Artículo

Abrahamyan, L.G.; Chatel-Chaix, L.; Ajamian, L.; Milev, M.P.; Monette, A.; Clément, J.-F.; Song, R.; Lehmann, M.; DesGroseillers, L.; Laughrea, M.; Boccaccio, G.; Mouland, A.J. "Novel Staufen1 ribonucleoproteins prevent formation of stress granules but favour encapsidation of HIV-1 genomic RNA" (2010) Journal of Cell Science. 123(3):369-383
Este artículo es de Acceso Abierto y puede ser descargado en su versión final desde nuestro repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Human immunodeficiency virus type 1 (HIV-1) Gag selects for and mediates genomic RNA (vRNA) encapsidation into progeny virus particles. The host protein, Staufen1 interacts directly with Gag and is found in ribonucleoprotein (RNP) complexes containing vRNA, which provides evidence that Staufen1 plays a role in vRNA selection and encapsidation. In this work, we show that Staufen1, vRNA and Gag are found in the same RNP complex. These cellular and viral factors also colocalize in cells and constitute novel Staufen1 RNPs (SHRNPs) whose assembly is strictly dependent on HIV-1 expression. SHRNPs are distinct from stress granules and processing bodies, are preferentially formed during oxidative stress and are found to be in equilibrium with translating polysomes. Moreover, SHRNPs are stable, and the association between Staufen1 and vRNA was found to be evident in these and other types of RNPs. We demonstrate that following Staufen1 depletion, apparent supraphysiologic-sized SHRNP foci are formed in the cytoplasm and in which Gag, vRNA and the residual Staufen1 accumulate. The depletion of Staufen1 resulted in reduced Gag levels and deregulated the assembly of newly synthesized virions, which were found to contain several-fold increases in vRNA, Staufen1 and other cellular proteins. This work provides new evidence that Staufen1-containing HIV-1 RNPs preferentially form over other cellular silencing foci and are involved in assembly, localization and encapsidation of vRNA.

Registro:

Documento: Artículo
Título:Novel Staufen1 ribonucleoproteins prevent formation of stress granules but favour encapsidation of HIV-1 genomic RNA
Autor:Abrahamyan, L.G.; Chatel-Chaix, L.; Ajamian, L.; Milev, M.P.; Monette, A.; Clément, J.-F.; Song, R.; Lehmann, M.; DesGroseillers, L.; Laughrea, M.; Boccaccio, G.; Mouland, A.J.
Filiación:HIV-1 RNA Trafficking Laboratory, Lady Davis Institute for Medical Research-Sir Mortimer B. Davis Jewish General Hospital, Montréal, QC, H3T 1E2, Canada
Lady Davis Institute for Medical Research-Sir Mortimer B. Davis Jewish General Hospital, Montréal, QC, H3T 1E2, Canada
Department of Biochemistry, Université de Montréal, Montréal, QC, H3C 3J7, Canada
Department of Medicine, Division of Experimental Medicine, McGill University, Montréal, QC, H3A 2B4, Canada
Department of Microbiology and Immunology, McGill University, Montréal, QC, H3A 2B4, Canada
Instituto Leloir, IIBBA CONICET and Facultad de Ciencias Exactas Y Naturales, University of Buenos Aires, Buenos Aires C1405BWE, Argentina
Palabras clave:AIDS; HIV-1; Intracellular traffic; Ribonucleoprotein; RNA encapsidation; SHRNP; sIRNA; Staufen1; Staufen1 HIV-1-dependent RNP; Virus-host interaction; Gag protein; genomic RNA; ribonucleoprotein; Staufen 1 ribonucleoprotein; unclassified drug; virus RNA; article; cell granule; cell level; cell stress; cellular distribution; controlled study; human; human cell; Human immunodeficiency virus 1; nonhuman; oxidative stress; polysome; priority journal; protein assembly; protein depletion; protein function; protein localization; virion; virus capsid; virus cell interaction; virus expression; Blotting, Western; Cell Line; Cytoplasmic Granules; Cytoskeletal Proteins; gag Gene Products, Human Immunodeficiency Virus; Hela Cells; Humans; Immunoprecipitation; In Situ Hybridization, Fluorescence; Models, Biological; Protein Binding; Reverse Transcriptase Polymerase Chain Reaction; Ribonucleoproteins; RNA, Viral; RNA-Binding Proteins; Virus Assembly; Human immunodeficiency virus 1
Año:2010
Volumen:123
Número:3
Página de inicio:369
Página de fin:383
DOI: http://dx.doi.org/10.1242/jcs.055897
Título revista:Journal of Cell Science
Título revista abreviado:J. Cell Sci.
