Skip to main content

The Role of Non-coding RNAs in Cerebellar Development

  • Chapter
  • First Online:
Development of the Cerebellum from Molecular Aspects to Diseases

Part of the book series: Contemporary Clinical Neuroscience ((CCNE))

Abstract

Since the sequencing of the human and various mammalian genomes, it is clear that there are far too few protein-coding genes to specify and coordinate the complex series of developmental events that results in a mature brain. Non-coding RNAs (ncRNAs) are seen as a fount of transcriptional richness that can regulate gene expression in time and space. Together, protein-coding RNAs and ncRNAs can reproducibly replicate a formed and functioning brain. In this chapter, we focus on the roles of three dominant species of ncRNAs – enhancers, long non-coding RNAs, and microRNAs – in driving the development and function in the mouse cerebellum.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Goldowitz D, Hamre K. The cells and molecules that make a cerebellum. Trends Neurosci. 1998;21(9):375–82.

    Article  CAS  PubMed  Google Scholar 

  2. Ha T, Swanson D, Larouche M, Glenn R, Weeden D, Zhang P, et al. CbGRiTS: cerebellar gene regulation in time and space. Dev Biol. 2015;397(1):18–30.

    Article  CAS  PubMed  Google Scholar 

  3. Mattick JS. Non-coding RNAs: the architects of eukaryotic complexity. EMBO Rep. 2001;2(11):986–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Ha TJ, Zhang PGY, Robert R, Yeung J, Swanson DJ, Mathelier A, et al. Identification of novel cerebellar developmental transcriptional regulators with motif activity analysis. BMC Genomics. 2019;20(1):718. https://doi.org/10.1186/s12864-019-6063-9

  5. Kanamori-Katayama M, Itoh M, Kawaji H, Lassmann T, Katayama S, Kojima M, et al. Unamplified cap analysis of gene expression on a single-molecule sequencer. Genome Res. 2011;21(7):1150–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Kawaji H, Kasukawa T, Forrest A, Carninci P, Hayashizaki Y. The FANTOM5 collection, a data series underpinning mammalian transcriptome atlases in diverse cell types. Scientific Data. 2017;4(1):1–3.

    Article  Google Scholar 

  7. Andersson R, Gebhard C, Miguel-Escalada I, Hoof I, Bornholdt J, Boyd M, et al. An atlas of active enhancers across human cell types and tissues. Nature. 2014;507(7493):455–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Arner E, Daub CO, Vitting-Seerup K, Andersson R, Lilje B, Drabløs F, et al. Transcribed enhancers lead waves of coordinated transcription in transitioning mammalian cells. Science. 2015;347(6225):1010–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. De Rie D, Abugessaisa I, Alam T, Arner E, Arner P, Ashoor H, et al. An integrated expression atlas of miRNAs and their promoters in human and mouse. Nat Biotechnol. 2017;35(9):872–8.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Hon C-C, Ramilowski JA, Harshbarger J, Bertin N, Rackham OJ, Gough J, et al. An atlas of human long non-coding RNAs with accurate 5′ ends. Nature. 2017;543(7644):199–204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Jensen P, Zoghbi HY, Goldowitz D. Dissection of the cellular and molecular events that position cerebellar Purkinje cells: a study of the math1null-mutant mouse. J Neurosci. 2002;22(18):8110–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Swanson DJ, Tong Y, Goldowitz D. Disruption of cerebellar granule cell development in the Pax6 mutant, Sey mouse. Develop Brain Res. 2005;160(2):176–93.

    Article  CAS  Google Scholar 

  13. Zhang F, Lupski JR. Non-coding genetic variants in human disease. Hum Mol Genet. 2015;24(R1):R102–R10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Barr C, Misener V. Decoding the non-coding genome: elucidating genetic risk outside the coding genome. Genes Brain Behav. 2016;15(1):187–204.

    Article  CAS  PubMed  Google Scholar 

  15. Parikshak NN, Swarup V, Belgard TG, Irimia M, Ramaswami G, Gandal MJ, et al. Genome-wide changes in lncRNA, splicing, and regional gene expression patterns in autism. Nature. 2016;540(7633):423–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Wu YE, Parikshak NN, Belgard TG, Geschwind DH. Genome-wide, integrative analysis implicates microRNA dysregulation in autism spectrum disorder. Nat Neurosci. 2016;19(11):1463–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Nord AS, West AE. Neurobiological functions of transcriptional enhancers. Nat Neurosci. 2020;23(1):5–14.

