D.; Beard, J.W. Ribonucleic acid components of BAI strain A (myeloblastosis) avian tumor virus. Cancer Res. 1967, 27, 1138–1157.
14. Faras, A.J.; Dahlberg, J.E.; Sawyer, R.C.; Harada, F.; Taylor, J.M.; Levinson, W.E.; Bishop, J.M.; Goodman, H.M. Transcription of DNA from the 70S RNA of Rous sarcoma virus. II. Structure of a 4S RNA primer. J. Virol. 1974, 13, 1134–1142.
15. Moore, M.D.; Hu, W.S. HIV-1 RNA dimerization: It takes two to tango. AIDS Rev. 2009, 11, 91–102.
16. Huang, Y.; Mak, J.; Cao, Q.; Li, Z.; Wainberg, M.A.; Kleiman, L. Incorporation of excess wild-type and mutant tRNA(3Lys) into human immunodeficiency virus type 1. J. Virol. 1994, 68, 7676–7683.
17. Pavon-Eternod, M.; Wei, M.; Pan, T.; Kleiman, L. Profiling non-lysyl tRNAs in HIV-1. RNA 2010, 16, 267–273.
18. Bishop, J.M.; Levinson, W.E.; Sullivan, D.; Fanshier, L.; Quintrell, N.; Jackson, J. The low molecular weight RNAs of Rous sarcoma virus. II. The 7 S RNA. Virology 1970, 42, 927–937.
19. Giles, K.; Caputi, M.; Beemon, K.L. Packaging and reverse transcription of snRNAs by retroviruses may generate pseudogenes. RNA 2004, 10, 299–307.
20. Garcia, E.L.; Onafuwa-Nuga, A.; Sim, S.; King, S.R.; Wolin, S.L.; Telesnitsky, A. Packaging of host mY RNAs by murine leukemia virus may occur early in Y RNA biogenesis. J. Virol. 2009, 83, 12526–12534.
21. French, N.S.; Norton, J.D. Structure and functional properties of mouse VL30 retrotransposons. Biochim. Biophys. Acta 1997, 1352, 33–47.
22. Patience, C.; Takeuchi, Y.; Cosset, F.L.; Weiss, R.A. Packaging of endogenous retroviral sequences in retroviral vectors produced by murine and human packaging cells. J. Virol. 1998, 72, 2671–2676.
23. Van der Kuyl, A.C. HIV infection and HERV expression: A review. Retrovirology 2012, 9, 6.
24. Zeilfelder, U.; Frank, O.; Sparacio, S.; Schon, U.; Bosch, V.; Seifarth, W.; Leib-Mosch, C. The potential of retroviral vectors to cotransfer human endogenous retroviruses (HERVs) from human packaging cell lines. Gene 2007, 390, 175–179.
25. Schopman, N.C.; van Montfort, T.; Willemsen, M.; Knoepfel, S.A.; Pollakis, G.; van Kampen, A.; Sanders, R.W.; Haasnoot, J.; Berkhout, B. Selective packaging of cellular miRNAs in HIV-1 particles. Virus Res. 2012, 169, 438–447.
26. Kincaid, R.P.; Burke, J.M.; Sullivan, C.S. RNA virus microRNA that mimics a B-cell oncomiR. Proc. Natl. Acad. Sci. USA 2012, 109, 3077–3082.
27. Swaminathan, G.; Navas-Martin, S.; Martin-Garcia, J. MicroRNAs and HIV-1 infection: Antiviral activities and beyond. J. Mol. Biol. 2014, 426, 1178–1197.
28. Rice, A.P. Roles of microRNAs and long-noncoding RNAs in human immunodeficiency virus replication. Wiley Interdiscip. Rev. RNA 2015, 6, 661–670.
29. Telesnitsky, A.; Goff, S.P. Reverse Transcriptase and the Generation of Retroviral DNA. In Retroviruses; Coffin, J.M., Hughes, S.H., Varmus, H.E., Eds.; Cold Spring Harbor: New York, NY, USA, 1997.
