Stage-specific modulation of cortical neuronal development by Mmu-miR-134

Cerebral Cortex

Volumn 21, Issue 8, 2011, Pages 1857-1869

  Gaughwin, Philip ^a,b   Ciesla, MacIej ^c   Yang, Henry ^d   Lim, Bing ^a,e   Brundin, Patrik ^b  

^a GENOME INSTITUTE OF SINGAPORE   (Singapore)

^b LUND UNIVERSITY   (Sweden)

^c JAGIELLONIAN UNIVERSITY   (Poland)

^d BIOINFORMATICS INSTITUTE   (Singapore)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

cortex; microRNAs; migration; mmu miR 134

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CHORDIN; CHORDIN LIKE 1; DOUBLECORTIN; MICRORNA; MICRORNA 134; MICROTUBULE ASSOCIATED PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CORTEX; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; EMBRYONIC STEM CELL; GENE EXPRESSION; GENETIC TRANSCRIPTION; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CEREBRAL CORTEX; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE TARGETING; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICRORNAS; MICROTUBULE-ASSOCIATED PROTEINS; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; NEUROPEPTIDES;

EID: 79960752625     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhq262     Document Type: Article

References (61)

1. Allendoerfer KL, Shatz CJ. 1994. The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Annu Rev Neurosci. 17:185-218. (Pubitemid 24117029)
2. Ayala R, Shu T, Tsai L. 2007. Trekking across the brain: the journey of neuronal migration. Cell. 128:29-43. (Pubitemid 46055273)
3. Bai J, Ramos R, Ackman J, Thomas A, Lee R, Loturco J. 2003. RNAi reveals doublecortin is required for radial migration in rat neo-cortex. Nat Neurosci. 6:1277-1283. (Pubitemid 37485121)
4. Boekhoorn K, Sarabdjitsingh A, Kommerie H, de Punder K, Schouten T, Lucassen PJ, Vreugdenhil E. 2008. Doublecortin (DCX) and doublecortin-like (DCL) are differentially expressed in the early but not late stages of murine neocortical development. J Comp Neurol. 507:1639-1652. (Pubitemid 351436259)
5. Borghesani PR, Peyrin JM, Klein R, Rubin J, Carter AR, Schwartz PM, Luster A, Corfas G, Segal RA. 2002. BDNF stimulates migration of cerebellar granule cells. Development. 129:1435-1442. (Pubitemid 34874164)
6. Cheng X, Hsu C, Currle DS, Hu JS, Barkovich AJ, Monuki ES. 2006. Central roles of the roof plate in telencephalic development and holoprosencephaly. J Neurosci. 26:7640-7649. (Pubitemid 44315183)
7. Chua S. 2006. A novel normalization method for effective removal of systematic variation in microarray data. Nucleic Acids Res. 34:e38.
8. Coffinier C, Tran U, Larrain J, De Robertis EM. 2001. Neuralin-1 is a novel Chordin-related molecule expressed in the mouse neural plate. Mech Dev. 100:119-122.
9. Colak D, Mori T, Brill MS, Pfeifer A, Falk S, Deng C, Monteiro R, Mummery C, Sommer L, Gotz M. 2008. Adult neurogenesis requires Smad4-mediated bone morphogenic protein signaling in stem cells. J Neurosci. 28:434-446.
10. De Pietri Tonelli D, Pulvers JN, Haffner C, Murchison EP, Hannon GJ, Huttner WB. 2008. miRNAs are essential for survival and differentiation of newborn neurons but not for expansion of neural progenitors during early neurogenesis in the mouse embryonic neocortex. Development. 135:3911-3921.
11. Dehay C, Kennedy H. 2007. Cell-cycle control and cortical development. Nat Rev Neurosci. 8:438-450. (Pubitemid 46789227)
12. Deleyrolle L, Marchal-Victorion S, Dromard C, Fritz V, Saunier M, Sabourin J-C, Tran Van Ba C, Privat A, Hugnot J-P. 2006. Exogenous and fibroblast growth factor 2/epidermal growth factor-regulated endogenous cytokines regulate neural precursor cell growth and differentiation. Stem Cells. 24:748-762. (Pubitemid 44464780)
13. Dogini D, Ribeiro P, Rocha C, Pereira T, Lopes-Cendes I. 2008. MicroRNA expression profile in murine central nervous system development. J Mol Neurosci. 35(3):331-337.
14. Ebendal T, Bengtsson H, Soderstrom S. 1998. Bone morphogenetic proteins and their receptors: potential functions in the brain. J Neurosci Res. 51:139-146. (Pubitemid 28073021)
15. Esquenazi S, Monnerie H, Kaplan P, Le Roux P. 2002. BMP-7 and excess glutamate: opposing effects on dendrite growth from cerebral cortical neurons in vitro. Exp Neurol. 176:41-54. (Pubitemid 34762104)
