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Cell and Tissue Research

, Volume 362, Issue 3, pp 569–575 | Cite as

Characterization of miRNA processing machinery in the embryonic chick lung

  • Rute Silva MouraEmail author
  • Patrícia Vaz-Cunha
  • Carla Silva-Gonçalves
  • Jorge Correia-Pinto
Regular Article

Abstract

Lung development is a very complex process that relies on the interaction of several signaling pathways that are controlled by precise regulatory mechanisms. Recently, microRNAs (miRNAs), small non-coding regulatory RNAs, have emerged as new players involved in gene expression regulation controlling several biological processes, such as cellular differentiation, apoptosis and organogenesis, in both developmental and disease processes. Failure to correctly express some specific miRNAs or a component of their biosynthetic machinery during embryonic development is disastrous, resulting in severe abnormalities. Several miRNAs have already been identified as modulators of lung development. Regarding the spatial distribution of the processing machinery of miRNAs, only two of its members (dicer1 and argonaute) have been characterized. The present work characterizes the expression pattern of drosha, dgcr8, exportin-5 and dicer1 in early stages of the embryonic chick lung by whole mount in situ hybridization and cross-section analysis. Overall, these genes are co-expressed in dorsal and distal mesenchyme and also in growing epithelial regions. The expression pattern of miRNA processing machinery supports the previously recognized regulatory role of this mechanism in epithelial and mesenchymal morphogenesis.

Keywords

drosha dgcr8 exportin-5 dicer1 Chick lung 

Notes

Acknowledgments

The authors would like to thank Dr. Raquel P. Andrade for providing the probes used in this manuscript. We also acknowledge Luís Martins and Ana Lima for slide sectioning.

