The Diversity of MLE Helicase Functions in the Regulation of Gene Expression in Higher Eukaryotes

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MLE (Maleless) protein of D. melanogaster is a conserved helicase involved in a wide range of gene expression regulation processes. MLE ortholog, named DHX9, has been found in many higher eukaryotes, including humans. It is involved in such diverse processes as maintenance of genome stability, replication, transcription, splicing, editing and transport of cellular and viral RNAs, and translation regulation. Some of these functions have been studied in detail to date, but the most of them remain uncharacterized. The study of the functions of MLE ortholog in mammals in vivo is limited by the fact that the loss of function of this protein is lethal at the embryonic stage. Helicase MLE in D. melanogaster was originally discovered and studied for a long time as a participant in the dosage compensation process. However, in recent years, evidence has emerged that in D. melanogaster helicase MLE is involved in cellular processes similar to those in which it participates in mammals, and that many functions of this protein are conserved in evolution. In addition, in experiments on D. melanogaster new important functions of MLE were discovered, such as participation in hormone-dependent regulation of transcription, interaction with the SAGA transcription complex and other transcription cofactors and chromatin remodeling complexes. In contrast to mammals, in D. melanogaster, MLE mutations do not lead to death at the embryonic stage and allow the functions of this protein to be studied in vivo throughout ontogenesis in females and up to the pupal stage in males. The MLE ortholog in humans is a potential target for anticancer and antiviral therapy. Therefore, continued study of the functions of this helicase in the D. melanogaster model organism seems important and promising in both fundamental and practical aspects. In this review, the systematic position, domain structure, and conserved and specific functions of MLE helicase in D. melanogaster are discussed.

作者简介

J. Nikolenko

Engelhardt Institute of Molecular Biology, Russian Academy of Sciences

编辑信件的主要联系方式.
Email: julia.v.nikolenko@gmail.com
Russia, 119991, Moscow

S. Georgieva

Engelhardt Institute of Molecular Biology, Russian Academy of Sciences

Email: julia.v.nikolenko@gmail.com
Russia, 119991, Moscow

D. Kopytova

Engelhardt Institute of Molecular Biology, Russian Academy of Sciences

Email: julia.v.nikolenko@gmail.com
Russia, 119991, Moscow

参考

  1. Fairman-Williams M.E., Guenther U.-P., Jankowsky E. (2010) SF1 and SF2 helicases: family matters. Curr. Opin. Struct. Biol. 20, 313–324.
  2. Lee C.-G. (1997) The NTPase/helicase activities of Drosophila maleless, an essential factor in dosage compensation. EMBO J. 16, 2671–2681.
  3. Gorbalenya A.E., Koonin E.V. (1993) Helicases: amino acid sequence comparisons and structure-function relationships. Curr. Opin. Struct. Biol. 3, 419–429.
  4. Singleton M.R., Dillingham M.S., Wigley D.B. (2007) Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 76, 23–50.
  5. Lee C.G., Hurwitz J. (1993) Human RNA helicase A is homologous to the maleless protein of Drosophila. J. Biol. Chem. 268, 16822–16830.
  6. Walstrom K.M., Schmidt D., Bean C.J., Kelly W.G. (2005) RNA helicase A is important for germline transcriptional control, proliferation, and meiosis in C. elegans. Mech. Dev. 122, 707–720.
  7. Wei W., Twell D., Lindsey K. (1997) A novel nucleic acid helicase gene identified by promoter trapping in Arabidopsis. Plant J. 11, 1307–1314.
  8. Sato H., Oshiumi H., Takaki H., Hikono H., Seya T. (2015) Evolution of the DEAD box helicase family in chicken: chickens have no DHX9 ortholog. Microbiol. Immunol. 59, 633–640.
  9. Barber M.R.W., Aldridge J.R., Webster R.G., Magor K.E. (2010) Association of RIG-I with innate immunity of ducks to influenza. Proc. Natl. Acad. Sci. USA. 107, 5913–5918.