ISSN:00219533
CODEN:JNCSA
CAS:Cytoskeletal Proteins; RNA, Viral; RNA-Binding Proteins; Ribonucleoproteins; STAU1 protein, human; gag Gene Products, Human Immunodeficiency Virus
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_00219533_v123_n3_p369_Abrahamyan.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00219533_v123_n3_p369_Abrahamyan

Referencias:

  • Ajamian, L., Abrahamyan, L., Milev, M., Ivanov, P.V., Kulozik, A.E., Gehring, N.H., Mouland, A.J., Unexpected roles for UPF1 in HIV-1 RNA metabolism and translation (2008) RNA, 14, pp. 914-927
  • Alvarez, E., Castello, A., Menendez-Arias, L., Carrasco, L., HIV protease cleaves poly(A)-binding protein (2006) Biochem. J, 396, pp. 219-226
  • Anderson, E.C., Lever, A.M., Human immunodeficiency virus type 1 Gag polyprotein modulates its own translation (2006) J. Virol, 80, pp. 10478-10486
  • Anderson, P., Kedersha, N., Stress granules: The Tao of RNA triage (2008) Trends Biochem. Sci, 33, pp. 141-150
  • Barbee, S.A., Estes, P.S., Cziko, A.M., Hillebrand, J., Luedeman, R.A., Coller, J.M., Johnson, N., Ueda, R., Staufen- and FMRP-containing neuronal RNPs are structurally and functionally related to somatic P bodies (2006) Neuron, 52, pp. 997-1009
  • Beckham, C.J., Parker, R., P bodies, stress granules, and viral life cycles (2008) Cell Host Microbe, 3, pp. 206-212
  • Beliakova-Bethell, N., Beckham, C., Giddings Jr, T.H., Winey, M., Parker, R., Sandmeyer, S., Virus-like particles of the Ty3 retrotransposon assemble in association with P-body components (2006) RNA, 12, pp. 94-101
  • Bennasser, Y., Le, S.Y., Benkirane, M., Jeang, K.T., Evidence that HIV-1 encodes an siRNA and a suppressor of RNA silencing (2005) Immunity, 22, pp. 607-619
  • Beriault, V., Clement, J.F., Levesque, K., Lebel, C., Yong, X., Chabot, B., Cohen, E.A., Mouland, A.J., A late role for the association of hnRNP A2 with the HIV-1 hnRNP A2 response elements in genomic RNA, Gag, and Vpr localization (2004) J. Biol. Chem, 279, pp. 44141-44153
  • Brendel, C., Rehbein, M., Kreienkamp, H.J., Buck, F., Richter, D., Kindler, S., Characterization of Staufen 1 ribonucleoprotein complexes (2004) Biochem. J, 384, pp. 239-246
  • Bruno, I., Wilkinson, M.F., P-bodies react to stress and nonsense (2006) Cell, 125, pp. 1036-1038
  • Butsch, M., Boris-Lawrie, K., Translation is not required To generate virion precursor RNA in human immunodeficiency virus type 1-infected T cells (2000) J. Virol, 74, pp. 11531-11537
  • Chatel-Chaix, L., Clement, J.F., Martel, C., Beriault, V., Gatignol, A., DesGroseillers, L., Mouland, A.J., Identification of Staufen in the human immunodeficiency virus type 1 Gag ribonucleoprotein complex and a role in generating infectious viral particles (2004) Mol. Cell. Biol, 24, pp. 2637-2648
  • Chatel-Chaix, L., Abrahamyan, L., Frechina, C., Mouland, A.J., DesGroseillers, L., The host protein Staufen1 participates in human immunodeficiency virus type 1 assembly in live cells by influencing pr55Gag multimerization (2007) J. Virol, 81, pp. 6216-6230
  • Chatel-Chaix, L., Boulay, K., Mouland, A.J., Desgroseillers, L., The host protein Staufen1 interacts with the Pr55Gag zinc fingers and regulates HIV-1 assembly via its N-terminus (2008) Retrovirology, 5, p. 41
  • Chiu, Y.L., Witkowska, H.E., Hall, S.C., Santiago, M., Soros, V.B., Esnault, C., Heidmann, T., Greene, W.C., High-molecular-mass APOBEC3G complexes restrict Alu retrotransposition (2006) Proc. Natl. Acad. Sci. USA, 103, pp. 15588-15593
