Молекулярная биология, 2022, T. 56, № 2, стр. 259-274

Белки SFPQ, NONO и длинная некодирующая РНК NEAT1: функции в клетке и в жизненном цикле ВИЧ-1

О. А. Шадрина ab, Т. Ф. Кихай a, Ю. Ю. Агапкина ab, М. Б. Готтих ab*

a Химический факультет Московского государственного университета им. М.В. Ломоносова
119991 Москва, Россия

b Научно-исследовательский институт физико-химической биологии имени А.Н. Белозерского Московского государственного университета им. М.В. Ломоносова
119991 Москва, Россия

* E-mail: gottikh@belozersky.msu.ru

Поступила в редакцию 06.09.2021
После доработки 06.10.2021
Принята к публикации 06.10.2021

Аннотация

Около 20 лет назад в ядрах клеток обнаружили большие РНК-белковые комплексы, названные параспеклями, основными компонентами которых являются длинная некодирующая РНК NEAT1 и белки SFPQ и NONO. Позднее эти белки нашли в свободном состоянии в ядре и даже в цитоплазме. Функции NEAT1 и белков параспеклей достаточно разнообразны, в их число входят удержание в ядре РНК, подвергшихся множественному редактированию аденозина в инозин, ответ на повреждения ДНК, а также регуляция транскрипции, контроль стабильности мРНК, регуляция сплайсинга, участие в ответе клетки на вирусную инфекцию. Так, получены достаточно многочисленные, хотя и противоречивые, данные об участии NEAT1, SFPQ и NONO в репликативном цикле ВИЧ-1 на разных его этапах. В настоящем обзоре мы постарались кратко рассмотреть основные клеточные функции РНК NEAT1 и белков SFPQ и NONO, а также суммировать и по возможности систематизировать данные об их роли в жизненном цикле ВИЧ-1.

Ключевые слова: SFPQ, NONO, NEAT1 РНК, вирус иммунодефицита человека

Список литературы

  1. Fox A.H., Lam Y.W., Leung A.K.L., Lyon C.E., Andersen J., Mann M., Lamond A.I. (2002) Paraspeckles: a novel nuclear domain. Curr. Biol. 12, 13–25.

  2. Chen L.-L., Carmichael G.G. (2009) Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells: functional role of a nuclear noncoding RNA. Mol. Cell. 35, 467–478.

  3. Naganuma T., Nakagawa S., Tanigawa A., Sasaki Y.F., Goshima N., Hirose T. (2012) Alternative 3′-end processing of long noncoding RNA initiates construction of nuclear paraspeckles. EMBO J. 31, 4020–4034.

  4. Sasaki Y.T.F., Ideue T., Sano M., Mituyama T., Hirose T. (2009) MENε/β noncoding RNAs are essential for structural integrity of nuclear paraspeckles. Proc. Natl. Acad. Sci. USA. 106, 2525–2530.

  5. Knott G.J., Bond C.S., Fox A.H. (2016) The DBHS proteins SFPQ, NONO and PSPC1: a multipurpose molecular scaffold. Nucl. Acids Res. 44, 3989–4004.

  6. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403–410.

  7. Blast [Internet]. Bethesda (MD): National Library of Medicine (US), National Center for Biotechnology Information; 2004. https://blast.ncbi.nlm.nih.gov/Blast.cgi

  8. Ren S., She M., Li M., Zhou Q., Liu R., Lu H., Yang C., Xiong D. (2014) The RNA/DNA-binding protein PSF relocates to cell membrane and contributes cells’ sensitivity to antitumor drug, doxorubicin. Cytometry A. 85, 231–241.

  9. Furukawa M.T., Sakamoto H., Inoue K. (2015) Interaction and colocalization of HERMES/RBPMS with NonO, PSF, and G3BP1 in neuronal cytoplasmic RNP granules in mouse retinal line cells. Genes Cells. 20, 257–266.

  10. Passon D.M., Lee M., Rackham O., Stanley W.A., Sadowska A., Filipovska A., Fox A.H., Bond C.S. (2012) Structure of the heterodimer of human NONO and paraspeckle protein component 1 and analysis of its role in subnuclear body formation. Proc. Natl. Acad. Sci. USA. 109, 4846–4850.

