Axonal mitochondrial transport and potential are correlated

Journal of Cell Science

Volumn 117, Issue 13, 2004, Pages 2791-2804

  Miller, Kyle E ^a   Sheetz, Michael P ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

2 Deoxyglucose; Antimycin; JC 1; Mitochondria; Mitochondrial potential; Statistical analysis

Indexed keywords

ADENOSINE TRIPHOSPHATE; CITRININ; DEOXYGLUCOSE; MANNITOL;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CORRELATION COEFFICIENT; ELECTRON TRANSPORT; GROWTH CONE; HISTOCHEMISTRY; MICROPIPETTE; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; NERVE CELL MEMBRANE POTENTIAL; NERVE FIBER TRANSPORT; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; STATISTICAL ANALYSIS;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANTIMYCIN A; AXONS; BENZIMIDAZOLES; BIOLOGICAL TRANSPORT; CARBOCYANINES; CARBONYL CYANIDE M-CHLOROPHENYL HYDRAZONE; CELLS, CULTURED; CHICK EMBRYO; DEOXYGLUCOSE; ELECTRON TRANSPORT COMPLEX III; FLUORESCENT DYES; GANGLIA, SPINAL; GROWTH CONES; MANNITOL; MEMBRANE POTENTIALS; MITOCHONDRIA; NEURONS; STATISTICS; UNCOUPLING AGENTS;

ANIMALIA;

EID: 3242875557     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01130     Document Type: Article

References (86)

