Differential endocytic sorting of p75NTR and TrkA in response to NGF: A role for late endosomes in TrkA trafficking

Molecular and Cellular Neuroscience

Volumn 28, Issue 3, 2005, Pages 571-587

  Saxena, Smita ^a   Howe, Charles L ^b   Cosgaya, José M ^c,f   Steiner, Pascal ^d   Hirling, Harald ^d   Chan, Jonah R ^c   Weis, Joachim ^a,e   Krüttgen, Alex ^a,e  

^a UNIVERSITY OF BERN   (Switzerland)

^b MAYO CLINIC   (United States)

^c STANFORD UNIVERSITY   (United States)

^d EPFL   (Switzerland)

^e RWTH AACHEN UNIVERSITY   (Germany)

^f INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

NERVE GROWTH FACTOR; NERVE GROWTH FACTOR RECEPTOR; NEUROTROPHIN RECEPTOR; PROTEIN P75; PROTEIN TYROSINE KINASE A;

ANIMAL CELL; ARTICLE; CELL ORGANELLE; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; ENZYME PHOSPHORYLATION; IMMUNOREACTIVITY; LYSOSOME; NEUROCHEMISTRY; NEUROPATHOLOGY; NEUROPHARMACOLOGY; NONHUMAN; PHARMACODYNAMICS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; RAT; RECEPTOR BINDING; SIGNAL TRANSDUCTION;

EID: 14644394937     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2004.11.011     Document Type: Article

References (79)

