Temporally defined neocortical translation and polysome assembly are determined by the RNA-binding protein Hu antigen R

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 36, 2014, Pages E3815-E3824

  Kraushar, Matthew L ^a   Thompson, Kevin ^a   Wijeratne, H R Sagara ^a   Viljetic, Barbara ^a   Sakers, Kristina ^a   Marson, Justin W ^a   Kontoyiannis, Dimitris L ^b   Buyske, Steven ^c   Hart, Ronald P ^c   Rasin, Mladen Roko ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b BIOMEDICAL SCIENCES RESEARCH CENTER ALEXANDER FLEMING   (Greece)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

Elav; GCN2; Posttranscriptional regulation; Profiling; Ribosome

Indexed keywords

EIF2AK4 PROTEIN, MOUSE; ELAV LIKE PROTEIN 1; ELAV PROTEIN; ELAVL1 PROTEIN, HUMAN; INITIATION FACTOR 2; MESSENGER RNA; PROTEIN SERINE THREONINE KINASE; RIBOSOME PROTEIN; RNA BINDING PROTEIN;

ANIMAL; BIOLOGICAL MODEL; CORPUS CALLOSUM; CYTOLOGY; EMBRYOLOGY; GENE DELETION; GENE INACTIVATION; GENETIC TRANSCRIPTION; GENETICS; GLIA; METABOLISM; MITOSIS; MOUSE; NEOCORTEX; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROEPITHELIUM CELL; PHOSPHORYLATION; POLYSOME; PROTEIN SYNTHESIS; TIME;

ANIMALS; CORPUS CALLOSUM; ELAV PROTEINS; ELAV-LIKE PROTEIN 1; EUKARYOTIC INITIATION FACTOR-2; GENE DELETION; GENE KNOCKOUT TECHNIQUES; MICE; MITOSIS; MODELS, BIOLOGICAL; NEOCORTEX; NEURAL STEM CELLS; NEUROEPITHELIAL CELLS; NEUROGENESIS; NEUROGLIA; NEURONS; PHOSPHORYLATION; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; PROTEIN-SERINE-THREONINE KINASES; RIBOSOMAL PROTEINS; RNA, MESSENGER; RNA-BINDING PROTEINS; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 84906968560     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1408305111     Document Type: Article

References (45)

