Preview

Proceedings of the National Academy of Sciences of Belarus, Biological Series

Advanced search

LONG NON-CODING RNAS AND THEIR FUNCTIONS

Abstract

The review examines the role of long non-coding RNAs (lncRNAs) in the regulation of gene networks with a high degree of complexity. There are such divisions as the role of lncRNAs in: the genome and transcriptome organization; the regulation of a gene specific transcription; the post-transcriptional regulation; X chromosome inactivation; the development of oncopathology and some other diseases; the regulation of telomere length; the expression in tissues of the nervous system. We discuss the literature data on several kinds of non-coding RNA, the participation of lncRNAs in the transmission and coordination of information flows in the epigenetic, transcriptional and post-transcriptional processes. For example, there is a list of noncoding RNAs including both long non-coding RNAs (lncRNAs) and other RNA types (micro RNAs (miRNA), small interfering RNAs (siRNA), piwi-interacting RNAs (piRNA), small nucleolar RNAs (snoRNA), etc.) Our article also deals with the role of such RNAs as HOTAIR – RNA reprogramming chromatin state, Xist, which causes an inactivation of X chromosome genes, or TelRNA involved in replicative aging. Some features of lncRNA expression in tissues of the nervous system are discussed on example of such an evolutionary conservative molecule as TUNA, probably involved in the development of Huntington’s disease. In addition, we consider the probable role of lncRNAs in the development of a number of diseases, including cancer and cardiovascular ones (PCGEM1 – prostate tumor, MALAT1 – non-small cell lung cancer; Miat – myocardial infarction, ANRIL – atherosclerosis, etc.). 

About the Authors

N. A. Balashenko
Institute of Genetics and Cytology of the National Academy of Sciences of Belarus, Minsk
Belarus

Master of Biology, Postgraduate student

27, Akademicheskaya Str., 220072



S. E. Dromashko
Institute of Genetics and Cytology of the National Academy of Sciences of Belarus, Minsk
Belarus

D. Sc. (Biol.), Professor, Head of the Laboratory

27, Akademicheskaya Str., 220072



References

1. Mattick J. S. Non-coding RNAs: the architects of eukaryotic complexity. EMBO reports, 2001, vol. 2, no. 11, pp. 986–991. DOI: 10.1093/embo-reports/kve230

2. Perkel J. M. Visiting “noncodarnia”. BioTechniques, 2013, vol. 54, no. 6, pp. 301, 303–304. DOI: 10.2144/000114037

3. Lafontaine D. L., Tollervey D. Ribosomal RNA. Wiley Online Library, 2001. Available at: http://onlinelibrary.wiley.com/ doi/10.1038/npg.els.0000877/abstract (accessed 19 April 2017).

4. Ullu E., Tschudi C. Alu sequences are processed 7SL RNA genes. Nature, 1984, vol. 312, no. 5990, pp. 171–172. DOI: 10.1038/312171a0

5. Sharp S. J., Schaack J., Cooley L., Burke D. J., Söll D. Structure and transcription of eukaryotic tRNA genes. CRC Critical Reviews in Biochemistry, 1985, vol. 19, no. 2, pp. 107–144. DOI: 10.3109/10409238509082541

6. Gottesman S., Roche E., Zhou Y., Sauer R. T. The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system. Genes and Development, 1998, vol. 12, no. 9, pp. 1338–1347.

7. Hadjiolov A. A., Venkov P. V., Tsanev R. G. Ribonucleic acids fractionation by density-gradient centrifugation and by agar gel electrophoresis: a comparison. Analytical Biochemistry, 1966, vol. 17, no. 2, pp. 263–267. DOI: 10.1016/0003-2697(66)90204-1

8. Maden B. E., Hughes J. M. Eukaryotic ribosomal RNA: the recent excitement in the nucleotide modification problem. Chromosoma, 1997, vol. 105, no. 7–8, pp. 391–400.

