Noncanonical functions of lysyl-tRNA synthethase in HIV-1 packaging
DOI:
https://doi.org/10.14456/tjg.2011.9Keywords:
lysyl-tRNA synthetase, diadenosine polyphosphate, HIV-1 capsid protein, HIV-1 packagingAbstract
Lysyl-tRNA synthetase (LysRS) catalyzesthe formation of Lys-tRNALys. Addition to its role inthe translation apparatus, LyRS has other alternativefunctions which are of great interest. LysRSinvolves in the production of diadenosinetetraphosphate, acts as a cytokine-like molecule andplay a major role in HIV-1 packaging. Interestingly,reverse transcription of the HIV-1 genome is primedby a human tRNALys3 which is packaged into thevirion by the HIV-1 Gag and LysRS. However, thestructural basis for simultaneous packaging oftRNALys3, LysRS and Gag is still not understood.Better understanding of the interaction amongtRNALys3, LysRS and Gag might open the way forthe design and screening of small peptides and/orother small molecules capable of potentiallyinterfering with the HIV-1 life cycle by blockadinginteractions between LysRS and the Gag CA-Cdomain.References
Berkowitz, R., Fisher, J. and Goff, S.P. 1996. RNA
packaging. Curr Top Microbiol Immunol 214:
-218.
Blanqet, S., Plateau, P. and Brevet, A. 1983. The
role of zinc in 5,5- diadenosine tetraphosphate
production by aminoacyl-transfer RNA
synthetase. Mol Cell Biochem 52:3-11.
Brevet, A., Chen, J, and et. al. 1995. Comparison of
the enzymatic properties of the two E. coli
lysyl-tRNA synthetase species. J Bol Chem
: 14439-14444.
Cen, S., Javanbakht, H., Kim, S., Shiba, K., Craven,
R., Rein, A., Ewalt, K., Schimmel, P.,
Musier-Forsyth, K. and Kleiman, L. 2002.
Retrovirus-specific packaging of aminoacyltRNA
synthetases with cognate primer tRNAs.
J Virol 76: 13111-13115.
Cen, S., Javanbakht, H., Niu, M. and Kleiman, L.
Ability of wild-type and mutant
lysyl-tRNA synthetase to facilitate tRNALys
incorporation into human immunodeficiency
virus type 1. J Virol 78: 1595-1601.
Cen, S., Khorchid, A., Javanbakht, H., Gabor, J.,
Stello, T., Shiba, K., Musier-Forsyth, K. and
Kleiman, L. 2001. Incorporation of lysyl-tRNA
synthetase into human immunodeficiency
virus type 1. J Virol 75: 5043-5048.
Charlier, J. and Sanchez, R. 1987. Lysyl-tRNA
synthetase from E. coli K12 chromatographic
heterogeneity and the lysU gene product.
Biochem J 248: 43-51.
Francin, M., Kaminska, M., Kerjan, P. and Mirande,
M. 2002. The N-terminal domain of mammalian
lysyl-tRNA synthetase is a functional
tRNA-binding domain. J Biol Chem 277:
-1769.
Francin, M. and Mirande, M. 2003. Functional
dissection of the eukaryotic-specific tRNAinteracting
factor of lysyl-tRNA synthetase.
J Biol Chem 278: 1472-1479.
Gabor, J., Cen, S., Javanbakht, H., Niu, M. and
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.
Garrison, P.N., and Barnes, L.D. 1992. Determination
of dinucleoside polyphosphates. In: A.G.
McLennan (ed.), Ap4A and Other Dinucleoside
Polyphosphates. Boca Raton: CRC Press. pp
-61.
Geigenmuller, U. and Linial, M.L. 1996. Specific
binding of human immunodeficiency virus
type 1 (HIV-1) Gag-derived proteins to a 5’
HIV-1 genomic RNA sequence. J Virol 70:
-671.
G nther Sillero, M.A., and Cameselle, J.C. 1992.
