Non-coding RNA regulation of synaptic plasticity and memory: Implications for aging

Ageing Research Reviews

Volumn 17, Issue , 2014, Pages 34-42

  Earls, Laurie R ^a   Westmoreland, Joby J ^a   Zakharenko, Stanislav S ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Aging; Learning; Memory; MicroRNA; Non coding RNA; Synaptic plasticity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; LONG UNTRANSLATED RNA; MESSENGER RNA; MICRORNA; MICRORNA 134; MICRORNA 182; PIWI INTERACTING RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

AGING; AMNESIA; CENTRAL NERVOUS SYSTEM; HUMAN; MEMORY; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN FUNCTION; REVIEW; RNA TRANSLATION; SYNAPSE; SYNAPTIC TRANSMISSION; ANIMAL; METABOLISM; PHYSIOLOGY;

AGING; ANIMALS; HUMANS; MEMORY; NEURONAL PLASTICITY; RNA, UNTRANSLATED;

EID: 84906791742     PISSN: 15681637     EISSN: 18729649     Source Type: Journal    
DOI: 10.1016/j.arr.2014.03.004     Document Type: Review

References (112)

1. Araki T., Sasaki Y., Milbrandt J. Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 2004, 305:1010-1013.
2. Banerjee S., Neveu P., Kosik K.S. A coordinated local translational control point at the synapse involving relief from silencing and MOV10 degradation. Neuron 2009, 64:871-884.
3. Barry G., Briggs J.A., Vanichkina D.P., Poth E.M., Beveridge N.J., Ratnu V.S., Nayler S.P., Nones K., Hu J., Bredy T.W., Nakagawa S., Rigo F., Taft R.J., Cairns M.J., Blackshaw S., Wolvetang E.J., Mattick J.S. The long non-coding RNA Gomafu is acutely regulated in response to neuronal activation and involved in schizophrenia-associated alternative splicing. Mol. Psychiatry 2013, (Epub ahead of print 04/30/2013).
4. Beyret E., Liu N., Lin H. piRNA biogenesis during adult spermatogenesis in mice is independent of the ping-pong mechanism. Cell Res. 2012, 22:1429-1439.
5. Blundon J.A., Zakharenko S.S. Dissecting the components of long-term potentiation. Neuroscientist 2008, 14:598-608.
6. Boric K., Munoz P., Gallagher M., Kirkwood A. Potential adaptive function for altered long-term potentiation mechanisms in aging hippocampus. J. Neurosci. 2008, 28:8034-8039.
7. Cabili M.N., Trapnell C., Goff L., Koziol M., Tazon-Vega B., Regev A., Rinn J.L. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 2011, 25:1915-1927.
8. Cao X., Yeo G., Muotri A.R., Kuwabara T., Gage F.H. Noncoding RNAs in the mammalian central nervous system. Annu. Rev. Neurosci. 2006, 29:77-103.
9. Capel B., Swain A., Nicolis S., Hacker A., Walter M., Koopman P., Goodfellow P., Lovell-Badge R. Circular transcripts of the testis-determining gene Sry in adult mouse testis. Cell 1993, 73:1019-1030.
10. Carninci P., Kasukawa T., Katayama S., Gough J., Frith M.C., Maeda N., Oyama R., Ravasi T., Lenhard B., Wells C., Kodzius R., Shimokawa K., Bajic V.B., Brenner S.E., Batalov S., Forrest A.R., Zavolan M., Davis M.J., Wilming L.G., Aidinis V., Allen J.E., Ambesi-Impiombato A., Apweiler R., Aturaliya R.N., Bailey T.L., Bansal M., Baxter L., Beisel K.W., Bersano T., Bono H., Chalk A.M., Chiu K.P., Choudhary V., Christoffels A., Clutterbuck D.R., Crowe M.L., Dalla E., Dalrymple B.P., de B.B., Della G.G., di B.D., Down T., Engstrom P., Fagiolini M., Faulkner G., Fletcher C.F., Fukushima T., Furuno M., Futaki S., Gariboldi M., Georgii-Hemming P., Gingeras T.R., Gojobori T., Green R.E., Gustincich S., Harbers M., Hayashi Y., Hensch T.K., 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 S.P., Kruger A., Kummerfeld S.K., Kurochkin I.V., Lareau L.F., Lazarevic D., Lipovich L., Liu J., Liuni S., McWilliam S., Madan B.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 K.C., Pavan W.J., Pavesi G., Pesole G., Petrovsky N., Piazza S., Reed J., Reid J.F., Ring B.Z., Ringwald M., Rost B., Ruan Y., Salzberg S.L., Sandelin A., Schneider C., Schonbach C., Sekiguchi K., Semple C.A., 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 S.L., Tang S., Taylor M.S., Tegner J., Teichmann S.A., Ueda H.R., van N.E., Verardo R., Wei C.L., Yagi K., Yamanishi H., Zabarovsky E., Zhu S., Zimmer A., Hide W., Bult C., Grimmond S.M., Teasdale R.D., Liu E.T., Brusic V., Quackenbush J., Wahlestedt C., Mattick J.S., Hume D.A., 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. The transcriptional landscape of the mammalian genome. Science 2005, 309:1559-1563.
