Role of microRNAs in Semaphorin function and neural circuit formation

Seminars in Cell and Developmental Biology

Volumn 24, Issue 3, 2013, Pages 146-155

  Baudet, Marie Laure ^a   Bellon, Anaïs ^b   Holt, Christine E ^b  

^a UNIVERSITY OF TRENTO   (Italy)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Axon guidance; Cancer; Cardiovascular system; MicroRNAs; Nervous system; Semaphorin

Indexed keywords

MICRORNA; NEUROPILIN 1; NEUROPILIN 2; PLEXIN; SEMAPHORIN;

CANCER GROWTH; CARDIOVASCULAR SYSTEM; CELL MIGRATION; DISEASE COURSE; FASCICULATION; KIDNEY CARCINOMA; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE FIBER; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; SYNAPTOGENESIS; TUMOR MICROENVIRONMENT;

EUKARYOTA;

EID: 84875603404     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2012.11.004     Document Type: Review

References (155)

1. 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.
2. 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, 75:843-854.
3. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
4. Lee Y., Ahn C., Han J., Choi H., Kim J., Yim J., et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003, 425:415-419.
5. Gregory R.I., Yan K.-P., Amuthan G., Chendrimada T., Doratotaj B., Cooch N., et al. The Microprocessor complex mediates the genesis of microRNAs. Nature 2004, 432:235-240.
6. Han J., Lee Y., Yeom K.-H., Kim Y.-K., Jin H., Kim V.N. The Drosha-DGCR8 complex in primary microRNA processing. Genes and Development 2004, 18:3016-3027.
7. Denli A.M., Tops B.B.J., Plasterk R.H.A., Ketting R.F., Hannon G.J. Processing of primary microRNAs by the Microprocessor complex. Nature 2004, 432:231-235.
8. Ruby J.G., Jan C.H., Bartel D.P. Intronic microRNA precursors that bypass Drosha processing. Nature 2007, 448:83-86.
9. Yi R., Qin Y., Macara I.G., Cullen B.R. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes and Development 2003, 17:3011-3016.
10. Lund E., Güttinger S., Calado A., Dahlberg J.E., Kutay U. Nuclear export of microRNA precursors. Science (New York, NY) 2004, 303:95-98.
11. Knight S.W., Bass B.L. A role for the RNase III enzyme DCR-1 in RNA interference and germ line development in Caenorhabditis elegans. Science (New York, NY) 2001, 293:2269-2271.
12. Hutvagner G., McLachlan J., Pasquinelli A.E., Bálint E., Tuschl T., Zamore P.D. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science (New York, NY) 2001, 293:834-838.
13. Ketting R.F., Fischer S.E., Bernstein E., Sijen T., Hannon G.J., Plasterk R.H. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes and Development 2001, 15:2654-2659.
14. Cheloufi S., Dos Santos C.O., Chong M.M.W., Hannon G.J. A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 2010, 465:584-589.
15. Cifuentes D., Xue H., Taylor D.W., Patnode H., Mishima Y., Cheloufi S., et al. A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science (New York, NY) 2010, 328:1694-1698.
16. Kim V.N. MicroRNA biogenesis: coordinated cropping and dicing. Nature Reviews Molecular Cell Biology 2005, 6:376-385.
17. Bazzini A.A., Lee M.T., Giraldez A.J. Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in Zebrafish. Science (New York, NY) 2012, 336:233-237.
18. Djuranovic S., Nahvi A., Green R. miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science (New York, NY) 2012, 336:237-240.
19. Reinhart B.J., Slack F.J., Basson M., Pasquinelli A.E., Bettinger J.C., Rougvie A.E., et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 403:901-906.
20. Baek D., Villén J., Shin C., Camargo F.D., Gygi S.P., Bartel D.P. The impact of microRNAs on protein output. Nature 2008, 455:64-71.
21. Selbach M., Schwanhäusser B., Thierfelder N., Fang Z., Khanin R., Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature 2008, 455:58-63.
