When small RNAs become smaller: non - canonical functions of snoRNAs and their derivatives

  • Anna Maria Mleczko Institute of Bioorganic Chemistry Polish Academy of Sciences
  • Kamilla Bąkowska-Żywicka Institute of Bioorganic Chemistry Polish Academy of Sciences
Keywords: small RNAs, snoRNAs, sdRNAs, microRNAs, regulatory RNAs

Abstract

Small nucleolar RNAs (snoRNAs) are molecules placed in the cell nucleolus and in Cajal bodies. Many scientific reports clearly show that snoRNAs are not only responsible for modifications of other RNAs but also possess multiple other functions such as metabolic stress regulation or modulation of alternative splicing. Full-length snoRNAs as well as small RNAs derived from snoRNAs have been implied in human diseases such as cancer or Prader – Willi Syndrome.  In this review we would like to describe these non – canonical roles of snoRNAs and their derivatives  with the emphasis on their role in human diseases. 

References

Babiarz JE, Hsu R, Melton C, Thomas M, Ullian EM , Blelloch R (2011) A role for noncanonical microRNAs in the mammalian brain revealed by phenotypic differences in Dgcr8 versus Dicer1 knockouts and small RNA sequencing. RNA 17(8): 1489-1501. doi 10.1261/rna.2442211

Babiarz JE, Ruby JG, Wang Y, Bartel DP, Blelloch R (2008) Mouse ES cells express endogenous shRNAs, siRNAs, and other Microprocessor-independent, Dicer-dependent small RNAs. Genes Dev 22(20): 2773-2785. doi 10.1101/gad.1705308

Bai B, Yegnasubramanian S, Wheelan SJ, Laiho M (2014) RNA-Seq of the nucleolus reveals abundant SNORD44-derived small RNAs. PLoS One 9(9): e107519. doi 10.1371/journal.pone.0107519

Belin S, Beghin A, Solano-Gonzalez E, Bezin L, Brunet-Manquat S, Textoris J, Prats AC, Mertani HC, Dumontet C, Diaz JJ (2009) Dysregulation of ribosome biogenesis and translational capacity is associated with tumor progression of human breast cancer cells. PLoS One 4(9): e7147. doi 10.1371/journal.pone.0007147

Bortolin-Cavaille ML, Cavaille J (2012) The SNORD115 (H/MBII-52) and SNORD116 (H/MBII-85) gene clusters at the imprinted Prader-Willi locus generate canonical box C/D snoRNAs. Nucleic Acids Res 40(14): 6800-6807. doi 10.1093/nar/gks321

Brameier M, Herwig A, Reinhardt R, Walter L, Gruber J (2011) Human box C/D snoRNAs with miRNA like functions: expanding the range of regulatory RNAs. Nucleic Acids Res 39(2): 675-686. doi 10.1093/nar/gkq776

Burroughs AM, Ando Y, de Hoon MJ, Tomaru Y, Suzuki H, Hayashizaki Y, Daub CO (2011) Deep-sequencing of human Argonaute-associated small RNAs provides insight into miRNA sorting and reveals Argonaute association with RNA fragments of diverse origin. RNA Biol 8(1): 158-177

Chang LS, Lin SY, Lieu AS, Wu TL (2002) Differential expression of human 5S snoRNA genes. Biochem Biophys Res Commun 299(2): 196-200

de los Santos T, Schweizer J, Rees CA, Francke U (2000) Small evolutionarily conserved RNA, resembling C/D box small nucleolar RNA, is transcribed from PWCR1, a novel imprinted gene in the Prader-Willi deletion region, which Is highly expressed in brain. Am J Hum Genet 67(5): 1067-1082. doi 10.1086/303106

de Smith AJ, Purmann C, Walters RG, Ellis RJ, Holder SE, Van Haelst MM, Brady AF, Fairbrother UL, Dattani M, Keogh JM, Henning E, Yeo GS, O'Rahilly S, Froguel P, Farooqi IS, Blakemore AI (2009) A deletion of the HBII-85 class of small nucleolar RNAs (snoRNAs) is associated with hyperphagia, obesity and hypogonadism. Hum Mol Genet 18(17): 3257-3265. doi 10.1093/hmg/ddp263

Dong JT (2001) Chromosomal deletions and tumor suppressor genes in prostate cancer. Cancer Metastasis Rev 20(3-4): 173-193

Dong XY, Guo P, Boyd J, Sun X, Li Q, Zhou W, Dong JT (2009) Implication of snoRNA U50 in human breast cancer. J Genet Genomics 36(8): 447-454. doi 10.1016/S1673-8527(08)60134-4

