Skip to main content

Advertisement

Log in

Sensational MicroRNAs: Neurosensory Roles of the MicroRNA-183 Family

  • Review
  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNAs, miRs) are short noncoding RNAs that act to repress expression of proteins from target mRNA transcripts. miRNAs influence many cellular processes including stemness, proliferation, differentiation, maintenance, and survival, and miRNA mutations or misexpression are associated with a variety of disease states. The miR-183 family gene cluster including miR-183, miR-96, and miR-182 is highly conserved among vertebrate and invertebrate organisms, and the miRNAs are coordinately expressed with marked specificity in sensory neurons and sensory epithelial cells. The crucial functions of these miRNAs in normal cellular processes are not yet fully understood, but expectedly dependent upon the transcriptomes of specific cell types at different developmental stages or in various maintenance circumstances. This article provides an overview of evidence supporting roles for miR-183 family members in normal biology of the nervous system, including mechanoreception for auditory and vestibular function, electroreception, chemoreception, photoreception, circadian rhythms, sensory ganglia and pain, and memory formation.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

1KO:

miR-182 knockout

2KO:

miR-183/96 knockout

3KO:

miR-183/96/182 knockout

AC:

Anterior crista

ADCY6:

Adenylate cyclase VI

Atoh1:

Atonal bHLH transcription factor 1

BDNF:

Brain-derived neurotrophic factor

BKCa :

Potassium large conductance calcium-activated channel

CKO:

Conditional knockout

CLIC5:

Chloride intracellular channel 5

Ddx3x:

DEAD-box helicase 3 X-linked

DGCR8:

DiGeorge syndrome critical region 8

EPHB1:

Ephrin type-b receptor 1

FOXO3a:

Forkhead box O3

GFI1:

Growth factor independent 1

HC:

Horizontal crista

HEI-OC1:

The House Ear Institute Organ of Corti 1 mouse auditory cell line

HET:

Heterozygous

HIBI:

Hypoxic-ischemia brain injury

iMOP:

Immortalized multipotent otic progenitor cell line

Kb:

Kilobase

KO:

Knockout

KV1.6:

Potassium voltage-gated channel subfamily A member 6

LTMRs:

Low-threshold mechanoreceptors

mESC:

Mouse embryonic stem cells

miRNAs, miRs:

microRNAs

miR-183, miR-96, miR-182:

miR-183 family

MITF:

microphthalmia-associated transcription factor

NaV1.3:

Sodium voltage-gated channel alpha subunit 3

NIHL:

Noise-induced hearing loss

NRF1:

Nuclear respiratory factor 1

OC:

Organ of Corti

OLF1:

Olfactory neuron-specific transcription factor 1

PC:

Posterior crista

pre-miRNAs:

Precursor microRNAs

pri-miRNAs:

Primary microRNAs

RT-PCR:

Reverse transcription polymerase chain reaction

S:

Saccular macula

SCN:

Suprachiasmatic nucleus

Shox2:

Short stature homeobox 2

Taok1:

TAO kinase 1

TRBP:

Trans-activation response RNA-binding protein

SG:

Spiral ganglion

U:

Utricular macula

Ube2h:

Ubiquitin-conjugating enzyme E2 H

UTR:

Untranslated region

References

  1. Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P et al (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425(6956):415–419. https://doi.org/10.1038/nature01957

    Article  CAS  PubMed  Google Scholar 

  2. Ambros V (2004) The functions of animal microRNAs. Nature 431(7006):350–355. https://doi.org/10.1038/nature02871

    Article  CAS  Google Scholar 

  3. Meister G, Tuschl T (2004) Mechanisms of gene silencing by double-stranded RNA. Nature 431(7006):343–349. https://doi.org/10.1038/nature02873

    Article  CAS  PubMed  Google Scholar 

  4. Bushati N, Cohen SM (2007) microRNA functions. Annu Rev Cell Dev Biol 23:175–205. https://doi.org/10.1146/annurev.cellbio.23.090506.123406

    Article  CAS  PubMed  Google Scholar 

  5. Aboobaker AA, Tomancak P, Patel N, Rubin GM, Lai EC (2005) Drosophila microRNAs exhibit diverse spatial expression patterns during embryonic development. Proc Natl Acad Sci U S A 102(50):18017–18022. https://doi.org/10.1073/pnas.0508823102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. 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 U S A 103(39):14385–14389. https://doi.org/10.1073/pnas.0603529103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Kloosterman WP, Wienholds E, de Bruijn E, Kauppinen S, Plasterk RH (2006) In situ detection of miRNAs in animal embryos using LNA-modified oligonucleotide probes. Nat Methods 3(1):27–29. https://doi.org/10.1038/nmeth843

    Article  CAS  PubMed  Google Scholar 

  8. Wienholds E, Kloosterman WP, Miska E, Alvarez-Saavedra E, Berezikov E, de Bruijn E, Horvitz HR, Kauppinen S et al (2005) MicroRNA expression in zebrafish embryonic development. Science 309(5732):310–311. https://doi.org/10.1126/science.1114519

    Article  CAS  PubMed  Google Scholar 

  9. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP (2008) The impact of microRNAs on protein output. Nature 455(7209):64–71. https://doi.org/10.1038/nature07242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N (2008) Widespread changes in protein synthesis induced by microRNAs. Nature 455(7209):58–63. https://doi.org/10.1038/nature07228

    Article  CAS  PubMed  Google Scholar 

  11. Friedman RC, Farh KK, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19(1):92–105. https://doi.org/10.1101/gr.082701.108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS (2003) MicroRNA targets in Drosophila. Genome Biol 5(1):R1. https://doi.org/10.1186/gb-2003-5-1-r1