  10. Lee T., Pelletier J. (2016) The biology of DHX9 and its potential as a therapeutic target. Oncotarget. 7, 42716–42739.
  11. Aratani S., Kageyama Y., Nakamura A., Fujita H., Fujii R., Nishioka K., Nakajima T. (2008) MLE activates transcription via the minimal transactivation domain in Drosophila. Int. J. Mol. Med. 21, 469–476.
  12. Prabu J.R., Müller M., Thomae A.W., Schüssler S., Bonneau F., Becker P.B., Conti E. (2015) Structure of the RNA helicase MLE reveals the molecular mechanisms for uridine specificity and RNA–ATP coupling. Mol. Cell. 60, 487–499.
  13. Xing L., Zhao X., Niu M., Kleiman L. (2014) Helicase associated 2 domain is essential for helicase activity of RNA helicase A. Biochim. Biophys. Acta (BBA) – Proteins Proteomics. 1844, 1757–1764.
  14. Kuroda M.I., Kernan M.J., Kreber R., Ganetzky B., Baker B.S. (1991) The maleless protein associates with the X chromosome to regulate dosage compensation in Drosophila. Cell. 66, 935–947.
  15. Izzo A., Regnard C., Morales V., Kremmer E., Becker P.B. (2008) Structure-function analysis of the RNA helicase maleless. Nucl. Acids Res. 36, 950–962.
  16. Robinson J., Raguseo F., Nuccio S.P., Liano D., Di Antonio M. (2021) DNA G-quadruplex structures: more than simple roadblocks to transcription? Nucl. Acids Res. 49, 8419–8431.
  17. Makki R., Meller V.H. (2021) When down is up: heterochromatin, nuclear organization and X upregulation. Cells. 10, 3416.
  18. Samata M., Akhtar A. (2018) Dosage compensation of the X chromosome: a complex epigenetic assignment involving chromatin regulators and long noncoding RNAs. Annu. Rev. Biochem. 87, 323–350.
  19. Kuroda M.I., Hilfiker A., Lucchesi J.C. (2016) Dosage compensation in Drosophila – a model for the coordinate regulation of transcription. Genetics. 204, 435–450.
  20. Keller C.I., Akhtar A. (2015) The MSL complex: juggling RNA–protein interactions for dosage compensation and beyond. Curr. Opin. Genet. Develop. 31, 1–11.
  21. Georgiev P., Chlamydas S., Akhtar A. (2011) Drosophila dosage compensation. Fly (Austin). 5, 147–154.
  22. Franke A., Baker B.S. (1999) The Rox1 and Rox2 RNAs are essential components of the compensasome, which mediates dosage compensation in Drosophila. Mol. Cell. 4, 117–122.
  23. Meller V.H. (2002) The RoX genes encode redundant male-specific lethal transcripts required for targeting of the MSL complex. EMBO J. 21, 1084–1091.
  24. Park S.-W., Kuroda M.I., Park Y. (2008) Regulation of histone H4 Lys16 acetylation by predicted alternative secondary structures in RoX noncoding RNAs. Mol. Cell. Biol. 28, 4952–4962.
  25. Park S.-W., Kang Y.I., Sypula J.G., Choi J., Oh H., Park Y. (2007) An evolutionarily conserved domain of RoX2 RNA is sufficient for induction of H4-Lys16 acetylation on the Drosophila X chromosome. Genetics. 177, 1429–1437.
  26. Stuckenholz C., Meller V.H., Kuroda M.I. (2003) Functional redundancy within roX1, a noncoding RNA involved in dosage compensation in Drosophila melanogaster. Genetics. 164, 1003–1014.
  27. Kelley R.L., Lee O.-K., Shim Y.-K. (2008) Transcription rate of noncoding roX1 RNA controls local spreading of the Drosophila MSL chromatin remodeling complex. Mech. Devel. 125, 1009–1019.
