Fate of HIV-1 cDNA intermediates during reverse transcription is dictated by transcription initiation site of virus genomic RNA

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Masuda, Takao ^a   Sato, Yoko ^a   Huang, Yu Lun ^a   Koi, Satoshi ^a   Takahata, Tatsuro ^a   Hasegawa, Atsuhiko ^a   Kawai, Gota ^b   Kannagi, Mari ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b CHIBA INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; NUCLEOCAPSID PROTEIN; VIRUS RNA;

GENETICS; HEK293 CELL LINE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; PATHOGENICITY; REVERSE TRANSCRIPTION; TRANSCRIPTION INITIATION SITE; VIROLOGY;

DNA, COMPLEMENTARY; HEK293 CELLS; HIV-1; HUMANS; NUCLEOCAPSID PROTEINS; REVERSE TRANSCRIPTION; RNA, VIRAL; TRANSCRIPTION INITIATION SITE;

EID: 84949293481     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep17680     Document Type: Article

References (50)

1. Ilina, T., Labarge, K., Sarafianos, S. G., Ishima, R. & Parniak, M. A. Inhibitors of HIV-1 Reverse Transcriptase-Associated Ribonuclease H Activity. Biology 1, 521-541 (2012).
2. Cook, P. R. A model for reverse transcription by a dimeric enzyme. The Journal of general virology 74, 691-697 (1993).
3. Hizi, A., McGill, C. & Hughes, S. H. Expression of soluble, enzymatically active, human immunodeficiency virus reverse transcriptase in Escherichia coli and analysis of mutants. Proc Natl Acad Sci USA 85, 1218-1222 (1988).
4. Jacobo-Molina, A. et al. Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with doublestranded DNA at 3.0 A resolution shows bent DNA. Proc Natl Acad Sci USA 90, 6320-6324 (1993).
5. Sevilya, Z., Loya, S., Hughes, S. H. & Hizi, A. The ribonuclease H activity of the reverse transcriptases of human immunodeficiency viruses type 1 and type 2 is affected by the thumb subdomain of the small protein subunits. J Mol Biol 311, 957-971 (2001).
6. Sevilya, Z., Loya, S., Adir, N. & Hizi, A. The ribonuclease H activity of the reverse transcriptases of human immunodeficiency viruses type 1 and type 2 is modulated by residue 294 of the small subunit. Nucleic Acids Res 31, 1481-1487 (2003).
7. Chung, S. et al. Examining the role of the HIV-1 reverse transcriptase p51 subunit in positioning and hydrolysis of RNA/DNA hybrids. J Biol Chem 288, 16177-16184 (2013).
8. Kohlstaedt, L. A. & Steitz, T. A. Reverse transcriptase of human immunodeficiency virus can use either human tRNA(3Lys) or Escherichia coli tRNA(2Gln) as a primer in an in vitro primer-utilization assay. Proc Natl Acad Sci USA 89, 9652-9656 (1992).
9. Jiang, M. et al. Identification of tRNAs incorporated into wild-type and mutant human immunodeficiency virus type 1. J Virol 67, 3246-3253 (1993).
10. Isel, C. et al. Specific initiation and switch to elongation of human immunodeficiency virus type 1 reverse transcription require the post-transcriptional modifications of primer tRNA3Lys. The EMBO journal 15, 917-924 (1996).
11. Pavon-Eternod, M., Wei, M., Pan, T. & Kleiman, L. Profiling non-lysyl tRNAs in HIV-1. RNA 16, 267-273 (2010).
12. Basu, V. P. et al. Strand transfer events during HIV-1 reverse transcription. Virus research 134, 19-38 (2008).
13. Herschhorn, A. & Hizi, A. Retroviral reverse transcriptases. Cellular and molecular life sciences: CMLS 67, 2717-2747 (2010).
14. Hu, W. S. & Hughes, S. H. HIV-1 reverse transcription. Cold Spring Harbor perspectives in medicine 2, (2012).
15. Guo, J., Henderson, L. E., Bess, J., Kane, B. & Levin, J. G. Human immunodeficiency virus type 1 nucleocapsid protein promotes efficient strand transfer and specific viral DNA synthesis by inhibiting TAR-dependent self-priming from minus-strand strongstop DNA. J Virol 71, 5178-5188 (1997).
16. Godet, J. et al. Site-selective probing of cTAR destabilization highlights the necessary plasticity of the HIV-1 nucleocapsid protein to chaperone the first strand transfer. Nucleic Acids Res 41, 5036-5048 (2013).
17. Levin, J. G., Mitra, M., Mascarenhas, A. & Musier-Forsyth, K. Role of HIV-1 nucleocapsid protein in HIV-1 reverse transcription. RNA biology 7, 754-774 (2010).
18. Doitsh, G. et al. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 505, 509-514 (2014).
19. Monroe, K. M. et al. IFI16 DNA sensor is required for death of lymphoid CD4 T cells abortively infected with HIV. Science 343, 428-432 (2014).
20. Menees, T. M., Muller, B. & Krausslich, H. G. The major 5′ end of HIV type 1 RNA corresponds to G456. AIDS Res Hum Retroviruses 23, (2007).
21. Muesing, M. A. et al. Nucleic acid structure and expression of the human AIDS/lymphadenopathy retrovirus. Nature 313, 450-458 (1985).
22. Starcich, B. et al. Characterization of long terminal repeat sequences of HTLV-III. Science 227, 538-540 (1985).
23. Kannagi, M. et al. Interference with human immunodeficiency virus (HIV) replication by CD8+ T cells in peripheral blood leukocytes of asymptomatic HIV carriers in vitro. J Virol 64, 3399-3406 (1990).