    Article  PubMed  PubMed Central  Google Scholar 

  13. Christensen M, Schratt GM (2009) microRNA involvement in developmental and functional aspects of the nervous system and in neurological diseases. Neurosci Lett 466(2):55–62. https://doi.org/10.1016/j.neulet.2009.04.043

    Article  CAS  PubMed  Google Scholar 

  14. Davis GM, Haas MA, Pocock R (2015) MicroRNAs: not “fine-tuners” but key regulators of neuronal development and function. Front Neurol 6:245. https://doi.org/10.3389/fneur.2015.00245

    Article  PubMed  PubMed Central  Google Scholar 

  15. Choi PS, Zakhary L, Choi WY, Caron S, Alvarez-Saavedra E, Miska EA, McManus M, Harfe B et al (2008) Members of the miRNA-200 family regulate olfactory neurogenesis. Neuron 57(1):41–55. https://doi.org/10.1016/j.neuron.2007.11.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. 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. https://doi.org/10.1016/j.ydbio.2009.01.037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. 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. https://doi.org/10.1002/dvdy.22591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Lugli G, Larson J, Martone ME, Jones Y, Smalheiser NR (2005) Dicer and eIF2c are enriched at postsynaptic densities in adult mouse brain and are modified by neuronal activity in a calpain-dependent manner. J Neurochem 94(4):896–905. https://doi.org/10.1111/j.1471-4159.2005.03224.x

    Article  CAS  PubMed  Google Scholar 

  19. Sim SE, Bakes J, Kaang BK (2014) Neuronal activity-dependent regulation of microRNAs. Mol Cell 37(7):511–517. https://doi.org/10.14348/molcells.2014.0132

    Article  CAS  Google Scholar 

  20. Micallef L, Rodgers P (2014) eulerAPE: drawing area-proportional 3-Venn diagrams using ellipses. PLoS One 9(7):e101717. https://doi.org/10.1371/journal.pone.0101717

    Article  PubMed  PubMed Central  Google Scholar 

  21. Agarwal V, Bell GW, Nam JW, Bartel DP (2015) Predicting effective microRNA target sites in mammalian mRNAs. Elife 4. https://doi.org/10.7554/eLife.05005

  22. Lewis MA, Quint E, Glazier AM, Fuchs H, De Angelis MH, Langford C, van Dongen S, Abreu-Goodger C et al (2009) An ENU-induced mutation of miR-96 associated with progressive hearing loss in mice. Nat Genet 41(5):614–618. https://doi.org/10.1038/ng.369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Mencia A, Modamio-Hoybjor S, Redshaw N, Morin M, Mayo-Merino F, Olavarrieta L, Aguirre LA, del Castillo I et al (2009) Mutations in the seed region of human miR-96 are responsible for nonsyndromic progressive hearing loss. Nat Genet 41(5):609–613. https://doi.org/10.1038/ng.355

    Article  CAS  PubMed  Google Scholar 

  24. Solda G, Robusto M, Primignani P, Castorina P, Benzoni E, Cesarani A, Ambrosetti U, Asselta R et al (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. https://doi.org/10.1093/hmg/ddr493

    Article  CAS  PubMed  Google Scholar 

  25. Dambal S, Shah M, Mihelich B, Nonn L (2015) The microRNA-183 cluster: the family that plays together stays together. Nucleic Acids Res 43(15):7173–7188. https://doi.org/10.1093/nar/gkv703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Pierce ML, Weston MD, Fritzsch B, Gabel HW, Ruvkun G, Soukup GA (2008) MicroRNA-183 family conservation and ciliated neurosensory organ expression. Evol Dev 10(1):106–113. https://doi.org/10.1111/j.1525-142X.2007.00217.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. 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. https://doi.org/10.1074/jbc.M700501200

    Article  CAS  PubMed  Google Scholar 

  28. 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. https://doi.org/10.1016/j.brainres.2006.07.006

    Article  CAS  PubMed  Google Scholar 

  29. Saini HK, Enright AJ, Griffiths-Jones S (2008) Annotation of mammalian primary microRNAs. BMC Genomics 9:564. https://doi.org/10.1186/1471-2164-9-564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Lumayag S, Haldin CE, Corbett NJ, Wahlin KJ, Cowan C, Turturro S, Larsen PE, Kovacs B et al (2013) Inactivation of the microRNA-183/96/182 cluster results in syndromic retinal degeneration. Proc Natl Acad Sci U S A 110(6):E507–E516. https://doi.org/10.1073/pnas.1212655110

    Article  PubMed  PubMed Central  Google Scholar 

  31. Friedman LM, Dror AA, Mor E, Tenne T, Toren G, Satoh T, Biesemeier DJ, Shomron N et al (2009) MicroRNAs are essential for development and function of inner ear hair cells in vertebrates. Proc Natl Acad Sci U S A 106(19):7915–7920. https://doi.org/10.1073/pnas.0812446106

    Article  PubMed  PubMed Central  Google Scholar 

  32. Li H, Kloosterman W, Fekete DM (2010) MicroRNA-183 family members regulate sensorineural fates in the inner ear. J Neurosci 30(9):3254–3263. https://doi.org/10.1523/JNEUROSCI.4948-09.2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. 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. https://doi.org/10.1016/j.gep.2009.01.003

    Article  CAS  PubMed  Google Scholar 

  34. 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. https://doi.org/10.1097/WNR.0b013e328338864b