1. R.F. Alderson, R. Curtis, A.L. Alterman, R.M. Lindsay, and P.S. DiStefano Truncated TrkB mediates the endocytosis and release of BDNF and neurotrophin-4/5 by rat astrocytes and Schwann cells in vitro Brain Res. 871 2000 210 222
2. P.A. Barker, and E.M. Shooter Disruption of NGF binding to the low affinity neurotrophin receptor p75LNTR reduces NGF binding to TrkA on PC12 cells Neuron 13 1994 203 215
3. E.C. Beattie, C.L. Howe, A. Wilde, F.M. Brodsky, and W.C. Mobley NGF signals through TrkA to increase clathrin at the plasma membrane and enhance clathrin-mediated membrane trafficking J. Neurosci. 20 2000 7325 7333
4. M.M. Berg, D.W. Sternberg, L.F. Parada, and M.V. Chao K-252a inhibits nerve growth factor-induced trk proto-oncogene tyrosine phosphorylation and kinase activity J. Biol. Chem. 267 1992 13 16
5. A. Bhattacharyya, F.L. Watson, S.L. Pomeroy, Y.Z. Zhang, C.D. Stiles, and R.A. Segal High-resolution imaging demonstrates dynein-based vesicular transport of activated Trk receptors J. Neurobiol. 51 2002 302 312
6. M. Bibel, E. Hoppe, and Y.A. Barde Biochemical and functional interactions between the neurotrophin receptors trk and p75NTR EMBO J. 18 1999 616 622
7. M. Bomsel, R. Parton, S.A. Kuznetsov, T.A. Schroer, and J. Gruenberg Microtubule- and motor-dependent fusion in vitro between apical and basolateral endocytic vesicles from MDCK cells Cell 62 1990 719 731
8. M. Bothwell Functional interactions of neurotrophins and neurotrophin receptors Annu. Rev. Neurosci. 18 1995 223 253
9. M. Bothwell, and E. Giniger Alzheimer's disease: neurodevelopment converges with neurodegeneration Cell 102 2000 271 273
10. F.C. Bronfman, M. Tcherpakov, T.M. Jovin, and M. Fainzilber Ligand-induced internalization of the p75 neurotrophin receptor: a slow route to the signaling endosome J. Neurosci. 23 2003 3209 3220
11. S. Buxser, D. Decker, and P. Ruppel Relationship among types of nerve growth factor receptors on PC12 cells J. Biol. Chem. 265 1990 12701 12710
12. N. Cabrera, E. Diaz-Rodriguez, E. Becker, D. Martin-Zanca, and A. Pandiella TrkA receptor ectodomain cleavage generates a tyrosine-phosphorylated cell-associated fragment J. Cell. Biol. 132 1996 427 436
13. P. Claude, E. Hawrot, D.A. Dunis, and R.B. Campenot Binding, internalization, and retrograde transport of 125I-nerve growth factor in cultured rat sympathetic neurons J. Neurosci. 2 1982 431 442
14. G. Dechant, and Y.A. Barde The neurotrophin receptor p75(NTR): novel functions and implications for diseases of the nervous system Nat. Neurosci. 5 2002 1131 1136
15. J.D. Delcroix, J.S. Valletta, C. Wu, S.J. Hunt, A.S. Kowal, and W.C. Mobley NGF signaling in sensory neurons: evidence that early endosomes carry NGF retrograde signals Neuron. 39 2003 69 84
16. E. Diaz-Rodriguez, N. Cabrera, A. Esparis-Ogando, J.C. Montero, and A. Pandiella Cleavage of the TrkA neurotrophin receptor by multiple metalloproteases generates signalling-competent truncated forms Eur. J. Neurosci. 11 1999 1421 1430
17. P.P. Di Fiore, and P. De Camilli Endocytosis and signaling. An inseparable partnership Cell 106 2001 1 4
18. L. Dombrowski, R. Faure, and A. Marette Sustained activation of insulin receptors internalized in GLUT4 vesicles of insulin-stimulated skeletal muscle Diabetes 49 2000 1772 1782
19. D.D. Eveleth, and R.A. Bradshaw Nerve growth factor nonresponsive pheochromocytoma cells: altered internalization results in signaling dysfunction J. Cell. Biol. 117 1992 291 299
20. S. Felder, K. Miller, G. Moehren, A. Ullrich, J. Schlessinger, and C.R. Hopkins Kinase activity controls the sorting of the epidermal growth factor receptor within the multivesicular body Cell 61 1990 623 634
