Epigenetically regulated microRNAs in Alzheimer's disease

Neurobiology of Aging

Volumn 35, Issue 4, 2014, Pages 731-745

  Van den Hove, Daniel L ^a,b   Kompotis, Konstantinos ^a   Lardenoije, Roy ^a   Kenis, Gunter ^a   Mill, Jonathan ^c,d   Steinbusch, Harry W ^a   Lesch, Klaus Peter ^a,b   Fitzsimons, Carlos P ^e   De Strooper, Bart ^f,g   Rutten, Bart P F ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF EXETER MEDICAL SCHOOL   (United Kingdom)

^e UNIVERSITY OF AMSTERDAM   (Netherlands)

^f DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^g UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Alzheimer's disease; DNA methylation; Epigenetics; MicroRNAs

Indexed keywords

MICRORNA; MICRORNA 107; MICRORNA 124; MICRORNA 125B; MICRORNA 132; MICRORNA 137; MICRORNA 146A; MICRORNA 148A; MICRORNA 184; MICRORNA 200; MICRORNA 212; MICRORNA 34; MICRORNA 9; UNCLASSIFIED DRUG;

AGING; ALZHEIMER DISEASE; DNA METHYLATION; DNA MODIFICATION; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; GENE MUTATION; GENE REGULATORY NETWORK; GENETIC ANALYSIS; GENETIC EPIGENESIS; HISTONE MODIFICATION; HUMAN; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROMOTER REGION; REVIEW;

ALZHEIMER'S DISEASE; DNA METHYLATION; EPIGENETICS; MICRORNAS;

ALZHEIMER DISEASE; DNA METHYLATION; EPIGENESIS, GENETIC; HISTONES; HUMANS; MICRORNAS; NEUROGLIA; NEURONS; TRANSCRIPTION, GENETIC;

EID: 84891371158     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.10.082     Document Type: Review

References (254)

1. Abe M., Bonini N.M. MicroRNAs and neurodegeneration: role and impact. Trends Cell Biol. 2013, 23:30-36.
2. Abuhatzira L., Makedonski K., Kaufman Y., Razin A., Shemer R. MeCP2 deficiency in the brain decreases BDNF levels by REST/CoREST-mediated repression and increases TRKB production. Epigenetics 2007, 2:214-222.
3. Adwan L., Zawia N.H. Epigenetics: a novel therapeutic approach for the treatment of Alzheimer's disease. Pharmacol. Ther. 2013, 139:41-50.
4. Agiostratidou G., Muros R.M., Shioi J., Marambaud P., Robakis N.K. The cytoplasmic sequence of E-cadherin promotes non-amyloidogenic degradation of A beta precursors. J.Neurochem. 2006, 96:1182-1188.
5. Agirre X., Vilas-Zornoza A., Jimenez-Velasco A., Martin-Subero J.I., Cordeu L., Garate L., San Jose-Eneriz E., Abizanda G., Rodriguez-Otero P., Fortes P., Rifon J., Bandres E., Calasanz M.J., Martin V., Heiniger A., Torres A., Siebert R., Roman-Gomez J., Prosper F. Epigenetic silencing of the tumor suppressor microRNA Hsa-miR-124a regulates CDK6 expression and confers a poor prognosis in acute lymphoblastic leukemia. Cancer Res. 2009, 69:4443-4453.
6. Ando T., Yoshida T., Enomoto S., Asada K., Tatematsu M., Ichinose M., Sugiyama T., Ushijima T. DNA methylation of microRNA genes in gastric mucosae of gastric cancer patients: its possible involvement in the formation of epigenetic field defect. Int. J. Cancer 2009, 124:2367-2374.
7. Aufsatz W., Mette M.F., van der Winden J., Matzke A.J., Matzke M. RNA-directed DNA methylation in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A 2002, 99:16499-16506.
8. Baer C., Claus R., Frenzel L.P., Zucknick M., Park Y.J., Gu L., Weichenhan D., Fischer M., Pallasch C.P., Herpel E., Rehli M., Byrd J.C., Wendtner C.M., Plass C. Extensive promoter DNA hypermethylation and hypomethylation is associated with aberrant microRNA expression in chronic lymphocytic leukemia. Cancer Res. 2012, 72:3775-3785.
9. Bamburg J.R., Bernstein B.W., Davis R.C., Flynn K.C., Goldsbury C., Jensen J.R., Maloney M.T., Marsden I.T., Minamide L.S., Pak C.W., Shaw A.E., Whiteman I., Wiggan O. ADF/Cofilin-actin rods in neurodegenerative diseases. Curr. Alzheimer Res. 2010, 7:241-250.
10. Bandres E., Agirre X., Bitarte N., Ramirez N., Zarate R., Roman-Gomez J., Prosper F., Garcia-Foncillas J. Epigenetic regulation of microRNA expression in colorectal cancer. Int. J. Cancer 2009, 125:2737-2743.
11. Bayne E.H., Allshire R.C. RNA-directed transcriptional gene silencing in mammals. Trends Genet. 2005, 21:370-373.
12. Bellenchi G.C., Gurniak C.B., Perlas E., Middei S., Ammassari-Teule M., Witke W. N-cofilin is associated with neuronal migration disorders and cell cycle control in the cerebral cortex. Genes Dev. 2007, 21:2347-2357.
13. Bemis L.T., Chen R., Amato C.M., Classen E.H., Robinson S.E., Coffey D.G., Erickson P.F., Shellman Y.G., Robinson W.A. MicroRNA-137 targets microphthalmia-associated transcription factor in melanoma cell lines. Cancer Res. 2008, 68:1362-1368.
14. Blondel S., Navarro C., Levy N., Peschanski M., Nissan X. [miR-9: the sentinel of neurons in progeria]. Med. Sci. (Paris) 2012, 28:663-666.
15. Boissart C., Nissan X., Giraud-Triboult K., Peschanski M., Benchoua A. miR-125 potentiates early neural specification of human embryonic stem cells. Development 2012, 139:1247-1257.
16. Brait M., Sidransky D. Cancer epigenetics: above and beyond. Toxicol. Mech. Methods 2011, 21:275-288.
17. Brouwers N., Sleegers K., Engelborghs S., Maurer-Stroh S., Gijselinck I., van der Zee J., Pickut B.A., Van den Broeck M., Mattheijssens M., Peeters K., Schymkowitz J., Rousseau F., Martin J.J., Cruts M., De Deyn P.P., Van Broeckhoven C. Genetic variability in progranulin contributes to risk for clinically diagnosed Alzheimer disease. Neurology 2008, 71:656-664.
18. Brueckner B., Stresemann C., Kuner R., Mund C., Musch T., Meister M., Sultmann H., Lyko F. The human let-7a-3 locus contains an epigenetically regulated microRNA gene with oncogenic function. Cancer Res. 2007, 67:1419-1423.
19. Cao X., Pfaff S.L., Gage F.H. Afunctional study of miR-124 in the developing neural tube. Genes Dev. 2007, 21:531-536.
20. Carrington J.C., Ambros V. Role of microRNAs in plant and animal development. Science 2003, 301:336-338.
21. Chen-Plotkin A.S., Unger T.L., Gallagher M.D., Bill E., Kwong L.K., Volpicelli-Daley L., Busch J.I., Akle S., Grossman M., Van Deerlin V., Trojanowski J.Q., Lee V.M. TMEM106B, the risk gene for frontotemporal dementia, is regulated by the microRNA-132/212 cluster and affects progranulin pathways. J.Neurosci. 2012, 32:11213-11227.
22. Chen L., Chen X.R., Zhang R., Li P., Liu Y., Yan K., Jiang X.D. MicroRNA-107 inhibits glioma cell migration and invasion by modulating Notch2 expression. J.Neurooncol. 2013, 102:59-66.
23. Chen L., Zhang R., Li P., Liu Y., Qin K., Fa Z.Q., Liu Y.J., Ke Y.Q., Jiang X.D. P53-induced microRNA-107 inhibits proliferation of glioma cells and down-regulates the expression of CDK6 and Notch-2. Neuroscience Lett. 2013, 534:327-332.
