microRNAs: Tiny regulators of synapse function in development and disease

Journal of Cellular and Molecular Medicine

Volumn 12, Issue 5A, 2008, Pages 1466-1476

  Bicker, Silvia ^a   Schratt, Gerhard ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Dendritic spine; microRNA; Nervous system; Neurologic disease; Neuron; Plasticity; Synapse

Indexed keywords

MICRORNA;

ANIMAL; DENDRITE; GENE EXPRESSION REGULATION; GENERAL ASPECTS OF DISEASE; GENETICS; HUMAN; METABOLISM; REVIEW; SYNAPSE; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; DENDRITES; DISEASE; GENE EXPRESSION REGULATION; HUMANS; MICRORNAS; SYNAPSES;

VERTEBRATA;

EID: 54049150793     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2008.00400.x     Document Type: Review

References (106)

1. Valencia-Sanchez MA, Liu J, Hannon GJ, Parker R. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev. 2006 20 : 515 24.
2. Bartel D P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004 116 : 281 97.
3. Ambros V. The functions of animal microRNAs. Nature. 2004 431 : 350 5.
4. Brennecke J, Hipfner DR, Stark A, Russell RB, Cohen SM. bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell. 2003 113 : 25 36.
5. Chen CZ, Li L, Lodish HF, Bartel D P. MicroRNAs modulate hematopoietic lineage differentiation. Science. 2004 303 : 83 6.
6. Kloosterman WP, Plasterk RH. The diverse functions of microRNAs in animal development and disease. Dev Cell. 2006 11 : 441 50.
7. Poy MN, Eliasson L, Krutzfeldt J, Kuwajima S, Ma X, Macdonald PE, Pfeffer S, Tuschl T, Rajewsky N, Rorsman P, Stoffel M. A pancreatic islet-specific microRNA regulates insulin secretion. Nature. 2004 432 : 226 30.
8. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN. MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 2004 23 : 4051 60.
9. Borchert GM, Lanier W, Davidson BL. RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol. 2006 13 : 1097 101.
10. Denli AM, Tops BB, Plasterk RH, Ketting RF, Hannon GJ. Processing of primary microRNAs by the Microprocessor complex. Nature. 2004 432 : 231 5.
11. Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, Shiekhattar R. The Microprocessor complex mediates the genesis of microRNAs. Nature. 2004 432 : 235 40.
12. Han J, Lee Y, Yeom KH, Kim YK, Jin H, Kim VN. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev. 2004 18 : 3016 27.
13. Bernstein E, Caudy AA, Hammond SM, Hannon GJ. Role for a bidentate ribonucle-ase in the initiation step of RNA interference. Nature. 2001 409 : 363 6.
14. Lee Y, Jeon K, Lee JT, Kim S, Kim VN. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J. 2002 21 : 4663 70.
15. Kim VN, Nam JW. Genomics of microRNA. Trends Genet. 2006 22 : 165 73.
16. Schwarz DS, Hutvagner G, Du T, Xu Z, Aronin N, Zamore PD. Asymmetry in the assembly of the RNAi enzyme complex. Cell. 2003 115 : 199 208.
17. Du T, Zamore PD. microPrimer: the biogenesis and function of microRNA. Development. 2005 132 : 4645 52.
18. Khvorova A, Reynolds A, Jayasena SD. Functional siRNAs and miRNAs exhibit strand bias. Cell. 2003 115 : 209 16.
19. Pillai RS. MicroRNA function: multiple mechanisms for a tiny RNA? RNA. 2005 11 : 1753 61.
20. Jones-Rhoades MW, Bartel DP, Bartel B. MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol. 2006 57 : 19 53.
21. Tang G. siRNA and miRNA: an insight into RISCs. Trends Biochem Sci. 2005 30 : 106 14.
22. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W. Relief of microRNA-mediated transla-tional repression in human cells subjected to stress. Cell. 2006 125 : 1111 24.
23. Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME, Kiebler M, Greenberg ME. A brain-specific microRNA regulates dendritic spine development. Nature. 2006 439 : 283 9.
24. Vasudevan S, Tong Y, Steitz JA. Switching from repression to activation: microRNAs can up-regulate translation. Science. 2007 318 : 1931 4.
25. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-tran-scriptional regulation by microRNAs: are the answers in sight Nat Rev Genet. 2008 9 : 102 14.
26. Nilsen TW. Mechanisms of microRNA-mediated gene regulation in animal cells. Trends Genet. 2007 23 : 243 9.
27. Cawley S, Bekiranov S, Ng HH, Kapranov P, Sekinger EA, Kampa D, Piccolboni A, Sementchenko V, Cheng J, Williams AJ, Wheeler R, Wong B, Drenkow J, Yamanaka M, Patel S, Brubaker S, Tammana H, Helt G, Struhl K, Gingeras TR. Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell. 2004 116 : 499 509.
28. Zhao Y, Srivastava D. A developmental view of microRNA function. Trends Biochem Sci. 2007 32 : 189 97.
29. Cullen BR. Transcription and processing of human microRNA precursors. Mol Cell. 2004 16 : 861 5.
30. Rodriguez A, Griffiths-Jones S, Ashurst JL, Bradley A. Identification of mammalian microRNA host genes and transcription units. Genome Res. 2004 14 : 1902 10.
31. Conaco C, Otto S, Han JJ, Mandel G. Reciprocal actions of REST and a microRNA promote neuronal identity. Proc Natl Acad Sci USA. 2006 103 : 2422 7.
32. Kim J, Inoue K, Ishii J, Vanti WB, Voronov SV, Murchison E, Hannon G, Abeliovich A. A MicroRNA feedback circuit in midbrain dopamine neurons. Science. 2007 317 : 1220 4.
33. Obernosterer G, Leuschner PJ, Alenius M, Martinez J. Post-transcriptional regulation of microRNA expression. RNA. 2006 12 : 1161 7.
34. Thomson JM, Newman M, Parker JS, Morin-Kensicki EM, Wright T, Hammond SM. Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev. 2006 20 : 2202 7.
35. Cao X, Yeo G, Muotri AR, Kuwabara T, Gage FH. Noncoding RNAs in the mammalian central nervous system. Annu Rev Neurosci. 2006 29 : 77 103.
36. Kosik KS, Krichevsky AM. The elegance of the microRNAs: a neuronal perspective. Neuron. 2005 47 : 779 82.
37. Giraldez AJ, Cinalli RM, Glasner ME, Enright AJ, Thomson JM, Baskerville S, Hammond SM, Bartel DP, Schier AF. MicroRNAs regulate brain morphogenesis in zebrafish. Science. 2005 308 : 833 8.
38. Krichevsky AM, Sonntag KC, Isacson O, Kosik KS. Specific microRNAs modulate embryonic stem cell-derived neurogene-sis. Stem Cells. 2006 24 : 857 64.
39. Cao X, Pfaff SL, Gage FH. A functional study of miR-124 in the developing neural tube. Genes Dev. 2007 21 : 531 6.
40. Visvanathan J, Lee S, Lee B, Lee JW, Lee SK. The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev. 2007 21 : 744 9.
41. Makeyev EV, Zhang J, Carrasco MA, Maniatis T. The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell. 2007 27 : 435 48.
42. Schaefer A, O'Carroll D, Tan CL, Hillman D, Sugimori M, Llinas R, Greengard P. Cerebellar neurodegeneration in the absence of microRNAs. J Exp Med. 2007 204 : 1553 8.
43. Damiani D, Alexander JJ, O'Rourke JR, McManus M, Jadhav AP, Cepko CL, Hauswirth WW, Harfe BD, Strettoi E. Dicer inactivation leads to progressive functional and structural degeneration of the mouse retina. J Neurosci. 2008 28 : 4878 87.