    Article  CAS  PubMed  Google Scholar 

  35. Hilgers V, Bushati N, Cohen SM (2010) Drosophila microRNAs 263a/b confer robustness during development by protecting nascent sense organs from apoptosis. PLoS Biol 8(6):e1000396. https://doi.org/10.1371/journal.pbio.1000396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Geng R, Furness DN, Muraleedharan CK, Zhang J, Dabdoub A, Lin V, Xu S (2018) The microRNA-183/96/182 cluster is essential for stereociliary bundle formation and function of cochlear sensory hair cells. Sci Rep 8(1):18022. https://doi.org/10.1038/s41598-018-36894-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Weston MD, Tarang S, Pierce ML, Pyakurel U, Rocha-Sanchez SM, McGee J, Walsh EJ, Soukup GA (2018) A mouse model of miR-96, miR-182 and miR-183 misexpression implicates miRNAs in cochlear cell fate and homeostasis. Sci Rep 8(1):3569. https://doi.org/10.1038/s41598-018-21811-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Xiang L, Chen XJ, Wu KC, Zhang CJ, Zhou GH, Lv JN, Sun LF, Cheng FF et al (2017) miR-183/96 plays a pivotal regulatory role in mouse photoreceptor maturation and maintenance. Proc Natl Acad Sci U S A 114(24):6376–6381. https://doi.org/10.1073/pnas.1618757114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Fan J, Jia L, Li Y, Ebrahim S, May-Simera H, Wood A, Morell RJ, Liu P et al (2017) Maturation arrest in early postnatal sensory receptors by deletion of the miR-183/96/182 cluster in mouse. Proc Natl Acad Sci U S A 114(21):E4271–E4280. https://doi.org/10.1073/pnas.1619442114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Kuhn S, Johnson SL, Furness DN, Chen J, Ingham N, Hilton JM, Steffes G, Lewis MA et al (2011) miR-96 regulates the progression of differentiation in mammalian cochlear inner and outer hair cells. Proc Natl Acad Sci U S A 108(6):2355–2360. https://doi.org/10.1073/pnas.1016646108

    Article  PubMed  PubMed Central  Google Scholar 

  41. Mendell JT, Olson EN (2012) MicroRNAs in stress signaling and human disease. Cell 148(6):1172–1187. https://doi.org/10.1016/j.cell.2012.02.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Schluter T, Berger C, Rosengauer E, Fieth P, Krohs C, Ushakov K, Steel KP, Avraham KB et al (2018) miR-96 is required for normal development of the auditory hindbrain. Hum Mol Genet 27(5):860–874. https://doi.org/10.1093/hmg/ddy007

    Article  CAS  PubMed  Google Scholar 

  43. Lewis MA, Buniello A, Hilton JM, Zhu F, Zhang WI, Evans S, van Dongen S, Enright AJ et al (2016) Exploring regulatory networks of miR-96 in the developing inner ear. Sci Rep 6:23363. https://doi.org/10.1038/srep23363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Zhang KD, Stoller ML, Fekete DM (2015) Expression and Misexpression of the miR-183 family in the developing hearing organ of the chicken. PLoS One 10(7):e0132796. https://doi.org/10.1371/journal.pone.0132796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Ebeid M, Sripal P, Pecka J, Beisel KW, Kwan K, Soukup GA (2017) Transcriptome-wide comparison of the impact of Atoh1 and miR-183 family on pluripotent stem cells and multipotent otic progenitor cells. PLoS One 12(7):e0180855. https://doi.org/10.1371/journal.pone.0180855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Fritzsch B, Matei VA, Nichols DH, Bermingham N, Jones K, Beisel KW, Wang VY (2005) Atoh1 null mice show directed afferent fiber growth to undifferentiated ear sensory epithelia followed by incomplete fiber retention. Dev Dyn 233(2):570–583. https://doi.org/10.1002/dvdy.20370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Matei V, Pauley S, Kaing S, Rowitch D, Beisel KW, Morris K, Feng F, Jones K et al (2005) Smaller inner ear sensory epithelia in Neurog 1 null mice are related to earlier hair cell cycle exit. Dev Dyn 234(3):633–650. https://doi.org/10.1002/dvdy.20551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Zhang Z, Liu K, Chen Y, Li Z, Yan N, Zhang J (2014) The expression of miR-183 family in the pathogenesis and development of noise-induced deafness. Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 28(7):468–472

    CAS  PubMed  Google Scholar 

  49. Patel M, Cai Q, Ding D, Salvi R, Hu Z, Hu BH (2013) The miR-183/Taok1 target pair is implicated in cochlear responses to acoustic trauma. PLoS One 8(3):e58471. https://doi.org/10.1371/journal.pone.0058471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. 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. https://doi.org/10.1016/j.tiv.2012.07.008

    Article  CAS  PubMed  Google Scholar 

  51. Kim CW, Han JH, Wu L, Choi JY (2018) microRNA-183 is essential for hair cell regeneration after neomycin injury in zebrafish. Yonsei Med J 59(1):141–147. https://doi.org/10.3349/ymj.2018.59.1.141

    Article  CAS  PubMed  Google Scholar 

  52. Zhou W, Du J, Jiang D, Wang X, Chen K, Tang H, Zhang X, Cao H et al (2018) microRNA183 is involved in the differentiation and regeneration of Notch signalingprohibited hair cells from mouse cochlea. Mol Med Rep 18(2):1253–1262. https://doi.org/10.3892/mmr.2018.9127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Li Y, Li A, Wu J, He Y, Yu H, Chai R, Li H (2016) MiR-182-5p protects inner ear hair cells from cisplatin-induced apoptosis by inhibiting FOXO3a. Cell Death Dis 7(9):e2362. https://doi.org/10.1038/cddis.2016.246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Bell CC (1979) Central nervous system physiology of electroreception, a review. J Physiol Paris 75(4):361–379

    CAS  PubMed  Google Scholar 

  55. 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. https://doi.org/10.1261/rna.783108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Mackay-Sim A, Kittel PW (1991) On the life span of olfactory receptor neurons. Eur J Neurosci 3(3):209–215

