Subcellular transcriptomes and proteomes of developing axon projections in the cerebral cortex.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
01 2019
01 2019
Historique:
received:
20
10
2016
accepted:
05
12
2018
pubmed:
11
1
2019
medline:
16
7
2019
entrez:
11
1
2019
Statut:
ppublish
Résumé
The development of neural circuits relies on axon projections establishing diverse, yet well-defined, connections between areas of the nervous system. Each projection is formed by growth cones-subcellular specializations at the tips of growing axons, encompassing sets of molecules that control projection-specific growth, guidance, and target selection
Identifiants
pubmed: 30626971
doi: 10.1038/s41586-018-0847-y
pii: 10.1038/s41586-018-0847-y
pmc: PMC6484835
mid: NIHMS1022743
doi:
Substances chimiques
Proteome
0
TOR Serine-Threonine Kinases
EC 2.7.11.1
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
356-360Subventions
Organisme : NINDS NIH HHS
ID : R01 NS049553
Pays : United States
Organisme : NINDS NIH HHS
ID : R37 NS041590
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS041590
Pays : United States
Organisme : NIA NIH HHS
ID : T32 AG000222
Pays : United States
Organisme : NIH HHS
ID : NS041590
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS045523
Pays : United States
Organisme : NIH HHS
ID : NS045523
Pays : United States
Organisme : NIH HHS
ID : NS075672
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS075672
Pays : United States
Organisme : NINDS NIH HHS
ID : DP1 NS106665
Pays : United States
Organisme : NIH HHS
ID : NS049553
Pays : United States
Références
Lowery, L. A. & Van Vactor, D. The trip of the tip: understanding the growth cone machinery. Nat. Rev. Mol. Cell Biol. 10, 332–343 (2009).
doi: 10.1038/nrm2679
Saxton, R. A. & Sabatini, D. M. mTOR signaling in growth, metabolism, and disease. Cell 168, 960–976 (2017).
doi: 10.1016/j.cell.2017.02.004
Meyuhas, O., Avni, D. & Shama, S. Translational control of ribosomal protein mRNAs in eukaryotes. 30, 363–388 (1996).
Fonseca, B. D. et al. La-related protein 1 (LARP1) represses terminal oligopyrimidine (TOP) mRNA translation downstream of mTOR complex 1 (mTORC1). J. Biol. Chem. 290, 15996–16020 (2015).
doi: 10.1074/jbc.M114.621730
Greig, L. C., Woodworth, M. B., Galazo, M. J., Padmanabhan, H. & Macklis, J. D. Molecular logic of neocortical projection neuron specification, development and diversity. Nat. Rev. Neurosci. 14, 755–769 (2013).
doi: 10.1038/nrn3586
Pfenninger, K. H., Ellis, L., Johnson, M. P., Friedman, L. B. & Somlo, S. Nerve growth cones isolated from fetal rat brain: subcellular fractionation and characterization. Cell 35, 573–584 (1983).
doi: 10.1016/0092-8674(83)90191-5
Lohse, K. et al. Axonal origin and purity of growth cones isolated from fetal rat brain. Brain Res. Dev. Brain Res. 96, 83–96 (1996).
doi: 10.1016/0165-3806(96)00076-4
Fame, R. M., MacDonald, J. L. & Macklis, J. D. Development, specification, and diversity of callosal projection neurons. Trends Neurosci. 34, 41–50 (2011).
doi: 10.1016/j.tins.2010.10.002
Greig, L. C., Woodworth, M. B., Greppi, C. & Macklis, J. D. Ctip1 controls acquisition of sensory area identity and establishment of sensory input fields in the developing neocortex. Neuron 90, 261–277 (2016).
doi: 10.1016/j.neuron.2016.03.008
Llorca, O. et al. Eukaryotic type II chaperonin CCT interacts with actin through specific subunits. Nature 402, 693–696 (1999).
doi: 10.1038/45294
Moccia, R. et al. An unbiased cDNA library prepared from isolated Aplysia sensory neuron processes is enriched for cytoskeletal and translational mRNAs. J. Neurosci. 23, 9409–9417 (2003).
doi: 10.1523/JNEUROSCI.23-28-09409.2003
Leung, K.-M. et al. Asymmetrical beta-actin mRNA translation in growth cones mediates attractive turning to netrin-1. Nat. Neurosci. 9, 1247–1256 (2006).