  • Cimarelli, A., Luban, J., Translation elongation factor 1-alpha interacts specifically with the human immunodeficiency virus type 1 Gag polyprotein (1999) J. Virol, 73, pp. 5388-5401
  • Dahm, R., Zeitelhofer, M., Gotze, B., Kiebler, M.A., Macchi, P., Visualizing mRNA localization and local protein translation in neurons (2008) Methods Cell Biol, 85, pp. 293-327
  • Dayton, A.I., Hitting HIV where it hides (2008) Retrovirology, 5, p. 15
  • De Guzman, R.N., Wu, Z.R., Stalling, C.C., Pappalardo, L., Borer, P.N., Summers, M.F., Structure of the HIV-1 nucleocapsid protein bound to the SL3 psi-RNA recognition element (1998) Science, 279, pp. 384-388
  • D'Souza, V., Summers, M.F., Structural basis for packaging the dimeric genome of Moloney murine leukaemia virus (2004) Nature, 431, pp. 586-590
  • D'Souza, V., Summers, M.F., How retroviruses select their genomes (2005) Nat. Rev. Microbiol, 3, pp. 643-655
  • Duchaine, T., Wang, H.J., Luo, M., Steinberg, S.V., Nabi, I.R., DesGroseillers, L., A novel murine Staufen isoform modulates the RNA content of Staufen complexes (2000) Mol. Cell. Biol, 20, pp. 5592-5601
  • Duchaine, T.F., Hemraj, I., Furic, L., Deitinghoff, A., Kiebler, M.A., DesGroseillers, L., Staufen2 isoforms localize to the somatodendritic domain of neurons and interact with different organelles (2002) J. Cell Sci, 115, pp. 3285-3295
  • Dugre-Brisson, S., Elvira, G., Boulay, K., Chatel-Chaix, L., Mouland, A.J., DesGroseillers, L., Interaction of Staufen1 with the 5′ end of mRNA facilitates translation of these RNAs (2005) Nucleic Acids Res, 33, pp. 4797-4812
  • Emara, M.M., Brinton, M.A., Interaction of TIA-1/TIAR with West Nile and dengue virus products in infected cells interferes with stress granule formation and processing body assembly (2007) Proc. Natl. Acad. Sci. USA, 104, pp. 9041-9046
  • Eulalio, A., Behm-Ansmant, I., Schweizer, D., Izaurralde, E., P-body formation is a consequence, not the cause, of RNA-mediated gene silencing (2007) Mol. Cell. Biol, 27, pp. 3970-3981
  • Farny, N.G., Kedersha, N.L., Silver, P.A., Metazoan stress granule assembly is mediated by P-eIF2alpha-dependent and -independent mechanisms (2009) RNA, 15, pp. 1814-1821
  • Ferrandon, D., Koch, I., Westhof, E., Nusslein-Volhard, C., RNA-RNA interaction is required for the formation of specific bicoid mRNA 3′ UTR-STAUFEN ribonucleoprotein particles (1997) EMBO J, 16, pp. 1751-1758
  • Franks, T.M., Lykke-Andersen, J., TTP and BRF proteins nucleate processing body formation to silence mRNAs with AU-rich elements (2007) Genes Dev, 21, pp. 719-735
  • Gale Jr, M., Tan, S.L., Katze, M.G., Translational control of viral gene expression in eukaryotes (2000) Microbiol. Mol. Biol. Rev, 64, pp. 239-280
  • Gallois-Montbrun, S., Kramer, B., Swanson, C.M., Byers, H., Lynham, S., Ward, M., Malim, M.H., Antiviral protein APOBEC3G localizes to ribonucleoprotein complexes found in P bodies and stress granules (2007) J. Virol, 81, pp. 2165-2178
  • Jonson, L., Vikesaa, J., Krogh, A., Nielsen, L.K., Hansen, T.V., Borup, R., Johnsen, A.H., Nielsen, F.C., Molecular composition of IMP1 ribonucleoprotein granules (2007) Mol. Cell Proteomics, 6, pp. 798-811
  • Kaye, J.F., Lever, A.M., Human immunodeficiency virus types 1 and 2 differ in the predominant mechanism used for selection of genomic RNA for encapsidation (1999) J. Virol, 73, pp. 3023-3031
