Skip to main content

Advertisement

SpringerLink
Log in

Non-coding RNAs in the development of sensory organs and related diseases

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Genomes are transcribed well beyond the conventionally annotated protein-encoding genes and produce many thousands of regulatory non-coding RNAs (ncRNAs). In the last few years, ncRNAs, especially microRNAs and long non-coding RNA, have received increasing attention because of their implication in the function of chromatin-modifying complexes and in the regulation of transcriptional and post-transcriptional events. The morphological events and the genetic networks responsible for the development of sensory organs have been well delineated and therefore sensory organs have provided a useful scenario to address the role of ncRNAs. In this review, we summarize the current information on the importance of microRNAs and long non-coding RNAs during the development of the eye, inner ear, and olfactory system in vertebrates. We will also discuss those cases in which alteration of ncRNA expression has been linked to pathological conditions affecting these organs.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

lncRNA:

Long non-coding RNA

miRNAs:

microRNAs

NATs:

Natural antisense transcripts

ncRNAs:

Non-coding RNAs

NFAT:

Nuclear factor of the activated T cells

NGS:

Next-generation sequencing

OB:

Olfactory bulb

OE:

Olfactory epithelium

OMP:

Olfactory marker proteins

PRC2:

Polycomb repressive complex 2

RGC:

Retinal ganglion cells

RNCR2:

Retinal non-coding RNA 2

RPE:

Retinal pigment epithelium

Uchl1:

Ubiquitin carboxy-terminal hydrolase L1

References

  1. Jalali S, Jayaraj GG, Scaria V (2012) Integrative transcriptome analysis suggest processing of a subset of long non-coding RNAs to small RNAs. Biol Direct 7:25

    PubMed  CAS  Google Scholar 

  2. Carninci P, Hayashizaki Y (2007) Noncoding RNA transcription beyond annotated genes. Curr Opin Genet Dev 17(2):139–144

    PubMed  CAS  Google Scholar 

  3. Qureshi IA, Mehler MF (2012) Emerging roles of non-coding RNAs in brain evolution, development, plasticity and disease. Nat Rev Neurosci 13(8):528–541

    PubMed  CAS  Google Scholar 

  4. Preker P, Nielsen J, Kammler S, Lykke-Andersen S, Christensen MS, Mapendano CK, Schierup MH, Jensen TH (2008) RNA exosome depletion reveals transcription upstream of active human promoters. Science 322(5909):1851–1854

    PubMed  CAS  Google Scholar 

  5. Jacquier A (2009) The complex eukaryotic transcriptome: unexpected pervasive transcription and novel small RNAs. Nat Rev Genet 10(12):833–844

    PubMed  CAS  Google Scholar 

  6. Rosa A, Brivanlou AH (2009) MicroRNAs in early vertebrate development. Cell Cycle 8(21):3513–3520

    Google Scholar 

  7. Harfe BD (2005) MicroRNAs in vertebrate development. Curr Opin Genet Dev 15(4):410–415

    PubMed  CAS  Google Scholar 

  8. Pauli A, Rinn JL, Schier AF (2011) Non-coding RNAs as regulators of embryogenesis. Nat Rev Genet 12(2):136–149

    PubMed  CAS  Google Scholar 

  9. Bushati N, Cohen SM (2007) microRNA functions. Annu Rev Cell Dev Biol 23:175–205

    PubMed  CAS  Google Scholar 

  10. Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75(5):843–854

    PubMed  CAS  Google Scholar 

  11. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403(6772):901–906

    PubMed  CAS  Google Scholar 

  12. Pasquinelli AE, Reinhart BJ, Slack F, Martindale MQ, Kuroda MI, Maller B, Hayward DC, Ball EE, Degnan B, Muller P, Spring J, Srinivasan A, Fishman M, Finnerty J, Corbo J, Levine M, Leahy P, Davidson E, Ruvkun G (2000) Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408(6808):86–89

    PubMed  CAS  Google Scholar 

  13. Winter J, Jung S, Keller S, Gregory RI, Diederichs S (2009) Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 11(3):228–234

    PubMed  CAS  Google Scholar 

  14. Guo H, Ingolia NT, Weissman JS, Bartel DP (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466(7308):835–840. doi:10.1038/nature09267

    PubMed  CAS  Google Scholar 

  15. Bazzini AA, Lee MT, Giraldez AJ (2012) Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish. Science 336(6078):233–237.doi:10.1126/science.1215704

    PubMed  CAS  Google Scholar 

  16. Djuranovic S, Nahvi A, Green R (2012) miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 336(6078):237–240

    PubMed  CAS  Google Scholar 

  17. He L, Hannon GJ (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5(7):522–531

    PubMed  CAS  Google Scholar 

  18. Lee I, Ajay SS, Yook JI, Kim HS, Hong SH, Kim NH, Dhanasekaran SM, Chinnaiyan AM, Athey BD (2009) New class of microRNA targets containing simultaneous 5′-UTR and 3′-UTR interaction sites. Genome Res 19(7):1175–1183

    PubMed  CAS  Google Scholar 

  19. Tay Y, Zhang J, Thomson AM, Lim B, Rigoutsos I (2008) MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 455(7216):1124–1128

    PubMed  CAS  Google Scholar 

  20. Lytle JR, Yario TA, Steitz JA (2007) Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5′ UTR as in the 3′ UTR. Proc Natl Acad Sci USA 104(23):9667–9672

    PubMed  CAS  Google Scholar 

  21. Gonzalez S, Pisano DG, Serrano M (2008) Mechanistic principles of chromatin remodeling guided by siRNAs and miRNAs. Cell Cycle 7(16):2601–2608

    PubMed  CAS  Google Scholar 

  22. Chitnis NS, Pytel D, Bobrovnikova-Marjon E, Pant D, Zheng H, Maas NL, Frederick B, Kushner JA, Chodosh LA, Koumenis C, Fuchs SY, Diehl JA (2012) miR-211 Is a prosurvival microRNA that regulates chop expression in a PERK-dependent manner. Mol Cell 48(3):353–364

    PubMed  CAS  Google Scholar 

  23. Chen X, Liang H, Zhang J, Zen K, Zhang CY (2012) Horizontal transfer of microRNAs: molecular mechanisms and clinical applications. Protein Cell 3(1):28–37

    PubMed  CAS  Google Scholar 

  24. Fabbri M, Paone A, Calore F, Galli R, Gaudio E, Santhanam R, Lovat F, Fadda P, Mao C, Nuovo GJ, Zanesi N, Crawford M, Ozer GH, Wernicke D, Alder H, Caligiuri MA, Nana-Sinkam P, Perrotti D, Croce CM (2012) MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci USA 109(31):E2110–E2116

