Skip to main content
SpringerLink
Log in

Regulation of Transcription by RNA Polymerase III Promotors in the Norm and Pathology

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

Abstract—RNA polymerase III synthesizes a wide range of noncoding RNAs shorter than 400 nucleotides in length. These RNAs are involved in protein synthesis (tRNA, 5S rRNA, and 7SL RNA), maturation, and splicing of different types of RNA (RPR, MRP RNA, and U6 snRNA), regulation of transcription (7SK RNA), replication (Y RNA), and intracellular transport (vault RNA). BC200 and BC1 RNA genes are transcribed by RNA polymerase III in neurons only where these RNAs regulate protein synthesis. Mutations in the regulatory elements of the genes transcribed by RNA polymerase III as well as in transcription factors of this RNA polymerase are associated with the development of a number of diseases, primarily oncological and neurological. In this regard, the mechanisms of regulation of the expression of the genes containing various RNA polymerase III promoters were actively studied. This review describes the structural and functional classification of polymerase III promoters, as well as the factors involved in the regulation of promoters of different types. A number of examples demonstrate the role of the described factors in the pathogenesis of human diseases.

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.

Similar content being viewed by others

REFERENCES

  1. Yeganeh M., Hernandez N. 2020. RNA polymerase III transcription as a disease factor. Genes Dev. 34, 865‒882.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Wolffe A.P. 1991. RNA polymerase III transcription. Curr. Opin. Cell Biol. 3, 461‒466.

    Article  CAS  PubMed  Google Scholar 

  3. Walter P., Blobel G. 1982. Signal recognition particle contains a 7S RNA essential for protein translocation across the endoplasmic reticulum. Nature. 299, 691‒698.

    Article  CAS  PubMed  Google Scholar 

  4. Brow D.A., Guthrie C. 1988. Spliceosomal RNA U6 is remarkably conserved from yeast to mammals. Nature. 334, 213‒218.

    Article  CAS  PubMed  Google Scholar 

  5. Kulaberoglu Y., Malik Y., Borland G., Selman C., Alic N., Tullet J.M.A. 2021. RNA polymerase III, ageing and longevity. Front. Genet. 12, 705122.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Yoshimoto R., Nakayama Y., Yamamoto I., Tanaka S., Kurihara M., Suzuki Y., Kobayashi T., Kozuka-Hata H., Oyama M., Mito M., Iwasaki S., Yamazaki T., Hirose T., Araki K., Nakagawa S. 2022. 4.5SH RNA counteracts deleterious exonization of SINE B1 in mice. Res. Square. https://assets.researchsquare.com/files/rs-1949270/v1_covered.pdf?c= 1664371339.

  7. Yoshimoto R., Nakagawa S. 2023. SINE-derived short noncoding RNAs: Their evolutionary origins, molecular mechanisms, and physiological significance. Front. RNA Res. 1, 1‒7.

    Article  Google Scholar 

  8. Kikovska E., Svard S.G., Kirsebom L.A. 2007. Eukaryotic RNase P RNA mediates cleavage in the absence of protein. Proc. Natl. Acad. Sci. U. S. A. 104, 2062‒2067.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Horos R., Buscher M., Kleinendorst R., Alleau-me A.M., Tarafder A.K., Schwarzl T., Dziuba D., Tischer C., Zielonka E.M., Adak A., Castello A., Hu-ber W., Sachse C., Hentze M.W. 2019. The small non-coding vault RNA1-1 acts as a riboregulator of autophagy. Cell. 176, 1054‒1067 e1012.

  10. Kheir E., Krude T. 2017. Non-coding Y RNAs associate with early replicating euchromatin in concordance with the origin recognition complex. J. Cell Sci. 130, 1239‒1250.

    CAS  PubMed  Google Scholar 

  11. Quaresma A.J., Bugai A., Barboric M. 2016. Cracking the control of RNA polymerase II elongation by 7SK snRNP and P-TEFb. Nucleic Acids Res. 44, 7527‒7539.

    Article  Google Scholar 

  12. Oler A.J., Alla R.K., Roberts D.N., Wong A., Hollenhorst P.C., Chandler K.J., Cassiday P.A., Nelson C.A., Hagedorn C.H., Graves B.J., Cairns B.R. 2010. Human RNA polymerase III transcriptomes and relationships to Pol II promoter chromatin and enhancer-binding factors. Nat. Struct. Mol. Biol. 17, 620‒628.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Lin D., Pestova T.V., Hellen C.U., Tiedge H. 2008. Translational control by a small RNA: Dendritic BC1 RNA targets the eukaryotic initiation factor 4A helicase mechanism. Mol. Cell Biol. 28, 3008‒3019.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ludwig A., Rozhdestvensky T.S., Kuryshev V.Y., Schmitz J., Brosius J. 2005. An unusual primate locus that attracted two independent Alu insertions and facilitates their transcription. J. Mol. Biol. 350, 200‒214.

