 |
||||
|
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, December 1, 2001, 21(23):9291-9303
A Functional Role for Intra-Axonal Protein Synthesis during Axonal Regeneration from Adult Sensory Neurons
Jun-Qi Zheng1, 4, Theresa K. Kelly1, 3, Bieshia Chang1, Sergey Ryazantsev2, Ayyappan K. Rajasekaran1, Kelsey C. Martin2, 3, and Jeffery L. Twiss1, 3 Departments of 1 Pathology and Laboratory Medicine and 2 Biological Chemistry and 3 Brain Research Institute, University of California, Los Angeles, California 90095, and 4 Department of Neuroanatomy, Shenyang Medical College and Medical University of China, Shenyang, China 110001
Although intradendritic protein synthesis has been documented in adult neurons, the question of whether axons actively synthesize proteins remains controversial. Adult sensory neurons that are conditioned by axonal crush can rapidly extend processes in vitro by regulating the translation of existing mRNAs (Twiss et al., 2000). These regenerating processes contain axonal but not dendritic proteins. Here we show that these axonal processes of adult sensory neurons cultured after conditioning injury contain ribosomal proteins, translational initiation factors, and rRNA. Pure preparations of regenerating axons separated from the DRG cell bodies can actively synthesize proteins in vitro and contain ribosome-bound
-actin and neurofilament mRNAs. Blocking protein synthesis in these regenerating sensory axons causes a rapid retraction of their growth cones when communication with the cell body is blocked by axotomy or colchicine treatment. These findings indicate that axons of adult mammalian neurons can synthesize proteins and suggest that, under some circumstances, intra-axonal translation contributes to structural integrity of the growth cone in regenerating axons. By immunofluorescence, translation factors, ribosomal proteins, and rRNA were also detected in motor axons of ventral spinal roots analyzed after 7 d in vivo after a peripheral axonal crush injury. Thus, adult motor neurons are also likely capable of intra-axonal protein synthesis in vivo after axonal injury.
Key words: mRNA localization; local protein synthesis; conditioned neuron; axonal regeneration; nerve regeneration
Copyright © 2001 Society for Neuroscience 0270-6474/01/21239291-13$05.00/0
This article has been cited by other articles:
M. Hassanein, A. S. Bojja, L. Glazewski, G. Lu, and R.W. Mason
Protein processing by the placental protease, cathepsin P
Mol. Hum. Reprod., July 1, 2009; 15(7): 433 - 442.
[Abstract] [Full Text] [PDF]
A. M. Taylor, N. C. Berchtold, V. M. Perreau, C. H. Tu, N. Li Jeon, and C. W. Cotman
Axonal mRNA in Uninjured and Regenerating Cortical Mammalian Axons
J. Neurosci., April 15, 2009; 29(15): 4697 - 4707.
[Abstract] [Full Text] [PDF]
M. Bisbal, J. Wojnacki, D. Peretti, A. Ropolo, J. Sesma, I. Jausoro, and A. Caceres
KIF4 Mediates Anterograde Translocation and Positioning of Ribosomal Constituents to Axons
J. Biol. Chem., April 3, 2009; 284(14): 9489 - 9497.
[Abstract] [Full Text] [PDF]
F. K. Roche, B. M. Marsick, and P. C. Letourneau
Protein Synthesis in Distal Axons Is Not Required for Growth Cone Responses to Guidance Cues
J. Neurosci., January 21, 2009; 29(3): 638 - 652.
[Abstract] [Full Text] [PDF]
A. Giuditta, J. Tai Chun, M. Eyman, C. Cefaliello, A. P. Bruno, and M. Crispino
Local Gene Expression in Axons and Nerve Endings: The Glia-Neuron Unit
Physiol Rev, April 1, 2008; 88(2): 515 - 555.
[Abstract] [Full Text] [PDF]
T. J. Price, M. H. Rashid, M. Millecamps, R. Sanoja, J. M. Entrena, and F. Cervero
Decreased Nociceptive Sensitization in Mice Lacking the Fragile X Mental Retardation Protein: Role of mGluR1/5 and mTOR
J. Neurosci., December 19, 2007; 27(51): 13958 - 13967.
[Abstract] [Full Text] [PDF]
A. Hayashi, T. Kasahara, K. Iwamoto, M. Ishiwata, M. Kametani, C. Kakiuchi, T. Furuichi, and T. Kato
The Role of Brain-derived Neurotrophic Factor (BDNF)-induced XBP1 Splicing during Brain Development
J. Biol. Chem., November 23, 2007; 282(47): 34525 - 34534.
[Abstract] [Full Text] [PDF]
D. E. Willis, E. A. van Niekerk, Y. Sasaki, M. Mesngon, T. T. Merianda, G. G. Williams, M. Kendall, D. S. Smith, G. J. Bassell, and J. L. Twiss
Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs
J. Cell Biol., September 7, 2007; 178(6): 965 - 980.
[Abstract] [Full Text] [PDF]
R. M. S. Weragoda and E. T. Walters
Serotonin Induces Memory-Like, Rapamycin-Sensitive Hyperexcitability in Sensory Axons of Aplysia That Contributes to Injury Responses
J Neurophysiol, September 1, 2007; 98(3): 1231 - 1239.