30. Harada, F.; Sawyer, R.C.; Dahlberg, J.E. A primer ribonucleic acid for initiation of in vitro Rous sarcarcoma virus deoxyribonucleic acid synthesis. J. Biol. Chem. 1997, 250, 3487–3497.
31. Levin, J.G.; Seidman, J.G. Effect of polymerase mutations on packaging of primer tRNAPro during murine leukemia virus assembly. J. Virol. 1981, 38, 403–408.
32. Wain-Hobson, S.; Sonigo, P.; Danos, O.; Cole, S.; Alizon, M. Nucleotide sequence of the AIDS virus, LAV. Cell 1985, 40, 9–17.
33. Miller, S.B.; Yildiz, F.Z.; Lo, J.A.; Wang, B.; D’Souza, V.M. A structure-based mechanism for tRNA and retroviral RNA remodelling during primer annealing. Nature 2014, 515, 591–595.
34. Mak, J.; Jiang, M.; Wainberg, M.A.; Hammarskjold, M.L.; Rekosh, D.; Kleiman, L. Role of Pr160gag-pol in mediating the selective incorporation of tRNA(Lys) into human immunodeficiency virus type 1 particles. J. Virol. 1994, 68, 2065–2072.
35. Jiang, M.; Mak, J.; Ladha, A.; Cohen, E.; Klein, M.; Rovinski, B.; Kleiman, L. Identification of tRNAs incorporated into wild-type and mutant human immunodeficiency virus type 1. J. Virol. 1993, 67, 3246–3253.
36. Zaitseva, L.; Myers, R.; Fassati, A. tRNAs promote nuclear import of HIV-1 intracellular reverse transcription complexes. PLoS Biol. 2006, 4, e332.
37. Javanbakht, H.; Cen, S.; Musier-Forsyth, K.; Kleiman, L. Correlation between tRNALys3 aminoacylation and its incorporation into HIV-1. J. Biol. Chem. 2002, 277, 17389–17396.
38. Arion, D.; Harada, R.; Li, X.; Wainberg, M.A.; Parniak, M.A. HIV-1 reverse transcriptase shows no specificity for the binding of primer tRNA(Lys3). Biochem. Biophys. Res. Commun. 1996, 225, 839–843.
39. Saadatmand, J.; Kleiman, L. Aspects of HIV-1 assembly that promote primer tRNA(Lys3) annealing to viral RNA.Virus Res. 2012, 169, 340–348.
40. Erikson, E.; Erikson, R.L.; Henry, B.; Pace, N.R. Comparison of oligonucleotides produced by RNase T1 digestion of 7 S RNA from avian and murine oncornaviruses and from uninfected cells. Virology 1973, 53, 40–46.
41. Peters, G.; Harada, F.; Dahlberg, J.E.; Panet, A.; Haseltine, W.A.; Baltimore, D. Low-molecular-weight RNAs of Moloney murine leukemia virus: Identification of the primer for RNA-directed DNA synthesis. J. Virol. 1977, 21, 1031–1041.
42. Sawyer, R.C.; Dahlberg, J.E. Small RNAs of Rous sarcoma virus: Characterization by two-dimensional polyacrylamide gel electrophoresis and fingerprint analysis. J. Virol. 1973, 12, 1226–1237.
43. Walker, T.A.; Pace, N.R.; Erikson, R.L.; Erikson, E.; Behr, F. The 7S RNA common to oncornaviruses and normal cells is associated with polyribosomes. Proc. Natl. Acad. Sci. USA 1974, 71, 3390–3394.
44. Brameier, M.; Ibing, W.; Hofer, K.; Montag, J.; Stahl-Hennig, C.; Motzkus, D. Mapping the small RNA content of simian immunodeficiency virions (SIV). PLoS ONE 2013, 8, e75063.