    Article  CAS  PubMed  Google Scholar 

  15. Kramerov D.A., Vassetzky N.S. 2005. Short retroposons in eukaryotic genomes. Int. Rev. Cytol. 247, 165‒221.

    Article  CAS  PubMed  Google Scholar 

  16. Kramerov D.A., Vassetzky N.S. 2011. SINEs. Wiley Interdiscip. Rev. RNA. 2, 772‒786.

    Article  CAS  PubMed  Google Scholar 

  17. Parrott A.M., Tsai M., Batchu P., Ryan K., Ozer H.L., Tian B., Mathews M.B. 2011. The evolution and expression of the snaR family of small non-coding RNAs. Nucleic Acids Res. 39, 1485‒1500.

    Article  CAS  PubMed  Google Scholar 

  18. Kim J., Martignetti J.A., Shen M.R., Brosius J., Deininger P. 1994. Rodent BC1 RNA gene as a master gene for ID element amplification. Proc. Natl. Acad. Sci. U. S. A. 91, 3607‒3611.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Gogolevskaya I.K., Kramerov D.A. 2002. Evolutionary history of 4.5SI RNA and indication that it is functional. J. Mol. Evol. 54, 354‒364.

    Article  CAS  PubMed  Google Scholar 

  20. Gogolevskaya I.K., Koval A.P., Kramerov D.A. 2005. Evolutionary history of 4.5SH RNA. Mol. Biol. Evol. 22, 1546‒1554.

    Article  CAS  PubMed  Google Scholar 

  21. Tatosyan K.A., Koval A.P., Gogolevskaya I.K., Kra-merov D.A. 2017. 4.5SI and 4.5SH RNAs: Expression in various rodent organs and abundance and distribution in the cell. Mol. Biol. (Moscow) 51, 122‒129. https://doi.org/10.1134/S0026893317010174

    Article  CAS  Google Scholar 

  22. Arimbasseri A.G., Rijal K., Maraia R.J. 2013. Transcription termination by the eukaryotic RNA polymerase III. Biochim. Biophys. Acta. 1829, 318‒330.

    Article  CAS  PubMed  Google Scholar 

  23. Vassetzky N.S., Borodulina O.R., Ustyantsev I.G., Kosushkin S.A., Kramerov D.A. 2021. Analysis of SINE families B2, Dip, and Ves with special reference to polyadenylation signals and transcription terminators. Int. J. Mol. Sci. 22 (18), 9897.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Orioli A., Pascali C., Quartararo J., Diebel K.W., Praz V., Romascano D., Percudani R., van Dyk L.F., Hernandez N., Teichmann M., Dieci G. 2011. Widespread occurrence of non-canonical transcription termination by human RNA polymerase III. Nucleic Acids Res. 39, 5499‒5512.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Mus E., Hof P.R., Tiedge H. 2007. Dendritic BC200 RNA in aging and in Alzheimer’s disease. Proc. Natl. Acad. Sci. U. S. A. 104, 10679‒10684.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Borck G., Hog F., Dentici M.L., Tan P.L., Sowada N., Medeira A., Gueneau L., Thiele H., Kousi M., Lepri F., Wenzeck L., Blumenthal I., Radicioni A., Schwarzenberg T.L., Mandriani B., Fischetto R., Morris-Rosendahl D.J., Altmuller J., Reymond A., Nurnberg P., Merla G., Dallapiccola B., Katsanis N., Cramer P., Kubisch C. 2015. BRF1 mutations alter RNA polymerase III-dependent transcription and cause neurodevelopmental anomalies. Genome Res. 25, 155‒166.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Zhong Q., Xi S., Liang J., Shi G., Huang Y., Zhang Y., Levy D., Zhong S. 2016. The significance of Brf1 overexpression in human hepatocellular carcinoma. Oncotarget. 7, 6243‒6254.

    Article  PubMed  Google Scholar 

  28. Leal J.F., Fominaya J., Cascon A., Guijarro M.V., Blanco-Aparicio C., Lleonart M., Castro M.E., Ramon Y.C.S., Robledo M., Beach D.H., Carnero A. 2008. Cellular senescence bypass screen identifies new putative tumor suppressor genes. Oncogene. 27, 1961‒1970.

    Article  CAS  PubMed  Google Scholar 

  29. Lockwood W.W., Chari R., Coe B.P., Thu K.L., Garnis C., Malloff C.A., Campbell J., Williams A.C., Hwang D., Zhu C.Q., Buys T.P., Yee J., English J.C., Macaulay C., Tsao M.S., Gazdar A.F., Minna J.D., Lam S., Lam W.L. 2010. Integrative genomic analyses identify BRF2 as a novel lineage-specific oncogene in lung squamous cell carcinoma. PLoS Med. 7, e1000315.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Wambach J.A., Wegner D.J., Patni N., Kircher M., Willing M.C., Baldridge D., Xing C., Agarwal A.K., Vergano S.A.S., Patel C., Grange D.K., Kenney A., Najaf T., Nickerson D.A., Bamshad M.J., Cole F.S., Garg A. 2018. Bi-allelic POLR3A loss-of-function variants cause autosomal-recessive wiedemann-rautenstrauch syndrome. Am. J. Hum. Genet. 103, 968‒975.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Francisco S., Ferreira M., Moura G., Soares A.R., Santos M.A.S. 2020. Does proteostasis get lost in translation? Implications for protein aggregation across the lifespan. Ageing. Res. Rev. 62, 101119.