1. Allen, R. D., Metuzals, J., Tasaki, I., Brady, S. T. and Gilbert, S. P. (1982). Fast axonal transport in squid giant axon. Science 218, 1127-1129.
2. Alto, N. M., Soderling, J. and Scott, J. D. (2002). Rab32 is an A-kinase anchoring protein and participates in mitochondrial dynamics. J. Cell Biol. 158, 659-668.
3. Banker, G. and Goslin, K. (1998). Culturing nerve cells. Cambridge, MA: MIT Press.
4. Baud, V. and Karin, M. (2001). Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol. 11, 372-377.
5. Bereiter-Hahn, J. and Voth, M. (1983). Metabolic control of shape and structure of mitochondria in situ. Biol. Cell 47, 309-322.
6. Bereiter-Hahn, J. and Voth, M. (1994). Dynamics of mitochondria in living cells, shape changes, dislocations, fusion, and fission of mitochondria. Microsc. Res. Tech. 27, 198-219.
7. Bindokas, V. P., Lee, C. C., Colmers, W. E. and Miller, R. J. (1998). Changes in mitochondrial function resulting from synaptic activity in the rat hippocampal slice. J. Neurosci. 18, 4570-4587.
8. Boldogh, I., Vojtov, N., Karmon, S. and Pon, L. A. (1998). Interaction between mitochondria and the actin cytoskeleton in budding yeast requires two integral mitochondrial outer membrane proteins, Mmm1p and Mdm10p. J. Cell Biol. 141, 1371-1381.
9. Borgdorff, A. J., Somjen, G. G. and Wadman, W. J. (2000). Two mechanisms that raise free intracellular calcium in rat hippocampal neurons during hypoosmotic and low NaCl treatment. J. Neurophysiol. 83, 81-89.
10. 2+ homeostasis. J. Neurochem. 66, 403-411.
11. Burkhardt, J. K., Echeverri, C. J., Nilsson, T. and Vallee, R. B. (1997). Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J. Cell Biol. 139, 469-484.
12. Burton, P. R. and Paige, J. L. (1981). Polarity of axoplasmic microtubules in the olfactory nerve of the frog. Proc. Natl. Acad. Sci. USA 78, 3269-3273.
13. Chada, S. R. and Hollenbeck, P. J. (2003). Mitochondrial movement and positioning in axons, the role of growth factor signaling. J. Exp. Biol. 206, 1985-1992.
14. Collins, T. J., Berridge, M. J., Lipp, P. and Bootman, M. D. (2002). Mitochondria are morphologically and functionally heterogeneous within cells. EMBO J. 21, 1616-1627.
15. Cunarro, J. and Weiner, M. W. (1975). Mechanism of action of agents which uncouple oxidative phosphorylation, direct correlation between proton-carrying and respiratory-releasing properties using rat liver mitochondria. Biochim. Biophys. Acta Mol. Cell Res. 387, 234-240.
16. Davis, A. F. and Clayton, D. A. (1996). In situ localization of mitochondrial DNA replication in intact mammalian cells. J. Cell Biol. 135, 883-893.
17. de Graaf, R. A., van Kranenburg, A. and Nicolay, K. (2000). In vivo (31)PNMR diffusion spectroscopy of ATP and phosphocreatine in rat skeletal muscle. Biophys. J. 78, 1657-1664.
18. De Vos, K., Goossens, V., Boone, E., Vercammen, D., Vancompernolle, K., Vandenabeele, P., Haegeman, G., Fiers, W. and Grooten, J. (1998). The 55-kDa tumor necrosis factor receptor induces clustering of mitochondria through its membrane-proximal region. J. Biol. Chem. 273, 9673-9680.
19. De Vos, K., Severin, F., van Herreweghe, F., Vancompernolle, K., Goossens, V., Hyman, A. and Grooten, J. (2000). Tumor necrosis factor induces hyperphosphorylation of kinesin light chain and inhibits kinesin-mediated transport of mitochondria. J. Cell Biol. 149, 1207-1214.
20. De Vos, K. J., Sable, J., Miller, K. E. and Sheetz, M. P. (2003). Expression of phosphatidylinositol (4,5) bisphosphate-specific pleckstrin homology domains alters direction but not the level of axonal transport of mitochondria. Mol. Biol. Cell 14, 3636-3649.
21. Desagher, S. and Martinou, J. C. (2000). Mitochondria as the central control point of apoptosis. Trends Cell Biol. 10, 369-377.
22. Ferhat, L., Kuriyama, R., Lyons, G. E., Micales, B. and Baas, P. W. (1998). Expression of the mitotlic motor protein CHO1/MKLP1 in postmitotic neurons. Eur. J. Neurosci. 10, 1383-1393.