45. Keene, S.E.; King, S.R.; Telesnitsky, A. 7SL RNA is retained in HIV-1 minimal virus-like particles as an S-domain fragment. J. Virol. 2010, 84, 9070–9077.
46. O’Carroll, I.P.; Crist, R.M.; Mirro, J.; Harvin, D.; Soheilian, F.; Kamata, A.; Nagashima, K.; Rein, A. Functional redundancy in HIV-1 viral particle assembly. J. Virol. 2012, 86, 12991–12996.
47. Walter, P.; Blobel, G. Subcellular distribution of signal recognition particle and 7SL-RNA determined with polypeptide-specific antibodies and complementary DNA probe. J. Cell Biol. 1983, 97, 1693–1699.
48. Elvekrog, M.M.; Walter, P. Dynamics of co-translational protein targeting. Curr. Opin. Chem. Biol. 2015, 29, 79–86.
49. Bradshaw, N.; Neher, S.B.; Booth, D.S.; Walter, P. Signal sequences activate the catalytic switch of SRP RNA. Science 2009, 323, 127–130.
50. Ullu, E.; Tschudi, C. Alu sequences are processed 7SL RNA genes. Nature 1984, 312, 171–172.
51. Kramerov, D.A.; Vassetzky, N.S. Origin and evolution of SINEs in eukaryotic genomes. Heredity (Edinb) 2011, 107, 487–495.
52. Kramerov, D.A.; Vassetzky, N.S. SINEs. Wiley Interdiscip. Rev. RNA 2011, 2, 772–786.
53. Kramerov, D.A.; Vassetzky, N.S. Short retroposons in eukaryotic genomes. Int. Rev. Cytol. 2005, 247, 165–221.
54. Rein, A.; Datta, S.A.; Jones, C.P.; Musier-Forsyth, K. Diverse interactions of retroviral Gag proteins with RNAs. Trends Biochem. Sci. 2011, 36, 373–380.
55. Kutluay, S.B.; Bieniasz, P.D. Analysis of the initiating events in HIV-1 particle assembly and genome packaging. PLoS Pathog. 2010, 6, e1001200.
56. Flynn, J.A.; An, W.; King, S.R.; Telesnitsky, A. Nonrandom dimerization of murine leukemia virus genomic RNAs. J. Virol. 2004, 78, 12129–12139.
57. Ferrer, M.; Clerte, C.; Chamontin, C.; Basyuk, E.; Laine, S.; Hottin, J.; Bertrand, E.; Margeat, E.; Mougel, M. Imaging HIV-1 RNA dimerization in cells by multicolor super-resolution and fluctuation microscopies. Nucleic Acids Res. 2016.
58. Chen, J.; Rahman, S.A.; Nikolaitchik, O.A.; Grunwald, D.; Sardo, L.; Burdick, R.C.; Plisov, S.; Liang, E.; Tai, S.; Pathak, V.K.; et al. 2016. HIV-1 RNA genome dimerizes on the plasma membrane in the presence of Gag protein. Proc. Natl. Acad. Sci. USA 2016, 113, E201–E208.
59. Sim, S.; Wolin, S.L. Emerging roles for the Ro 60-kDa autoantigen in noncoding RNA metabolism. Wiley Interdiscip. Rev. RNA 2011, 2, 686–699.
60. Labbe, J.C.; Hekimi, S.; Rokeach, L.A. The levels of the RoRNP-associated Y RNA are dependent upon the presence of ROP-1, the Caenorhabditis elegans Ro60 protein. Genetics 1999, 151, 143–150.
61. Chen, X.; Smith, J.D.; Shi, H.; Yang, D.D.; Flavell, R.A.; Wolin, S.L. The Ro autoantigen binds misfolded U2 small nuclear RNAs and assists mammalian cell survival after UV irradiation. Curr. Biol. 2003, 13, 2206–2211.