[Abstract] [Full Text] [PDF]
E. A. van Niekerk, D. E. Willis, J. H. Chang, K. Reumann, T. Heise, and J. L. Twiss
Sumoylation in axons triggers retrograde transport of the RNA-binding protein La
PNAS, July 31, 2007; 104(31): 12913 - 12918.
[Abstract] [Full Text] [PDF]
B. K. Ng, L. Chen, W. Mandemakers, J. M. Cosgaya, and J. R. Chan
Anterograde Transport and Secretion of Brain-Derived Neurotrophic Factor along Sensory Axons Promote Schwann Cell Myelination
J. Neurosci., July 11, 2007; 27(28): 7597 - 7603.
[Abstract] [Full Text] [PDF]
E. C. Johnson, L. Jia, W. O. Cepurna, T. A. Doser, and J. C. Morrison
Global Changes in Optic Nerve Head Gene Expression after Exposure to Elevated Intraocular Pressure in a Rat Glaucoma Model
Invest. Ophthalmol. Vis. Sci., July 1, 2007; 48(7): 3161 - 3177.
[Abstract] [Full Text] [PDF]
J. van Bergeijk, K. Rydel-Konecke, C. Grothe, and P. Claus
The spinal muscular atrophy gene product regulates neurite outgrowth: importance of the C terminus
FASEB J, May 1, 2007; 21(7): 1492 - 1502.
[Abstract] [Full Text] [PDF]
A. K. Murashov, V. Chintalgattu, R. R. Islamov, T. E. Lever, E. S. Pak, P. L. Sierpinski, L. C. Katwa, and M. R. Van Scott
RNAi pathway is functional in peripheral nerve axons
FASEB J, March 1, 2007; 21(3): 656 - 670.
[Abstract] [Full Text] [PDF]
J. Bi, N.-P. Tsai, Y.-P. Lin, H. H. Loh, and L.-N. Wei
Axonal mRNA transport and localized translational regulation of {kappa}-opioid receptor in primary neurons of dorsal root ganglia
PNAS, December 26, 2006; 103(52): 19919 - 19924.
[Abstract] [Full Text] [PDF]
H. H. Yin, M. I. Davis, J. A. Ronesi, and D. M. Lovinger
The Role of Protein Synthesis in Striatal Long-Term Depression.
J. Neurosci., November 15, 2006; 26(46): 11811 - 11820.
[Abstract] [Full Text] [PDF]
N.-P. Tsai, J. Bi, H. H. Loh, and L.-N. Wei
Netrin-1 signaling regulates de novo protein synthesis of kappa opioid receptor by facilitating polysomal partition of its mRNA.
J. Neurosci., September 20, 2006; 26(38): 9743 - 9749.
[Abstract] [Full Text] [PDF]
K. C. Martin and R. S. Zukin
RNA trafficking and local protein synthesis in dendrites: an overview.
J. Neurosci., July 5, 2006; 26(27): 7131 - 7134.
[Abstract] [Full Text] [PDF]
M.-Y. Jung, L. Lorenz, and J. D. Richter
Translational Control by Neuroguidin, a Eukaryotic Initiation Factor 4E and CPEB Binding Protein.
Mol. Cell. Biol., June 1, 2006; 26(11): 4277 - 4287.
[Abstract] [Full Text] [PDF]
M. P. Steinmetz, K. P. Horn, V. J. Tom, J. H. Miller, S. A. Busch, D. Nair, D. J. Silver, and J. Silver
Chronic Enhancement of the Intrinsic Growth Capacity of Sensory Neurons Combined with the Degradation of Inhibitory Proteoglycans Allows Functional Regeneration of Sensory Axons through the Dorsal Root Entry Zone in the Mammalian Spinal Cord
J. Neurosci., August 31, 2005; 25(35): 8066 - 8076.
[Abstract] [Full Text] [PDF]
L. Bonetta
Growth cones make proteins, too
J. Cell Biol., June 20, 2005; 169(6): 839 - 839.
[Full Text] [PDF]
A. M. Apergis-Schoute, J. Debiec, V. Doyere, J. E. LeDoux, and G. E. Schafe
Auditory Fear Conditioning and Long-Term Potentiation in the Lateral Amygdala Require ERK/MAP Kinase Signaling in the Auditory Thalamus: A Role for Presynaptic Plasticity in the Fear System