44. Cuellar TL, Davis TH, Nelson PT, Loeb GB, Harfe BD, Ullian E, McManus MT. Dicer loss in striatal neurons produces behavioral and neuroanatomical pheno-types in the absence of neurodegeneration. Proc Natl Acad Sci USA. 2008 105 : 5614 9.
45. Davis TH, Cuellar TL, Koch SM, Barker AJ, Harfe BD, McManus MT, Ullian EM. Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J Neurosci. 2008 28 : 4322 30.
46. Ashraf SI, Kunes S. A trace of silence: memory and microRNA at the synapse. Curr Opin Neurobiol. 2006 16 : 535 9.
47. Kosik KS. The neuronal microRNA system. Nat Rev Neurosci. 2006 7 : 911 20.
48. Vo N, Klein ME, Varlamova O, Keller DM, Yamamoto T, Goodman RH, Impey S. A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc Natl Acad Sci USA. 2005 102 : 16426 31.
49. Konur S, Ghosh A. Calcium signaling and the control of dendritic development. Neuron. 2005 46 : 401 5.
50. Cheng HY, Papp JW, Varlamova O, Dziema H, Russell B, Curfman JP, Nakazawa T, Shimizu K, Okamura H, Impey S, Obrietan K. microRNA modulation of circadian-clock period and entrain-ment. Neuron. 2007 54 : 813 29.
51. Ralph MR, Foster RG, Davis FC, Menaker M. Transplanted suprachiasmatic nucleus determines circadian period. Science. 1990 247 : 975 8.
52. Simon DJ, Madison JM, Conery AL, Thompson-Peer KL, Soskis M, Ruvkun GB, Kaplan JM, Kim JK. The microRNA miR-1 regulates a MEF-2-dependent retrograde signal at neuromuscular junctions. Cell. 2008 133 : 903 15.
53. Bailey CH, Kandel ER, Si K. The persistence of long-term memory: a molecular approach to self-sustaining changes in learning-induced synaptic growth. Neuron. 2004 44 : 49 57.
54. Kim J, Krichevsky A, Grad Y, Hayes GD, Kosik KS, Church GM, Ruvkun G. Identification of many microRNAs that copurify with polyribosomes in mammalian neurons. Proc Natl Acad Sci USA. 2004 101 : 360 5.
55. Lugli G, Larson J, Martone ME, Jones Y, Smalheiser NR. 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. 2005 94 : 896 905.
56. Martin KC, Kosik KS. Synaptic tagging - who's it? Nat Rev Neurosci. 2002 3 : 813 20.
57. Ashraf SI, McLoon AL, Sclarsic SM, Kunes S. Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell. 2006 124 : 191 205.
58. Hwang HW, Wentzel EA, Mendell JT. A hexanucleotide element directs microRNA nuclear import. Science. 2007 315 : 97 100.
59. Robertson MM. Diagnosing Tourette syndrome: is it a common disorder? J Psychosom Res. 2003 55 : 3 6.
60. Abelson JF, Kwan KY, O'Roak BJ, Baek DY, Stillman AA, Morgan TM, Mathews CA, Pauls DL, Rasin MR, Gunel M, Davis NR, Ercan-Sencicek AG, Guez DH, Spertus JA, Leckman JF, Dure LSt, Kurlan R, Singer HS, Gilbert DL, Farhi A, Louvi A, Lifton R P, Sestan N, State MW. Sequence variants in SLITRK1 are associated with Tourette's syndrome. Science. 2005 310 : 317 20.
61. Frugier T, Nicole S, Cifuentes-Diaz C, Melki J. The molecular bases of spinal muscular atrophy. Curr Opin Genet Dev. 2002 12 : 294 8.
62. Monani UR. Spinal muscular atrophy: a deficiency in a ubiquitous protein; a motor neuron-specific disease. Neuron. 2005 48 : 885 96.
63. Kolb SJ, Battle DJ, Dreyfuss G. Molecular functions of the SMN complex. J Child Neurol. 2007 22 : 990 4.
64. Dostie J, Mourelatos Z, Yang M, Sharma A, Dreyfuss G. Numerous microRNPs in neuronal cells containing novel microRNAs. RNA. 2003 9 : 180 6.
65. Stromme P, Bjornstad PG, Ramstad K. Prevalence estimation of Williams syndrome. J Child Neurol. 2002 17 : 269 71.