11. Cesana M., Cacchiarelli D., Legnini I., Santini T., Sthandier O., Chinappi M., Tramontano A., Bozzoni I. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 2011, 147:358-369.
12. Chapleau C.A., Boggio E.M., Calfa G., Percy A.K., Giustetto M., Pozzo-Miller L. Hippocampal CA1 pyramidal neurons of Mecp2 mutant mice show a dendritic spine phenotype only in the presymptomatic stage. Neural Plast. 2012, 2012:976164.
13. Chooniedass-Kothari S., Emberley E., Hamedani M.K., Troup S., Wang X., Czosnek A., Hube F., Mutawe M., Watson P.H., Leygue E. The steroid receptor RNA activator is the first functional RNA encoding a protein. FEBS Lett. 2004, 566:43-47.
14. Cohen H.Y., Miller C., Bitterman K.J., Wall N.R., Hekking B., Kessler B., Howitz K.T., Gorospe M., de C.R., Sinclair D.A. Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science 2004, 305:390-392.
15. Czech B., Hannon G.J. Small RNA sorting: matchmaking for Argonautes. Nat. Rev. Genet. 2011, 12:19-31.
16. Day J.J., Sweatt J.D. Epigenetic mechanisms in cognition. Neuron 2011, 70:813-829.
17. Derrien T., Johnson R., Bussotti G., Tanzer A., Djebali S., Tilgner H., Guernec G., Martin D., Merkel A., Knowles D.G., Lagarde J., Veeravalli L., Ruan X., Ruan Y., Lassmann T., Carninci P., Brown J.B., Lipovich L., Gonzalez J.M., Thomas M., Davis C.A., Shiekhattar R., Gingeras T.R., Hubbard T.J., Notredame C., Harrow J., Guigo R. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 2012, 22:1775-1789.
18. Earls L.R., Bayazitov I.T., Fricke R.G., Berry R.B., Illingworth E., Mittleman G., Zakharenko S.S. Dysregulation of presynaptic calcium and synaptic plasticity in a mouse model of 22q11 deletion syndrome. J. Neurosci. 2010, 30:15843-15855.
19. Earls L.R., Fricke R.G., Yu J., Berry R.B., Baldwin L.T., Zakharenko S.S. Age-dependent microRNA control of synaptic plasticity in 22q11 deletion syndrome and schizophrenia. J. Neurosci. 2012, 32:14132-14144.
20. Earls L.R., Zakharenko S.S. A synaptic function approach to investigating complex psychiatric diseases. Neuroscientist 2013, (Epub ahead of print 11/14/2013).
21. Eda A., Takahashi M., Fukushima T., Hohjoh H. Alteration of microRNA expression in the process of mouse brain growth. Gene 2011, 485:46-52.
22. Edbauer D., Neilson J.R., Foster K.A., Wang C.F., Seeburg D.P., Batterton M.N., Tada T., Dolan B.M., Sharp P.A., Sheng M. Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron 2010, 65:373-384.
23. Ekdahl Y., Farahani H.S., Behm M., Lagergren J., Ohman M. A-to-I editing of microRNAs in the mammalian brain increases during development. Genome Res. 2012, 22:1477-1487.