62. Johnson, S.F.; Garcia, E.L.; Summers, M.F.; Telesnitsky, A. Moloney murine leukemia virus genomic RNA packaged in the absence of a full complement of wild type nucleocapsid protein. Virology 2012, 430, 100–109.
63. Didierlaurent, L.; Racine, P.J.; Houzet, L.; Chamontin, C.; Berkhout, B.; Mougel, M. Role of HIV-1 RNA and protein determinants for the selective packaging of spliced and unspliced viral RNA and host U6 and 7SL RNA in virus particles. Nucleic Acids Res. 2011, 39, 8915–8927.
64. Peters, G.; Dahlberg, J.E. RNA-directed DNA synthesis in Moloney murine leukemia virus: Interaction between the primer tRNA and the genome RNA. J. Virol. 1979, 31, 398–407.
65. Ciufo, L.F.; Brown, J.D. Nuclear export of yeast signal recognition particle lacking Srp54p by the Xpo1p/Crm1p NES-dependent pathway. Curr. Biol. 2000, 10, 1256–1264.
66. Politz, J.C.; Yarovoi, S.; Kilroy, S.M.; Gowda, K.; Zwieb, C.; Pederson, T. Signal recognition particle components in the nucleolus. Proc. Natl. Acad. Sci. USA 2000, 97, 55–60.
67. Grosshans, H.; Deinert, K.; Hurt, E.; Simos, G. Biogenesis of the signal recognition particle (SRP) involves import of SRP proteins into the nucleolus, assembly with the SRP-RNA, and Xpo1p-mediated export. J. Cell Biol. 2001, 153, 745–762.
68. Khan, M.A.; Goila-Gaur, R.; Opi, S.; Miyagi, E.; Takeuchi, H.; Kao, S.; Strebel, K. Analysis of the contribution of cellular and viral RNA to the packaging of APOBEC3G into HIV-1 virions. Retrovirology 2007, 4, 48.
69. Zwieb, C.; van Nues, R.W.; Rosenblad, M.A.; Brown, J.D.; Samuelsson, T. A nomenclature for all signal recognition particle RNAs. RNA 2005, 11, 7–13.
70. Engeland, C.E.; Brown, N.P.; Borner, K.; Schumann, M.; Krause, E.; Kaderali, L.; Muller, G.A.; Krausslich, H.G. Proteome analysis of the HIV-1 Gag interactome. Virology 2014, 460, 194–206.
71. Kutluay, S.B.; Zang, T.; Blanco-Melo, D.; Powell, C.; Jannain, D.; Errando, M.; Bieniasz, P.D. Global changes in the RNA binding specificity of HIV-1 gag regulate virion genesis. Cell 2014, 159, 1096–1109.
72. Keene, S.E.; Telesnitsky, A. cis-Acting determinants of 7SL RNA packaging by HIV-1. J. Virol. 2012, 86, 7934–7942.
73. Noltet Hoen, E.N.; Buermans, H.P.; Waasdorp, M.; Stoorvogel, W.; Wauben, M.H.; t Hoen, P.A. Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions. Nucleic Acids Res. 2012, 40, 9272–9285.
74. Chen, P.J.; Cywinski, A.; Taylor, J.M. Reverse transcription of 7S L RNA by an avian retrovirus. J. Virol. 1985, 54, 278–284.
75. Tian, C.; Wang, T.; Zhang, W.; Yu, X.F. Virion packaging determinants and reverse transcription of SRP RNA in HIV-1 particles. Nucleic Acids Res. 2007, 35, 7288–7302.
76. Hopper, A.K. Cellular dynamics of small RNAs. Crit. Rev. Biochem. Mol. Biol. 2006, 41, 3–19.
77. Tanese, N.; Telesnitsky, A.; Goff, S.P. Abortive reverse transcription by mutants of Moloney murine leukemia virus deficient in the reverse transcriptase-associated RNase H function. J. Virol. 1991, 65, 4387–4397.