References

  1. Abdelfattah AM, Park C, Choi MY (2014) Update on non-canonical microRNAs. Biomol Concepts 5(4):275–287PubMedCentralCrossRefPubMedGoogle Scholar
  2. Banerjee A, Schambach F, DeJong CS, Hammond SM, Reiner SL (2010) Micro-RNA-155 inhibits IFN-gamma signaling in CD4+ T cells. Eur J Immunol 40:225–231PubMedCentralCrossRefPubMedGoogle Scholar
  3. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297CrossRefPubMedGoogle Scholar
  4. Berezikov E, Chung WJ, Willis J, Cuppen E, Lai EC (2007) Mammalian mirtron genes. Mol Cell 28:328–336PubMedCentralCrossRefPubMedGoogle Scholar
  5. Bernstein E, Kim SY, Carmell MA, Murchison EP, Alcorn H, Li MZ, Mills AA, Elledge SJ, Anderson KV, Hannon GJ (2003) Dicer is essential for mouse development. Nat Genet 35:215–217CrossRefPubMedGoogle Scholar
  6. Bhaskaran M, Wang Y, Zhang H, Weng T, Baviskar P, Guo Y, Gou D, Liu L (2009) MicroRNA-127 modulates fetal lung development. Physiol Genomics 37:268–278PubMedCentralCrossRefPubMedGoogle Scholar
  7. Bhaskaran M, Xi D, Wang Y, Huang C, Narasaraju T, Shu W, Zhao C, Xiao X, More S, Breshears M, Liu L (2012) Identification of microRNAs changed in the neonatal lungs in response to hyperoxia exposure. Physiol Genomics 44:970–980PubMedCentralCrossRefPubMedGoogle Scholar
  8. Carraco G, Gonçalves AN, Serra C, Andrade RP (2014) MicroRNA processing machinery in the developing chick embryo. Gene Expr Patterns 16(2):114–121CrossRefPubMedGoogle Scholar
  9. Carraro G, El-Hashash A, Guidolin D, Tiozzo C, Turcatel G, Young BM, De Langhe SP, Bellusci S, Shi W, Parnigotto PP, Warburton D (2009) miR-17 family of microRNAs controls FGF10-mediated embryonic lung epithelial branching morphogenesis through MAPK14 and STAT3 regulation of E-Cadherin distribution. Dev Biol 333(2):238–250PubMedCentralCrossRefPubMedGoogle Scholar
  10. Carraro G, Shrestha A, Rostkovius J, Contreras A, Chao CM, El Agha E, Mackenzie B, Dilai S, Guidolin D, Taketo MM, Günther A, Kumar ME, Seeger W, De Langhe S, Barreto G, Bellusci S (2014) miR-142-3p balances proliferation and differentiation of mesenchymal cells during lung development. Development 141(6):1272–1281PubMedCentralCrossRefPubMedGoogle Scholar
  11. Dakhlallah D, Batte K, Wang Y, Cantemir-Stone CZ, Yan P, Nuovo G, Mikhail A, Hitchcock CL, Wright VP, Nana-Sinkam SP, Piper MG, Marsh CB (2013) Epigenetic regulation of miR-17 ~ 92 contributes to the pathogenesis of pulmonary fibrosis. Am J Respir Crit Care Med 187(4):397–405PubMedCentralCrossRefPubMedGoogle Scholar
  12. Dong J, Jiang G, Asmann YW, Tomaszek S, Jen J, Kislinger T, Wigle DA (2010) MicroRNA networks in mouse lung organogenesis. PLoS ONE 5(5):e1085CrossRefGoogle Scholar
  13. Glazov EA, Cottee PA, Barris WC, Moore RJ, Dalrymple BP, Tizard ML (2008) A microRNA catalog of the developing chicken embryo identified by a deep sequencing approach. Genome Res 18:957–964PubMedCentralCrossRefPubMedGoogle Scholar
  14. Hamburger V, Hamilton HL (1992) A series of normal stages in the development of the chick embryo. Dev Dyn 195:231–272CrossRefPubMedGoogle Scholar
  15. Harris KS, Zhang Z, McManus MT, Harfe BD, Sun X (2006) Dicer function is essential for lung epithelium morphogenesis. Proc Natl Acad Sci USA 103(7):2208–2213Google Scholar
  16. Henrique D, Adam J, Myat A, Chitnis A, Lewis J, Ish-Horowicz D (1995) Expression of a Delta homologue in prospective neurons in the chick. Nature 375:787–790CrossRefPubMedGoogle Scholar
  17. Herriges M, Morrisey EE (2014) Lung development: orchestrating the generation and regeneration of a complex organ. Development 141(3):502–513PubMedCentralCrossRefPubMedGoogle Scholar
  18. Hogan BLM (1999) Morphogenesis. Cell 96:225–233CrossRefPubMedGoogle Scholar
  19. Jiang Z, Cushing L, Ai X, Lü J (2014) miR-326 is downstream of Sonic hedgehog signaling and regulates the expression of Gli2 and smoothened. Am J Respir Cell Mol Biol 51(2):273–283PubMedCentralPubMedGoogle Scholar
  20. Johanson TM, Lew AM, Chong MM (2013) MicroRNA-independent roles of the RNase III enzymes Drosha and Dicer. Open Biol 3(10):130144PubMedCentralCrossRefPubMedGoogle Scholar
