Ligand-induced internalization of the p75 neurotrophin receptor: A slow route to the signaling endosome

Journal of Neuroscience

Volumn 23, Issue 8, 2003, Pages 3209-3220

  Bronfman, Francisca C ^a   Tcherpakov, Marianna ^a   Jovin, Thomas M ^b   Fainzilber, Mike ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

Internalization; Neurotrophin; p75 receptor; Recycling endosome; Retrograde transport; Signaling endosome

Indexed keywords

CLATHRIN; NERVE GROWTH FACTOR; NEUROTROPHIN RECEPTOR; PROTEIN TYROSINE KINASE; TRANSFERRIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING KINETICS; BIOTINYLATION; CELL DIFFERENTIATION; CELL FRACTIONATION; COMPLEX FORMATION; CONTROLLED STUDY; ENDOSOME; INTERNALIZATION; MOLECULAR MECHANICS; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSPORT KINETICS; WESTERN BLOTTING;

ANIMALS; ANTIBODIES; AXONAL TRANSPORT; BINDING, COMPETITIVE; BIOTIN; BIOTINYLATION; CARRIER PROTEINS; COATED PITS, CELL-MEMBRANE; DNA-BINDING PROTEINS; ENDOSOMES; FLUORESCENT DYES; IODINE; LIGANDS; MACROMOLECULAR SUBSTANCES; MEMBRANE PROTEINS; NEOPLASM PROTEINS; NERVE GROWTH FACTOR; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PC12 CELLS; PROTEIN BINDING; PROTEIN TRANSPORT; RATS; RECEPTOR, NERVE GROWTH FACTOR; RECEPTOR, TRKA; RECEPTORS, NERVE GROWTH FACTOR; SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS; TRANSFERRIN;

EID: 0037547112     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (78)