Dong XY, Rodriguez C, Guo P, Sun X, Talbot JT, Zhou W, Petros J, Li Q, Vessella RL, Kibel AS, Stevens VL, Calle EE, Dong JT (2008) SnoRNA U50 is a candidate tumor-suppressor gene at 6q14.3 with a mutation associated with clinically significant prostate cancer. Hum Mol Genet 17(7): 1031-1042. doi 10.1093/hmg/ddm375

Duker AL, Ballif BC, Bawle EV, Person RE, Mahadevan S, Alliman S, Thompson R, Traylor R, Bejjani BA, Shaffer LG, Rosenfeld JA, Lamb AN, Sahoo T (2010) Paternally inherited microdeletion at 15q11.2 confirms a significant role for the SNORD116 C/D box snoRNA cluster in Prader-Willi syndrome. Eur J Hum Genet 18(11): 1196-1201. doi 10.1038/ejhg.2010.102

Ender C, Krek A, Friedlander MR, Beitzinger M, Weinmann L, Chen W, Pfeffer S, Rajewsky N, Meister G (2008) A human snoRNA with microRNA-like functions. Mol Cell 32(4): 519-528. doi 10.1016/j.molcel.2008.10.017

Falaleeva M, Stamm S (2013) Processing of snoRNAs as a new source of regulatory non-coding RNAs: snoRNA fragments form a new class of functional RNAs. Bioessays 35(1): 46-54. doi 10.1002/bies.201200117

Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127(12): 2893-2917. doi 10.1002/ijc.25516

Houseley J, Tollervey D (2008) The nuclear RNA surveillance machinery: the link between ncRNAs and genome structure in budding yeast? Biochim Biophys Acta 1779(4): 239-246. doi 10.1016/j.bbagrm.2007.12.008

Hutzinger R, Feederle R, Mrazek J, Schiefermeier N, Balwierz PJ, Zavolan M, Polacek N, Delecluse HJ, Huttenhofer A (2009) Expression and processing of a small nucleolar RNA from the Epstein-Barr virus genome. PLoS Pathog 5(8): e1000547. doi 10.1371/journal.ppat.1000547

Kishore S, Khanna A, Zhang Z, Hui J, Balwierz PJ, Stefan M, Beach C, Nicholls RD, Zavolan M, Stamm S (2010) The snoRNA MBII-52 (SNORD 115) is processed into smaller RNAs and regulates alternative splicing. Hum Mol Genet 19(7): 1153-1164. doi 10.1093/hmg/ddp585

Kishore S, Stamm S (2006) The snoRNA HBII-52 regulates alternative splicing of the serotonin receptor 2C. Science 311(5758): 230-232. doi 10.1126/science.1118265

Li W, Saraiya AAWang CC (2011) Gene regulation in Giardia lambia involves a putative microRNA derived from a small nucleolar RNA. PLoS Negl Trop Dis 5(10): e1338. doi 10.1371/journal.pntd.0001338

Li Z, Ender C, Meister G, Moore PS, Chang Y, John B (2012) Extensive terminal and asymmetric processing of small RNAs from rRNAs, snoRNAs, snRNAs, and tRNAs. Nucleic Acids Res 40(14): 6787-6799. doi 10.1093/nar/gks307

Liao J, Yu L, Mei Y, Guarnera M, Shen J, Li R, Liu Z, Jiang F (2010) Small nucleolar RNA signatures as biomarkers for non-small-cell lung cancer. Mol Cancer 9: 198. doi 10.1186/1476-4598-9-198

Martens-Uzunova ES, Hoogstrate Y, Kalsbeek A, Pigmans B, Vredenbregt-van den Berg M, Dits N, Nielsen SJ, Baker A, Visakorpi T, Bangma C, Jenster G (2015) C/D-box snoRNA-derived RNA production is associated with malignant transformation and metastatic progression in prostate cancer. Oncotarget 6(19): 17430-17444. doi 10.18632/oncotarget.4172

Martens-Uzunova ES, Jalava SE, Dits NF, van Leenders GJ, Moller S, Trapman J, Bangma CH, Litman T, Visakorpi T, Jenster G (2012) Diagnostic and prognostic signatures from the small non-coding RNA transcriptome in prostate cancer. Oncogene 31(8): 978-991. doi 10.1038/onc.2011.304

Mei YP, Liao JP, Shen J, Yu L, Liu BL, Liu L, Li RY, Ji L, Dorsey SG, Jiang ZR, Katz RL, Wang J, YJiang F (2012) Small nucleolar RNA 42 acts as an oncogene in lung tumorigenesis. Oncogene 31(22): 2794-2804. doi 10.1038/onc.2011.449

Michel CI, Holley CL, Scruggs BS, Sidhu R, Brookheart RT, Listenberger LL, Behlke MA, Ory DS, Schaffer JE (2011) Small nucleolar RNAs U32a, U33, and U35a are critical mediators of metabolic stress. Cell Metab 14(1): 33-44. doi 10.1016/j.cmet.2011.04.009