    Article  CAS  PubMed  Google Scholar 

  32. Guzzi N., Bellodi C. 2020. Novel insights into the emerging roles of tRNA-derived fragments in mammalian development. RNA Biol. 17, 1214‒1222.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Schramm L., Hernandez N. 2002. Recruitment of RNA polymerase III to its target promoters. Genes Dev. 16, 2593‒2620.

    Article  CAS  PubMed  Google Scholar 

  34. Bogenhagen D.F. 1985. The intragenic control region of the Xenopus 5S RNA gene contains two factor A binding domains that must be aligned properly for efficient transcription initiation. J. Biol. Chem. 260, 6466‒6471.

    Article  CAS  PubMed  Google Scholar 

  35. Arnold G.J., Kahnt B., Herrenknecht K., Gross H.J. 1987. A variant gene and a pseudogene for human 5S RNA are transcriptionally active in vitro. Gene. 60, 137‒144.

    Article  CAS  PubMed  Google Scholar 

  36. Hallenberg C., Frederiksen S. 2001. Effect of mutations in the upstream promoter on the transcription of human 5S rRNA genes. Biochim. Biophys. Acta. 1520, 169‒173.

    Article  CAS  PubMed  Google Scholar 

  37. Vierna J., Wehner S., Honer zu Siederdissen C., Martinez-Lage A., Marz M. 2013. Systematic analysis and evolution of 5S ribosomal DNA in metazoans. Heredity (Edinb.). 111, 410‒421.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ogilvie M.K., Hanas J.S. 1997. Molecular biology of vertebrate transcription factor IIIA: Cloning and characterization of TFIIIA from channel catfish oocytes. Gene. 203, 103‒112.

    Article  CAS  PubMed  Google Scholar 

  39. Paule M.R., White R.J. 2000. Survey and summary: Transcription by RNA polymerases I and III. Nucleic Acids Res. 28, 1283‒1298.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Dumay-Odelot H., Marck C., Durrieu-Gaillard S., Lefebvre O., Jourdain S., Prochazkova, M., Pflieger A., Teichmann M. 2007. Identification, molecular cloning, and characterization of the sixth subunit of human transcription factor TFIIIC. J. Biol. Chem. 282, 17179‒17189.

    Article  CAS  PubMed  Google Scholar 

  41. Lassar A.B., Martin P.L., Roeder R.G. 1983. Transcription of class III genes: Formation of preinitiation complexes. Science. 222, 740‒748.

    Article  CAS  PubMed  Google Scholar 

  42. Hsieh Y.J., Wang Z., Kovelman R., Roeder R.G. 1999. Cloning and characterization of two evolutionarily conserved subunits (TFIIIC102 and TFIIIC63) of human TFIIIC and their involvement in functional interactions with TFIIIB and RNA polymerase III. Mol. Cell. Biol. 19, 4944‒4952.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Hsieh Y.J., Kundu T.K., Wang Z., Kovelman R., Roeder R.G. 1999. The TFIIIC90 subunit of TFIIIC inte-racts with multiple components of the RNA polymerase III machinery and contains a histone-specific acetyltransferase activity. Mol. Cell Biol. 19, 7697‒7704.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Kenneth N.S., Ramsbottom B.A., Gomez-Roman N., Marshall L., Cole P.A., White R.J. 2007. TRRAP and GCN5 are used by c-Myc to activate RNA polymerase III transcription. Proc. Natl. Acad. Sci. U. S. A. 104, 14917‒14922.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. White R.J. 2005. RNA polymerases I and III, growth control and cancer. Nat. Rev. Mol. Cell Biol. 6, 69‒78.

    Article  CAS  PubMed  Google Scholar 

  46. Dorboz I., Dumay-Odelot H., Boussaid K., Bouyacoub Y., Barreau P., Samaan S., Jmel H., Eymard-Pierre E., Cances C., Bar C., Poulat A.L., Rousselle C., Renaldo F., Elmaleh-Berges M., Teichmann M., Boespflug-Tanguy O. 2018. Mutation in POLR3K causes hypomyelinating leukodystrophy and abnormal ribosomal RNA regulation. Neurol. Gen-et. 4, e289.