22. Guo H., Ingolia N.T., Weissman J.S., Bartel D.P. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466:835-840.
23. Ebert M.S., Sharp P.A. Roles for microRNAs in conferring robustness to biological processes. Cell 2012, 149:515-524.
24. Unified nomenclature for the semaphorins/collapsins. Semaphorin Nomenclature Committee. Cell 1999, 97:551-552.
25. Kumanogoh A., Kikutani H. Semaphorins and their receptors: novel features of neural guidance molecules. Proceedings of the Japan Academy - Series B: Physical & Biological 2010, 86:611-620.
26. Tran T.S., Kolodkin A.L., Bharadwaj R. Semaphorin regulation of cellular morphology. Annual Review of Cell and Developmental Biology 2007, 23:263-292.
27. Kolodkin A.L., Matthes D.J., O'Connor T.P., Patel N.H., Admon A., Bentley D., et al. Fasciclin IV: sequence, expression, and function during growth cone guidance in the grasshopper embryo. Neuron 1992, 9:831-845.
28. Luo Y., Raible D., Raper J.A. Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 1993, 75:217-227.
29. Godenschwege T.A., Hu H., Shan-Crofts X., Goodman C.S., Murphey R.K. Bi-directional signalling by Semaphorin 1a during central synapse formation in Drosophila. Nature Neuroscience 2002, 5:1294-1301.
30. Zhou Y., Gunput R.A., Pasterkamp R.J. Semaphorin signalling: progress made and promises ahead. Trends in Biochemical Sciences 2008, 33:161-170.
31. Takamatsu H., Okuno T., Kumanogoh A. Regulation of immune cell responses by semaphorins and their receptors. Cellular & Molecular Immunology 2010, 7:83-88.
32. Takamatsu H., Kumanogoh A. Diverse roles for semaphorin-plexin signalling in the immune system. Trends in Immunology 2012, 33:127-135.
33. Adams R.H., Eichmann A. Axon guidance molecules in vascular patterning. Cold Spring Harbor Perspectives in Biology 2010, 2:a001875.
34. Roth L., Koncina E., Satkauskas S., Cremel G., Aunis D., Bagnard D. The many faces of semaphorins: from development to pathology. Cellular and Molecular Life Sciences 2009, 66:649-666.
35. Toyofuku T., Kikutani H. Semaphorin signalling during cardiac development. Advances in Experimental Medicine and Biology 2007, 600:109-117.
36. Pasterkamp R.J. Getting neural circuits into shape with semaphorins. Nature Reviews Neuroscience 2012, 13:605-618.
37. Mann F., Chauvet S., Rougon G. Semaphorins in development and adult brain: implication for neurological diseases. Progress in Neurobiology 2007, 82:57-79.
38. Flannery E., Duman-Scheel M. Semaphorins at the interface of development and cancer. Current Drug Targets 2009, 10:611-619.
39. Muratori C., Tamagnone L. Semaphorin signals tweaking the tumor microenvironment. Advances in Cancer Research 2012, 114:59-85.
40. Sakurai A., Doci C.L., Gutkind J.S. Semaphorin signalling in angiogenesis, lymphangiogenesis and cancer. Cell Research 2012, 22:23-32.
41. Kong Y.W., Ferland-McCollough D., Jackson T.J., Bushell M. microRNAs in cancer management. Lancet Oncology 2012, 13:e249-e258.
42. Cochella L., Hobert O. Diverse functions of microRNAs in nervous system development. Current Topics in Developmental Biology 2012, 99:115-143.
43. Contreras J., Rao D.S. MicroRNAs in inflammation and immune responses. Leukemia 2012, 26:404-413.
44. Im H.I., Kenny P.J. MicroRNAs in neuronal function and dysfunction. Trends in Neurosciences 2012, 35:325-334.
45. Small E.M., Olson E.N. Pervasive roles of microRNAs in cardiovascular biology. Nature 2011, 469:336-342.
46. Urbich C., Kuehbacher A., Dimmeler S. Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovascular Research 2008, 79:581-588.
