Molecular mimicry of human tRNALys anti-codon domain by HIV-1 RNA genome facilitates tRNA primer annealing

RNA

Volumn 19, Issue 2, 2013, Pages 219-229

  Jones, Christopher P ^a   Saadatmand, Jenan ^b   Kleiman, Lawrence ^b   Musier Forsyth, Karin ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Lysyl tRNA synthetase; Primer placement; Reverse transcription; TRNA anti codon like element

Indexed keywords

GAG PROTEIN; GAGPOL PROTEIN; LYSINE TRANSFER RNA; PRIMER RNA; RNA BINDING PROTEIN; TRANSFER RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

5' UNTRANSLATED REGION; ANTICODON; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DNA PACKAGING; GEL MOBILITY SHIFT ASSAY; GENE MUTATION; GENE SEQUENCE; GENOME ANALYSIS; HOST CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; MOLECULAR MIMICRY; PRIORITY JOURNAL; PROTEIN DOMAIN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA BINDING; VIRION; VIRUS NUCLEOCAPSID;

BASE PAIRING; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GENOME, VIRAL; HIV ENHANCER; HIV-1; HUMANS; LYSINE-TRNA LIGASE; MOLECULAR MIMICRY; MUTATION; PROTEIN STRUCTURE, TERTIARY; RNA; RNA, TRANSFER, LYS; RNA, VIRAL; VIRUS ASSEMBLY; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84872577495     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.036681.112     Document Type: Article

References (69)