24. Errico F., Nistico R., Napolitano F., Oliva A.B., Romano R., Barbieri F., Florio T., Russo C., Mercuri N.B., Usiello A. Persistent increase of d-aspartate in d-aspartate oxidase mutant mice induces a precocious hippocampal age-dependent synaptic plasticity and spatial memory decay. Neurobiol. Aging 2011, 32:2061-2074.
25. Errico F., Nistico R., Palma G., Federici M., Affuso A., Brilli E., Topo E., Centonze D., Bernardi G., Bozzi Y., D'Aniello A., Di L.R., Mercuri N.B., Usiello A. Increased levels of d-aspartate in the hippocampus enhance LTP but do not facilitate cognitive flexibility. Mol. Cell. Neurosci. 2008, 37:236-246.
26. Faghihi M.A., Modarresi F., Khalil A.M., Wood D.E., Sahagan B.G., Morgan T.E., Finch C.E., St L.G., Kenny P.J., Wahlestedt C. Expression of a noncoding RNA is elevated in Alzheimer's disease and drives rapid feed-forward regulation of beta-secretase. Nat. Med. 2008, 14:723-730.
27. Faghihi M.A., Wahlestedt C. Regulatory roles of natural antisense transcripts. Nat. Rev. Mol. Cell Biol. 2009, 10:637-643.
28. Faure J., Lachenal G., Court M., Hirrlinger J., Chatellard-Causse C., Blot B., Grange J., Schoehn G., Goldberg Y., Boyer V., Kirchhoff F., Raposo G., Garin J., Sadoul R. Exosomes are released by cultured cortical neurones. Mol. Cell. Neurosci. 2006, 31:642-648.
29. Figurov A., Pozzo-Miller L.D., Olafsson P., Wang T., Lu B. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 1996, 381:706-709.
30. Furuno M., Pang K.C., Ninomiya N., Fukuda S., Frith M.C., Bult C., Kai C., Kawai J., Carninci P., Hayashizaki Y., Mattick J.S., Suzuki H. Clusters of internally primed transcripts reveal novel long noncoding RNAs. PLoS Genet. 2006, 2:e37.
31. Galindo M.I., Pueyo J.I., Fouix S., Bishop S.A., Couso J.P. Peptides encoded by short ORFs control development and define a new eukaryotic gene family. PLoS Biol. 2007, 5:e106.
32. Gao J., Wang W.Y., Mao Y.W., Graff J., Guan J.S., Pan L., Mak G., Kim D., Su S.C., Tsai L.H. A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature 2010, 466:1105-1109.
33. Girard A., Sachidanandam R., Hannon G.J., Carmell M.A. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 2006, 442:199-202.
34. Gong C., Maquat L.E. lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3' UTRs via Alu elements. Nature 2011, 470:284-288.
35. Griggs E.M., Young E.J., Rumbaugh G., Miller C.A. MicroRNA-182 regulates amygdala-dependent memory formation. J. Neurosci. 2013, 33:1734-1740.
36. Grutzendler J., Kasthuri N., Gan W.B. Long-term dendritic spine stability in the adult cortex. Nature 2002, 420:812-816.
37. Gu T., Buaas F.W., Simons A.K., Ackert-Bicknell C.L., Braun R.E., Hibbs M.A. Canonical A-to-I and C-to-U RNA editing is enriched at 3'UTRs and microRNA target sites in multiple mouse tissues. PLoS One 2012, 7:e33720.
38. Hansen K.F., Karelina K., Sakamoto K., Wayman G.A., Impey S., Obrietan K. miRNA-132: a dynamic regulator of cognitive capacity. Brain Struct. Funct. 2013, 218:817-831.
39. Hansen T.B., Jensen T.I., Clausen B.H., Bramsen J.B., Finsen B., Damgaard C.K., Kjems J. Natural RNA circles function as efficient microRNA sponges. Nature 2013, 495:384-388.
40. Hentze M.W., Preiss T. Circular RNAs: splicing's enigma variations. EMBO J. 2013, 32:923-925.
41. Howitz K.T., Bitterman K.J., Cohen H.Y., Lamming D.W., Lavu S., Wood J.G., Zipkin R.E., Chung P., Kisielewski A., Zhang L.L., Scherer B., Sinclair D.A. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 2003, 425:191-196.
42. Iacoangeli A., Tiedge H. Translational control at the synapse: role of RNA regulators. Trends Biochem. Sci. 2013, 38:47-55.