    PubMed  CAS  Google Scholar 

  25. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C, Kodzius R, Shimokawa K, Bajic VB, Brenner SE, Batalov S, Forrest AR, Zavolan M, Davis MJ, Wilming LG, Aidinis V, Allen JE, Ambesi-Impiombato A, Apweiler R, Aturaliya RN, Bailey TL, Bansal M, Baxter L, Beisel KW, Bersano T, Bono H, Chalk AM, Chiu KP, Choudhary V, Christoffels A, Clutterbuck DR, Crowe ML, Dalla E, Dalrymple BP, de Bono B, Della Gatta G, di Bernardo D, Down T, Engstrom P, Fagiolini M, Faulkner G, Fletcher CF, Fukushima T, Furuno M, Futaki S, Gariboldi M, Georgii-Hemming P, Gingeras TR, Gojobori T, Green RE, Gustincich S, Harbers M, Hayashi Y, Hensch TK, Hirokawa N, Hill D, Huminiecki L, Iacono M, Ikeo K, Iwama A, Ishikawa T, Jakt M, Kanapin A, Katoh M, Kawasawa Y, Kelso J, Kitamura H, Kitano H, Kollias G, Krishnan SP, Kruger A, Kummerfeld SK, Kurochkin IV, Lareau LF, Lazarevic D, Lipovich L, Liu J, Liuni S, McWilliam S, Madan Babu M, Madera M, Marchionni L, Matsuda H, Matsuzawa S, Miki H, Mignone F, Miyake S, Morris K, Mottagui-Tabar S, Mulder N, Nakano N, Nakauchi H, Ng P, Nilsson R, Nishiguchi S, Nishikawa S, Nori F, Ohara O, Okazaki Y, Orlando V, Pang KC, Pavan WJ, Pavesi G, Pesole G, Petrovsky N, Piazza S, Reed J, Reid JF, Ring BZ, Ringwald M, Rost B, Ruan Y, Salzberg SL, Sandelin A, Schneider C, Schonbach C, Sekiguchi K, Semple CA, Seno S, Sessa L, Sheng Y, Shibata Y, Shimada H, Shimada K, Silva D, Sinclair B, Sperling S, Stupka E, Sugiura K, Sultana R, Takenaka Y, Taki K, Tammoja K, Tan SL, Tang S, Taylor MS, Tegner J, Teichmann SA, Ueda HR, van Nimwegen E, Verardo R, Wei CL, Yagi K, Yamanishi H, Zabarovsky E, Zhu S, Zimmer A, Hide W, Bult C, Grimmond SM, Teasdale RD, Liu ET, Brusic V, Quackenbush J, Wahlestedt C, Mattick JS, Hume DA, Kai C, Sasaki D, Tomaru Y, Fukuda S, Kanamori-Katayama M, Suzuki M, Aoki J, Arakawa T, Iida J, Imamura K, Itoh M, Kato T, Kawaji H, Kawagashira N, Kawashima T, Kojima M, Kondo S, Konno H, Nakano K, Ninomiya N, Nishio T, Okada M, Plessy C, Shibata K, Shiraki T, Suzuki S, Tagami M, Waki K, Watahiki A, Okamura-Oho Y, Suzuki H, Kawai J, Hayashizaki Y (2005) The transcriptional landscape of the mammalian genome. Science 309(5740):1559–1563

    PubMed  CAS  Google Scholar 

  26. Dinger ME, Pang KC, Mercer TR, Mattick JS (2008) Differentiating protein-coding and noncoding RNA: challenges and ambiguities. PLoS Comput Biol 4(11):e1000176

    PubMed  Google Scholar 

  27. Frith MC, Bailey TL, Kasukawa T, Mignone F, Kummerfeld SK, Madera M, Sunkara S, Furuno M, Bult CJ, Quackenbush J, Kai C, Kawai J, Carninci P, Hayashizaki Y, Pesole G, Mattick JS (2006) Discrimination of non-protein-coding transcripts from protein-coding mRNA. RNA Biol 3(1):40–48

    PubMed  CAS  Google Scholar 

  28. Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, Stadler PF, Hertel J, Hackermuller J, Hofacker IL, Bell I, Cheung E, Drenkow J, Dumais E, Patel S, Helt G, Ganesh M, Ghosh S, Piccolboni A, Sementchenko V, Tammana H, Gingeras TR (2007) RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316(5830):1484–1488

    PubMed  CAS  Google Scholar 

  29. Saxena A, Carninci P (2011) Long non-coding RNA modifies chromatin: epigenetic silencing by long non-coding RNAs. Bioessays 33(11):830–839

    PubMed  CAS  Google Scholar 

  30. Blackshaw S, Harpavat S, Trimarchi J, Cai L, Huang H, Kuo WP, Weber G, Lee K, Fraioli RE, Cho SH, Yung R, Asch E, Ohno-Machado L, Wong WH, Cepko CL (2004) Genomic analysis of mouse retinal development. PLoS Biol 2(9):E247

    PubMed  Google Scholar 

  31. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, Chang HY (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129(7):1311–1323

    PubMed  CAS  Google Scholar 

  32. 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

    PubMed  CAS  Google Scholar 

  33. Ravasi T, Suzuki H, Pang KC, Katayama S, Furuno M, Okunishi R, Fukuda S, Ru K, Frith MC, Gongora MM, Grimmond SM, Hume DA, Hayashizaki Y, Mattick JS (2006) Experimental validation of the regulated expression of large numbers of non-coding RNAs from the mouse genome. Genome Res 16(1):11–19

    PubMed  CAS  Google Scholar 

  34. 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

    PubMed  CAS  Google Scholar 

  35. Clemson CM, Hutchinson JN, Sara SA, Ensminger AW, Fox AH, Chess A, Lawrence JB (2009) An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol Cell 33(6):717–726

    PubMed  CAS  Google Scholar 

  36. Hutchinson JN, Ensminger AW, Clemson CM, Lynch CR, Lawrence JB, Chess A (2007) A screen for nuclear transcripts identifies two linked noncoding RNAs associated with SC35 splicing domains. BMC genomics 8:39

    PubMed  Google Scholar 

  37. Sone M, Hayashi T, Tarui H, Agata K, Takeichi M, Nakagawa S (2007) The mRNA-like noncoding RNA Gomafu constitutes a novel nuclear domain in a subset of neurons. J Cell Sci 120(Pt 15):2498–2506

    PubMed  CAS  Google Scholar 

  38. Sunwoo H, Dinger ME, Wilusz JE, Amaral PP, Mattick JS, Spector DL (2009) MEN epsilon/beta nuclear-retained non-coding RNAs are up-regulated upon muscle differentiation and are essential components of paraspeckles. Genome Res 19(3):347–359

    PubMed  CAS  Google Scholar 

  39. Szymanski M, Barciszewska MZ, Erdmann VA, Barciszewski J (2005) A new frontier for molecular medicine: noncoding RNAs. Biochim Biophys Acta 1756(1):65–75

    PubMed  CAS  Google Scholar 

  40. Prasanth KV, Spector DL (2007) Eukaryotic regulatory RNAs: an answer to the ‘genome complexity’ conundrum. Genes Dev 21(1):11–42

    PubMed  CAS  Google Scholar 

  41. Chen G, Wang Z, Wang D, Qiu C, Liu M, Chen X, Zhang Q, Yan G, Cui Q (2012) LncRNAdisease: a database for long-non-coding RNA-associated diseases. Nucleic Acids Res 41:D983–D986. doi:10.1093/nar/gks1099

    PubMed  Google Scholar 

  42. Rackham O, Shearwood AM, Mercer TR, Davies SM, Mattick JS, Filipovska A (2011) Long noncoding RNAs are generated from the mitochondrial genome and regulated by nuclear-encoded proteins. RNA 17(12):2085–2093