47. Bonauer A., Boon R.A., Dimmeler S. Vascular microRNAs. Current Drug Targets 2010, 11:943-949.
48. Zhou X., Jeker L.T., Fife B.T., Zhu S., Anderson M.S., McManus M.T., et al. Selective miRNA disruption in Treg cells leads to uncontrolled autoimmunity. Journal of Experimental Medicine 2008, 205:1983-1991.
49. Saxena A., Tabin C.J. miRNA-processing enzyme Dicer is necessary for cardiac outflow tract alignment and chamber septation. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:87-91.
50. Dunwoodie S.L. Combinatorial signalling in the heart orchestrates cardiac induction, lineage specification and chamber formation. Seminars in Cell and Developmental Biology 2007, 18:54-66.
51. Herbert S.P., Stainier D.Y. Molecular control of endothelial cell behaviour during blood vessel morphogenesis. Nature Reviews Molecular Cell Biology 2011, 12:551-564.
52. Gerhardt H., Golding M., Fruttiger M., Ruhrberg C., Lundkvist A., Abramsson A., et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. Journal of Cell Biology 2003, 161:1163-1177.
53. Carmeliet P., Tessier-Lavigne M. Common mechanisms of nerve and blood vessel wiring. Nature 2005, 436:193-200.
54. Arese M., Serini G., Bussolino F. Nervous vascular parallels: axon guidance and beyond. International Journal of Developmental Biology 2011, 55:439-445.
55. Fukushima Y., Okada M., Kataoka H., Hirashima M., Yoshida Y., Mann F., et al. Sema3E-PlexinD1 signalling selectively suppresses disoriented angiogenesis in ischemic retinopathy in mice. Journal of Clinical Investigation 2011, 121:1974-1985.
56. Kim J., Oh W.J., Gaiano N., Yoshida Y., Gu C. Semaphorin 3E-Plexin-D1 signalling regulates VEGF function in developmental angiogenesis via a feedback mechanism. Genes and Development 2011, 25:1399-1411.
57. Biyashev D., Veliceasa D., Topczewski J., Topczewska J.M., Mizgirev I., Vinokour E., et al. miR-27b controls venous specification and tip cell fate. Blood 2012, 119:2679-2687.
58. Xin M., Small E.M., Sutherland L.B., Qi X., McAnally J., Plato C.F., et al. MicroRNAs miR-143 and miR-145 modulate cytoskeletal dynamics and responsiveness of smooth muscle cells to injury. Genes and Development 2009, 23:2166-2178.
59. Cordes K.R., Sheehy N.T., White M.P., Berry E.C., Morton S.U., Muth A.N., et al. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 2009, 460:705-710.
60. Kuehbacher A., Urbich C., Zeiher A.M., Dimmeler S. Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circulation Research 2007, 101:59-68.
61. Urbich C., Kaluza D., Fromel T., Knau A., Bennewitz K., Boon R.A., et al. MicroRNA-27a/b controls endothelial cell repulsion and angiogenesis by targeting semaphorin 6A. Blood 2012, 119:1607-1616.
62. Cui Y., Han Z., Hu Y., Song G., Hao C., Xia H., et al. MicroRNA-181b and microRNA-9 mediate arsenic-induced angiogenesis via NRP1. Journal of Cellular Physiology 2012, 227:772-783.
63. Pedrioli D.M., Karpanen T., Dabouras V., Jurisic G., van de Hoek G., Shin J.W., et al. miR-31 functions as a negative regulator of lymphatic vascular lineage-specific differentiation in vitro and vascular development in vivo. Molecular and Cellular Biology 2010, 30:3620-3634.
64. Jones D., Li Y., He Y., Xu Z., Chen H., Min W. Mirtron microRNA-1236 inhibits VEGFR-3 signalling during inflammatory lymphangiogenesis. Arteriosclerosis, Thrombosis, and Vascular Biology 2012, 32:633-642.
65. Capparuccia L., Tamagnone L. Semaphorin signalling in cancer cells and in cells of the tumor microenvironment - two sides of a coin. Journal of Cell Science 2009, 122:1723-1736.
66. Melo S.A., Esteller M. Dysregulation of microRNAs in cancer: playing with fire. FEBS Letters 2011, 585:2087-2099.
67. Liu H., Brannon A.R., Reddy A.R., Alexe G., Seiler M.W., Arreola A., et al. Identifying mRNA targets of microRNA dysregulated in cancer: with application to clear cell Renal Cell Carcinoma. BMC Systems Biology 2010, 4:51.