78. Hajjar, A.M.; Linial, M.L. A model system for nonhomologous recombination between retroviral and cellular RNA. J. Virol. 1993, 67, 3845–3853.
79. Stuhlmann, H.; Berg, P. Homologous recombination of copackaged retrovirus RNAs during reverse transcription. J. Virol. 1992, 66, 2378–2388.
80. Linial, M. Creation of a processed pseudogene by retroviral infection. Cell 1987, 49, 93–102.
81. Hajjar, A.M.; Linial, M.L. Characterization of a unique retroviral recombinant containing 7S L sequences. J. Virol. 1993,67, 7677–7679.
82. Onafuwa-Nuga, A.; Telesnitsky, A. The remarkable frequency of human immunodeficiency virus type 1 genetic recombination. Microbiol. Mol. Biol. Rev. 2009, 73, 451–480.
83. Sugden, B. How some retroviruses got their oncogenes. Trends Biochem. Sci. 1993, 18, 233–235.
84. Sun, G.; O’Neil, P.K.; Yu, H.; Ron, Y.; Preston, B.D.; Dougherty, J.P. Transduction of cellular sequence by a human immunodeficiency virus type 1-derived vector. J. Virol. 2001, 75, 11902–11906.
85. Duggal, N.K.; Goo, L.; King, S.R.; Telesnitsky, A. Effects of identity minimization on Moloney murine leukemia virus template recognition and frequent tertiary template-directed insertions during nonhomologous recombination. J. Virol. 2007, 81, 12156–12168.
86. Mikkelsen, J.G.; Pedersen, F.S. Genetic reassortment and patch repair by recombination in retroviruses. J. Biomed. Sci.2000, 7, 77–99.
87. Zhang, J.; Temin, H.M. Rate and mechanism of nonhomologous recombination during a single cycle of retroviral replication. Science 1993, 259, 234–238.
88. Takebe, Y.; Telesnitsky, A. Evidence for the acquisition of multi-drug resistance in an HIV-1 clinical isolate via human sequence transduction. Virology 2006, 351, 1–6.
89. Megens, S.; Vaira, D.; De Baets, G.; Dekeersmaeker, N.; Schrooten, Y.; Li, G.; Schymkowitz, J.; Rousseau, F.; Vandamme, A.M.; Moutschen, M.; et al. Horizontal gene transfer from human host to HIV-1 reverse transcriptase confers drug resistance and partly compensates for replication deficits. Virology 2014, 456, 310–318.
90. Muriaux, D.; Mirro, J.; Harvin, D.; Rein, A. RNA is a structural element in retrovirus particles. Proc. Natl. Acad. Sci. USA 2001, 98, 5246–5251.
91. Campbell, S.; Fisher, R.J.; Towler, E.M.; Fox, S.; Issaq, H.J.; Wolfe, T.; Phillips, L.R.; Rein, A. Modulation of HIV-like particle assembly in vitro by inositol phosphates. Proc. Natl. Acad. Sci. USA 2001, 98, 10875–10879.
92. Ott, D.E.; Coren, L.V.; Chertova, E.N.; Gagliardi, T.D.; Nagashima, K.; Sowder, R.C.; Poon, D.T., 2nd; Gorelick, R.J. Elimination of protease activity restores efficient virion production to a human immunodeficiency virus type 1 nucleocapsid deletion mutant. J. Virol. 2003, 77, 5547–5556.
93. Ott, D.E.; Coren, L.V.; Shatzer, T. The nucleocapsid region of human immunodeficiency virus type 1 Gag assists in the coordination of assembly and Gag processing: Role for RNA-Gag binding in the early stages of assembly. J. Virol.2009, 83, 7718–7727.
94. Campbell, S.; Rein, A. In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain. J. Virol. 1999, 73, 2270–2279.
95. Campbell, S.; Vogt, V.M. Self-assembly in vitro of purified CA-NC proteins from Rous sarcoma virus and human immunodeficiency virus type 1. J. Virol. 1995, 69, 6487–6497.