1. Barker PA (1998) p75NTR: a study in contrasts. Cell Death Differ 5:346-356.
2. Berger-Sweeney J, Stearns NA, Murg SL, Floerke-Nashner LR, Lappi DA, Baxter MG (2001) Selective immunolesions of cholinergic neurons in mice: effects on neuroanatomy, neurochemistry, and behavior. J Neurosci 21:8164-8173.
3. Bhattacharyya A, Watson FL, Bradlee TA, Pomeroy SL, Stiles CD, Segal RA (1997) Trk receptors function as rapid retrograde signal carriers in the adult nervous system. J Neurosci 17:7007-7016.
4. Blagoveshchenskaya AD, Cutler DF (2000) Sorting to synaptic-like microvesicles from early and late endosomes requires overlapping but not identical targeting signals. Mol Biol Cell 11:1801-1814.
5. Blagoveshchenskaya AD, Hewitt EW, Cutler DF (1999) A complex web of signal-dependent trafficking underlies the triorganellar distribution of P-selectin in neuroendocrine PC12 cells. J Cell Biol 145:1419-1433.
6. Brann AB, Scott R, Neuberger Y, Abulafia D, Boldin S, Fainzilber M, Futerman AH (1999) Ceramide signaling downstream of the p75 neurotrophin receptor mediates the effects of nerve growth factor on outgrowth of cultured hippocampal neurons. J Neurosci 19:8199-8206.
7. Bronfman FC, Moechars D, Van Leuven F (2000) Acetylcholinesterase-positive fiber deafferentation and cell shrinkage in the septohippocampal pathway of aged amyloid precursor protein london mutant transgenic mice. Neurobiol Dis 7:152-168.
8. Butowt R, von Bartheld CS (2001) Sorting of internalized neurotrophins into an endocytic transcytosis pathway via the Golgi system: ultrastructural analysis in retinal ganglion cells. J Neurosci 21:8915-8930.
9. Chandler CE, Parsons LM, Hosang M, Shooter EM (1984) A monoclonal antibody modulates the interaction of nerve growth factor with PC12 cells. J Biol Chem 259:6882-6889.
10. Chatterjee S, Smith ER, Hanada K, Stevens VL, Mayor S (2001) GPI anchoring leads to sphingolipid-dependent retention of endocytosed proteins in the recycling endosomal compartment. EMBO J 20:1583-1592.
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. Curtis R, Adryan KM, Stark JL, Park JS, Compton DL, Weskamp G, Huber LJ, Chao MV, Jaenisch R, Lee KF (1995) Differential role of the low affinity neurotrophin receptor (p75) in retrograde axonal transport of the neurotrophins. Neuron 14:1201-1211.
13. Della-Bianca V, Rossi F, Armato U, Dal-Pra I, Costantini C, Perini G, Politi V, DellaValle G (2001) Neurotrophin p75 receptor is involved in neuronal damage by prion peptide 106-126. J Biol Chem 276:38929-38933.
14. DiFiore PP, De Camilli P (2001) Endocytosis and signaling. An inseparable partnership. Cell 106:1-4.
15. Esposito D, Patel P, Stephens RM, Perez P, Chao MV, Kaplan DR, Hempstead BL (2001) The cytoplasmic and transmembrane domains of the p75 and Trk A receptors regulate high affinity binding to nerve growth factor. J Biol Chem 276:32687-32695.
16. Eveleth DD, Bradshaw RA (1992) Nerve growth factor nonresponsive pheochromocytoma cells: altered internalization results in signaling dysfunction. J Cell Biol 117:291-299.
17. Fainzilber M, Smit AB, Syed NI, Wildering WC, Hermann P, Van der Schors RC, Jimenez C, Li KW, Van Minnen J, Bulloch AG, Ibanez CF, Geraerts WP (1996) CRNF, a molluscan neurotrophic factor that interacts with the p75 neurotrophin receptor. Science 274:1540-1543.
18. Futter CE, Pearse A, Hewlett LJ, Hopkins CR (1996) Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J Cell Biol 132:1011-1023.
19. Gargano N, Levi A, Alema S (1997) Modulation of nerve growth factor internalization by direct interaction between p75 and TrkA receptors. J Neurosci Res 50:1-12.
20. Gatzinsky KP, Haugland RP, Thrasivoulou C, Orike N, Budi-Santoso AW, CowenT (2001) p75 and TrkA receptors are both required for uptake of NGF in adult sympathetic neurons: use of a novel fluorescent NGF conjugate. Brain Res 920:226-238.
21. Ginty DD, Segal RA (2002) Retrograde neurotrophin signaling: Trk-ing along the axon. Curr Opin Neurobiol 12:268-274.
22. Grimes ML, Beattie E, Mobley WC (1997) A signaling organelle containing the nerve growth factor-activated receptor tyrosine kinase, TrkA. Proc Natl Acad Sci USA 94:9909-9914.
23. Gruenberg J, Maxfield FR (1995) Membrane transport in the endocytic pathway. Curr Opin Cell Biol 7:552-563.
24. Heckers S, Ohtake T, Wiley RG, Lappi DA, Geula C, Mesulam MM (1994) Complete and selective cholinergic denervation of rat neocortex and hippocampus but not amygdala by an immunotoxin against the p75 NGF receptor. J Neurosci 14:1271-1289.
25. Heerssen HM, Segal RA (2002) Location, location, location: a spatial view of neurotrophin signal transduction. Trends Neurosci 25:160-165.