    Article  CAS  Google Scholar 

  47. Baez-Becerra C.T., Valencia-Rincon E., Velasquez-Mendez K., Ramirez-Suarez N.J., Guevara C., Sandoval-Hernandez A., Arboleda-Bustos C.E., Olivos-Cisneros L., Gutierrez-Ospina G., Arboleda H., Arboleda G. 2020. Nucleolar disruption, activation of P53 and premature senescence in POLR3A-mutated Wiedemann‒Rautenstrauch syndrome fibroblasts. Mech. Ageing Dev. 192, 111360.

    Article  CAS  PubMed  Google Scholar 

  48. Winter A.G., Sourvinos G., Allison S.J., Tosh K., Scott P.H., Spandidos D.A., White R.J. 2000. RNA polymerase III transcription factor TFIIIC2 is overexpressed in ovarian tumors. Proc. Natl. Acad. Sci. U. S. A. 97, 12619‒12624.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Fang Z., Yi Y., Shi G., Li S., Chen S., Lin Y., Li Z., He Z., Li W., Zhong S. 2017. Role of Brf1 interaction with ERalpha, and significance of its overexpression, in human breast cancer. Mol. Oncol. 11, 1752‒1767.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Sloan K.E., Bohnsack M.T., Watkins N.J. 2013. The 5S RNP couples p53 homeostasis to ribosome biogenesis and nucleolar stress. Cell Rep. 5, 237‒247.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Vassetzky N.S., Kramerov D.A. 2013. SINEBase: A database and tool for SINE analysis. Nucleic Acids Res. 41, D83‒89.

    Article  CAS  PubMed  Google Scholar 

  52. Giuliodori S., Percudani R., Braglia P., Ferrari R., Guffanti E., Ottonello S., Dieci G. 2003. A composite upstream sequence motif potentiates tRNA gene transcription in yeast. J. Mol. Biol. 333, 1‒20.

    Article  CAS  PubMed  Google Scholar 

  53. Zhang G., Lukoszek R., Mueller-Roeber B., Ignatova Z. 2011. Different sequence signatures in the upstream regions of plant and animal tRNA genes shape distinct modes of regulation. Nucleic Acids Res. 39, 3331‒3339.

    Article  CAS  PubMed  Google Scholar 

  54. Hamada M., Huang Y., Lowe T.M., Maraia R.J. 2001. Widespread use of TATA elements in the core promoters for RNA polymerases III, II, and I in fission yeast. Mol. Cell Biol. 21, 6870‒6881.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Conti A., Carnevali D., Bollati V., Fustinoni S., Pellegrini M., Dieci G. 2015. Identification of RNA polymerase III-transcribed Alu loci by computational screening of RNA-Seq data. Nucleic Acids Res. 43, 817‒835.

    Article  CAS  PubMed  Google Scholar 

  56. Tatosyan K.A., Stasenko D.V., Koval A.P., Gogolevskaya I.K., Kramerov D.A. 2020. TATA-like boxes in RNA polymerase III promoters: Requirements for nucleotide sequences. Int. J. Mol. Sci. 21 (10), 3706.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Geiduschek E.P., Kassavetis G.A. 2001. The RNA polymerase III transcription apparatus. J. Mol. Biol. 310, 1‒26.

    Article  CAS  PubMed  Google Scholar 

  58. Roy A.M., West N.C., Rao A., Adhikari P., Aleman C., Barnes A.P., Deininger P.L. 2000. Upstream flanking sequences and transcription of SINEs. J. Mol. Biol. 302, 17‒25.

    Article  CAS  PubMed  Google Scholar 

  59. Englert M., Felis M., Junker V., Beier H. 2004. Novel upstream and intragenic control elements for the RNA polymerase III-dependent transcription of human 7SL RNA genes. Biochimie. 86, 867‒874.

    Article  CAS  PubMed  Google Scholar 

  60. Kickhoefer V.A., Emre N., Stephen A.G., Poderycki M.J., Rome L.H. 2003. Identification of conserved vault RNA expression elements and a non-expressed mouse vault RNA gene. Gene. 309, 65‒70.

    Article  CAS  PubMed  Google Scholar 

  61. Gogolevskaya I.K., Stasenko D.V., Tatosyan K.A., Kramerov D.A. 2018. Influence of 5'-flanking sequence on 4.5SI RNA gene transcription by RNA polymerase III. Genome. 61, 367‒370.

    Article  CAS  PubMed  Google Scholar 

  62. Howe J.G., Shu M.D. 1993. Upstream basal promoter element important for exclusive RNA polymerase III transcription of the EBER 2 gene. Mol. Cell Biol. 13, 2655‒2665.

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Niller H.H., Salamon D., Ilg K., Koroknai A., Banati F., Bauml G., Rucker O., Schwarzmann F., Wolf H., Minarovits J. 2003. The in vivo binding site for oncoprotein c-Myc in the promoter for Epstein−Barr virus (EBV) encoding RNA (EBER) 1 suggests a specific role for EBV in lymphomagenesis. Med. Sci. Monit. 9, HY1‒9.