68. Dhanabal M., Wu F., Alvarez E., McQueeney K.D., Jeffers M., MacDougall J., et al. Recombinant semaphorin 6A-1 ectodomain inhibits in vivo growth factor and tumor cell line-induced angiogenesis. Cancer Biology and Therapy 2005, 4:659-668.
69. Bullock M.D., Sayan A.E., Packham G.K., Mirnezami A.H. MicroRNAs: critical regulators of epithelial to mesenchymal (EMT) and mesenchymal to epithelial transition (MET) in cancer progression. Biologie Cellulaire 2012, 104:3-12.
70. Zhang Y., He X., Liu Y., Ye Y., Zhang H., He P., et al. microRNA-320a inhibits tumor invasion by targeting neuropilin 1 and is associated with liver metastasis in colorectal cancer. Oncology Reports 2012, 27:685-694.
71. Parikh A.A., Fan F., Liu W.B., Ahmad S.A., Stoeltzing O., Reinmuth N., et al. Neuropilin-1 in human colon cancer: expression, regulation, and role in induction of angiogenesis. American Journal of Pathology 2004, 164:2139-2151.
72. Ochiumi T., Kitadai Y., Tanaka S., Akagi M., Yoshihara M., Chayama K. Neuropilin-1 is involved in regulation of apoptosis and migration of human colon cancer. International Journal of Oncology 2006, 29:105-116.
73. Qiang R., Wang F., Shi L.Y., Liu M., Chen S., Wan H.Y., et al. Plexin-B1 is a target of miR-214 in cervical cancer and promotes the growth and invasion of HeLa cells. International Journal of Biochemistry and Cell Biology 2011, 43:632-641.
74. Gomez Roman J.J., Garay G.O., Saenz P., Escuredo K., Sanz Ibayondo C., Gutkind S., et al. Plexin B1 is downregulated in renal cell carcinomas and modulates cell growth. Translational Research 2008, 151:134-140.
75. Granziero L., Circosta P., Scielzo C., Frisaldi E., Stella S., Geuna M., et al. CD100/Plexin-B1 interactions sustain proliferation and survival of normal and leukemic CD5+ B lymphocytes. Blood 2003, 101:1962-1969.
76. Rody A., Karn T., Ruckhaberle E., Hanker L., Metzler D., Muller V., et al. Loss of Plexin B1 is highly prognostic in low proliferating ER positive breast cancers - results of a large scale microarray analysis. European Journal of Cancer 2009, 45:405-413.
77. Valente G., Nicotra G., Arrondini M., Castino R., Capparuccia L., Prat M., et al. Co-expression of plexin-B1 and Met in human breast and ovary tumours enhances the risk of progression. Cellular Oncology 2009, 31:423-436.
78. Wong O.G., Nitkunan T., Oinuma I., Zhou C., Blanc V., Brown R.S., et al. Plexin-B1 mutations in prostate cancer. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:19040-19045.
79. Alajez N.M., Lenarduzzi M., Ito E., Hui A.B., Shi W., Bruce J., et al. MiR-218 suppresses nasopharyngeal cancer progression through downregulation of survivin and the SLIT2-ROBO1 pathway. Cancer Research 2011, 71:2381-2391.
80. Tie J., Pan Y., Zhao L., Wu K., Liu J., Sun S., et al. MiR-218 inhibits invasion and metastasis of gastric cancer by targeting the Robo1 receptor. PLoS Genetics 2010, 6:e1000879.
81. Taniguchi M., Yuasa S., Fujisawa H., Naruse I., Saga S., Mishina M., et al. Disruption of semaphorin III/D gene causes severe abnormality in peripheral nerve projection. Neuron 1997, 19:519-530.
82. Bagri A., Cheng H.-J., Yaron A., Pleasure S.J., Tessier-Lavigne M. Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family. Cell 2003, 113:285-299.
