Mitochondrial movement and positioning in axons: The role of growth factor signaling

Journal of Experimental Biology

Volumn 206, Issue 12, 2003, Pages 1985-1992

  Chada, Sonita R ^a   Hollenbeck, Peter J ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Growth cone; Mitochondrial movement; Nerve growth factor; Neuronal homeostasis; NGF; Phosphoinositide 3 kinase; Sensory axon; Signaling

Indexed keywords

NERVE GROWTH FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE A;

ANIMAL; CHICK EMBRYO; FLUORESCENCE MICROSCOPY; GROWTH CONE; IMMUNOHISTOCHEMISTRY; METABOLISM; MITOCHONDRION; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CHICK EMBRYO; GROWTH CONES; IMMUNOHISTOCHEMISTRY; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; NERVE GROWTH FACTOR; RECEPTOR, TRKA; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0037933255     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.00263     Document Type: Review

References (51)

1. Benshalom, G. and Reese, T. S. (1985). Ultrastructural observations on the cytoarchitecture of axons processed by rapid-freezing and substitution. J. Neurocytol. 14, 943-960.
2. Bindokas, V. P., Lee, C. C., Colmers, W. F. and Miller, R. J. (1998). Changes in mitochondrial function resulting from synaptic activity in the rat hippocampal slice. J. Neurosci. 18, 4570-4587.
3. Brunet, A., Datta, S. R. and Greenberg, M. E. (2001). Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr. Opin. Neurobiol. 11, 297-305.
4. Campenot, R. B. (1994). NGF and the local control of nerve terminal growth. J. Neurobiol. 25, 599-611.
5. Cheatham, B., Vlahos, C. J., Cheatham, L., Wang, L., Blenis, J. and Kahn, C. R. (1994). Phosphatidylinositol 3-kinase activation is required for insulin stimulation of pp70 S6 kinase, DNA synthesis, and glucose transporter translocation. Mol. Cell. Biol. 14, 4902-4911.
6. Davies, A. M. (1994). The role of neurotrophins in the developing nervous system. J. Neurobiol. 25, 1334-1348.
7. Diamond, J., Holmes, M. and Coughlin, M. (1992). Endogenous NGF and nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult rat. J. Neurosci. 12, 1454-1466.
8. Farinas, I. (1999). Neurotrophin actions during the development of the peripheral nervous system. Microsc. Res. Tech. 45, 233-242.
9. Gallo, G., Lefcort, F. B. and Letourneau, P. C. (1997). The trkA receptor mediates growth cone turning toward a localized source of nerve growth factor. J. Neurosci. 17, 5445-5454.
10. Gallo, G. and Letourneau, P. C. (1998). Localized sources of neurotrophins initiate axon collateral sprouting. J. Neurosci. 18, 5403-5414.
11. Gallo, G. and Letourneau, P. C. (2000). Neurotrophins and the dynamic regulation of the neuronal cytoskeleton. J. Neurobiol. 44, 159-173.
12. Gundersen, R. W. and Barrett, J. N. (1979). Neuronal chemotaxis: chick dorsal-root axons turn toward high concentrations of nerve growth factor. Science 206, 1079-1080.
13. Gundersen, R. W. and Barrett, J. N. (1980). Characterization of the turning response of dorsal root neurites toward nerve growth factor. J. Cell Biol. 87, 546-554.
14. Heerssen, H. M. and Segal, R. A. (2002). Location, location, location: a spatial view of neurotrophin signal transduction. Trends Neurosci. 25, 160-165.
15. Hirokawa, N. (1982). Cross-linker system between neurofilaments, microtubules, and membranous organelles in frog axons revealed by the quick-freeze, deep-etching method. J. Cell Biol. 94, 129-142.
16. Hollenbeck, P. J. (1993). Products of endocytosis and autophagy are retrieved from axons by regulated retrograde organelle transport. J. Cell Biol. 121, 205-215.
17. Hollenbeck, P. J. (1996). The pattern and mechanism of mitochondrial transport in axons. Front. Biosci. 1, 91-102.
18. 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.
19. Huang, E. J. and Reichardt, L. F. (2001). Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24, 677-736.
20. Johnson, L. V., Walsh, M. L., Bockus, B. J. and Chen, L. B. (1981). Monitoring of relative mitochondrial membrane potential in living cells by fluorescence microscopy. J. Cell Biol. 88, 526-535.
21. Jung, D., Filliol, D., Miehe, M. and Rendon, A. (1993). Interaction of brain mitochondria with microtubules reconstituted from brain tubulin and MAP2 or tau. Cell Motil. Cytoskeleton 24, 245-255.
22. Kageyama, G. H. and Wong-Riley, M. (1982). Histochemical localization of cytochrome oxidase in the hippocampus: correlation with specific neuronal types and afferent pathways. Neurosci. 7, 2337-2361.
23. Kaplan, D. R. and Stephens, R. M. (1994). Neurotrophin signal transduction by Trk receptor. J. Neurobiol. 25, 1404-1417.