    CAS  PubMed  Google Scholar 

  64. Fowlkes D.M., Shenk T. 1980. Transcriptional control regions of the adenovirus VAI RNA gene. Cell. 22, 405‒413.

    Article  CAS  PubMed  Google Scholar 

  65. Piras G., Dittmer J., Radonovich M.F., Brady J.N. 1996. Human T-cell leukemia virus type I Tax protein transactivates RNA polymerase III promoter in vitro and in vivo. J. Biol. Chem. 271, 20501‒20506.

    Article  CAS  PubMed  Google Scholar 

  66. Stasenko D.V., Tatosyan K.A., Borodulina O.R., Kramerov D.A. 2023. Nucleotide context can modulate promoter strength in genes transcribed by RNA polymerase III. Genes (Basel). 14 (4), 802.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. White R.J., Jackson S.P. 1992. Mechanism of TATA-binding protein recruitment to a TATA-less class III promoter. Cell. 71, 1041‒1053.

    Article  CAS  PubMed  Google Scholar 

  68. Chesnokov I., Chu W.M., Botchan M.R., Schmid C.W. 1996. p53 inhibits RNA polymerase III-directed transcription in a promoter-dependent manner. Mol. Cell. Biol. 16, 7084‒7088.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Moqtaderi Z., Struhl K. 2004. Genome-wide occupancy profile of the RNA polymerase III machinery in Saccharomyces cerevisiae reveals loci with incomplete transcription complexes. Mol. Cell. Biol. 24, 4118‒4127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Kleinschmidt R.A., LeBlanc K.E., Donze D. 2011. Autoregulation of an RNA polymerase II promoter by the RNA polymerase III transcription factor III C (TF(III)C) complex. Proc. Natl. Acad. Sci. U. S. A. 108, 8385‒8389.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Chesnokov I., Schmid C.W. 1996. Flanking sequences of an Alu source stimulate transcription in vitro by interacting with sequence-specific transcription factors. J. Mol. Evol. 42, 30‒36.

    Article  CAS  PubMed  Google Scholar 

  72. Liu W.M., Maraia R.J., Rubin C.M., Schmid C.W. 1994. Alu transcripts: Cytoplasmic localisation and regulation by DNA methylation. Nucleic Acids Res. 22, 1087‒1095.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Varshney D., Vavrova-Anderson J., Oler A.J., Cowling V.H., Cairns B.R., White R.J. 2015. SINE transcription by RNA polymerase III is suppressed by histone methylation but not by DNA methylation. Nat. Commun. 6, 6569.

    Article  CAS  PubMed  Google Scholar 

  74. Varshney D., Vavrova-Anderson J., Oler A.J., Cairns B.R., White R.J. 2015. Selective repression of SINE transcription by RNA polymerase III. Mob. Genet. Elements. 5, 86‒91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Orellana E.A., Siegal E., Gregory R.I. 2022. tRNA dysregulation and disease. Nat. Rev. Genet. 23, 651‒664.

    Article  CAS  PubMed  Google Scholar 

  76. White R.J. 2011. Transcription by RNA polymerase III: More complex than we thought. Nat. Rev. Genet. 12, 459‒463.

    Article  CAS  PubMed  Google Scholar 

  77. Boyer L.A., Latek R.R., Peterson C.L. 2004. The SANT domain: A unique histone-tail-binding module? Nat. Rev. Mol. Cell Biol. 5, 158‒163.

    Article  CAS  PubMed  Google Scholar 

  78. Moqtaderi Z., Wang J., Raha D., White R.J., Snyder M., Weng Z., Struhl K. 2010. Genomic binding profiles of functionally distinct RNA polymerase III transcription complexes in human cells. Nat. Struct. Mol. Biol. 17, 635‒640.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Azmanov D.N., Siira S.J., Chamova T., Kaprelyan A., Guergueltcheva V., Shearwood A.J., Liu G., Morar B., Rackham O., Bynevelt M., Grudkova M., Kame-nov Z., Svechtarov V., Tournev I., Kalaydjieva L., Filipovska A. 2016. Transcriptome-wide effects of a POLR3A gene mutation in patients with an unusual phenotype of striatal involvement. Hum. Mol. Genet. 25, 4302‒4314.