43. Impey S., McCorkle S.R., Cha-Molstad H., Dwyer J.M., Yochum G.S., Boss J.M., McWeeney S., Dunn J.J., Mandel G., Goodman R.H. Defining the CREB regulon: a genome-wide analysis of transcription factor regulatory regions. Cell 2004, 119:1041-1054.
44. Jeon Y., Lee J.T. YY1 tethers Xist RNA to the inactive X nucleation center. Cell 2011, 146:119-133.
45. Ji Y., Lu Y., Yang F., Shen W., Tang T.T., Feng L., Duan S., Lu B. Acute and gradual increases in BDNF concentration elicit distinct signaling and functions in neurons. Nat. Neurosci. 2010, 13:302-309.
46. Jiang Y.H., Armstrong D., Albrecht U., Atkins C.M., Noebels J.L., Eichele G., Sweatt J.D., Beaudet A.L. Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation. Neuron 1998, 21:799-811.
47. Jimenez-Mateos E.M., Engel T., Merino-Serrais P., McKiernan R.C., Tanaka K., Mouri G., Sano T., O'Tuathaigh C., Waddington J.L., Prenter S., Delanty N., Farrell M.A., O'Brien D.F., Conroy R.M., Stallings R.L., DeFelipe J., Henshall D.C. Silencing microRNA-134 produces neuroprotective and prolonged seizure-suppressive effects. Nat. Med. 2012, 18:1087-1094.
48. Juliano C., Wang J., Lin H. Uniting germline and stem cells: the function of Piwi proteins and the piRNA pathway in diverse organisms. Annu. Rev. Genet. 2011, 45:447-469.
49. Kaeberlein M., McVey M., Guarente L. The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev. 1999, 13:2570-2580.
50. Kapranov P., Cheng J., Dike S., Nix D.A., Duttagupta R., Willingham A.T., Stadler P.F., Hertel J., Hackermuller J., Hofacker I.L., Bell I., Cheung E., Drenkow J., Dumais E., Patel S., Helt G., Ganesh M., Ghosh S., Piccolboni A., Sementchenko V., Tammana H., Gingeras T.R. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 2007, 316:1484-1488.
51. Kim D., Nguyen M.D., Dobbin M.M., Fischer A., Sananbenesi F., Rodgers J.T., Delalle I., Baur J.A., Sui G., Armour S.M., Puigserver P., Sinclair D.A., Tsai L.H. SIRT1 deacetylase protects against neurodegeneration in models for Alzheimer's disease and amyotrophic lateral sclerosis. EMBO J. 2007, 26:3169-3179.
52. Klein M.E., Lioy D.T., Ma L., Impey S., Mandel G., Goodman R.H. Homeostatic regulation of MeCP2 expression by a CREB-induced microRNA. Nat. Neurosci. 2007, 10:1513-1514.
53. Koles K., Nunnari J., Korkut C., Barria R., Brewer C., Li Y., Leszyk J., Zhang B., Budnik V. Mechanism of evenness interrupted (Evi)-exosome release at synaptic boutons. J. Biol. Chem. 2012, 287:16820-16834.
54. Korkut C., Ataman B., Ramachandran P., Ashley J., Barria R., Gherbesi N., Budnik V. Trans-synaptic transmission of vesicular Wnt signals through Evi/Wntless. Cell 2009, 139:393-404.
55. Korkut C., Li Y., Koles K., Brewer C., Ashley J., Yoshihara M., Budnik V. Regulation of postsynaptic retrograde signaling by presynaptic exosome release. Neuron 2013, 77:1039-1046.
56. Korzus E., Rosenfeld M.G., Mayford M. CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 2004, 42:961-972.
57. Kosik K.S. The neuronal microRNA system. Nat. Rev. Neurosci. 2006, 7:911-920.
58. Krichevsky A.M., King K.S., Donahue C.P., Khrapko K., Kosik K.S. A microRNA array reveals extensive regulation of microRNAs during brain development. RNA 2003, 9:1274-1281.
59. Lang C., Barco A., Zablow L., Kandel E.R., Siegelbaum S.A., Zakharenko S.S. Transient expansion of synaptically connected dendritic spines upon induction of hippocampal long-term potentiation. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:16665-16670.