    Google Scholar 

  18. Klisch TJ, Xi Y, Flora A, Wang L, Li W, Zoghbi HY. In vivo Atoh1 targetome reveals how a proneural transcription factor regulates cerebellar development. Proc Natl Acad Sci. 2011;108(8):3288–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Lindtner S, Catta-Preta R, Tian H, Su-Feher L, Price JD, Dickel DE, et al. Genomic resolution of DLX-orchestrated transcriptional circuits driving development of forebrain GABAergic neurons. Cell Rep. 2019;28(8):2048–63. e8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Mazzoni EO, Mahony S, Closser M, Morrison CA, Nedelec S, Williams DJ, et al. Synergistic binding of transcription factors to cell-specific enhancers programs motor neuron identity. Nat Neurosci. 2013;16(9):1219–27.

    Article  CAS  PubMed  Google Scholar 

  21. Mikhaylichenko O, Bondarenko V, Harnett D, Schor IE, Males M, Viales RR, et al. The degree of enhancer or promoter activity is reflected by the levels and directionality of eRNA transcription. Genes Dev. 2018;32(1):42–57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Tyssowski KM, DeStefino NR, Cho J-H, Dunn CJ, Poston RG, Carty CE, et al. Different neuronal activity patterns induce different gene expression programs. Neuron. 2018;98(3):530–46. e11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Wu H, Nord AS, Akiyama JA, Shoukry M, Afzal V, Rubin EM, et al. Tissue-specific RNA expression marks distant-acting developmental enhancers. PLoS Genet. 2014;10(9):e1004610.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Arnold PR, Wells AD, Li XC. Diversity and emerging roles of enhancer RNA in regulation of gene expression and cell fate. Front Cell Develop Biol. 2020;7:377.

    Article  Google Scholar 

  25. Frank CL, Liu F, Wijayatunge R, Song L, Biegler MT, Yang MG, et al. Regulation of chromatin accessibility and Zic binding at enhancers in the developing cerebellum. Nat Neurosci. 2015;18(5):647–56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Sarropoulos I, Sepp M, Frömel R, Leiss K, Trost N, Leushkin E, et al. Developmental and evolutionary dynamics of cis-regulatory elements in mouse cerebellar cells. Science. 2021;373(6558):eabg4696.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Ramirez CM. Identification and characterization of active enhancers in the developing cerebellum. University of British Columbia; 2022.

    Google Scholar 

  28. Cajigas I, Chakraborty A, Swyter KR, Luo H, Bastidas M, Nigro M, et al. The Evf2 Ultraconserved enhancer lncRNA functionally and spatially organizes Megabase distant genes in the developing forebrain. Mol Cell. 2018;71(6):956–72.e9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Carullo NVN, Phillips Iii RA, Simon RC, Soto SAR, Hinds JE, Salisbury AJ, et al. Enhancer RNAs predict enhancer-gene regulatory links and are critical for enhancer function in neuronal systems. Nucleic Acids Res. 2020;48(17):9550–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM, Wu J, et al. Widespread transcription at neuronal activity-regulated enhancers. Nature. 2010;465(7295):182–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Yao P, Lin P, Gokoolparsadh A, Assareh A, Thang MW, Voineagu I. Coexpression networks identify brain region-specific enhancer RNAs in the human brain. Nat Neurosci. 2015;18(8):1168–74.

    Article  CAS  PubMed  Google Scholar 

  32. Lai F, Gardini A, Zhang A, Shiekhattar R. Integrator mediates the biogenesis of enhancer RNAs. Nature. 2015;525(7569):399–403.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Li W, Notani D, Ma Q, Tanasa B, Nunez E, Chen AY, et al. Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature. 2013;498(7455):516–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Kim YJ, Xie P, Cao L, Zhang MQ, Kim TH. Global transcriptional activity dynamics reveal functional enhancer RNAs. Genome Res. 2018;28(12):1799–811.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Cichewicz MA, Kiran M, Przanowska RK, Sobierajska E, Shibata Y, Dutta A. MUNC, an enhancer RNA upstream from the MYOD gene, induces a subgroup of myogenic transcripts in trans independently of MyoD. Mol Cell Biol. 2018;38(20):e00655–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kouno T, Moody J, Kwon AT-J, Shibayama Y, Kato S, Huang Y, et al. C1 CAGE detects transcription start sites and enhancer activity at single-cell resolution. Nat Commun. 2019;10(1):1–12.

