Journal of Molecular Histology

, Volume 42, Issue 2, pp 105–112 | Cite as

Expression of non-coding RNA AB063319 derived from Rian gene during mouse development

  • Tiantian Gu
  • Hongjuan He
  • Yanjiang Xing
  • Qi Liu
  • Ning Gu
  • Sugimoto Kenkichi
  • Huijie Jiang
  • Qiong Wu
Original Paper

Abstract

The regulatory functions of many non-coding RNAs (ncRNAs) were widely recognized. However, there are very few publications on long intronic ncRNAs. The transcriptional hierarchy driving a large amount of long and short ncRNAs originated from the maternal chromosome is not clarified in the Dlk1-Dio3 imprinted clusters of mouse distal chromosome 12. Here, we only focused on the previously identified long ncRNA AB063319 which derives from the large imprinted gene Rian and contains three retained introns of Rian, and tried to unsderstand this ncRNAs part of biological functions. We used in situ hybridization and quantitative real-time RT-PCR (QRT-PCR) to characterize the spatiotemporal expression pattern of AB063319 during mouse development. The in situ hybridization results showed that AB063319 was prominently expressed in the brain at embryonic day 10.5 (E10.5) and E11.5, and abundantly expressed in brain, muscle, liver, lung and neuroendocrine tissues at E15.5. Furthermore, quantitative analyses results showed that AB063319 was gradually up-regulated from E9.5 to E18.5 and down-regulated at E19.5 during the mouse embryonic development, and AB063319 was highly expressed in tongue and brain at E12.5, E15.5 and E18.5. Alternatively, AB063319 expression was also predominantly detected in tongue and brain at mouse postnatal day 6 (P6) by semi-quantitative RT-PCR. These results indicated that AB063319, as a stable transcriptional ncRNA, might play the important roles in the morphogenesis of diverse organs and tissues, especially associated with brain and muscle development at mouse embryonic and postnatal stages.