60. Lee E.J., Banerjee S., Zhou H., Jammalamadaka A., Arcila M., Manjunath B.S., Kosik K.S. Identification of piRNAs in the central nervous system. RNA 2011, 17:1090-1099.
61. Levenson J.M., O'Riordan K.J., Brown K.D., Trinh M.A., Molfese D.L., Sweatt J.D. Regulation of histone acetylation during memory formation in the hippocampus. J. Biol. Chem. 2004, 279:40545-40559.
62. Lin Q., Wei W., Coelho C.M., Li X., Baker-Andresen D., Dudley K., Ratnu V.S., Boskovic Z., Kobor M.S., Sun Y.E., Bredy T.W. The brain-specific microRNA miR-128b regulates the formation of fear-extinction memory. Nat. Neurosci. 2011, 14:1115-1117.
63. Lugli G., Torvik V.I., Larson J., Smalheiser N.R. Expression of microRNAs and their precursors in synaptic fractions of adult mouse forebrain. J. Neurochem. 2008, 106:650-661.
64. Mabb A.M., Judson M.C., Zylka M.J., Philpot B.D. Angelman syndrome: insights into genomic imprinting and neurodevelopmental phenotypes. Trends Neurosci. 2011, 34:293-303.
65. Magill S.T., Cambronne X.A., Luikart B.W., Lioy D.T., Leighton B.H., Westbrook G.L., Mandel G., Goodman R.H. microRNA-132 regulates dendritic growth and arborization of newborn neurons in the adult hippocampus. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:20382-20387.
66. Magnusson K.R., Nelson S.E., Young A.B. Age-related changes in the protein expression of subunits of the NMDA receptor. Brain Res. Mol. Brain Res. 2002, 99:40-45.
67. Malone C.D., Hannon G.J. Molecular evolution of piRNA and transposon control pathways in Drosophila. Cold Spring Harb. Symp. Quant. Biol. 2009, 74:225-234.
68. Malone C.D., Hannon G.J. Small RNAs as guardians of the genome. Cell 2009, 136:656-668.
69. Mattick J.S. The functional genomics of noncoding RNA. Science 2005, 309:1527-1528.
70. Maze I., Noh K.M., Allis C.D. Histone regulation in the CNS: basic principles of epigenetic plasticity. Neuropsychopharmacology 2013, 38:3-22.
71. Meister G. Argonaute proteins: functional insights and emerging roles. Nat. Rev. Genet. 2013, 14:447-459.
72. Mellios N., Sugihara H., Castro J., Banerjee A., Le C., Kumar A., Crawford B., Strathmann J., Tropea D., Levine S.S., Edbauer D., Sur M. miR-132, an experience-dependent microRNA, is essential for visual cortex plasticity. Nat. Neurosci. 2011, 14:1240-1242.
73. Memczak S., Jens M., Elefsinioti A., Torti F., Krueger J., Rybak A., Maier L., Mackowiak S.D., Gregersen L.H., Munschauer M., Loewer A., Ziebold U., Landthaler M., Kocks C., le N.F., Rajewsky N. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 2013, 495:333-338.
74. Mercer T.R., Dinger M.E., Sunkin S.M., Mehler M.F., Mattick J.S. Specific expression of long noncoding RNAs in the mouse brain. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:716-721.
75. Miska E.A., Alvarez-Saavedra E., Townsend M., Yoshii A., Sestan N., Rakic P., Constantine-Paton M., Horvitz H.R. Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol. 2004, 5:R68.
76. Modarresi F., Faghihi M.A., Lopez-Toledano M.A., Fatemi R.P., Magistri M., Brothers S.P., van der Brug M.P., Wahlestedt C. Inhibition of natural antisense transcripts in vivo results in gene-specific transcriptional upregulation. Nat. Biotechnol. 2012, 30:453-459.
77. Morel L., Regan M., Higashimori H., Ng S.K., Esau C., Vidensky S., Rothstein J., Yang Y. Neuronal exosomal miRNA-dependent translational regulation of astroglial glutamate transporter GLT1. J. Biol. Chem. 2013, 288:7105-7116.
78. Nakazawa T., Kuriu T., Tezuka T., Umemori H., Okabe S., Yamamoto T. Regulation of dendritic spine morphology by an NMDA receptor-associated Rho GTPase-activating protein, p250GAP. J. Neurochem. 2008, 105:1384-1393.