96. Crist, R.M.; Datta, S.A.; Stephen, A.G.; Soheilian, F.; Mirro, J.; Fisher, R.J.; Nagashima, K.; Rein, A. Assembly properties of human immunodeficiency virus type 1 Gag-leucine zipper chimeras: Implications for retrovirus assembly. J. Virol. 2009, 83, 2216–2225.
97. Jouvenet, N.; Simon, S.M.; Bieniasz, P.D. Imaging the interaction of HIV-1 genomes and Gag during assembly of individual viral particles. Proc. Natl. Acad. Sci. USA 2009, 106, 19114–19119.
98. Wang, T.; Tian, C.; Zhang, W.; Luo, K.; Sarkis, P.T.; Yu, L.; Liu, B.; Yu, Y.; Yu, X.F. 7SL RNA mediates virion packaging of the antiviral cytidine deaminase APOBEC3G. J. Virol. 2007, 81, 13112–13124.
99. Bach, D.; Peddi, S.; Mangeat, B.; Lakkaraju, A.; Strub, K.; Trono, D. Characterization of APOBEC3G binding to 7SL RNA. Retrovirology 2008, 5, 54.
100. Apolonia, L.; Schulz, R.; Curk, T.; Rocha, P.; Swanson, C.M.; Schaller, T.; Ule, J.; Malim, M.H. Promiscuous RNA binding ensures effective encapsidation of APOBEC3 proteins by HIV-1. PLoS Pathog. 2015, 11, e1004609.
101. Ono, A.; Ablan, S.D.; Lockett, S.J.; Nagashima, K.; Freed, E.O. Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 Gag targeting to the plasma membrane. Proc. Natl. Acad. Sci. USA 2004, 101, 14889–14894.
102. Spearman, P.; Wang, J.J.; Vander Heyden, N.; Ratner, L. Identification of human immunodeficiency virus type 1 Gag protein domains essential to membrane binding and particle assembly. J. Virol. 1994, 68, 3232–3242.
103. Rhee, S.S.; Hunter, E. Amino acid substitutions within the matrix protein of type D retroviruses affect assembly, transport and membrane association of a capsid. EMBO J. 1991, 10, 535–546.
104. Chukkapalli, V.; Hogue, I.B.; Boyko, V.; Hu, W.S.; Ono, A. Interaction between the human immunodeficiency virus type 1 Gag matrix domain and phosphatidylinositol-(4,5)-bisphosphate is essential for efficient gag membrane binding. J. Virol. 2008, 82, 2405–2417.
105. Chukkapalli, V.; Oh, S.J.; Ono, A. Opposing mechanisms involving RNA and lipids regulate HIV-1 Gag membrane binding through the highly basic region of the matrix domain. Proc. Natl. Acad. Sci. USA 2010, 107, 1600–1605.
106. Chukkapalli, V.; Inlora, J.; Todd, G.C.; Ono, A. Evidence in support of RNA-mediated inhibition of phosphatidylserine-dependent HIV-1 Gag membrane binding in cells. J. Virol. 2013, 87, 7155–7159.
107. Ono, A.; Freed, E.O. Cell-type-dependent targeting of human immunodeficiency virus type 1 assembly to the plasma membrane and the multivesicular body. J. Virol. 2004, 78, 1552–1563.
108. Reed, J.C.; Molter, B.; Geary, C.D.; McNevin, J.; McElrath, J.; Giri, S.; Klein, K.C.; Lingappa, J.R. HIV-1 Gag co-opts a cellular complex containing DDX6, a helicase that facilitates capsid assembly. J. Cell Biol. 2012, 198, 439–456.
109. Robinson, B.A.; Reed, J.C.; Geary, C.D.; Swain, J.V.; Lingappa, J.R. A temporospatial map that defines specific steps at which critical surfaces in the Gag MA and CA domains act during immature HIV-1 capsid assembly in cells. J. Virol.2014, 88, 5718–5741.
