An intracellular domain fragment of the p75 neurotrophin receptor (p75 NTR) enhances tropomyosin receptor kinase A(TrkA) receptor function

Journal of Biological Chemistry

Volumn 288, Issue 16, 2013, Pages 11144-11154

  Matusica, Dusan ^a   Skeldal, Sune ^a   Sykes, Alex M ^a   Palstra, Nickless ^a   Sharma, Aanchal ^a   Coulson, Elizabeth J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONAL CHANGE; EXTRACELLULAR DOMAINS; INTRACELLULAR DOMAIN; NEURITE OUTGROWTH; NEUROTROPHIC ACTIVITIES; NEUROTROPHINS; P75 NEUROTROPHIN RECEPTOR; RECEPTOR KINASE;

BIOCHEMISTRY; BIOLOGY;

ENZYME ACTIVITY;

MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NERVE GROWTH FACTOR; NEUROTROPHIN RECEPTOR P75; PROTEIN KINASE B; PROTEIN TYROSINE KINASE A;

AMINO ACID SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; EXTRACELLULAR SPACE; HUMAN; HUMAN CELL; INTRACELLULAR SPACE; NERVE FIBER GROWTH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SYMPATHETIC NERVE CELL;

ANIMALS; HEK293 CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURONS; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; RECEPTOR, TRKA; RECEPTORS, NERVE GROWTH FACTOR;

EID: 84876553840     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.436469     Document Type: Article

References (58)