  • Kedersha, N.L., Gupta, M., Li, W., Miller, I., Anderson, P., RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules (1999) J. Cell Biol, 147, pp. 1431-1442
  • Kedersha, N., Cho, M.R., Li, W., Yacono, P.W., Chen, S., Gilks, N., Golan, D.E., Anderson, P., Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules (2000) J. Cell Biol, 151, pp. 1257-1268
  • Kedersha, N., Chen, S., Gilks, N., Li, W., Miller, I.J., Stahl, J., Anderson, P., Evidence that ternary complex (eIF2-GTP-tRNA(i) (Met))-deficient preinitiation complexes are core constituents of mammalian stress granules (2002) Mol. Biol. Cell, 13, pp. 195-210
  • Kedersha, N., Stoecklin, G., Ayodele, M., Yacono, P., Lykke-Andersen, J., Fritzler, M.J., Scheuner, D., Anderson, P., Stress granules and processing bodies are dynamically linked sites of mRNP remodeling (2005) J. Cell Biol, 169, pp. 871-884
  • Kim, Y.K., Furic, L., Desgroseillers, L., Maquat, L.E., Mammalian Staufen1 recruits Upf1 to specific mRNA 3'UTRs so as to elicit mRNA decay (2005) Cell, 120, pp. 195-208
  • Kohrmann, M., Luo, M., Kaether, C., DesGroseillers, L., Dotti, C.G., Kiebler, M.A., Microtubule-dependent recruitment of Staufen-green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons (1999) Mol. Biol. Cell, 10, pp. 2945-2953
  • Kozak, S.L., Marin, M., Rose, K.M., Bystrom, C., Kabat, D., The anti-HIV-1 editing enzyme APOBEC3G binds HIV-1 RNA and messenger RNAs that shuttle between polysomes and stress granules (2006) J. Biol. Chem, 281, pp. 29105-29119
  • Laughrea, M., Jette, L., HIV-1 genome dimerization: Kissing-loop hairpin dictates whether nucleotides downstream of the 5′ splice junction contribute to loose and tight dimerization of human immunodeficiency virus RNA (1997) Biochemistry, 36, pp. 9501-9508
  • Lehmann, M., Milev, M.P., Abrahamyan, L., Yao, X.J., Pante, N., Mouland, A.J., Intracellular transport of human immunodeficiency virus type 1 genomic RNA and viral production are dependent on Dynein motor function and late endosome positioning (2009) J. Biol. Chem, 284, pp. 14572-14585
  • Levesque, K., Halvorsen, M., Abrahamyan, L., Chatel-Chaix, L., Poupon, V., Gordon, H., DesGroseillers, L., Mouland, A.J., Trafficking of HIV-1 RNA is mediated by heterogeneous nuclear ribonucleoprotein A2 expression and impacts on viral assembly (2006) Traffic, 7, pp. 1177-1193
  • Lingappa, J.R., Dooher, J.E., Newman, M.A., Kiser, P.K., Klein, K.C., Basic residues in the nucleocapsid domain of Gag are required for interaction of HIV-1 gag with ABCE1 (HP68), a cellular protein important for HIV-1 capsid assembly (2006) J. Biol. Chem, 281, pp. 3773-3784
  • Liu, B., Dai, R., Tian, C.J., Dawson, L., Gorelick, R., Yu, X.F., Interaction of the human immunodeficiency virus type 1 nucleocapsid with actin (1999) J. Virol, 73, pp. 2901-2908
  • Macchi, P., Brownawell, A.M., Grunewald, B., DesGroseillers, L., Macara, I.G., Kiebler, M.A., The brain-specific double-stranded RNA-binding protein Staufen2: Nucleolar accumulation and isoform-specific exportin-5-dependent export (2004) J. Biol. Chem, 279, pp. 31440-31444
  • Malagon, F., Jensen, T.H., The T body, a new cytoplasmic RNA granule in Saccharomyces cerevisiae (2008) Mol. Cell. Biol, 28, pp. 6022-6032
  • Mallardo, M., Deitinghoff, A., Muller, J., Goetze, B., Macchi, P., Peters, C., Kiebler, M.A., From the cover: Isolation and characterization of Staufen-containing ribonucleoprotein particles from rat brain (2003) Proc. Natl. Acad. Sci. USA, 100, pp. 2100-2105