  28. Ilik I.A., Quinn J., Georgiev P., Tavares-Cadete F., Maticzka D., Toscano S., Wan Y., Spitale R., Luscombe N., Backofen R., Chang H., Akhtar A. (2013) Tandem stem-loops in roX RNAs act together to mediate X chromosome dosage compensation in Drosophila. Mol. Cell. 51, 156–173.
  29. Militti C., Maenner S., Becker P.B., Gebauer F. (2014) UNR facilitates the interaction of MLE with the lncRNA roX2 during Drosophila dosage compensation. Nat. Commun. 5, 4762.
  30. Maenner S., Müller M., Fröhlich J., Langer D., Becker P.B. (2013) ATP-dependent roX RNA remodeling by the helicase maleless enables specific association of MSL proteins. Mol. Cell. 51, 174–184.
  31. Bashaw G.J., Baker B.S. (1997) The regulation of the Drosophila msl-2 gene reveals a function for sex-lethal in translational control. Cell. 89, 789–798.
  32. Kelley R.L., Wang J., Bell L., Kuroda M.I. (1997) Sex lethal controls dosage compensation in Drosophila by a non-splicing mechanism. Nature. 387, 195–199.
  33. Morra R., Smith E.R., Yokoyama R., Lucchesi J.C. (2008) The MLE subunit of the Drosophila MSL complex uses its ATPase activity for dosage compensation and its helicase activity for targeting. Mol. Cell. Biol. 28, 958–966.
  34. Morra R., Yokoyama R., Ling H., Lucchesi J.C. (2011) Role of the ATPase/helicase maleless (MLE) in the assembly, targeting, spreading and function of the male-specific lethal (MSL) complex of Drosophila. Epigenet. Chromatin. 4, 6.
  35. Akhtar A., Becker P.B. (2000) Activation of transcription through histone H4 acetylation by MOF, an acetyltransferase essential for dosage compensation in Drosophila. Mol. Cell. 5, 367–375.
  36. Sun L., Johnson A.F., Donohue R.C., Li J., Cheng J., Birchler J.A. (2013) Dosage compensation and inverse effects in triple X metafemales of Drosophila. Proc. Natl. Acad. Sci. USA. 110, 7383–7388.
  37. Deng X., Meller V.H. (2006) roX RNAs are required for increased expression of X-linked genes in Drosophila melanogaster males. Genetics. 174, 1859–1866.
  38. Straub T., Gilfillan G.D., Maier V.K., Becker P.B. (2005) The Drosophila MSL complex activates the transcription of target genes. Genes Dev. 19, 2284–2288.
  39. Hamada F.N., Park P.J., Gordadze P.R., Kuroda M.I. (2005) Global regulation of X chromosomal genes by the MSL complex in Drosophila melanogaster. Genes Dev. 19, 2289–2294.
  40. Aleman J.R., Kuhn T.M., Pascual-Garcia P., Gospocic J., Lan Y., Bonasio R., Little S.C., Capelson M. (2021) Correct dosage of X chromosome transcription is controlled by a nuclear pore component. Cell Rep. 35, 109236.
  41. Bhadra U., Gandhi S.G., Palaparthi R., Balyan M.K., Pal-Bhadra M. (2016) Drosophila maleless gene counteracts X global aneuploid effects in males. FEBS J. 283, 3457–3470.
  42. Sun L., Fernandez H.R., Donohue R.C., Li J., Cheng J., Birchler J.A. (2013) Male-specific lethal complex in Drosophila counteracts histone acetylation and does not mediate dosage compensation. Proc. Natl. Acad. Sci. USA. 110, E808–E817.
  43. Sun L., Johnson A.F., Li J., Lambdin A.S., Cheng J., Birchler J.A. (2013) Differential effect of aneuploidy on the X chromosome and genes with sex-biased expression in Drosophila. Proc. Natl. Acad. Sci. USA. 110, 16514–16519.