83. Liu X.-B., Low L.K., Jones E.G., Cheng H.-J. Stereotyped axon pruning via plexin signalling is associated with synaptic complex elimination in the hippocampus. Journal of Neuroscience 2005, 25:9124-9134.
84. Cloutier J.-F., Giger R.J., Koentges G., Dulac C., Kolodkin A.L., Ginty D.D. Neuropilin-2 mediates axonal fasciculation, zonal segregation, but not axonal convergence, of primary accessory olfactory neurons. Neuron 2002, 33:877-892.
85. Cloutier J.-F., Sahay A., Chang E.C., Tessier-Lavigne M., Dulac C., Kolodkin A.L., et al. Differential requirements for semaphorin 3F and Slit-1 in axonal targeting, fasciculation, and segregation of olfactory sensory neuron projections. Journal of Neuroscience 2004, 24:9087-9096.
86. Schwarting G.A., Kostek C., Ahmad N., Dibble C., Pays L., Püschel A.W. Semaphorin 3A is required for guidance of olfactory axons in mice. Journal of Neuroscience 2000, 20:7691-7697.
87. Walz A., Rodriguez I., Mombaerts P. Aberrant sensory innervation of the olfactory bulb in neuropilin-2 mutant mice. Journal of Neuroscience 2002, 22:4025-4035.
88. Liu Y., Berndt J., Su F., Tawarayama H., Shoji W., Kuwada J.Y., et al. Semaphorin3D guides retinal axons along the dorsoventral axis of the tectum. Journal of Neuroscience 2004, 24:310-318.
89. Komiyama T., Sweeney L.B., Schuldiner O., Garcia K.C., Luo L. Graded expression of semaphorin-1a cell-autonomously directs dendritic targeting of olfactory projection neurons. Cell 2007, 128:399-410.
90. Imai T., Yamazaki T., Kobayakawa R., Kobayakawa K., Abe T., Suzuki M., et al. Pre-target axon sorting establishes the neural map topography. Science (New York, NY) 2009, 325:585-590.
91. Lim L.P., Lau N.C., Garrett-Engele P., Grimson A., Schelter J.M., Castle J., et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433:769-773.
92. Takeuchi H., Inokuchi K., Aoki M., Suto F., Tsuboi A., Matsuda I., et al. Sequential arrival and graded secretion of Sema3F by olfactory neuron axons specify map topography at the bulb. Cell 2010, 141:1056-1067.
93. Sweeney L.B., Couto A., Chou Y.-H., Berdnik D., Dickson B.J., Luo L., et al. Temporal target restriction of olfactory receptor neurons by Semaphorin-1a/PlexinA-mediated axon-axon interactions. Neuron 2007, 53:185-200.
94. Paradis S., Harrar D.B., Lin Y., Koon A.C., Hauser J.L., Griffith E.C., et al. An RNAi-based approach identifies molecules required for glutamatergic and GABAergic synapse development. Neuron 2007, 53:217-232.
95. Lin X., Ogiya M., Takahara M., Yamaguchi W., Furuyama T., Tanaka H., et al. Sema4D-plexin-B1 implicated in regulation of dendritic spine density through RhoA/ROCK pathway. Neuroscience Letters 2007, 428:1-6.
96. Yamashita N., Morita A., Uchida Y., Nakamura F., Usui H., Ohshima T., et al. Regulation of spine development by semaphorin3A through cyclin-dependent kinase 5 phosphorylation of collapsin response mediator protein 1. Journal of Neuroscience 2007, 27:12546-12554.
97. Tran T.S., Rubio M.E., Clem R.L., Johnson D., Case L., Tessier-Lavigne M., et al. Secreted semaphorins control spine distribution and morphogenesis in the postnatal CNS. Nature 2009, 462:1065-1069.
98. Morita A., Yamashita N., Sasaki Y., Uchida Y., Nakajima O., Nakamura F., et al. Regulation of dendritic branching and spine maturation by semaphorin3A-Fyn signalling. Journal of Neuroscience 2006, 26:2971-2980.