1. Amarasinghe GK, De Guzman RN, Turner RB, Summers MF. 2000. NMR structure of stem-loop SL2 of the HIV-1 Ψ RNA packaging signal reveals a novel A-U-A base-triple platform. J Mol Biol 299: 145-156.
2. Andreev DE, Hirnet J, Terenin IM, Dmitriev SE, Niepmann M, Shatsky IN. 2012. Glycyl-tRNA synthetase specifically binds to the poliovirus IRES to activate translation initiation. Nucleic Acids Res 40: 5602-5614.
3. Arts EJ, Stetor SR, Li X, Rausch JW, Howard KJ, Ehresmann B, North TW, Wohrl BM, Goody RS, Wainberg MA, et al. 1996. Initiation of (-) strand DNA synthesis from tRNA3 Lys on lentiviral RNAs: Implications of specific HIV-1 RNA-tRNA3 Lys interactions inhibiting primer utilization by retroviral reverse transcriptases. Proc Natl Acad Sci 93: 10063-10068.
4. Balvay L, Soto Rifo R, Ricci EP, Decimo D, Ohlmann T. 2009. Structural and functional diversity of viral IRESes. Biochim Biophys Acta 1789: 542-557.
5. Beerens N, Groot F, Berkhout B. 2001. Initiation of HIV-1 reverse transcription is regulated by a primer activation signal. J Biol Chem 276: 31247-31256.
6. Berkhout B, Arts K, Abbink TE. 2011. Ribosomal scanning on the 5'-untranslated region of the human immunodeficiency virus RNA genome. Nucleic Acids Res 39: 5232-5244.
7. Bolinger C, Boris-Lawrie K. 2009. Mechanisms employed by retroviruses to exploit host factors for translational control of a complicated proteome. Retrovirology 6: 8.
8. Brasey A, Lopez-Lastra M, Ohlmann T, Beerens N, Berkhout B, Darlix JL, Sonenberg N. 2003. The leader of human immunodeficiency virus type 1 genomic RNA harbors an internal ribosome entry segment that is active during the G2/M phase of the cell cycle. J Virol 77: 3939-3949.
9. Brule F, Bec G, Keith G, Le Grice SF, Roques BP, Ehresmann B, Ehresmann C, Marquet R. 2000. In vitro evidence for the interaction of tRNA3 Lys with U3 during the first strand transfer of HIV-1 reverse transcription. Nucleic Acids Res 28: 634-640.
10. Cen S, Khorchid A, Javanbakht H, Gabor J, Stello T, Shiba K, Musier- Forsyth K, Kleiman L. 2001. Incorporation of lysyl-tRNA synthetase into human immunodeficiency virus type 1. J Virol 75: 5043-5048.
11. Cen S, Javanbakht H, Kim S, Shiba K, Craven R, Rein A, Ewalt K, Schimmel P, Musier-Forsyth K, Kleiman L. 2002. Retrovirus-specific packaging of aminoacyl-tRNA synthetases with cognate primer tRNAs. J Virol 76: 13111-13115.
12. Coffin JM, Hughes SH, Varmus H. 1997. Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
13. Costantino DA, Pfingsten JS, Rambo RP, Kieft JS. 2008. tRNA-mRNA mimicry drives translation initiation from a viral IRES. Nat Struct Mol Biol 15: 57-64.
14. Damgaard CK, Dyhr-Mikkelsen H, Kjems J. 1998. Mapping the RNA binding sites for human immunodeficiency virus type-1 gag and NC proteins within the complete HIV-1 and -2 untranslated leader regions. Nucleic Acids Res 26: 3667-3676.
15. De Guzman RN, Wu ZR, Stalling CC, Pappalardo L, Borer PN, Summers MF. 1998. Structure of the HIV-1 nucleocapsid protein bound to the SL3 Ψ-RNA recognition element. Science 279: 384-388.
16. Dreher TW. 2009. Role of tRNA-like structures in controlling plant virus replication. Virus Res 139: 217-229.
17. Feng YX, Campbell S, Harvin D, Ehresmann B, Ehresmann C, Rein A. 1999. The human immunodeficiency virus type 1 Gag polyprotein has nucleic acid chaperone activity: Possible role in dimerization of genomic RNA and placement of tRNA on the primer binding site. J Virol 73: 4251-4256.
18. Fersht AR, Ashford JS, Bruton CJ, Jakes R, Koch GL, Hartley BS. 1975. Active site titration and aminoacyl adenylate binding stoichiometry of aminoacyl-tRNA synthetases. Biochemistry 14: 1-4.
19. Francin M, Mirande M. 2006. Identity elements for specific aminoacylation of a tRNA by mammalian lysyl-tRNA synthetase bearing a nonspecific tRNA-interacting factor. Biochemistry 45: 10153-10160.
20. Francin M, Kaminska M, Kerjan P, Mirande M. 2002. The N-terminal domain of mammalian lysyl-tRNA synthetase is a functional tRNA-binding domain. J Biol Chem 277: 1762-1769.
21. Gabor J, Cen S, Javanbakht H, Niu M, Kleiman L. 2002. Effect of altering the tRNALys3 concentration in human immunodeficiency virus type 1 upon its annealing to viral RNA, GagPol incorporation, and viral infectivity. J Virol 76: 9096-9102.
22. Gao F, Robertson DL, Carruthers CD, Li Y, Bailes E, Kostrikis LG, Salminen MO, Bibollet-Ruche F, Peeters M, Ho DD, et al. 1998. An isolate of human immunodeficiency virus type 1 originally classified as subtype I represents a complex mosaic comprising three different group M subtypes (A, G, and I). J Virol 72: 10234-10241.