66. Frangiskakis JM, Ewart AK, Morris CA, Mervis CB, Bertrand J, Robinson BF, Klein BP, Ensing GJ, Everett LA, Green ED, Proschel C, Gutowski NJ, Noble M, Atkinson DL, Odelberg SJ, Keating MT. LIM-kinase1 hemizygosity implicated in impaired visuospatial constructive cognition. Cell. 1996 86 : 59 69.
67. Hoogenraad CC, Akhmanova A, Galjart N, De Zeeuw CI. LIMK1 and CLIP-115: linking cytoskeletal defects to Williams syndrome. Bioessays. 2004 26 : 141 50.
68. Meng Y, Zhang Y, Tregoubov V, Janus C, Cruz L, Jackson M, Lu WY, MacDonald JF, Wang JY, Falls DL, Jia Z. Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice. Neuron. 2002 35 : 121 33.
69. Amir RE, Van Den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet. 1999 23 : 185 8.
70. Chahrour M, Zoghbi HY. The story of Rett syndrome: from clinic to neurobiology. Neuron. 2007 56 : 422 37.
71. Klein ME, Lioy DT, Ma L, Impey S, Mandel G, Goodman RH. Homeostatic regulation of MeCP2 expression by a CREB-induced microRNA. Nat Neurosci. 2007 10 : 1513 4.
72. Perkins DO, Jeffries CD, Jarskog LF, Thomson JM, Woods K, Newman MA, Parker JS, Jin J, Hammond SM. microRNA expression in the prefrontal cortex of individuals with schizophrenia and schizoaffective disorder. Genome Biol. 2007 8 : R27.
73. Hansen T, Olsen L, Lindow M, Jakobsen KD, Ullum H, Jonsson E, Andreassen OA, Djurovic S, Melle I, Agartz I, Hall H, Timm S, Wang AG, Werge T. Brain expressed microRNAs implicated in schizophrenia etiology. PLoS ONE. 2007 2 : e873.
74. Stark KL, Xu B, Bagchi A, Lai WS, Liu H, Hsu R, Wan X, Pavlidis P, Mills AA, Karayiorgou M, Gogos JA. Altered brain microRNA biogenesis contributes to phe-notypic deficits in a 22q11-deletion mouse model. Nat Genet. 2008 40 : 751 60.
75. Wang WX, Rajeev BW, Stromberg AJ, Ren N, Tang G, Huang Q, Rigoutsos I, Nelson PT. 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 23.
76. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, Denis P, Teplow DB, Ross S, Amarante P, Loeloff R, Luo Y, Fisher S, Fuller J, Edenson S, Lile J, Jarosinski MA, Biere AL, Curran E, Burgess T, Louis JC, Collins F, Treanor J, Rogers G, Citron M. Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science. 1999 286 : 735 41.
77. Guo T, Hobbs DW. Development of BACE1 inhibitors for Alzheimer's disease. Curr Med Chem. 2006 13 : 1811 29.
78. Lukiw WJ. Micro-RNA speciation in fetal, adult and Alzheimer's disease hippocampus. Neuroreport. 2007 18 : 297 300.
79. Brown WT. The FRAXE Syndrome: is it time for routine screening? Am J Hum Genet. 1996 58 : 903 5.
80. Pieretti M, Zhang FP, Fu YH, Warren ST, Oostra BA, Caskey CT, Nelson DL. Absence of expression of the FMR-1 gene in fragile X syndrome. Cell. 1991 66 : 817 22.
81. O'Donnell WT, Warren ST. A decade of molecular studies of fragile X syndrome. Annu Rev Neurosci. 2002 25 : 315 38.
82. Caudy AA, Myers M, Hannon GJ, Hammond SM. Fragile X-related protein and VIG associate with the RNA interference machinery. Genes Dev. 2002 16 : 2491 6.
83. Jin P, Zarnescu DC, Ceman S, Nakamoto M, Mowrey J, Jongens TA, Nelson DL, Moses K, Warren ST. Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nat Neurosci. 2004 7 : 113 7.
84. Ishizuka A, Siomi MC, Siomi H. A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev. 2002 16 : 2497 508.
85. Weiler IJ, Spangler CC, Klintsova AY, Grossman AW, Kim SH, Bertaina-Anglade V, Khaliq H, de Vries FE, Lambers FA, Hatia F, Base CK, Greenough WT. Fragile X mental retardation protein is necessary for neurotrans-mitter-activated protein translation at synapses. Proc Natl Acad Sci USA. 2004 101 : 17504 9.
