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Published online September 4, 2007
doi:10.1083/jcb.200703209
The Journal of Cell Biology, Vol. 178, No. 6, 965-980
The Rockefeller University Press, 0021-9525 $30.00
© 2007 Willis et al.
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Article

 Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs

Dianna E. Willis1, Erna A. van Niekerk2, Yukio Sasaki3, Mariano Mesngon4, Tanuja T. Merianda1, Gervan G. Williams1, Marvin Kendall1, Deanna S. Smith4, Gary J. Bassell3, and Jeffery L. Twiss1,2

1 Nemours Biomedical Research, Alfred I. duPont Hospital for Children, Wilmington, DE 19803
2 Department of Biological Sciences, University of Delaware, Newark, DE 19716
3 Department of Cell Biology, Emory University, Atlanta, GA 30322
4 Department of Biology, University of South Carolina, Columbia, SC 29208

Correspondence to Jeffery L. Twiss: twiss{at}medsci.udel.edu

Subcellular regulation of protein synthesis requires the correct localization of messenger RNAs (mRNAs) within the cell. In this study, we investigate whether the axonal localization of neuronal mRNAs is regulated by extracellular stimuli. By profiling axonal levels of 50 mRNAs detected in regenerating adult sensory axons, we show that neurotrophins can increase and decrease levels of axonal mRNAs. Neurotrophins (nerve growth factor, brain-derived neurotrophic factor, and neurotrophin-3) regulate axonal mRNA levels and use distinct downstream signals to localize individual mRNAs. However, myelin-associated glycoprotein and semaphorin 3A regulate axonal levels of different mRNAs and elicit the opposite effect on axonal mRNA levels from those observed with neurotrophins. The axonal mRNAs accumulate at or are depleted from points of ligand stimulation along the axons. The translation product of a chimeric green fluorescent protein–ß-actin mRNA showed similar accumulation or depletion adjacent to stimuli that increase or decrease axonal levels of endogenous ß-actin mRNA. Thus, extracellular ligands can regulate protein generation within subcellular regions by specifically altering the localized levels of particular mRNAs.

Abbreviations used in this paper: AV, adenovirus; BDNF, brain-derived neurotrophic factor; db-cAMP, dibutyral cAMP; DRB, 5,6-dichlorobenzimidazole riboside; DRG, dorsal root ganglion; eGFP, enhanced GFP; EHNA, erythro-9-(2-hydroxy-3-nonyl)adenine hydrochloride; GAP-43, 43-kD growth-associated protein; MAG, myelin-associated glycoprotein; NT3, neurotrophin-3; PI3K, phosphatidyl inositol-3 kinase; qPCR, quantitative PCR; Sema3A, semaphorin 3A; UTR, untranslated region.


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