24. Cheng H.Y., Papp J.W., Varlamova O., Dziema H., Russell B., Curfman J.P., Nakazawa T., Shimizu K., Okamura H., Impey S., Obrietan K. microRNA modulation of circadian-clock period and entrainment. Neuron 2007, 54:813-829.
25. Cheng L.C., Pastrana E., Tavazoie M., Doetsch F. miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat. Neurosci. 2009, 12:399-408.
26. Chestnut B.A., Chang Q., Price A., Lesuisse C., Wong M., Martin L.J. Epigenetic regulation of motor neuron cell death through DNA methylation. J.Neurosci. 2011, 31:16619-16636.
27. Choi P.S., Zakhary L., Choi W.Y., Caron S., Alvarez-Saavedra E., Miska E.A., McManus M., Harfe B., Giraldez A.J., Horvitz H.R., Schier A.F., Dulac C. Members of the miRNA-200 family regulate olfactory neurogenesis. Neuron 2008, 57:41-55.
28. Chouliaras L., Rutten B.P., Kenis G., Peerbooms O., Visser P.J., Verhey F., van Os J., Steinbusch H.W., van den Hove D.L. Epigenetic regulation in the pathophysiology of Alzheimer's disease. Prog. Neurobiol. 2010, 90:498-510.
29. Chouliaras L., van den Hove D.L., Kenis G., Dela Cruz J., Lemmens M.A., van Os J., Steinbusch H.W., Schmitz C., Rutten B.P. Caloric restriction attenuates age-related changes of DNA methyltransferase 3a in mouse hippocampus. Brain Behav. Immun. 2011, 25:616-623.
30. Christoffersen N.R., Shalgi R., Frankel L.B., Leucci E., Lees M., Klausen M., Pilpel Y., Nielsen F.C., Oren M., Lund A.H. p53-independent upregulation of miR-34a during oncogene-induced senescence represses MYC. Cell Death Differ. 2010, 17:236-245.
31. Christoffersen N.R., Silahtaroglu A., Orom U.A., Kauppinen S., Lund A.H. miR-200b mediates post-transcriptional repression of ZFHX1B. RNA 2007, 13:1172-1178.
32. Chuang J.C., Jones P.A. Epigenetics and microRNAs. Pediatr. Res. 2007, 61:24R-29R.
33. Clovis Y.M., Enard W., Marinaro F., Huttner W.B., De Pietri Tonelli D. Convergent repression of Foxp2 3'UTR by miR-9 and miR-132 in embryonic mouse neocortex: implications for radial migration of neurons. Development 2012, 139:3332-3342.
34. Cogswell J.P., Ward J., Taylor I.A., Waters M., Shi Y., Cannon B., Kelnar K., Kemppainen J., Brown D., Chen C., Prinjha R.K., Richardson J.C., Saunders A.M., Roses A.D., Richards C.A. Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways. J.Alzheimer's disease 2008, 14:27-41.
35. Conaco C., Otto S., Han J.J., Mandel G. Reciprocal actions of REST and a microRNA promote neuronal identity. Proc. Natl. Acad. Sci. U.S.A 2006, 103:2422-2427.
36. Corney D.C., Flesken-Nikitin A., Godwin A.K., Wang W., Nikitin A.Y. MicroRNA-34b and MicroRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Res. 2007, 67:8433-8438.
37. Covic M., Karaca E., Lie D.C. Epigenetic regulation of neurogenesis in the adult hippocampus. Heredity (Edinb) 2010, 105:122-134.
38. Cui Y., Xiao Z., Han J., Sun J., Ding W., Zhao Y., Chen B., Li X., Dai J. MiR-125b orchestrates cell proliferation, differentiation and migration in neural stem/progenitor cells by targeting Nestin. BMC Neurosci. 2012, 13:116.
39. Das S., Foley N., Bryan K., Watters K.M., Bray I., Murphy D.M., Buckley P.G., Stallings R.L. MicroRNA mediates DNA demethylation events triggered by retinoic acid during neuroblastoma cell differentiation. Cancer Res. 2010, 70:7874-7881.
40. Davalos V., Moutinho C., Villanueva A., Boque R., Silva P., Carneiro F., Esteller M. Dynamic epigenetic regulation of the microRNA-200 family mediates epithelial and mesenchymal transitions in human tumorigenesis. Oncogene 2012, 31:2062-2074.
41. Day J.J., Sweatt J.D. Epigenetic treatments for cognitive impairments. Neuropsychopharmacology 2012, 37:247-260.
42. Delay C., Mandemakers W., Hebert S.S. MicroRNAs in Alzheimer's disease. Neurobiol. Disease 2012, 46:285-290.
43. Dews M., Homayouni A., Yu D., Murphy D., Sevignani C., Wentzel E., Furth E.E., Lee W.M., Enders G.H., Mendell J.T., Thomas-Tikhonenko A. Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat. Genet. 2006, 38:1060-1065.
44. Duursma A.M., Kedde M., Schrier M., le Sage C., Agami R. miR-148 targets human DNMT3b protein coding region. RNA 2008, 14:872-877.
45. 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.
46. Egger G., Liang G., Aparicio A., Jones P.A. Epigenetics in human disease and prospects for epigenetic therapy. Nature 2004, 429:457-463.
47. Fang M., Wang J., Zhang X., Geng Y., Hu Z., Rudd J.A., Ling S., Chen W., Han S. The miR-124 regulates the expression of BACE1/beta-secretase correlated with cell death in Alzheimer's disease. Toxicology Lett. 2012, 209:94-105.
48. Fazi F., Rosa A., Fatica A., Gelmetti V., De Marchis M.L., Nervi C., Bozzoni I. Aminicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPalpha regulates human granulopoiesis. Cell 2005, 123:819-831.
49. Feng L., Xie Y., Zhang H., Wu Y. miR-107 targets cyclin-dependent kinase 6 expression, induces cell cycle G1 arrest and inhibits invasion in gastric cancer cells. Med. Oncol. 2012, 29:856-863.
50. Ferretti E., De Smaele E., Miele E., Laneve P., Po A., Pelloni M., Paganelli A., Di Marcotullio L., Caffarelli E., Screpanti I., Bozzoni I., Gulino A. Concerted microRNA control of Hedgehog signalling in cerebellar neuronal progenitor and tumour cells. EMBO J. 2008, 27:2616-2627.
51. Fineberg S.K., Datta P., Stein C.S., Davidson B.L. MiR-34a represses Numbl in murine neural progenitor cells and antagonizes neuronal differentiation. PloS one 2012, 7:e38562.
52. Fiore R., Khudayberdiev S., Christensen M., Siegel G., Flavell S.W., Kim T.K., Greenberg M.E., Schratt G. Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels. EMBO J. 2009, 28:697-710.
53. Fitzsimons C.P., van Hooijdonk L.W., Schouten M., Zalachoras I., Brinks V., Zheng T., Schouten T.G., Saaltink D.J., Dijkmans T., Steindler D.A., Verhaagen J., Verbeek F.J., Lucassen P.J., de Kloet E.R., Meijer O.C., Karst H., Joels M., Oitzl M.S., Vreugdenhil E. Knockdown of the glucocorticoid receptor alters functional integration of newborn neurons in the adult hippocampus and impairs fear-motivated behavior. Mol. Psychiatry 2012, 18:993-1005.
54. Flynn K.C., Hellal F., Neukirchen D., Jacob S., Tahirovic S., Dupraz S., Stern S., Garvalov B.K., Gurniak C., Shaw A.E., Meyn L., Wedlich-Soldner R., Bamburg J.R., Small J.V., Witke W., Bradke F. ADF/cofilin-mediated actin retrograde flow directs neurite formation in the developing brain. Neuron 2012, 76:1091-1107.
55. Foley N.H., Bray I.M., Tivnan A., Bryan K., Murphy D.M., Buckley P.G., Ryan J., O'Meara A., O'Sullivan M., Stallings R.L. MicroRNA-184 inhibits neuroblastoma cell survival through targeting the serine/threonine kinase AKT2. Mol. Cancer 2010, 9:83.