  44. Zhang S., Qi H., Huang C., Yuan L., Zhang L., Wang R., Tian Y., Sun L. (2021) Interaction of male specific lethal complex and genomic imbalance on global gene expression in Drosophila. Sci. Rep. 11, 19679.
  45. Birchler J.A. (2016) Parallel universes for models of X chromosome dosage compensation in Drosophila: a review. Cytogenet. Genome Res. 148, 52–67.
  46. Nawata H., Kashino G., Tano K., Daino K., Shimada Y., Kugoh H., Oshimura M., Watanabe M. (2011) Dysregulation of gene expression in the artificial human trisomy cells of chromosome 8 associated with transformed cell phenotypes. PLoS One. 6, e25319.
  47. Torres E.M., Williams B.R., Amon A. (2008) Aneuploidy: cells losing their balance. Genetics. 179, 737–746.
  48. Jallepalli P.V., Pellman D. (2007) Aneuploidy in the balance. Science. 317, 904–905.
  49. Williams B.R., Amon A. (2009) Aneuploidy: cancer’s fatal flaw? Cancer Res. 69, 5289–5291.
  50. Taylor A.M., Shih J., Ha G., Gao G.F., Zhang X., Berger A.C., Schumacher S.E., Wang C., Hu H., Liu J., Lazar A.J., Cancer Genome Atlas Research Network; Cherniack A.D., Beroukhim R., Meyerson M. (2018) Genomic and functional approaches to understanding cancer aneuploidy. Cancer Cell. 33, 676–689,e3.
  51. Aratani S., Fujii R., Fujita H., Fukamizu A., Nakajima T. (2003) Aromatic residues are required for RNA helicase A mediated transactivation. Int. J. Mol. Med. 12, 175–180.
  52. Aratani S., Fujii R., Oishi T., Fujita H., Amano T., Ohshima T., Hagiwara M., Fukamizu A., Nakajima T. (2001) Dual roles of RNA helicase A in CREB-dependent transcription. Mol. Cell. Biol. 21, 4460–4469.
  53. Kotlikova I.V., Demakova O.V., Semeshin V.F., Shloma V.V., Boldyreva L.V., Kuroda M.I., Zhimulev I.F. (2006) The Drosophila dosage compensation complex binds to polytene chromosomes independently of developmental changes in transcription. Genetics. 172, 963–974.
  54. Ish-Horowicz D., Pinchin S.M., Gausz J., Gyurkovics H., Bencze G., Goldschmidt-Clermont M., Holden J.J. (1979) Deletion mapping of two D. melanogaster loci that code for the 70,000 dalton heat-induced protein. Cell. 17, 565–571.
  55. Sharma A., Lakhotia S.C. (1995) In situ quantification of hsp70 and alpha-beta transcripts at 87A and 87C loci in relation tohsr-omega gene activity in polytene cells of Drosophila melanogaster. Chromosome Res. 3, 386–393.
  56. Myöhänen S., Baylin S.B. (2001) Sequence-specific DNA binding activity of RNA helicase A to the p16 promoter. J. Biol. Chem. 276, 1634–1642.
  57. Zhong X., Safa A.R. (2004) RNA helicase A in the MEF1 transcription factor complex up-regulates the MDR1 gene in multidrug-resistant cancer cells. J. Biol. Chem. 279, 17134–17141.
  58. Huo L., Wang Y.-N., Xia W., Hsu S.-C., Lai C.-C., Li L.-Y., Chang W.-C., Wang Y., Hsu M.-C., Yu Y.-L., Huang T.-H., Ding Q., Chen C.-H., Tsai C.-H., Hung M.-C. (2010) RNA helicase A is a DNA-binding partner for EGFR-mediated transcriptional activation in the nucleus. Proc. Natl. Acad. Sci. USA. 107, 16125–16130.
  59. Nakajima T., Uchida C., Anderson S.F., Lee C.-G., Hurwitz J., Parvin J.D., Montminy M. (1997) RNA helicase A mediates association of CBP with RNA polymerase II. Cell. 90, 1107–1112.
