Dynein motors transport activated Trks to promote survival of target-dependent neurons

Nature Neuroscience

Volumn 7, Issue 6, 2004, Pages 596-604

  Heerssen, Heather M ^a   Pazyra, Maria F ^a   Segal, Rosalind A ^a  

^a DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; FLUORESCENT DYE; MOLECULAR MOTOR; NERVE GROWTH FACTOR RECEPTOR; NEUROTROPHIN; NEUROTROPHIN RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DEGENERATIVE DISEASE; EMBRYO; ENZYME ACTIVITY; IMAGING; INTERNALIZATION; MUTATION; NERVE CELL; NERVE CELL DEGENERATION; NERVE ENDING; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; RAT; TARGET CELL;

ANIMALS; AXONAL TRANSPORT; CELL SURVIVAL; CELLS, CULTURED; DYNEIN ATPASE; FEMALE; GANGLIA, SPINAL; NERVE GROWTH FACTORS; NEURONS; PREGNANCY; RATS; RECEPTORS, NERVE GROWTH FACTOR;

EID: 2542421751     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1242     Document Type: Article

References (50)

1. Goldstein, L.S. & Yang, Z. Microtubule-based transport systems in neurons: the roles of kinesins and dyneins. Annu. Rev. Neurosci. 23, 39-71 (2000).
2. Puls, I. et al. Mutant dynactin in motor neuron disease. Nat. Genet. 33, 455-456 (2003).
3. Hafezparast, M. et al. Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science 300, 808-812 (2003).
4. LaMonte, B. et al. Disruption of dynein/dynactin inhibits axonal transport in motor neurons causing late-onset progressive degeneration. Neuron 34, 715-727 (2002).
5. Segal, R.A. Selectivity in neurotrophin signaling: theme and variations. Annu. Rev. Neurosci. 26, 299-330 (2003).
6. Beattie, E.C. et al. A signaling endosome hypothesis to explain NGF actions: potential implications for neurodegeneration. Cold Spring Harb. Symp. Quant. Biol. 61, 389-406 (1996).
7. 125I-nerve growth factor in cultured rat sympathetic neurons. J. Neurosci. 2, 431-442 (1982).
8. Howe, C.L., Valletta, J.S., Rusnak, A.S. & Mobley, W.C. NGF signaling from clathrin-coated vesicles, evidence that signaling endosomes serve as a platform for the ras-MAPK pathway. Neuron 32, 801-814 (2001).
9. Watson, F.L. et al. Rapid nuclear responses to target-derived neurotrophins require retrograde transport of ligand-receptor complex. J. Neurosci. 19, 7889-7900 (1999).
10. Korsching, S. & Thoenen, H. Quantitative demonstration of the retrograde axonal transport of endogenous nerve growth factor. Neurosci. Lett. 39, 1-4 (1983).
11. Tsui-Pierchala, B.A. & Ginty, D.D. Characterization of an NGF-P-trkA retrograde-signaling complex and age-dependent regulation of TrkA phosphorylation in sympathetic neurons. J. Neurosci. 19, 8207-8218 (1999).
12. Delcroix, J.D. et al. NGF signaling in sensory neurons: evidence that early endosomes carry NGF retrograde signals. Neuron 39, 69-84 (2003).
13. MacInnis, B.L. & Campenot, R.B. Retrograde support of neuronal survival without retrograde transport of nerve growth factor. Science 295, 1536-1539 (2002).
14. Ye, H., Kuruvilla, R., Zweifel, L.S. & Ginty, D.D. Evidence in support of signaling endosome-based retrograde survival of sympathetic neurons. Neuron 39, 57-68 (2003).
15. Campenot, R.B. Local control of neurite development by nerve growth factor. Proc. Natl. Acad. Sci. USA 74, 4516-4519 (1977).
16. Campenot, R.B. NGF and the local control of nerve terminal growth. J. Neurobiol. 25, 599-611 (1994).
17. Hendry, I.A., Stach, R. & Herrup, K. Characteristics of the retrograde axonal transport system for nerve growth factor in the sympathetic nervous system. Brain Res. 82, 117-128 (1974).
18. Stockel, K., Schwab, M. & Thoenen, H. Comparison between the retrograde axonal transport of nerve growth factor and tetanus toxin in motor, sensory and adrenergic neurons. Brain Res. 99, 1-16 (1975).
19. Ure, D.R. & Campenot, R.B. Retrograde transport and steady-state distribution of 1-125-nerve growth factor in rat sympathetic neurons in compartmented cultures. J. Neurosci. 17, 1282-1290 (1997).
20. Watson, F.L. et al. Neurotrophins use the Erk5 pathway to mediate a retrograde survival response. Nat. Neurosci. 4, 981-988 (2001).
21. Zhang, Y., Moheban, D., Conway, B., Bhattacharyya, A. & Segal, R. Cell surface Trk receptors mediate NGF-induced survival while internalized receptors regulate NGF-induced differentiation. J. Neurosci. 20, 5671-5678 (2000).
22. Damke, H., Baba, T., Warnock, D.E. & Schmid, S.L. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell. Biol. 127, 915-934 (1994).