    Article  Google Scholar 

  57. Hamamichi R, Asano-Miyoshi M, Emori Y (2006) Taste bud contains both short-lived and long-lived cell populations. Neuroscience 141(4):2129–2138. https://doi.org/10.1016/j.neuroscience.2006.05.061

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Krol J, Busskamp V, Markiewicz I, Stadler MB, Ribi S, Richter J, Duebel J, Bicker S et al (2010) Characterizing light-regulated retinal microRNAs reveals rapid turnover as a common property of neuronal microRNAs. Cell 141(4):618–631. https://doi.org/10.1016/j.cell.2010.03.039

    Article  CAS  PubMed  Google Scholar 

  60. 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. https://doi.org/10.1186/gb-2007-8-11-r248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. 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. https://doi.org/10.1016/j.exer.2008.08.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Gessert S, Bugner V, Tecza A, Pinker M, Kuhl M (2010) FMR1/FXR1 and the miRNA pathway are required for eye and neural crest development. Dev Biol 341(1):222–235. https://doi.org/10.1016/j.ydbio.2010.02.031

    Article  CAS  PubMed  Google Scholar 

  63. Soukup GA (2009) Little but loud: small RNAs have a resounding affect on ear development. Brain Res 1277:104–114. https://doi.org/10.1016/j.brainres.2009.02.027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. 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. https://doi.org/10.1074/jbc.M111.259028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Busskamp V, Krol J, Nelidova D, Daum J, Szikra T, Tsuda B, Juttner J, Farrow K et al (2014) miRNAs 182 and 183 are necessary to maintain adult cone photoreceptor outer segments and visual function. Neuron 83(3):586–600. https://doi.org/10.1016/j.neuron.2014.06.020

    Article  CAS  PubMed  Google Scholar 

  66. Sundermeier TR, Palczewski K (2016) The impact of microRNA gene regulation on the survival and function of mature cell types in the eye. FASEB J 30(1):23–33. https://doi.org/10.1096/fj.15-279745

    Article  CAS  PubMed  Google Scholar 

  67. Reppert SM, Weaver DR (2001) Molecular analysis of mammalian circadian rhythms. Annu Rev Physiol 63:647–676. https://doi.org/10.1146/annurev.physiol.63.1.647

    Article  CAS  PubMed  Google Scholar 

  68. Ben-Moshe Z, Alon S, Mracek P, Faigenbloom L, Tovin A, Vatine GD, Eisenberg E, Foulkes NS et al (2014) The light-induced transcriptome of the zebrafish pineal gland reveals complex regulation of the circadian clockwork by light. Nucleic Acids Res 42(6):3750–3767. https://doi.org/10.1093/nar/gkt1359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Clokie SJ, Lau P, Kim HH, Coon SL, Klein DC (2012) MicroRNAs in the pineal gland: miR-483 regulates melatonin synthesis by targeting arylalkylamine N-acetyltransferase. J Biol Chem 287(30):25312–25324. https://doi.org/10.1074/jbc.M112.356733

    Article  PubMed  PubMed Central  Google Scholar 

  70. Ding X, Sun B, Huang J, Xu L, Pan J, Fang C, Tao Y, Hu S et al (2015) The role of miR-182 in regulating pineal CLOCK expression after hypoxia-ischemia brain injury in neonatal rats. Neurosci Lett 591:75–80. https://doi.org/10.1016/j.neulet.2015.02.026

    Article  CAS  PubMed  Google Scholar 

  71. Yang M, Lee JE, Padgett RW, Edery I (2008) Circadian regulation of a limited set of conserved microRNAs in Drosophila. BMC Genomics 9:83. https://doi.org/10.1186/1471-2164-9-83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Saus E, Soria V, Escaramis G, Vivarelli F, Crespo JM, Kagerbauer B, Menchon JM, Urretavizcaya M et al (2010) Genetic variants and abnormal processing of pre-miR-182, a circadian clock modulator, in major depression patients with late insomnia. Hum Mol Genet 19(20):4017–4025. https://doi.org/10.1093/hmg/ddq316

    Article  CAS  PubMed  Google Scholar 

  73. Darnell DK, Kaur S, Stanislaw S, Konieczka JH, Yatskievych TA, Antin PB (2006) MicroRNA expression during chick embryo development. Dev Dyn 235(11):3156–3165. https://doi.org/10.1002/dvdy.20956

    Article  CAS  PubMed  Google Scholar 

  74. Aldrich BT, Frakes EP, Kasuya J, Hammond DL, Kitamoto T (2009) Changes in expression of sensory organ-specific microRNAs in rat dorsal root ganglia in association with mechanical hypersensitivity induced by spinal nerve ligation. Neuroscience 164(2):711–723. https://doi.org/10.1016/j.neuroscience.2009.08.033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Murchison EP, Kheradpour P, Sachidanandam R, Smith C, Hodges E, Xuan Z, Kellis M, Grutzner F et al (2008) Conservation of small RNA pathways in platypus. Genome Res 18(6):995–1004. https://doi.org/10.1101/gr.073056.107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Peng C, Li L, Zhang MD, Bengtsson Gonzales C, Parisien M, Belfer I, Usoskin D, Abdo H et al (2017) miR-183 cluster scales mechanical pain sensitivity by regulating basal and neuropathic pain genes. Science 356(6343):1168–1171. https://doi.org/10.1126/science.aam7671

    Article  CAS  PubMed  Google Scholar 

  77. Lin CR, Chen KH, Yang CH, Huang HW, Sheen-Chen SM (2014) Intrathecal miR-183 delivery suppresses mechanical allodynia in mononeuropathic rats. Eur J Neurosci 39(10):1682–1689. https://doi.org/10.1111/ejn.12522