  60. Anderson S.F., Schlegel B.P., Nakajima T., Wolpin E.S., Parvin J.D. (1998) BRCA1 protein is linked to the RNA polymerase II holoenzyme complex via RNA helicase A. Nat. Genet. 19, 254–256.
  61. Colla E., Lee S.D., Sheen M.R., Woo S.K., Kwon H.M. (2006) TonEBP is inhibited by RNA helicase A via interaction involving the E′F loop. Biochem. J. 393, 411–419.
  62. Kernan M.J., Kuroda M.I., Kreber R., Baker B.S., Ganetzky B. (1991) napts, a mutation affecting sodium channel activity in Drosophila, is an allele of mle a regulator of X chromosome transcription. Cell. 66, 949–959.
  63. Reenan R.A., Hanrahan C.J., Ganetzky B. (2000) The mle(napts) RNA helicase mutation in Drosophila results in a splicing catastrophe of the para Na+ channel transcript in a region of RNA editing. Neuron. 25, 139–149.
  64. Hanrahan C.J., Palladino M.J., Ganetzky B., Reenan R.A. (2000) RNA editing of the Drosophila para Na+ channel transcript: evolutionary conservation and developmental regulation. Genetics. 155, 1149–1160.
  65. Cugusi S., Kallappagoudar S., Ling H., Lucchesi J.C. (2015) The Drosophila helicase maleless (MLE) is implicated in functions distinct from its role in dosage compensation. Mol. Cell. Proteomics. 14, 1478–1488.
  66. Piacentini L., Fanti L., Negri R., del Vescovo V., Fatica A., Altieri F., Pimpinelli S. (2009) Heterochromatin protein 1 (HP1a) positively regulates euchromatic gene expression through RNA transcript association and interaction with hnRNPs in Drosophila. PLoS Genet. 5, e1000670.
  67. Herold N., Will C.L., Wolf E., Kastner B., Urlaub H., Lührmann R. (2009) Conservation of the protein composition and electron microscopy structure of Drosophila melanogaster and human spliceosomal complexes. Mol. Cell. Biol. 29, 281–301.
  68. Borah S., Wong A.C., Steitz J.A. (2009) Drosophila hnRNP A1 homologs Hrp36/Hrp38 enhance U2-type versus U12-type splicing to regulate alternative splicing of the prospero twintron. Proc. Natl. Acad. Sci. USA. 106, 2577–2582.
  69. Hartmuth K., Urlaub H., Vornlocher H.-P., Will C.L., Gentzel M., Wilm M., Lührmann R. (2002) Protein composition of human prespliceosomes isolated by a tobramycin affinity-selection method. Proc. Natl. Acad. Sci. USA. 99, 16719–16724.
  70. Zhang S., Herrmann C., Grosse F. (1999) Pre-mRNA and mRNA binding of human nuclear DNA helicase II (RNA helicase A). J. Cell Sci. 112, 1055–1064.
  71. Paul S., Dansithong W., Jog S.P., Holt I., Mittal S., Brook J.D., Morris G.E., Comai L., Reddy S. (2011) Expanded CUG repeats dysregulate RNA splicing by altering the stoichiometry of the muscleblind 1 complex. J. Biol. Chem. 286, 38427–38438.
  72. Terns M.P., Terns R.M. (2001) Macromolecular complexes: SMN – the master assembler. Curr. Biol. 11, R862–R864.
  73. Bratt E., Öhman M. (2003) Coordination of editing and splicing of glutamate receptor pre-mRNA. RNA. 9, 309–318.
  74. Cugusi S., Li Y., Jin P., Lucchesi J.C. (2016) The Drosophila helicase MLE targets hairpin structures in genomic transcripts. PLoS Genet. 12, e1005761.
  75. Николенко Ю.В., Куршакова М.М., Краснов А.Н., Георгиева С.Г. (2021) Хеликаза MLE – новый участник регуляции транскрипции гена ftz-f1, кодирующего ядерный рецептор у высших эукариот. Докл. Акад. Наук. Науки о жизни. 496, 48–51.