9. Xie J., Zhang M., Zhou T., Hua X., Tang L., Wu W. Sno/scaRNAbase: a curated database for small nucleolar RNAs and cajal body-specific RNAs. Nucleic Acids Research, 2007, vol. 35, suppl. 1 (database issue), pp. 183–187. DOI: 10.1093/nar/gkl873

10. Jones T. A., Otto W., Marz M., Eddy S. R., Stadler P. F. A survey of nematode SmY RNAs. RNA Biology, 2009, vol. 6, no. 1, pp. 5–8.

11. Jády B. E. , Kiss T. A small nucleolar guide RNA functions both in 2′-O-ribose methylation and pseudouridylation of the U5 spliceosomal RNA. The EMBO journal, 2001, vol. 20, no. 3, pp. 541–551. DOI: 10.1093/emboj/20.3.541

12. Stuart K., Allen T. E., Kable M. L., Lawson S. Kinetoplastid RNA editing: complexes and catalysts. Current Opinion in Chemical Biology, 1997, vol. 1, no. 3, pp. 340–346.

13. Guerrier-Takada C., Gardiner K., Marsh T., Pace N., Altman S. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell, 1983, vol. 35, no. 3, pt 2, pp. 849–857. DOI: 10.1016/0092-8674(83)90117-4

14. Kiss T., Marshallsay C., Filipowicz W. 7-2/MRP RNAs in plant and mammalian cells: association with higher order structures in the nucleolus. The EMBO journal, 1992, vol. 11, no. 10, pp. 3737–3746.

15. Hall A. E., Turnbull C., Dalmay T. Y RNAs: recent developments. Biomolecular concepts, 2013, vol. 4, no. 2, pp. 103–110. DOI: 10.1515/bmc-2012-0050

16. Feng J., Funk W. D., Wang S. S., Weinrich S. L., Avilion A. A., Chiu C. P., Adams R. R., Chang E., Allsopp R. C., Yu J., et al. The RNA component of human telomerase. Science, 1995, vol. 269, no. 5228, pp. 1236–1241. DOI: 10.1126/science.7544491

17. Dassanayake R. S., Chandrasekharan N. V., Karunanayake E. H. Trans-spliced leader RNA, 5S-rRNA genes and novel variant orphan spliced-leader of the lymphatic filarial nematode Wuchereria bancrofti, and a sensitive polymerase chain reaction based detection assay. Gene, 2001, vol. 269, no. 1–2, pp. 185–193. DOI: 10.1016/S0378-1119(01)00438-3

18. Mizuno T., Chou M. Y., Inouye M. A unique mechanism regulating gene expression: Translational inhibition by a complementary RNA transcript (micRNA). Proceedings of the National Academy of Sciences of the United States of America, 1984, vol. 81, no. 7, pp. 1966–1970. DOI: 10.1073/pnas.81.7.1966

19. Osato N., Suzuki Y., Ikeo K., Gojobori T. Transcriptional interferences in cis natural antisense transcripts of humans and mice. Genetics, 2007, vol. 176, no. 12, pp. 1299–1306. DOI: 10.1534/genetics.106.069484

20. Deltcheva E., Chylinski K., Sharma C. M., Gonzales K., Chao Y., Pirzada Z. A., Eckert M. R., Vogel J., Charpentier E. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature, 2011, vol. 471, no. 7340, pp. 602–607. DOI: 10.1038/nature09886

21. Ma L., Bajic V. B., Zhang Z. On the classification of long non-coding RNAs. RNA biology, 2014, vol. 10, no. 6, pp. 924–933. DOI: 10.4161/rna.24604.