110. Fassati, A.; Goff, S.P. Characterization of intracellular reverse transcription complexes of human immunodeficiency virus type 1. J. Virol. 2001, 75, 3626–3635.
111. Gao, G.; Goff, S.P. Somatic cell mutants resistant to retrovirus replication: Intracellular blocks during the early stages of infection. Mol. Biol. Cell 1999, 10, 1705–1717.
112. Gao, G.; Goff, S.P. Isolation of suppressor genes that restore retrovirus susceptibility to a virus-resistant cell line. Retrovirology 2004, 1, 30.
113. Zennou, V.; Perez-Caballero, D.; Gottlinger, H.; Bieniasz, P.D. APOBEC3G incorporation into human immunodeficiency virus type 1 particles. J. Virol. 2004, 78, 12058–12061.
114. Burnett, A.; Spearman, P. APOBEC3G multimers are recruited to the plasma membrane for packaging into human immunodeficiency virus type 1 virus-like particles in an RNA-dependent process requiring the NC basic linker. J. Virol. 2007, 81, 5000–5013.
115. Bogerd, H.P.; Cullen, B.R. Single-stranded RNA facilitates nucleocapsid: APOBEC3G complex formation. RNA 2008,14, 1228–1236.
116. Doyle, T.; Goujon, C.; Malim, M.H. HIV-1 and interferons: Who’s interfering with whom? Nat. Rev. Microbiol. 2015, 13, 403–413.
117. Gao, D.; Wu, J.; Wu, Y.T.; Du, F.; Aroh, C.; Yan, N.; Sun, L.; Chen, Z.J. Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 2013, 341, 903–906.
118. Compton, A.A.; Bruel, T.; Porrot, F.; Mallet, A.; Sachse, M.; Euvrard, M.; Liang, C.; Casartelli, N.; Schwartz, O. IFITM proteins incorporated into HIV-1 virions impair viral fusion and spread. Cell Host Microbe 2014, 16, 736–747.
119. Galloway, N.L.; Doitsh, G.; Monroe, K.M.; Yang, Z.; Munoz-Arias, I.; Levy, D.N.; Greene, W.C. Cell-to-Cell Transmission of HIV-1 Is Required to Trigger Pyroptotic Death of Lymphoid-Tissue-Derived CD4 T Cells. Cell Rep.2015, 12, 1555–1563.
120. Coffin, J.M. Structure, replication, and recombination of retrovirus genomes: Some unifying hypotheses. J. Gen. Virol.1979, 42, 1–26.
121. Beignon, A.S.; McKenna, K.; Skoberne, M.; Manches, O.; DaSilva, I.; Kavanagh, D.G.; Larsson, M.; Gorelick, R.J.; Lifson, J.D.; Bhardwaj, N. Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions. J. Clin. Investig. 2005, 115, 3265–3275.
122. Kane, M.; Case, L.K.; Wang, C.; Yurkovetskiy, L.; Dikiy, S.; Golovkina, T.V. Innate immune sensing of retroviral infection via Toll-like receptor 7 occurs upon viral entry. Immunity 2011, 35, 135–145.
123. Green, N.M.; Moody, K.S.; Debatis, M.; Marshak-Rothstein, A. Activation of autoreactive B cells by endogenous TLR7 and TLR3 RNA ligands. J. Biol. Chem. 2012, 287, 39789–39799.
124. Huang, Y.; Kong, W.P.; Nabel, G.J. Human immunodeficiency virus type 1-specific immunity after genetic immunization is enhanced by modification of Gag and Pol expression. J. Virol. 2001, 75, 4947–4951.
125. Keene, S.E. The Packaging of 7SL RNA by HIV-1. Ph.D. Thesis, University of Michigan, Ann Arbor, MI, USA, 2012.