Interactions of dinucleoside polyphophates
with enzymes and other proteins. In: A.G.
McLennan (ed.), Ap4A and Other
Dinucleoside Polyphosphates). Boca Raton:
CRC Press. pp. 205-228.
Guo, F., Cen, S., Niu, M., Javanbakht, H. and
Kleiman, L. 2003. Specific inhibition of the
synthesis of human lysyl-tRNA synthetase
results in decreases in tRNALys incorporation,
tRNALys3 annealing to viral RNA, and viral
infectivity in human immunodeficiency virus
type 1. J Virol 77: 9817-9822.
Guo, M., Ignatov, M., Musier-Forsyth, K.,
Schimmel, P. and Yang, X.L. 2008. Crystal
structure of tetrameric form of human lysyl-tRNA
synthetase: implications for multisynthetase complex formation. Proc Natl Acad Sci USA
: 2331-2336.
Guo, M., Shapiro, R., Morris, G.M., Yang, X.L. and
Schimmel, P. 2010. Packaging HIV virion
components through dynamic equilibria of a
human tRNA synthetase. J Phys Chem B 114:
-16279.
Hassani, M., Pincus, D. H, Bennett, G.N. and
Hirshfield, I.N. 1992. Temperature-dependent
induction of an acid-inducible stimulon of
E. coli in broth. Appl Environ Microbiol 58:
-2707.
Hassani, M., Saluta, M.V. Bennett, G.N. and
Hirshfield, I.N. 1991. Partial characterization
of lysU mutant of E. coli K12. J Bacteriol 173:
-1970.
Huang, Y., Mak, J., Cao, Q., Li, Z., Wainberg, M.A.
and Kleiman, L. 1994. Incorporation of excess
wild-type and mutant tRNALys3 into human
immunodeficiency virus type 1. J Virol 68:
-7683.
Ibba, M., Morgan, S., Curnow, A.W., Pridmore,
D.R., Vothknecht, U.C., Gardner, W., Lin,W.,
Woese, C.R. and S ll, D. 1997a. A
euryarchaeal lysyl-tRNA synthetase: resemblance
to class I synthetase. Science 278: 1119-1122.
Ibba, M., Bono, J.L., Rosa, P.A. and S ll, D. 1997b.
Archaeal-type lysyl-tRNA synthetase in the
Lyme disease spirochete Borrelia burgdorferi.
Proc Natl Acad Sci USA 94: 14383-14388.
Ivanov, D., Stone, J.R., Maki, J.L., Collins, T. and
Wagner, G. 2005. Mammalian SCAN domain
dimer is a domain-swapped homolog of the
HIV capsid C-terminal domain. Mol Cell 17:
-143.
Javanbakht, H., Cen, S., Musier-Forsyth, K. and
Kleiman, L. 2002. Correlation between
tRNALys3 aminoacylation and its incorporation
into HIV-1. J Biol Chem 277: 17389-17396.
Javanbakht, H., Halwani, R., Cen, S., Saadatmand,
J., Musier-Forsyth, K., Gottlinger, H. and
Kleiman, L. 2003. The interaction between
HIV-1 Gag and human lysyl-tRNA synthetase
during viral assembly. J Biol Chem 278:
-27651.
Khorchid, A., Javanbakht, H., Wise, S., Halwani, R.,
Parniak, M.A., Wainberg, M.A. and Kleiman,
L. 2000. Sequences within Pr160gag-pol
affecting the selective packaging of primer
tRNALys3 into HIV-1. J Mol Biol 299: 17-26.
Kisselev, L.L., and Baturina, I.D. 1972. Two
enzymatically active forms of lysyl-tRNA
synthetase from E. coli B. FEBS Lett 22: 231-
Kleiman, L. and Cen, S. 2004. The tRNALys
packaging complex in HIV-1. Int J Biochem B
: 1776-1786.