79. Natera-Naranjo O., Aschrafi A., Gioio A.E., Kaplan B.B. Identification and quantitative analyses of microRNAs located in the distal axons of sympathetic neurons. RNA 2010, 16:1516-1529.
80. Ng S.Y., Lin L., Soh B.S., Stanton L.W. Long noncoding RNAs in development and disease of the central nervous system. Trends Genet. 2013, 29:461-468.
81. Nudelman A.S., DiRocco D.P., Lambert T.J., Garelick M.G., Le J., Nathanson N.M., Storm D.R. Neuronal activity rapidly induces transcription of the CREB-regulated microRNA-132, in vivo. Hippocampus 2010, 20:492-498.
82. Osato N., Suzuki Y., Ikeo K., Gojobori T. Transcriptional interferences in cis natural antisense transcripts of humans and mice. Genetics 2007, 176:1299-1306.
83. Peleg S., Sananbenesi F., Zovoilis A., Burkhardt S., Bahari-Javan S., Agis-Balboa R.C., Cota P., Wittnam J.L., Gogol-Doering A., Opitz L., Salinas-Riester G., Dettenhofer M., Kang H., Farinelli L., Chen W., Fischer A. Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 2010, 328:753-756.
84. Peng J.C., Lin H. Beyond transposons: the epigenetic and somatic functions of the Piwi-piRNA mechanism. Curr. Opin. Cell Biol. 2013, 25:190-194.
85. Peng Z., Cheng Y., Tan B.C., Kang L., Tian Z., Zhu Y., Zhang W., Liang Y., Hu X., Tan X., Guo J., Dong Z., Liang Y., Bao L., Wang J. Comprehensive analysis of RNA-Seq data reveals extensive RNA editing in a human transcriptome. Nat. Biotechnol. 2012, 30:253-260.
86. Pitcher G.M., Beggs S., Woo R.S., Mei L., Salter M.W. ErbB4 is a suppressor of long-term potentiation in the adult hippocampus. Neuroreport 2008, 19:139-143.
87. Pruunsild P., Kazantseva A., Aid T., Palm K., Timmusk T. Dissecting the human BDNF locus: bidirectional transcription, complex splicing, and multiple promoters. Genomics 2007, 90:397-406.
88. Qureshi I.A., Mattick J.S., Mehler M.F. Long non-coding RNAs in nervous system function and disease. Brain Res. 2010, 1338:20-35.
89. Qureshi I.A., Mehler M.F. Emerging roles of non-coding RNAs in brain evolution, development, plasticity and disease. Nat. Rev. Neurosci. 2012, 13:528-541.
90. Rajasethupathy P., Antonov I., Sheridan R., Frey S., Sander C., Tuschl T., Kandel E.R. A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity. Cell 2012, 149:693-707.
91. Ravasi T., Suzuki H., Pang K.C., Katayama S., Furuno M., Okunishi R., Fukuda S., Ru K., Frith M.C., Gongora M.M., Grimmond S.M., Hume D.A., Hayashizaki Y., Mattick J.S. Experimental validation of the regulated expression of large numbers of non-coding RNAs from the mouse genome. Genome Res. 2006, 16:11-19.
92. Redfern A.D., Colley S.M., Beveridge D.J., Ikeda N., Epis M.R., Li X., Foulds C.E., Stuart L.M., Barker A., Russell V.J., Ramsay K., Kobelke S.J., Li X., Hatchell E.C., Payne C., Giles K.M., Messineo A., Gatignol A., Lanz R.B., O'Malley B.W., Leedman P.J. RNA-induced silencing complex (RISC) Proteins PACT, TRBP, and Dicer are SRA binding nuclear receptor coregulators. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:6536-6541.
93. Sasaki Y., Gross C., Xing L., Goshima Y., Bassell G.J. Identification of axon-enriched microRNAs localized to growth cones of cortical neurons. Dev. Neurobiol. 2013, (Epub ahead of print 04/29/2013).