16. Fiore R, Khudayberdiev S, Christensen M, Siegel G, Flavell SW, Kim TK, Greenberg ME, Schratt G. 2009. Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels. EMBO J. 28:697-710.
17. Fortunel NO, Otu HH, Ng HH, Chen J, Mu X, Chevassut T, Li X, Joseph M, Bailey C, Hatzfeld JA, et al. 2003. Comment on "'Stemness': transcriptional profiling of embryonic and adult stem cells' and "a stem cell molecular signature". Science. 302:393; author reply 393.
18. Friocourt G, Liu J, Antypa M, Rakic S, Walsh C, Parnavelas J. 2007. Both doublecortin and doublecortin-like kinase play a role in cortical interneuron migration. J Neurosci. 27:3875-3883. (Pubitemid 46557665)
19. Furuta Y, Piston DW, Hogan BL. 1997. Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development. 124:2203-2212. (Pubitemid 27283241)
20. Gleeson J, Allen KM, Fox JW, Lamperti ED, Berkovic S, Scheffer I, Cooper EC, Dobyns WB, Minnerath SR, Ross ME, et al. 1998. Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell. 92:63-72. (Pubitemid 28053298)
21. Graham V, Khudyakov J, Ellis P, Pevny L. 2003. SOX2 functions to maintain neural progenitor identity. Neuron. 39:749-765. (Pubitemid 37088088)
22. Guillemot F, Molnar Z, Tarabykin V, Stoykova A. 2006. Molecular mechanisms of cortical differentiation. Eur J Neurosci. 23:857-868. (Pubitemid 43348549)
23. Hack MA, Sugimori M, Lundberg C, Nakafuku M, Gotz M. 2004. Regionalization and fate specification in neurospheres: the role of Olig2 and Pax6. Mol Cell Neurosci. 25:664-678. (Pubitemid 38481475)
24. Hassoun AT, Erdelyi F, Szabo G, Davis MI. 2007. A rapid screening method for population-specific neuronal motogens, substrates and associated signaling pathways. J Neurosci Methods. 166:178-194. (Pubitemid 350016397)
25. He L, Hannon GJ. 2004. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet. 5:522-531. (Pubitemid 38868508)
26. Hohjoh H, Fukushima T. 2007. Expression profile analysis of microRNA (miRNA) in mouse central nervous system using a new miRNA detection system that examines hybridization signals at every step of washing. Gene. 391:39-44. (Pubitemid 46356784)
27. Horisawa K, Imai T, Okano H, Yanagawa H. 2009. 3'-Untranslated region of doublecortin mRNA is a binding target of the Musashi1 RNA-binding protein. FEBS Lett. 583:2429-2434.
28. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 4:249-264.
29. Ivanova NB, Dimos JT, Schaniel C, Hackney JA, Moore KA, Lemischka IR. 2002. A stem cell molecular signature. Science. 298:601-604.
30. Kapsimali M, Kloosterman WP, de Bruijn E, Rosa F, Plasterk RHA, Wilson SW. 2007. MicroRNAs show a wide diversity of expression profiles in the developing and mature central nervous system. Genome Biol. 8:R173.
31. Khudayberdiev S, Fiore R, Schratt G. 2009. MicroRNA as modulators of neuronal responses. Commun Integr Biol. 2:411-413.
32. Larman BW, Karolak MJ, Adams DC, Oxburgh L. 2009. Chordin-like 1 and twisted gastrulation 1 regulate BMP signaling following kidney injury. J Am Soc Nephrol. 20:1020-1031.
33. Leucht C, Stigloher C, Wizenmann A, Klafke R, Folchert A, Bally-Cuif L. 2008. MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nat Neurosci. 11:641-648. (Pubitemid 351748112)
34. Li W, Loturco J. 2000. Noggin is a negative regulator of neuronal differentiation in developing neocortex. Dev Neurosci. 22:68-73. (Pubitemid 30098907)
35. Liu A, Niswander L. 2005. Bone morphogenetic protein signalling and vertebrate nervous system development. Nat Rev Neurosci. 6:945-954. (Pubitemid 41753088)
36. Ma L, Teruya-Feldstein J, Weinberg R. 2007. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 449:682-688. (Pubitemid 47552092)
37. Mabie PC, Mehler MF, Kessler JA. 1999. Multiple roles of bone morphogenetic protein signaling in the regulation of cortical cell number and phenotype. J Neurosci. 19:7077-7088. (Pubitemid 29380133)
38. Marin O, Rubenstein JLR. 2003. Cell migration in the forebrain. Annu Rev Neurosci. 26:441-483. (Pubitemid 37064941)
39. McMahon JA, Takada S, Zimmerman LB, Fan CM, Harland RM, McMahon AP. 1998. Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev. 12:1438-1452. (Pubitemid 28243629)
40. Mehler MF, Mabie PC, Zhu G, Gokhan S, Kessler JA. 2000. Developmental changes in progenitor cell responsiveness to bone morphogenetic proteins differentially modulate progressive CNS lineage fate. Dev Neurosci. 22:74-85. (Pubitemid 30098908)