    Article  PubMed  Google Scholar 

  78. Cai W, Zhao Q, Shao J, Zhang J, Li L, Ren X, Su S, Bai Q et al (2018) MicroRNA-182 alleviates neuropathic pain by regulating Nav1.7 following spared nerve injury in rats. Sci Rep 8(1):16750. https://doi.org/10.1038/s41598-018-34755-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Zhou X, Zhang C, Zhang C, Peng Y, Wang Y, Xu H (2017) MicroRNA-182-5p regulates nerve injury-induced nociceptive hypersensitivity by targeting ephrin type-b receptor 1. Anesthesiology 126(5):967–977. https://doi.org/10.1097/ALN.0000000000001588

    Article  CAS  PubMed  Google Scholar 

  80. Peng C, Furlan A, Zhang MD, Su J, Lubke M, Lonnerberg P, Abdo H, Sontheimer J et al (2018) Termination of cell-type specification gene programs by the miR-183 cluster determines the population sizes of low-threshold mechanosensitive neurons. Development 145(18). https://doi.org/10.1242/dev.165613

    Article  Google Scholar 

  81. Davis HP, Squire LR (1984) Protein synthesis and memory: a review. Psychol Bull 96(3):518–559

    Article  CAS  Google Scholar 

  82. Sutton MA, Schuman EM (2006) Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127(1):49–58. https://doi.org/10.1016/j.cell.2006.09.014

    Article  CAS  PubMed  Google Scholar 

  83. Ashraf SI, Kunes S (2006) A trace of silence: memory and microRNA at the synapse. Curr Opin Neurobiol 16(5):535–539. https://doi.org/10.1016/j.conb.2006.08.007

    Article  CAS  PubMed  Google Scholar 

  84. Griggs EM, Young EJ, Rumbaugh G, Miller CA (2013) MicroRNA-182 regulates amygdala-dependent memory formation. J Neurosci 33(4):1734–1740. https://doi.org/10.1523/JNEUROSCI.2873-12.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Woldemichael BT, Jawaid A, Kremer EA, Gaur N, Krol J, Marchais A, Mansuy IM (2016) The microRNA cluster miR-183/96/182 contributes to long-term memory in a protein phosphatase 1-dependent manner. Nat Commun 7:12594. https://doi.org/10.1038/ncomms12594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Jawaid A, Woldemichael BT, Kremer EA, Laferriere F, Gaur N, Afroz T, Polymenidou M, Mansuy IM (2018) Memory decline and its reversal in aging and neurodegeneration involve miR-183/96/182 biogenesis. Mol Neurobiol. https://doi.org/10.1007/s12035-018-1314-3

    Article  Google Scholar 

  87. Lippi G, Steinert JR, Marczylo EL, D'Oro S, Fiore R, Forsythe ID, Schratt G, Zoli M et al (2011) Targeting of the Arpc3 actin nucleation factor by miR-29a/b regulates dendritic spine morphology. J Cell Biol 194(6):889–904. https://doi.org/10.1083/jcb.201103006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Zhang QH, Sun HM, Zheng RZ, Li YC, Zhang Q, Cheng P, Tang ZH, Huang F (2013) Meta-analysis of microRNA-183 family expression in human cancer studies comparing cancer tissues with noncancerous tissues. Gene 527(1):26–32. https://doi.org/10.1016/j.gene.2013.06.006

    Article  CAS  PubMed  Google Scholar 

  89. Cai T, Jen HI, Kang H, Klisch TJ, Zoghbi HY, Groves AK (2015) Characterization of the transcriptome of nascent hair cells and identification of direct targets of the Atoh1 transcription factor. J Neurosci 35(14):5870–5883. https://doi.org/10.1523/JNEUROSCI.5083-14.2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Liu H, Pecka JL, Zhang Q, Soukup GA, Beisel KW, He DZ (2014) Characterization of transcriptomes of cochlear inner and outer hair cells. J Neurosci 34(33):11085–11095. https://doi.org/10.1523/JNEUROSCI.1690-14.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. da Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44–57. https://doi.org/10.1038/nprot.2008.211

    Article  CAS  Google Scholar 

  92. Chen D, Li SG, Chen JY, Xiao M (2018) MiR-183 maintains canonical Wnt signaling activity and regulates growth and apoptosis in bladder cancer via targeting AXIN2. Eur Rev Med Pharmacol Sci 22(15):4828–4836. https://doi.org/10.26355/eurrev_201808_15618

    Article  CAS  PubMed  Google Scholar 

  93. Chen G, Yu W, Li Z, Wang Q, Yang Q, Du Z, Zhang G, Song Y (2019) Potential regulatory effects of miR-182-3p in osteosarcoma via targeting EBF2. Biomed Res Int 2019:4897905. https://doi.org/10.1155/2019/4897905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Chen HP, Zhou W, Kang LM, Yan H, Zhang L, Xu BH, Cai WH (2014) Intrathecal miR-96 inhibits Nav1.3 expression and alleviates neuropathic pain in rat following chronic construction injury. Neurochem Res 39(1):76–83. https://doi.org/10.1007/s11064-013-1192-z

    Article  CAS  PubMed  Google Scholar 

  95. Iwai N, Yasui K, Tomie A, Gen Y, Terasaki K, Kitaichi T, Soda T, Yamada N et al (2018) Oncogenic miR-96-5p inhibits apoptosis by targeting the caspase-9 gene in hepatocellular carcinoma. Int J Oncol 53(1):237–245. https://doi.org/10.3892/ijo.2018.4369