56. Forman J.J., Legesse-Miller A., Coller H.A. Asearch for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence. Proc. Natl. Acad. Sci. U.S.A 2008, 105:14879-14884.
57. Formosa A., Lena A.M., Markert E.K., Cortelli S., Miano R., Mauriello A., Croce N., Vandesompele J., Mestdagh P., Finazzi-Agro E., Levine A.J., Melino G., Bernardini S., Candi E. DNA methylation silences miR-132 in prostate cancer. Oncogene 2012, 32:127-134.
58. Fraga M.F. Genetic and epigenetic regulation of aging. Curr. Opin. Immunol. 2009, 21:446-453.
59. Fuks F., Hurd P.J., Wolf D., Nan X., Bird A.P., Kouzarides T. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J.Biol. Chem. 2003, 278:4035-4040.
60. Geekiyanage H., Chan C. MicroRNA-137/181c regulates serine palmitoyltransferase and in turn amyloid beta, novel targets in sporadic Alzheimer's disease. J.Neurosci. 2011, 31:14820-14830.
61. Georgiades P., Watkins M., Surani M.A., Ferguson-Smith A.C. Parental origin-specific developmental defects in mice with uniparental disomy for chromosome 12. Development 2000, 127:4719-4728.
62. Goodman R.H., Smolik S. CBP/p300 in cell growth, transformation, and development. Genes Dev. 2000, 14:1553-1577.
63. Grayson D.R., Guidotti A. The dynamics of DNA methylation in schizophrenia and related psychiatric disorders. Neuropsychopharmacology 2013, 38:138-166.
64. Guo L.M., Pu Y., Han Z., Liu T., Li Y.X., Liu M., Li X., Tang H. MicroRNA-9 inhibits ovarian cancer cell growth through regulation of NF-kappaB1. FEBS J. 2009, 276:5537-5546.
65. Han L., Witmer P.D., Casey E., Valle D., Sukumar S. DNA methylation regulates microRNA expression. Cancer Biol. Ther. 2007, 6:1284-1288.
66. Hansen K.F., Sakamoto K., Wayman G.A., Impey S., Obrietan K. Transgenic miR132 alters neuronal spine density and impairs novel object recognition memory. PloS one 2010, e15497.
67. 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, 5:384-388.
68. Hashimoto Y., Akiyama Y., Otsubo T., Shimada S., Yuasa Y. Involvement of epigenetically silenced microRNA-181c in gastric carcinogenesis. Carcinogenesis 2010, 31:777-784.
69. Hawkes C. Olfaction in neurodegenerative disorder. Adv. Otorhinolaryngo. 2006, 63:133-151.
70. He L., He X., Lim L.P., de Stanchina E., Xuan Z., Liang Y., Xue W., Zender L., Magnus J., Ridzon D., Jackson A.L., Linsley P.S., Chen C., Lowe S.W., Cleary M.A., Hannon G.J. AmicroRNA component of the p53 tumour suppressor network. Nature 2007, 447:1130-1134.
71. He S., Wang F., Yang L., Guo C., Wan R., Ke A., Xu L., Hu G., Xu X., Shen J., Wang X. Expression of DNMT1 and DNMT3a are regulated by GLI1 in human pancreatic cancer. PloS one 2011, 6:e27684.
72. Hebert S.S., De Strooper B. Molecular biology. miRNAs in neurodegeneration. Science 2007, 317:1179-1180.
73. Hebert S.S., Horre K., Nicolai L., Bergmans B., Papadopoulou A.S., Delacourte A., De Strooper B. MicroRNA regulation of Alzheimer's amyloid precursor protein expression. Neurobiol. Dis. 2009, 33:422-428.
74. Hebert S.S., Horre K., Nicolai L., Papadopoulou A.S., Mandemakers W., Silahtaroglu A.N., Kauppinen S., Delacourte A., De Strooper B. Loss of microRNA cluster miR-29a/b-1 in sporadic Alzheimer's disease correlates with increased BACE1/beta-secretase expression. Proc. Natl. Acad. Sci. U.S.A 2008, 105:6415-6420.
75. Hennessy E.J., Sheedy F.J., Santamaria D., Barbacid M., O'Neill L.A. Toll-like receptor-4 (TLR4) down-regulates microRNA-107, increasing macrophage adhesion via cyclin-dependent kinase 6. J.Biol. Chem. 2011, 286:25531-25539.
76. Hernandez P., Lee G., Sjoberg M., Maccioni R.B. Tau phosphorylation by cdk5 and fyn in response to amyloid peptide abeta (25-35): involvement of lipid rafts. J.Alzheimers Dis. 2009, 16:149-156.
77. Hildebrandt M.A., Gu J., Lin J., Ye Y., Tan W., Tamboli P., Wood C.G., Wu X. Hsa-miR-9 methylation status is associated with cancer development and metastatic recurrence in patients with clear cell renal cell carcinoma. Oncogene 2010, 29:5724-5728.
78. Holz-Schietinger C., Reich N.O. RNA modulation of the human DNA methyltransferase 3A. Nucleic Acids Res. 2012, 40:8550-8557.
79. Hooper C., Meimaridou E., Tavassoli M., Melino G., Lovestone S., Killick R. p53 is upregulated in Alzheimer's disease and induces tau phosphorylation in HEK293a cells. Neurosci. Lett. 2007, 418:34-37.
80. Hulf T., Sibbritt T., Wiklund E.D., Bert S., Strbenac D., Statham A.L., Robinson M.D., Clark S.J. Discovery pipeline for epigenetically deregulated miRNAs in cancer: integration of primary miRNA transcription. BMC genomics 2011, 12:54.
81. Incoronato M., Urso L., Portela A., Laukkanen M.O., Soini Y., Quintavalle C., Keller S., Esteller M., Condorelli G. Epigenetic regulation of miR-212 expression in lung cancer. PloS one 2011, 6:e27722.
82. Iorio M.V., Piovan C., Croce C.M. Interplay between microRNAs and the epigenetic machinery: an intricate network. Biochim. Biophys. Acta 2010, 1799:694-701.
83. Iyer A., Zurolo E., Prabowo A., Fluiter K., Spliet W.G., van Rijen P.C., Gorter J.A., Aronica E. MicroRNA-146a: a key regulator of astrocyte-mediated inflammatory response. PloS one 2012, 7:e44789.
84. Jeffries A.R., Perfect L.W., Ledderose J., Schalkwyk L.C., Bray N.J., Mill J., Price J. Stochastic choice of allelic expression in human neural stem cells. Stem Cells 2012, 30:1938-1947.
85. Jeffries C.D., Fried H.M., Perkins D.O. Nuclear and cytoplasmic localization of neural stem cell microRNAs. RNA 2011, 17:675-686.
86. Jiang M., Xiang Y., Wang D., Gao J., Liu D., Liu Y., Liu S., Zheng D. Dysregulated expression of miR-146a contributes to age-related dysfunction of macrophages. Aging Cell 2012, 11:29-40.
87. Jobe E.M., McQuate A.L., Zhao X. Crosstalk among epigenetic pathways regulates neurogenesis. Front. Neurosci. 2012, 6:59.
88. Jorgensen H.F., Ben-Porath I., Bird A.P. Mbd1 is recruited to both methylated and nonmethylated CpGs via distinct DNA binding domains. Mol. Cell. Biol. 2004, 24:3387-3395.
89. Jung Y.H., Gupta M.K., Shin J.Y., Uhm S.J., Lee H.T. MicroRNA signature in testes-derived male germ-line stem cells. Mol. Hum. Reprod. 2010, 16:804-810.
90. Karres J.S., Hilgers V., Carrera I., Treisman J., Cohen S.M. The conserved microRNA miR-8 tunes atrophin levels to prevent neurodegeneration in Drosophila. Cell 2007, 131:136-145.
91. Kawashima H., Numakawa T., Kumamaru E., Adachi N., Mizuno H., Ninomiya M., Kunugi H., Hashido K. Glucocorticoid attenuates brain-derived neurotrophic factor-dependent upregulation of glutamate receptors via the suppression of microRNA-132 expression. Neuroscience 2010, 165:1301-1311.