    Article  Google Scholar 

  37. Mousavi K, Zare H, Dell’Orso S, Grontved L, Gutierrez-Cruz G, Derfoul A, et al. eRNAs promote transcription by establishing chromatin accessibility at defined genomic loci. Mol Cell. 2013;51(5):606–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Tsai P-F, Dell’Orso S, Rodriguez J, Vivanco KO, Ko K-D, Jiang K, et al. A muscle-specific enhancer RNA mediates cohesin recruitment and regulates transcription in trans. Mol Cell. 2018;71(1):129–41. e8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Sakaguchi Y, Nishikawa K, Seno S, Matsuda H, Takayanagi H, Ishii M. Roles of enhancer RNAs in RANKL-induced osteoclast differentiation identified by genome-wide cap-analysis of gene expression using CRISPR/Cas9. Sci Rep. 2018;8(1):1–11.

    Article  CAS  Google Scholar 

  40. Brazão TF, Johnson JS, Müller J, Heger A, Ponting CP, Tybulewicz VL. Long noncoding RNAs in B-cell development and activation. Blood J Am Soc Hematol. 2016;128(7):e10–e9.

    Google Scholar 

  41. Isoda T, Moore AJ, He Z, Chandra V, Aida M, Denholtz M, et al. Non-coding transcription instructs chromatin folding and compartmentalization to dictate enhancer-promoter communication and T cell fate. Cell. 2017;171(1):103–19. e18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Ounzain S, Pezzuto I, Micheletti R, Burdet F, Sheta R, Nemir M, et al. Functional importance of cardiac enhancer-associated noncoding RNAs in heart development and disease. J Mol Cell Cardiol. 2014;76:55–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Consortium EP. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489(7414):57.

    Article  Google Scholar 

  44. A promoter-level mammalian expression atlas. Nature. 2014;507(7493):462–70.

    Google Scholar 

  45. Noguchi S, Arakawa T, Fukuda S, Furuno M, Hasegawa A, Hori F, et al. FANTOM5 CAGE profiles of human and mouse samples. Scientific Data. 2017;4(1):1–10.

    Article  Google Scholar 

  46. Liu G, Mattick J, Taft RJ. A meta-analysis of the genomic and transcriptomic composition of complex life. Cell Cycle. 2013;12(13):2061–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Mercer TR, Mattick JS. Structure and function of long noncoding RNAs in epigenetic regulation. Nat Struct Mol Biol. 2013;20(3):300–7.

    Article  CAS  PubMed  Google Scholar 

  48. Amaral PP, Mattick JS. Noncoding RNA in development. Mamm Genome. 2008;19(7):454–92.

    Article  CAS  PubMed  Google Scholar 

  49. Taft RJ, Pheasant M, Mattick JS. The relationship between non-protein-coding DNA and eukaryotic complexity. BioEssays. 2007;29(3):288–99.

    Article  CAS  PubMed  Google Scholar 

  50. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, et al. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 2011;25(18):1915–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, et al. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 2012;22(9):1775–89.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Briggs JA, Wolvetang EJ, Mattick JS, Rinn JL, Barry G. Mechanisms of long non-coding RNAs in mammalian nervous system development, plasticity, disease, and evolution. Neuron. 2015;88(5):861–77.

    Article  CAS  PubMed  Google Scholar 

  53. Ng SY, Johnson R, Stanton LW. Human long non-coding RNAs promote pluripotency and neuronal differentiation by association with chromatin modifiers and transcription factors. EMBO J. 2012;31(3):522–33.

    Article  CAS  PubMed  Google Scholar 

  54. Kodzius R, Kojima M, Nishiyori H, Nakamura M, Fukuda S, Tagami M, et al. CAGE: cap analysis of gene expression. Nat Methods. 2006;3(3):211–22.

    Article  CAS  PubMed  Google Scholar 

  55. Frankish A, Diekhans M, Ferreira A-M, Johnson R, Jungreis I, Loveland J, et al. GENCODE reference annotation for the human and mouse genomes. Nucleic Acids Res. 2019;47(D1):D766–D73.