doi: 10.1038/nn1775
Crino, P. B. & Eberwine, J. Molecular characterization of the dendritic growth cone: regulated mRNA transport and local protein synthesis. Neuron 17, 1173–1187 (1996).
doi: 10.1016/S0896-6273(00)80248-2
Taylor, A. M. et al. Axonal mRNA in uninjured and regenerating cortical mammalian axons. J. Neurosci. 29, 4697–4707 (2009).
doi: 10.1523/JNEUROSCI.6130-08.2009
Zivraj, K. H. et al. Subcellular profiling reveals distinct and developmentally regulated repertoire of growth cone mRNAs. J. Neurosci. 30, 15464–15478 (2010).
doi: 10.1523/JNEUROSCI.1800-10.2010
Jung, H., Yoon, B. C. & Holt, C. E. Axonal mRNA localization and local protein synthesis in nervous system assembly, maintenance and repair. Nat. Rev. Neurosci. 13, 308–324 (2012).
doi: 10.1038/nrn3210
Catapano, L. A., Arnold, M. W., Perez, F. A. & Macklis, J. D. Specific neurotrophic factors support the survival of cortical projection neurons at distinct stages of development. J. Neurosci. 21, 8863–8872 (2001).
doi: 10.1523/JNEUROSCI.21-22-08863.2001
Arlotta, P. et al. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45, 207–221 (2005).
doi: 10.1016/j.neuron.2004.12.036
Özdinler, P. H. & Macklis, J. D. IGF-I specifically enhances axon outgrowth of corticospinal motor neurons. Nat. Neurosci. 9, 1371–1381 (2006).
doi: 10.1038/nn1789
Meyuhas, O. & Kahan, T. The race to decipher the top secrets of TOP mRNAs. Biochim. Biophys. Acta 1849, 801–811 (2015).
doi: 10.1016/j.bbagrm.2014.08.015
Geiger, T., Wehner, A., Schaab, C., Cox, J. & Mann, M. Comparative proteomic analysis of eleven common cell lines reveals ubiquitous but varying expression of most proteins. Mol. Cell. Proteomics 11, M111.014050 (2012).
doi: 10.1074/mcp.M111.014050
Liebermeister, W. et al. Visual account of protein investment in cellular functions. Proc. Natl Acad. Sci. USA 111, 8488–8493 (2014).
doi: 10.1073/pnas.1314810111
Tang, H. et al. Amino acid-induced translation of TOP mRNAs is fully dependent on phosphatidylinositol 3-kinase-mediated signaling, is partially inhibited by rapamycin, and is independent of S6K1 and rpS6 phosphorylation. Mol. Cell. Biol. 21, 8671–8683 (2001).
doi: 10.1128/MCB.21.24.8671-8683.2001
Thoreen, C. C. et al. A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 485, 109–113 (2012).
doi: 10.1038/nature11083
Laplante, M. & Sabatini, D. M. mTOR signaling in growth control and disease. Cell 149, 274–293 (2012).
doi: 10.1016/j.cell.2012.03.017
Kye, M. J. et al. SMN regulates axonal local translation via miR-183/mTOR pathway. Hum. Mol. Genet. 23, 6318–6331 (2014).
doi: 10.1093/hmg/ddu350
Tcherkezian, J. et al. Proteomic analysis of cap-dependent translation identifies LARP1 as a key regulator of 5'TOP mRNA translation. Genes Dev. 28, 357–371 (2014).
doi: 10.1101/gad.231407.113
Dhand, R. et al. PI 3-kinase: structural and functional analysis of intersubunit interactions. EMBO J. 13, 511–521 (1994).
doi: 10.1002/j.1460-2075.1994.tb06289.x
Itoh, Y. et al. PDK1-Akt pathway regulates radial neuronal migration and microtubules in the developing mouse neocortex. Proc. Natl Acad. Sci. USA 113, E2955–E2964 (2016).
doi: 10.1073/pnas.1516321113
Lu, Y., Belin, S. & He, Z. Signaling regulations of neuronal regenerative ability. Curr. Opin. Neurobiol. 27, 135–142 (2014).