  11. Lee M., Sadowska A., Bekere I., Ho D., Gully B.S., Lu Y., Iyer K.S., Trewhella J., Fox A.H., Bond C.S. (2015) The structure of human SFPQ reveals a coiled-coil mediated polymer essential for functional aggregation in gene regulation. Nucl. Acids Res. 43, 3826–3840.

  12. Li S., Li Z., Shu F.-J., Xiong H., Phillips A.C., Dynan W.S. (2014) Double-strand break repair deficiency in NONO knockout murine embryonic fibroblasts and compensation by spontaneous upregulation of the PSPC1 paralog. Nucl. Acids Res. 42, 9771–9780.

  13. Fox A.H., Bond C.S., Lamond A.I. (2005) P54nrb forms a heterodimer with PSP1 that localizes to paraspeckles in an RNA-dependent manner. Mol. Biol. Cell. 16, 5304–5315.

  14. Prasanth K.V., Prasanth S.G., Xuan Z., Hearn S., Freier S.M., Bennett C.F., Zhang M.Q., Spector D.L. (2005) Regulating gene expression through RNA nuclear retention. Cell. 123, 249–263.

  15. Clemson C.M., Hutchinson J.N., Sara S.A., Ensminger A.W., Fox A.H., Chess A., Lawrence J.B. (2009) An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol. Cell. 33, 717–726.

  16. Sunwoo H., Dinger M.E., Wilusz J.E., Amaral. PP., Mattick J.S., Spector D.L. (2008) MEN/nuclear-retained non-coding RNAs are up-regulated upon muscle differentiation and are essential components of paraspeckles. Genome Res. 19, 347–359.

  17. Carmo-Fonseca M., Rino J. (2011) RNA seeds nuclear bodies. Nat. Cell. Biol. 13, 110–112.

  18. Simko E.A.J., Liu H., Zhang T., Velasquez A., Teli S., Haeusler A.R., Wang J. (2020) G-quadruplexes offer a conserved structural motif for NONO recruitment to NEAT1 architectural lncRNA. Nucl. Acids Res. 48, 7421–7438.

  19. Naganuma T., Hirose T. (2013) Paraspeckle formation during the biogenesis of long non-coding RNAs. RNA Biol. 10, 456–461.

  20. Wilusz J.E., JnBaptiste C.K., Lu L.Y., Kuhn C.-D., Joshua-Tor L., Sharp P.A. (2012) A triple helix stabilizes the 3' ends of long noncoding RNAs that lack poly(A) tails. Genes Dev. 26, 2392–2407.

  21. Nakagawa S., Naganuma T., Shioi G., Hirose T. (2011) Paraspeckles are subpopulation-specific nuclear bodies that are not essential in mice. J. Cell. Biol. 193, 31–39.

  22. Shevtsov S.P., Dundr M. (2011) Nucleation of nuclear bodies by RNA. Nat. Cell. Biol. 13, 167–173.

  23. Li R., Harvey A.R., Hodgetts S.I., Fox A.H. (2017) Functional dissection of NEAT1 using genome editing reveals substantial localization of the NEAT1_1 isoform outside paraspeckles. RNA. 23, 872–881.

  24. Souquere S., Beauclair G., Harper F., Fox A., Pierron G. (2010) Highly ordered spatial organization of the structural long noncoding NEAT1 RNAs within paraspeckle nuclear bodies. Mol. Biol. Cell. 21, 4020–4027.

  25. West J.A., Mito M., Kurosaka S., Takumi T., Tanegashima C., Chujo T., Yanaka K., Kingston R.E., Hirose T., Bond C., Fox A., Nakagawa S. (2016) Structural, super-resolution microscopy analysis of paraspeckle nuclear body organization. J. Cell. Biol. 214, 817–830.

  26. Chen L.-L., DeCerbo J.N., Carmichael G.G. (2008) Alu element-mediated gene silencing. EMBO J. 27, 1694–1705.

  27. Zhang Z., Carmichael G.G. (2001) The fate of dsRNA in the nucleus. Cell. 106, 465–476.

  28. Hirose T., Virnicchi G., Tanigawa A., Naganuma T., Li R., Kimura H., Yokoi T., Nakagawa S., Bénard M., Fox A.H., Pierron G. (2014) NEAT1 long noncoding RNA regulates transcription via protein sequestration within subnuclear bodies. Mol. Biol. Cell. 25, 169–183.