26. Hempstead BL (2002) The many faces of p75(NTR). Curr Opin Neurobiol 12:260-267.
27. Herreros J, Ng T, Schiavo G (2001) Lipid rafts act as specialized domains for tetanus toxin binding and internalization into neurons. Mol Biol Cell 12:2947-2960.
28. Howe CL, Valletta JS, Rusnak AS, Mobley WC (2001) NGF signaling from clathrin-coated vesicles: evidence that signaling endosomes serve as a platform for the Ras-MAPK pathway. Neuron 32:801-814.
29. Huang CS, Zhou J, Feng AK, Lynch CC, Klumperman J, DeArmond SJ, Mobley WC (1999) Nerve growth factor signaling in caveolae-like domains at the plasma membrane. J Biol Chem 274:36707-36714.
30. Hutson LD, Bothwell M (2001) Expression and function of Xenopus laevis p75(NTR) suggest evolution of developmental regulatory mechanisms. J Neurobiol 49:79-98.
31. Ibanez CF (1995) Neurotrophic factors: from structure-function studies to designing effective therapeutics. Trends Biotechnol 13:217-227.
32. Innamorati G, Sadeghi HM, Tran NT, Birnbaumer M (1998) A serine cluster prevents recycling of the V2 vasopressin receptor. Proc Natl Acad Sci USA 95:2222-2226.
33. Innamorati G, Le Gouill C, Balamotis M, Birnbaumer M (2001) The long and the short cycle. Alternative intracellular routes for trafficking of G-protein-coupled receptors. J Biol Chem 276:13096-13103.
34. Kahle P, Hertel C (1992) Nerve growth factor (NGF) receptor on rat glial cell lines. Evidence for NGF internalization via p75NGFR. J Biol Chem 267:13917-13923.
35. Kahle P, Barker PA, Shooter EM, Hertel C (1994) p75 nerve growth factor receptor modulates p140trkA kinase activity, but not ligand internalization, in PC12 cells. J Neurosci Res 38:599-606.
36. Kao S, Jaiswal RK, Kolch W, Landreth GE (2001) Identification of the mechanisms regulating the differential activation of the mapk cascade by epidermal growth factor and nerve growth factor in PC12 cells. J Biol Chem 276:18169-18177.
37. Kaplan DR, Miller FD (2000) Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol 10:381-391.
38. Kasaian MT, Jacobberger JW, Neet KE (1994) Flow cytometric analysis of fluorescein-labeled nerve growth-factor binding to A875 human-melanoma cells. Exp Cell Res 210:77-85.
39. Khursigara G, Orlinick JR, Chao MV (1999) Association of the p75 neurotrophin receptor with TRAF6. J Biol Chem 274:2597-2600.
40. Kramer BM, Van der Zee CE, Hagg T (1999) P75 nerve growth factor receptor is important for retrograde transport of neurotrophins in adult cholinergic basal forebrain neurons. Neuroscience 94:1163-1172.
41. Kuruvilla R, Ye H, Ginty DD (2000) Spatially and functionally distinct roles of the PI3-K effector pathway during NGF signaling in sympathetic neurons. Neuron 27:499-512.
42. Lalli G, Schiavo G (2002) Analysis of retrograde transport in motor neurons reveals common endocytic carriers for tetanus toxin and neurotrophin receptor p75NTR. J Cell Biol 156:233-239.
43. Larkin JM, Brown MS, Goldstein JL, Anderson RG (1983) Depletion of intracellular potassium arrests coated pit formation and receptor-mediated endocytosis in fibroblasts. Cell 33:273-285.
44. Lee R, Kermani P, Teng KK, Hempstead BL (2001) Regulation of cell survival by secreted proneurotrophins. Science 294:1945-1948.
45. Lichtenstein Y, Desnos C, Faundez V, Kelly RB, Clift-O'Grady L (1998) Vesiculation and sorting from PC12-derived endosomes in vitro. Proc Natl Acad Sci USA 95:11223-11228.
46. Lonze BE, Riccio A, Cohen S, Ginty DD (2002) Apoptosis, axonal growth defects, and degeneration of peripheral neurons in mice lacking CREB. Neuron 34:371-385.
47. MacInnis BL, Campenot RB (2002) Retrograde support of neuronal survival without retrograde transport of nerve growth factor. Science 295:1536-1539.
48. Maliartchouk S, Saragovi HU (1997) Optimal nerve growth factor trophic signals mediated by synergy of TrkA and p75 receptor-specific ligands. J Neurosci 17:6031-6037.
49. Marquez-Sterling NR, Lo AC, Sisodia SS, Koo EH (1997) Trafficking of cell-surface beta-amyloid precursor protein: evidence that a sorting intermediate participates in synaptic vesicle recycling. J Neurosci 17:140-151.
50. Mellman I (1996) Membranes and sorting. Curr Opin Cell Biol 8:497-498.
51. Miller FD, Kaplan DR (2001) On Trk for retrograde signaling. Neuron 32:767-770.
52. Mills IG, Jones AT, Clague MJ (1998) Involvement of the endosomal autoantigen EEA1 in homotypic fusion of early endosomes. Curr Biol 8:881-884.
53. Mukherjee S, Ghosh RN, Maxfield FR (1997) Endocytosis. Physiol Rev 77:759-803.
54. Neet KE, Campenot RB (2001) Receptor binding, internalization, and retrograde transport of neurotrophic factors. Cell Mol Life Sci 58:1021-1035.