doi: 10.1016/j.conb.2014.03.007
Okabe, M., Ikawa, M., Kominami, K., Nakanishi, T. & Nishimune, Y. ‘Green mice’ as a source of ubiquitous green cells. FEBS Lett. 407, 313–319 (1997).
doi: 10.1016/S0014-5793(97)00313-X
Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133–140 (2010).
doi: 10.1038/nn.2467
Gallardo, T., Shirley, L., John, G. B. & Castrillon, D. H. Generation of a germ cell-specific mouse transgenic Cre line, Vasa-Cre. Genesis 45, 413–417 (2007).
doi: 10.1002/dvg.20310
Risson, V. et al. Muscle inactivation of mTOR causes metabolic and dystrophin defects leading to severe myopathy. J. Cell Biol. 187, 859–874 (2009).
doi: 10.1083/jcb.200903131
Rhee, J. M. et al. In vivo imaging and differential localization of lipid-modified GFP-variant fusions in embryonic stem cells and mice. Genesis 44, 202–218 (2006).
doi: 10.1002/dvg.20203
Matsuda, T. & Cepko, C. L. Electroporation and RNA interference in the rodent retina in vivo and in vitro. Proc. Natl Acad. Sci. USA 101, 16–22 (2004).
doi: 10.1073/pnas.2235688100
Saito, T. & Nakatsuji, N. Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev. Biol. 240, 237–246 (2001).
doi: 10.1006/dbio.2001.0439
Biesemann, C. et al. Proteomic screening of glutamatergic mouse brain synaptosomes isolated by fluorescence activated sorting. EMBO J. 33, 157–170 (2014).
doi: 10.1002/embj.201386120
Catapano, L. A., Arlotta, P., Cage, T. A. & Macklis, J. D. Stage-specific and opposing roles of BDNF, NT-3 and bFGF in differentiation of purified callosal projection neurons toward cellular repair of complex circuitry. Eur. J. Neurosci. 19, 2421–2434 (2004).
doi: 10.1111/j.0953-816X.2004.03303.x
Molyneaux, B. J. et al. Novel subtype-specific genes identify distinct subpopulations of callosal projection neurons. J. Neurosci. 29, 12343–12354 (2009).
doi: 10.1523/JNEUROSCI.6108-08.2009
Galazo, M. J., Emsley, J. G. & Macklis, J. D. Corticothalamic projection neuron development beyond subtype specification: Fog2 and intersectional controls regulate intraclass neuronal diversity. Neuron 91, 90–106 (2016).
doi: 10.1016/j.neuron.2016.05.024
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
doi: 10.1093/bioinformatics/bts635
Patro, R., Mount, S. M. & Kingsford, C. Sailfish enables alignment-free isoform quantification from RNA-seq reads using lightweight algorithms. Nat. Biotechnol. 32, 462–464 (2014).
doi: 10.1038/nbt.2862
Okonechnikov, K., Conesa, A. & García-Alcalde, F. Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data. Bioinformatics 32, 292–294 (2016).
pubmed: 26428292
Cox, J. et al. Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol. Cell. Proteomics 13, 2513–2526 (2014).
doi: 10.1074/mcp.M113.031591
Tyanova, S. et al. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat. Methods 13, 731–740 (2016).
doi: 10.1038/nmeth.3901
Berriz, G. F. & Roth, F. P. The Synergizer service for translating gene, protein and other biological identifiers. Bioinformatics 24, 2272–2273 (2008).
doi: 10.1093/bioinformatics/btn424
Binder, J. X. et al. COMPARTMENTS: unification and visualization of protein subcellular localization evidence. Database (Oxford) 2014, bau012 (2014).
doi: 10.1093/database/bau012
Szklarczyk, D. et al. STRING v10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 43, D447–D452 (2015).
doi: 10.1093/nar/gku1003
Cox, J. & Mann, M. 1D and 2D annotation enrichment: a statistical method integrating quantitative proteomics with complementary high-throughput data. BMC Bioinformatics 13 (Suppl. 16), S12 (2012).
doi: 10.1186/1471-2105-13-S16-S12
Spandidos, A., Wang, X., Wang, H. & Seed, B. PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res. 38, D792–D799 (2010).
doi: 10.1093/nar/gkp1005
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
doi: 10.1038/nmeth.2019