  29. Imamura K., Imamachi N., Akizuki G., Kumakura M., Kawaguchi A., Nagata K., Kato A., Kawaguchi Y., Sato H., Yoneda M., Kai C., Yada T., Suzuki Y., Yamada T., Ozawa T., Kaneki K., Inoue T., Kobayashi M., Kodama T., Wada Y., Sekimizu K., Akimitsu N. (2014) Long noncoding RNA NEAT1-dependent SFPQ relocation from promoter region to paraspeckle mediates IL8 expression upon immune stimuli. Mol. Cell. 53, 393–406.

  30. Zeng Y., Wu W., Fu Y., Chen S., Chen T., Yang B., Ou Q. (2019) Toll-like receptors, long non-coding RNA NEAT1, and RIG-I expression are associated with HBeAg-positive chronic hepatitis B patients in the active phase. J. Clin. Lab. Anal. 33, e22886.

  31. Morchikh M., Cribier A., Raffel R., Amraoui S., Cau J., Severac D., Dubois E., Schwartz O., Bennasser Y., Benkirane M. (2017) HEXIM1 and NEAT1 long non-coding RNA form a multi-subunit complex that regulates DNA-mediated innate immune response. Mol. Cell. 67, 387–399.e5.

  32. Li Q., Cooper J.J., Altwerger G.H., Feldkamp M.D., Shea M.A., Price D.H. (2007) HEXIM1 is a promiscuous double-stranded RNA-binding protein and interacts with RNAs in addition to 7SK in cultured cells. Nucl. Acids Res. 35, 2503–2512.

  33. Zhou B., Wu F., Han J., Qi F., Ni T., Qian F. (2019) Exploitation of nuclear protein SFPQ by the encephalomyocarditis virus to facilitate its replication. Biochem. Biophys. Res. Commun. 510, 65–71.

  34. Jin C., Peng X., Xie T., Lu X., Liu F., Wu H., Yang Z., Wang J., Cheng L., Wu N. (2016) Detection of the long noncoding RNAs nuclear-enriched autosomal transcript 1 (NEAT1) and metastasis associated lung adenocarcinoma transcript 1 in the peripheral blood of HIV-1-infected patients. HIV Med. 17, 68–72.

  35. Zhang Q., Chen C.-Y., Yedavalli V.S.R.K., Jeang K.-T. (2013) NEAT1 long noncoding RNA and paraspeckle bodies modulate HIV-1 posttranscriptional expression. MBio. 4, e00596–e00612.

  36. Lahaye X., Gentili M., Silvin A., Conrad C., Picard L., Jouve M., Zueva E., Maurin M., Nadalin F., Knott G.J., Zhao B., Du F., Rio M., Amiel J., Fox A. H., Li P., Etienne L., Bond C.S., Colleaux L., Manel N. (2018) NONO detects the nuclear HIVcapsid to promote cGAS-mediated innate immune activation. Cell. 175, 488–501.e22.

  37. Mathur M., Tucker P.W., Samuels H.H. (2001) PSF is a novel corepressor that mediates its effect through Sin3A and the DNA binding domain of nuclear hormone receptors. Mo.l Cell. Biol. 21, 2298–2311.

  38. Dong X., Shylnova O., Challis J.R.G., Lye S.J. (2005) Identification and characterization of the protein-associated splicing factor as a negative co-regulator of the progesterone receptor. J. Biol. Chem. 280, 13329–13340.

  39. Dong X., Sweet J., Challis J.R.G., Brown T., Lye S.J. (2007) Transcriptional activity of androgen receptor is modulated by two RNA splicing factors, PSF and p54nrb. Mol. Cell. Biol. 27, 4863–4875.

  40. Dong X., Yu C., Shynlova O., Challis J.R.G., Rennie P.S., Lye S.J. (2009) p54nrb is a transcriptional corepressor of the progesterone receptor that modulates transcription of the labor-associated gene, connexin 43 (Gja1). Mol. Endocrinol. 23, 1147–1160.

  41. Ishitani K., Yoshida T., Kitagawa H., Ohta H., Nozawa S., Kato S. (2003) p54nrb acts as a transcriptional coactivator for activation function 1 of the human androgen receptor. Biochem. Biophys. Res. Commun. 306, 660–665.

  42. Emili A., Shales M., McCracken S., Xie W., Tucker P.W., Kobayashi R., Blencowe B.J., Ingles C.J. (2002) Splicing and transcription-associated proteins PSF and p54nrb/nonO bind to the RNA polymerase II CTD. RNA. 8, 1102–1111.