23. Feynman, R. P., Leighton, R. B. and Sands, M. L. (1963). The Feynman Lectures on Physics. Reading, MA: Addison-Wesley.
24. Fishman, R. A., Reiner, M. and Chan, P. H. (1977). Metabolic changes associated with iso-osmotic regulation in brain cortex slices. J. Neurochem. 28, 1061-1067.
25. Fransson, A., Ruusala, A. and Aspenstrom, P. (2003). Atypical Rho GTPases have roles in mitochondrial homeostasis and apoptosis. J. Biol. Chem. 278, 6495-6502.
26. Friede, R. L. and Ho, K. C. (1977). The relation of axonal transport of mitochondria with microtubules and other axoplasmic organelles. J. Physiol. 265, 507-519.
27. Gross, S. P., Welte, M. A., Block, S. M. and Wieschaus, E. F. (2002). Coordination of opposite-polarity microtubule motors. J. Cell Biol. 156, 715-724.
28. Gunawardena, S. and Goldstein, L. S. (2001). Disruption of axonal transport and neuronal viability by amyloid precursor protein mutations in Drosophila. Neuron 32, 389-401.
29. Gunawardena, S., Her, L. S., Brusch, R. G., Laymon, R. A., Niesman, I. R., Gordesky-Gold, B., Sintasath, L., Bonini, N. M. and Goldstein, L. S. (2003). Disruption of axonal transport by toss of huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron 40, 25-40.
30. Ha, H. (1970). Axonal bifurcation in the dorsal root ganglion of the cat, a light and electron microscopic study. J. Comp. Neurol. 140, 227-240.
31. Habermann, A., Schroer, T. A., Griffiths, G. and Burkhardt, J. K. (2001). Immunolocalization of cytoplasmic dynein and dynactin subunits in cultured macrophages, enrichment on early endocytic organelles. J. Cell Sci. 114, 229-240.
32. Hagen, T. M., Yowe, D. L., Bartholomew, J. C., Wehr, C. M., Do, K. L., Park, J. Y. and Ames, B. N. (1997). Mitochondrial decay in hepatocytes from old rats, membrane potential declines, heterogeneity and oxidants increase. Proc. Natl. Acad. Sci. USA 94, 3064-3069.
33. Heidemann, S. R., Landers, J. M. and Hamborg, M. A. (1981). Polarity orientation of axonal microtubules. J. Cell Biol. 91, 661-665.
34. Hollenbeck, P. J. (1993). Products of endocytosis and autophagy are retrieved from axons by regulated retrograde organelle transport. J. Cell Biol. 121, 305-315.
35. Hollenbeck, P. J. (1996). The pattern and mechanism of mitochondrial transport in axons. Front. Biosci. 1, 91-102.
36. Hollenbeck, P. J. and Bray, D. (1987). Rapidly transported organelles containing membrane and cytoskeletal components, their relation to axonal growth. J. Cell Biol. 105, 2827-2835.
37. Hollenbeck, P. J., Bray, D. and Adams, R. J. (1985). Effects of the uncoupling agents FCCP and CCCP on the saltatory movements of cytoplasmic organelles. Cell Biol. Int. Rep. 9, 193-199.
38. Huang, J. D., Brady, S. T., Richards, B. W., Stenolen, D., Resau, J. H., Copeland, N. G. and Jenkins, N. A. (1999). Direct interaction of microtubule- and actin-based transport motors. Nature 397, 267-270.
39. Hurd, D. D. and Saxton, W. M. (1996). Kinesin mutations cause motor neuron disease phenotypes by disrupting fast axonal transport in Drosophila. Genetics 144, 1075-1085.
40. Huser, J. and Blatter, L. A. (1999). Fluctuations in mitochondrial membrane potential caused by repetitive gating of the permeability transition pore. Biochem. J. 343, 311-317.
41. Kanai, A., Hiruma, H., Katakura, T., Sase, S., Kawakami, T. and Hoka, S. (2001). Low-concentration lidocaine rapidly inhibits axonal transport in cultured mouse dorsal root ganglion neurons. Anesthesiology 95, 675-680.
42. Kaniuga, Z., Gardas, A. and Bryla, J. (1968). Studies on the mechanism of inhibition of the mitochondrial electron transport by antimycin. I. Reversal of the inhibition by diethyl ether extraction. Biochim. Biophys. Acta Mol. Cell Res. 153, 60-69.
43. Kanje, M., Edstrom, A. and Hanson, M. (1981). Inhibition of rapid axonal transport in vitro by the ionophores X-537 A and A 23187. Brain Res. 204, 43-50.
44. Kendal, W. S., Koles, Z. J. and Smith, R. S. (1983). Oscillatory motion of intra-axonal organelles of Xenopus laevis following inhibition of their rapid transport. J. Physiol. 345, 501-513.