99. Baudet M.L., Zivraj K.H., Abreu-Goodger C., Muldal A., Armisen J., Blenkiron C., et al. miR-124 acts through CoREST to control onset of Sema3A sensitivity in navigating retinal growth cones. Nature Neuroscience 2012, 15:29-38.
100. Campbell D.S., Regan A.G., Lopez J.S., Tannahill D., Harris W.A., Holt C.E. Semaphorin 3A elicits stage-dependent collapse, turning, and branching in Xenopus retinal growth cones. Journal of Neuroscience 2001, 21:8538-8547.
101. Decembrini S., Bressan D., Vignali R., Pitto L., Mariotti S., Rainaldi G., et al. MicroRNAs couple cell fate and developmental timing in retina. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:21179-21184.
102. Schoenherr C.J., Anderson D.J. The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science (New York, NY) 1995, 267:1360-1363.
103. Clark A.M., Goldstein L.D., Tevlin M., Tavaré S., Shaham S., Miska E.A. The microRNA miR-124 controls gene expression in the sensory nervous system of Caenorhabditis elegans. Nucleic Acids Research 2010, 38:3780-3793.
104. Gao F-B. Context-dependent functions of specific microRNAs in neuronal development. Neural Development 2010, 5:25.
105. Schratt G. Fine-tuning neural gene expression with microRNAs. Current Opinion in Neurobiology 2009, 19:213-219.
106. Seitz H. Redefining microRNA targets. Current Biology 2009, 19:870-873.
107. Conaco C., Otto S., Han J.-J., Mandel G. Reciprocal actions of REST and a microRNA promote neuronal identity. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:2422-2427.
108. 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 and Development 2007, 21:744-749.
109. Makeyev E.V., Maniatis T. Multilevel regulation of gene expression by microRNAs. Science (New York, NY) 2008, 319:1789-1790.
110. Zivraj K.H., Tung Y.C.L., Piper M., Gumy L., Fawcett J.W., Yeo G.S.H., et al. Subcellular profiling reveals distinct and developmentally regulated repertoire of growth cone mRNAs. Journal of Neuroscience 2010, 30:15464-15478.
111. Ballas N., Mandel G. The many faces of REST oversee epigenetic programming of neuronal genes. Current Opinion in Neurobiology 2005, 15:500-506.
112. Pasterkamp R.J., Giger R.J. Semaphorin function in neural plasticity and disease. Current Opinion in Neurobiology 2009, 19:263-274.
113. Ding J.B., Oh W.J., Sabatini B.L., Gu C. Semaphorin 3E-Plexin-D1 signalling controls pathway-specific synapse formation in the striatum. Nature Neuroscience 2012, 15:215-223.
114. Pecho-Vrieseling E., Sigrist M., Yoshida Y., Jessell T.M., Arber S. Specificity of sensory-motor connections encoded by Sema3e-Plxnd1 recognition. Nature 2009, 459:842-846.
115. Burkhardt C., Muller M., Badde A., Garner C.C., Gundelfinger E.D., Puschel A.W. Semaphorin 4B interacts with the post-synaptic density protein PSD-95/SAP90 and is recruited to synapses through a C-terminal PDZ-binding motif. FEBS Letters 2005, 579:3821-3828.
116. Sahay A., Kim C.H., Sepkuty J.P., Cho E., Huganir R.L., Ginty D.D., et al. Secreted semaphorins modulate synaptic transmission in the adult hippocampus. Journal of Neuroscience 2005, 25:3613-3620.
117. Bouzioukh F., Daoudal G., Falk J., Debanne D., Rougon G., Castellani V. Semaphorin3A regulates synaptic function of differentiated hippocampal neurons. European Journal of Neuroscience 2006, 23:2247-2254.
118. Stark K.L., Xu B., Bagchi A., Lai W.S., Liu H., Hsu R., et al. Altered brain microRNA biogenesis contributes to phenotypic deficits in a 22q11-deletion mouse model. Nature Genetics 2008, 40:751-760.
119. Fenelon K., Mukai J., Xu B., Hsu P.K., Drew L.J., Karayiorgou M., et al. Deficiency of Dgcr8, a gene disrupted by the 22q11.2 microdeletion, results in altered short-term plasticity in the prefrontal cortex. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:4447-4452.
