Endocytosis of activated trkA: Evidence that nerve growth factor induces formation of signaling endosomes

Journal of Neuroscience

Volumn 16, Issue 24, 1996, Pages 7950-7964

  Grimes, Mark L ^a   Zhou, Jie ^b   Beattie, Eric C ^c   Yuen, Eric C ^b   Hall, Deborah E ^b   Valletta, Janice S ^b   Topp, Kimberly S ^b,c   LaVail, Jennifer H ^b,c   Bunnett, Nigel W ^c   Mobley, William C ^b  

^a MASSEY UNIVERSITY   (New Zealand)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

clathrin; endosome; NGF; PLC 1; signaling; TrkA

Indexed keywords

ALPHA ADAPTIN; CELL PROTEIN; CLATHRIN; GLYCOPROTEIN GP 140; NERVE GROWTH FACTOR; PHOSPHOLIPASE C; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL ORGANELLE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; INTERNALIZATION; NONHUMAN; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

EID: 10544248585     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-24-07950.1996     Document Type: Article

References (75)

1. Balch WE, Rothman JE (1985) Characterization of protein transport between successive compartments of the Golgi apparatus: asymmetric properties of donor and acceptor activities in a cell-free system. Arch Biochem Biophys 240:413-425.
2. Barker PA, Shooter EM (1994) Disruption of NGF binding to the low affinity neurotrophin receptor p75LNTR reduces NGF binding to trkA on PC12 cells. Neuron 13:203-215.
3. Bernd P, Greene LA (1983) Electron microscopic radioautographic localization of iodinated nerve growth factor bound to and internalized by PC12 cells. J Neurosci 3:631-643.
4. 125I-nerve growth factor with PC12 pheochromocytoma cells: evidence for internalization via high-affinity receptors only and for long-term regulation by nerve growth factor of both high- and low-affinity receptors. J Biol Chem 259:15509-15516.
5. Bothwell M (1995) Functional interactions of neurotrophins and neurotrophin receptors. Annu Rev Neurosci 18:223-253.
6. Bothwell M (1996) p75NTR: a receptor after all. Science 272:506-507.
7. Brodsky FM (1985) Clathrin structure characterized with monoclonal antibodies. I. Analysis of multiple antigenic sites. J Cell Biol 101:2047-2054.
8. Campenot RB (1977) Local control of neurite development by nerve growth factor. Proc Natl Acad Sci USA 74:4516-4519.
9. Carter BD, Kaltschmidt C, Kaltschmidt B, Offenhäuser N, Böhm-Matthaei R, Baeuerle PA, Barde Y-A (1996) Selective activation of NF-kappaB by nerve growth factor through the neurotrophin receptor p75. Science 272:542-545.
10. Chin DJ, Straubinger RM, Acton S, Nathke I, Brodsky FM (1989) 100 kDa polypeptides in peripheral clathrin-coated vesicles are require for receptor-mediated endocytosis. Proc Natl Acad Sci USA 86:9289-9293.
11. Clary DO, Weskamp G, Austin LR, Reichardt LF (1994) TrkA cross-linking mimics neuronal responses to nerve growth factor. Mol Biol Cell 5:549-563.
12. 125I-nerve growth factor in cultured rat sympathetic neurons. J Neurosci 2:431-442.
13. Crowley C, Spencer SD, Nishimura MC, Chen KS, Pitts MS, Armanini MP, Ling LH, MacMahon SB, Shelton DL, Levinson AD, et al (1994) Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76:1001-1011.
14. Curtis R, Adryan KM, Stark JL (1995) Differential role of the low affinity neurotrophin receptor (p75) in retrograde axonal transport of the neurotrophins. Neuron 14:1201-1211.
15. Davies AM, Lee K-F, Jaenisch R (1993) p75-deficient trigeminal sensory neurons have an altered response to NGF hut not to other neurotrophins. Neuron 11:565-574.