  21. Khoshgoo N, Kholdebarin R, Iwasiow BM, Keijzer R (2013) MicroRNAs and lung development. Pediatr Pulmonol 48(8):317–323CrossRefPubMedGoogle Scholar
  22. Lü J, Qian J, Chen F, Tang X, Li C, Cardoso WV (2005) Differential expression of components of the microRNA machinery during mouse organogenesis. Biochem Biophys Res Commun 334(2):319–323CrossRefPubMedGoogle Scholar
  23. Lu Y, Thomson JM, Wong HY, Hammond SM, Hogan BL (2007) Transgenic over-expression of the microRNA miR-17-92 cluster promotes proliferation and inhibits differentiation of lung epithelial progenitor cells. Dev Biol 310(2):442–453PubMedCentralCrossRefPubMedGoogle Scholar
  24. Metzger RJ, Klein OD, Martin GR, Krasnow MA (2008) The branching programme of mouse lung development. Nature 453:745–750PubMedCentralCrossRefPubMedGoogle Scholar
  25. Moura RS, Carvalho-Correia E, daMota P, Correia-Pinto J (2014) Canonical Wnt signaling activity in early stages of chick lung development. PLoS ONE 9(3):e112388PubMedCentralCrossRefPubMedGoogle Scholar
  26. Moura RS, Coutinho-Borges JP, Pacheco AP, daMota PO, Correia-Pinto J (2011) FGF signaling pathway in the developing chick lung: expression and inhibition studies. PLoS ONE 6(3):e17660PubMedCentralCrossRefPubMedGoogle Scholar
  27. Mujahid S, Logvinenko T, Volpe MV, Nielsen HC (2013) miRNA regulated pathways in late stage murine lung development. BMC Dev Biol 13:13PubMedCentralCrossRefPubMedGoogle Scholar
  28. Nana-Sinkam SP, Karsies T, Riscili B, Ezzie M, Piper M (2009) Lung microRNA: from development to disease. Expert Rev Respir Med 3(4):373–385CrossRefPubMedGoogle Scholar
  29. Okamura K, Hagen JW, Duan H, Tyler DM, Lai EC (2007) The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 130:89–100PubMedCentralCrossRefPubMedGoogle Scholar
  30. Ouellet DL, Perron MP, Gobeil LA, Plante P, Provost P (2006) MicroRNAs in gene regulation: when the smallest governs it all. J Biomed Biotechnol 2006(4):69616PubMedCentralPubMedGoogle Scholar
  31. Ruby JG, Jan CH, Bartel DP (2007) Intronic microRNA precursors that bypass Drosha processing. Nature 448:83–87PubMedCentralCrossRefPubMedGoogle Scholar
  32. Sato T, Liu X, Nelson A, Nakanishi M, Kanaji N, Wang X, Kim M, Li Y, Sun J, Michalski J, Patil A, Basma H, Holz O, Magnussen H, Rennard SI (2010) Reduced miR146a increases prostaglandin E(2) in chronic obstructive pulmonary disease fibroblasts. Am J Respir Crit Care Med 182:1020–1029PubMedCentralCrossRefPubMedGoogle Scholar
  33. Sayed D, Abdellatif M (2011) MicroRNAs in development and disease. Physiol Rev 91(3):827–887CrossRefPubMedGoogle Scholar
  34. Stefani G, Slack FJ (2008) Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol 9(3):219–230CrossRefPubMedGoogle Scholar
  35. Warburton D, El-Hashash A, Carraro G, Tiozzo C, Sala F, Rogers O, De Langhe S, Kemp PJ, Riccardi D, Torday J, Bellusci S, Shi W, Lubkin SR, Jesudason E (2010) Lung organogenesis. Curr Top Dev Biol 90:73–158PubMedCentralCrossRefPubMedGoogle Scholar
  36. Williams AE, Moschos SA, Perry MM, Barnes PJ, Lindsay MA (2007) Maternally imprinted microRNAs are differentially expressed during mouse and human lung development. Dev Dyn 236(2):572–580PubMedCentralCrossRefPubMedGoogle Scholar
  37. Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M, Stephens RM, Okamoto A, Yokota J, Tanaka T, Calin GA, Liu CG, Croce CM, Harris CC (2006) Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 9:189–198CrossRefPubMedGoogle Scholar
  38. Yang Y, Kai G, Pu XD, Qing K, Guo XR, Zhou XY (2012) Expression profile of microRNAs in fetal lung development of Sprague–Dawley rats. Int J Mol Med 29(3):393–402PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Rute Silva Moura
    • 1
    • 2
    • 3
    Email author
  • Patrícia Vaz-Cunha
    • 1
    • 2
  • Carla Silva-Gonçalves
    • 1
    • 2
  • Jorge Correia-Pinto
    • 1
    • 2
    • 4
  1. 1.Life and Health Sciences Research Institute (ICVS), School of Health SciencesUniversity of MinhoBragaPortugal
  2. 2.ICVS/3B’s - PT Government Associate LaboratoryBragaPortugal
  3. 3.Biology Department, School of SciencesUniversity of MinhoBragaPortugal
  4. 4.Department of Pediatric SurgeryHospital de BragaBragaPortugal

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