22. Chen K., Rajewsky N. The evolution of gene regulation by transcription factors and microRNAs. Nature reviews. Genetics, 2007, vol. 8, no. 2, pp. 93–103. DOI: 10.1038/nrg1990

23. Seto A. G., Kingston R. E., Lau N. C. The coming of age for Piwi proteins. Molecular Cell, 2007, vol. 26, no. 5, pp. 603–609. DOI: 10.1016/j.molcel.2007.05.021

24. Kim V. N. Small RNAs: classification, biogenesis, and function. Molecules and Cells, 2005, vol. 19, no. 1, pp. 1–15.

25. Vazquez F., Vaucheret H., Rajagopalan R., Lepers C., Gasciolli V., Mallory A. C., Hilbert J. L., Bartel D. P., Crété P. Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Molecular Cell, 2004, vol. 16, no. 1, pp. 69–79. DOI: 10.1016/j.molcel.2004.09.028

26. Peragine A., Yoshikawa M., Wu G., Albrecht H. L., Poethig R. S. SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes and Development, 2004, vol. 18, no. 19, pp. 2368–2379. DOI: 10.1101/gad.1231804

27. Aravin A. A., Naumova N. M., Tulin A. V., Vagin V. V., Rozovsky Y. M., Gvozdev V. A. Double-stranded RNAmediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Current Biology: CB, 2001, vol. 11, no. 13, pp. 1017–1027.

28. Diribarne G., Bensaude O. 7SK RNA, a non-coding RNA regulating P-TEFb, a general transcription factor. RNA Biology, 2009, vol. 6, no. 2, pp. 122–128.

29. Francia S. Non-coding RNA: Sequence-specific guide for chromatin modification and DNA damage signaling. Frontiers in Genetics, 2015, vol. 6, p. 320. DOI: 10.3389/fgene.2015.00320

30. Quinodoz S., Guttman M. Long non-coding RNAs: An emerging link between gene regulation and nuclear organization. Trends in Cell Biology, 2014, vol. 24, no. 11, pp. 651–663. DOI: 10.1016/j.tcb.2014.08.009

31. Kapranov P., Willingham A. T., Gingeras T. R. Genome-wide transcription and the implications for genomic organization. Nature reviews. Genetics, 2007, vol. 8, no. 6, pp. 413–423. DOI: 10.1038/nrg2083

32. Rasmussen T. P., Wutz A. P., Pehrson J. R., Jaenisch R. R. Expression of Xist RNA is sufficient to initiate macrochromatin body formation. Chromosoma, 2001, vol. 110, no. 6, pp. 411–420. DOI: 10.1007/s004120100158

33. Klattenhoff C. A., Scheuermann J. C., Surface L. E., Bradley R. K., Fields P. A., Steinhauser M. L., Ding H., Butty V. L., Torrey L., Haas S., Abo R., Tabebordbar M., Lee R. T., Burge C. B., Boyer L. A. Braveheart, a long noncoding RNA required for cardiovascular lineage commitment. Cell, 2013, vol. 152, no. 3, pp. 570–583. DOI: 10.1016/j.cell.2013.01.003

34. Nagano T., Mitchell J. A., Sanz L. A., Pauler F. M., Ferguson-Smith A. C., Feil R., Fraser P. The Air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin. Science, 2008, vol. 322, no. 5908, pp. 1717–1720. DOI: 10.1126/science.1163802

35. Yamasaki Y., Kayashima T., Soejima H., Kinoshita A., Yoshiura K., Matsumoto N., Ohta T., Urano T., Masuzaki H., Ishimaru T., Mukai T., Niikawa N., Kishino T. Neuron-specific relaxation of Igf2r imprinting is associated with neuronspecific histone modifications and lack of its antisense transcript Air. Human Molecular Genetics, 2005, vol. 14, no. 17, pp. 2511–2520. DOI: 10.1093/hmg/ddi255