21. D.D. Ginty, and R.A. Segal Retrograde neurotrophin signaling: Trk-ing along the axon Curr. Opin. Neurobiol. 12 2002 268 274
22. M.L. Grimes, J. Zhou, E.C. Beattie, E.C. Yuen, D.E. Hall, J.S. Valletta, K.S. Topp, J.H. LaVail, N.W. Bunnett, and W.C. Mobley Endocytosis of activated TrkA: evidence that nerve growth factor induces formation of signaling endosomes J. Neurosci. 16 1996 7950 7964
23. J. Gruenberg The endocytic pathway: a mosaic of domains Nat. Rev., Mol. Cell Biol. 2 2001 721 730
24. A. Haapasalo, I. Sipola, K. Larsson, K.E. Akerman, P. Stoilov, S. Stamm, G. Wong, and E. Castren Regulation of TRKB surface expression by brain-derived neurotrophic factor and truncated TRKB isoforms J. Biol. Chem. 277 2002 43160 43167
25. X.L. He, and K.C. Garcia Structure of nerve growth factor complexed with the shared neurotrophin receptor p75 Science 304 2004 870 875
26. A. Hemar, A. Subtil, M. Lieb, E. Morelon, R. Hellio, and A. Dautry-Varsat Endocytosis of interleukin 2 receptors in human T lymphocytes: distinct intracellular localization and fate of the receptor alpha, beta, and gamma chains J. Cell Biol. 129 1995 55 64
27. B.L. Hempstead The many faces of p75NTR Curr. Opin. Neurobiol. 12 2002 260 267
28. B.L. Hempstead, D. Martin-Zanca, D.R. Kaplan, L.F. Parada, and M.V. Chao High-affinity NGF binding requires coexpression of the trk proto-oncogene and the low-affinity NGF receptor Nature 350 1991 678 683
29. L.P. Henderson, L. Lin, A. Prasad, C.A. Paul, T.Y. Chang, and R.A. Maue Embryonic striatal neurons from Niemann-pick type C mice exhibit defects in cholesterol metabolism and neurotrophin responsiveness J. Biol. Chem. 275 2000 20179 20187
30. M. Hosang, and E.M. Shooter The internalization of nerve growth factor by high-affinity receptors on pheochromocytoma PC12 cells EMBO J. 6 1987 1197 1202
31. C.L. Howe, J.S. Valletta, A.S. Rusnak, and W.C. Mobley NGF signaling from clathrin-coated vesicles: evidence that signaling endosomes serve as a platform for the Ras-MAPK pathway Neuron 32 2001 801 814
32. S. Jing, P. Tapley, and M. Barbacid Nerve growth factor mediates signal transduction through trk homodimer receptors Neuron 9 1992 1067 1079
33. J. Jullien, V. Guili, L.F. Reichardt, and B.B. Rudkin Molecular kinetics of nerve growth factor receptor trafficking and activation J. Biol. Chem. 277 2002 38700 38708
34. J. Jullien, V. Guili, E.A. Derrington, J.L. Darlix, L.F. Reichardt, and B.B. Rudkin Trafficking of TrkA-green fluorescent protein chimerae during nerve growth factor-induced differentiation J. Biol. Chem. 278 2003 8706 8716
35. K.M. Jung, S. Tan, N. Landman, K. Petrova, S. Murray, R. Lewis, P.K. Kim, D.S. Kim, S.H. Ryu, M.V. Chao, and T.W. Kim Regulated intramembrane proteolysis of the p75 neurotrophin receptor modulates its association with the TrkA receptor J. Biol. Chem. 278 2003 42161 42169
36. P. Kahle, P.A. Barker, E.M. Shooter, and C. Hertel p75 nerve growth factor receptor modulates p140trkA kinase activity, but not ligand internalization, in PC12 cells J. Neurosci. Res. 38 1994 599 606
37. K.C. Kanning, M. Hudson, P.S. Amieux, J.C. Wiley, M. Bothwell, and L.C. Schecterson Proteolytic processing of the p75 neurotrophin receptor and two homologs generates C-terminal fragments with signaling capability J. Neurosci. 23 2003 5425 5436
38. D.R. Kaplan, and F.D. Miller Neurotrophin signal transduction in the nervous system Curr. Opin. Neurobiol. 10 2000 381 391
39. S.P. Lad, D.A. Peterson, R.A. Bradshaw, and K.E. Neet Individual and combined effects of TrkA and p75NTR nerve growth factor receptors. A role for the high affinity receptor site J. Biol. Chem. 278 2003 24808 24817
40. P.G. Layer, and E.M. Shooter Binding and degradation of nerve growth factor by PC12 pheochromocytoma cells J. Biol. Chem. 258 1983 3012 3018