94. Saxe J.P., Lin H. Small noncoding RNAs in the germline. Cold Spring Harb. Perspect. Biol. 2011, 3:a002717.
95. Scott H.L., Tamagnini F., Narduzzo K.E., Howarth J.L., Lee Y.B., Wong L.F., Brown M.W., Warburton E.C., Bashir Z.I., Uney J.B. MicroRNA-132 regulates recognition memory and synaptic plasticity in the perirhinal cortex. Eur. J. Neurosci. 2012, 36:2941-2948.
96. Sempere L.F., Freemantle S., Pitha-Rowe I., Moss E., Dmitrovsky E., Ambros V. Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 2004, 5:R13.
97. Shamir A., Kwon O.B., Karavanova I., Vullhorst D., Leiva-Salcedo E., Janssen M.J., Buonanno A. The importance of the NRG-1/ErbB4 pathway for synaptic plasticity and behaviors associated with psychiatric disorders. J. Neurosci. 2012, 32:2988-2997.
98. Siegel G., Obernosterer G., Fiore R., Oehmen M., Bicker S., Christensen M., Khudayberdiev S., Leuschner P.F., Busch C.J., Kane C., Hubel K., Dekker F., Hedberg C., Rengarajan B., Drepper C., Waldmann H., Kauppinen S., Greenberg M.E., Draguhn A., Rehmsmeier M., Martinez J., Schratt G.M. A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nat. Cell Biol. 2009, 11:705-716.
99. Silva J., Mak W., Zvetkova I., Appanah R., Nesterova T.B., Webster Z., Peters A.H., Jenuwein T., Otte A.P., Brockdorff N. Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes. Dev. Cell 2003, 4:481-495.
100. Smalheiser N.R., Lugli G., Torvik V.I., Mise N., Ikeda R., Abe K. Natural antisense transcripts are co-expressed with sense mRNAs in synaptoneurosomes of adult mouse forebrain. Neurosci. Res. 2008, 62:236-239.
101. Tetta C., Ghigo E., Silengo L., Deregibus M.C., Camussi G. Extracellular vesicles as an emerging mechanism of cell-to-cell communication. Endocrine 2013, 44:11-19.
102. Thomson T., Lin H. The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu. Rev. Cell Dev. Biol. 2009, 25:355-376.
103. Tiedge H., Chen W., Brosius J. Primary structure, neural-specific expression, and dendritic location of human BC200 RNA. J. Neurosci. 1993, 13:2382-2390.
104. Tiedge H., Fremeau R.T., Weinstock P.H., Arancio O., Brosius J. Dendritic location of neural BC1 RNA. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:2093-2097.
105. Ulitsky I., Shkumatava A., Jan C.H., Sive H., Bartel D.P. Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell 2011, 147:1537-1550.
106. Vo N., Klein M.E., Varlamova O., Keller D.M., Yamamoto T., Goodman R.H., Impey S. A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:16426-16431.
107. Wang I.T., Reyes A.R., Zhou Z. Neuronal morphology in MeCP2 mouse models is intrinsically variable and depends on age, cell type, and Mecp2 mutation. Neurobiol. Dis. 2013, 58:3-12.
108. Wayman G.A., Davare M., Ando H., Fortin D., Varlamova O., Cheng H.Y., Marks D., Obrietan K., Soderling T.R., Goodman R.H., Impey S. An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:9093-9098.
109. Wibrand K., Panja D., Tiron A., Ofte M.L., Skaftnesmo K.O., Lee C.S., Pena J.T., Tuschl T., Bramham C.R. Differential regulation of mature and precursor microRNA expression by NMDA and metabotropic glutamate receptor activation during LTP in the adult dentate gyrus in vivo. Eur. J. Neurosci. 2010, 31:636-645.
110. Yan Z., Hu H.Y., Jiang X., Maierhofer V., Neb E., He L., Hu Y., Hu H., Li N., Chen W., Khaitovich P. Widespread expression of piRNA-like molecules in somatic tissues. Nucleic Acids Res. 2011, 39:6596-6607.
111. Zeng Y., Tan M., Kohyama J., Sneddon M., Watson J.B., Sun Y.E., Xie C.W. Epigenetic enhancement of BDNF signaling rescues synaptic plasticity in aging. J. Neurosci. 2011, 31:17800-17810.
112. Zovkic I.B., Guzman-Karlsson M.C., Sweatt J.D. Epigenetic regulation of memory formation and maintenance. Learn. Mem. 2013, 20:61-74.