    Article  CAS  PubMed  Google Scholar 

  96. Jia L, Luo S, Ren X, Li Y, Hu J, Liu B, Zhao L, Shan Y et al (2017) miR-182 and miR-135b mediate the tumorigenesis and invasiveness of colorectal cancer cells via targeting ST6GALNAC2 and PI3K/AKT pathway. Dig Dis Sci 62(12):3447–3459. https://doi.org/10.1007/s10620-017-4755-z

    Article  CAS  PubMed  Google Scholar 

  97. Li Y, Zhang H, Li Y, Zhao C, Fan Y, Liu J, Li X, Liu H et al (2018) MiR-182 inhibits the epithelial to mesenchymal transition and metastasis of lung cancer cells by targeting the Met gene. Mol Carcinog 57(1):125–136. https://doi.org/10.1002/mc.22741

    Article  CAS  PubMed  Google Scholar 

  98. Li Y, Chen S, Shan Z, Bi L, Yu S, Li Y, Xu S (2017) miR-182-5p improves the viability, mitosis, migration, and invasion ability of human gastric cancer cells by down-regulating RAB27A. Biosci Rep 37(3). https://doi.org/10.1042/BSR20170136

  99. Li Y, Li S, Yan J, Wang D, Yin R, Zhao L, Zhu Y, Zhu X (2016) miR-182 (microRNA-182) suppression in the hippocampus evokes antidepressant-like effects in rats. Prog Neuro-Psychopharmacol Biol Psychiatry 65:96–103. https://doi.org/10.1016/j.pnpbp.2015.09.004

    Article  CAS  Google Scholar 

  100. Long MD, Singh PK, Russell JR, Llimos G, Rosario S, Rizvi A, van den Berg PR, Kirk J et al (2019) The miR-96 and RARgamma signaling axis governs androgen signaling and prostate cancer progression. Oncogene 38(3):421–444. https://doi.org/10.1038/s41388-018-0450-6

    Article  CAS  PubMed  Google Scholar 

  101. Moazzeni H, Najafi A, Khani M (2017) Identification of direct target genes of miR-7, miR-9, miR-96, and miR-182 in the human breast cancer cell lines MCF-7 and MDA-MB-231. Mol Cell Probes 34:45–52. https://doi.org/10.1016/j.mcp.2017.05.005

    Article  CAS  PubMed  Google Scholar 

  102. Muraleedharan CK, McClellan SA, Ekanayaka SA, Francis R, Zmejkoski A, Hazlett LD, Xu S (2019) The miR-183/96/182 cluster regulates macrophage functions in response to Pseudomonas aeruginosa. J Innate Immun 1–12. https://doi.org/10.1159/000495472

  103. Shi DN, Yuan YT, Ye D, Kang LM, Wen J, Chen HP (2018) MiR-183-5p alleviates chronic constriction injury-induced neuropathic pain through inhibition of TREK-1. Neurochem Res 43(6):1143–1149. https://doi.org/10.1007/s11064-018-2529-4

    Article  CAS  PubMed  Google Scholar 

  104. Zhang L, Liu X, Liu J, Zhou Z, Song Y, Cao B, An X (2017) miR-182 aids in receptive endometrium development in dairy goats by down-regulating PTN expression. PLoS One 12(7):e0179783. https://doi.org/10.1371/journal.pone.0179783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Zhang S, Zhang Q, Shi G, Yin J (2018) MiR-182-5p regulates BCL2L12 and BCL2 expression in acute myeloid leukemia as a potential therapeutic target. Biomed Pharmacother 97:1189–1194. https://doi.org/10.1016/j.biopha.2017.11.002

    Article  CAS  PubMed  Google Scholar 

  106. Zhang Z, Jiang W, Yang H, Lin Q, Qin X (2018) The miR-182/SORT1 axis regulates vascular smooth muscle cell calcification in vitro and in vivo. Exp Cell Res 362(2):324–331. https://doi.org/10.1016/j.yexcr.2017.11.033

    Article  CAS  PubMed  Google Scholar 

  107. Yu J, Tian X, Chang J, Liu P, Zhang R (2017) RUNX3 inhibits the proliferation and metastasis of gastric cancer through regulating miR-182/HOXA9. Biomed Pharmacother 96:782–791. https://doi.org/10.1016/j.biopha.2017.08.144

    Article  CAS  PubMed  Google Scholar 

  108. Xu T, Du XW, Hu JB, Zhu YF, Wu HL, Dai GP, Shu YM, Ouyang J (2018) Anticancer effect of miR-96 inhibitor in bladder cancer cell lines. Oncol Lett 15(3):3814–3819. https://doi.org/10.3892/ol.2018.7745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Xue J, Zhou A, Wu Y, Morris SA, Lin K, Amin S, Verhaak R, Fuller G et al (2016) miR-182-5p Induced by STAT3 Activation Promotes Glioma Tumorigenesis. Cancer Res 76(14):4293–4304. https://doi.org/10.1158/0008-5472.CAN-15-3073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Wang G, Wang S, Li C (2017) MiR-183 overexpression inhibits tumorigenesis and enhances DDP-induced cytotoxicity by targeting MTA1 in nasopharyngeal carcinoma. Tumour Biol 39(6):1010428317703825. https://doi.org/10.1177/1010428317703825

    Article  CAS  PubMed  Google Scholar 

  111. Wang M, Wang W, Wang J, Zhang J (2018) MiR-182 promotes glucose metabolism by upregulating hypoxia-inducible factor 1alpha in NSCLC cells. Biochem Biophys Res Commun 504(2):400–405. https://doi.org/10.1016/j.bbrc.2018.06.035