120. Edbauer D., Neilson J.R., Foster K.A., Wang C.F., Seeburg D.P., Batterton M.N., et al. Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron 2010, 65:373-384.
121. Lippi G., Steinert J.R., Marczylo E.L., D'Oro S., Fiore R., Forsythe I.D., et al. Targeting of the Arpc3 actin nucleation factor by miR-29a/b regulates dendritic spine morphology. Journal of Cell Biology 2011, 194:889-904.
122. Cohen J.E., Lee P.R., Chen S., Li W., Fields R.D. MicroRNA regulation of homeostatic synaptic plasticity. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:11650-11655.
123. Impey S., Davare M., Lesiak A., Fortin D., Ando H., Varlamova O., et al. An activity-induced microRNA controls dendritic spine formation by regulating Rac1-PAK signalling. Molecular and Cellular Neurosciences 2010, 43:146-156.
124. Siegel G., Obernosterer G., Fiore R., Oehmen M., Bicker S., Christensen M., et al. A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nature Cell Biology 2009, 11:705-716.
125. Schratt G.M., Tuebing F., Nigh E.A., Kane C.G., Sabatini M.E., Kiebler M., et al. A brain-specific microRNA regulates dendritic spine development. Nature 2006, 439:283-289.
126. Tognini P., Putignano E., Coatti A., Pizzorusso T. Experience-dependent expression of miR-132 regulates ocular dominance plasticity. Nature Neuroscience 2011, 14:1237-1239.
127. Smibert P., Bejarano F., Wang D., Garaulet D.L., Yang J.S., Martin R., et al. A Drosophila genetic screen yields allelic series of core microRNA biogenesis factors and reveals post-developmental roles for microRNAs. RNA 2011, 17:1997-2010.
128. Lee K., Kim J.H., Kwon O.B., An K., Ryu J., Cho K., et al. An activity-regulated microRNA, miR-188, controls dendritic plasticity and synaptic transmission by downregulating neuropilin-2. Journal of Neuroscience 2012, 32:5678-5687.
129. De Roo M., Klauser P., Garcia P.M., Poglia L., Muller D. Spine dynamics and synapse remodeling during LTP and memory processes. Progress in Brain Research 2008, 169:199-207.
130. Cooke S.F., Bliss T.V. Plasticity in the human central nervous system. Brain 2006, 129:1659-1673.
131. Good P.F., Alapat D., Hsu A., Chu C., Perl D., Wen X., et al. A role for semaphorin 3A signalling in the degeneration of hippocampal neurons during Alzheimer's disease. Journal of Neurochemistry 2004, 91:716-736.
132. De Winter F., Vo T., Stam F.J., Wisman L.A.B., Bar P.R., Niclou S.P., et al. The expression of the chemorepellent Semaphorin 3A is selectively induced in terminal Schwann cells of a subset of neuromuscular synapses that display limited anatomical plasticity and enhanced vulnerability in motor neuron disease. Molecular and Cellular Neuroscience 2006, 32:102-117.
133. Lesnick T.G., Sorenson E.J., Ahlskog J.E., Henley J.R., Shehadeh L., Papapetropoulos S., et al. Beyond Parkinson disease: amyotrophic lateral sclerosis and the axon guidance pathway. PLoS ONE 2008, 3.
134. Pinter R., Hindges R. Perturbations of microRNA function in mouse dicer mutants produce retinal defects and lead to aberrant axon pathfinding at the optic chiasm. PLoS ONE 2010, 5:e10021.
135. Castellani V., De Angelis E., Kenwrick S., Rougon G. Cis and trans interactions of L1 with neuropilin-1 control axonal responses to semaphorin 3A. EMBO Journal 2002, 21:6348-6357.
136. Dickson B.J., Zou Y. Navigating intermediate targets: the nervous system midline. Cold Spring Harbor Perspectives in Biology 2010, 2:a002055.
137. Kuwajima T., Yoshida Y., Takegahara N., Petros T.J., Kumanogoh A., Jessell T.M., et al. Optic chiasm presentation of Semaphorin6D in the context of Plexin-A1 and Nr-CAM promotes retinal axon midline crossing. Neuron 2012, 74:676-690.