36. Gupta R. A., Shah N., Wang K. C., Kim J., Horlings H. M., Wong D. J., Tsai M. C., Hung T., Argani P., Rinn J. L., Wang Y., Brzoska P., Kong B., Li R., West R. B., van de Vijver M. J., Sukumar S., Chang H. Y. Long non-coding RNA reprograms chromatin state to promote cancer metastasis. Nature, 2010, vol. 464, no. 7291, pp. 1071–1076. : DOI 10.1038/nature08975

37. Chu C., Qu K., Zhong F. L., Artandi S. E., Chang H. Y. Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Molecular Cell, 2011, vol. 344, no. 4, pp. 667–678. DOI: 10.1016/j.molcel.2011.08.027

38. Guttman M., Donaghey J., Carey B. W., Garber M., Grenier J. K., Munson G., Young G., Lucas A. B., Ach R., Bruhn L., Yang X., Amit I., Meissner A., Regev A., Rinn J. L., Root D. E., Lander E. S. LincRNAs act in the circuitry controlling pluripotency and differentiation. Nature, 2011, vol. 477, no. 7364, pp. 295–300. DOI: 10.1038/nature10398

39. Sauvageau M., Goff L. A., Lodato S., Bonev B., Groff A. F., Gerhardinger C., Sanchez-Gomez D. B., Hacisuleyman E., Li E., Spence M., Liapis S. C., Mallard W., Morse M., Swerdel M. R., D’Ecclessis M. F., Moore J. C., Lai V., Gong G., Yancopoulos G. D., Frendewey D., Kellis M., Hart R. P., Valenzuela D. M., Arlotta P., Rinn J. L. Multiple knockout mouse models reveal lincRNAs are required for life and brain development. Elife, 2013, vol. 2, e01749. DOI: 10.7554/eLife.01749

40. Ulitsky I., Shkumatava A., Jan C. H., Sive H., Bartel D. P. Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell, 2011, vol. 147, no. 7, pp. 1537–1550. DOI: 10.1016/j.cell.2011.11.055

41. Kulinski T. M., Barlow D. P., Hudson Q. J. Imprinted silencing is extended over broad chromosomal domains in mouse extra-embryonic lineages. Current Opinion in Cell Biology, 2013, vol. 25, no. 3, pp. 297–304. DOI: 10.1016/j.ceb.2013.02.012

42. Carpenter S., Aiello D., Atianand M. K., Ricci E. P., Gandhi P., Hall L. L., Byron M., Monks B., Henry-Bezy M., Lawrence J. B., O’Neill L. A., Moore M. J., Caffrey D. R., Fitzgerald K. A. A long noncoding RNA mediates both activation and repression of immune response genes. Science, 2013, vol. 341, no. 6147, pp. 789–792. DOI: 10.1126/science.1240925

43. Han P., Li W., Lin C. H., Yang J., Shang C., Nurnberg S. T., Jin K. K., Xu W., Lin C. Y., Lin C. J., Xiong Y., Chien H. C., Zhou B., Ashley E., Bernstein D., Chen P. S., Chen H. S., Quertermous T., Chang C. P. A long noncoding RNA protects the heart from pathological hypertrophy. Nature, 2014, vol. 514, no. 7520, pp. 102–106. DOI: 10.1038/nature13596

44. Wang P., Xue Y., Han Y., Lin L., Wu C., Xu S., Jiang Z., Xu J., Liu Q., Cao X. The STAT3-binding long noncoding RNA lnc-DC controls human dendritic cell differentiation. Science, 2014, vol. 344, no. 6181, pp. 310–313. DOI: 10.1126/science.1251456

45. Gutschner T., Hämmerle M., Eissmann M., Hsu J., Kim Y., Hung G., Revenko A., Arun G., Stentrup M., Gross M., Zörnig M., MacLeod A. R., Spector D. L., Diederichs S. The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer Research, 2013, vol. 73, no. 3, pp. 1180–1189. DOI: 10.1158/0008-5472.CAN-12-2850