J. Neurosci., June 15, 2005; 25(24): 5730 - 5739.
[Abstract] [Full Text] [PDF]
D. Willis, K. W. Li, J.-Q. Zheng, J. H. Chang, A. Smit, T. Kelly, T. T. Merianda, J. Sylvester, J. van Minnen, and J. L. Twiss
Differential Transport and Local Translation of Cytoskeletal, Injury-Response, and Neurodegeneration Protein mRNAs in Axons
J. Neurosci., January 26, 2005; 25(4): 778 - 791.
[Abstract] [Full Text] [PDF]
P. Verma, S. Chierzi, A. M. Codd, D. S. Campbell, R. L. Meyer, C. E. Holt, and J. W. Fawcett
Axonal Protein Synthesis and Degradation Are Necessary for Efficient Growth Cone Regeneration
J. Neurosci., January 12, 2005; 25(2): 331 - 342.
[Abstract] [Full Text] [PDF]
R. M. S. Weragoda, E. Ferrer, and E. T. Walters
Memory-Like Alterations in Aplysia Axons after Nerve Injury or Localized Depolarization
J. Neurosci., November 17, 2004; 24(46): 10393 - 10401.
[Abstract] [Full Text] [PDF]
S. Hanz and M. Fainzilber
Integration of Retrograde Axonal and Nuclear Transport Mechanisms in Neurons: Implications for Therapeutics
Neuroscientist, October 1, 2004; 10(5): 404 - 408.
[Abstract] [PDF]
S. Nedelec, I. Foucher, I. Brunet, C. Bouillot, A. Prochiantz, and A. Trembleau
Emx2 homeodomain transcription factor interacts with eukaryotic translation initiation factor 4E (eIF4E) in the axons of olfactory sensory neurons
PNAS, July 20, 2004; 101(29): 10815 - 10820.
[Abstract] [Full Text] [PDF]
C. Li, Y. Sasaki, K. Takei, H. Yamamoto, M. Shouji, Y. Sugiyama, T. Kawakami, F. Nakamura, T. Yagi, T. Ohshima, et al.
Correlation between Semaphorin3A-Induced Facilitation of Axonal Transport and Local Activation of a Translation Initiation Factor Eukaryotic Translation Initiation Factor 4E
J. Neurosci., July 7, 2004; 24(27): 6161 - 6170.
[Abstract] [Full Text] [PDF]
R. Molteni, J.-Q. Zheng, Z. Ying, F. Gomez-Pinilla, and J. L. Twiss
Voluntary exercise increases axonal regeneration from sensory neurons
PNAS, June 1, 2004; 101(22): 8473 - 8478.
[Abstract] [Full Text] [PDF]
S.-K. Lee and P. J. Hollenbeck
Organization and translation of mRNA in sympathetic axons
J. Cell Sci., November 1, 2003; 116(21): 4467 - 4478.
[Abstract] [Full Text] [PDF]
R. Moccia, D. Chen, V. Lyles, E. Kapuya, Y. E, S. Kalachikov, C. M. T. Spahn, J. Frank, E. R. Kandel, M. Barad, et al.
An Unbiased cDNA Library Prepared from Isolated Aplysia Sensory Neuron Processes Is Enriched for Cytoskeletal and Translational mRNAs
J. Neurosci., October 15, 2003; 23(28): 9409 - 9417.
[Abstract] [Full Text] [PDF]
J. Bi, X. Hu, H. H. Loh, and L.-N. Wei
Mouse {kappa}-Opioid Receptor mRNA Differential Transport in Neurons
Mol. Pharmacol., September 1, 2003; 64(3): 594 - 599.
[Abstract] [Full Text] [PDF]
H. L. Zhang, F. Pan, D. Hong, S. M. Shenoy, R. H. Singer, and G. J. Bassell
Active Transport of the Survival Motor Neuron Protein and the Role of Exon-7 in Cytoplasmic Localization
J. Neurosci., July 23, 2003; 23(16): 6627 - 6637.
[Abstract] [Full Text] [PDF]
D.-Y. Wu, J.-Q. Zheng, M. A. McDonald, B. Chang, and J. L. Twiss
PKC Isozymes in the Enhanced Regrowth of Retinal Neurites after Optic Nerve Injury
Invest. Ophthalmol. Vis. Sci., June 1, 2003; 44(6): 2783 - 2790.
[Abstract] [Full Text] [PDF]
J. L. Goldberg
How does an axon grow?
Genes & Dev., April 15, 2003; 17(8): 941 - 958.
[Full Text] [PDF]
I. A. Muslimov, M. Titmus, E. Koenig, and H. Tiedge
Transport of Neuronal BC1 RNA in Mauthner Axons
J. Neurosci., June 1, 2002; 22(11): 4293 - 4301.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|