41. Miranda K, Huynh T, Tay Y, Ang Y, Tam W, Thomson A, Lim B, Rigoutsos I. 2006. A pattern-based method for the identification of microRNA binding sites and their corresponding heteroduplexes. Cell. 126:1203-1217. (Pubitemid 44380294)
42. Miska EA, Alvarez-Saavedra E, Townsend M, Yoshii A, Sestan N, Rakic P, Constantine-Paton M, Horvitz HR. 2004. Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol. 5:R68.
43. Ocbina PJ, Dizon MLV, Shin L, Szele FG. 2006. Doublecortin is necessary for the migration of adult subventricular zone cells from neuro-spheres. Mol Cell Neurosci. 33:126-135. (Pubitemid 44430059)
44. Rakic P, Hashimoto-Torii K, Sarkisian MR. 2007. Genetic determinants of neuronal migration in the cerebral cortex. Novartis Found Symp. 288:45-53; discussion. 53-48, 96-148.
45. Ramos RL, Bai J, LoTurco JJ. 2006. Heterotopia formation in rat but not mouse neocortex after RNA interference knockdown of DCX. Cereb Cortex. 16:1323-1331. (Pubitemid 44289105)
46. Rao MS, Shetty AK. 2004. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur J Neurosci. 19:234-246. (Pubitemid 38177862)
47. Saito T. 2001. Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev Biol. 240:237-246. (Pubitemid 33141120)
48. Sakuta H. 2001. Ventroptin: a BMP-4 antagonist expressed in a double-gradient pattern in the retina. Science. 293:111-115. (Pubitemid 32625506)
49. Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME, Kiebler M, Greenberg ME. 2006. A brain-specific microRNA regulates dendritic spine development. Nature. 439:283-289. (Pubitemid 43128846)
50. Seitz H, Royo H, Bortolin M, Lin S, Ferguson-Smith AC, Cavaille J. 2004. A large imprinted microRNA gene cluster at the mouse Dlk1-Gtl2 domain. Genome Res. 14:1741-1748. (Pubitemid 39276432)
51. Shibata M, Kurokawa D, Nakao H, Ohmura T, Aizawa S. 2008. MicroRNA-9 modulates Cajal-Retzius cell differentiation by suppressing Foxg1 expression in mouse medial pallium. J Neurosci. 28:10415-10421.
52. Sim F, Lang J, Waldau B, Roy N, Schwartz T, Pilcher W, Chandross K, Natesan S, Merrill J, Goldmanm S. 2006. Complementary patterns of gene expression by human oligodendrocyte progenitors and their environment predict determinants of progenitor maintenance and differentiation. Ann Neurol. 59:763-779. (Pubitemid 43673154)
53. Smirnova L, Grafe A, Seiler A, Schumacher S, Nitsch R, Wulczyn FG. 2005. Regulation of miRNA expression during neural cell specification. Eur J Neurosci. 21:1469-1477. (Pubitemid 40646593)
54. Tabata H, Nakajima K. 2008. Labeling embryonic mouse central nervous system cells by in uteroelectroporation. Dev Growth Differ. 50:507-511.
55. Tay YM, Tam W, Ang Y, Gaughwin PM, Yang H, Wang W, Liu R, George J, Ng H, Perera RJ, et al. 2008. MicroRNA-134 modulates the differentiation of mouse embryonic stem cells, where it causes post-transcriptional attenuation of Nanog and LRH1. Stem Cells. 26:17-29.
56. Tay YM, Zhang J, Thomson A, Lim B, Rigoutsos I. 2008. MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature. 455:1124-1128.
57. Ueki T, Tanaka M, Yamashita K, Mikawa S, Qiu Z, Maragakis NJ, Hevner RF, Miura N, Sugimura H, Sato K. 2003. A novel secretory factor, neurogenesin-1, provides neurogenic environmental cues for neural stem cells in the adult hippocampus. J Neurosci. 23:11732-11740. (Pubitemid 38021300)
58. Walker T, Yasuda T, Adams D, Bartlett P. 2007. The doublecortin- expressing population in the developing and adult brain contains multipotential precursors in addition to neuronal-lineage cells. J Neurosci. 27:3734-3742. (Pubitemid 46557670)
59. Walsh CA. 2000. Genetics of neuronal migration in the cerebral cortex. Ment Retard Dev Disabil Res Rev. 6:34-40. (Pubitemid 30141810)
60. Withers GS, Higgins D, Charette M, Banker G. 2000. Bone morphoge-netic protein-7 enhances dendritic growth and receptivity to innervation in cultured hippocampal neurons. Eur J Neurosci. 12:106-116. (Pubitemid 30068416)
61. Yung S, Gokhan S, Jurcsak J, Molero AE, Abrajano JJ, Mehler MF. 2002. Differential modulation of BMP signaling promotes the elaboration of cerebral cortical GABAergic neurons or oligodendrocytes from a common sonic hedgehog-responsive ventral forebrain progenitor species. Proc Natl Acad Sci USA. 99:16273-16278. (Pubitemid 35462785)