23. Gao F, Kasprzak W, Stupina VA, Shapiro BA, Simon AE. 2012. A ribosome- binding, 3' translational enhancer has a T-shaped structure and engages in a long-distance RNA-RNA interaction. J Virol 86: 9828-9842.
24. Gendron K, Ferbeyre G, Heveker N, Brakier-Gingras L. 2011. The activity of the HIV-1 IRES is stimulated by oxidative stress and controlled by a negative regulatory element. Nucleic Acids Res 39: 902-912.
25. Goldschmidt V, Paillart JC, Rigourd M, Ehresmann B, Aubertin AM, Ehresmann C, Marquet R. 2004. Structural variability of the initiation complex of HIV-1 reverse transcription. J Biol Chem 279: 35923-35931.
26. Guo F, Cen S, Niu M, Javanbakht H, Kleiman L. 2003. Specific inhibition of the synthesis of human lysyl-tRNA synthetase results in decreases in tRNALys incorporation, tRNA3 Lys annealing to viral RNA, and viral infectivity in human immunodeficiency virus type 1. J Virol 77: 9817-9822.
27. Guo F, Gabor J, Cen S, Hu K, Mouland AJ, Kleiman L. 2005. Inhibition of cellular HIV-1 protease activity by lysyl-tRNA synthetase. J Biol Chem 280: 26018-26023.
28. Guo F, Saadatmand J, Niu M, Kleiman L. 2009. Roles of Gag and NCp7 in facilitating tRNALys3 annealing to viral RNA in human immunodeficiency virus type 1. J Virol 83: 8099-8107.
29. Hammond JA, Rambo RP, Filbin ME, Kieft JS. 2009. Comparison and functional implications of the 3D architectures of viral tRNA-like structures. RNA 15: 294-307.
30. Heacock D, Forsyth C, Shiba K, Musier-Forsyth K. 1996. Synthesis and aminoacyl-tRNA synthetase inhibitory activity of prolyl adenylate analogs. Bioorg Chem 24: 273-289.
31. Huang Y, Mak J, Cao Q, Li Z, Wainberg MA, Kleiman L. 1994. Incorporation of excess wild type and mutant tRNALys3 into HIV- 1. J Virol 68: 7676-7683.
32. Huang Y, Shalom A, Li Z, Wang J, Mak J, Wainberg MA, Kleiman L. 1996. Effects of modifying the tRNALys3 anticodon on the initiation of Human Immunodeficiency Virus Type 1 reverse transcription. J Virol 70: 4700-4706.
33. Huang Y, Wang J, Shalom A, Li Z, Khorchid A, Wainberg MA, Kleiman L. 1997. Primer tRNA3 Lys on the viral genome exists in unextended and two-base extended forms within mature human immunodeficiency virus type 1. J Virol 71: 726-728.
34. Isel C, Marquet R, Keith G, Ehresmann C, Ehresmann B. 1993. Modified nucleotides of tRNA3 Lys modulate primer/template looploop interaction in the initiation complex of HIV-1 reverse transcription. J Biol Chem 268: 25269-25272.
35. Isel C, Ehresmann C, Keith G, Ehresmann B, Marquet R. 1995. Initiation of reverse transcription of HIV-1: Secondary structure of the HIV-1 RNA/tRNA3 Lys (template/primer). J Mol Biol 247: 236-250.
36. Iwatani Y, Rosen AE, Guo J, Musier-Forsyth K, Levin JG. 2003. Efficient initiation of HIV-1 reverse transcription in vitro. Requirement for RNA sequences downstream of the primer binding site abrogated by nucleocapsid protein-dependent primer-template interactions. J Biol Chem 278: 14185-14195.
37. Javanbakht H, Cen S, Musier-Forsyth K, Kleiman L. 2002. Correlation between tRNALys3 aminoacylation and its incorporation into HIV- 1. J Biol Chem 277: 17389-17396.
38. Javanbakht H, Halwani R, Cen S, Saadatmand J, Musier-Forsyth K, Gottlinger H, Kleiman L. 2003. The interaction between HIV-1 Gag and human lysyl-tRNA synthetase during viral assembly. J Biol Chem 278: 27644-27651.
39. Jiang M, Mak J, Ladha A, Cohen E, Klein M, Rovinski B, Kleiman L. 1993. Identification of tRNAs incorporated into wild-type and mutant human immunodeficiency virus type 1. J Virol 67: 3246-3253.
40. Jones CP, Datta SA, Rein A, Rouzina I, Musier-Forsyth K. 2011. Matrix domain modulates HIV-1 Gag's nucleic acid chaperone activity via inositol phosphate binding. J Virol 85: 1594-1603.
41. Khorchid A, Javanbakht H, Wise S, Halwani R, Parniak MA, Wainberg MA, Kleiman L. 2000. Sequences within Pr160gag-pol affecting the selective packaging of primer tRNALys3 into HIV-1. J Mol Biol 299: 17-26.
42. Kim S, You S, Hwang D. 2011. Aminoacyl-tRNA synthetases and tumorigenesis: More than housekeeping. Nat Rev Cancer 11: 708-718.
43. Kleiman L, Jones CP, Musier-Forsyth K. 2010. Formation of the tRNALys packaging complex in HIV-1. FEBS Lett 584: 359-365.
44. Kobbi L, Octobre G, Dias J, Comisso M, Mirande M. 2011. Association of mitochondrial lysyl-tRNA synthetase with HIV-1 GagPol involves catalytic domain of the synthetase and transframe and integrase domains of Pol. J Mol Biol 410: 875-886.
45. Kovaleski BJ, Kennedy R, Khorchid A, Kleiman L, Matsuo H, Musier- Forsyth K. 2007. Critical role of helix 4 of HIV-1 capsid C-terminal domain in interactions with human lysyl-tRNA synthetase. J Biol Chem 282: 32274-32279.
