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The Journal of Neuroscience, January 26, 2005, 25(4):778-791; doi:10.1523/JNEUROSCI.4235-04.2005

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Development/Plasticity/Repair
Differential Transport and Local Translation of Cytoskeletal, Injury-Response, and Neurodegeneration Protein mRNAs in Axons

Dianna Willis,^1 * Ka Wan Li,^2 * Jun-Qi Zheng,¹ Jay H. Chang,⁴ August Smit,² Theresa Kelly,³ Tanuja T. Merianda,¹ James Sylvester,⁵ Jan van Minnen,² and Jeffery L. Twiss^1,6

¹Nemours Biomedical Research, Alfred I. DuPont Hospital for Children, Wilmington, Delaware 19803, ²Department of Molecular and Cellular Neurobiology, Faculty of Earth and Life Sciences, Vrije Universiteit, 1081 HV Amsterdam, The Netherlands, ³Neuroscience and ⁴Cellular and Molecular Pathology Graduate Programs, University of California Los Angeles, Los Angeles, California 90095, ⁵Nemours Biomedical Research, Jacksonville, Florida 32247, and ⁶Department of Biological Sciences, University of Delaware, Newark, Delaware 19716

Recent studies have begun to focus on the signals that regulate axonal protein synthesis and the functional significance of localized protein synthesis. However, identification of proteins that are synthesized in mammalian axons has been mainly based on predictions. Here, we used axons purified from cultures of injury-conditioned adult dorsal root ganglion (DRG) neurons and proteomics methodology to identify axonally synthesized proteins. Reverse transcription (RT)-PCR from axonal preparations was used to confirm that the mRNA for each identified protein extended into the DRG axons. Proteins and the encoding mRNAs for the cytoskeletal proteins -actin, peripherin, vimentin, -tropomyosin 3, and cofilin 1 were present in the axonal preparations. In addition to the cytoskeletal elements, several heat shock proteins (HSP27, HSP60, HSP70, grp75, B crystallin), resident endoplasmic reticulum (ER) proteins (calreticulin, grp78/BiP, ERp29), proteins associated with neurodegenerative diseases (ubiquitin C-terminal hydrolase L1, rat ortholog of human DJ-1/Park7, -synuclein, superoxide dismutase 1), anti-oxidant proteins (peroxiredoxins 1 and 6), and metabolic proteins (e.g., phosphoglycerate kinase 1 (PGK 1), enolase, aldolase C/Zebrin II) were included among the axonally synthesized proteins. Detection of the mRNAs encoding each of the axonally synthesized proteins identified by mass spectrometry in the axonal compartment indicates that the DRG axons have the potential to synthesize a complex population of proteins. Local treatment of the DRG axons with NGF or BDNF increased levels of cytoskeletal mRNAs into the axonal compartment by twofold to fivefold but had no effect on levels of the other axonal mRNAs studied. Neurotrophins selectively increased transport of -actin, peripherin, and vimentin mRNAs from the cell body into the axons rather than changing transcription or mRNA survival in the axonal compartment.

Key words: axonal protein synthesis; mRNA transport; neurotrophin; cytoskeleton; protein trafficking; heat shock protein

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Received July 19, 2004; revised November 29, 2004; accepted November 30, 2004.

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