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Memory Decline and Its Reversal in Aging and Neurodegeneration Involve miR-183/96/182 Biogenesis

Jawaid, Ali, Woldemichael, Bisrat T., Kremer, Eloïse A., Laferriere, Florent, Gaur, Niharika, Afroz, Tariq, Polymenidou, Magdalini, Mansuy, Isabelle M.·2019·Molecular Neurobiology
DOI 10.1007/s12035-018-1314-3
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Abstract

Aging is characterized by progressive memory decline that can lead to dementia when associated with neurodegeneration. Here, we show in mice that aging-related memory decline involves defective biogenesis of microRNAs (miRNAs), in particular miR-183/96/182 cluster, resulting from increased protein phosphatase 1 (PP1) and altered receptor SMAD (R-SMAD) signaling. Correction of the defect by miR-183/96/182 overexpression in hippocampus or by environmental enrichment that normalizes PP1 activity restores memory in aged animals. Regulation of miR-183/96/182 biogenesis is shown to involve the neurodegeneration-related RNA-binding proteins TDP-43 and FUS. Similar alterations in miR-183/96/182, PP1, and R-SMADs are observed in the brains of patients with amyotrophic lateral sclerosis (ALS) or frontotemporal lobar degeneration (FTLD), two neurodegenerative diseases with pathological aggregation of TDP-43. Overall, these results identify new mechanistic links between miR-183/96/182, PP1, TDP-43, and FUS in age-related memory deficits and their reversal.

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Research works printed but not linked: 38