138. Giraldez A.J., Cinalli R.M., Glasner M.E., Enright A.J., Thomson J.M., Baskerville S., et al. MicroRNAs regulate brain morphogenesis in Zebrafish. Science (New York, NY) 2005, 308:833-838.
139. Gammil L., Gonzalez C., Bronner-Fraser M. Neuropilin 2/Semaphorin 3F is essential for cranial neural crest migration and trigeminal ganglion condensation. Journal of Neurobiology 2007, 67:47-56.
140. Wolman M.A., Liu Y., Tawarayama H., Shoji W., Halloran M.C. Repulsion and attraction of axons by semaphorin3D are mediated by different neuropilins in vivo. Journal of Neuroscience 2004, 24:8428-8435.
141. Wolman M.A., Regnery A.M., Becker T., Becker C.G., Halloran M.C. Semaphorin3D regulates axon-axon interactions by modulating levels of L1 cell adhesion molecule. Journal of Neuroscience 2007, 27:9653-9663.
142. Yu H.-H., Houart C., Moens C.B. Cloning and embryonic expression of Zebrafish neuropilin genes. Gene Expression Patterns: GEP 2004, 4:371-378.
143. Halloran M.C., Severance S.M., Yee C.S., Gemza D.L., Raper J.A., Kuwada J.Y. Analysis of a Zebrafish semaphorin reveals potential functions in vivo. Developmental Dynamics: An Official Publication of the American Association of Anatomists 1999, 214:13-25.
144. Anderson R.B., Jackson S.C., Fujisawa H., Key B. Expression and putative role of neuropilin-1 in the early scaffold of axon tracts in embryonic Xenopus brain. Developmental Dynamics: An Official Publication of the American Association of Anatomists 2000, 219:102-108.
145. Berdnik D., Fan A.P., Potter C.J., Luo L. MicroRNA processing pathway regulates olfactory neuron morphogenesis. Current Biology 2008, 18:1754-1759.
146. Jefferis G.S., Marin E.C., Stocker R.F., Luo L. Target neuron prespecification in the olfactory map of Drosophila. Nature 2001, 414:204-208.
147. Dajas-Bailador F., Bonev B., Garcez P., Stanley P., Guillemot F., Papalopulu N. microRNA-9 regulates axon extension and branching by targeting Map1b in mouse cortical neurons. Nature Neuroscience 2012, 15:697-699.
148. Leucht C., Stigloher C., Wizenmann A., Klafke R., Folchert A., Bally-Cuif L. MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nature Neuroscience 2008, 11:641-648.
149. Krichevsky A.M., Sonntag K.C., Isacson O., Kosik K.S. Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells 2006, 24:857-864.
150. Dent E.W., Barnes A.M., Tang F., Kalil K. Netrin-1 and semaphorin 3A promote or inhibit cortical axon branching, respectively, by reorganization of the cytoskeleton. Journal of Neuroscience 2004, 24:3002-3012.
151. Hilario J.D., Rodino-Klapac L.R., Wang C., Beattie C.E. Semaphorin 5A is a bifunctional axon guidance cue for axial motoneurons in vivo. Developmental Biology 2009, 326:190-200.
152. Liu Y., Halloran M.C. Central and peripheral axon branches from one neuron are guided differentially by Semaphorin3D and transient axonal glycoprotein-1. Journal of Neuroscience 2005, 25:10556-10563.
153. Feldner J., Becker T., Goishi K., Schweitzer J., Lee P., Schachner M., et al. Neuropilin-1a is involved in trunk motor axon outgrowth in embryonic Zebrafish. Developmental Dynamics 2005, 234:535-549.
154. Salmena L., Poliseno L., Tay Y., Kats L., Pandolfi P.P. A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language. Cell 2011, 146:353-358.
155. Miska E.A., Alvarez-Saavedra E., Abbott A.L., Lau N.C., Hellman A.B., McGonagle S.M., et al. Most Caenorhabditis elegans microRNAs are individually not essential for development or viability. PLoS Genetics 2007, 3:e215.