Kleiman, L., Jones, C.P. and Musier-Forsyth, K.
Formation of the tRNALys packaging
complex in HIV-1. FEBS Lett 584: 359-365.
Kovaleski, B.J., Kennedy, R., Hong, M.K., Datta, S.
A., Kleiman, L., Rein, A. and Musier-Forsyth,
K. 2006. In vitro characterization of the
interaction between HIV-1 Gag and human
lysyl-tRNA synthetase. J Biol Chem 281:
-19456.
Kovaleski, B.J., Kennedy, R., Khorchid, A.,
Kleiman, L., Matsuo, H. and 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
: 32274-32279.
Martin, F., Pintor, J., Rovira, J.M., Ripoll, C.,
Miras-Portugal, M.T. and Soria, B. 1998. Intracellular diadenosine polyphosphates: a
novel second messenger in stimulus-secretion
coupling. FASEB J 12: 1499-1506.
McLennan, A.G. 2000. Dinucleoside polyphosphatesfriend
or foe? Pharmacol Therapeut 87: 73-89.
Na Nakorn, P., Treesuwan, W., Choowongkomon,
K., Hannongbua, S. and Boonyalai, N. 2011.
In vitro and in silico binding study of the
peptide derived from HIV-1 CA-CTD and
LysRS as a potential HIV-1 blocking site.
J Theor Biol 270: 88-97.
Nathanson, L. and Deutscher, M.P. 2000. Active
aminoacyl-tRNA synthetases are present
in nuclei as a high molecular weight
multienzyme complex. J Biol Chem 275:
-31562.
Onesti, S., Miller, A.D, and Brick, P. 1995. The
crystal structure of the lysyl-tRNA synthetse
(LysU) form E. coli. Structure 3: 163-176.
Paulovich, A.G., Toczyski, D.P. and Hartwell, L.H.
When check-points fail. Cell 88: 315-
Pettit, S.C., Everitt, L.E., Choudhury, S., Dunn,
B.M. and Kaplan, A.H. 2004. Initial cleavage
of the human immunodeficiency virus type 1
GagPol precursor by its activated protease
occurs by an intramolecular mechanism.
J Virol 78: 8477-8485.
Rapaport, E., and Zamecnik, P.C. 1976. Presence of
diadenosine 5, 5 -P1,P4-tetraphosphate (Ap4A)
in mammalian cells in levels varying widely
with proliferative activity of the tissue: a
possible positive “pleiotypic activator”. Proc
Natl Acad Sci USA 73: 3984-3988.
Saadatmand, J., Guo, F., Cen, S., Niu, M. and
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.
Terada, T., Nureki, O., Ishitani, R., Ambrogelly, A.,
Ibba, M., S ll, D. and Yokoyama, S. 2002.
Functional convergence of two lysyl-tRNA
synthetase with unrelated topologies. Nat
Struct Biol 9: 257-262.
Weinmann-Dorsch, C., Hedl, A., Grummt, I.,
Albert, W., Ferdinand, F.J., Friis, R.R.,
Pierron, G., Moll, W. and Grummt, F. 1984.
Drastic rise of intracellular adenosine -5-
tetraphospho -5- adenosine correlates with
onset of DNA synthesis in eukaryotic cells.
Eur J Biochem 138: 179-185.
Wills, J.W. and Craven, R.C. 1991. Form, function,
and use of retroviral Gag proteins. AIDS
(London) 5: 639-654.
Worthylake, D.K., Wang, H., Yoo, S., Sundquist,
W.I. and Hill, C.P. 1999. Structures of the
HIV-1 capsid protein dimerization domain at
6 resolution. Acta Crystallogr D D55: 85-
Wright, M., Boonyalai, N., Tanner, J.A., Hindley,
A.D. and Miller, A.D. 2006. The duality of
LysU, a catalyst for both Ap4A and Ap3A
formation. FEBS J 273: 3534-3544.