Pan YZ, Zhou A, Hu Z, Yu AM (2013) Small nucleolar RNA-derived microRNA hsa-miR-1291 modulates cellular drug disposition through direct targeting of ABC transporter ABCC1. Drug Metab Dispos 41(10): 1744-1751. doi 10.1124/dmd.113.052092

Qu G, Kruszka K, Plewka P, Yang SY, Chiou TJ, Jarmolowski A, Szweykowska-Kulinska Z, Echeverria M, Karlowski WM (2015) Promoter-based identification of novel non-coding RNAs reveals the presence of dicistronic snoRNA-miRNA genes in Arabidopsis thaliana. BMC Genomics 16: 1009. doi 10.1186/s12864-015-2221-x

Sahoo T, del Gaudio D, German JR, Shinawi M, Peters SU, Person RE, Garnica A, Cheung SW, Beaudet AL (2008) Prader-Willi phenotype caused by paternal deficiency for the HBII-85 C/D box small nucleolar RNA cluster. Nat Genet 40(6): 719-721. doi 10.1038/ng.158

Saraiya AA, Wang CC (2008) snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog 4(11): e1000224. doi 10.1371/journal.ppat.1000224

Scott MS, Ono M, Yamada K, Endo A, Barton GJ, Lamond AI (2012) Human box C/D snoRNA processing conservation across multiple cell types. Nucleic Acids Res 40(8): 3676-3688. doi 10.1093/nar/gkr1233

Taft RJ, Glazov EA, Lassmann T, Hayashizaki Y, Carninci P, Mattick JS (2009) Small RNAs derived from snoRNAs. RNA 15(7): 1233-1240. doi 10.1261/rna.1528909

Tyczewska A, Bąkowska-Żywicka K, Gracz J, Twardowski T (2016) Stress responsive non-protein coding RNAs, Abiotic and Biotic Stress in Plants - Recent Advances and Future Perspectives, chapter 7

Valleron W, Laprevotte E, Gautier EF, Quelen C, Demur C, Delabesse E, Agirre X, Prosper F, Kiss T, Brousset P (2012) Specific small nucleolar RNA expression profiles in acute leukemia. Leukemia 26(9): 2052-2060. doi 10.1038/leu.2012.111

Valleron W, Ysebaert L, Berquet L, Fataccioli V, Quelen C, Martin A, Parrens M, Lamant L, de Leval L, Gisselbrecht C, Gaulard P, Brousset P (2012) Small nucleolar RNA expression profiling identifies potential prognostic markers in peripheral T-cell lymphoma. Blood 120(19): 3997-4005. doi 10.1182/blood-2012-06-438135

Walkowiak M, Mleczko AM, Bąkowska – Żywicka K (2016) Evaluation of methods for detection of low-abundant snoRNA-derived small RNAs in Saccharomyces cerevisiae. BioTechnologia 97(1): 19-26. DOI: 10.5114/bta.2016.58540

Xu G, Yang F, Ding CL, Zhao LJ, Ren H, Zhao P, Wang W, Qi ZT (2014) Small nucleolar RNA 113-1 suppresses tumorigenesis in hepatocellular carcinoma. Mol Cancer 13: 216. doi 10.1186/1476-4598-13-216

Yu F, Bracken CP, Pillman KA, Lawrence DM, Goodall GJ, Callen DF, Neilsen PM (2015) p53 Represses the Oncogenic Sno-MiR-28 Derived from a SnoRNA. PLoS One 10(6): e0129190. doi 10.1371/journal.pone.0129190

Zheng D, Zhang J, Ni J, Luo J, Wang J, Tang L, Zhang L, Wang L, Xu J, Su B, Chen G (2015) Small nucleolar RNA 78 promotes the tumorigenesis in non-small cell lung cancer. J Exp Clin Cancer Res 34: 49. doi 10.1186/s13046-015-0170-

Zou AE, Ku J, Honda TK, Yu V, Kuo SZ, Zheng H, Xuan Y, Saad MA, Hinton A, Brumund KT, Lin JH, Wang-Rodriguez J, Ongkeko WM (2015) Transcriptome sequencing uncovers novel long noncoding and small nucleolar RNAs dysregulated in head and neck squamous cell carcinoma. RNA 21(6): 1122-1134. doi 10.1261/rna.049262.114

Zywicki M, Bakowska-Zywicka K, Polacek N (2012) Revealing stable processing products from ribosome-associated small RNAs by deep-sequencing data analysis. Nucleic Acids Res 40(9): 4013-4024. doi 10.1093/nar/gks020

Published
2017-03-04