46. Huarte M., Guttman M., Feldser D., Garber M., Koziol M. J., Kenzelmann-Broz D., Khalil A. M., Zuk O., Amit I., Rabani M., Attardi L. D., Regev A., Lander E. S., Jacks T., Rinn J. L. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell, 2010, vol. 142, no. 3, pp. 409–419. DOI: 10.1016/j.cell.2010.06.040

47. Trimarchi T., Bilal E., Ntziachristos P., Fabbri G., Dalla-Favera R., Tsirigos A., Aifantis I. Genome-wide mapping and characterization of notch-regulated long noncoding RNAs in acute leukemia. Cell, 2014, vol. 158, no. 3, pp. 593–606. DOI: 10.1016/j.cell.2014.05.049

48. Yang L., Lin C., Jin C., Yang J. C., Tanasa B., Li W., Merkurjev D., Ohgi K. A., Meng D., Zhang J., Evans C. P., Rosenfeld M. G. LncRNA-dependent mechanisms of androgen-receptor-regulated gene activation programs. Nature, 2013, vol. 500, no. 7464, pp. 598–602. DOI: 10.1038/nature12451

49. Wang K. C., Yang Y. W., Liu B., Sanyal A., Corces-Zimmerman R., Chen Y., Lajoie B. R., Protacio A., Flynn R. A., Gupta R. A., Wysocka J., Lei M., Dekker J., Helms J. A., Chang H. Y. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature, 2011, vol. 472, no. 7341, pp. 120–124. DOI: 10.1038/nature09819

50. Rinn J. L., Kertesz M., Wang J. K., Squazzo S. L., Xu X., Brugmann S. A., Goodnough L. H., Helms J. A., Farnham P. J., Segal E., Chang H. Y. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell, 2007, vol. 129, no. 7, pp. 1311–1323. DOI: 10.1016/j.cell.2007.05.022

51. Lai F., Orom U. A., Cesaroni M., Beringer M., Taatjes D. J., Blobel G. A., Shiekhattar R. Activating RNAs associate with mediator to enhance chromatin architecture and transcription. Nature, 2013, vol. 494, no. 7438, pp. 497–501. DOI: 10.1038/nature11884

52. Plath K., Mlynarczyk-Evans S., Nusinow D. A., Panning B. Xist RNA and the mechanism of X chromosome inactivation. Annual Review of Genetics, 2002, vol. 36, pp. 233–278. DOI: 10.1146/annurev.genet.36.042902.092433

53. Beletskii A., Hong Y. K., Pehrson J., Egholm M., Strauss W. M. PNA interference mapping demonstrates functional domains in the noncoding RNA Xist. Proceedings of the National Academy of Sciences of the United States of America, 2001, vol. 98, no. 16, pp. 9215–9220. DOI: 10.1073/pnas.161173098

54. Wutz A., Rasmussen T. P., Jaenisch R. Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nature Genetics, 2002, vol. 30, no. 2, pp. 167–174. DOI: 10.1038/ng820

55. Senner C. E., Nesterova T. B., Norton S., Dewchand H., Godwin J., Mak W., Brockdorff N. Disruption of a conserved region of Xist exon 1 impairs Xist RNA localisation and X-linked gene silencing during random and imprinted X chromosome inactivation. Development, 2011, vol. 138, no. 8, pp. 1541–1550. DOI: 10.1242/dev.056812

56. Jiang J., Jing Y., Cost G. J., Chiang J. C., Kolpa H. J., Cotton A. M., Carone D. M., Carone B. R., Shivak D. A., Guschin D. Y., Pearl J. R., Rebar E. J., Byron M., Gregory P. D., Brown C. J., Urnov F. D., Hall L. L., Lawrence J. B. Translating dosage compensation to trisomy 21. Nature, 2013, vol. 500, no. 7462, pp. 296–300. DOI: 10.1038/nature12394