Keywords

Intronic non-coding RNA AB063319 In situ hybridization QRT-PCR 

References

  1. Amaral PP, Mattick JS (2008) Noncoding RNA in development. Mamm Genome 19(7–8):454–492. doi:10.1007/s00335-008-9136-7 PubMedCrossRefGoogle Scholar
  2. Brito GC, Fachel AA, Vettore AL, Vignal GM, Gimba ER, Campos FS, Barcinski MA, Verjovski-Almeida S, Reis EM (2008) Identification of protein-coding and intronic noncoding RNAs down-regulated in clear cell renal carcinoma. Mol Carcinog 47(10):757–767. doi:10.1002/mc.20433 PubMedCrossRefGoogle Scholar
  3. Brown JW, Marshall DF, Echeverria M (2008) Intronic noncoding RNAs and splicing. Trends Plant Sci 13(7):335–342. doi:10.1016/j.tplants.2008.04.010 PubMedCrossRefGoogle Scholar
  4. Cavaille J, Seitz H, Paulsen M, Ferguson-Smith AC, Bachellerie JP (2002) Identification of tandemly-repeated C/D snoRNA genes at the imprinted human 14q32 domain reminiscent of those at the Prader-Willi/Angelman syndrome region. Hum Mol Genet 11(13):1527–1538PubMedCrossRefGoogle Scholar
  5. da Rocha ST, Tevendale M, Knowles E, Takada S, Watkins M, Ferguson-Smith AC (2007) Restricted co-expression of Dlk1 and the reciprocally imprinted non-coding RNA, Gtl2: implications for cis-acting control. Dev Biol 306(2):810–823. doi:10.1016/j.ydbio.2007.02.043 PubMedCrossRefGoogle Scholar
  6. da Rocha ST, Edwards CA, Ito M, Ogata T, Ferguson-Smith AC (2008) Genomic imprinting at the mammalian Dlk1-Dio3 domain. Trends Genet 24(6):306–316. doi:10.1016/j.tig.2008.03.011 PubMedCrossRefGoogle Scholar
  7. Dinger ME, Amaral PP, Mercer TR, Pang KC, Bruce SJ, Gardiner BB, Askarian-Amiri ME, Ru K, Solda G, Simons C, Sunkin SM, Crowe ML, Grimmond SM, Perkins AC, Mattick JS (2008) Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res 18(9):1433–1445. doi:10.1101/gr.078378.108 PubMedCrossRefGoogle Scholar
  8. Donsante A, Miller DG, Li Y, Vogler C, Brunt EM, Russell DW, Sands MS (2007) AAV vector integration sites in mouse hepatocellular carcinoma. Science 317(5837):477. doi:10.1126/science.1142658 Google Scholar
  9. Dupuy AJ, Rogers LM, Kim J, Nannapaneni K, Starr TK, Liu P, Largaespada DA, Scheetz TE, Jenkins NA, Copeland NG (2009) A modified sleeping beauty transposon system that can be used to model a wide variety of human cancers in mice. Cancer Res 69(20):8150–8156. doi:10.1158/0008-5472.CAN-09-1135 PubMedCrossRefGoogle Scholar
  10. Eis PS, Tam W, Sun L, Chadburn A, Li Z, Gomez MF, Lund E, Dahlberg JE (2005) Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc Natl Acad Sci USA 102(10):3627–3632. doi:10.1073/pnas.0500613102 PubMedCrossRefGoogle Scholar
  11. Gabory A, Jammes H, Dandolo L (2010) The H19 locus: role of an imprinted non-coding RNA in growth and development. Bioessays 32(6):473–480. doi:10.1002/bies.200900170 PubMedCrossRefGoogle Scholar
  12. Hagan JP, O’Neill BL, Stewart CL, Kozlov SV, Croce CM (2009) At least ten genes define the imprinted Dlk1-Dio3 cluster on mouse chromosome 12qF1. PLoS ONE 4(2):e4352. doi:10.1371/journal.pone.0004352
  13. Hatada I, Morita S, Obata Y, Sotomaru Y, Shimoda M, Kono T (2001) Identification of a new imprinted gene, Rian, on mouse chromosome 12 by fluorescent differential display screening. J Biochem 130(2):187–190PubMedGoogle Scholar
  14. Kino T, Hurt DE, Ichijo T, Nader N, Chrousos GP (2010) Noncoding RNA gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor. Sci Signal 3 (107):ra8. doi:10.1126/scisignal.2000568
  15. Leung KN, Vallero RO, DuBose AJ, Resnick JL, LaSalle JM (2009) Imprinting regulates mammalian snoRNA-encoding chromatin decondensation and neuronal nucleolar size. Hum Mol Genet 18(22):4227–4238. doi:10.1093/hmg/ddp373 PubMedCrossRefGoogle Scholar
  16. Louro R, El-Jundi T, Nakaya HI, Reis EM, Verjovski-Almeida S (2008) Conserved tissue expression signatures of intronic noncoding RNAs transcribed from human and mouse loci. Genomics 92(1):18–25. doi:10.1016/j.ygeno.2008.03.013 PubMedCrossRefGoogle Scholar
  17. Louro R, Smirnova AS, Verjovski-Almeida S (2009) Long intronic noncoding RNA transcription: expression noise or expression choice? Genomics 93(4):291–298. doi:10.1016/j.ygeno.2008.11.009 PubMedCrossRefGoogle Scholar
  18. Mallardo M, Poltronieri P, D’Urso OF (2008) Non-protein coding RNA biomarkers and differential expression in cancers: a review. J Exp Clin Cancer Res 27:19. doi:10.1186/1756-9966-27-19 PubMedCrossRefGoogle Scholar
  19. McLaughlin D, Vidaki M, Renieri E, Karagogeos D (2006) Expression pattern of the maternally imprinted gene Gtl2 in the forebrain during embryonic development and adulthood. Gene Expr Patterns 6(4):394–399. doi:10.1016/j.modgep.2005.09.007 PubMedCrossRefGoogle Scholar
  20. Mehler MF, Mattick JS (2007) Noncoding RNAs and RNA editing in brain development, functional diversification, and neurological disease. Physiol Rev 87(3):799–823. doi:10.1152/physrev.00036.2006 PubMedCrossRefGoogle Scholar