45. Klionsky, D. J. and Emr, S. D. (2000). Autophagy as a regulated pathway of cellular degradation. Science 290, 1717-1721.
46. Lee, K. D. and Hollenbeek, P. J. (1995). Phosphorylation of kinesin in vivo correlates with organelle association and neurite outgrowth. J. Biol. Chem. 270, 5600-5605.
47. Lemasters, J. J., Nieminen, A. L., Qian, T., Trost, L. C., Elmore, S. P., Nishimura, Y., Crowe, R. A., Cascio, W. E., Bradham, C. A., Brenner, D. A. et al. (1998). The mitochondrial permeability transition in cell death, a common mechanism in necrosis, apoptosis and autophagy. Biochim. Biophys. Acta Mol. Cell Res. 1366, 177-196.
48. Ligon, L. A. and Steward, O. (2000). Movement of mitochondria in the axons and dendrites of cultured hippocampal neurons. J. Comp. Neurol. 427, 340-350.
49. Lindesmith, L., MeIlvain, J. M., Jr, Argon, Y. and Sheetz, M. P. (1997). Phosphotransferases associated with the regulation of kinesin motor activity. J. Biol. Chem. 272, 22929-22933.
50. Luo, X., Budihardjo, I., Zou, H., Slaughter, C. and Wang, X. (1998). Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94, 481-490.
51. Martenson, C. H., Odom, A., Sheetz, M. P. and Graham, D. G. (1995). The effect of acrylamide and other sulfhydryl alkylators on the ability of dynein and kinesin to translocate microtubules in vitro. Toxicol. Appl. Pharmacol. 133, 73-81.
52. Matthies, H. J., Miller, R. J. and Palfrey, H. C. (1993). Calmodulin binding to and cAMP-dependent phosphorylation of kinesin light chains modulate kinesin ATPase activity. J. Biol. Chem. 268, 11176-11187.
53. McIlvain, J. M., Jr, Burkhardt, J. K., Hamm-Alvarez, S., Argon, Y. and Sheetz, M. P. (1994). Regulation of kinesin activity by phosphorylation of kinesin-associated proteins. J. Biol. Chem. 269, 19176-19182.
54. Menzies, R. A. and Gold, P. H. (1971). The turnover of mitochondria in a variety of tissues of young adult and aged rats. J. Biol. Chem. 246, 2425-2429.
55. Minamikawa, T., Sriratana, A., Williams, D. A., Bowser, D. N., Hill, J. S. and Nagley, P. (1999). Chloromethyi-X-rosamine (MitoTracker Red) photosensitises mitochondria and induces apoptosis in intact human cells. J. Cell Sci. 112, 2419-2430.
56. Morris, R. L. and Hollenbeck, P. J. (1993). The regulation of bidirectional mitochondrial transport is coordinated with axonal outgrowth. J. Cell Sci. 104, 917-927.
57. Nangaku, M., Sato-Yoshitake, R., Okada, Y., Noda, Y., Takemura, R., Yamazaki, H. and Hirokawa, N. (1994). KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell 79, 1209-1220.
58. Nicholls, D. G. and Budd, S. L. (2000). Mitochondria and neuronal survival. Physiol. Rev. 80, 315-360.
59. Ochs, S. and Hollingsworth, D. (1971). Dependence of fast axoplasmic transport in nerve on oxidative metabolism. J. Neurochem. 18, 107-114.
60. Ochs, S. and Jersild, R. A., Jr (1984). Calcium localization in nerve fibers in relation to axoplasmic transport. Neurochem. Res. 9, 823-836.
61. Ochs, S. and Smith, C. B. (1971). Fast axoplasmic transport in mammalian nerve in vitro after block of glycolysis with iodoacetic acid. J. Neurochem. 18, 833-843.
62. Ochs, S., Worth, R. M. and Chan, S. Y. (1977). Calcium requirement for axoplasmic transport in mammalian nerve. Nature 270, 748-750.
63. Okada, Y., Sato-Yoshitake, R. and Hirokawa, N. (1995). The activation of protein kinase A pathway selectively inhibits anterograde axonal transport of vesicles but not mitochondria transport or retrograde transport in vivo. J. Neurosci. 15, 3053-3064.
64. Overly, C. C., Rieff, H. I. and Hollenbeck, P. J. (1996). Organelle motility and metabolism in axons vs dendrites of cultured hippocampal neurons. J. Cell Sci. 109, 971-980.
65. Papa, S. (1996). Mitochondrial oxidative phosphorylation changes in the life span. Molecular aspects and physiopathological implications. Biochim. Biophys. Acta Mol. Cell Res. 1276, 87-105.
66. Pereira, A. J., Dalby, B., Stewart, R. J., Doxsey, S. J. and Goldstein, L. S. (1997). Mitochondrial association of a plus end-directed microtubule motor expressed during mitosis in Drosophila. J. Cell Biol. 136, 1081-1090.