    Article  CAS  PubMed  Google Scholar 

  80. Lata E., Choquet K., Sagliocco F., Brais B., Bernard G., Teichmann M. 2021. RNA polymerase III subunit mutations in genetic diseases. Front. Mol. Biosci. 8, 696438.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Abdelmohsen K., Panda A.C., Kang M.J., Guo R., Kim J., Grammatikakis I., Yoon J.H., Dudekula D.B., Noh J.H., Yang X., Martindale J.L., Gorospe M. 2014. 7SL RNA represses p53 translation by competing with HuR. Nucleic Acids Res. 42, 10099‒10111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Goodarzi H., Nguyen H.C.B., Zhang S., Dill B.D., Molina H., Tavazoie S.F. 2016. Modulated expression of specific tRNAs drives gene expression and cancer progression. Cell. 165, 1416‒1427.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Clarke C.J., Berg T.J., Birch J., Ennis D., Mitchell L., Cloix C., Campbell A., Sumpton D., Nixon C., Campbell K., Bridgeman V.L., Vermeulen P.B., Foo S., Kostaras E., Jones J.L., Haywood L., Pulleine E., Yin H., Strathdee D., Sansom O., Blyth K., McNeish I., Zanivan S., Reynolds A.R., Norman J.C. 2016. The initiator methionine tRNA drives secretion of type II collagen from stromal fibroblasts to promote tumor growth and angiogenesis. Curr. Biol. 26, 755‒765.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Muddashetty R., Khanam T., Kondrashov A., Bundman M., Iacoangeli A., Kremerskothen J., Duning K., Barnekow A., Huttenhofer A., Tiedge H., Brosius J. 2002. Poly(A)-binding protein is associated with neuronal BC1 and BC200 ribonucleoprotein particles. J. Mol. Biol. 321, 433‒445.

    Article  CAS  PubMed  Google Scholar 

  85. Chen X., Zhao Y., Wang D., Lin Y., Hou J., Xu X., Wu J., Zhong L., Zhou Y., Shen J., Zhang W., Cao H., Hong X., Hu T., Zhan Y.Y. 2021. The HNF4alpha-BC200-FMR1-positive feedback loop promotes growth and metastasis in invasive mucinous lung adenocarcinoma. Cancer Res. 81, 5904‒5918.

    Article  CAS  PubMed  Google Scholar 

  86. Wu D.I., Wang T., Ren C., Liu L., Kong D., Jin X., Li X., Zhang G. 2016. Down regulation of BC200 in ovarian cancer contributes to cancer cell proliferation and chemoresistance to carboplatin. Oncol. Lett. 11, 1189‒1194.

    Article  CAS  PubMed  Google Scholar 

  87. Lin Y.H., Wu M.H., Huang Y.H., Yeh C.T., Chi H.C., Tsai C.Y., Chuang W.Y., Yu C.J., Chung I.H., Chen C.Y., Lin K.H. 2018. Thyroid hormone negatively regulates tumorigenesis through suppression of BC200. Endocr. Relat. Cancer. 25, 967‒979.

    Article  CAS  PubMed  Google Scholar 

  88. Wu K., Xu K., Liu K., Huang J., Chen J., Zhang J., Zhang N. 2018. Long noncoding RNA BC200 regulates cell growth and invasion in colon cancer. Int. J. Biochem. Cell Biol. 99, 219‒225.

    Article  CAS  PubMed  Google Scholar 

  89. Shin H., Lee J., Kim Y., Jang S., Lee Y., Kim S., Lee Y. 2017. Knockdown of BC200 RNA expression reduces cell migration and invasion by destabilizing mRNA for calcium-binding protein S100A11. RNA Biol. 14, 1418‒1430.

    Article  PubMed  PubMed Central  Google Scholar 

  90. Hu T., Lu Y.R. 2015. BCYRN1, a c-MYC-activated long non-coding RNA, regulates cell metastasis of non-small-cell lung cancer. Cancer Cell Int. 15, 36.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Singh R., Gupta S.C., Peng W.X., Zhou N., Pochampally R., Atfi A., Watabe K., Lu Z., Mo Y.Y. 2016. Regulation of alternative splicing of Bcl-x by BC200 contributes to breast cancer pathogenesis. Cell Death Dis. 7, e2262.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Booy E.P., McRae E.K., Ezzati P., Choi T., Gussakovsky D., McKenna S.A. 2018. Comprehensive analysis of the BC200 ribonucleoprotein reveals a reciprocal regulatory function with CSDE1/UNR. Nucleic Acids Res. 46, 11575‒11591.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Lee K., Kunkeaw N., Jeon S.H., Lee I., Johnson B.H., Kang G.Y., Bang J.Y., Park H.S., Leelayuwat C., Lee Y.S. 2011. Precursor miR-886, a novel noncoding RNA repressed in cancer, associates with PKR and modulates its activity. RNA. 17, 1076‒1089.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Lee Y. S., Bao X., Lee H.H., Jang J.J., Saruuldalai E., Park G., Im W.R., Park J.L., Kim S.Y., Shin S., Jeon S.H., Kang S., Lee H.S., Lee J.S., Zhang K., Park E.J., Kim I.H., Lee Y.S. 2021. Nc886, a novel suppressor of the type I interferon response upon pathogen intrusion. Int. J. Mol. Sci. 22, 2003.