92. Kim V.N., Nam J.W. Genomics of microRNA. Trends Genet. 2006, 22:165-173.
93. 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.
94. Kong D., Heath E., Chen W., Cher M.L., Powell I., Heilbrun L., Li Y., Ali S., Sethi S., Hassan O., Hwang C., Gupta N., Chitale D., Sakr W.A., Menon M., Sarkar F.H. Loss of let-7 up-regulates EZH2 in prostate cancer consistent with the acquisition of cancer stem cell signatures that are attenuated by BR-DIM. PloS one 2012, 7:e33729.
95. Kozaki K., Imoto I., Mogi S., Omura K., Inazawa J. Exploration of tumor-suppressive microRNAs silenced by DNA hypermethylation in oral cancer. Cancer Res. 2008, 68:2094-2105.
96. Krichevsky A.M., King K.S., Donahue C.P., Khrapko K., Kosik K.S. AmicroRNA array reveals extensive regulation of microRNAs during brain development. RNA 2003, 9:1274-1281.
97. Krol J., Busskamp V., Markiewicz I., Stadler M.B., Ribi S., Richter J., Duebel J., Bicker S., Fehling H.J., Schubeler D., Oertner T.G., Schratt G., Bibel M., Roska B., Filipowicz W. Characterizing light-regulated retinal microRNAs reveals rapid turnover as a common property of neuronal microRNAs. Cell 2010, 141:618-631.
98. Kumamoto K., Spillare E.A., Fujita K., Horikawa I., Yamashita T., Appella E., Nagashima M., Takenoshita S., Yokota J., Harris C.C. Nutlin-3a activates p53 to both down-regulate inhibitor of growth 2 and up-regulate mir-34a, mir-34b, and mir-34c expression, and induce senescence. Cancer Res. 2008, 68:3193-3203.
99. Kurosawa K., Sasaki H., Sato Y., Yamanaka M., Shimizu M., Ito Y., Okuyama T., Matsuo M., Imaizumi K., Kuroki Y., Nishimura G. Paternal UPD14 is responsible for a distinctive malformation complex. Am. J. Med. Genet. 2002, 110:268-272.
100. Lambert T.J., Storm D.R., Sullivan J.M. MicroRNA132 modulates short-term synaptic plasticity but not basal release probability in hippocampal neurons. PloS one 2010, 5:e15182.
101. Landry C.D., Kandel E.R., Rajasethupathy P. New mechanisms in memory storage: piRNAs and epigenetics. Trends Neurosci. 2013, 36:535-542.
102. Le M.T., Xie H., Zhou B., Chia P.H., Rizk P., Um M., Udolph G., Yang H., Lim B., Lodish H.F. MicroRNA-125b promotes neuronal differentiation in human cells by repressing multiple targets. Mol. Cell. Biol. 2009, 29:5290-5305.
103. Lee K.H., Lotterman C., Karikari C., Omura N., Feldmann G., Habbe N., Goggins M.G., Mendell J.T., Maitra A. Epigenetic silencing of microRNA miR-107 regulates cyclin-dependent kinase 6 expression in pancreatic cancer. Pancreatology 2009, 9:293-301.
104. Lee R.C., Feinbaum R.L., Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 843-854.
105. Lee S.T., Chu K., Jung K.H., Yoon H.J., Jeon D., Kang K.M., Park K.H., Bae E.K., Kim M., Lee S.K., Roh J.K. MicroRNAs induced during ischemic preconditioning. Stroke 2010, 75:1646-1651.
106. Lee Y.S., Kim H.K., Chung S., Kim K.S., Dutta A. Depletion of human micro-RNA miR-125b reveals that it is critical for the proliferation of differentiated cells but not for the down-regulation of putative targets during differentiation. J.Biol. Chem. 2005, 280:16635-16641.
107. Legesse-Miller A., Elemento O., Pfau S.J., Forman J.J., Tavazoie S., Coller H.A. let-7 Overexpression leads to an increased fraction of cells in G2/M, direct down-regulation of Cdc34, and stabilization of Wee1 kinase in primary fibroblasts. J.Biol. Chem. 2009, 284:6605-6609.
108. Lehmann S.M., Kruger C., Park B., Derkow K., Rosenberger K., Baumgart J., Trimbuch T., Eom G., Hinz M., Kaul D., Habbel P., Kalin R., Franzoni E., Rybak A., Nguyen D., Veh R., Ninnemann O., Peters O., Nitsch R., Heppner F.L., Golenbock D., Schott E., Ploegh H.L., Wulczyn F.G., Lehnardt S. An unconventional role for miRNA: let-7 activates toll-like receptor 7 and causes neurodegeneration. Nat. Neurosci. 2012, 15:827-835.
109. Lehmann U., Hasemeier B., Christgen M., Muller M., Romermann D., Langer F., Kreipe H. Epigenetic inactivation of microRNA gene hsa-mir-9-1 in human breast cancer. J.Pathol. 2008, 214:17-24.
110. Letzen B.S., Liu C., Thakor N.V., Gearhart J.D., All A.H., Kerr C.L. MicroRNA expression profiling of oligodendrocyte differentiation from human embryonic stem cells. PloS one 2010, 5:e10480.
111. Li J., Harris R.A., Cheung S.W., Coarfa C., Jeong M., Goodell M.A., White L.D., Patel A., Kang S.H., Shaw C., Chinault A.C., Gambin T., Gambin A., Lupski J.R., Milosavljevic A. Genomic hypomethylation in the human germline associates with selective structural mutability in the human genome. PLoS Genet. 2012, 8:e1002692.
112. Li X., Zhang Y., Shi Y., Dong G., Liang J., Han Y., Wang X., Zhao Q., Ding J., Wu K., Fan D. MicroRNA-107, an oncogene microRNA that regulates tumour invasion and metastasis by targeting DICER1 in gastric cancer. J.Cell. Mol. Med. 2011, 15:1887-1895.
113. Li Y.Y., Cui J.G., Dua P., Pogue A.I., Bhattacharjee S., Lukiw W.J. Differential expression of miRNA-146a-regulated inflammatory genes in human primary neural, astroglial and microglial cells. Neurosci. Lett. 2011, 499:109-113.
114. Li Y.Y., Cui J.G., Hill J.M., Bhattacharjee S., Zhao Y., Lukiw W.J. Increased expression of miRNA-146a in Alzheimer's disease transgenic mouse models. Neurosci. Lett. 2011, 487:94-98.
115. Lindsay M.A. microRNAs and the immune response. Trends Immunol 2008, 29:343-351.
116. Liu C., Teng Z.Q., Santistevan N.J., Szulwach K.E., Guo W., Jin P., Zhao X. Epigenetic regulation of miR-184 by MBD1 governs neural stem cell proliferation and differentiation. Cell Stem Cell 2010, 6:433-444.
117. Liu S.J., Zhang A.H., Li H.L., Wang Q., Deng H.M., Netzer W.J., Xu H., Wang J.Z. Overactivation of glycogen synthase kinase-3 by inhibition of phosphoinositol-3 kinase and protein kinase C leads to hyperphosphorylation of tau and impairment of spatial memory. J. Neurochem. 2003, 87:1333-1344.
118. Lodygin D., Tarasov V., Epanchintsev A., Berking C., Knyazeva T., Korner H., Knyazev P., Diebold J., Hermeking H. Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell Cycle 2008, 7:2591-2600.
119. Luikart B.W., Bensen A.L., Washburn E.K., Perederiy J.V., Su K.G., Li Y., Kernie S.G., Parada L.F., Westbrook G.L. miR-132 mediates the integration of newborn neurons into the adult dentate gyrus. PloS one 2011, 6:e19077.
120. Lujambio A., Calin G.A., Villanueva A., Ropero S., Sanchez-Cespedes M., Blanco D., Montuenga L.M., Rossi S., Nicoloso M.S., Faller W.J., Gallagher W.M., Eccles S.A., Croce C.M., Esteller M. AmicroRNA DNA methylation signature for human cancer metastasis. Proc. Natl. Acad. Sci. U.S.A 2008, 13556-13561.