  1. Blahna MT, Hata A (2012) Smad-mediated regulation of microRNA biosynthesis. FEBS Lett 586:1906–1912 · DOI
  2. Bilan V, Allegra D, Kuchenbauer F, Mertens D (2014) In vivo processing assay based on a dual-luciferase reporter system to evaluate DROSHA enzymatic activity. Methods Mol Biol 1095:87–93 · DOI
  3. Capitano F, Camon J, Licursi V, Ferretti V, Maggi L, Scianni M, del Vecchio G, Rinaldi A et al (2017) MicroRNA-335-5p modulates spatial memory and hippocampal synaptic plasticity. Neurobiol Learn Mem 139:63–68 · DOI
  4. Dannhauser TM, Cleverley M, Whitfield TJ, Fletcher B, Stevens T, Walker Z (2014) A complex multimodal activity intervention to reduce the risk of dementia in mild cognitive impairment--ThinkingFit: pilot and feasibility study for a randomized controlled trial. BMC Psychiatry 14:129 · DOI
  5. Davis BN, Hilyard AC, Lagna G, Hata A (2008) SMAD proteins control DROSHA-mediated microRNA maturation. Nature 454:56–61 · DOI
  6. Davis BN, Hilyard AC, Nguyen PH, Lagna G, Hata A (2010) Smad proteins bind a conserved RNA sequence to promote microRNA maturation by Drosha. Mol Cell 39:373–384 · DOI
  7. De Conti L et al (2015) TDP-43 affects splicing profiles and isoform production of genes involved in the apoptotic and mitotic cellular pathways. Nucleic Acids Res 43:8990–9005 · DOI
  8. Di Carlo V et al (2013) TDP-43 regulates the microprocessor complex activity during in vitro neuronal differentiation. Mol Neurobiol 48:952–963 · DOI
  9. Dong C-M et al (2014) A stress-induced cellular aging model with postnatal neural stem cells. Cell Death Dis 5:e1116 · DOI
  10. Ford L, Crossley M, Williams T, Thorpe JR, Serpell LC, Kemenes G (2015) Effects of Aβ exposure on long-term associative memory and its neuronal mechanisms in a defined neuronal network. Sci Rep 5:10614 · DOI
  11. Hernandez-Rapp J, Smith PY, Filali M, Goupil C, Planel E, Magill ST, Goodman RH, Hébert SS (2015) Memory formation and retention are affected in adult miR-132/212 knockout mice. Behav Brain Res 287:15–26 · DOI · Paper page
  12. Hernandez-Rapp J, Rainone S, Hébert SS (2017) MicroRNAs underlying memory deficits in neurodegenerative disorders. Prog Neuro-Psychopharmacology Biol Psychiatry 73:79–86 · DOI
  13. Hudson MB et al (2014) miR-182 attenuates atrophy-related gene expression by targeting FoxO3 in skeletal muscle. Am J Physiol Cell Physiol 307:C314–C319 · DOI
  14. Inukai S, de Lencastre A, Turner M, Slack F (2012) Novel microRNAs differentially expressed during aging in the mouse brain. PLoS One 7:e40028 · DOI
  15. Ishihara H, Martin BL, Brautigan DL, Karaki H, Ozaki H, Kato Y, Fusetani N, Watabe S et al (1989) Calyculin A and okadaic acid: inhibitors of protein phosphatase activity. Biochem Biophys Res Commun 159:871–877 · DOI
  16. Kawahara Y, Mieda-Sato A (2012) TDP-43 promotes microRNA biogenesis as a component of the Drosha and Dicer complexes. Proc Natl Acad Sci U S A 109:3347–3352 · DOI
  17. Kremer EA, Gaur N, Lee MA, Engmann O, Bohacek J, Mansuy IM (2018) Interplay between TETs and microRNAs in the adult brain for memory formation. Sci Rep 8:1678 · DOI
  18. Koshibu K, Graff J, Beullens M, Heitz FD, Berchtold D, Russig H, Farinelli M, Bollen M et al (2009) Protein phosphatase 1 regulates the histone code for long-term memory. J Neurosci 29:13079–13089 · DOI
  19. Kosik KS, Rapp PR, Raz N, Small SA, Sweatt JD, Tsai LH (2012) Mechanisms of age-related cognitive change and targets for intervention: epigenetics. J Gerontol A Biol Sci Med Sci 67:741–746 · DOI
  20. Kye MJ, Niederst ED, Wertz MH, Gonçalves ICG, Akten B, Dover KZ, Peters M, Riessland M et al (2014) SMN regulates axonal local translation via miR-183/mTOR pathway. Hum Mol Genet 23:6318–6331 · DOI
  21. Li Y et al (2016) miR-182 (microRNA-182) suppression in the hippocampus evokes antidepressant-like effects in rats. Prog Neuropsychopharmacol Biol Psychiatry 65:96–103 · DOI
  22. Luttenberger K, Hofner B, Graessel E (2012) Are the effects of a non-drug multimodal activation therapy of dementia sustainable? Follow-up study 10 months after completion of a randomised controlled trial. BMC Neurol 12:151 · DOI
  23. Meerson A, Cacheaux L, Goosens KA, Sapolsky RM, Soreq H, Kaufer D (2010) Changes in brain MicroRNAs contribute to cholinergic stress reactions. J Mol Neurosci 40:47–55 · DOI
  24. Michely J, Kraft S, Müller U (2017) miR-12 and miR-124 contribute to defined early phases of long-lasting and transient memory. Sci Rep 7:7910 · DOI
  25. Morlando M, Dini Modigliani S, Torrelli G, Rosa A, di Carlo V, Caffarelli E, Bozzoni I (2012) FUS stimulates microRNA biogenesis by facilitating co-transcriptional Drosha recruitment. EMBO J 31:4502–4510 · DOI
  26. Munton RP, Vizi S, Mansuy IM (2004) The role of protein phosphatase-1 in the modulation of synaptic and structural plasticity. FEBS Lett 567:121–128 · DOI
  27. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, Bruce J, Schuck T et al (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314:130–133 · DOI · Paper page
  28. Neumann M, Rademakers R, Roeber S, Baker M, Kretzschmar HA, Mackenzie IRA (2009) A new subtype of frontotemporal lobar degeneration with FUS pathology. Brain 132:2922–2931 · DOI · Paper page
  29. Perera ND, Sheean RK, Scott JW, Kemp BE, Horne MK, Turner BJ (2014) Mutant TDP-43 deregulates AMPK activation by PP2A in ALS models. PLoS One 9:e90449 · DOI
  30. Rabkin JG, Albert SM, del Bene ML, O'Sullivan I, Tider T, Rowland LP, Mitsumoto H (2005) Prevalence of depressive disorders and change over time in late-stage ALS. Neurology 65:62–67 · DOI
  31. Ringholz GM, Appel SH, Bradshaw M, Cooke NA, Mosnik DM, Schulz PE (2005) Prevalence and patterns of cognitive impairment in sporadic ALS. Neurology 65:586–590 · DOI
  32. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C (T) method. Nat Protoc 3:1101–1108 · DOI · Paper page
  33. Schwartz JC, Ebmeier CC, Podell ER, Heimiller J, Taatjes DJ, Cech TR (2012) FUS binds the CTD of RNA polymerase II and regulates its phosphorylation at Ser2. Genes Dev 26:2690–2695 · DOI
  34. Stanford PM, Brooks WS, Teber ET, Hallupp M, McLean C, Halliday GM, Martins RN, Kwok JB et al (2004) Frequency of tau mutations in familial and sporadic frontotemporal dementia and other tauopathies. J Neurol 251:1098–1104 · DOI
  35. Witgert M, Salamone AR, Strutt AM, Jawaid A, Massman PJ, Bradshaw M, Mosnik D, Appel SH et al (2010) Frontal-lobe mediated behavioral dysfunction in amyotrophic lateral sclerosis. Eur J Neurol 17:103–110 · DOI
  36. 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 · DOI
  37. Woldemichael BT, Mansuy IM (2016) Micro-RNAs in cognition and cognitive disorders: Potential for novel biomarkers and therapeutics. Biochem Pharmacol 104:1–7 · DOI
  38. Xu XF et al (2017) miR-181a participates in contextual fear memory formation via activating mTOR signaling pathway. Cereb Cortex 22:1–13

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Metadata

Authors
Jawaid, A., Woldemichael, B. T., Kremer, E. A., Laferriere, F., Gaur, N., Afroz, T., Polymenidou, M., & Mansuy, I. M.
ORCID
Mansuy, Isabelle M.
Venue
Molecular Neurobiology
Publisher
Springer Science and Business Media LLC
Published
2018-08-20
Volume
56
Issue
5
Pages
3451-3462
ISSN
  • 0893-7648
  • 1559-1182
DOI
10.1007/s12035-018-1314-3
Cited by
39
References
6
Language
en
Licence
www.springer.com/tdm (tdm)

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