    Article  CAS  PubMed  Google Scholar 

  56. Lagarde J, Uszczynska-Ratajczak B, Carbonell S, Pérez-Lluch S, Abad A, Davis C, et al. High-throughput annotation of full-length long noncoding RNAs with capture long-read sequencing. Nat Genet. 2017;49(12):1731–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Mudge JM, Harrow J. Creating reference gene annotation for the mouse C57BL6/J genome assembly. Mamm Genome. 2015;26(9):366–78.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Kryuchkova-Mostacci N, Robinson-Rechavi M. A benchmark of gene expression tissue-specificity metrics. Brief Bioinform. 2017;18(2):205–14.

    CAS  PubMed  Google Scholar 

  59. Gupta I. Spatiotemporal characterisation of some trascriptional signatures in early cerebellar development. University of British Columbia; 2020.

    Google Scholar 

  60. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science. 2001;294(5543):853–8.

    Article  CAS  PubMed  Google Scholar 

  61. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116(2):281–97.

    Article  CAS  PubMed  Google Scholar 

  62. Siegel G, Saba R, Schratt G. microRNAs in neurons: manifold regulatory roles at the synapse. Curr Opin Genet Dev. 2011;21(4):491–7.

    Article  CAS  PubMed  Google Scholar 

  63. Cao X, Yeo G, Muotri AR, Kuwabara T, Gage FH. Noncoding RNAs in the mammalian central nervous system. Annu Rev Neurosci. 2006;29:77–103.

    Article  CAS  PubMed  Google Scholar 

  64. John B, Sander C, Marks DS. Prediction of human microRNA targets. Methods Mol Biol. 2006;342:101–13.

    CAS  PubMed  Google Scholar 

  65. Ye J, Xu M, Tian X, Cai S, Zeng S. Research advances in the detection of miRNA. J Pharmaceut Anal. 2019;9(4):217–26.

    Google Scholar 

  66. Zou H-Y, Guo L, Zhang B, Chen S, Wu X-R, Liu X-D, et al. Aberrant miR-339-5p/neuronatin signaling causes prodromal neuronal calcium dyshomeostasis in mutant presenilin mice. J Clin Invest. 2022;132(8)

    Google Scholar 

  67. Hayman DJ, Modebadze T, Charlton S, Cheung K, Soul J, Lin H, et al. Increased hippocampal excitability in miR-324-null mice. Sci Rep 2021;11(1):1–17.

    Google Scholar 

  68. Shu P, Wu C, Liu W, Ruan X, Liu C, Hou L, et al. The spatiotemporal expression pattern of microRNAs in the developing mouse nervous system. J Biol Chem. 2019;294(10):3444–53.

    Article  CAS  PubMed  Google Scholar 

  69. Ziats MN, Rennert OM. Identification of differentially expressed microRNAs across the developing human brain. Mol Psychiatry. 2014;19(7):848–52.

    Article  CAS  PubMed  Google Scholar 

  70. Bak M, Silahtaroglu A, Møller M, Christensen M, Rath MF, Skryabin B, et al. MicroRNA expression in the adult mouse central nervous system. RNA. 2008;14(3):432–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Hohjoh H, Fukushima T. Expression profile analysis of microRNA (miRNA) in mouse central nervous system using a new miRNA detection system that examines hybridization signals at every step of washing. Gene. 2007;391(1–2):39–44.

    Article  CAS  PubMed  Google Scholar 

  72. Giraldez AJ, Cinalli RM, Glasner ME, Enright AJ, Thomson JM, Baskerville S, et al. MicroRNAs regulate brain morphogenesis in zebrafish. Science. 2005;308(5723):833–8.

    Article  CAS  PubMed  Google Scholar 

  73. Leucht C, Stigloher C, Wizenmann A, Klafke R, Folchert A, Bally-Cuif L. MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nat Neurosci. 2008;11(6):641–8.

    Article  CAS  PubMed  Google Scholar 

  74. Jönsson ME, Nelander Wahlestedt J, Åkerblom M, Kirkeby A, Malmevik J, Brattaas PL, et al. Comprehensive analysis of microRNA expression in regionalized human neural progenitor cells reveals microRNA-10 as a caudalizing factor. Development. 2015;142(18):3166–77.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Abu-Elneel K, Liu T, Gazzaniga FS, Nishimura Y, Wall DP, Geschwind DH, et al. Heterogeneous dysregulation of microRNAs across the autism spectrum. Neurogenetics. 2008;9(3):153–61.