121. Lujambio A., Ropero S., Ballestar E., Fraga M.F., Cerrato C., Setien F., Casado S., Suarez-Gauthier A., Sanchez-Cespedes M., Git A., Spiteri I., Das P.P., Caldas C., Miska E., Esteller M. Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Res. 2007, 105:1424-1429.
122. Lukiw W.J. Micro-RNA speciation in fetal, adult and Alzheimer's disease hippocampus. Neuroreport 2007, 18:297-300.
123. Lukiw W.J., Zhao Y., Cui J.G. An NF-kappaB-sensitive micro RNA-146a-mediated inflammatory circuit in Alzheimer disease and in stressed human brain cells. J.Biol. Chem. 2008, 283:31315-31322.
124. 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.
125. Makeyev E.V., Zhang J., Carrasco M.A., Maniatis T. The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell 2007, 27:435-448.
126. Maki Y., Asano H., Toyooka S., Soh J., Kubo T., Katsui K., Ueno T., Shien K., Muraoka T., Tanaka N., Yamamoto H., Tsukuda K., Kishimoto T., Kanazawa S., Miyoshi S. MicroRNA miR-34b/c enhances cellular radiosensitivity of malignant pleural mesothelioma cells. Anticancer Res. 2012, 32:4871-4875.
127. Mastroeni D., Grover A., Delvaux E., Whiteside C., Coleman P.D., Rogers J. Epigenetic changes in Alzheimer's disease: decrements in DNA methylation. Neurobiol. Aging 2010, 31:2025-2037.
128. Mastroeni D., Grover A., Delvaux E., Whiteside C., Coleman P.D., Rogers J. Epigenetic mechanisms in Alzheimer's disease. Neurobiol. Aging 2011, 32:1161-1180.
129. Mazar J., Khaitan D., DeBlasio D., Zhong C., Govindarajan S.S., Kopanathi S., Zhang S., Ray A., Perera R.J. Epigenetic regulation of microRNA genes and the role of miR-34b in cell invasion and motility in human melanoma. PloS one 2011, 6:e24922.
130. 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.
131. 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 Noble F., Rajewsky N. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 2013, 495:333-338.
132. Migliore C., Petrelli A., Ghiso E., Corso S., Capparuccia L., Eramo A., Comoglio P.M., Giordano S. MicroRNAs impair MET-mediated invasive growth. Cancer Res. 2008, 68:10128-10136.
133. Mizrak A., Senol O., Ozdener G.B., Saydam O. Tumors of the central nervous system. Meningiomas and Schwannomas: Springer Link 2012, 59-67. M.A. Hayat (Ed.).
134. Moloney A.M., Griffin R.J., Timmons S., O'Connor R., Ravid R., O'Neill C. Defects in IGF-1 receptor, insulin receptor and IRS-1/2 in Alzheimer's disease indicate possible resistance to IGF-1 and insulin signalling. Neurobiol. Aging 2010, 31:224-243.
135. Moncini S., Salvi A., Zuccotti P., Viero G., Quattrone A., Barlati S., De Petro G., Venturin M., Riva P. The role of miR-103 and miR-107 in regulation of CDK5R1 expression and in cellular migration. PloS one 2011, 6:e20038.
136. Morrione A., Navarro M., Romano G., Dews M., Reiss K., Valentinis B., Belletti B., Baserga R. The role of the insulin receptor substrate-1 in the differentiation of rat hippocampal neuronal cells. Oncogene 2001, 20:4842-4852.
137. Moss E.G., Lee R.C., Ambros V. The cold shock domain protein LIN-28 controls developmental timing in C. elegans and is regulated by the lin-4 RNA. Cell 1997, 88:637-646.
138. Mourelatos Z., Dostie J., Paushkin S., Sharma A., Charroux B., Abel L., Rappsilber J., Mann M., Dreyfuss G. miRNPs: a novel class of ribonucleoproteins containing numerous microRNAs. Genes Dev. 2002, 16:720-728.
139. Mu Y., Gage F.H. Adult hippocampal neurogenesis and its role in Alzheimer's disease. Mol Neurodegener. 2011, 6:85.
140. Nan X., Ng H.H., Johnson C.A., Laherty C.D., Turner B.M., Eisenman R.N., Bird A. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998, 393:386-389.
141. Nelson P.T., Wang W.X. MiR-107 is reduced in Alzheimer's disease brain neocortex: validation study. J.Alzheimer's Dis. 2010, 21:75-79.
142. Neves R., Scheel C., Weinhold S., Honisch E., Iwaniuk K.M., Trompeter H.I., Niederacher D., Wernet P., Santourlidis S., Uhrberg M. Role of DNA methylation in miR-200c/141 cluster silencing in invasive breast cancer cells. BMC Res. Notes 2010, 3:219.
143. Nishi M., Eguchi-Ishimae M., Wu Z., Gao W., Iwabuki H., Kawakami S., Tauchi H., Inukai T., Sugita K., Hamasaki Y., Ishii E., Eguchi M. Suppression of the let-7b microRNA pathway by DNA hypermethylation in infant acute lymphoblastic leukemia with MLL gene rearrangements. Leukemia 2012, 27:389-397.
144. Nishino J., Kim I., Chada K., Morrison S.J. Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf Expression. Cell 2008, 135:227-239.
145. Nissan X., Blondel S., Navarro C., Maury Y., Denis C., Girard M., Martinat C., De Sandre-Giovannoli A., Levy N., Peschanski M. Unique preservation of neural cells in Hutchinson- Gilford progeria syndrome is due to the expression of the neural-specific miR-9 microRNA. Cell Rep. 2012, 2:1-9.
146. Nomura T., Kimura M., Horii T., Morita S., Soejima H., Kudo S., Hatada I. MeCP2-dependent repression of an imprinted miR-184 released by depolarization. Hum. Mol. Genet. 2008, 17:1192-1199.
147. 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, invivo. Hippocampus 2010, 20:492-498.
148. Numakawa T., Yamamoto N., Chiba S., Richards M., Ooshima Y., Kishi S., Hashido K., Adachi N., Kunugi H. Growth factors stimulate expression of neuronal and glial miR-132. Neurosci. Lett. 2011, 505:242-247.
149. O'Donnell K.A., Wentzel E.A., Zeller K.I., Dang C.V., Mendell J.T. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 2005, 839-843.
150. O'Hagan H.M., Mohammad H.P., Baylin S.B. Double strand breaks can initiate gene silencing and SIRT1-dependent onset of DNA methylation in an exogenous promoter CpG island. PLoS Genet. 2008, 4:e1000155.
151. O'Neill J.S., Hastings M.H. Circadian clocks: timely interference by microRNAs. Curr. Biol. 2007, 17:R760-R762.
152. Olde Loohuis N.F., Kos A., Martens G.J., Van Bokhoven H., Nadif Kasri N., Aschrafi A. MicroRNA networks direct neuronal development and plasticity. Cell. Mol. Life Sci. 2012, 69:89-102.
153. Omura N., Li C.P., Li A., Hong S.M., Walter K., Jimeno A., Hidalgo M., Goggins M. Genome-wide profiling of methylated promoters in pancreatic adenocarcinoma. Cancer Biol. Ther. 2008, 7:1146-1156.
154. Packer A.N., Xing Y., Harper S.Q., Jones L., Davidson B.L. The bifunctional microRNA miR-9/miR-9* regulates REST and CoREST and is downregulated in Huntington's disease. J.Neurosci. 2008, 28:14341-14346.
155. Paradis E., Douillard H., Koutroumanis M., Goodyer C., LeBlanc A. Amyloid beta peptide of Alzheimer's disease downregulates Bcl-2 and upregulates bax expression in human neurons. J.Neurosci. 1996, 16:7533-7539.
156. Park S.M., Gaur A.B., Lengyel E., Peter M.E. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 2008, 22:894-907.
157. Pathania M., Torres-Reveron J., Yan L., Kimura T., Lin T.V., Gordon V., Teng Z.Q., Zhao X., Fulga T.A., Van Vactor D., Bordey A. miR-132 enhances dendritic morphogenesis, spine density, synaptic integration, and survival of newborn olfactory bulb neurons. PloS one 2012, 7:e38174.