41. C. Lebrand, M. Corti, H. Goodson, P. Cosson, V. Cavalli, N. Mayran, J. Faure, and J. Gruenberg Late endosome motility depends on lipids via the small GTPase Rab7 EMBO J. 21 2002 1289 1300
42. F.S. Lee, A.H. Kim, G. Khursigara, and M.V. Chao The uniqueness of being a neurotrophin receptor Curr. Opin. Neurobiol. 11 2001 281 286
43. F. Liang, and R.L. Huganir Coupling of agonist-induced AMPA receptor internalization with receptor recycling J. Neurochem. 77 2001 1626 1631
44. S.X. Lin, W.G. Mallet, A.Y. Huang, and F.R. Maxfield Endocytosed cation-independent mannose 6-phosphate receptor traffics via the endocytic recycling compartment en route to the trans-Golgi network and a subpopulation of late endosomes Mol. Biol. Cell 15 2004 721 733
45. K.E. Longva, F.D. Blystad, E. Stang, A.M. Larsen, L.E. Johannessen, and I.H. Madshus Ubiquitination and proteasomal activity is required for transport of the EGF receptor to inner membranes of multivesicular bodies J. Cell Biol. 156 2002 843 854
46. B.L. MacInnis, and R.B. Campenot Retrograde support of neuronal survival without retrograde transport of nerve growth factor Science 295 2002 1536 1539
47. D. Mahadeo, L. Kaplan, M.V. Chao, and B.L. Hempstead High affinity nerve growth factor binding displays a faster rate of association than p140trk binding. Implications for multi-subunit polypeptide receptors J. Biol. Chem. 269 1994 6884 6891
48. F.R. Maxfield, and T.E. McGraw Endocytic recycling Nat. Rev., Mol. Cell Biol. 5 2004 121 132
49. S.O. Meakin, and E.M. Shooter The nerve growth factor family of receptors Trends. Neurosci. 15 1992 323 331
50. A. Meyer-Franke, G.A. Wilkinson, A. Kruttgen, M. Hu, E. Munro, M.G. Hanson Jr., L.F. Reichardt, and B.A. Barres Depolarization and cAMP elevation rapidly recruit TrkB to the plasma membrane of CNS neurons Neuron 21 1998 681 693
51. K.E. Neet, and R.B. Campenot Receptor binding, internalization, and retrograde transport of neurotrophic factors Cell. Mol. Life. Sci. 58 2001 1021 1035
52. M.P. Oksvold, E. Skarpen, L. Wierod, R.E. Paulsen, and H.S. Huitfeldt Re-localization of activated EGF receptor and its signal transducers to multivesicular compartments downstream of early endosomes in response to EGF Eur. J. Cell. Biol. 80 2001 285 294
53. R.G. Parton, K. Simons, and C.G. Dotti Axonal and dendritic endocytic pathways in cultured neurons J. Cell. Biol. 119 1992 123 137
54. A.A. Peden, V. Oorschot, B.A. Hesser, C.D. Austin, R.H. Scheller, and J. Klumperman Localization of the AP-3 adaptor complex defines a novel endosomal exit site for lysosomal membrane proteins J. Cell Biol. 164 2004 1065 1076
55. P.P. Roux, and P.A. Barker Neurotrophin signaling through the p75 neurotrophin receptor Prog. Neurobiol. 67 2002 203 233
56. G. Rudenko, L. Henry, K. Henderson, K. Ichtchenko, M.S. Brown, J.L. Goldstein, and J. Deisenhofer Structure of the LDL receptor extracellular domain at endosomal pH Science 298 2002 2353 2358
57. S. Saxena, C.L. Howe, J.M. Cosgaya, M. Hu, J. Weis, and A. Kruttgen Differences in the surface binding and endocytosis of neurotrophins by p75NTR Mol. Cell. Neurosci. 26 2004 292 307
58. R.A. Segal Selectivity in neurotrophin signaling: theme and variations Annu. Rev. Neurosci. 26 2003 299 330
59. A. Simonsen, R. Lippe, S. Christoforidis, J.M. Gaullier, A. Brech, J. Callaghan, B.H. Toh, C. Murphy, M. Zerial, and H. Stenmark EEA1 links PI(3)K function to Rab5 regulation of endosome fusion Nature 394 1998 494 498
60. W.D. Snider Functions of the neurotrophins during nervous system development: what the knockouts are teaching us Cell 77 1994 627 638