46. Li M, Kao E, Gao X, Sandig H, Limmer K, Pavon-Eternod M, Jones TE, Landry S, Pan T, Weitzman MD, et al. 2012. Codon-usage-based inhibition of HIV protein synthesis by human schlafen 11. Nature 491: 125-128.
47. McBride MS, Panganiban AT. 1996. The human immunodeficiency virus type 1 encapsidation site is a multipartite RNA element composed of functional hairpin structures. J Virol 70: 2963-2973.
48. Miele G, Mouland A, Harrison GP, Cohen E, Lever AM. 1996. The human immunodeficiency virus type 1 5' packaging signal structure affects translation but does not function as an internal ribosome entry site structure. J Virol 70: 944-951.
49. Milligan JF, Groebe DR, Witherell GW, Uhlenbeck OC. 1987. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res 15: 8783-8798.
50. Nechushtan H, Kim S, Kay G, Razin E. 2009. Chapter 1: The physiological role of lysyl tRNA synthetase in the immune system. Adv Immunol 103: 1-27.
51. Pagano JM, Farley BM, McCoig LM, Ryder SP. 2007. Molecular basis of RNA recognition by the embryonic polarity determinant MEX-5. J Biol Chem 282: 8883-8894.
52. Paillart JC, Marquet R, Skripkin E, Ehresmann B, Ehresmann C. 1994. Mutational analysis of the bipartite dimer linkage structure of human immunodeficiency virus type 1 genomic RNA. J Biol Chem 269: 27486-27493.
53. Pavon-Eternod M, Wei M, Pan T, Kleiman L. 2010. Profiling non-lysyl tRNAs in HIV-1. RNA 16: 267-273.
54. Piekna-Przybylska D, DiChiacchio L, Mathews DH, Bambara RA. 2010. A sequence similar to tRNA3 Lys gene is embedded in HIV-1 U3-R and promotes minus-strand transfer. Nat Struct Mol Biol 17: 83-89.
55. Puglisi EV, Puglisi JD. 1998. HIV-1 A-rich RNA loop mimics the tRNA anticodon structure. Nat Struct Biol 5: 1033-1036.
56. Roldan A, Warren OU, Russell RS, Liang C, Wainberg MA. 2005. A HIV-1 minimal gag protein is superior to nucleocapsid at in vitro annealing and exhibits multimerization-induced inhibition of reverse transcription. J Biol Chem 280: 17488-17496.
57. Saadatmand J, Kleiman L. 2012. Aspects of HIV-1 assembly that promote primer tRNALys3 annealing to viral RNA. Virus Res 169: 340-348.
58. Saadatmand J, Guo F, Cen S, Niu M, Kleiman L. 2008. Interactions of reverse transcriptase sequences in Pol with Gag and LysRS in the HIV-1 tRNALys3 packaging/annealing complex. Virology 380: 109-117.
59. Shiba K, Stello T, Motegi H, Noda T, Musier-Forsyth K, Schimmel P. 1997. Human lysyl-tRNA synthetase accepts nucleotide 73 variants and rescues Escherichia coli double-defective mutant. J Biol Chem 272: 22809-22816.
60. Song M, Balakrishnan M, Gorelick RJ, Bambara RA. 2009. A succession of mechanisms stimulate efficient reconstituted HIV-1 minus strand strong stop DNA transfer. Biochemistry 48: 1810-1819.
61. Stello T, Hong M, Musier-Forsyth K. 1999. Efficient aminoacylation of tRNALys,3 by human lysyl-tRNA synthetase is dependent on covalent continuity between the acceptor stem and the anticodon domain. Nucleic Acids Res 27: 4823-4829.
62. Stewart-Maynard KM, Cruceanu M, Wang F, Vo MN, Gorelick RJ, Williams MC, Rouzina I, Musier-Forsyth K. 2008. Retroviral nucleocapsid proteins display nonequivalent levels of nucleic acid chaperone activity. J Virol 82: 10129-10142.
63. Taylor Jr. 1997. An introduction to error analysis: The study of uncertainties in physical measurements. University Science Books, Sausalito, CA
64. van Weringh A, Ragonnet-Cronin M, Pranckeviciene E, Pavon- Eternod M, Kleiman L, Xia X. 2011. HIV-1 modulates the tRNA pool to improve translation efficiency. Mol Biol Evol 28: 1827-1834.
65. Wakasugi K, Slike BM, Hood J, Otani A, Ewalt KL, Friedlander M, Cheresh DA, Schimmel P. 2002. A human aminoacyl-tRNA synthetase as a regulator of angiogenesis. Proc Natl Acad Sci 99: 173-177.
66. Watts JM, Dang KK, Gorelick RJ, Leonard CW, Bess JW Jr, Swanstrom R, Burch CL, Weeks KM. 2009. Architecture and secondary structure of an entire HIV-1 RNA genome. Nature 460: 711-716.
67. Wei X, Decker JM, Liu H, Zhang Z, Arani RB, Kilby JM, Saag MS, Wu X, Shaw GM, Kappes JC. 2002. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother 46: 1896-1905.
68. Wilkinson KA, Gorelick RJ, Vasa SM, Guex N, Rein A, Mathews DH, Giddings MC, Weeks KM. 2008. High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biol 6: e96.
69. Zhu J, Korostelev A, Costantino DA, Donohue JP, Noller HF, Kieft JS. 2011. Crystal structures of complexes containing domains from two viral internal ribosome entry site (IRES) RNAs bound to the 70S ribosome. Proc Natl Acad Sci 108: 1839-1844.