  • Martinez, N.W., Xue, X., Berro, R.G., Kreitzer, G., Resh, M.D., Kinesin KIF4 regulates intracellular trafficking and stability of the human immunodeficiency virus type 1 Gag polyprotein (2008) J. Virol, 82, pp. 9937-9950
  • Mazroui, R., Di Marco, S., Kaufman, R.J., Gallouzi, I.E., Inhibition of the ubiquitin-proteasome system induces stress granule formation (2007) Mol. Biol. Cell, 18, pp. 2603-2618
  • McInerney, G.M., Kedersha, N.L., Kaufman, R.J., Anderson, P., Liljestrom, P., Importance of eIF2alpha phosphorylation and stress granule assembly in alphavirus translation regulation (2005) Mol. Biol. Cell, 16, pp. 3753-3763
  • Meignin, C., Bailly, J.L., Arnaud, F., Dastugue, B., Vaury, C., The 5′ untranslated region and Gag product of Idefix, a long terminal repeat-retrotransposon from Drosophila melanogaster, act together to initiate a switch between translated and untranslated states of the genomic mRNA (2003) Mol. Cell. Biol, 23, pp. 8246-8254
  • Menager, P., Roux, P., Megret, F., Bourgeois, J.P., Le Sourd, A.M., Danckaert, A., Lafage, M., Lafon, M., Toll-like receptor 3 (TLR3) plays a major role in the formation of rabies virus Negri Bodies (2009) PLoS Pathog, 5, pp. e1000315
  • Monshausen, M., Gehring, N.H., Kosik, K.S., The mammalian RNA-binding protein Staufen2 links nuclear and cytoplasmic RNA processing pathways in neurons (2004) Neuromolecular Med, 6, pp. 127-144
  • Mouland, A.J., Mercier, J., Luo, M., Bernier, L., DesGroseillers, L., Cohen, E.A., The double-stranded RNA-binding protein Staufen is incorporated in human immunodeficiency virus type 1, evidence for a role in genomic RNA encapsidation (2000) J. Virol, 74, pp. 5441-5451
  • Mouland, A.J., Xu, H., Cui, H., Krueger, W., Munro, T.P., Prasol, M., Mercier, J., Barbarese, E., RNA trafficking signals in human immunodeficiency virus type 1 (2001) Mol. Cell. Biol, 21, pp. 2133-2143
  • Nathans, R., Chu, C.Y., Serquina, A.K., Lu, C.C., Cao, H., Rana, T.M., Cellular microRNA and P bodies modulate host-HIV-1 interactions (2009) Mol. Cell, 34, pp. 696-709
  • Ooms, M., Huthoff, H., Russell, R., Liang, C., Berkhout, B., A riboswitch regulates RNA dimerization and packaging in human immunodeficiency virus type 1 virions (2004) J. Virol, 78, pp. 10814-10819
  • Paillart, J.C., Shehu-Xhilaga, M., Marquet, R., Mak, J., Dimerization of retroviral RNA genomes: An inseparable pair (2004) Nat. Rev. Microbiol, 2, pp. 461-472
  • Poole, E., Strappe, P., Mok, H.P., Hicks, R., Lever, A.M., HIV-1 Gag-RNA interaction occurs at a perinuclear/centrosomal site; analysis by confocal microscopy and FRET (2005) Traffic, 6, pp. 741-755
  • Poon, D.T., Chertova, E.N., Ott, D.E., Human immunodeficiency virus type 1 preferentially encapsidates genomic RNAs that encode Pr55(Gag): Functional linkage between translation and RNA packaging (2002) Virology, 293, pp. 368-378
  • Scacheri, P.C., Rozenblatt-Rosen, O., Caplen, N.J., Wolfsberg, T.G., Umayam, L., Lee, J.C., Hughes, C.M., Meyerson, M., Short interfering RNAs can induce unexpected and divergent changes in the levels of untargeted proteins in mammalian cells (2004) Proc. Natl. Acad. Sci. USA, 101, pp. 1892-1897
  • Schneider, R.J., Mohr, I., Translation initiation and viral tricks (2003) Trends Biochem. Sci, 28, pp. 130-136
  • Snee, M.J., Macdonald, P.M., Dynamic organization and plasticity of sponge bodies (2009) Dev. Dyn, 238, pp. 918-930