    PubMed  CAS  Google Scholar 

  43. Zhao J, Sun BK, Erwin JA, Song JJ, Lee JT (2008) Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322(5902):750–756

    PubMed  CAS  Google Scholar 

  44. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL, Wang Y, Brzoska P, Kong B, Li R, West RB, van de Vijver MJ, Sukumar S, Chang HY (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464(7291):1071–1076

    PubMed  CAS  Google Scholar 

  45. Hung T, Chang HY (2010) Long noncoding RNA in genome regulation: prospects and mechanisms. RNA Biol 7(5):582–585

    PubMed  CAS  Google Scholar 

  46. Mohammad F, Mondal T, Guseva N, Pandey GK, Kanduri C (2010) Kcnq1ot1 noncoding RNA mediates transcriptional gene silencing by interacting with Dnmt1. Development 137(15):2493–2499

    PubMed  CAS  Google Scholar 

  47. Bertani S, Sauer S, Bolotin E, Sauer F (2011) The noncoding RNA Mistral activates Hoxa6 and Hoxa7 expression and stem cell differentiation by recruiting MLL1 to chromatin. Mol Cell 43(6):1040–1046

    PubMed  CAS  Google Scholar 

  48. Willingham AT, Orth AP, Batalov S, Peters EC, Wen BG, Aza-Blanc P, Hogenesch JB, Schultz PG (2005) A strategy for probing the function of noncoding RNAs finds a repressor of NFAT. Science 309(5740):1570–1573

    PubMed  CAS  Google Scholar 

  49. Moran VA, Perera RJ, Khalil AM (2012) Emerging functional and mechanistic paradigms of mammalian long non-coding RNAs. Nucleic Acids Res 40(14):6391–6400

    PubMed  CAS  Google Scholar 

  50. Gong C, Maquat LE (2011) lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3′ UTRs via Alu elements. Nature 470(7333):284–288

    PubMed  CAS  Google Scholar 

  51. Faghihi MA, Modarresi F, Khalil AM, Wood DE, Sahagan BG, Morgan TE, Finch CE, St Laurent G 3rd, Kenny PJ, Wahlestedt C (2008) Expression of a noncoding RNA is elevated in Alzheimer’s disease and drives rapid feed-forward regulation of β-secretase. Nat Med 14(7):723–730

    PubMed  CAS  Google Scholar 

  52. Carrieri C, Cimatti L, Biagioli M, Beugnet A, Zucchelli S, Fedele S, Pesce E, Ferrer I, Collavin L, Santoro C, Forrest AR, Carninci P, Biffo S, Stupka E, Gustincich S (2012) Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature 491(7424):454–457

    PubMed  CAS  Google Scholar 

  53. Poliseno L, Salmena L, Zhang J, Carver B, Haveman WJ, Pandolfi PP (2010) A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465(7301):1033–1038

    PubMed  CAS  Google Scholar 

  54. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, Garcia JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39(8):1033–1037

    PubMed  CAS  Google Scholar 

  55. Tay Y, Kats L, Salmena L, Weiss D, Tan SM, Ala U, Karreth F, Poliseno L, Provero P, Di Cunto F, Lieberman J, Rigoutsos I, Pandolfi PP (2011) Coding-independent regulation of the tumor suppressor PTEN by competing endogenous mRNAs. Cell 147(2):344–357

    PubMed  CAS  Google Scholar 

  56. Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, Tramontano A, Bozzoni I (2011) A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147(2):358–369

    PubMed  CAS  Google Scholar 

  57. Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP (2011) A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146(3):353–358

    PubMed  CAS  Google Scholar 

  58. Bond AM, Vangompel MJ, Sametsky EA, Clark MF, Savage JC, Disterhoft JF, Kohtz JD (2009) Balanced gene regulation by an embryonic brain ncRNA is critical for adult hippocampal GABA circuitry. Nat Neurosci 12(8):1020–1027

    PubMed  CAS  Google Scholar 

  59. Klattenhoff CA, Scheuermann JC, Surface LE, Bradley RK, Fields PA, Steinhauser ML, Ding H, Butty VL, Torrey L, Haas S, Abo R, Tabebordbar M, Lee RT, Burge CB, Boyer LA (2013) Braveheart, a long noncoding RNA required for cardiovascular lineage commitment. Cell 152(3):570–583

    PubMed  CAS  Google Scholar 

  60. Alsina B, Giraldez F, Pujades C (2009) Patterning and cell fate in ear development. Int J Dev Biol 53(8–10):1503–1513

    PubMed  Google Scholar 

  61. Cole LK, Le Roux I, Nunes F, Laufer E, Lewis J, Wu DK (2000) Sensory organ generation in the chicken inner ear: contributions of bone morphogenetic protein 4, serrate1, and lunatic fringe. J Comp Neurol 424(3):509–520

    PubMed  CAS  Google Scholar 

  62. Lleras-Forero L, Streit A (2012) Development of the sensory nervous system in the vertebrate head: the importance of being on time. Curr Opin Genet Dev 22(4):315–322

    PubMed  CAS  Google Scholar 

  63. Groves AK, Fekete DM (2012) Shaping sound in space: the regulation of inner ear patterning. Development 139(2):245–257

    PubMed  CAS  Google Scholar 

  64. Wu DK, Kelley MW (2012) Molecular mechanisms of inner ear development. Cold Spring Harb Perspect Biol 4(8):a008409

    PubMed  Google Scholar 

  65. Brigande JV, Kiernan AE, Gao X, Iten LE, Fekete DM (2000) Molecular genetics of pattern formation in the inner ear: do compartment boundaries play a role? Proc Natl Acad Sci USA 97(22):11700–11706

    PubMed  CAS  Google Scholar 

  66. Cantos R, Cole LK, Acampora D, Simeone A, Wu DK (2000) Patterning of the mammalian cochlea. Proc Natl Acad Sci USA 97(22):11707–11713

    PubMed  CAS  Google Scholar 

  67. Patel M, Hu BH (2012) MicroRNAs in inner ear biology and pathogenesis. Hear Res 287(1–2):6–14

    PubMed  CAS  Google Scholar 

  68. Weston MD, Pierce ML, Rocha-Sanchez S, Beisel KW, Soukup GA (2006) MicroRNA gene expression in the mouse inner ear. Brain Res 1111(1):95–104

    PubMed  CAS  Google Scholar 

  69. Hirai M, Maeda Y, Fukushima K, Sugaya A, Kataoka Y, Nishizaki K (2011) Expression analysis of microRNAs in murine cochlear explants. NeuroReport 22(13):652–654

    PubMed  CAS  Google Scholar 

  70. Elkan-Miller T, Ulitsky I, Hertzano R, Rudnicki A, Dror AA, Lenz DR, Elkon R, Irmler M, Beckers J, Shamir R, Avraham KB (2011) Integration of transcriptomics, proteomics, and microRNA analyses reveals novel microRNA regulation of targets in the mammalian inner ear. PLoS ONE 6(4):e18195

    PubMed  CAS  Google Scholar 

  71. Friedman LM, Dror AA, Mor E, Tenne T, Toren G, Satoh T, Biesemeier DJ, Shomron N, Fekete DM, Hornstein E, Avraham KB (2009) MicroRNAs are essential for development and function of inner ear hair cells in vertebrates. Proc Natl Acad Sci USA 106(19):7915–7920