24. Kimura, K., Hattori, S., Kabuyama, Y., Shizawa, Y., Takayanagi, J., Nakamura, S., Toki, S., Matsuda, Y., Onodera, K., and Fukui, Y. (1994). Neurite outgrowth of PC12 cells is suppressed by wortmannin, a specific inhibitor of phosphatidylinositol 3-kinase. J. Biol. Chem. 269, 18961-18967.
25. Kuruvilla, R., Ye, H. and Ginty, D. D. (2000). Spatially and functionally distinct roles of the PI3-K effector pathway during NGF signaling in sympathetic neurons. Neuron 27, 499-512.
26. Leterrier, J. F., Rusakov, D. A., Nelson, B. D. and Linden, M. (1994). Interactions between brain mitochondria and cytosleleton: evidence for specialized outer membrane domains involved in the association of cytoskeleton-associated proteins to mitochondria in situ and in vitro. Microsc. Res. Tech. 27, 233-261.
27. Letourneau, P. C. (1978). Chemotactic response of nerve fiber elongation to nerve growth factor. Dev. Biol. 66, 183-196.
28. Lewin, G. R. and Barde, Y. A. (1996). Physiology of the neurotrophins. Annu. Rev. Neurosci. 19, 289-317.
29. 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.
30. Linden, M., Nelson, B. D. and Leterrier, J. F. (1989). The specific binding of the microtubule-associated protein 2 (MAP2) to the outer membrane of rat brain mitochondria. Biochem. J. 261, 167-173.
31. MacInnis, B. L. and Campenot, R. B. (2002). Retrograde support of neuronal survival without retrograde transport of nerve growth factor. Science 295, 1536-1539.
32. Morfini, G., Szebenyi, G., Elluru, R., Ratner, N. and Brady, S. T. (2002). Glycogen synthase kinase 3 phosphorylates kinesin light chains and negatively regulates kinesin-based motility. EMBO J. 21, 281-293.
33. 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.
34. Morris, R. L. and Hollenbeck, P. J. (1995). Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons. J. Cell Biol. 131, 1315-1326.
35. Otten, U., Goedert, M., Mayer, N. and Lembeck, F. (1980). Requirement of nerve growth factor for development of substance P-containing sensory neurones. Nature 287, 158-159.
36. Overly, C. C., Rieff, H. I. and Hollenbeck, P. J. (1996). Axonal and dendritic organelle transport in hippocampal neurons: differences in organization and behavior. J. Cell Sci. 109, 971-980.
37. Patapoutian, A. and Reichardt, L. F. (2001). Trk receptors: mediators of neurotrophin action. Curr. Opin. Neurobiol. 11, 272-280.
38. Paves, H. and Saarma, M. (1997). Neurotrophins as in vitro growth cone guidance molecules for embryonic sensory neurons. Cell Tissue Res. 290, 285-297.
39. Reilein, A. R., Rogers, S. L., Tuma, M. C. and Gelfand, V. I. (2001). Regulation of molecular motor proteins. Int. Rev. Cytol. 204, 179-238.
40. Schnapp, B. J. and Reese, T. S. (1982). Cytoplasmic structure in rapid-frozen axons. J. Cell Biol. 94, 667-679.
41. Schu, P. V., Takegawa, K., Fry, M. J., Stack, J. H., Waterfield, M. D. and Emr, S. D. (1993). Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science 260, 88-91.
42. Smith, D. S., Jarlfors, U. and Cayer, M. L. (1977). Structural cross-bridges between microtubules and mitochondria in central axons of an insect (Periplaneta americana). J. Cell Sci. 27, 255-272.
43. Sofroniew, M. V., Howe, C. L. and Mobley, W. C. (2001) Nerve growth factor signaling, neuroprotection, and neural repair. Annu. Rev. Neurosci. 24, 1217-1281.
44. Toma, J. G., Rogers, D., Senger, D. L., Campenot, R. B. and Miller, F. D. (1997). Spatial regulation of neuronal gene expression in response to nerve growth factor. Dev. Biol. 184, 1-9.
45. Tuma, M. C. and Gelfand, V. I. (1999). Molecular mechanisms of pigment transport in melanophores. Pigment Cell Res. 12, 283-294.
46. Verge, V. M., Riopelle, R. J. and Richardson, P. M. (1989). Nerve growth factor receptors on normal and injured sensory neurons. J. Neurosci. 9, 914-922.
47. Vlahos, C. J., Matter, W. F., Hui, K. Y. and Brown, R. F. (1994). A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269, 5241-5248.
48. Walker, E. H., Pacold M. E., Perisic, O., Stephens, L., Hawkins, P. T., Wymann, M. P. and Williams, R. L. (2000). Structural determinants of phosphoinositide 3-kinase inhibition by wortmannin, LY294002, quercetin, myricetin, and staurosporine. Mol. Cell 6, 909-919.
49. Wong-Riley, M. and Welt, C. (1980). Histochemical changes in cytochrome oxidase of cortical barrels after vibrissal removal in neonatal and adult mice. Proc. Natl. Acad. Sci. USA 77, 2333-2337.
50. Yano, H., Nakanishi, S., Kimura, K., Hanai, N., Saitoh, Y., Fukui, Y., Nonomura, Y. and Matsuda, Y. (1993). Inhibition of histamine secretion by wortmannin through the blockade of phosphatidylinositol 3-kinase in RBL-2H3 cells. J. Biol. Chem. 268, 25846-25856.
51. Yasuda, T., Sobue, G., Ito, T., Mitsuma, T. and Takahashi, A. (1990). Nerve growth factor enhances neurite arborization of adult sensory neurons; a study in single-cell culture. Brain Res. 524, 54-63.