16. Ehlers MD, Kaplan DR, Price DL, Koliatsos VE (1995) NGF-stimulated retrograde transport of TrkA in the mammalian nervous system. J Cell Biol 130:1-8.
17. Eveleth DD, Bradshaw RA (1988) Internalization and cycling of nerve growth factor in PC12 cells: interconversion of type II (fast) and type I (slow) nerve growth factor receptors. Neuron 1:929-936.
18. Grady EF, Garland AM, Gamp PD, Lovett M, Payan DG, Bunnett NW (1995) Delineation of the endocytic pathway of substance P and its seven-transmembrane domain NK1 receptor. Mol Biol Cell 6:509-524.
19. Grimaldi KA, Hutton JC, Siddle K (1987) Production and characterization of monoclonal antibodies to insulin secretory granule membranes. Biochem J 245:557-566.
20. Grimes ML, Kelly RB (1992a) Sorting of chromogranin B into immature secretory granules in pheochromocytoma (PC12) cells. Ann NY Acad Sci 674:38-52.
21. Grimes ML, Kelly RB (1992b) Intermediates in the constitutive and regulated secretory pathways released in vitro from semi-intact cells. J Cell Biol 117:539-549.
22. Grimes ML, Zhou J, Li Y, Holtzman D, Mobley WC (1993) Neurotrophin signalling in the nervous system. Semin Neurosci 5:239-247.
23. Haass C, Koo EH, Mellon A, Hung AY, Selkoe DJ (1992) Targeting of cell-surface beta-amyloid precursor protein to lysosomes: alternative processing into amyloid-bearing fragments. Nature 357:500-503.
24. Hantzopoulos PA, Suri C, Glass DJ, Goldfarb MP, Yancopoulos GD (1994) The low affinity NGF receptor, p75, can collaborate with each of the trks to potentiate functional responses to the neurotrophins. Neuron 13:187-201.
25. Hartman DS, McCormack M, Schubenel R, Hertel C (1992) Multiple trkA proteins in PC12 cells bind NGF with a slow association rate. J Biol Chem 267:24516-24522.
26. Hendry IA (1977) The effect of the retrograde axonal transport of nerve growth factor on the morphology of adrenergic neurones. Brain Res 134:213-223.
27. Hendry I, Bonyhady R (1980) Retrogradely transported nerve growth factor increases ornithine decarboxylase activity in rat superior cervical ganglia. Brain Res 200:39-45.
28. Hendry IA, Stach R, Herrup K (1974a) Characteristics of the retrograde axonal transport system for nerve growth factor in the sympathetic nervous system. Brain Res 82:117-128.
29. Hendry IA, Stockel K, Thoenen H, Iversen LL (1974b) The retrograde axonal transport of nerve growth factor. Brain Res 68:103-121.
30. Heumann R, Schwab M, Merkl R, Thoenen H (1984) Nerve growth factor-mediated induction of choline acetyltransferase in PC12 cells: evaluation of the site of action of nerve growth factor and the involvement of lysosomal degradation products of nerve growth factor. J Neurosci 4:3039-3050.
31. Hollenbeck PJ (1993) Products of endocytosis and autophagy are retrieved from axons by regulated retrograde organelle transport. J Cell Biol 121:305-315.
32. Holtzman DM, Kilbridge J, Li Y, Cunningham ET, Lenn NJ, Clary DO, Reichardt LF, Mobley WC (1995) TrkA expression in the CNS: evidence for the existence of several novel NGF-responsive CNS neurons. J Neurosci 15:1567-1576.
33. Hosang M, Shooter EM (1987) The internalization of nerve growth factor by high-affinity receptors on pheochromocytoma PC12 cells. EMBO J 6:1197-1202.
34. Jing S, Tapley P, Barbacid M (1992) Nerve growth factor mediates signal transduction through trk homodimer receptors. Neuron 9:1067-1079.