    PubMed  CAS  Google Scholar 

  72. Hertzano R, Elkon R (2012) High throughput gene expression analysis of the inner ear. Hear Res 288(1–2):77–88

    PubMed  CAS  Google Scholar 

  73. Wienholds E, Kloosterman WP, Miska E, Alvarez-Saavedra E, Berezikov E, de Bruijn E, Horvitz HR, Kauppinen S, Plasterk RH (2005) MicroRNA expression in zebrafish embryonic development. Science 309(5732):310–311

    PubMed  CAS  Google Scholar 

  74. Wang XR, Zhang XM, Zhen J, Zhang PX, Xu G, Jiang H (2010) MicroRNA expression in the embryonic mouse inner ear. NeuroReport 21(9):611–617

    PubMed  CAS  Google Scholar 

  75. Ohyama T, Groves AK (2004) Generation of Pax2-Cre mice by modification of a Pax2 bacterial artificial chromosome. Genesis 38(4):195–199

    PubMed  CAS  Google Scholar 

  76. Soukup GA, Fritzsch B, Pierce ML, Weston MD, Jahan I, McManus MT, Harfe BD (2009) Residual microRNA expression dictates the extent of inner ear development in conditional Dicer knockout mice. Dev Biol 328(2):328–341

    PubMed  CAS  Google Scholar 

  77. Weston MD, Pierce ML, Jensen-Smith HC, Fritzsch B, Rocha-Sanchez S, Beisel KW, Soukup GA (2011) MicroRNA-183 family expression in hair cell development and requirement of microRNAs for hair cell maintenance and survival. Dev Dyn 240(4):808–819

    PubMed  CAS  Google Scholar 

  78. Kersigo J, D’Angelo A, Gray BD, Soukup GA, Fritzsch B (2011) The role of sensory organs and the forebrain for the development of the craniofacial shape as revealed by Foxg1-cre-mediated microRNA loss. Genesis 49(4):326–341

    PubMed  CAS  Google Scholar 

  79. Bohne BA, Yohman L, Gruner MM (1987) Cochlear damage following interrupted exposure to high-frequency noise. Hear Res 29(2–3):251–264

    PubMed  CAS  Google Scholar 

  80. Fechter LD, Liu Y, Pearce TA (1997) Cochlear protection from carbon monoxide exposure by free radical blockers in the guinea pig. Toxicol Appl Pharmacol 142(1):47–55

    PubMed  CAS  Google Scholar 

  81. Hu BH, Henderson D, Nicotera TM (2002) Involvement of apoptosis in progression of cochlear lesion following exposure to intense noise. Hear Res 166(1–2):62–71

    PubMed  Google Scholar 

  82. Sha SH, Taylor R, Forge A, Schacht J (2001) Differential vulnerability of basal and apical hair cells is based on intrinsic susceptibility to free radicals. Hear Res 155(1–2):1–8

    PubMed  CAS  Google Scholar 

  83. Sacheli R, Nguyen L, Borgs L, Vandenbosch R, Bodson M, Lefebvre P, Malgrange B (2009) Expression patterns of miR-96, miR-182, and miR-183 in the development inner ear. Gene Expr Patterns 9(5):364–370

    PubMed  CAS  Google Scholar 

  84. Xu S, Witmer PD, Lumayag S, Kovacs B, Valle D (2007) MicroRNA (miRNA) transcriptome of mouse retina and identification of a sensory organ-specific miRNA cluster. J Biol Chem 282(34):25053–25066

    PubMed  CAS  Google Scholar 

  85. Jalvy-Delvaille S, Maurel M, Majo V, Pierre N, Chabas S, Combe C, Rosenbaum J, Sagliocco F, Grosset CF (2012) Molecular basis of differential target regulation by miR-96 and miR-182: the Glypican-3 as a model. Nucleic Acids Res 40(3):1356–1365

    PubMed  CAS  Google Scholar 

  86. Lewis MA, Quint E, Glazier AM, Fuchs H, De Angelis MH, Langford C, van Dongen S, Abreu-Goodger C, Piipari M, Redshaw N, Dalmay T, Moreno-Pelayo MA, Enright AJ, Steel KP (2009) An ENU-induced mutation of miR-96 associated with progressive hearing loss in mice. Nat Genet 41(5):614–618

    PubMed  CAS  Google Scholar 

  87. Li H, Kloosterman W, Fekete DM (2010) MicroRNA-183 family members regulate sensorineural fates in the inner ear. J Neurosci 30(9):3254–3263

    PubMed  CAS  Google Scholar 

  88. Wang XR, Zhang XM, Du J, Jiang H (2012) MicroRNA-182 regulates otocyst-derived cell differentiation and targets T-box1 gene. Hear Res 286(1–2):55–63

    PubMed  CAS  Google Scholar 

  89. Gu C, Li X, Tan Q, Wang Z, Chen L, Liu Y (2013) MiR-183 family regulates chloride intracellular channel 5 expression in inner ear hair cells. Toxicol In Vitro 27(1):486–491

    PubMed  CAS  Google Scholar 

  90. Hertzano R, Elkon R, Kurima K, Morrisson A, Chan SL, Sallin M, Biedlingmaier A, Darling DS, Griffith AJ, Eisenman DJ, Strome SE (2011) Cell type-specific transcriptome analysis reveals a major role for Zeb1 and miR-200b in mouse inner ear morphogenesis. PLoS Genet 7(9):e1002309

    PubMed  CAS  Google Scholar 

  91. Frucht CS, Santos-Sacchi J, Navaratnam DS (2011) MicroRNA181a plays a key role in hair cell regeneration in the avian auditory epithelium. Neurosci Lett 493(1–2):44–48

    PubMed  CAS  Google Scholar 

  92. Mencia A, Modamio-Hoybjor S, Redshaw N, Morin M, Mayo-Merino F, Olavarrieta L, Aguirre LA, del Castillo I, Steel KP, Dalmay T, Moreno F, Moreno-Pelayo MA (2009) Mutations in the seed region of human miR-96 are responsible for nonsyndromic progressive hearing loss. Nat Genet 41(5):609–613

    PubMed  CAS  Google Scholar 

  93. Solda G, Robusto M, Primignani P, Castorina P, Benzoni E, Cesarani A, Ambrosetti U, Asselta R, Duga S (2012) A novel mutation within the MIR96 gene causes non-syndromic inherited hearing loss in an Italian family by altering pre-miRNA processing. Hum Mol Genet 21(3):577–585

    PubMed  CAS  Google Scholar 

  94. Cioffi JA, Yue WY, Mendolia-Loffredo S, Hansen KR, Wackym PA, Hansen MR (2010) MicroRNA-21 overexpression contributes to vestibular schwannoma cell proliferation and survival. Otol Neurotol 31(9):1455–1462

    PubMed  Google Scholar 

  95. Friedland DR, Eernisse R, Erbe C, Gupta N, Cioffi JA (2009) Cholesteatoma growth and proliferation: posttranscriptional regulation by microRNA-21. Otol Neurotol 30(7):998–1005

    PubMed  Google Scholar 

  96. Roberts KA, Abraira VE, Tucker AF, Goodrich LV, Andrews NC (2012) Mutation of Rubie, a novel long non-coding RNA located upstream of Bmp4, causes vestibular malformation in mice. PLoS ONE 7(1):e29495