    Article  CAS  PubMed  Google Scholar 

  76. Simeone A. Positioning the isthmic organizer: where Otx2 and Gbx2 meet. Trends Genet. 2000;16(6):237–40.

    Article  CAS  PubMed  Google Scholar 

  77. Millet S, Campbell K, Epstein DJ, Losos K, Harris E, Joyner AL. A role for Gbx2 in repression of Otx2 and positioning the mid/hindbrain organizer. Nature. 1999;401(6749):161–4.

    Article  CAS  PubMed  Google Scholar 

  78. Huang T, Liu Y, Huang M, Zhao X, Cheng L. Wnt1-cre-mediated conditional loss of dicer results in malformation of the midbrain and cerebellum and failure of neural crest and dopaminergic differentiation in mice. J Mol Cell Biol. 2010;2(3):152–63.

    Article  CAS  PubMed  Google Scholar 

  79. Pieczora L, Stracke L, Vorgerd M, Hahn S, Theiss C, Theis V. Unveiling of miRNA expression patterns in purkinje cells during development. Cerebellum. 2017;16(2):376–87.

    Article  CAS  PubMed  Google Scholar 

  80. Sotelo C, Dusart I. Intrinsic versus extrinsic determinants during the development of Purkinje cell dendrites. Neuroscience. 2009;162(3):589–600.

    Article  CAS  PubMed  Google Scholar 

  81. Schaefer A, Dn O’C, Tan CL, Hillman D, Sugimori M, Llinas R, et al. Cerebellar neurodegeneration in the absence of microRNAs. J Exp Med. 2007;204(7):1553–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Ferretti E, De Smaele E, Miele E, Laneve P, Po A, Pelloni M, et al. Concerted microRNA control of Hedgehog signalling in cerebellar neuronal progenitor and tumour cells. EMBO J. 2008;27(19):2616–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Wechsler-Reya RJ, Scott MP. Control of neuronal precursor proliferation in the cerebellum by sonic hedgehog. Neuron. 1999;22(1):103–14.

    Article  CAS  PubMed  Google Scholar 

  84. Ma M, Wu W, Li Q, Li J, Sheng Z, Shi J, et al. N-myc is a key switch regulating the proliferation cycle of postnatal cerebellar granule cell progenitors. Sci Rep. 2015;5(1):1–13.

    Google Scholar 

  85. Kuang Y, Liu Q, Shu X, Zhang C, Huang N, Li J, et al. Dicer1 and MiR-9 are required for proper Notch1 signaling and the Bergmann glial phenotype in the developing mouse cerebellum. Glia. 2012;60(11):1734–46.

    Article  PubMed  Google Scholar 

  86. Tao J, Wu H, Lin Q, Wei W, Lu X-H, Cantle JP, et al. Deletion of astroglial dicer causes non-cell-autonomous neuronal dysfunction and degeneration. J Neurosci. 2011;31(22):8306–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Serrano M. Epigenetic cerebellar diseases. Handb Clin Neurol. 2018;155:227–44.

    Article  PubMed  Google Scholar 

  88. Roussel MF, Hatten ME. Cerebellum: development and medulloblastoma. Curr Top Dev Biol. 2011;94:235–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Hatten ME, Roussel MF. Development and cancer of the cerebellum. Trends Neurosci. 2011;34(3):134–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Ferretti E, De Smaele E, Po A, Di Marcotullio L, Tosi E, Espinola MSB, et al. MicroRNA profiling in human medulloblastoma. Int J Cancer. 2009;124(3):568–77.

    Article  CAS  PubMed  Google Scholar 

  91. Schepici G, Cavalli E, Bramanti P, Mazzon E. Autism spectrum disorder and miRNA: an overview of experimental models. Brain Sci. 2019;9(10):265.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Genovesi LA, Carter KW, Gottardo NG, Giles KM, Dallas PB. Integrated analysis of miRNA and mRNA expression in childhood medulloblastoma compared with neural stem cells. PLoS One. 2011;6(9):e23935.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Kumar V, Kumar V, Chaudhary AK, Coulter DW, McGuire T, Mahato RI. Impact of miRNA-mRNA profiling and their correlation on medulloblastoma tumorigenesis. Mol Therapy Nucleic Acids. 2018;12:490–503.