  95. Saruuldalai E., Park J., Kang D., Shin S.P., Im W.R., Lee H.H., Jang J.J., Park J.L., Kim S.Y., Hwang J.A., Kim Y.D., Lee J.H., Park E.J., Lee Y.S., Kim I.H., Lee S.J., Lee Y.S. 2022. A host non-coding RNA, nc886, plays a pro-viral role by promoting virus trafficking to the nucleus. Mol. Ther. Oncolytics. 24, 683‒694.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Di Ruocco F., Basso V., Rivoire M., Mehlen P., Ambati J., De Falco S., Tarallo V. 2018. Alu RNA accumulation induces epithelial-to-mesenchymal transition by modulating miR-566 and is associated with cancer progression. Oncogene. 37, 627‒637.

    Article  CAS  PubMed  Google Scholar 

  97. Kaneko H., Dridi S., Tarallo V., Gelfand B.D., Fowler B.J., Cho W.G., Kleinman M.E., Po-nicsan S.L., Hauswirth W.W., Chiodo V.A., Kariko K., Yoo J.W., Lee D.K., Hadziahmetovic M., Song Y., Misra S., Chaudhuri G., Buaas F.W., Braun R.E., Hinton D.R., Zhang Q., Grossniklaus H.E., Provis J.M., Madigan M.C., Milam A.H., Justice N.L., Albuquerque R.J., Blandford A.D., Bogdanovich S., Hirano Y., Witta J., Fuchs E., Littman D.R., Ambati B.K., Rudin C.M., Chong M.M., Provost P., Kugel J.F., Goodrich J.A., Dunaief J.L., Baffi J.Z., Ambati J. 2011. DICER1 deficit induces Alu RNA toxicity in age-related macular degeneration. Nature. 471, 325‒330.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Tarallo V., Hirano Y., Gelfand B.D., Dridi S., Kerur N., Kim Y., Cho W.G., Kaneko H., Fowler B.J., Bogdanovich S., Albuquerque R.J., Hauswirth W.W., Chiodo V.A., Kugel J.F., Goodrich J.A., Ponicsan,S.L., Chaudhuri G., Murphy M.P., Dunaief J.L., Ambati B.K., Ogura Y., Yoo J.W., Lee D.K., Provost P., Hinton D.R., Nunez G., Baffi J.Z., Kleinman M.E., Ambati J. 2012. DICER1 loss and Alu RNA induce age-related macular degeneration via the NLRP3 inflammasome and MyD88. Cell. 149, 847‒859.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Danzeiser D.A., Urso O., Kunkel G.R. 1993. Functional characterization of elements in a human U6 small nuclear RNA gene distal control region. Mol. Cell Biol. 13, 4670‒4678.

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Dieci G., Fiorino G., Castelnuovo M., Teichmann M., Pagano A. 2007. The expanding RNA polymerase III transcriptome. Trends Genet. 23, 614‒622.

    Article  CAS  PubMed  Google Scholar 

  101. Murphy S., Yoon J.B., Gerster T., Roeder R.G. 1992. Oct-1 and Oct-2 potentiate functional interactions of a transcription factor with the proximal sequence element of small nuclear RNA genes. Mol. Cell Biol. 12, 3247‒3261.

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Ramsay E.P., Vannini A. 2018. Structural rearrangements of the RNA polymerase III machinery during tRNA transcription initiation. Biochim. Biophys. Acta Gene Regul. Mech. 1861, 285‒294.

    Article  CAS  PubMed  Google Scholar 

  103. Mittal V., Ma B., Hernandez N. 1999. SNAP(c): A core promoter factor with a built-in DNA-binding damper that is deactivated by the Oct-1 POU domain. Genes Dev. 13, 1807‒1821.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Mittal V., Hernandez N. 1997. Role for the amino-terminal region of human TBP in U6 snRNA transcription. Science. 275, 1136‒1140.

    Article  CAS  PubMed  Google Scholar 

  105. Ma B., Hernandez N. 2001. A map of protein-protein contacts within the small nuclear RNA-activating protein complex SNAPc. J. Biol. Chem. 276, 5027‒5035.

    Article  CAS  PubMed  Google Scholar 

  106. Mittal V., Cleary M.A., Herr W., Hernandez N. 1996. The Oct-1 POU-specific domain can stimulate small nuclear RNA gene transcription by stabilizing the basal transcription complex SNAPc. Mol. Cell. Biol. 16, 1955‒1965.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Zhao X., Pendergrast P.S., Hernandez N. 2001. A positioned nucleosome on the human U6 promoter allows recruitment of SNAPc by the Oct-1 POU domain. Mol. Cell. 7, 539‒549.

    Article  CAS  PubMed  Google Scholar 

  108. Kowalski M.P., Krude T. 2015. Functional roles of non-coding Y RNAs. Int. J. Biochem. Cell Biol. 66, 20‒29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Christov C.P., Trivier E., Krude T. 2008. Noncoding human Y RNAs are overexpressed in tumours and required for cell proliferation. Br. J. Cancer. 98, 981‒988.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Tolkach Y., Niehoff E.M., Stahl A.F., Zhao C., Kristiansen G., Muller S.C., Ellinger J. 2018. YRNA expression in prostate cancer patients: Diagnostic and prognostic implications. World J. Urol. 36, 1073‒1078.