  43. Amelio A.L., Miraglia L.J., Conkright J.J., Mercer B.A., Batalov S., Cavett V., Orth A.P., Busby J., Hogenesch J.B., Conkright M.D. (2007) A coactivator trap identifies NONO (p54nrb) as a component of the cAMP-signaling pathway. Proc. Natl. Acad. Sci. USA. 104, 20314–20319.

  44. Ong S.A., Tan J.J., Tew W.L., Chen K.-S. (2011) Rasd1 modulates the coactivator function of NonO in the cyclic AMP pathway. PLoS One. 6, e24401.

  45. Duong H.A., Robles M.S., Knutti D., Weitz C.J. (2011) A molecular mechanism for circadian clock negative feedback. Science. 332(6036), 1436–1439.

  46. Kaneko S., Rozenblatt-Rosen O., Meyerson M., Manley J.L. (2007) The multifunctional protein p54nrb/ PSF recruits the exonuclease XRN2 to facilitate pre-mRNA 3’ processing and transcription termination. Genes Dev. 21, 1779–1789.

  47. Bladen C.L., Udayakumar D., Takeda Y., Dynan W.S. (2005) Identification of the polypyrimidine tract binding protein-associated splicing factor·p54(nrb) complex as a candidate DNA double-strand break rejoining factor. J. Biol. Chem. 280, 5205–5210.

  48. Udayakumar D., Dynan W.S. (2015) Characterization of DNA binding and pairing activities associated with the native SFPQ·NONO DNA repair protein complex. Biochem. Biophys. Res. Commun. 463, 473–478.

  49. Li S., Kuhne W.W., Kulharya A., Hudson F.Z., Ha K., Cao Z., Dynan W.S. (2009) Involvement of p54(nrb), a PSF partner protein, in DNA double-strand break repair and radioresistance. Nucl. Acids Res. 37, 6746–6753.

  50. Salton M., Lerenthal Y., Wang S.-Y., Chen D.J., Shiloh Y. (2010) Involvement of matrin 3 and SFPQ/NONO in the DNA damage response. Cell Cycle. 9, 1568–1576.

  51. Morozumi Y., Takizawa Y., Takaku M., Kurumizaka H. (2009) Human PSF binds to RAD51 and modulates its homologous-pairing and strand-exchange activities. Nucl. Acids Res. 37, 4296–4307.

  52. Rajesh C., Baker D.K., Pierce A.J., Pittman D.L. (2011) The splicing-factor related protein SFPQ/PSF interacts with RAD51D and is necessary for homology-directed repair and sister chromatid cohesion. Nucl. Acids Res. 39, 132–145.

  53. Kuhnert A., Schmidt U., Monajembashi S., Franke C., Schlott B., Grosse F., Greulich K.O., Saluz H.-P., Hänel F. (2011) Proteomic identification of PSF and p54(nrb) as TopBP1-interacting proteins. J. Cell. Biochem. 113, 1744–1753.

  54. Morozumi Y., Ino R., Takaku M., Hosokawa M., Chuma S., Kurumizaka H. (2012) Human PSF concentrates DNA and stimulates duplex capture in DMC1-mediated homologous pairing. Nucl. Acids Res. 40, 3031–3041.

  55. de Silva H., Lin M., Phillips L., Martin L., Baxter R. (2019) IGFBP-3 interacts with NONO and SFPQ in PARP-dependent DNA damage repair in triple-negative breast cancer. Cell. Mol. Life Sci. 76, 2015–2030.

  56. Krietsch J., Caron M.-C., Gagné J.-P., Ethier C., Vignard J., Vincent M., Rouleau M., Hendzel M.J., Poirier G.G., Masson J.-Y. (2012) PARP activation regulates the RNA-binding protein NONO in the DNA damage response to DNA double-strand breaks. Nucl. Acids Res. 40, 10287–10301.

  57. Petti E., Buemi V., Zappone A., Schillaci O., Broccia P.V., Dinami R., Matteoni S., Benetti R., Schoeftner S. (2019) SFPQ and NONO suppress RNA:DNA-hybrid-related telomere instability. Nat. Commun. 10, 1–14.

  58. Santos-Pereira J.M., Aguilera A. (2015) R loops: new modulators of genome dynamics and function. Nat. Rev. Genet. 16, 583–597.