    Article  Google Scholar 

  94. Venkataraman S, Alimova I, Fan R, Harris P, Foreman N, Vibhakar R. MicroRNA 128a increases intracellular ROS level by targeting Bmi-1 and inhibits medulloblastoma cancer cell growth by promoting senescence. PLoS One. 2010;5(6):e10748.

    Article  PubMed  PubMed Central  Google Scholar 

  95. Venkataraman S, Birks DK, Balakrishnan I, Alimova I, Harris PS, Patel PR, et al. MicroRNA 218 acts as a tumor suppressor by targeting multiple cancer phenotype-associated genes in medulloblastoma. J Biol Chem. 2013;288(3):1918–28.

    Article  CAS  PubMed  Google Scholar 

  96. Garzia L, Andolfo I, Cusanelli E, Marino N, Petrosino G, De Martino D, et al. MicroRNA-199b-5p impairs cancer stem cells through negative regulation of HES1 in medulloblastoma. PLoS One. 2009;4(3):e4998.

    Article  PubMed  PubMed Central  Google Scholar 

  97. Kanchan RK, Perumal N, Atri P, Chirravuri Venkata R, Thapa I, Klinkebiel DL, et al. MiR-1253 exerts tumor-suppressive effects in medulloblastoma via inhibition of CDK6 and CD276 (B7-H3). Brain Pathol. 2020;30(4):732–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Xue P, Huang S, Han X, Zhang C, Yang L, Xiao W, et al. Exosomal miR-101-3p and miR-423-5p inhibit medulloblastoma tumorigenesis through targeting FOXP4 and EZH2. Cell Death Different. 2021:1–14.

    Google Scholar 

  99. Rodríguez-Lebrón E, doCarmo Costa M, Luna-Cancalon K, Peron TM, Fischer S, Boudreau RL, et al. Silencing mutant ATXN3 expression resolves molecular phenotypes in SCA3 transgenic mice. Mol Ther. 2013;21(10):1909–18.

    Article  PubMed  PubMed Central  Google Scholar 

  100. Carmona V, Cunha-Santos J, Onofre I, Simões AT, Vijayakumar U, Davidson BL, et al. Unravelling endogenous microRNA system dysfunction as a new pathophysiological mechanism in Machado-Joseph disease. Mol Ther. 2017;25(4):1038–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Borgonio-Cuadra VM, Valdez-Vargas C, Romero-Córdoba S, Hidalgo-Miranda A, Tapia-Guerrero Y, Cerecedo-Zapata CM, et al. Wide profiling of circulating MicroRNAs in spinocerebellar ataxia type 7. Mol Neurobiol. 2019;56(9):6106–20.

    Article  CAS  PubMed  Google Scholar 

  102. Sellier C, Freyermuth F, Tabet R, Tran T, He F, Ruffenach F, et al. Sequestration of DROSHA and DGCR8 by expanded CGG RNA repeats alters microRNA processing in fragile X-associated tremor/ataxia syndrome. Cell Rep. 2013;3(3):869–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Sarachana T, Zhou R, Chen G, Manji HK, Hu VW. Investigation of post-transcriptional gene regulatory networks associated with autism spectrum disorders by microRNA expression profiling of lymphoblastoid cell lines. Genome Med 2010;2(4):23.

    Google Scholar 

  104. Talebizadeh Z, Butler MG, Theodoro MF. Feasibility and relevance of examining lymphoblastoid cell lines to study role of microRNAs in autism. Autism Res. 2008;1(4):240–50.

    Article  PubMed  PubMed Central  Google Scholar 

  105. Khan AW, Ziemann M, Rafehi H, Maxwell S, Ciccotosto GD, El-Osta A. MeCP2 interacts with chromosomal microRNAs in brain. Epigenetics. 2017;12(12):1028–37.

    Article  PubMed  Google Scholar 

  106. Pall GS, Codony-Servat C, Byrne J, Ritchie L, Hamilton A. Carbodiimide-mediated cross-linking of RNA to nylon membranes improves the detection of siRNA, miRNA and piRNA by northern blot. Nucleic Acids Res. 2007;35(8):e60.