    PubMed  CAS  Google Scholar 

  97. Esteve P, Bovolenta P (2006) Secreted inducers in vertebrate eye development: more functions for old morphogens. Curr Opin Neurobiol 16(1):13–19

    PubMed  CAS  Google Scholar 

  98. Martinez-Morales JR, Rodrigo I, Bovolenta P (2004) Eye development: a view from the retina pigmented epithelium. Bioessays: News Rev Mol Cell Dev Biol 26(7):766–777

    CAS  Google Scholar 

  99. Beccari L, Marco-Ferreres R, Bovolenta P (2013) The logic of gene regulatory networks in early vertebrate forebrain patterning. Mech Dev 130:95–111

    Google Scholar 

  100. Bassett EA, Wallace VA (2012) Cell fate determination in the vertebrate retina. Trends Neurosci 35(9):565–573

    PubMed  CAS  Google Scholar 

  101. Shaham O, Menuchin Y, Farhy C, Ashery-Padan R (2012) Pax6: a multi-level regulator of ocular development. Prog Retin Eye Res 31(5):351–376

    PubMed  CAS  Google Scholar 

  102. Fuhrmann S (2010) Eye morphogenesis and patterning of the optic vesicle. Curr Top Dev Biol 93:61–84

    PubMed  Google Scholar 

  103. Frederikse PH, Donnelly R, Partyka LM (2006) MiRNA and Dicer in the mammalian lens: expression of brain-specific miRNAs in the lens. Histochem Cell Biol 126(1):1–8

    PubMed  CAS  Google Scholar 

  104. Karali M, Peluso I, Gennarino VA, Bilio M, Verde R, Lago G, Dolle P, Banfi S (2010) miRNeye: a microRNA expression atlas of the mouse eye. BMC Genomics 11:715

    PubMed  CAS  Google Scholar 

  105. Karali M, Peluso I, Marigo V, Banfi S (2007) Identification and characterization of microRNAs expressed in the mouse eye. Invest Ophthalmol Vis Sci 48(2):509–515

    PubMed  Google Scholar 

  106. Ryan DG, Oliveira-Fernandes M, Lavker RM (2006) MicroRNAs of the mammalian eye display distinct and overlapping tissue specificity. Mol Vis 12:1175–1184

    PubMed  CAS  Google Scholar 

  107. Makarev E, Spence JR, Del Rio-Tsonis K, Tsonis PA (2006) Identification of microRNAs and other small RNAs from the adult newt eye. Mol Vis 12:1386–1391. doi:v12/a156

    PubMed  CAS  Google Scholar 

  108. Wu C, Lin H, Wang Q, Chen W, Luo H, Zhang H (2012) Discrepant expression of microRNAs in transparent and cataractous human lenses. Invest Ophthalmol Vis Sci 53(7):3906–3912

    PubMed  CAS  Google Scholar 

  109. Yan N, Ma K, Ma J, Chen W, Wang Y, Cao G, Man-Kit Lam D, Liu X (2010) Profiling microRNAs differentially expressed in rabbit retina. Adv Exp Med Biol 664:203–209

    PubMed  CAS  Google Scholar 

  110. Hackler L Jr, Wan J, Swaroop A, Qian J, Zack DJ (2010) MicroRNA profile of the developing mouse retina. Invest Ophthalmol Vis Sci 51(4):1823–1831

    PubMed  Google Scholar 

  111. Arora A, Guduric-Fuchs J, Harwood L, Dellett M, Cogliati T, Simpson DA (2010) Prediction of microRNAs affecting mRNA expression during retinal development. BMC Dev Biol 10:1

    PubMed  Google Scholar 

  112. Arora A, McKay GJ, Simpson DA (2007) Prediction and verification of miRNA expression in human and rat retinas. Invest Ophthalmol Vis Sci 48(9):3962–3967

    PubMed  Google Scholar 

  113. Li Y, Piatigorsky J (2009) Targeted deletion of Dicer disrupts lens morphogenesis, corneal epithelium stratification, and whole eye development. Dev Dyn 238(9):2388–2400

    PubMed  Google Scholar 

  114. Pinter R, Hindges R (2010) Perturbations of microRNA function in mouse dicer mutants produce retinal defects and lead to aberrant axon pathfinding at the optic chiasm. PLoS ONE 5(4):e10021

    PubMed  Google Scholar 

  115. Iida A, Shinoe T, Baba Y, Mano H, Watanabe S (2011) Dicer plays essential roles for retinal development by regulation of survival and differentiation. Invest Ophthalmol Vis Sci 52(6):3008–3017

    PubMed  CAS  Google Scholar 

  116. Georgi SA, Reh TA (2010) Dicer is required for the transition from early to late progenitor state in the developing mouse retina. J Neurosci 30(11):4048–4061

    PubMed  CAS  Google Scholar 

  117. Damiani D, Alexander JJ, O’Rourke JR, McManus M, Jadhav AP, Cepko CL, Hauswirth WW, Harfe BD, Strettoi E (2008) Dicer inactivation leads to progressive functional and structural degeneration of the mouse retina. J Neurosci 28(19):4878–4887

    PubMed  CAS  Google Scholar 

  118. Decembrini S, Andreazzoli M, Barsacchi G, Cremisi F (2008) Dicer inactivation causes heterochronic retinogenesis in Xenopus laevis. Int J Dev Biol 52(8):1099–1103

    PubMed  CAS  Google Scholar 

  119. Davis N, Mor E, Ashery-Padan R (2011) Roles for Dicer1 in the patterning and differentiation of the optic cup neuroepithelium. Development 138(1):127–138

    PubMed  CAS  Google Scholar 

  120. Kaneko H, Dridi S, Tarallo V, Gelfand BD, Fowler BJ, Cho WG, Kleinman ME, Ponicsan SL, Hauswirth WW, Chiodo VA, Kariko K, Yoo JW, Lee DK, Hadziahmetovic M, Song Y, Misra S, Chaudhuri G, Buaas FW, Braun RE, Hinton DR, Zhang Q, Grossniklaus HE, Provis JM, Madigan MC, Milam AH, Justice NL, Albuquerque RJ, Blandford AD, Bogdanovich S, Hirano Y, Witta J, Fuchs E, Littman DR, Ambati BK, Rudin CM, Chong MM, Provost P, Kugel JF, Goodrich JA, Dunaief JL, Baffi JZ, Ambati J (2011) DICER1 deficit induces Alu RNA toxicity in age-related macular degeneration. Nature 471(7338):325–330

    PubMed  CAS  Google Scholar 

  121. Qiu R, Liu Y, Wu JY, Liu K, Mo W, He R (2009) Misexpression of miR-196a induces eye anomaly in Xenopus laevis. Brain Res Bull 79(1):26–31

    PubMed  CAS  Google Scholar 

  122. Walker JC, Harland RM (2009) microRNA-24a is required to repress apoptosis in the developing neural retina. Genes Dev 23(9):1046–1051

    PubMed  CAS  Google Scholar 

  123. Qiu R, Liu K, Liu Y, Mo W, Flynt AS, Patton JG, Kar A, Wu JY, He R (2009) The role of miR-124a in early development of the Xenopus eye. Mech Dev 126(10):804–816