35. Johnson EMJ, Taniuchi M, Clark HB, Springer JE, Koh S, Tayrien MW, Loy R (1987) Demonstration of the retrograde transport of nerve growth factor receptor in the peripheral and central nervous system. J Neurosci 7:923-929.
36. Kaplan DR, Hempstead BL, Martin-Zanca D, Chao MV, Parada LF (1991) The trk proto-oncogene product: a signal transducing receptor for nerve growth factor. Science 252:554-558.
37. Kaplan DR, Stephens RM (1994) Neurotrophin signal transduction by the Trk receptor. J Neurobiol 25:1404-1417.
38. Kiss J, Shooter EM, Patel AJ (1993) A low-affinity nerve growth factor receptor antibody is internalized and retrogradely transported selectively into cholinergic neurons of the rat basal forebrain. Neuroscience 57:297-305.
39. Klein R, Jing SQ, Nanduri V, O'Rourke E, Barbacid M (1991) The trk proto-oncogene encodes a receptor for nerve growth factor. Cell 65:189-197.
40. Knüsel B, Rabin S, Hefti F, Kaplan D (1994) Regulated neurotrophin receptor responsiveness during neuronal migration and early differentiation. J Neurosci 14:1542-1554.
41. Lamaze C, Schmid SL (1995) Recruitment of epidermal growth factor receptors into coated pits requires their activated tyrosine kinase. J Cell Biol 129:47-54.
42. Layer PG, Shooter EM (1983) Binding and degradation of nerve growth factor by PC12 pheochromocytoma cells. J Biol Chem 258:3012-3018.
43. Lee K-F, Bachman K, Landis S, Jaenisch R (1994) Dependence on p75 for innervation of some sympathetic targets. Science 263:1447-1449.
44. Levi-Montalcini R (1987) The nerve growth factor 35 years later. Science 237:1154-1161.
45. Li Y, Holtzman DM, Kromer LF, Kaplan DR, Chua-Couzens J, Clary DO, Knusel B, Mobley WC (1995) Regulation of TrkA and ChAT expression in developing rat basal forebrain: evidence that both exogenous and endogenous NGF regulate differentiation of cholinergic neurons. J Neurosci 15:2888-2905.
46. Loeb DM, Greene LA (1993) Transfection with trk restores "slow" NGF binding, efficient NGF uptake, and multiple NGF responses to NGF-nonresponsive PC12 cell mutants. J Neurosci 13:2919-2929.
47. Loeb DM, Tsao H, Cobb MH, Greene LA (1992) NGF and other growth factors induce an association between ERK1 and the NGF receptor, gp140protoTrk. Neuron 9:1053-1065.
48. Longo FM, Holtzman DM, Grimes ML, Mobley WC (1993) Nerve growth factor: actions in the peripheral and central nervous systems. In: Neurotrophic factors (Fallon J, Loughlin S, eds), pp 209-256. New York: Academic.
49. Lucidi-Phillipi CA, Clary DO, Reichardt LF, Gage FH (1996) TrkA activation is sufficient to rescue axotomized cholinergic neurons. Neuron 16:653-663.
50. Mahadeo D, Kaplan L, Chao MV, Hempstead BL (1994) High affinity nerve growth factor binding displays a faster rate of association than p140trk binding. J Biol Chem 269:6884-6891.
51. 2+-activated secretion in GH3 pituitary cells. J Biol Chem 264:10299-10308.
52. Martin-Zanca D, Oskam R, Mitra G, Copeland T, Barbacid M (1989) Molecular and biochemical characterization of the human trk protooncogene. Mol Cell Biol 9:24-33.
53. Meakin SO, Shooter EM (1991) Tyrosine kinase activity coupled to the high-affinity nerve growth factor-receptor complex. Proc Natl Acad Sci USA 88:5862-5866.
54. Meakin SO, Shooter EM (1992) The nerve growth factor family of receptors. Trends Neurosci 15:323-331.
