Skip to main content
SpringerLink
Log in

SFPQ and NONO Proteins and Long Non-Coding NEAT1 RNA: Cellular Functions and Role in the HIV-1 Life Cycle

  • REVIEWS
  • Published:
Molecular Biology Aims and scope Submit manuscript

Abstract

About 20 years ago, large RNA–protein complexes called paraspeckles were discovered in cell nuclei. The main components of these complexes are SFPQ and NONO proteins and the long noncoding RNA NEAT1. Later, these proteins were found free in the nucleus and even in the cytoplasm. The functions of NEAT1 and paraspeckle proteins are quite diverse including retention of RNAs subjected to multiple editing of adenosine to inosine in the nucleus, response to DNA damage, transcription regulation, control of mRNA stability, regulation of splicing, and participation in the cell response to viral infection. Thus, there are numerous, albeit contradictory, data on the involvement of NEAT1, SFPQ, and NONO in the HIV-1 replicative cycle at its various stages. Here, we tried to briefly review the main cellular functions of NEAT1 RNA and SFPQ and NONO proteins. The goal of this review was also to summarize and, if possible, systematize the existing data on their role in the HIV-1 life cycle.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

REFERENCES

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. U. S. A. 106, 2525–2530.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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. U. S. A. 109, 4846–4850.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. Nucleic Acids Res. 43, 3826–3840.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. Nucleic Acids Res. 42, 9771–9780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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. Nucleic Acids Res. 48, 7421–7438.

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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., et al. 2014. Long noncoding RNA NEAT1-dependent SFPQ relocation from promoter region to paraspeckle mediates IL8 expression upon immune stimuli. Mol. Cell. 53, 393–406.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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. Nucleic Acids Res. 35, 2503–2512.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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., et al. 2018. NONO detects the nuclear HIV capsid to promote cGAS-mediated innate immune activation. Cell. 175, 488–501. e22.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Amelio A.L., Miraglia L.J., Conkright J.J., Mercer B.A., Batalov S., Cavett V., Orth A.P., Busby J., Hoge-nesch 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. Nucleic Acids Res. 37, 6746–6753.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. Nucleic Acids Res. 39, 132–145.

    Article  CAS  PubMed  Google Scholar 

  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.

    Google Scholar 

  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. Nucleic Acids Res. 40, 3031–3041.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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. Nucleic Acids Res. 40, 10287–10301.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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. Nature. 522, 89–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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., et al. 2017. Non-nuclear pool of splicing factor SFPQ regulates axonal transcripts required for normal motor development. Neuron. 94, 322–336. e5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Luisier R., Tyzack G.E., Hall C.E., Mitchell J.S., Devine H., Taha D.M., Malik B., Meyer I., Greensmith 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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., et al. 2020. Aberrant interaction between FUS and SFPQ in neurons in a wide range of FTLD spectrum diseases. Brain. 143, 2398–2405.

    Article  PubMed  Google Scholar 

  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. Nucleic Acids Res. 48, 3356–3365.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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., Ciborowski P., Belshan M. 2013. Proteomic analysis of early HIV-1 nucleoprotein complexes. J. Proteome Res. 12, 559–572.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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. Nucleic Acids Res. 46, 7366–7378.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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. U. S. A. 88, 8096–8100.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. Nucleic Acids Res. 37, 5848–5858.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The work was supported by grant no. 20-04-00437 from the Russian Foundation for Basic Research.

Author information

Authors and Affiliations

  1. Chemical Department, Moscow State University, 119991, Moscow, Russia

    O. A. Shadrina, T. F. Kikhay, Yu. Yu. Agapkina & M. B. Gottikh

  2. Belozersky Institute of Physical and Chemical Biology, Moscow State University, 119991, Moscow, Russia

    O. A. Shadrina, Yu. Yu. Agapkina & M. B. Gottikh

Authors
  1. O. A. Shadrina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. F. Kikhay
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yu. Yu. Agapkina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. B. Gottikh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. B. Gottikh.

Ethics declarations

Conflict of interests. The authors declare that they have no conflicts of interest.

This article does not contain any studies with the use of humans as objects of research.

Additional information

Translated by A. Levina

Abbreviations: INS, instability regions; LTR, long terminal repeat; NHEJ, non-homologous end joining; NONO, non-POU domain-containing octamer-binding protein; RRE, Rev-responsive element; SFPQ, splicing factor proline glutamine rich; TAR, trans-activation response element; TLR3, toll-like receptor 3; VSV-G, vesicular stomatitis virus glycoprotein G; HIV, human immunodeficiency virus; PIC, pre-integration complex.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shadrina, O.A., Kikhay, T.F., Agapkina, Y.Y. et al. SFPQ and NONO Proteins and Long Non-Coding NEAT1 RNA: Cellular Functions and Role in the HIV-1 Life Cycle. Mol Biol 56, 196–209 (2022). https://doi.org/10.1134/S0026893322020133

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026893322020133

Keywords:

Search

Navigation