    PubMed  CAS  Google Scholar 

  124. Liu K, Liu Y, Mo W, Qiu R, Wang X, Wu JY, He R (2011) MiR-124 regulates early neurogenesis in the optic vesicle and forebrain, targeting NeuroD1. Nucleic Acids Res 39(7):2869–2879

    PubMed  CAS  Google Scholar 

  125. Baudet ML, Zivraj KH, Abreu-Goodger C, Muldal A, Armisen J, Blenkiron C, Goldstein LD, Miska EA, Holt CE (2012) miR-124 acts through CoREST to control onset of Sema3A sensitivity in navigating retinal growth cones. Nat Neurosci 15(1):29–38

    CAS  Google Scholar 

  126. Decembrini S, Bressan D, Vignali R, Pitto L, Mariotti S, Rainaldi G, Wang X, Evangelista M, Barsacchi G, Cremisi F (2009) MicroRNAs couple cell fate and developmental timing in retina. Proc Natl Acad Sci USA 106(50):21179–21184

    PubMed  CAS  Google Scholar 

  127. Conte I, Carrella S, Avellino R, Karali M, Marco-Ferreres R, Bovolenta P, Banfi S (2010) miR-204 is required for lens and retinal development via Meis2 targeting. Proc Natl Acad Sci USA 107(35):15491–15496

    PubMed  CAS  Google Scholar 

  128. Wang FE, Zhang C, Maminishkis A, Dong L, Zhi C, Li R, Zhao J, Majerciak V, Gaur AB, Chen S, Miller SS (2010) MicroRNA-204/211 alters epithelial physiology. FASEB J 24(5):1552–1571

    PubMed  CAS  Google Scholar 

  129. Adijanto J, Castorino JJ, Wang ZX, Maminishkis A, Grunwald GB, Philp NJ (2012) Microphthalmia-associated transcription factor (MITF) promotes differentiation of human retinal pigment epithelium (RPE) by regulating microRNAs-204/211 expression. J Biol Chem 287(24):20491–20503

    PubMed  CAS  Google Scholar 

  130. Zhu Q, Sun W, Okano K, Chen Y, Zhang N, Maeda T, Palczewski K (2011) Sponge transgenic mouse model reveals important roles for the microRNA-183 (miR-183)/96/182 cluster in postmitotic photoreceptors of the retina. J Biol Chem 286(36):31749–31760

    PubMed  CAS  Google Scholar 

  131. Lumayag S, Haldin CE, Corbett NJ, Wahlin KJ, Cowan C, Turturro S, Larsen PE, Kovacs B, Witmer PD, Valle D, Zack DJ, Nicholson DA, Xu S (2013) Inactivation of the microRNA-183/96/182 cluster results in syndromic retinal degeneration. Proc Natl Acad Sci USA. doi:10.1073/pnas.1212655110

    PubMed  Google Scholar 

  132. Jin ZB, Hirokawa G, Gui L, Takahashi R, Osakada F, Hiura Y, Takahashi M, Yasuhara O, Iwai N (2009) Targeted deletion of miR-182, an abundant retinal microRNA. Mol Vis 15:523–533

    PubMed  CAS  Google Scholar 

  133. Sanuki R, Onishi A, Koike C, Muramatsu R, Watanabe S, Muranishi Y, Irie S, Uneo S, Koyasu T, Matsui R, Cherasse Y, Urade Y, Watanabe D, Kondo M, Yamashita T, Furukawa T (2011) miR-124a is required for hippocampal axogenesis and retinal cone survival through Lhx2 suppression. Nat Neurosci 14(9):1125–1134

    PubMed  CAS  Google Scholar 

  134. Ramachandran R, Fausett BV, Goldman D (2010) Ascl1a regulates Muller glia dedifferentiation and retinal regeneration through a Lin-28-dependent, let-7 microRNA signalling pathway. Nat Cell Biol 12(11):1101–1107

    PubMed  CAS  Google Scholar 

  135. Li Y, Li C, Chen Z, He J, Tao Z, Yin ZQ (2012) A microRNA, mir133b, suppresses melanopsin expression mediated by failure dopaminergic amacrine cells in RCS rats. Cell Signal 24(3):685–698

    PubMed  CAS  Google Scholar 

  136. Shen J, Yang X, Xie B, Chen Y, Swaim M, Hackett SF, Campochiaro PA (2008) MicroRNAs regulate ocular neovascularization. Mol Ther 16(7):1208–1216

    PubMed  CAS  Google Scholar 

  137. Small EM, Sutherland LB, Rajagopalan KN, Wang S, Olson EN (2010) MicroRNA-218 regulates vascular patterning by modulation of Slit-Robo signaling. Circ Res 107(11):1336–1344

    PubMed  CAS  Google Scholar 

  138. Krol J, Busskamp V, Markiewicz I, Stadler MB, Ribi S, Richter J, Duebel J, Bicker S, Fehling HJ, Schubeler D, Oertner TG, Schratt G, Bibel M, Roska B, Filipowicz W (2010) Characterizing light-regulated retinal microRNAs reveals rapid turnover as a common property of neuronal microRNAs. Cell 141(4):618–631

    PubMed  CAS  Google Scholar 

  139. Silva VA, Polesskaya A, Sousa TA, Correa VM, Andre ND, Reis RI, Kettelhut IC, Harel-Bellan A, De Lucca FL (2011) Expression and cellular localization of microRNA-29b and RAX, an activator of the RNA-dependent protein kinase (PKR), in the retina of streptozotocin-induced diabetic rats. Mol Vis 17:2228–2240

    PubMed  CAS  Google Scholar 

  140. Loscher CJ, Hokamp K, Kenna PF, Ivens AC, Humphries P, Palfi A, Farrar GJ (2007) Altered retinal microRNA expression profile in a mouse model of retinitis pigmentosa. Genome Biol 8(11):R248

    PubMed  Google Scholar 

  141. Loscher CJ, Hokamp K, Wilson JH, Li T, Humphries P, Farrar GJ, Palfi A (2008) A common microRNA signature in mouse models of retinal degeneration. Exp Eye Res 87(6):529–534

    PubMed  CAS  Google Scholar 

  142. Ishida W, Fukuda K, Higuchi T, Kajisako M, Sakamoto S, Fukushima A (2011) Dynamic changes of microRNAs in the eye during the development of experimental autoimmune uveoretinitis. Invest Ophthalmol Vis Sci 52(1):611–617

    PubMed  CAS  Google Scholar 

  143. Kovacs B, Lumayag S, Cowan C, Xu S (2011) MicroRNAs in early diabetic retinopathy in streptozotocin-induced diabetic rats. Invest Ophthalmol Vis Sci 52(7):4402–4409

    PubMed  CAS  Google Scholar 

  144. Peng CH, Liu JH, Woung LC, Lin TJ, Chiou SH, Tseng PC, Du WY, Cheng CK, Hu CC, Chien KH, Chen SJ (2012) MicroRNAs and cataracts: correlation among let-7 expression, age and the severity of lens opacity. Br J Ophthalmol 96(5):747–751

    PubMed  Google Scholar 

  145. Hughes AE, Bradley DT, Campbell M, Lechner J, Dash DP, Simpson DA, Willoughby CE (2011) Mutation altering the miR-184 seed region causes familial keratoconus with cataract. Am J Hum Genet 89(5):628–633