55. Mobley WC, Rutkowski JL, Tennekoon GI, Gemski J, Buchanan K, Johnston MV (1986) Nerve growth factor increases choline acetyltransferase activity in developing basal forebrain neurons. Mol Brain Res 387:53-62.
56. Nixon RA, Cataldo AM (1995) The endosomal-lysosomal system of neurons: new roles. Trends Neurosci 18:489-496.
57. Overly CC, Lee K-D, Berthiaume E, Hollenbeck PJ (1995) Quantitative measurement of intraorganelle pH in the endosomal-lysosomal pathway in neurons by using ratiometric imaging with pyranine. Proc Natl Acad Sci USA 92:3156-3160.
58. Paravicini U, Stoeckel K, Thoenen H (1975) Biological importance of retrograde axonal transport of nerve growth factor in adrenergic neurons. Brain Res 84:279-291.
59. Parton RG, Dotti CG (1993) Cell biology of neuronal endocytosis. J Neurosci Res 36:1-9.
60. Parton RG, Simons K, Dotti CG (1992) Axonal and dendritic endocytic pathways in cultured neurons. J Cell Biol 119:123-137.
61. Podlisny MB, Tolan DR, Selkoe DJ (1991) Homology of the amyloid beta protein precursor in monkey and human supports a primate model for beta amyloidosis in Alzheimer's disease. Am J Pathol 138:1423-1435.
62. Radeke MJ, Feinslein SC (1991) Analytical purification of the slow, high affinity NGF receptor: identification of a novel 135 kd polypeptide. Neuron 7:141-150.
63. Raivich G, Hellweg R, Kreutzberg GW (1991) NGF receptor-mediated reduction in axonal NGF uptake and retrograde transport following sciatic nerve injury and during regeneration. Neuron 7:151-164.
64. Schmid SL, Carter LL (1990) ATP is required for receptor-mediated endocytosis in intact cells. J Cell Biol 111:2307-2318.
65. Schwab ME (1977) Ultrastructural localization of a nerve growth factor-horseradish peroxidase (NGF-HRP) coupling product after retrograde axonal transport in adrenergic neurons. Brain Res 130:190-196.
66. Smeyne RJ, Klein R, Schnapp A, Long LK, Bryant S, Lewin A, Lira SA, Barbacid M (1994) Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene. Nature 368:246-249.
67. Stephens RM, Loeb DM, Copeland TD, Pawson T, Greene LA, Kaplan DR (1994) Trk receptors use redundant signal transduction pathways involving SHC and PLC-γ1 to mediate NGF responses. Neuron 12:691-705.
68. Taniuchi M, Johnson EMJ (1985) Characterization of the binding properties and retrograde axonal transport of a monoclonal antibody directed against the rat nerve growth factor receptor. J Cell Biol 101:1100-1106.
69. Tischler AS, Greene LA (1975) Nerve growth factor-induced process formation by cultured rat pheochromocytoma cells. Nature 258:341-342.
70. Vale RD, Shooter EM (1985) Assaying binding of nerve growth factor to cell surface receptors. Methods Enzymol 109:21-39.
71. Vale RD, Ignatius MJ, Shooter EM (1985) Association of nerve growth factor receptors with the Triton X-100 cytoskeleton of PC12 cells. J Neurosci 5:2762-2770.
72. van der Geer P, Hunter T, Lindberg RA (1994) Receptor protein-tyrosine kinases and their signal transduction pathways. Annu Rev Cell Biol 10:251-337.
73. LNGFR regulates trk signal transduction and NGF-induced neuronal differentiation in MAH cells. Neuron 12:733-745.
74. Yuen EC, Mobley WC (1995) Therapeutic applications of neurotrophic factors in disorders of motor neurons and peripheral nerves. Mol Med Today 1:278-286.
75. Zhou J, Valletta JS, Grimes ML, Mobley WC (1995) Multiple levels for regulation of TrkA in PC12 cells by nerve growth factor. J Neurochem 65:1146-1156.