158. Peters A.H., Mermoud J.E., O'Carroll D., Pagani M., Schweizer D., Brockdorff N., Jenuwein T. Histone H3 lysine 9 methylation is an epigenetic imprint of facultative heterochromatin. Nat. Genet. 2002, 30:77-80.
159. Peters J., Robson J.E. Imprinted noncoding RNAs. Mamm. Genome 2008, 19:493-502.
160. Pigazzi M., Manara E., Baron E., Basso G. miR-34b targets cyclic AMP-responsive element binding protein in acute myeloid leukemia. Cancer Res. 2009, 69:2471-2478.
161. Pogribny I.P., Shpyleva S.I., Muskhelishvili L., Bagnyukova T.V., James S.J., Beland F.A. Role of DNA damage and alterations in cytosine DNA methylation in rat liver carcinogenesis induced by a methyl-deficient diet. Mutat. Res. 2009, 669:56-62.
162. Pogue A.I., Cui J.G., Li Y.Y., Zhao Y., Culicchia F., Lukiw W.J. Micro RNA-125b (miRNA-125b) function in astrogliosis and glial cell proliferation. Neurosci. Lett. 2010, 476:18-22.
163. Pogue A.I., Percy M.E., Cui J.G., Li Y.Y., Bhattacharjee S., Hill J.M., Kruck T.P., Zhao Y., Lukiw W.J. Up-regulation of NF-kB-sensitive miRNA-125b and miRNA-146a in metal sulfate-stressed human astroglial (HAG) primary cell cultures. J.Inorg. Biochem. 2011, 105:1434-1437.
164. Ponomarev E.D., Veremeyko T., Barteneva N., Krichevsky A.M., Weiner H.L. MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-alpha-PU.1 pathway. Nat. Med. 2011, 17:64-70.
165. Rajasethupathy P., Fiumara F., Sheridan R., Betel D., Puthanveettil S.V., Russo J.J., Sander C., Tuschl T., Kandel E. Characterization of small RNAs in Aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB. Neuron 2009, 63:803-817.
166. Remenyi J., Hunter C.J., Cole C., Ando H., Impey S., Monk C.E., Martin K.J., Barton G.J., Hutvagner G., Arthur J.S. Regulation of the miR-212/132 locus by MSK1 and CREB in response to neurotrophins. Biochem. J. 2010, 428:281-291.
167. Rio P., Agirre X., Garate L., Banos R., Alvarez L., San Jose-Eneriz E., Badell I., Casado J.A., Garin M., Prosper F., Bueren J.A. Down-regulated expression of hsa-miR-181c in Fanconi anemia patients: implications in TNFalpha regulation and proliferation of hematopoietic progenitor cells. Blood 2012, 119:3042-3049.
168. Rodriguez-Otero P., Roman-Gomez J., Vilas-Zornoza A., Jose-Eneriz E.S., Martin-Palanco V., Rifon J., Torres A., Calasanz M.J., Agirre X., Prosper F. Deregulation of FGFR1 and CDK6 oncogenic pathways in acute lymphoblastic leukaemia harbouring epigenetic modifications of the MIR9 family. Br. J. Haematol. 2011, 155:73-83.
169. Rotkrua P., Akiyama Y., Hashimoto Y., Otsubo T., Yuasa Y. MiR-9 downregulates CDX2 expression in gastric cancer cells. Int. J. Cancer 2011, 129:2611-2620.
170. Royo H., Cavaille J. Non-coding RNAs in imprinted gene clusters. Biol. Cell 2008, 100:149-166.
171. Ruegger S., Grosshans H. MicroRNA turnover: when, how, and why. Trends Biochem. Sci. 2012, 37:436-446.
172. Saba R., Goodman C.D., Huzarewich R.L., Robertson C., Booth S.A. AmiRNA signature of prion induced neurodegeneration. PloS one 2008, 3:e3652.
173. Saito Y., Saito H. MicroRNAs in cancers and neurodegenerative disorders. Front Genet. 2012, 3:194.
174. Saito Y., Suzuki H., Tsugawa H., Nakagawa I., Matsuzaki J., Kanai Y., Hibi T. Chromatin remodeling at Alu repeats by epigenetic treatment activates silenced microRNA-512-5p with downregulation of Mcl-1 in human gastric cancer cells. Oncogene 2009, 28:2738-2744.
175. Salta E., De Strooper B. Non-coding RNAs with essential roles in neurodegenerative disorders. Lancet Neurol. 2012, 11:189-200.
176. Sato F., Tsuchiya S., Meltzer S.J., Shimizu K. MicroRNAs and epigenetics. FEBS J. 2011, 278:1598-1609.
177. Schipper H.M., Maes O.C., Chertkow H.M., Wang E. MicroRNA expression in Alzheimer blood mononuclear cells. Gene. Regul. Syst. Bio. 2007, 1:263-274.
178. Schonrock N., Gotz J. Decoding the non-coding RNAs in Alzheimer's disease. Cell. Mol. Life Sci. 2012, 69:3543-3559.
179. Schonrock N., Humphreys D.T., Preiss T., Gotz J. Target gene repression mediated by miRNAs miR-181c and miR-9 both of which are down-regulated by amyloid-beta. J.Mol. Neurosci. 2012, 46:324-335.
180. Schonrock N., Ke Y.D., Humphreys D., Staufenbiel M., Ittner L.M., Preiss T., Gotz J. Neuronal microRNA deregulation in response to Alzheimer's disease amyloid-beta. PloS one 2010, 5:e11070.
181. Schonrock N., Matamales M., Ittner L.M., Gotz J. MicroRNA networks surrounding APP and amyloid-beta metabolism-implications for Alzheimer's disease. Exp. Neurol. 2012, 235:447-454.
182. Schouten M., Aschrafi A., Bielefeld P., Doxakis E., Fitzsimons C.P. microRNAs and the regulation of neuronal plasticity under stress conditions. Neurosci. 2013, 241:188-205.
183. Schouten M., Buijink M.R., Lucassen P.J., Fitzsimons C.P. New neurons in aging brains: molecular control by small non-coding RNAs. Front. Neurosci. 2012, 6:25.
184. Schratt G.M., Tuebing F., Nigh E.A., Kane C.G., Sabatini M.E., Kiebler M., Greenberg M.E. Abrain-specific microRNA regulates dendritic spine development. Nature 2006, 439:283-289.
185. Schultz J., Lorenz P., Gross G., Ibrahim S., Kunz M. MicroRNA let-7b targets important cell cycle molecules in malignant melanoma cells and interferes with anchorage-independent growth. Cell Res. 2008, 18:549-557.
186. Scott G.K., Mattie M.D., Berger C.E., Benz S.C., Benz C.C. Rapid alteration of microRNA levels by histone deacetylase inhibition. Cancer Res. 2006, 66:1277-1281.
187. Senyuk V., Zhang Y., Liu Y., Ming M., Premanand K., Zhou L., Chen P., Chen J., Rowley J.D., Nucifora G., Qian Z. Critical role of miR-9 in myelopoiesis and EVI1-induced leukemogenesis. Proc. Natl. Acad. Sci. U.S.A 2013, 110:5594-5599.
188. Sethi P., Lukiw W.J. Micro-RNA abundance and stability in human brain: specific alterations in Alzheimer's disease temporal lobe neocortex. Neurosci. Lett. 2009, 459:100-104.
189. Shaked I., Meerson A., Wolf Y., Avni R., Greenberg D., Gilboa-Geffen A., Soreq H. MicroRNA-132 potentiates cholinergic anti-inflammatory signaling by targeting acetylcholinesterase. Immunity 2009, 31:965-973.
190. Silber J., Lim D.A., Petritsch C., Persson A.I., Maunakea A.K., Yu M., Vandenberg S.R., Ginzinger D.G., James C.D., Costello J.F., Bergers G., Weiss W.A., Alvarez-Buylla A., Hodgson J.G. miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC Med. 2008, 6:14.
191. Sleegers K., Brouwers N., Van Broeckhoven C. Role of progranulin as a biomarker for Alzheimer's disease. Biomark. Med. 2010, 4:37-50.