    PubMed  CAS  Google Scholar 

  146. Hoffmann A, Huang Y, Suetsugu-Maki R, Ringelberg CS, Tomlinson CR, Del Rio-Tsonis K, Tsonis PA (2012) Implication of the miR-184 and miR-204 competitive RNA network in control of mouse secondary cataract. Mol Med 18:528–538

    PubMed  CAS  Google Scholar 

  147. Georgiadis A, Tschernutter M, Bainbridge JW, Robbie SJ, McIntosh J, Nathwani AC, Smith AJ, Ali RR (2010) AAV-mediated knockdown of peripherin-2 in vivo using miRNA-based hairpins. Gene Ther 17(4):486–493

    PubMed  CAS  Google Scholar 

  148. Karali M, Manfredi A, Puppo A, Marrocco E, Gargiulo A, Allocca M, Corte MD, Rossi S, Giunti M, Bacci ML, Simonelli F, Surace EM, Banfi S, Auricchio A (2011) MicroRNA-restricted transgene expression in the retina. PLoS ONE 6(7):e22166

    PubMed  CAS  Google Scholar 

  149. Pihlmann M, Askou AL, Aagaard L, Bruun GH, Svalgaard JD, Holm-Nielsen MH, Dagnaes-Hansen F, Bek T, Mikkelsen JG, Jensen TG, Corydon TJ (2012) Adeno-associated virus-delivered polycistronic microRNA-clusters for knockdown of vascular endothelial growth factor in vivo. J Gene Med 14(5):328–338

    PubMed  CAS  Google Scholar 

  150. Bai Y, Bai X, Wang Z, Zhang X, Ruan C, Miao J (2011) MicroRNA-126 inhibits ischemia-induced retinal neovascularization via regulating angiogenic growth factors. Exp Mol Pathol 91(1):471–477

    PubMed  CAS  Google Scholar 

  151. McArthur K, Feng B, Wu Y, Chen S, Chakrabarti S (2011) MicroRNA-200b regulates vascular endothelial growth factor-mediated alterations in diabetic retinopathy. Diabetes 60(4):1314–1323

    PubMed  CAS  Google Scholar 

  152. Chen KC, Hsi E, Hu CY, Chou WW, Liang CL, Juo SH (2012) MicroRNA-328 may influence myopia development by mediating the PAX6 gene. Invest Ophthalmol Vis Sci 53(6):2732–2739

    PubMed  CAS  Google Scholar 

  153. Rapicavoli NA, Blackshaw S (2009) New meaning in the message: noncoding RNAs and their role in retinal development. Dev Dyn 238(9):2103–2114

    PubMed  CAS  Google Scholar 

  154. Geng X, Lavado A, Lagutin OV, Liu W, Oliver G (2007) Expression of Six3 Opposite Strand (Six3OS) during mouse embryonic development. Gene Expr Patterns 7(3):252–257

    PubMed  CAS  Google Scholar 

  155. Rapicavoli NA, Poth EM, Zhu H, Blackshaw S (2011) The long noncoding RNA Six3OS acts in trans to regulate retinal development by modulating Six3 activity. Neural Dev 6:32

    PubMed  CAS  Google Scholar 

  156. Meola N, Pizzo M, Alfano G, Surace EM, Banfi S (2012) The long noncoding RNA Vax2os1 controls the cell cycle progression of photoreceptor progenitors in the mouse retina. RNA 18(1):111–123

    PubMed  CAS  Google Scholar 

  157. Alfano G, Vitiello C, Caccioppoli C, Caramico T, Carola A, Szego MJ, McInnes RR, Auricchio A, Banfi S (2005) Natural antisense transcripts associated with genes involved in eye development. Hum Mol Genet 14(7):913–923

    PubMed  CAS  Google Scholar 

  158. Young TL, Matsuda T, Cepko CL (2005) The noncoding RNA taurine upregulated gene 1 is required for differentiation of the murine retina. Curr Biol 15(6):501–512

    PubMed  CAS  Google Scholar 

  159. Rapicavoli NA, Poth EM, Blackshaw S (2010) The long noncoding RNA RNCR2 directs mouse retinal cell specification. BMC Dev Biol 10:49

    PubMed  Google Scholar 

  160. Sheik Mohamed J, Gaughwin PM, Lim B, Robson P, Lipovich L (2010) Conserved long noncoding RNAs transcriptionally regulated by Oct4 and Nanog modulate pluripotency in mouse embryonic stem cells. RNA 16(2):324–337

    PubMed  Google Scholar 

  161. Tsuiji H, Yoshimoto R, Hasegawa Y, Furuno M, Yoshida M, Nakagawa S (2011) Competition between a noncoding exon and introns: gomafu contains tandem UACUAAC repeats and associates with splicing factor-1. Genes Cells: Devoted Mol Cell Mech 16(5):479–490

    CAS  Google Scholar 

  162. Mori K, Yoshihara Y (1995) Molecular recognition and olfactory processing in the mammalian olfactory system. Prog Neurobiol 45(6):585–619

    PubMed  CAS  Google Scholar 

  163. Yoshihara Y, Mori K (1997) Basic principles and molecular mechanisms of olfactory axon pathfinding. Cell Tissue Res 290(2):457–463

    PubMed  CAS  Google Scholar 

  164. Mori K, von Campenhause H, Yoshihara Y (2000) Zonal organization of the mammalian main and accessory olfactory systems. Philos Trans R Soc Lond B Biol Sci 355(1404):1801–1812

    PubMed  CAS  Google Scholar 

  165. Brunjes PC, Greer CA (2003) Progress and directions in olfactory development. Neuron 38(3):371–374

    PubMed  CAS  Google Scholar 

  166. Nicolay DJ, Doucette JR, Nazarali AJ (2006) Transcriptional regulation of neurogenesis in the olfactory epithelium. Cell Mol Neurobiol 26(4–6):803–821

    PubMed  CAS  Google Scholar 

  167. Lopez-Mascaraque L, de Castro F (2002) The olfactory bulb as an independent developmental domain. Cell Death Differ 9(12):1279–1286

    PubMed  CAS  Google Scholar 

  168. Ason B, Darnell DK, Wittbrodt B, Berezikov E, Kloosterman WP, Wittbrodt J, Antin PB, Plasterk RH (2006) Differences in vertebrate microRNA expression. Proc Natl Acad Sci USA 103(39):14385–14389

    PubMed  CAS  Google Scholar 

  169. Castoldi M, Schmidt S, Benes V, Noerholm M, Kulozik AE, Hentze MW, Muckenthaler MU (2006) A sensitive array for microRNA expression profiling (miChip) based on locked nucleic acids (LNA). RNA 12(5):913–920

    PubMed  CAS  Google Scholar 

  170. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33(20):e179

    PubMed  Google Scholar 

  171. Choi PS, Zakhary L, Choi WY, Caron S, Alvarez-Saavedra E, Miska EA, McManus M, Harfe B, Giraldez AJ, Horvitz HR, Schier AF, Dulac C (2008) Members of the miRNA-200 family regulate olfactory neurogenesis. Neuron 57(1):41–55