57. Fu X., Ravindranath L., Tran N., Petrovics G., Srivastava S. Regulation of apoptosis by a prostate-specific and prostate cancer-associated noncoding gene, PCGEM1. DNA and Cell Biology, 2006, vol. 25, no. 3, pp. 135–141. DOI: 10.1089/dna.2006.25.135

58. Sonkoly E., Bata-Csorgo Z., Pivarcsi A., Polyanka H., Kenderessy-Szabo A., Molnar G., Szentpali K., Bari L, Megyeri K., Mandi Y., Dobozy A., Kemeny L., Szell M. Identification and characterization of a novel, psoriasis susceptibilityrelated noncoding RNA gene, PRINS. The Journal of Biological Chemistry, 2005, vol. 280, no. 25, pp. 24159–24167. DOI: 10.1074/jbc.M501704200

59. Calin G. A., Liu C. G., Ferracin M., Hyslop T., Spizzo R., Sevignani C., Fabbri M., Cimmino A., Lee E. J., Wojcik S. E., Shimizu M., Tili E., Rossi S., Taccioli C., Pichiorri F., Liu X., Zupo S., Herlea V., Gramantieri L., Lanza G., Alder H., Rassenti L., Volinia S., Schmittgen T. D., Kipps T. J., Negrini M., Croce C. M. Ultraconserved regions encoding ncRNAs are altered in human leukemias and carcinomas. Cancer Cell, 2007, vol. 12, no. 3, pp. 215–229. DOI: 10.1016/j.ccr.2007.07.027

60. Ishii N., Ozaki K., Sato H., Mizuno H., Saito S., Takahashi A., Miyamoto Y., Ikegawa S., Kamatani N., Hori M., Saito S., Nakamura Y., Tanaka T. Identification of a novel non-coding RNA, MIAT, that confers risk of myocardial infarction. Journal of Human Genetics, 2006, vol. 51, no. 12, pp. 1087–1099. DOI: 10.1007/s10038-006-0070-9

61. Schoeftner S., Blasco M. A. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nature cell Biology, 2008, vol. 10, no. 2, pp. 228–236. DOI: 10.1038/ncb1685

62. Azzalin C. M., Reichenbach P., Khoriauli L., Giulotto E., Lingner J. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science, 2015, vol. 318, no. 5851, pp. 798–801. DOI: 10.1126/science.1147182

63. Derrien T., Johnson R., Bussotti G., Tanzer A., Djebali S., Tilgner H., Guernec G., Martin D., Merkel A., Knowles D. G., Lagarde J., Veeravalli L., Ruan X., Ruan Y., Lassmann T., Carninci P., Brown J. B., Lipovich L., Gonzalez J. M., Thomas M., Davis C. A., Shiekhattar R., Gingeras T. R., Hubbard T. J., Notredame C., Harrow J., Guigó R. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Research, 2012, vol. 22, no. 9, pp. 1775–1789. DOI: 10.1101/gr.132159.111

64. Webb A., Papp A. C., Curtis A., Newman L. C., Pietrzak M., Seweryn M., Handelman S. K., Rempala G. A., Wang D., Graziosa E., Tyndale R. F., Lerman C., Kelsoe J. R., Mash D. C., Sadee W. RNA sequencing of transcriptomes in human brain regions: protein-coding and non-coding RNAs, isoforms and alleles. BMC Genomics, 2015, vol. 16, p. 990. DOI: 10.1186/s12864-015-2207-8

65. Lin N., Chang K. Y., Li Z., Gates K., Rana Z. A., Dang J., Zhang D., Han T., Yang C. S., Cunningham T. J., Head S. R., Duester G., Dong P. D., Rana T. M. An evolutionarily conserved long noncoding RNA TUNA controls pluripotency and neural lineage commitment. Molecular Cell, 2014, vol. 53, no. 6, pp. 1005–1019. DOI: 10.1016/j.molcel.2014.01.021


Review

Views: 1878


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 1029-8940 (Print)
ISSN 2524-230X (Online)