    Article  CAS  PubMed  Google Scholar 

  112. Van den Ackerveken P, Mounier A, Huyghe A, Sacheli R, Vanlerberghe PB, Volvert ML, Delacroix L, Nguyen L et al (2017) The miR-183/ItgA3 axis is a key regulator of prosensory area during early inner ear development. Cell Death Differ 24(12):2054–2065. https://doi.org/10.1038/cdd.2017.127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Vahabi M, Pulito C, Sacconi A, Donzelli S, D'Andrea M, Manciocco V, Pellini R, Paci P et al (2019) miR-96-5p targets PTEN expression affecting radio-chemosensitivity of HNSCC cells. J Exp Clin Cancer Res 38(1):141. https://doi.org/10.1186/s13046-019-1119-x

    Article  PubMed  PubMed Central  Google Scholar 

  114. Sun L, Bai Y, Zhao R, Sun T, Cao R, Wang F, He G, Zhang W et al (2016) Oncological miR-182-3p, a novel smooth muscle cell phenotype modulator, evidences from model rats and patients. Arterioscler Thromb Vasc Biol 36(7):1386–1397. https://doi.org/10.1161/ATVBAHA.115.307412

    Article  CAS  PubMed  Google Scholar 

  115. Goeppert B, Schmezer P, Dutruel C, Oakes C, Renner M, Breinig M, Warth A, Vogel MN et al (2010) Down-regulation of tumor suppressor A kinase anchor protein 12 in human hepatocarcinogenesis by epigenetic mechanisms. Hepatology 52(6):2023–2033. https://doi.org/10.1002/hep.23939

    Article  CAS  PubMed  Google Scholar 

  116. Vishwamitra D, Li Y, Wilson D, Manshouri R, Curry CV, Shi B, Tang XM, Sheehan AM et al (2012) MicroRNA 96 is a post-transcriptional suppressor of anaplastic lymphoma kinase expression. Am J Pathol 180(5):1772–1780. https://doi.org/10.1016/j.ajpath.2012.01.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Krishnan K, Steptoe AL, Martin HC, Wani S, Nones K, Waddell N, Mariasegaram M, Simpson PT et al (2013) MicroRNA-182-5p targets a network of genes involved in DNA repair. RNA 19(2):230–242. https://doi.org/10.1261/rna.034926.112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A, Waldvogel B, Vannier C et al (2009) The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 11(12):1487–1495. https://doi.org/10.1038/ncb1998

    Article  CAS  Google Scholar 

  119. Moskwa P, Buffa FM, Pan Y, Panchakshari R, Gottipati P, Muschel RJ, Beech J, Kulshrestha R et al (2011) miR-182-mediated downregulation of BRCA1 impacts DNA repair and sensitivity to PARP inhibitors. Mol Cell 41(2):210–220. https://doi.org/10.1016/j.molcel.2010.12.005

    Article  CAS  PubMed  Google Scholar 

  120. Wang J, Wang X, Li Z, Liu H, Teng Y (2014) MicroRNA-183 suppresses retinoblastoma cell growth, invasion and migration by targeting LRP6. FEBS J 281(5):1355–1365. https://doi.org/10.1111/febs.12659

    Article  CAS  PubMed  Google Scholar 

  121. Ueno K, Hirata H, Shahryari V, Deng G, Tanaka Y, Tabatabai ZL, Hinoda Y, Dahiya R (2013) microRNA-183 is an oncogene targeting Dkk-3 and SMAD4 in prostate cancer. Br J Cancer 108(8):1659–1667. https://doi.org/10.1038/bjc.2013.125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Sarver AL, Li L, Subramanian S (2010) MicroRNA miR-183 functions as an oncogene by targeting the transcription factor EGR1 and promoting tumor cell migration. Cancer Res 70(23):9570–9580. https://doi.org/10.1158/0008-5472.CAN-10-2074

    Article  CAS  PubMed  Google Scholar 

  123. Pizzini S, Bisognin A, Mandruzzato S, Biasiolo M, Facciolli A, Perilli L, Rossi E, Esposito G et al (2013) Impact of microRNAs on regulatory networks and pathways in human colorectal carcinogenesis and development of metastasis. BMC Genomics 14:589. https://doi.org/10.1186/1471-2164-14-589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Wang G, Mao W, Zheng S (2008) MicroRNA-183 regulates Ezrin expression in lung cancer cells. FEBS Lett 582(25-26):3663–3668. https://doi.org/10.1016/j.febslet.2008.09.051

    Article  CAS  PubMed  Google Scholar 

  125. Mu Y, Zhang H, Che L, Li K (2014) Clinical significance of microRNA-183/Ezrin axis in judging the prognosis of patients with osteosarcoma. Med Oncol 31(2):821. https://doi.org/10.1007/s12032-013-0821-3

    Article  CAS  PubMed  Google Scholar 

  126. Jalvy-Delvaille S, Maurel M, Majo V, Pierre N, Chabas S, Combe C, Rosenbaum J, Sagliocco F et al (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. https://doi.org/10.1093/nar/gkr843

    Article  CAS  PubMed  Google Scholar 

  127. Hirata H, Ueno K, Shahryari V, Deng G, Tanaka Y, Tabatabai ZL, Hinoda Y, Dahiya R (2013) MicroRNA-182-5p promotes cell invasion and proliferation by down regulating FOXF2, RECK and MTSS1 genes in human prostate cancer. PLoS One 8(1):e55502. https://doi.org/10.1371/journal.pone.0055502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Guttilla IK, White BA (2009) Coordinate regulation of FOXO1 by miR-27a, miR-96, and miR-182 in breast cancer cells. J Biol Chem 284(35):23204–23216. https://doi.org/10.1074/jbc.M109.031427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Fendler A, Jung M, Stephan C, Erbersdobler A, Jung K, Yousef GM (2013) The antiapoptotic function of miR-96 in prostate cancer by inhibition of FOXO1. PLoS One 8(11):e80807. https://doi.org/10.1371/journal.pone.0080807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Segura MF, Hanniford D, Menendez S, Reavie L, Zou X, Alvarez-Diaz S, Zakrzewski J, Blochin E et al (2009) Aberrant miR-182 expression promotes melanoma metastasis by repressing FOXO3 and microphthalmia-associated transcription factor. Proc Natl Acad Sci U S A 106(6):1814–1819. https://doi.org/10.1073/pnas.0808263106