    PubMed  CAS  Google Scholar 

  172. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T (2002) Identification of tissue-specific microRNAs from mouse. Curr Biol 12(9):735–739

    PubMed  CAS  Google Scholar 

  173. Bak M, Silahtaroglu A, Moller M, Christensen M, Rath MF, Skryabin B, Tommerup N, Kauppinen S (2008) MicroRNA expression in the adult mouse central nervous system. RNA 14(3):432–444

    PubMed  CAS  Google Scholar 

  174. Obernosterer G, Martinez J, Alenius M (2007) Locked nucleic acid-based in situ detection of microRNAs in mouse tissue sections. Nat Protoc 2(6):1508–1514

    PubMed  CAS  Google Scholar 

  175. Korpal M, Lee ES, Hu G, Kang Y (2008) The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem 283(22):14910–14914

    PubMed  CAS  Google Scholar 

  176. Akerblom M, Sachdeva R, Barde I, Verp S, Gentner B, Trono D, Jakobsson J (2012) MicroRNA-124 is a subventricular zone neuronal fate determinant. J Neurosci 32(26):8879–8889

    PubMed  Google Scholar 

  177. Pathania M, Torres-Reveron J, Yan L, Kimura T, Lin TV, Gordon V, Teng ZQ, Zhao X, Fulga TA, Van Vactor D, Bordey A (2012) miR-132 enhances dendritic morphogenesis, spine density, synaptic integration, and survival of newborn olfactory bulb neurons. PLoS One 7(5):e38174

    PubMed  CAS  Google Scholar 

  178. de Chevigny A, Core N, Follert P, Gaudin M, Barbry P, Beclin C, Cremer H (2012) miR-7a regulation of Pax6 controls spatial origin of forebrain dopaminergic neurons. Nat Neurosci 15(8):1120–1126

    PubMed  Google Scholar 

  179. Meola N, Gennarino VA, Banfi S (2009) microRNAs and genetic diseases. Pathogenetics 2(1):7

    PubMed  Google Scholar 

  180. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, Lagarde J, Veeravalli L, Ruan X, Ruan Y, Lassmann T, Carninci P, Brown JB, Lipovich L, Gonzalez JM, Thomas M, Davis CA, Shiekhattar R, Gingeras TR, Hubbard TJ, Notredame C, Harrow J, Guigo R (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22(9):1775–1789

    PubMed  CAS  Google Scholar 

  181. Morozova O, Hirst M, Marra MA (2009) Applications of new sequencing technologies for transcriptome analysis. Annu Rev Genomics Hum Genet 10:135–151

    PubMed  CAS  Google Scholar 

  182. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T (2001) Identification of novel genes coding for small expressed RNAs. Science 294(5543):853–858

    PubMed  CAS  Google Scholar 

  183. Hutvagner G, Zamore PD (2002) A microRNA in a multiple-turnover RNAi enzyme complex. Science 297(5589):2056–2060

    PubMed  CAS  Google Scholar 

  184. Kim VN (2006) Small RNAs just got bigger: piwi-interacting RNAs (piRNAs) in mammalian testes. Genes Dev 20(15):1993–1997

    PubMed  CAS  Google Scholar 

  185. Taft RJ, Glazov EA, Cloonan N, Simons C, Stephen S, Faulkner GJ, Lassmann T, Forrest AR, Grimmond SM, Schroder K, Irvine K, Arakawa T, Nakamura M, Kubosaki A, Hayashida K, Kawazu C, Murata M, Nishiyori H, Fukuda S, Kawai J, Daub CO, Hume DA, Suzuki H, Orlando V, Carninci P, Hayashizaki Y, Mattick JS (2009) Tiny RNAs associated with transcription start sites in animals. Nat Genet 41(5):572–578

    PubMed  CAS  Google Scholar 

  186. Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, Lai F, Zytnicki M, Notredame C, Huang Q, Guigo R, Shiekhattar R (2010) Long noncoding RNAs with enhancer-like function in human cells. Cell 143(1):46–58

    PubMed  CAS  Google Scholar 

  187. Kiss T (2002) Small nucleolar RNAs: an abundant group of noncoding RNAs with diverse cellular functions. Cell 109(2):145–148

    PubMed  CAS  Google Scholar 

  188. Seila AC, Calabrese JM, Levine SS, Yeo GW, Rahl PB, Flynn RA, Young RA, Sharp PA (2008) Divergent transcription from active promoters. Science 322(5909):1849–1851

    PubMed  CAS  Google Scholar 

  189. Calin GA, Liu CG, Ferracin M, Hyslop T, Spizzo R, Sevignani C, Fabbri M, Cimmino A, Lee EJ, Wojcik SE, 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 TD, Kipps TJ, Negrini M, Croce CM (2007) Ultraconserved regions encoding ncRNAs are altered in human leukemias and carcinomas. Cancer Cell 12(3):215–229

    PubMed  CAS  Google Scholar 

  190. Katayama S, Tomaru Y, Kasukawa T, Waki K, Nakanishi M, Nakamura M, Nishida H, Yap CC, Suzuki M, Kawai J, Suzuki H, Carninci P, Hayashizaki Y, Wells C, Frith M, Ravasi T, Pang KC, Hallinan J, Mattick J, Hume DA, Lipovich L, Batalov S, Engstrom PG, Mizuno Y, Faghihi MA, Sandelin A, Chalk AM, Mottagui-Tabar S, Liang Z, Lenhard B, Wahlestedt C (2005) Antisense transcription in the mammalian transcriptome. Science 309(5740):1564–1566

    PubMed  Google Scholar 

  191. Huarte M, Guttman M, Feldser D, Garber M, Koziol MJ, Kenzelmann-Broz D, Khalil AM, Zuk O, Amit I, Rabani M, Attardi LD, Regev A, Lander ES, Jacks T, Rinn JL (2010) A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142(3):409–419

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Work in our laboratories is supported by grants from the Spanish MINECO (BFU2010-16031), Comunidad Autonoma de Madrid (CAM, S2010/BMD-2315), Fundaluce, Fundación ONCE and CIBERER to P.B, from MAE/MOST Israel–Italy Joint Innovation Program to I.C. and from the Italian Telethon Foundation (TGM11SB2) to S.B.

Author information

Authors and Affiliations

  1. Telethon Institute of Genetics and Medicine, Via Pietro Castellino, 111, 80131, Naples, Italy

    Ivan Conte & Sandro Banfi

  2. Department of Biochemistry, Biophysics and General Pathology, Second University of Naples, Naples, Italy

    Sandro Banfi

  3. Centro de Biología Molecular ‘Severo Ochoa’, CSIC–UAM, c/Nicolas Cabrera 1, Cantoblanco, 28049, Madrid, Spain

    Paola Bovolenta

  4. CIBER de Enfermedades Raras, ISCIII, Madrid, Spain

    Paola Bovolenta

Authors
  1. Ivan Conte
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sandro Banfi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paola Bovolenta
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Ivan Conte, Sandro Banfi or Paola Bovolenta.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Conte, I., Banfi, S. & Bovolenta, P. Non-coding RNAs in the development of sensory organs and related diseases. Cell. Mol. Life Sci. 70, 4141–4155 (2013). https://doi.org/10.1007/s00018-013-1335-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-013-1335-z

Keywords

Search

Navigation