67. Pilatus, U., Aboagye, E., Artemov, D., Mori, N., Ackerstaff, E. and Bhujwalla, Z. M. (2001). Real-time measurements of cellular oxygen consumption, pH, and energy metabolism using nuclear magnetic resonance spectroscopy. Magn. Reson. Med. 45, 749-755.
68. Reers, M., Smith, T. W. and Chen, L. B. (1991). J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry 30, 4480-4486.
69. Rizzuto, R. (2001). Intracellular Ca(2+) pools in neuronal signalling. Curr. Opin. Neurobiol. 11, 306-311.
70. Rottenberg, H. and Wu, S. (1998). Quantitative assay by flow cytometry of the mitochondrial membrane potential in intact cells. Biochim. Biophys. Acta Mol. Cell Res. 1404, 693-404.
71. Sato-Yoshitake, R., Yorifuji, H., Inagaki, M. and Hirokawa, N. (1992). The phosphorylation of kinesin regulates its binding to synaptic vesicles. J. Biol. Chem. 267, 23930-23936.
72. Schwarzer, C., Barnikol-Watanabe, S., Thinnes, F. P. and Hilschmann, N. (2002). Voltage-dependent anion-selective channel (VDAC) interacts with the dynein light chain Tctex1 and the heat-shock protein PBP74. Int. J. Biochem. Cell Biol. 34, 1059-1070.
73. Smiley, S. T., Reers, M., Mottola-Hartshorn, C., Lin, M., Chen, A., Smith, T. W., Steele, G. D., Jr and Chen, L. B. (1991). Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc. Natl. Acad. Sci. USA 88, 3671-3675.
74. Stowers, R. S., Megeath, L. J., Gorska-Andrzejak, J., Meinertzhagen, I. A. and Schwarz, T. L. (2002). Axonal transport of mitochondria to synapses depends on Milton, a novel Drosophila protein. Neuron 36, 1063-1077.
75. Tai, A. W., Chuang, J. Z., Bode, C., Wolfrum, U. and Sung, C. H. (1999). Rhodopsin's carboxy-terminal cytoplasmic tail acts as a membrane receptor for cytoplasmic dynein by binding to the dynein light chain Tctex-1. Cell 97, 877-887.
76. Tanaka, Y., Kanai, Y., Okada, Y., Nonaka, S., Takeda, S., Harada, A. and Hirokawa, N. (1998). Targeted disruption of mouse conventional kinesin heavy chain, Kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 93, 1147-1158.
77. Terasaki, M. and Reese, T. S. (1992). Characterization of endoplasmic reticulum by co-localization of BiP and dicarbocyanine dyes. J. Cell Sci. 101, 315-322.
78. Tolkovsky, A. M., Xue, L., Fletcher, G. C. and Borutaite, V. (2002). Mitochondrial disappearance from cells, a clue to the role of autophagy in programmed cell death and disease? Biochimie 84, 233-240.
79. Trinczek, B., Ebneth, A., Mandelkow, E. M. and Mandelkow, E. (1999). Tau regulates the attachment/detachment but not the speed of motors in microtubule-dependent transport of single vesicles and organelles. J. Cell Sci. 112, 2355-2367.
80. Tzung, S. P., Kim, K. M., Basanez, G., Giedt, C. D., Simon, J., Zimmerberg, J., Zhang, K. Y. and Hockenbery, D. M. (2001). Antimycin A mimics a cell-death-inducing Bcl-2 homology domain 3. Nat. Cell Biol. 3, 183-191.
81. van Deursen, J., Heerschap, A., Oerlemans, F., Ruitenbeek, W., Jap, P., ter Laak, H. and Wieringa, B. (1993). Skeletal muscles of mice deficient in muscle creatine kinase lack burst activity. Cell 74, 621-631.
82. Wagner, O. I., Lifshitz, J., Janmey, P. A., Linden, M., McIntosh, T. K. and Leterrier, J. F. (2003). Mechanisms of mitochondria-neurofilament interactions. J. Neurosci. 23, 9046-9058.
83. Wong-Riley, M. T. (1989). Cytochrome oxidase, an endogenous metabolic marker for neuronal activity. Trends Neurosci. 12, 94-101.
84. Xue, L., Fletcher, G. C. and Tolkovsky, A. M. (2001). Mitochondria are selectively eliminated from eukaryotic cells after blockade of caspases during apoptosis. Curr. Biol. 11, 361-365.
85. Zar, J. H. (1999). Biostatistical Analysis. Upper Saddler River, NJ: Prentice Hall.
86. Zhou, H. M., Brust-Mascher, I. and Scholey, J. M. (2001). Direct visualization of the movement of the monomeric axonal transport motor UNC-104 along neuronal processes in living Caenorhabditis elegans. J. Neurosci. 21, 3749-3755.