  76. Ilik I.A., Maticzka D., Georgiev P., Gutierrez N.M., Backofen R., Akhtar A. (2017) A mutually exclusive stem–loop arrangement in roX2 RNA is essential for X-chromosome regulation in Drosophila. Genes Dev. 31, 1973–1987.
  77. Ni J.Q., Markstein M., Binari R., Pfeiffer B., Liu L.-P., Villalta C., Booker M., Perkins L., Perrimon N. (2008) Vector and parameters for targeted transgenic RNA interference in Drosophila melanogaster. Nat. Meth. 5, 49–51.
  78. Ni J.Q., Liu L.P., Binari R., Hardy R., Shim H.S., Cavallaro A., Booker M., Pfeiffer B.D., Markstein M., Wang H., Villalta C., Laverty T., Perkins L., Perrimon N. (2009) A Drosophila resource of transgenic RNAi lines for neurogenetics. Genetics. 182, 1089–1100.
  79. Ni J.Q., Zhou R., Czech B., Liu L.P., Holderbaum L., Yang-Zhou D., Shim H.S., Tao R., Handler D., Karpowicz P., Binari R., Booker M., Brennecke J., Perkins L., Hannon G., Perrimon N. (2011) A genome-scale shRN-A resource for transgenic RNAi in Drosophila. Nat. Meth. 8, 405–407.
  80. Dietzl G., Chen D., Schnorrer F., Su K., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., Couto A., Marra V., Keleman K., Dickson B. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature. 448, 151–156.
  81. Fu Q., Yuan Y.A. (2013) Structural insights into RISC assembly facilitated by dsRNA-binding domains of human RNA helicase A (DHX9). Nucl. Acids Res. 41, 12–23.
  82. Robb G.B., Rana T.M. (2007) RNA helicase a interacts with RISC in human cells and functions in RISC loading. Mol. Cell. 26, 523–537.
  83. Liang X., Crooke S.T. (2013) RNA helicase A is not required for RISC activity. Biochim. Biophys. Acta (BBA) – Gene Regul. Mech. 1829, 1092–1101.
  84. Moshkin Y.M., Chalkley G., Kan T., Reddy B., Ozgur Z., van ljcken W., Dekkers D., Demmers J., Travers A., Verrijzer C.P. (2012) Remodelers organize cellular chromatin by counteracting intrinsic histone-DNA sequence preferences in a class-specific manner. Mol. Cell. Biol. 32, 675–688.
  85. Reddy B.A., Bajpe P.K., Bassett A., Moshkin Y.M., Kozhevnikova E., Bezstarosti K., Demmers J.A.A., Travers A.A., Verrijzer C.P. (2010) Drosophila transcription factor Tramtrack69 binds MEP1 to recruit the chromatin remodeler NuRD. Mol. Cell. Biol. 30, 5234–5244.
  86. Kunert N., Wagner E., Murawska M., Klinker H., Kremmer E., Brehm A. (2009) dMec: a novel Mi-2 chromatin remodelling complex involved in transcriptional repression. EMBO J. 28, 533–544.
  87. Murawska M., Hassler M., Renkawitz-Pohl R., Ladurner A., Brehm A. (2011) Stress-induced PARP activation mediates recruitment of Drosophila Mi-2 to promote heat shock gene expression. PLoS Genet. 7, e1002206.
  88. Fasulo B., Deuring R., Murawska M., Gause M., Dorighi K.M., Schaaf C.A., Dorsett D., Brehm A., Tamkun J.W. (2012) The Drosophila Mi-2 chromatin-remodeling factor regulates higher-order chromatin structure and cohesin dynamics in vivo. PLoS Genet. 8, e1002878.
  89. Николенко Ю.В., Краснов А.Н., Воробьева Н.Е. Ремоделирующий хроматин комплекс SWI/SNF влияет на пространственную организацию локуса гена ftz-f1. (2019) Генетика. 55, 156–164.