192. Smith P., Al Hashimi A., Girard J., Delay C., Hebert S.S. Invivo regulation of amyloid precursor protein neuronal splicing by microRNAs. J.Neurochem. 2011, 116:240-247.
193. Smrt R.D., Szulwach K.E., Pfeiffer R.L., Li X., Guo W., Pathania M., Teng Z.Q., Luo Y., Peng J., Bordey A., Jin P., Zhao X. MicroRNA miR-137 regulates neuronal maturation by targeting ubiquitin ligase mind bomb-1. Stem Cells 2010, 28:1060-1070.
194. Soreq H., Wolf Y. NeurimmiRs: microRNAs in the neuroimmune interface. Trends Mol. Med. 2011, 17:548-555.
195. Stappert L., Borghese L., Roese-Koerner B., Weinhold S., Koch P., Terstegge S., Uhrberg M., Wernet P., Brustle O. MicroRNA-based promotion of human neuronal differentiation and subtype specification. PloS one 2013, 8:e59011.
196. Strum J.C., Johnson J.H., Ward J., Xie H., Feild J., Hester A., Alford A., Waters K.M. MicroRNA 132 regulates nutritional stress-induced chemokine production through repression of SirT1. Mol. Endocrinol. 2009, 23:1876-1884.
197. Su J., Zhang A., Shi Z., Ma F., Pu P., Wang T., Zhang J., Kang C., Zhang Q. MicroRNA-200a suppresses the Wnt/beta-catenin signaling pathway by interacting with beta-catenin. Int. J. Oncol. 2012, 40:1162-1170.
198. Sun A.X., Crabtree G.R., Yoo A.S. MicroRNAs: regulators of neuronal fate. Curr. Opin. Cell Biol. 2013, 25:215-221.
199. Sun F., Fu H., Liu Q., Tie Y., Zhu J., Xing R., Sun Z., Zheng X. Downregulation of CCND1 and CDK6 by miR-34a induces cell cycle arrest. FEBS Lett. 2008, 582:1564-1568.
200. Sun G., Ye P., Murai K., Lang M.F., Li S., Zhang H., Li W., Fu C., Yin J., Wang A., Ma X., Shi Y. miR-137 forms a regulatory loop with nuclear receptor TLX and LSD1 in neural stem cells. Nat. Commun. 2011, 2:529.
201. Suzuki H., Maruyama R., Yamamoto E., Kai M. DNA methylation and microRNA dysregulation in cancer. Mol. Oncol. 2012, 6:567-578.
202. Suzuki H., Yamamoto E., Nojima M., Kai M., Yamano H.O., Yoshikawa K., Kimura T., Kudo T., Harada E., Sugai T., Takamaru H., Niinuma T., Maruyama R., Yamamoto H., Tokino T., Imai K., Toyota M., Shinomura Y. Methylation-associated silencing of microRNA-34b/c in gastric cancer and its involvement in an epigenetic field defect. Carcinogenesis 2010, 31:2066-2073.
203. Sytnikova Y.A., Kubarenko A.V., Schafer A., Weber A.N., Niehrs C. Gadd45a is an RNA binding protein and is localized in nuclear speckles. PloS one 2011, 6:e14500.
204. Szenthe K., Koroknai A., Banati F., Bathori Z., Lozsa R., Burgyan J., Wolf H., Salamon D., Nagy K., Niller H.H., Minarovits J. The 5' regulatory sequences of active miR-146a promoters are hypomethylated and associated with euchromatic histone modification marks in B lymphoid cells. Biochem. Biophys. Res. Commun. 2013, 433:489-495.
205. Szulwach K.E., Li X., Smrt R.D., Li Y., Luo Y., Lin L., Santistevan N.J., Li W., Zhao X., Jin P. Cross talk between microRNA and epigenetic regulation in adult neurogenesis. J.Cell Biol. 2010, 189:127-141.
206. Taganov K.D., Boldin M.P., Chang K.J., Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. U.S.A 2006, 103:12481-12486.
207. Takahashi M., Cuatrecasas M., Balaguer F., Hur K., Toiyama Y., Castells A., Boland C.R., Goel A. The clinical significance of MiR-148a as a predictive biomarker in patients with advanced colorectal cancer. PloS one 2012, 7:e46684.
208. Takahashi Y., Satoh M., Minami Y., Tabuchi T., Itoh T., Nakamura M. Expression of miR-146a/b is associated with the toll-like receptor 4 signal in coronary artery disease: effect of renin-angiotensin system blockade and statins on miRNA-146a/b and toll-like receptor 4 levels. Clin. Sci. (Lond) 2010, 119:395-405.
209. Takashima A., Noguchi K., Michel G., Mercken M., Hoshi M., Ishiguro K., Imahori K. Exposure of rat hippocampal neurons to amyloid beta peptide (25-35) induces the inactivation of phosphatidyl inositol-3 kinase and the activation of tau protein kinase I/glycogen synthase kinase-3 beta. Neurosci. Lett. 1996, 203:33-36.
210. Tan K.B., Magdalene Koh H.K., Tan S.Y. Double immunofluorescence shows coexpression of Bcl-x with GFAP in a variety of glial lesions. J. Neurooncol. 2006, 80:235-242.
211. Teng G.G., Wang W.H., Dai Y., Wang S.J., Chu Y.X., Li J. Let-7b is involved in the inflammation and immune responses associated with Helicobacter pylori infection by targeting Toll-like receptor 4. PloS one 2013, 8:e56709.
212. Tognini P., Pizzorusso T. MicroRNA212/132 family: molecular transducer of neuronal function and plasticity. Int. J. Biochem. Cell Biol. 2012, 44:6-10.
213. Tognini P., Putignano E., Coatti A., Pizzorusso T. Experience-dependent expression of miR-132 regulates ocular dominance plasticity. Nat. Neurosci. 2011, 14:1237-1239.
214. Toyota M., Suzuki H., Sasaki Y., Maruyama R., Imai K., Shinomura Y., Tokino T. Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res. 2008, 68:4123-4132.
215. Tsai K.W., Liao Y.L., Wu C.W., Hu L.Y., Li S.C., Chan W.C., Ho M.R., Lai C.H., Kao H.W., Fang W.L., Huang K.H., Lin W.C. Aberrant hypermethylation of miR-9 genes in gastric cancer. Epigenetics 2011, 6:1189-1197.
216. Tycko B., Efstratiadis A. Genomic imprinting: piece of cake. Nature 2002, 417:913-914.
217. Visvanathan J., Lee S., Lee B., Lee J.W., Lee S.K. The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev. 2007, 21:744-749.
218. Vo N., Klein M.E., Varlamova O., Keller D.M., Yamamoto T., Goodman R.H., Impey S. AcAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc. Natl. Acad. Sci. U.S.A 2005, 102:16426-16431.
219. Vogt M., Munding J., Gruner M., Liffers S.T., Verdoodt B., Hauk J., Steinstraesser L., Tannapfel A., Hermeking H. Frequent concomitant inactivation of miR-34a and miR-34b/c by CpG methylation in colorectal, pancreatic, mammary, ovarian, urothelial, and renal cell carcinomas and soft tissue sarcomas. Virchows Arch. 2011, 458:313-322.
220. Vrba L., Jensen T.J., Garbe J.C., Heimark R.L., Cress A.E., Dickinson S., Stampfer M.R., Futscher B.W. Role for DNA methylation in the regulation of miR-200c and miR-141 expression in normal and cancer cells. PloS one 2010, 5:e8697.
221. Vreugdenhil E., Verissimo C.S., Mariman R., Kamphorst J.T., Barbosa J.S., Zweers T., Champagne D.L., Schouten T., Meijer O.C., de Kloet E.R., Fitzsimons C.P. MicroRNA 18 and 124a down-regulate the glucocorticoid receptor: implications for glucocorticoid responsiveness in the brain. Endocrinology 2009, 150:2220-2228.
222. Wada R., Akiyama Y., Hashimoto Y., Fukamachi H., Yuasa Y. miR-212 is downregulated and suppresses methyl-CpG-binding protein MeCP2 in human gastric cancer. Int. J. Cancer 2010, 127:1106-1114.