  21. Mercer TR, Dinger ME, Sunkin SM, Mehler MF, Mattick JS (2008) Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci USA 105(2):716–721. doi:10.1073/pnas.0706729105 PubMedCrossRefGoogle Scholar
  22. Mercer TR, Qureshi IA, Gokhan S, Dinger ME, Li G, Mattick JS, Mehler MF (2010) Long noncoding RNAs in neuronal-glial fate specification and oligodendrocyte lineage maturation. BMC Neurosci 11:14. doi:10.1186/1471-2202-11-14 PubMedCrossRefGoogle Scholar
  23. Miller NL, Wevrick R, Mellon PL (2009) Necdin, a Prader-Willi syndrome candidate gene, regulates gonadotropin-releasing hormone neurons during development. Hum Mol Genet 18(2):248–260. doi:10.1093/hmg/ddn344 PubMedCrossRefGoogle Scholar
  24. Moorman AF, Houweling AC, de Boer PA, Christoffels VM (2001) Sensitive nonradioactive detection of mRNA in tissue sections: novel application of the whole-mount in situ hybridization protocol. J Histochem Cytochem 49(1):1–8PubMedCrossRefGoogle Scholar
  25. Piette D, Hendrickx M, Willems E, Kemp CR, Leyns L (2008) An optimized procedure for whole-mount in situ hybridization on mouse embryos and embryoid bodies. Nat Protoc 3(7):1194–1201. doi:10.1038/nprot.2008.103 PubMedCrossRefGoogle Scholar
  26. Ponting CP, Oliver PL, Reik W (2009) Evolution and functions of long noncoding RNAs. Cell 136(4):629–641. doi:10.1016/j.cell.2009.02.006 PubMedCrossRefGoogle Scholar
  27. Royo H, Cavaille J (2008) Non-coding RNAs in imprinted gene clusters. Biol Cell 100(3):149–166. doi:10.1042/BC20070126 PubMedCrossRefGoogle Scholar
  28. Schuster-Gossler K, Bilinski P, Sado T, Ferguson-Smith A, Gossler A (1998) The mouse Gtl2 gene is differentially expressed during embryonic development, encodes multiple alternatively spliced transcripts, and may act as an RNA. Dev Dyn 212(2):214–228. doi:10.1002/(SICI)1097-0177 PubMedCrossRefGoogle Scholar
  29. Seitz H, Royo H, Bortolin ML, Lin SP, Ferguson-Smith AC, Cavaille J (2004) A large imprinted microRNA gene cluster at the mouse Dlk1-Gtl2 domain. Genome Res 14(9):1741–1748. doi:10.1101/gr.2743304gr.2743304 PubMedCrossRefGoogle Scholar
  30. Stadtfeld M, Apostolou E, Akutsu H, Fukuda A, Follett P, Natesan S, Kono T, Shioda T, Hochedlinger K (2010) Aberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells. Nature 465(7295):175–181. doi:10.1038/nature09017 PubMedCrossRefGoogle Scholar
  31. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, Hogenesch JB (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 101(16):6062–6067. doi:10.1073/pnas.04007821010400782101 PubMedCrossRefGoogle Scholar
  32. Tierling S, Dalbert S, Schoppenhorst S, Tsai CE, Oliger S, Ferguson-Smith AC, Paulsen M, Walter J (2006) High-resolution map and imprinting analysis of the Gtl2-Dnchc1 domain on mouse chromosome 12. Genomics 87(2):225–235. doi:10.1016/j.ygeno.2005.09.018 PubMedCrossRefGoogle Scholar
  33. Wallace C, Smyth DJ, Maisuria-Armer M, Walker NM, Todd JA, Clayton DG (2010) The imprinted DLK1-MEG3 gene region on chromosome 14q32.2 alters susceptibility to type 1 diabetes. Nat Genet 42(1):68–71. doi:10.1038/ng.493 Google Scholar
  34. Wilkinson DG, Nieto MA (1993) Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts. Methods Enzymol 225:361–373PubMedCrossRefGoogle Scholar
  35. Willingham AT, Gingeras TR (2006) TUF love for “junk” DNA. Cell 125(7):1215–1220. doi:10.1016/j.cell.2006.06.009 PubMedCrossRefGoogle Scholar
  36. Xiao Y, Zhou H, Qu LH (2006) Characterization of three novel imprinted snoRNAs from mouse Irm gene. Biochem Biophys Res Commun 340(4):1217–1223. doi:10.1016/j.bbrc.2005.12.128 PubMedCrossRefGoogle Scholar
  37. Yevtodiyenko A, Schmidt JV (2006) Dlk1 expression marks developing endothelium and sites of branching morphogenesis in the mouse embryo and placenta. Dev Dyn 235(4):1115–1123. doi:10.1002/dvdy.20705 PubMedCrossRefGoogle Scholar
  38. Zhang X, Zhou Y, Mehta KR, Danila DC, Scolavino S, Johnson SR, Klibanski A (2003) A pituitary-derived MEG3 isoform functions as a growth suppressor in tumor cells. J Clin Endocrinol Metab 88(11):5119–5126PubMedCrossRefGoogle Scholar
  39. Zhou Y, Cheunsuchon P, Nakayama Y, Lawlor MW, Zhong Y, Rice KA, Zhang L, Zhang X, Gordon FE, Lidov HG, Bronson RT, Klibanski A (2010) Activation of paternally expressed genes and perinatal death caused by deletion of the Gtl2 gene. Development 137(16):2643–2652. doi:10.1242/dev.045724 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Tiantian Gu
    • 1
  • Hongjuan He
    • 1
  • Yanjiang Xing
    • 1
  • Qi Liu
    • 1
  • Ning Gu
    • 1
  • Sugimoto Kenkichi
    • 2
  • Huijie Jiang
    • 3
    • 4
  • Qiong Wu
    • 1
  1. 1.State Key Laboratory of Urban Water Resource and Environment, Department of Life Science and EngineeringHarbin Institute of TechnologyHarbinChina
  2. 2.Department of Cell Science, Faculty of Graduate School of Science and TechnologyNiigata UniversityNiigataJapan
  3. 3.Cell Therapy Program, Princess Margaret HospitalTorontoAustralia
  4. 4.College of Life SciencesLudong UniversityYantaiChina

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