  90. Николенко Ю.В., Краснов А.Н., Мазина М.Ю., Георгиева С.Г., Воробьева Н.Е. (2017) Изучение свойств нового экдизонзависимого энхансера. Докл. Акад. Наук. 474, 756–759.
  91. Vorobyeva N.E., Nikolenko J.V., Nabirochkina E.N., Krasnov A.N., Shidlovskii Y.V., Georgieva S.G. (2012) SAYP and Brahma are important for ‘repressive’ and ‘transient’ Pol II pausing. Nucl. Acids Res. 40, 7319–7331.
  92. Amero S.A., Matunis M.J., Matunis E.L., Hockensmith J.W., Raychaudhuri G., Beyer A.L. (1993) A unique ribonucleoprotein complex assembles preferentially on ecdysone-responsive sites in Drosophila melanogaster. Mol. Cell. Biol. 13, 5323–5330.
  93. Николенко Ю.В., Куршакова М.М., Краснов А.Н. (2019) Мультифункциональный белок ENY2 взаимодействует с РНК-хеликазой MLE. Докл. Акад. Наук. 489, 637–640.
  94. Georgieva S., Nabirochkina E., Dilworth F.J., Eickhoff H., Becker P., Tora L., Georgiev P., Soldatov A. (2001) The novel transcription factor e(y)2 interacts with TAFII 40 and potentiates transcription activation on chromatin templates. Mol. Cell. Biol. 21, 5223–5231.
  95. Gurskiy D., Orlova A., Vorobyeva N., Nabirochkina E., Krasnov A., Shidlovskii Y., Georgieva S., Kopytova D. (2012) The DUBm subunit Sgf11 is required for mRNA export and interacts with Cbp80 in Drosophila. Nucl. Acids Res. 40, 10689–10700.
  96. Николенко Ю.В., Вдовинa Ю.А., Фефеловa Е.И., Глуховa А.А., Набирочкина Е.Н., Копытова Д.В. (2021) Деубиквитинирующий (DUB) модуль SAG-A участвует в Pol III-зависимой транскрипции. Молекуляр. биология. 55, 500–509.
  97. Kopytova D.V., Krasnov A.N., Orlova A.V., Gurskiy D.Ya., Nabirochkina E.N., Georgieva S.G., Shidlovskii Y.V. (2010) ENY2: Couple, triple … more? Cell Cycle. 9, 479–481.
  98. Popova V.V., Orlova A.V., Kurshakova M.M., Nikolenko J.V., Nabirochkina E.N., Georgieva S.G., Kopytova D.V. (2018) The role of SAGA coactivator complex in snRNA transcription. Cell Cycle. 17, 1859–1870.
  99. Kopytova D.V., Orlova A.V., Krasnov A.N., Gurskiy D.Ya., Nikolenko J.V., Nabirochkina E.N., Shidlovskii Y.V., Georgieva S.G. (2010) Multifunctional factor ENY2 is associated with the THO complex and promotes its recruitment onto nascent mRNA. Genes Dev. 24, 86–96.
  100. Фурсова Н.А., Николенко Ю.В., Сошникова Н.В., Мазина М.Ю., Воробьева Н.Е., Краснов А.Н. (2018) Белок CG9890 с доменами цинковых пальцев – новый компонент ENY2-содержащих комплексов дрозофилы. Acta Naturae. 10. 110–114.
  101. Zhou K. (2003) RNA helicase A interacts with dsDNA and topoisomerase II alpha. Nucl. Acids Res. 31, 2253–2260.
  102. Hartman T.R., Qian S., Bolinger C., Fernandez S., Schoenberg D.R., Boris-Lawrie K. (2006) RNA helicase A is necessary for translation of selected messenger RNAs. Nat. Struct. Mol. Biol. 13, 509–516.