  59. Skourti-Stathaki K., Proudfoot N. (2014) A double-edged sword: R loops as threats to genome integrity and powerful regulators of gene expression. Genes Dev. 28, 1384–1396.

  60. Takeuchi A., Iida K., Tsubota T., Hosokawa M., Denawa M., Brown J.B., Ninomiya K., Ito M., Kimura H., Abe T., Kiyonari H., Ohno K., Hagiwara M. (2018) Loss of Sfpq causes long-gene transcriptopathy in the brain. Cell Rep. 23, 1326–1341.

  61. Iida K., Hagiwara M., Takeuchi A. (2020) Multilateral bioinformatics analyses reveal the function-oriented target specificities and recognition of the RNA-binding protein SFPQ. iScience. 23, 101325.

  62. Gabel H.W., Kinde B., Stroud H., Gilbert C.S., Harmin D.A., Kastan N.R., Hemberg M., Ebert D.H., Greenberg M.E. (2015) Disruption of DNA-methylation-dependent long gene repression in Rett syndrome. Nat. 522, 89–93.

  63. Thomas-Jinu S., Gordon P.M., Fielding T., Taylor R., Smith B.N., Snowden V., Blanc E., Vance C., Topp S., Wong C.H., Bielen H., Williams K.L., McCann E.P., Nicholson G.A., Pan-Vazquez A., Fox A.H., Bond C.S., Talbot W.S., Blair I.P., Shaw C.E., Houart C. (2017) Non-nuclear pool of splicing factor SFPQ regulates axonal transcripts required for normal motor development. Neuron. 94, 322–336.e5.

  64. Luisier R., Tyzack G.E., Hall C.E., Mitchell J.S., Devine H., Taha D.M., Malik B., Meyer I., Green-smith L., Newcombe J., Ule J., Luscombe N.M., Patani R. (2018) Intron retention and nuclear loss of SFPQ are molecular hallmarks of ALS. Nat. Commun. 9, 2010.

  65. Younas N., Zafar S., Shafiq M., Noor A., Siegert A., Arora A., Galkin A., Zafar A., Schmitz M., Stadelmann C., Andreoletti O., Ferrer I., Zerr I. (2020) SFPQ and Tau: critical factors contributing to rapid progression of Alzheimer’s disease. Acta Neuropathol. 140, 317–339.

  66. Ishigaki S., Riku Y., Fujioka Y., Endo K., Iwade N., Kawai K., Ishibashi M., Yokoi S., Katsuno M., Watanabe H., Mori K., Akagi A., Yokota O., Terada S., Kawakami I., Suzuki N., Warita H., Aoki M., Yoshida M., Sobue G. (2020) Aberrant interaction between FUS and SFPQ in neurons in a wide range of FTLD spectrum diseases. Brain. 143, 2398–2405.

  67. Huang J., Ringuet M., Whitten A., Caria S., Lim Y., Badhan R., Anggono V., Lee M. (2020) Structural basis of the zinc-induced cytoplasmic aggregation of the RNA-binding protein SFPQ. Nucl. Acids Res. 48, 3356–3365.

  68. Lim Y., James D., Huang J., Lee M. (2020) The emerging role of the RNA-binding protein SFPQ in neuronal function and neurodegeneration. Int. J. Mol. Sci. 21, 1–16.

  69. Ruelas D.S., Greene W.C. (2013) An integrated overview of HIV-1 latency. Cell. 155, 519–529.

  70. Yedavalli V.S.R.K., Jeang K.-T. (2011) Rev-ing up post-transcriptional HIV-1 RNA expression. RNA Biol. 8, 195–199.

  71. Dayton A.I. (2004) Within you, without you: HIV-1 Rev and RNA export. Retrovirology. 1, 35.

  72. LeBlanc J., Weil J., Beemon K. (2013) Posttranscriptional regulation of retroviral gene expression: primary RNA transcripts play three roles as pre-mRNA, mRNA, and genomic RNA. WIREs RNA. 4, 567–580.

  73. Karn J., Stoltzfus C.M. (2012) Transcriptional and posttranscriptional regulation of HIV-1 gene expression. Cold Spring Harb Perspect Med. 2, a006916–a006916.

  74. Toro-Ascuy D., Rojas-Araya B., Valiente-Echeverría F., Soto-Rifo R. (2016) Interactions between the HIV-1 unspliced mRNA and host mRNA decay machineries. Viruses. 8, 320.