61. A. Sorkin, and M. Von Zastrow Signal transduction and endocytosis: close encounters of many kinds Nat. Rev., Mol. Cell Biol. 3 2002 600 614
62. P.D. Stahl, and M.A. Barbieri Multivesicular bodies and multivesicular endosomes: the "ins and outs" of endosomal traffic Sci. STKE 2002 PE32
63. B.S. Stein, K.G. Bensch, and H.H. Sussman Complete inhibition of transferrin recycling by monensin in K562 cells J. Biol. Chem. 259 1984 14762 14772
64. P. Steiner, J.C. Sarria, L. Glauser, S. Magnin, S. Catsicas, and H. Hirling Modulation of receptor cycling by neuron-enriched endosomal protein of 21 kD J. Cell. Biol. 157 2002 1197 1209
65. S.T. Sweeney, and G.W. Davis Unrestricted synaptic growth in spinster-a late endosomal protein implicated in TGF-beta-mediated synaptic growth regulation Neuron 36 2002 403 416
66. B.A. Tsui-Pierchala, and D.D. Ginty Characterization of an NGF-P-TrkA retrograde-signaling complex and age-dependent regulation of TrkA phosphorylation in sympathetic neurons J. Neurosci. 19 1999 8207 8218
67. J.L. Twiss, and E.M. Shooter Nerve growth factor promotes neurite regeneration in PC12 cells by translational control J. Neurochem. 64 2 1995 550 557
68. D.R. Ure, and R.B. Campenot Retrograde transport and steady-state distribution of 125I-nerve growth factor in rat sympathetic neurons in compartmented cultures J. Neurosci. 17 1997 1282 1290
69. R.G. Vickery, and M. von Zastrow Distinct dynamin-dependent and -independent mechanisms target structurally homologous dopamine receptors to different endocytic membranes J. Cell Biol. 144 1999 31 43
70. C.S. von Bartheld, R. Williams, F. Lefcort, D.O. Clary, L.F. Reichardt, and M. Bothwell Retrograde transport of neurotrophins from the eye to the brain in chick embryos: roles of the p75NTR and trkB receptors J. Neurosci. 16 1996 2995 3008
71. F.L. Watson, H.M. Heerssen, D.B. Moheban, M.Z. Lin, C.M. Sauvageot, A. Bhattacharyya, S.L. Pomeroy, and R.A. Segal Rapid nuclear responses to target-derived neurotrophins require retrograde transport of ligand-receptor complex J. Neurosci. 19 1999 7889 7900
72. G. Weskamp, J. Schlondorff, L. Lum, J.D. Becherer, T.W. Kim, P. Saftig, D. Hartmann, G. Murphy, and C.P. Blobel Evidence for a critical role of the tumor necrosis factor alpha convertase (TACE) in ectodomain shedding of the p75 neurotrophin receptor (p75NTR) J. Biol. Chem. 279 2004 4241 4249
73. W. Wunderlich, I. Fialka, D. Teis, A. Alpi, A. Pfeifer, R.G. Parton, F. Lottspeich, and L.A. Huber A novel 14-kilodalton protein interacts with the mitogen-activated protein kinase scaffold mp1 on a late endosomal/lysosomal compartment J. Cell Biol. 152 2001 765 776
74. Y. Yarden Biology of HER2 and its importance in breast cancer Oncology 61 Suppl. 2 2001 1 13
75. H. Ye, R. Kuruvilla, L.S. Zweifel, and D.D. Ginty Evidence in support of signaling endosome-based retrograde survival of sympathetic neurons Neuron 39 2003 57 68
76. A. Zapf-Colby, and J.M. Olefsky Nerve growth factor processing and trafficking events following TrkA-mediated endocytosis Endocrinology 139 1998 3232 3240
77. Y. Zhang, D.B. Moheban, B.R. Conway, A. Bhattacharyya, and R.A. Segal Cell surface Trk receptors mediate NGF-induced survival while internalized receptors regulate NGF-induced differentiation J. Neurosci. 20 2000 5671 5678
78. A.A. Zupan, and E.M. Johnson Jr. Evidence for endocytosis-dependent proteolysis in the generation of soluble truncated nerve growth factor receptors by A875 human melanoma cells J. Biol. Chem. 266 1991 15384 15390
79. A.A. Zupan, P.A. Osborne, C.E. Smith, N.R. Siegel, R.M. Leimgruber, and E.M. Johnson Jr. Identification, purification, and characterization of truncated forms of the human nerve growth factor receptor J. Biol. Chem. 264 1989 11714 11720