55. Nichols BI, Lippincott-Schwartz J (2001) Endocytosis without clathrin coats. Trends Cell Biol 11:406-412.
56. Patapoutian A, Reichardt LF (2001) Trk receptors: mediators of neurotrophin action. Curr Opin Neurobiol 11:272-280.
57. Riccio A, Pierchala BA, Ciarallo CL, Ginty DD (1997) An NGF-TrkA-mediated retrograde signal to transcription factor CREB in sympathetic neurons. Science 277:1097-1100.
58. Riccio A, Ahn S, Davenport CM, Blendy JA, Ginty DD (1999) Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons. Science 286:2358-2361.
59. Ryden M, Hempstead B, Ibanez CF (1997) Differential modulation of neuron survival during development by nerve growth factor binding to the p75 neurotrophin receptor. J Biol Chem 272:16322-16328.
60. Salem AH, Roux PP, Kubu CJ, Zeindler C, Bhakar A, Tannis LL, Verdi JM, Barker PA (2000) NRAGE, a novel MAGE protein, interacts with the p75 neurotrophin receptor and facilitates nerve growth factor-dependent apoptosis. Neuron 27:279-288.
61. Salehi AH, Xanthoudakis S, Barker PA (2002) NRAGE, a p75 neurotrophin receptor interacting protein, induces caspase activation and cell death through a JNK-dependent mitochondrial pathway. J Biol Chem 277:48043-48050.
62. Sandvig K, Olsnes S, Petersen OW, van Deurs B (1987) Acidification of the cytosol inhibits endocytosis from coated pits. J Cell Biol 105:679-689.
63. Senger DL, Campenot RB (1997) Rapid retrograde tyrosine phosphorylation of trkA and other proteins in rat sympathetic neurons in compartmented cultures. J Cell Biol 138:411-421.
64. Shogomori H, Futerman AH (2001) Cholera toxin is found in detergent-insoluble rafts/domains at the cell surface of hippocampal neurons but is internalized via a raft-independent mechanism. J Biol Chem 276:9182-9188.
65. Subtil A, Hemar A, Dautry-Varsat A (1994) Rapid endocytosis of interleukin 2 receptors when clathrin-coated pit endocytosis is inhibited. J Cell Sci 107:3461-3468.
66. Tcherpakov M, Bronfman FC, Conticello SG, Vaskovsky A, Levy Z, Niinobe M, Yoshikawa K, Arenas E, Fainzilber M (2002) The p75 neurotrophin receptor interacts with multiple MAGE proteins. J Biol Chem 277:49101-49104.
67. Tran D, Carpentier IL, Sawano F, Gorden P, Orci L (1987) Ligands internalized through coated or noncoated invaginations follow a common intracellular pathway. Proc Natl Acad Sci USA 84:7957-7961.
68. Tsui-Pierchala BA, Ginty DD (1999) Characterization of an NGF-P-TrkA retrograde-signaling complex and age-dependent regulation of TrkA phosphorylation in sympathetic neurons. J Neurosci 19:8207-8218.
69. Tuffereau C, Benejean J, Blondel D, Kieffer B, Flamand A (1998) Low-affinity nerve-growth factor receptor (P75NTR) can serve as a receptor for rabies virus. EMBO J 17:7250-7259.
70. Urdiales JL, Becker E, Andrieu M, Thomas A, Jullien J, van Grunsven LA, Menut S, Evan GI, Martin-Zanca D, Rudkin BB (1998) Cell cycle phase-specific surface expression of nerve growth factor receptors TrkA and p75(NTR). J Neurosci 18:6767-6775.
71. von Bartheld CS, Williams R, Lefcort F, Clary DO, Reichardt LF, Bothwell M (1996) Retrograde transport of neurotrophins from the eye to the brain in chick embryos: roles of the p75NTR and trkB receptors. J Neurosci 16:2995-3008.
72. von Schack D, Casademunt E, Schweigreiter R, Meyer M, Bibel M, Dechant G (2001) Complete ablation of the neurotrophin receptor p75NTR causes defects both in the nervous and the vascular system. Nat Neurosci 4:977-978.
73. Waterman H, Katz M, Rubin C, Shtiegman K, Lavi S, Elson A, Jovin T, Yarden Y (2002) A mutant EGF-receptor defective in ubiquitylation and endocytosis unveils a role for Grb2 in negative signaling. EMBO J 21:303-313.
74. Watson FL, Heerssen HM, Moheban DB, Lin MZ, Sauvageot CM, Bhattacharyya A, Pomeroy SL, Segal RA (1999) Rapid nuclear responses to target-derived neurotrophins require retrograde transport of ligand-receptor complex. J Neurosci 19:7889-7900.
75. Watson FL, Heerssen HM, Bhattacharyya A, Klesse L, Lin MZ, Segal RA (2001) Neurotrophins use the Erk5 pathway to mediate a retrograde survival response. Nat Neurosci 4:981-988.
76. Weible Jr MW, Bartlett SE, Reynolds AJ, Hendry IA (2001) Prolonged recycling of internalized neurotrophins in the nerve terminal. Cytometry 43:182-188.
77. Yano H, Lee FS, Kong H, Chuang J, Arevalo J, Perez P, Sung C, Chao MV (2001) Association of Trk neurotrophin receptors with components of the cytoplasmic dynein motor. J Neurosci 21:RC125(1-7).
78. Zapf-Colby A, Olefsky JM (1998) Nerve growth factor processing and trafficking events following TrkA-mediated endocytosis. Endocrinology 139:3232-3240.