    Article  PubMed  PubMed Central  Google Scholar 

  107. Torres AG, Fabani MM, Vigorito E, Gait MJ. MicroRNA fate upon targeting with anti-miRNA oligonucleotides as revealed by an improved northern-blot-based method for miRNA detection. RNA. 2011;17(5):933–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Mohammadi-Yeganeh S, Paryan M, Mirab Samiee S, Soleimani M, Arefian E, Azadmanesh K, et al. Development of a robust, low cost stem-loop real-time quantification PCR technique for miRNA expression analysis. Mol Biol Rep. 2013;40(5):3665–74.

    Article  CAS  PubMed  Google Scholar 

  109. Niu Y, Zhang L, Qiu H, Wu Y, Wang Z, Zai Y, et al. An improved method for detecting circulating microRNAs with S-poly (T) plus real-time PCR. Sci Rep. 2015;5(1):1–10.

    Article  Google Scholar 

  110. Czimmerer Z, Hulvely J, Simandi Z, Varallyay E, Havelda Z, Szabo E, et al. A versatile method to design stem-loop primer-based quantitative PCR assays for detecting small regulatory RNA molecules. PLoS One. 2013;8(1):e55168.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Li W, Ruan K. MicroRNA detection by microarray. Anal Bioanal Chem. 2009;394(4):1117–24.

    Article  CAS  PubMed  Google Scholar 

  112. Cissell KA, Deo SK. Trends in microRNA detection. Anal Bioanal Chem. 2009;394(4):1109–16.

    Article  CAS  PubMed  Google Scholar 

  113. Motameny S, Wolters S, Nürnberg P, Schumacher B. Next generation sequencing of miRNAs–strategies, resources and methods. Genes. 2010;1(1):70–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Pérez-Rodríguez D, López-Fernández H, Agís-Balboa RC. Application of miRNA-seq in neuropsychiatry: a methodological perspective. Comput Biol Med. 2021;135:104603.

    Article  PubMed  Google Scholar 

  115. Li R-D, Yin B-C, Ye B-C. Ultrasensitive, colorimetric detection of microRNAs based on isothermal exponential amplification reaction-assisted gold nanoparticle amplification. Biosens Bioelectron. 2016;86:1011–6.

    Article  CAS  PubMed  Google Scholar 

  116. Oishi M, Sugiyama S. An efficient particle-based DNA circuit system: catalytic disassembly of DNA/PEG-modified gold nanoparticle–magnetic bead composites for colorimetric detection of miRNA. Small. 2016;12(37):5153–8.

    Article  CAS  PubMed  Google Scholar 

  117. Pan M, Liang M, Sun J, Liu X, Wang F. Lighting up fluorescent silver clusters via target-catalyzed hairpin assembly for amplified biosensing. Langmuir. 2018;34(49):14851–7.

    Article  CAS  PubMed  Google Scholar 

  118. Foda MF, Huang L, Shao F, Han H-Y. Biocompatible and highly luminescent near-infrared CuInS2/ZnS quantum dots embedded silica beads for cancer cell imaging. ACS Appl Mater Interfaces. 2014;6(3):2011–7.

    Article  CAS  PubMed  Google Scholar 

  119. Jiang YS, Bhadra S, Li B, Wu YR, Milligan JN, Ellington AD. Robust strand exchange reactions for the sequence-specific, real-time detection of nucleic acid amplicons. Anal Chem. 2015;87(6):3314–20.

    Article  CAS  PubMed  Google Scholar 

  120. Kuhn DE, Martin MM, Feldman DS, Terry AV Jr, Nuovo GJ, Elton TS. Experimental validation of miRNA targets. Methods. 2008;44(1):47–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Riolo G, Cantara S, Marzocchi C, Ricci C. miRNA targets: from prediction tools to experimental validation. Methods Protocols. 2020;4(1):1.

    Article  PubMed  PubMed Central  Google Scholar 

  122. Huang Y, Zou Q, Song H, Song F, Wang L, Zhang G, et al. A study of miRNAs targets prediction and experimental validation. Protein Cell. 2010;1(11):979–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniel Goldowitz .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2023 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Rahimi-Balaei, M., Ramirez, M., Gupta, I., Goldowitz, D. (2023). The Role of Non-coding RNAs in Cerebellar Development. In: Marzban, H. (eds) Development of the Cerebellum from Molecular Aspects to Diseases. Contemporary Clinical Neuroscience. Springer, Cham. https://doi.org/10.1007/978-3-031-23104-9_6

Download citation

Publish with us

Policies and ethics