  75. Schwartz S., Campbell M., Nasioulas G., Harrison J., Felber B.K., Pavlakis G.N. (1992) Mutational inactivation of an inhibitory sequence in human immunodeficiency virus type 1 results in Rev-independent gag expression. J. Virol. 66, 7176–7182.

  76. Schwartz S., Felber B.K., Pavlakis G.N. (1992) Distinct RNA sequences in the gag region of human immunodeficiency virus type 1 decrease RNA stability and inhibit expression in the absence of Rev protein. J. Virol. 66, 150–159.

  77. Schneider R., Campbell M., Nasioulas G., Felber B.K., Pavlakis G.N. (1997) Inactivation of the human immunodeficiency virus type 1 inhibitory elements allows Rev-independent expression of Gag and Gag/protease and particle formation. J. Virol. 71, 4892–4903.

  78. Raghavendra N.K., Shkriabai N., Graham R.L., Hess S., Kvaratskhelia M., Wu L. (2010) Identification of host proteins associated with HIV-1 preintegration complexes isolated from infected CD4+ cells. Retrovirology. 7, 66.

  79. Naji S., Ambrus G., Cimermančič P., Reyes J.R., Johnson J.R., Filbrandt R., Huber M.D., Vesely P., Krogan N.J., Yates J.R., Saphire A.C., Gerace L. (2012) Host cell interactome of HIV-1 Rev includes RNA helicases involved in multiple facets of virus production. Mol. Cell. Proteomics. 11, M111.015313.

  80. Schweitzer C.J., Jagadish T., Haverland N., Ciboro-wski P., Belshan M. (2013) Proteomic analysis of early HIV-1 nucleoprotein complexes. J. Proteome Res. 12, 559–572.

  81. Yadav P., Sur S., Desai D., Kulkarni S., Sharma V., Tandon V. (2019) Interaction of HIV-1 integrase with polypyrimidine tract binding protein and associated splicing factor (PSF) and its impact on HIV-1 replication. Retrovirology. 16, 1–18.

  82. St. Gelais C., Roger J., Wu L. (2015) Non-POU domain-containing octamer-binding protein negatively regulates HIV-1 infection in CD4+ T cells. AIDS Res. Hum. Retroviruses. 31, 806–816.

  83. Zolotukhin A.S., Michalowski D., Bear J., Smulevitch S.V., Traish A.M., Peng R., Patton J., Shatsky I.N., Felber B.K. (2003) PSF acts through the human immunodeficiency virus type 1 mRNA instability elements to regulate virus expression. Mol. Cell Biol. 23, 6618–6630.

  84. Kula A., Gharu L., Marcello A. (2013) HIV-1 pre-mRNA commitment to Rev mediated export through PSF and Matrin 3. Virology. 435, 329–340.

  85. Singh G., Rife B.D., Seufzer B., Salemi M., Rendahl A., Boris-Lawrie K. (2018) Identification of conserved, primary sequence motifs that direct retrovirus RNA fate. Nucl. Acids Res. 46, 7366–7378.

  86. Liu H., Hu P.-W., Couturier J., Lewis D.E., Rice A.P. (2018) HIV-1 replication in CD4+ T cells exploits the down-regulation of antiviral NEAT1 long non-coding RNAs following T cell activation. Virology. 522, 193–198.

  87. Sharmeen L., Bass B., Sonenberg N., Weintraub H., Groudine M. (1991) Tat-dependent adenosine-to-inosine modification of wild-type transactivation response RNA. Proc. Natl. Acad. Sci. USA. 88, 8096–8100.

  88. Phuphuakrat A., Kraiwong R., Boonarkart C., Lauhakirti D., Lee T.-H., Auewarakul P. (2008) Double-stranded RNA adenosine deaminases enhance expression of human immunodeficiency virus type 1 proteins. J. Virol. 82, 10864–10872.

  89. Doria M., Neri F., Gallo A., Farace M.G., Michienzi A. (2009) Editing of HIV-1 RNA by the double-stranded RNA deaminase ADAR1 stimulates viral infection. Nucl. Acids Res. 37, 5848–5858.

  90. Rensen E., Mueller F., Scoca V., Parmar J.J., Souque P., Zimmer C., Nunzio F.Di. (2021) Clustering and reverse transcription of HIV-1 genomes in nuclear niches of macrophages. EMBO J. 40, e105247.

Дополнительные материалы отсутствуют.