  • Soros, V.B., Yonemoto, W., Greene, W.C., Newly synthesized APOBEC3G is incorporated into HIV virions, inhibited by HIV RNA, and subsequently activated by RNase H (2007) PLoS Pathog, 3, pp. e15
  • St Johnston, D., Beuchle, D., Nusslein-Volhard, C., Staufen, a gene required to localize maternal RNAs in the Drosophila egg (1991) Cell, 66, pp. 51-63
  • Thomas, M.G., Martinez Tosar, L.J., Loschi, M., Pasquini, J.M., Correale, J., Kindler, S., Boccaccio, G.L., Staufen recruitment into stress granules does not affect early mRNA transport in oligodendrocytes (2005) Mol. Biol. Cell, 16, pp. 405-420
  • Thomas, M.G., Tosar, L.J., Desbats, M.A., Leishman, C.C., Boccaccio, G.L., Mammalian Staufen 1 is recruited to stress granules and impairs their assembly (2009) J. Cell Sci, 122, pp. 563-573
  • Triboulet, R., Mari, B., Lin, Y.L., Chable-Bessia, C., Bennasser, Y., Lebrigand, K., Cardinaud, B., Baillat, V., Suppression of microRNA-silencing pathway by HIV-1 during virus replication (2007) Science, 315, pp. 1579-1582
  • Vessey, J.P., Macchi, P., Stein, J.M., Mikl, M., Hawker, K.N., Vogelsang, P., Wieczorek, K., Tubing, F., A loss of function allele for murine Staufen1 leads to impairment of dendritic Staufen1-RNP delivery and dendritic spine morphogenesis (2008) Proc. Natl. Acad. Sci. USA, 105, pp. 16374-16379
  • Villace, P., Marion, R.M., Ortin, J., The composition of Staufen-containing RNA granules from human cells indicates their role in the regulated transport and translation of messenger RNAs (2004) Nucleic Acids Res, 32, pp. 2411-2420
  • Watts, J.M., Dang, K.K., Gorelick, R.J., Leonard, C.W., Bess Jr, J.W., Swanstrom, R., Burch, C.L., Weeks, K.M., Architecture and secondary structure of an entire HIV-1 RNA genome (2009) Nature, 460, pp. 711-716
  • Zeitelhofer, M., Karra, D., Macchi, P., Tolino, M., Thomas, S., Schwarz, M., Kiebler, M., Dahm, R., Dynamic interaction between P-bodies and transport ribonucleoprotein particles in dendrites of mature hippocampal neurons (2008) J. Neurosci, 28, pp. 7555-7562

Citas:

---------- APA ----------
Abrahamyan, L.G., Chatel-Chaix, L., Ajamian, L., Milev, M.P., Monette, A., Clément, J.-F., Song, R.,..., Mouland, A.J. (2010) . Novel Staufen1 ribonucleoproteins prevent formation of stress granules but favour encapsidation of HIV-1 genomic RNA. Journal of Cell Science, 123(3), 369-383.
http://dx.doi.org/10.1242/jcs.055897
---------- CHICAGO ----------
Abrahamyan, L.G., Chatel-Chaix, L., Ajamian, L., Milev, M.P., Monette, A., Clément, J.-F., et al. "Novel Staufen1 ribonucleoproteins prevent formation of stress granules but favour encapsidation of HIV-1 genomic RNA" . Journal of Cell Science 123, no. 3 (2010) : 369-383.
http://dx.doi.org/10.1242/jcs.055897
---------- MLA ----------
Abrahamyan, L.G., Chatel-Chaix, L., Ajamian, L., Milev, M.P., Monette, A., Clément, J.-F., et al. "Novel Staufen1 ribonucleoproteins prevent formation of stress granules but favour encapsidation of HIV-1 genomic RNA" . Journal of Cell Science, vol. 123, no. 3, 2010, pp. 369-383.
http://dx.doi.org/10.1242/jcs.055897
---------- VANCOUVER ----------
Abrahamyan, L.G., Chatel-Chaix, L., Ajamian, L., Milev, M.P., Monette, A., Clément, J.-F., et al. Novel Staufen1 ribonucleoproteins prevent formation of stress granules but favour encapsidation of HIV-1 genomic RNA. J. Cell Sci. 2010;123(3):369-383.
http://dx.doi.org/10.1242/jcs.055897