24. Masuda, T., Planelles, V., Krogstad, P. & Chen, I. S. Genetic analysis of human immunodeficiency virus type 1 integrase and the U3 att site: unusual phenotype of mutants in the zinc finger-like domain. J Virol 69, 6687-6696 (1995).
25. Yee, J. K., Friedmann, T. & Burns, J. C. Generation of high-titer pseudotyped retroviral vectors with very broad host range. Methods Cell Biol 43 Pt A, 99-112 (1994).
26. Arai, T. et al. A new system for stringent, high-titer vesicular stomatitis virus G protein-pseudotyped retrovirus vector induction by introduction of Cre recombinase into stable prepackaging cell lines. J Virol 72, 1115-1121 (1998).
27. Ohishi, M., Shioda, T. & Sakuragi, J. Retro-transduction by virus pseudotyped with glycoprotein of vesicular stomatitis virus. Virology 362, 131-138 (2007).
28. Miyoshi, H., Blomer, U., Takahashi, M., Gage, F. H. & Verma, I. M. Development of a self-inactivating lentivirus vector. J Virol 72, 8150-8157 (1998).
29. Takahashi, K. et al. Structural requirement for the two-step dimerization of human immunodeficiency virus type 1 genome. RNA 6, 96-102 (2000).
30. Oz-Gleenberg, I., Herschhorn, A. & Hizi, A. Reverse transcriptases can clamp together nucleic acids strands with two complementary bases at their 3′-termini for initiating DNA synthesis. Nucleic Acids Res 39, 1042-1053 (2011).
31. Berkhout, B., Vastenhouw, N. L., Klasens, B. I. & Huthoff, H. Structural features in the HIV-1 repeat region facilitate strand transfer during reverse transcription. RNA 7, 1097-1114 (2001).
32. Balakrishnan, M., Roques, B. P., Fay, P. J. & Bambara, R. A. Template dimerization promotes an acceptor invasion-induced transfer mechanism during human immunodeficiency virus type 1 minus-strand synthesis. J Virol 77, 4710-4721 (2003).
33. Beerens, N. & Kjems, J. Circularization of the HIV-1 genome facilitates strand transfer during reverse transcription. RNA 16, 1226-1235 (2010).
34. Sato, K., Hamada, M., Asai, K. & Mituyama, T. CENTROIDFOLD: a web server for RNA secondary structure prediction. Nucleic Acids Res 37, W277-280 (2009).
35. Sakuragi, J., Ueda, S., Iwamoto, A. & Shioda, T. Possible role of dimerization in human immunodeficiency virus type 1 genome RNA packaging. J Virol 77, 4060-4069 (2003).
36. Williams, M. C. et al. Mechanism for nucleic acid chaperone activity of HIV-1 nucleocapsid protein revealed by single molecule stretching. Proc Natl Acad Sci USA 98, 6121-6126 (2001).
37. Vo, M. N., Barany, G., Rouzina, I. & Musier-Forsyth, K. HIV-1 nucleocapsid protein switches the pathway of transactivation response element RNA/DNA annealing from loop-loop "kissing" to "zipper". J Mol Biol 386, 789-801 (2009).
38. Wu, H. et al. Differential contribution of basic residues to HIV-1 nucleocapsid protein's nucleic acid chaperone function and retroviral replication. Nucleic Acids Res 42, 2525-2537 (2014).
39. You, J. C. & McHenry, C. S. HIV nucleocapsid protein. Expression in Escherichia coli, purification, and characterization. J Biol Chem 268, 16519-16527 (1993).
40. Wilkinson, K. A. et al. High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS biology 6, e96 (2008).
41. Cen, S. et al. Incorporation of lysyl-tRNA synthetase into human immunodeficiency virus type 1. J Virol 75, 5043-5048 (2001).
42. Jones, C. P., Saadatmand, J., Kleiman, L. & Musier-Forsyth, K. Molecular mimicry of human tRNALys anti-codon domain by HIV-1 RNA genome facilitates tRNA primer annealing. RNA 19, 219-229 (2013).
43. Le Grice, S. F. "In the beginning": initiation of minus strand DNA synthesis in retroviruses and LTR-containing retrotransposons. Biochemistry 42, 14349-14355 (2003).
44. D'Souza, V. & Summers, M. F. How retroviruses select their genomes. Nature reviews. Microbiology 3, 643-655 (2005).
45. Nishitsuji, H. et al. Augmentation of reverse transcription by integrase through an interaction with host factor, SIP1/Gemin2 Is critical for HIV-1 infection. PLoS One 4, e7825 (2009).
46. Hamamoto, S., Nishitsuji, H., Amagasa, T., Kannagi, M. & Masuda, T. Identification of a Novel Human Immunodeficiency Virus Type 1 Integrase Interactor, Gemin2, That Facilitates Efficient Viral cDNA Synthesis In Vivo. J Virol 80, 5670-5677 (2006).
47. Warren, K. et al. Eukaryotic elongation factor 1 complex subunits are critical HIV-1 reverse transcription cofactors. Proc Natl Acad Sci USA 109, 9587-9592 (2012).
48. Ikeda, T. et al. Evaluation of the functional involvement of human immunodeficiency virus type 1 integrase in nuclear import of viral cDNA during acute infection. J Virol 78, 11563-11573 (2004).
49. Zack, J. A. et al. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 61, 213-222 (1990).
50. Chattopadhyay, D. et al. Purification and characterization of heterodimeric human immunodeficiency virus type 1 (HIV-1) reverse transcriptase produced by in vitro processing of p66 with recombinant HIV-1 protease. J Biol Chem 267, 14227-14232 (1992).