  103. Ranji A., Shkriabai N., Kvaratskhelia M., Musier-Forsyth K., Boris-Lawrie K. (2011) Features of double-stranded RNA-binding domains of RNA helicase A are necessary for selective recognition and translation of complex mRNAs. J. Biol. Chem. 286, 5328–5337.
  104. Zhang S., Buder K., Burkhardt C., Schlott B., Görlach M., Grosse F. (2002) Nuclear DNA helicase II/RNA helicase A binds to filamentous actin. J. Biol. Chem. 277, 843–853.
  105. Tang H., Wong-Staal F. (2000) Specific interaction between RNA helicase A and tap, two cellular proteins that bind to the constitutive transport element of type D retrovirus. J. Biol. Chem. 275, 32694–32700.
  106. Wei X., Pacyna-Gengelbach M., Schlüns K., An Q., Gao Y., Cheng S., Petersen I. (2004) Analysis of the RNA helicase A gene in human lung cancer. Oncol. Rep. 11, 253–258.
  107. Sun Z., Wang L., Eckloff B., Deng B., Wang Y., Wampfler J., Jang J., Wieben E., Jen J., You M., Yang P. (2014) Conserved recurrent gene mutations correlate with pathway deregulation and clinical outcomes of lung adenocarcinoma in never-smokers. BMC Med. Genomics. 7, 486.
  108. Lee T., Paquet M., Larsson O., Pelletier J. (2016) Tumor cell survival dependence on the DHX9 DExH-box helicase. Oncogene. 35, 5093–5105.
  109. Chen Z.X., Wallis K., Fell S., Sobrado V., Hemmer M., Ramsköld D., Hellman U., Sandberg R., Kenchappa R., Martinson T., Johnsen J., Kogner P., Schlisio S. (2014) RNA helicase A is a downstream mediator of KIF1Bβ tumor-suppressor function in neuroblastoma. Cancer Discovery. 4, 434–451.
  110. Xing L., Niu M., Zhao X., Kleiman L. (2013) Roles of the linker region of RNA helicase A in HIV-1 RNA metabolism. PLoS One. 8, e78596.
  111. He Q.S., Tang H., Zhang J., Truong K., Wong-Staal F., Zhou D. (2008) Comparisons of RNAi approaches for validation of human RNA helicase A as an essential factor in hepatitis C virus replication. J. Virol. Meth. 154, 216–219.
  112. Lenarcic E.M., Ziehr B.J., Moorman N.J. (2015) An unbiased proteomics approach to identify human cytomegalovirus RNA-associated proteins. Virology. 481, 13–23.
  113. Liao H.-J., Kobayashi R., Mathews M.B. (1998) Activities of adenovirus virus-associated RNAs: purification and characterization of RNA binding proteins. Proc. Natl. Acad. Sci. USA. 95, 8514–8519.
  114. Fuchsová B., Novák P., Kafková J., Hozák P. (2002) Nuclear DNA helicase II is recruited to IFN-α–activated transcription sites at PML nuclear bodies. J. Cell Biol. 158, 463–473.
  115. Sadler A.J., Latchoumanin O., Hawkes D., Mak J., Williams B.R.G. (2009) An antiviral response directed by PKR phosphorylation of the RNA helicase A. PLoS Pathogens. 5, e1000311.
  116. Yamasaki Y., Narain S., Yoshida H., Hernandez L., Barker T., Hahn P., Sobel E., Segal M., Richards H., Chan E., Reeves W., Satoh M. (2007) Autoantibodies to RNA helicase A: a new serologic marker of early lupus. Arthritis Rheumatism. 56, 596–604.
  117. Vazquez-Del Mercado M., Palafox-Sanchez C., Munoz-Valle J., Orozco-Barocio G., Oregon-Romero E., Navarro-Hernandez R., Salazar-Paramo M., Armendariz-Borunda J., Gamez-Nava J., Gonzalez-Lopez L., Chan J., Chan E., Satoh M. (2010) High prevalence of autoantibodies to RNA helicase A in Mexican patients with systemic lupus erythematosus. Arthritis Res. Therapy. 12, R6

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