86. Greenough WT, Klintsova AY, Irwin SA, Galvez R, Bates KE, Weiler IJ. Synaptic regulation of protein synthesis and the fragile X protein. Proc Natl Acad Sci USA. 2001 98 : 7101 6.
87. Bagni C, Greenough WT. From mRNP trafficking to spine dysmorphogenesis: the roots of fragile X syndrome. Nat Rev Neurosci. 2005 6 : 376 87.
88. Klockgether T, Evert B. Genes involved in hereditary ataxias. Trends Neurosci. 1998 21 : 413 8.
89. Bilen J, Liu N, Burnett BG, Pittman RN, Bonini NM. MicroRNA pathways modulate polyglutamine-induced neurodegenera-tion. Mol Cell. 2006 24 : 157 63.
90. Hammond SM. MicroRNAs as oncogenes. Curr Opin Genet Dev. 2006 16 : 4 9.
91. Garzon R, Fabbri M, Cimmino A, Calin GA, Croce CM. MicroRNA expression and function in cancer. Trends Mol Med. 2006 12 : 580 7.
92. Sevignani C, Calin GA, Nnadi SC, Shimizu M, Davuluri RV, Hyslop T, Demant P, Croce CM, Siracusa LD. MicroRNA genes are frequently located near mouse cancer susceptibility loci. Proc Natl Acad Sci USA. 2007 104 : 8017 22.
93. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer. 2006 6 : 857 66.
94. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, Downing JR, Jacks T, Horvitz HR, Golub TR. MicroRNA expression profiles classify human cancers. Nature. 2005 435 : 834 8.
95. Ciafre SA, Galardi S, Mangiola A, Ferracin M, Liu CG, Sabatino G, Negrini M, Maira G, Croce CM, Farace MG. Extensive modulation of a set of microRNAs in primary glioblastoma. Biochem Biophys Res Commun. 2005 334 : 1351 8.
96. Chan JA, Krichevsky AM, Kosik KS. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res. 2005 65 : 6029 33.
97. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, Lanza G, Scarpa A, Vecchione A, Negrini M, Harris CC, Croce CM. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA. 2006 103 : 2257 61.
98. Nicholls RD, Knepper JL. Genome organization, function, and imprinting in Prader-Willi and Angelman syndromes. Annu Rev Genomics Hum Genet. 2001 2 : 153 75.
99. Lewis A, Redrup L. Genetic imprinting: conflict at the Callipyge locus. Curr Biol. 2005 15 : R291 4.
100. Seitz H, Royo H, Bortolin ML, Lin SP, Ferguson-Smith AC, Cavaille J. A large imprinted microRNA gene cluster at the mouse Dlk1-Gtl2 domain. Genome Res. 2004 14 : 1741 8.
101. Kloosterman WP, Lagendijk AK, Ketting RF, Moulton JD, Plasterk RH. Targeted inhibition of miRNA maturation with mor-pholinos reveals a role for miR-375 in pancreatic islet development. PLoS Biol. 2007 5 : e203.
102. Krutzfeldt J, Kuwajima S, Braich R, Rajeev KG, Pena J, Tuschl T, Manoharan M, Stoffel M. Specificity, duplex degradation and subcellular localization of antagomirs. Nucleic Acids Res. 2007 35 : 2885 92.
103. Elmen J, Lindow M, Schutz S, Lawrence M, Petri A, Obad S, Lindholm M, Hedtjarn M, Hansen HF, Berger U, Gullans S, Kearney P, Sarnow P, Straarup EM, Kauppinen S. LNA-mediated microRNA silencing in non-human primates. Nature. 2008 452 : 896 9.
104. Kumar P, Wu H, McBride JL, Jung KE, Kim MH, Davidson BL, Lee SK, Shankar P, Manjunath N. Transvascular delivery of small interfering RNA to the central nervous system. Nature. 2007 448 : 39 43.
105. Sharp KH, Eam B, Faulkner DJ, Haygood MG. Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl Environ Microbiol. 2007 73 : 622 9.
106. Ebert MS, Neilson JR, Sharp PA. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods. 2007 4 : 721 6.