1. Molyneaux BJ, Arlotta P, Menezes JRL, Macklis JD (2007) Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8(6):427-437.
2. Rakic P (2009) Evolution of the neocortex: A perspective from developmental biology. Nat Rev Neurosci 10(10):724-735.
3. Rasin M-R, et al. (2007) Numb and Numbl are required for maintenance of cadherin-based adhesion and polarity of neural progenitors. Nat Neurosci 10(7):819-827.
4. Kwan KY, Sestan N, Anton ES (2012) Transcriptional co-regulation of neuronal migration and laminar identity in the neocortex. Development 139(9):1535-1546.
5. Deboer EM, Kraushar ML, Hart RP, Rasin M-R (2013) Post-transcriptional regulatory elements and spatiotemporal specification of neocortical stem cells and projection neurons. Neuroscience 248C:499-528.
6. Leone DP, Srinivasan K, Chen B, Alcamo E, McConnell SK (2008) The determination of projection neuron identity in the developing cerebral cortex. Curr Opin Neurobiol 18(1):28-35.
7. Greig LC, Woodworth MB, Galazo MJ, Padmanabhan H, Macklis JD (2013) Molecular logic of neocortical projection neuron specification, development and diversity. Nat Rev Neurosci 14(11):755-769.
8. Saffary R, Xie Z (2011) FMRP regulates the transition from radial glial cells to intermediate progenitor cells during neocortical development. J Neurosci 31(4):1427-1439.
9. Yano M, Hayakawa-Yano Y, Mele A, Darnell RB (2010) Nova2 regulates neuronal migration through an RNA switch in disabled-1 signaling. Neuron 66(6):848-858.
10. Kusek G, et al. (2012) Asymmetric segregation of the double-stranded RNA binding protein Staufen2 during mammalian neural stem cell divisions promotes lineage progression. Cell Stem Cell 11(4):505-516.
11. Silver DL, et al. (2010) The exon junction complex component Magoh controls brain size by regulating neural stem cell division. Nat Neurosci 13(5):551-558.
12. Darnell RB (2013) RNA protein interaction in neurons. Annu Rev Neurosci 36:243-270.
13. Schwanhäusser B, et al. (2011) Global quantification of mammalian gene expression control. Nature 473(7347):337-342.
14. Kwan KY, et al. (2012) Species-dependent posttranscriptional regulation of NOS1 by FMRP in the developing cerebral cortex. Cell 149:899-911.
15. Keene JD (2007) RNA regulons: Coordination of post-transcriptional events. Nat Rev Genet 8(7):533-543.
16. Kong J, Lasko P (2012) Translational control in cellular and developmental processes. Nat Rev Genet 13(6):383-394.
17. Mathews M, Sonenberg N, Hershey J, eds (2007) Translational Control in Biology and Medicine (Cold Spring Harbor Lab Press, Cold Spring Harbor, NY).
18. Jackson RJ, Hellen CUT, Pestova TV (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11(2):113-127.
19. Barna M (2013) Ribosomes take control. Proc Natl Acad Sci USA 110(1):9-10.
20. Mukherjee N, et al. (2011) Integrative regulatory mapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability. Mol Cell 43(3):327-339.
21. Lebedeva S, et al. (2011) Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein HuR. Mol Cell 43(3):340-352.
22. Katsanou V, et al. (2005) HuR as a negative posttranscriptional modulator in inflammation. Mol Cell 19(6):777-789.
23. Ayoub AE, et al. (2011) Transcriptional programs in transient embryonic zones of the cerebral cortex defined by high-resolution mRNA sequencing. Proc Natl Acad Sci USA 108(36):14950-14955.
24. Miller JA, et al. (2014) Transcriptional landscape of the prenatal human brain. Nature 508(7495):199-206.
25. Bystron I, Blakemore C, Rakic P (2008) Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci 9(2):110-122.
26. García-Domínguez DJ, Morello D, Cisneros E, Kontoyiannis DL, Frade JM (2011) Stabilization of Dll1 mRNA by Elavl1/HuR in neuroepithelial cells undergoing mitosis. Mol Biol Cell 22(8):1227-1239.
27. Srikantan S, Gorospe M (2012) HuR function in disease. Front Biosci (Landmark Ed) 17:189-205.
28. Darnell JC, et al. (2011) FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146:247-261.
29. Esposito AM, et al. (2010) Eukaryotic polyribosome profile analysis. J Vis Exp (40):5-8.
30. Trapnell C, et al. (2012) Differential gene and transcript expression analysis of RNAseq experiments with TopHat and Cufflinks. Nat Protoc 7(3):562-578.
31. Gorski JA, et al. (2002) Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J Neurosci 22:6309-14.
32. Katsanou V, et al. (2009) The RNA-binding protein Elavl1/HuR is essential for placental branching morphogenesis and embryonic development. Mol Cell Biol 29(10):2762-2776.
33. Huang W, Sherman BT, Lempicki RA (2009) Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37(1):1-13.
34. Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44-57.
35. Belgard TG, et al. (2011) A transcriptomic atlas of mouse neocortical layers. Neuron 71(4):605-616.
36. Sivan G, Kedersha N, Elroy-Stein O (2007) Ribosomal slowdown mediates translational arrest during cellular division. Mol Cell Biol 27(19):6639-6646.
37. Ramirez M, Wek RC, Hinnebusch AG (1991) Ribosome association of GCN2 protein kinase, a translational activator of the GCN4 gene of Saccharomyces cerevisiae. Mol Cell Biol 11(6):3027-3036.
38. Chou S-J, Perez-Garcia CG, Kroll TT, O'Leary DDM (2009) Lhx2 specifies regional fate in Emx1 lineage of telencephalic progenitors generating cerebral cortex. Nat Neurosci 12:1381-1389.
39. Niquille M, et al. (2009) Transient neuronal populations are required to guide callosal axons: A role for semaphorin 3C. PLoS Biol 7:e1000230.
40. Shu T, Richards LJ (2001) Cortical axon guidance by the glial wedge during the development of the corpus callosum. J Neurosci 21:2749-2758.
41. Vattem KM, Wek RC (2004) Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc Natl Acad Sci USA 101(31):11269-11274.
42. Zhou D, et al. (2008) Phosphorylation of eIF2 directs ATF5 translational control in response to diverse stress conditions. J Biol Chem 283(11):7064-7073.
43. DeBoer EM, et al. (2014) Prenatal deletion of the RNA-binding protein HuD disrupts postnatal cortical circuit maturation and behavior. J Neurosci 34(10):3674-3686.
44. Anderson M (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32-46.
45. McArdle B, Anderson M (2001) Fitting multivariate models to community data: A comment on distance-based redundancy analysis. Ecology 82:290-297.