    Article  PubMed  PubMed Central  Google Scholar 

  131. Jensen KP, Covault J (2011) Human miR-1271 is a miR-96 paralog with distinct non-conserved brain expression pattern. Nucleic Acids Res 39(2):701–711. https://doi.org/10.1093/nar/gkq798

    Article  CAS  PubMed  Google Scholar 

  132. Xu J, Wong C (2008) A computational screen for mouse signaling pathways targeted by microRNA clusters. RNA 14(7):1276–1283. https://doi.org/10.1261/rna.997708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Li G, Luna C, Qiu J, Epstein DL, Gonzalez P (2010) Targeting of integrin beta1 and kinesin 2alpha by microRNA 183. J Biol Chem 285(8):5461–5471. https://doi.org/10.1074/jbc.M109.037127

    Article  CAS  PubMed  Google Scholar 

  134. Li XL, Hara T, Choi Y, Subramanian M, Francis P, Bilke S, Walker RL, Pineda M et al (2014) A p21-ZEB1 complex inhibits epithelial-mesenchymal transition through the microRNA 183-96-182 cluster. Mol Cell Biol 34(3):533–550. https://doi.org/10.1128/MCB.01043-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Yu S, Lu Z, Liu C, Meng Y, Ma Y, Zhao W, Liu J, Yu J et al (2010) miRNA-96 suppresses KRAS and functions as a tumor suppressor gene in pancreatic cancer. Cancer Res 70(14):6015–6025. https://doi.org/10.1158/0008-5472.CAN-09-4531

    Article  CAS  PubMed  Google Scholar 

  136. Chen J, Johnson SL, Lewis MA, Hilton JM, Huma A, Marcotti W, Steel KP (2014) A reduction in Ptprq associated with specific features of the deafness phenotype of the miR-96 mutant mouse diminuendo. Eur J Neurosci 39(5):744–756. https://doi.org/10.1111/ejn.12484

    Article  PubMed  PubMed Central  Google Scholar 

  137. Tang H, Wang Z, Liu Q, Liu X, Wu M, Li G (2014) Disturbing miR-182 and -381 inhibits BRD7 transcription and glioma growth by directly targeting LRRC4. PLoS One 9(1):e84146. https://doi.org/10.1371/journal.pone.0084146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Liu R, Li J, Teng Z, Zhang Z, Xu Y (2013) Overexpressed microRNA-182 promotes proliferation and invasion in prostate cancer PC-3 cells by down-regulating N-myc downstream regulated gene 1 (NDRG1). PLoS One 8(7):e68982. https://doi.org/10.1371/journal.pone.0068982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Du ZW, Ma LX, Phillips C, Zhang SC (2013) miR-200 and miR-96 families repress neural induction from human embryonic stem cells. Development 140(12):2611–2618. https://doi.org/10.1242/dev.092809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Li J, Fu H, Xu C, Tie Y, Xing R, Zhu J, Qin Y, Sun Z et al (2010) miR-183 inhibits TGF-beta1-induced apoptosis by downregulation of PDCD4 expression in human hepatocellular carcinoma cells. BMC Cancer 10:354. https://doi.org/10.1186/1471-2407-10-354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Pal S, Baiocchi RA, Byrd JC, Grever MR, Jacob ST, Sif S (2007) Low levels of miR-92b/96 induce PRMT5 translation and H3R8/H4R3 methylation in mantle cell lymphoma. EMBO J 26(15):3558–3569. https://doi.org/10.1038/sj.emboj.7601794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Sun Y, Fang R, Li C, Li L, Li F, Ye X, Chen H (2010) Hsa-mir-182 suppresses lung tumorigenesis through down regulation of RGS17 expression in vitro. Biochem Biophys Res Commun 396(2):501–507. https://doi.org/10.1016/j.bbrc.2010.04.127

    Article  CAS  PubMed  Google Scholar 

  143. Kondkar AA, Bray MS, Leal SM, Nagalla S, Liu DJ, Jin Y, Dong JF, Ren Q et al (2010) VAMP8/endobrevin is overexpressed in hyperreactive human platelets: suggested role for platelet microRNA. J Thromb Haemost 8(2):369–378. https://doi.org/10.1111/j.1538-7836.2009.03700.x

    Article  CAS  PubMed  Google Scholar 

  144. Oba S, Mizutani T, Suzuki E, Nishimatsu H, Takahashi M, Ogawa Y, Kimura K, Hirata Y et al (2013) A useful method of identifying of miRNAs which can down-regulate Zeb-2. BMC Res Notes 6:470. https://doi.org/10.1186/1756-0500-6-470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Prosser HM, Koike-Yusa H, Cooper JD, Law FC, Bradley A (2011) A resource of vectors and ES cells for targeted deletion of microRNAs in mice. Nat Biotechnol 29(9):840–845. https://doi.org/10.1038/nbt.1929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Garrett A. Soukup.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Banks, S.A., Pierce, M.L. & Soukup, G.A. Sensational MicroRNAs: Neurosensory Roles of the MicroRNA-183 Family. Mol Neurobiol 57, 358–371 (2020). https://doi.org/10.1007/s12035-019-01717-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12035-019-01717-3

Keywords

Navigation