    Article  CAS  PubMed  Google Scholar 

  111. Appaiah H.N., Goswami C.P., Mina L.A., Badve S., Sledge G.W., Jr., Liu Y., Nakshatri H. 2011. Persistent upregulation of U6:SNORD44 small RNA ratio in the serum of breast cancer patients. Breast Cancer Res. 13, R86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Gouge J., Satia K., Guthertz N., Widya M., Thompson A.J., Cousin P., Dergai O., Hernandez N., Vannini A. 2015. Redox signaling by the RNA polymerase III TFIIB-related factor Brf2. Cell. 163, 1375‒1387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Massone S., Vassallo I., Fiorino G., Castelnuovo M., Barbieri F., Borghi R., Tabaton M., Robello M., Gatta E., Russo C., Florio T., Dieci G., Cancedda R., Pagano A. 2011. 17A, a novel non-coding RNA, regulates GABA B alternative splicing and signaling in response to inflammatory stimuli and in Alzheimer disease. Neurobiol. Dis. 41, 308‒317.

    Article  CAS  PubMed  Google Scholar 

  114. Massone S., Ciarlo E., Vella S., Nizzari M., Florio T., Russo C., Cancedda R., Pagano A. 2012. NDM29, a RNA polymerase III-dependent non coding RNA, promotes amyloidogenic processing of APP and amyloid beta secretion. Biochim. Biophys. Acta. 1823, 1170‒1177.

    Article  CAS  PubMed  Google Scholar 

  115. Ciarlo E., Massone S., Penna I., Nizzari, M., Gigoni A., Dieci G., Russo C., Florio T., Cancedda R., Pagano A. 2013. An intronic ncRNA-dependent regulation of SORL1 expression affecting Abeta formation is upregulated in post-mortem Alzheimer’s disease brain samples. Dis. Model. Mech. 6, 424‒433.

    CAS  PubMed  Google Scholar 

  116. Penna I., Vassallo I., Nizzari M., Russo D., Costa D., Menichini P., Poggi A., Russo C., Dieci G., Florio T., Cancedda R., Pagano A. 2013. A novel snRNA-like transcript affects amyloidogenesis and cell cycle progression through perturbation of Fe65L1 (APBB2) alternative splicing. Biochim. Biophys. Acta. 1833, 1511‒1526.

    Article  CAS  PubMed  Google Scholar 

  117. Lopez-Flores I., Garrido-Ramos M.A. 2012. The repetitive DNA content of eukaryotic genomes. Genome Dyn. 7, 1‒28.

    Article  CAS  PubMed  Google Scholar 

  118. Bonhoure N., Byrnes A., Moir R.D., Hodroj W., Preitner F., Praz V., Marcelin G., Chua S.C., Jr., Martinez-Lopez N., Singh R., Moullan N., Auwerx J., Willemin G., Shah H., Hartil K., Vaitheesvaran B., Kurland I., Hernandez N., Willis I.M. 2015. Loss of the RNA polymerase III repressor MAF1 confers obesity resistance. Genes Dev. 29, 934‒947.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Chiu Y.H., Macmillan J.B., Chen Z.J. 2009. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell. 138, 576‒591.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Carter-Timofte M.E., Hansen A.F., Christiansen M., Paludan S.R., Mogensen T.H. 2019. Mutations in RNA polymerase III genes and defective DNA sensing in adults with varicella-zoster virus CNS infection. Genes Immun. 20, 214‒223.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The work was supported by the Russian Science Foundation (project no. 19-14-00327).

Author information

Authors and Affiliations

  1. Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, 119991, Moscow, Russia

    A. M. Schwartz, K. A. Tatosyan, D. V. Stasenko & D. A. Kramerov

  2. Department of Human Biology, Faculty of Natural Sciences, University of Haifa, 3498838, Haifa, Israel

    A. M. Schwartz

  3. Department of Biochemistry, Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, 31096, Haifa, Israel

    K. A. Tatosyan

Authors
  1. A. M. Schwartz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. A. Tatosyan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. V. Stasenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. A. Kramerov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. A. Kramerov.

Ethics declarations

CONFLICT OF INTEREST

The authors of this work declare that they have no conflicts of interest.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This work does not contain any studies involving human and animal subjects.

Additional information

Publisher’s Note.

Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schwartz, A.M., Tatosyan, K.A., Stasenko, D.V. et al. Regulation of Transcription by RNA Polymerase III Promotors in the Norm and Pathology. Mol Biol 58, 192–204 (2024). https://doi.org/10.1134/S0026893324020134

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026893324020134

Keywords:

Search

Navigation