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The Journal of Neuroscience, September 13, 2006, 26(37):9462-9470; doi:10.1523/JNEUROSCI.2625-06.2006

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Development/Plasticity/Repair
Activated c-Jun N-Terminal Kinase Is Required for Axon Formation

Anthony A. Oliva, Jr,¹ Coleen M. Atkins,² Lily Copenagle,¹ and Gary A. Banker¹

¹Center for Research on Occupational and Environmental Toxicology and ²The Vollum Institute, Oregon Health & Science University, Portland, Oregon 97239

Correspondence should be addressed to Dr. Anthony A. Oliva Jr, The Miami Project to Cure Paralysis, The University of Miami, Lois Pope LIFE Center (R-48), 1095 Northwest 14th Terrace, Miami, FL 33136. Email: aoliva{at}miamiproject.med.miami.edu

A critical transition in neuron development is formation of the axon, which establishes the polarized structure of the neuron that underlies its entire input and output capabilities. The morphological events that occur during axonogenesis have long been known, yet the molecular determinants underlying axonogenesis remain poorly understood. We demonstrate here that axonogenesis requires activated c-Jun N-terminal kinase (JNK). JNK is expressed throughout the neuron, but its phosphorylated, activated form is highly enriched in the axon. In young axons, activated JNK forms a proximodistal gradient of increasing intensity, beginning at about the point where the axon exceeds the lengths of the other neurites (minor processes). Treatment with SP600125, a specific inhibitor of JNK, reversibly inhibits axonogenesis but does not prevent the formation of minor processes or their differentiation into dendrites (based on their immunostaining with marker proteins). Expression of a dominant-negative construct against JNK similarly prevents axonogenesis. Investigation of JNK targets revealed that activating transcription factor-2 is phosphorylated under normal conditions in neurons, and its phosphorylation is significantly attenuated after JNK inhibition. These results demonstrate that activated JNK is required for axonogenesis but not formation of minor processes or development of dendrites.

Key words: axon formation; axonogenesis; c-Jun N-terminal kinase; JNK; ATF-2; JIP-1; axon; SP600125

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Received Jan. 17, 2006; revised July 26, 2006; accepted July 28, 2006.

Correspondence should be addressed to Dr. Anthony A. Oliva Jr, The Miami Project to Cure Paralysis, The University of Miami, Lois Pope LIFE Center (R-48), 1095 Northwest 14th Terrace, Miami, FL 33136. Email: aoliva{at}miamiproject.med.miami.edu

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