Transcriptome analysis of embryonic and adult sensory axons reveals changes in mRNA repertoire localization

被引:295
作者
Gumy, Laura F. [1 ]
Yeo, Giles S. H. [6 ]
Tung, Yi-Chun Loraine [6 ]
Zivraj, Krishna H. [2 ]
Willis, Dianna [3 ]
Coppola, Giovanni [4 ]
Lam, Brian Y. H. [6 ]
Twiss, Jeffery L. [5 ]
Holt, Christine E. [2 ]
Fawcett, James W. [1 ]
机构
[1] Univ Cambridge, Ctr Brain Repair, Cambridge CB2 0PY, England
[2] Univ Cambridge, Dept Physiol Dev & Neurosci, Cambridge CB2 3DY, England
[3] Burke Cornell Med Res Inst, White Plains, NY 10605 USA
[4] Univ Calif Los Angeles, David Geffen Sch Med, Dept Neurol, Program Neurogenet, Los Angeles, CA 90095 USA
[5] Drexel Univ, Dept Biol, Philadelphia, PA 19401 USA
[6] Univ Cambridge, Metab Res Labs, Inst Metab Sci, Addenbrookes Hosp, Cambridge CB2 0QQ, England
基金
英国医学研究理事会;
关键词
axon regeneration; local protein synthesis; microarray; dorsal root ganglion neurons; pain; development; mRNA; MICROTUBULE-ASSOCIATED PROTEIN-1B; LOCAL TRANSLATION; GROWTH CONES; NEURONAL MIGRATION; ACTIN; EXPRESSION; BINDING; NEUROTROPHINS; CYTOSKELETAL; INFLAMMATION;
D O I
10.1261/rna.2386111
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
mRNAs are transported, localized, and translated in axons of sensory neurons. However, little is known about the full repertoire of transcripts present in embryonic and adult sensory axons and how this pool of mRNAs dynamically changes during development. Here, we used a compartmentalized chamber to isolate mRNA from pure embryonic and adult sensory axons devoid of non-neuronal or cell body contamination. Genome-wide microarray analysis reveals that a previously unappreciated number of transcripts are localized in sensory axons and that this repertoire changes during development toward adulthood. Embryonic axons are enriched in transcripts encoding cytoskeletal-related proteins with a role in axonal outgrowth. Surprisingly, adult axons are enriched in mRNAs encoding immune molecules with a role in nociception. Additionally, we show Tubulin-beta3 (Tubb3) mRNA is present only in embryonic axons, with Tubb3 locally synthesized in axons of embryonic, but not adult neurons where it is transported, thus validating our experimental approach. In summary, we provide the first complete catalog of embryonic and adult sensory axonal mRNAs. In addition we show that this pool of axonal mRNAs dynamically changes during development. These data provide an important resource for studies on the role of local protein synthesis in axon regeneration and nociception during neuronal development.
引用
收藏
页码:85 / 98
页数:14
相关论文
共 62 条
[1]   Chemokines, chemokine receptors and pain [J].
Abbadie, C .
TRENDS IN IMMUNOLOGY, 2005, 26 (10) :529-534
[2]   An NGF-responsive element targets myo-inositol monophosphatase-1 mRNA to sympathetic neuron axons [J].
Andreassi, Catia ;
Zimmermann, Carola ;
Mitter, Richard ;
Fusco, Salvatore ;
Devita, Serena ;
Saiardi, Adolfo ;
Riccio, Antonella .
NATURE NEUROSCIENCE, 2010, 13 (03) :291-U6
[3]   Regulation of axonal trafficking of cytochrome c oxidase IV mRNA [J].
Aschrafi, Armaz ;
Natera-Naranjo, Orlangie ;
Gioio, Anthony E. ;
Kaplan, Barry B. .
MOLECULAR AND CELLULAR NEUROSCIENCE, 2010, 43 (04) :422-430
[4]   MicroRNA-338 Regulates Local Cytochrome c Oxidase IV mRNA Levels and Oxidative Phosphorylation in the Axons of Sympathetic Neurons [J].
Aschrafi, Armaz ;
Schwechter, Azik D. ;
Mameza, Marie G. ;
Natera-Naranjo, Orlangie ;
Gioio, Anthony E. ;
Kaplan, Barry B. .
JOURNAL OF NEUROSCIENCE, 2008, 28 (47) :12581-12590
[5]   Mechanisms of Disease: neuropathic pain - a clinical perspective [J].
Baron, R .
NATURE CLINICAL PRACTICE NEUROLOGY, 2006, 2 (02) :95-106
[6]  
Bassell GJ, 1998, J NEUROSCI, V18, P251
[7]   ASSOCIATION OF POLY(A) MESSENGER-RNA WITH MICROTUBULES IN CULTURED NEURONS [J].
BASSELL, GJ ;
SINGER, RH ;
KOSIK, KS .
NEURON, 1994, 12 (03) :571-582
[8]  
BLACK MM, 1994, J NEUROSCI, V14, P857
[9]   Profilin2 contributes to synaptic vesicle exocytosis, neuronal excitability, and novelty-seeking behavior [J].
Boyl, Pietro Pilo ;
Di Nardo, Alessia ;
Mulle, Christophe ;
Sassoe-Pognetto, Marco ;
Panzanelli, Patrizia ;
Mele, Andrea ;
Kneussel, Matthias ;
Costantini, Vivian ;
Perlas, Emerald ;
Massimi, Marzia ;
Vara, Hugo ;
Giustetto, Maurizio ;
Witke, Walter .
EMBO JOURNAL, 2007, 26 (12) :2991-3002
[10]   The ability of axons to regenerate their growth cones depends on axonal type and age, and is regulated by calcium, cAMP and ERK [J].
Chierzi, S ;
Ratto, GM ;
Verma, P ;
Fawcett, JW .
EUROPEAN JOURNAL OF NEUROSCIENCE, 2005, 21 (08) :2051-2062