|
|
|
|
|
|
|
|
|||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | |||||
Journal of Cell Science, Vol 109, Issue 5 971-980, Copyright © 1996 by Company of Biologists
JOURNAL ARTICLES |
CC Overly, HI Rieff and PJ Hollenbeck
Department of Neurobiology, Harvard Medical School, Boston MA 02115, USA.
Regional regulation of organelle transport seems likely to play an important role in establishing and maintaining distinct axonal and dendritic domains in neurons, and in managing differences in local metabolic demands. In addition, known differences in microtubule polarity and organization between axons and dendrites along with the directional selectivity of microtubule-based motor proteins suggest that patterns of organelle transport may differ in these two process types. To test this hypothesis, we compared the patterns of movement of different organelle classes in axons and different dendritic regions of cultured embryonic rat hippocampal neurons. We first examined the net direction of organelle transport in axons, proximal dendrites and distal dendrites by video-enhanced phase-contrast microscopy. We found significant regional variation in the net transport of large phase-dense vesicular organelles: they exhibited net retrograde transport in axons and distal dendrites, whereas they moved equally in both directions in proximal dendrites. No significant regional variation was found in the net transport of mitochondria or macropinosomes. Analysis of individual organelle motility revealed three additional differences in organelle transport between the two process types. First, in addition to the difference in net transport direction, the large phase-dense organelles exhibited more persistent changes in direction in proximal dendrites where microtubule polarity is mixed than in axons where microtubule polarity is uniform. Second, while the net direction of mitochondrial transport was similar in both processes, twice as many mitochondria were motile in axons than in dendrites. Third, the mean excursion length of moving mitochondria was significantly longer in axons than in dendrites. To determine whether there were regional differences in metabolic activity that might account for these motility differences, we labeled mitochondria with the vital dye, JC-1, which reveals differences in mitochondrial transmembrane potential. Staining of neurons with this dye revealed a greater proportion of highly charged, more metabolically active, mitochondria in dendrites than in axons. Together, our data reveal differences in organelle motility and metabolic properties in axons and dendrites of cultured hippocampal neurons.
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
This article has been cited by other articles:
|
|
 |
|
  A. Tsubouchi, T. Tsuyama, M. Fujioka, H. Kohda, K. Okamoto-Furuta, T. Aigaki, and T. Uemura Mitochondrial protein Preli-like is required for development of dendritic arbors and prevents their regression in the Drosophila sensory nervous system Development, November 15, 2009; 136(22): 3757 - 3766. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Verburg and P. J. Hollenbeck Mitochondrial Membrane Potential in Axons Increases with Local Nerve Growth Factor or Semaphorin Signaling J. Neurosci., August 13, 2008; 28(33): 8306 - 8315. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 O. Kann and R. Kovacs Mitochondria and neuronal activity Am J Physiol Cell Physiol, February 1, 2007; 292(2): C641 - C657. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Bartolini and G. G. Gundersen Generation of noncentrosomal microtubule arrays J. Cell Sci., October 15, 2006; 119(20): 4155 - 4163. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. T. W. Chang, A. S. Honick, and I. J. Reynolds Mitochondrial trafficking to synapses in cultured primary cortical neurons. J. Neurosci., June 28, 2006; 26(26): 7035 - 7045. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. L. Richardson, R. A. Shivdasani, C. Boers, J. H. Hartwig, and J. E. Italiano Jr Mechanisms of organelle transport and capture along proplatelets during platelet production Blood, December 15, 2005; 106(13): 4066 - 4075. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. J. Hollenbeck and W. M. Saxton The axonal transport of mitochondria J. Cell Sci., December 1, 2005; 118(23): 5411 - 5419. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Q. Cai, C. Gerwin, and Z.-H. Sheng Syntabulin-mediated anterograde transport of mitochondria along neuronal processes J. Cell Biol., September 12, 2005; 170(6): 959 - 969. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Takeuchi, T. Mizuno, G. Zhang, J. Wang, J. Kawanokuchi, R. Kuno, and A. Suzumura Neuritic Beading Induced by Activated Microglia Is an Early Feature of Neuronal Dysfunction Toward Neuronal Death by Inhibition of Mitochondrial Respiration and Axonal Transport J. Biol. Chem., March 18, 2005; 280(11): 10444 - 10454. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 I. J. Reynolds and G. L. Rintoul Mitochondrial Stop and Go: Signals That Regulate Organelle Movement Sci. Signal., September 21, 2004; 2004(251): pe46 - pe46. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. E. Miller and M. P. Sheetz Axonal mitochondrial transport and potential are correlated J. Cell Sci., June 1, 2004; 117(13): 2791 - 2804. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. V. Berghe, G. W. Hennig, and T. K. Smith Characteristics of intermittent mitochondrial transport in guinea pig enteric nerve fibers Am J Physiol Gastrointest Liver Physiol, April 1, 2004; 286(4): G671 - G682. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Bannai, T. Inoue, T. Nakayama, M. Hattori, and K. Mikoshiba Kinesin dependent, rapid, bi-directional transport of ER sub-compartment in dendrites of hippocampal neurons J. Cell Sci., January 15, 2004; 117(2): 163 - 175. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
O. I. Wagner, J. Lifshitz, P. A. Janmey, M. Linden, T. K. McIntosh, and J.-F. Leterrier Mechanisms of Mitochondria-Neurofilament Interactions J. Neurosci., October 8, 2003; 23(27): 9046 - 9058. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Ruthel and P. J. Hollenbeck Response of Mitochondrial Traffic to Axon Determination and Differential Branch Growth J. Neurosci., September 17, 2003; 23(24): 8618 - 8624. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. L. Rintoul, A. J. Filiano, J. B. Brocard, G. J. Kress, and I. J. Reynolds Glutamate Decreases Mitochondrial Size and Movement in Primary Forebrain Neurons J. Neurosci., August 27, 2003; 23(21): 7881 - 7888. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. R. Chada and P. J. Hollenbeck Mitochondrial movement and positioning in axons: the role of growth factor signaling J. Exp. Biol., June 15, 2003; 206(12): 1985 - 1992. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. Sytnyk, I. Leshchyns'ka, M. Delling, G. Dityateva, A. Dityatev, and M. Schachner Neural cell adhesion molecule promotes accumulation of TGN organelles at sites of neuron-to-neuron contacts J. Cell Biol., November 25, 2002; 159(4): 649 - 661. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. B. Mukherjee, M. Das, G. Sudhandiran, and C. Shaha Increase in Cytosolic Ca2+ Levels through the Activation of Non-selective Cation Channels Induced by Oxidative Stress Causes Mitochondrial Depolarization Leading to Apoptosis-like Death in Leishmania donovani Promastigotes J. Biol. Chem., June 28, 2002; 277(27): 24717 - 24727. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. P. Gross, M. A. Welte, S. M. Block, and E. F. Wieschaus Coordination of opposite-polarity microtubule motors J. Cell Biol., February 28, 2002; 156(4): 715 - 724. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. F. Buckman and I. J. Reynolds Spontaneous Changes in Mitochondrial Membrane Potential in Cultured Neurons J. Neurosci., July 15, 2001; 21(14): 5054 - 5065. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. P. Gross, M. A. Welte, S. M. Block, and E. F. Wieschaus Dynein-Mediated Cargo Transport in Vivo: A Switch Controls Travel Distance J. Cell Biol., March 6, 2000; 148(5): 945 - 956. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Martin, S. J. Iyadurai, A. Gassman, J. G. Gindhart Jr., T. S. Hays, and W. M. Saxton Cytoplasmic Dynein, the Dynactin Complex, and Kinesin Are Interdependent and Essential for Fast Axonal Transport Mol. Biol. Cell, November 1, 1999; 10(11): 3717 - 3728. [Abstract] [Full Text]
|
|
|
|
|
|
Y. Ouyang, A. Rosenstein, G. Kreiman, E. M. Schuman, and M. B. Kennedy Tetanic Stimulation Leads to Increased Accumulation of Ca2+/Calmodulin-Dependent Protein Kinase II via Dendritic Protein Synthesis in Hippocampal Neurons J. Neurosci., September 15, 1999; 19(18): 7823 - 7833. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. E. Rubio and R. J. Wenthold Differential Distribution of Intracellular Glutamate Receptors in Dendrites J. Neurosci., July 1, 1999; 19(13): 5549 - 5562. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. J. Koehnle and A. Brown Slow Axonal Transport of Neurofilament Protein in Cultured Neurons J. Cell Biol., February 8, 1999; 144(3): 447 - 458. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. M. G. Shepherd and K. M. Harris Three-Dimensional Structure and Composition of CA3right-arrowCA1 Axons in Rat Hippocampal Slices: Implications for Presynaptic Connectivity and Compartmentalization J. Neurosci., October 15, 1998; 18(20): 8300 - 8310. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. E. Lochner, M. Kingma, S. Kuhn, C. D. Meliza, B. Cutler, and B. A. Scalettar Real-Time Imaging of the Axonal Transport of Granules Containing a Tissue Plasminogen Activator/Green Fluorescent Protein Hybrid Mol. Biol. Cell, September 1, 1998; 9(9): 2463 - 2476. [Abstract] [Full Text]
|
|
|
|
|
|
V. P. Bindokas, C. C. Lee, W. F. Colmers, and R. J. Miller Changes in Mitochondrial Function Resulting from Synaptic Activity in the Rat Hippocampal Slice J. Neurosci., June 15, 1998; 18(12): 4570 - 4587. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. P. Gross, M. A. Welte, S. M. Block, and E. F. Wieschaus Coordination of opposite-polarity microtubule motors J. Cell Biol., February 28, 2002; 156(4): 715 - 724. [Abstract] [Full Text] [PDF]
|
|