223. Wanet A., Tacheny A., Arnould T., Renard P. miR-212/132 expression and functions: within and beyond the neuronal compartment. Nucleic acids Res. 2012, 40:4742-4753.
224. Wang P., Chen L., Zhang J., Chen H., Fan J., Wang K., Luo J., Chen Z., Meng Z., Liu L. Methylation-mediated silencing of the miR-124 genes facilitates pancreatic cancer progression and metastasis by targeting Rac1. Oncogene 2013, 10.1038/onc.2012.598.
225. Wang R.Y., Phang R.Z., Hsu P.H., Wang W.H., Huang H.T., Liu I.Y. Invivo knockdown of hippocampal miR-132 expression impairs memory acquisition of trace fear conditioning. Hippocampus 2013, 23:625-633.
226. Wang W.X., Rajeev B.W., Stromberg A.J., Ren N., Tang G., Huang Q., Rigoutsos I., Nelson P.T. The expression of microRNA miR-107 decreases early in Alzheimer's disease and may accelerate disease progression through regulation of beta-site amyloid precursor protein-cleaving enzyme 1. J.Neurosci. 2008, 28:1213-1223.
227. Wang W.X., Wilfred B.R., Madathil S.K., Tang G., Hu Y., Dimayuga J., Stromberg A.J., Huang Q., Saatman K.E., Nelson P.T. miR-107 regulates granulin/progranulin with implications for traumatic brain injury and neurodegenerative disease. Am. J. Pathol. 2010, 177:334-345.
228. Wang X., Cao L., Wang Y., Liu N., You Y. Regulation of let-7 and its target oncogenes (Review). Oncol. Lett. 2012, 3:955-960.
229. Wang X., Liu P., Zhu H., Xu Y., Ma C., Dai X., Huang L., Liu Y., Zhang L., Qin C. miR-34a, a microRNA up-regulated in a double transgenic mouse model of Alzheimer's disease, inhibits bcl2 translation. Brain Res. Bull. 2009, 80:268-273.
230. Wassenegger M. RNA-directed DNA methylation. Plant Mol. Biol. 2000, 43:203-220.
231. Welch C., Chen Y., Stallings R.L. MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells. Oncogene 2007, 26:5017-5022.
232. Wightman B., Ha I., Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 1993, 75:855-862.
233. Wiklund E.D., Kjems J., Clark S.J. Epigenetic architecture and miRNA: reciprocal regulators. Epigenomics 2010, 2:823-840.
234. Wilkinson L.S., Davies W., Isles A.R. Genomic imprinting effects on brain development and function. Nat. Rev. Neurosci. 2007, 8:832-843.
235. Willemsen M.H., Valles A., Kirkels L.A., Mastebroek M., Olde Loohuis N., Kos A., Wissink-Lindhout W.M., de Brouwer A.P., Nillesen W.M., Pfundt R., Holder-Espinasse M., Vallee L., Andrieux J., Coppens-Hofman M.C., Rensen H., Hamel B.C., van Bokhoven H., Aschrafi A., Kleefstra T. Chromosome 1p21.3 microdeletions comprising DPYD and MIR137 are associated with intellectual disability. J.Med. Genet. 2011, 48:810-818.
236. Wilting S.M., van Boerdonk R.A., Henken F.E., Meijer C.J., Diosdado B., Meijer G.A., le Sage C., Agami R., Snijders P.J., Steenbergen R.D. Methylation-mediated silencing and tumour suppressive function of hsa-miR-124 in cervical cancer. Mol. Cancer 2010, 9:167.
237. Wong K.Y., So C.C., Loong F., Chung L.P., Lam W.W., Liang R., Li G.K., Jin D.Y., Chim C.S. Epigenetic inactivation of the miR-124-1 in haematological malignancies. PloS one 2011, 6:e19027.
238. Wong K.Y., Yu L., Chim C.S. DNA methylation of tumor suppressormiRNA genes: a lesson from the miR-34 family. Epigenomics 2011, 3:83-92.
239. Wood M.A., Kaplan M.P., Park A., Blanchard E.J., Oliveira A.M., Lombardi T.L., Abel T. Transgenic mice expressing a truncated form of CREB-binding protein (CBP) exhibit deficits in hippocampal synaptic plasticity and memory storage. Learn Mem 2005, 12:111-119.
240. Wu H., Coskun V., Tao J., Xie W., Ge W., Yoshikawa K., Li E., Zhang Y., Sun Y.E. Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 2010, 329:444-448.
241. Wu L., Zhou H., Zhang Q., Zhang J., Ni F., Liu C., Qi Y. DNA methylation mediated by a microRNA pathway. Mol. Cell 2010, 38:465-475.
242. Xie Q., Chen X., Lu F., Zhang T., Hao M., Wang Y., Zhao J., McCrae M.A., Zhuang H. Aberrant expression of microRNA 155 may accelerate cell proliferation by targeting sex-determining region Y box 6 in hepatocellular carcinoma. Cancer 2012, 118:2431-2442.
243. Xu L., Wang F., Xu X.F., Mo W.H., Xia Y.J., Wan R., Wang X.P., Guo C.Y. Down-regulation of miR-212 expression by DNA hypermethylation in human gastric cancer cells. Med. Oncol. 2011, 28:S189-S196.
244. Xu Q., Jiang Y., Yin Y., Li Q., He J., Jing Y., Qi Y.T., Li W., Lu B., Peiper S.S., Jiang B.H., Liu L.Z. Aregulatory circuit of miR-148a/152 and DNMT1 in modulating cell transformation and tumor angiogenesis through IGF-IR and IRS1. J.Mol. Cell. Biol. 2012, 5:3-13.
245. Yamakuchi M., Ferlito M., Lowenstein C.J. miR-34a repression of SIRT1 regulates apoptosis. Proc. Natl. Acad. Sci. U.S.A 2008, 105:13421-13426.
246. Yan H., Choi A.J., Lee B.H., Ting A.H. Identification and functional analysis of epigenetically silenced microRNAs in colorectal cancer cells. PloS one 2011, 6:e20628.
247. Yang D., Li T., Wang Y., Tang Y., Cui H., Zhang X., Chen D., Shen N., Le W. miR-132 regulates the differentiation of dopamine neurons by directly targeting Nurr1 expression. J.Cell Sci. 2012, 125(Pt 7):1673-1682.
248. Yao J., Hennessey T., Flynt A., Lai E., Beal M.F., Lin M.T. MicroRNA-related cofilin abnormality in Alzheimer's disease. PloS one 2010, 5:e15546.
249. Yin H., Lin H. An epigenetic activation role of piwi and a piwi-associated piRNA in Drosophila melanogaster. Nature 2007, 450:304-308.
250. Zhang L., Dong L.Y., Li Y.J., Hong Z., Wei W.S. The microRNA miR-181c controls microglia-mediated neuronal apoptosis by suppressing tumor necrosis factor. J.Neuroinflammation 2012, 9:211.
251. Zhang Y., Yan L.X., Wu Q.N., Du Z.M., Chen J., Liao D.Z., Huang M.Y., Hou J.H., Wu Q.L., Zeng M.S., Huang W.L., Zeng Y.X., Shao J.Y. miR-125b is methylated and functions as a tumor suppressor by regulating the ETS1 proto-oncogene in human invasive breast cancer. Cancer Res. 2011, 71:3552-3562.
252. Zhao C., Sun G., Li S., Shi Y. Afeedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination. Nat. Struct. Mol. Biol. 2009, 16:365-371.
253. Zhu A., Xia J., Zuo J., Jin S., Zhou H., Yao L., Huang H., Han Z. MicroRNA-148a is silenced by hypermethylation and interacts with DNA methyltransferase 1 in gastric cancer. Med. Oncol. 2012, 29:2701-2709.
254. Zovoilis A., Agbemenyah H.Y., Agis-Balboa R.C., Stilling R.M., Edbauer D., Rao P., Farinelli L., Delalle I., Schmitt A., Falkai P., Bahari-Javan S., Burkhardt S., Sananbenesi F., Fischer A. microRNA-34c is a novel target to treat dementias. EMBO J. 2011, 30:4299-4308.