23. Henley, J.R., Krueger, E.W., Oswald, B.J. & McNiven, M.A. Dynamin-mediated internalization of caveolae. J. Cell. Biol. 141, 85-99 (1998).
24. Herskovits, J.S., Burgess, C.C., Obar, R.A. & Vallee, R.B. Effects of mutant rat dynamin on endocytosis. J. Cell. Biol. 122, 565-578 (1993).
25. Kranenburg, O., Verlaan, I. & Moolenaar, W. Dynamin is required for the activation of mitogen-activated protein (MAP) kinase by MAP kinase kinase. J. Biol. Chem. 274, 24575-24578 (1999).
26. Davies, P.J. et al. Studies on the effects of dansylcadaverine and related compounds on receptor-mediated endocytosis in cultured cells. Diabetes Care 7 (suppl. 1), 35-41 (1984).
27. Noda, Y. et al. KIFC3, a microtubule minus end-directed motor for the apical transport of annexin XIIIb-associated Triton-insoluble membranes. J. Cell. Biol. 155, 77-88 (2001).
28. Muresan, V. One axon, many kinesins: what's the logic? J. Neurocytol. 29, 799-818 (2000).
29. Bhattacharyya, A. et al. High resolution imaging demonstrates dynein based vesicular transport of activated Trk receptor. J. Neurobiol. 51, 302-312 (2002).
30. Yano, H. et al. Association of Trk neurotrophin receptors with components of the cytoplasmic dynein motor. J. Neurosci. 21, RC125 (2001).
31. Echeverri, C.J., Paschal, B.M., Vaughan, K.T. & Vallee, R.B. Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis. J. Cell Biol. 132, 617-633 (1996).
32. Presley, J.F. et al. ER-to-Golgi transport visualized in living cells. Nature 389, 81-85 (1997).
33. Burkhardt, J.K., Echeverri, C.J., Nilsson, T. & Vallee, R.B. Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J. Cell Biol. 139, 469-484 (1997).
34. Riccio, A., Pierchala, B.A., Ciarallo, C.L. & Ginty, D.D. An NGF-Trka-mediated retrograde signal to transcription factor CREB in sympathetic neurons. Science 277, 1097-1100 (1997).
35. Senger, D.L. & Campenot, R.B. Rapid retrograde tyrosine phosphorylation of TrkA and other proteins in rat sympathetic neurons in compartmented cultures. J. Cell. Biol. 138, 411-421 (1997).
36. Ginty, D.D. & Segal, R.A. Retrograde neurotrophin signaling: Trk-ing along the axon. Curr. Opin. Neurobiol. 12, 268-274 (2002).
37. Mayer, T.U. et al. Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science 286, 971-974 (1999).
38. Ferhat, L. et al. Expression of the mitotic motor protein Eg5 in postmitotic neurons: implications for neuronal development. J. Neurosci. 18, 7822-7835 (1998).
39. Verveer, P.J., Wouters, F.S., Reynolds, A.R. & Bastiaens, P.I. Quantitative imaging of lateral ErbB1 receptor signal propagation in the plasma membrane. Science 290, 1567-1570 (2000).
40. Hempstead, B.L. et al. Overexpression of the Trk tyrosine kinase rapidly accelerates nerve growth factor-induced differentiation. Neuron 9, 883-896 (1992).
41. Lee, F.S. & Chao, M.V. Activation of Trk neurotrophin receptors in the absence of neurotrophins. Proc. Natl. Acad. Sci. USA 98, 3555-3560 (2001).
42. Waterman, H., Sabanai, I., Geiger, B. & Yarden, Y. Alternative intracellular routing of ErbB receptors may determine signaling potency. J. Biol. Chem. 273, 13819-13827 (1998).
43. Yang, Y. et al. The gene encoding alsin, a protein with three guanine-nucleotide exchange factor domains, is mutated in a form of recessive amyotrophic lateral sclerosis. Nat. Genet. 29, 160-165 (2001).
44. Parkinson, N.J. et al. Mutant β-spectrin 4 causes auditory and motor neuropathies in quivering mice. Nat. Genet. 29, 61-65 (2001).
45. Liu, X. & Jaenisch, R. Severe peripheral sensory neuron loss and modest motor neuron reduction in mice with combined deficiency of brain-derived neurotrophic factor, neurotrophin 3 and neurotrophin 4/5. Dev. Dyn. 218, 94-101 (2000).
46. Henderson, C.E. et al. GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266, 1062-1064 (1994).
47. DeChiara, T.M. et al. Mice lacking the CNTF receptor, unlike mice lacking CNTF, exhibit profound motor neuron deficits at birth. Cell 83, 313-322 (1995).
48. Li, M., Sendtner, M. & Smith, A. Essential function of LIF receptor in motor neurons. Nature 378, 724-727 (1995).
49. Segal, R. et al. Differential utilization of Trk autophosphorylation sites. J. Biol. Chem. 271, 20175-20181 (1996).
50. He, T-C. et al. A simplified system for generating recombinant adenovirus. Proc. Natl. Acad. Sci. USA 95, 2509-2514 (1998).