1. Reichardt, L. F. (2006) Neurotrophin-regulated signalling pathways. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 361, 1545-1564.
2. Kaplan, D. R., and Stephens, R. M. (1994) Neurotrophin signal transduction by the Trk receptor. J. Neurobiol. 25, 1404-1417.
3. Kaplan, D. R., Hempstead, B. L., Martin-Zanca, D., Chao, M. V., and Parada, L. F. (1991) The trk proto-oncogene product: a signal transducing receptor for nerve growth factor. Science 252, 554-558.
4. Friedman, W. J., and Greene, L. A. (1999) Neurotrophin signaling via Trks and p75. Exp. Cell Res. 253, 131-142.
5. Block, T., and Bothwell, M. (1983) The nerve growth factor receptor on PC12 cells: interconversion between two forms with different binding properties. J. Neurochem. 40, 1654-1663.
6. Hempstead, B. L., Martin-Zanca, D., Kaplan, D. R., Parada, L. F., and Chao, M. V. (1991) High-affinity NGF binding requires coexpression of the trk proto-oncogene and the low-affinity NGF receptor. Nature 350, 678-683.
7. Davies, A. M., Lee, K. F., and Jaenisch, R. (1993) p75-deficient trigeminal sensory neurons have an altered response to NGF but not to other neurotrophins. Neuron 11, 565-574.
8. NTR.EMBOJ. 18, 616-622.
9. Chao, M. V., and Hempstead, B. L. (1995) p75 and Trk: a two-receptor system. Trends Neurosci. 18, 321-326.
10. Lee, K. F., Li, E., Huber, L. J., Landis, S. C., Sharpe, A. H., Chao, M. V., and Jaenisch, R. (1992) Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69, 737-749.
11. Lee, K. F., Davies, A. M., and Jaenisch, R. (1994) p75-deficient embryonic dorsal root sensory and neonatal sympathetic neurons display a decreased sensitivity to NGF. Development 120, 1027-1033.
12. Barker, P. A. (2007) High Affinity Not in the Vicinity? Neuron 53, 1-4.
13. Mahadeo, D., Kaplan, L., Chao, M. V., and Hempstead, B. L. (1994) 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, 6884-6891.
14. Barker, P. A., and Shooter, E. M. (1994) Disruption of NGF binding to the low affinity neurotrophin receptor p75LNTR reduces NGF binding to TrkA on PC12 cells. Neuron 13, 203-215.
15. NTR. J. Biol. Chem. 280, 33453-33460.
16. Wehrman, T., He, X., Raab, B., Dukipatti, A., Blau, H., and Garcia, K. C. (2007) Structural and mechanistic insights into nerve growth factor interactions with the TrkA and p75 receptors. Neuron 53, 25-38.
17. NTR symmetrical complex. Nature 454, 789-793.
18. Rydén, M., Hempstead, B., and Ibáñez, C. F. (1997) Differential modulation of neuron survival during development by nerve growth factor binding to the p75 neurotrophin receptor. J. Biol. Chem. 272, 16322-16328.
19. Hempstead, B. L., Patil, N., Thiel, B., and Chao, M. V. (1990) Deletion of cytoplasmic sequences of the nerve growth factor receptor leads to loss of high affinity ligand binding. J. Biol. Chem. 265, 9595-9598.
20. Esposito, D., Patel, P., Stephens, R. M., Perez, P., Chao, M. V., Kaplan, D. R., and Hempstead, B. L. (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.
21. Jung, K. M., Tan, S., Landman, N., Petrova, K., Murray, S., Lewis, R., Kim, P. K., Kim, D. S., Ryu, S. H., Chao, M. V., and Kim, T. W. (2003) Regulated intramembrane proteolysis of the p75 neurotrophin receptor modulates its association with the TrkA receptor. J. Biol. Chem. 278, 42161-42169.
22. Kanning, K. C., Hudson, M., Amieux, P. S., Wiley, J. C., Bothwell, M., and Schecterson, L. C. (2003) Proteolytic processing of the p75 neurotrophin receptor and two homologs generates C-terminal fragments with signaling capability. J. Neurosci. 23, 5425-5436.
23. NTR. Bioessays 33, 614-625.
24. Urra, S., Escudero, C. A., Ramos, P., Lisbona, F., Allende, E., Covarrubias, P., Parraguez, J. I., Zampieri, N., Chao, M. V., Annaert, W., and Bronfman, F. C. (2007) TrkA receptor activation by nerve growth factor induces shedding of the p75 neurotrophin receptor followed by endosomal γ-secretase-mediated release of the p75 intracellular domain. J. Biol. Chem. 282, 7606-7615.
25. NTR intracellular domain generated by neurotrophin-induced receptor cleavage potentiates Trk signaling. J. Cell Sci. 123, 2299-2307.
26. Kommaddi, R. P., Thomas, R., Ceni, C., Daigneault, K., and Barker, P. A. (2011) Trk-dependent ADAM17 activation facilitates neurotrophin survival signaling. FASEB J. 25, 2061-2070.
27. Sykes, A. M., Palstra, N., Abankwa, D., Hill, J. M., Skeldal, S., Matusica, D., Venkatraman, P., Hancock, J. F., and Coulson, E. J. (2012) The effects of transmembrane sequence and dimerization on cleavage of the p75 neurotrophin receptor by γ-secretase. J. Biol. Chem. 287, 43810-43824.
28. Coulson, E. J., Reid, K., Barrett, G. L., and Bartlett, P. F. (1999) p75 neurotrophin receptor-mediated neuronal death is promoted by Bcl-2 and prevented by Bcl-xL. J. Biol. Chem. 274, 16387-16391.
29. Coulson, E. J., Reid, K., Baca, M., Shipham, K. A., Hulett, S. M., Kilpatrick, T. J., and Bartlett, P. F. (2000) Chopper, a new death domain of the p75 neurotrophin receptor that mediates rapid neuronal cell death. J. Biol. Chem. 275, 30537-30545.
30. Coulson, E. J., Reid, K., Shipham, K. M., Morley, S., Kilpatrick, T. J., and Bartlett, P. F. (2004) The role of neurotransmission and the Chopper domain in p75 neurotrophin receptor death signaling. Prog. Brain Res. 146, 41-62.
31. NTR regulates death signaling and is required for subsequent cleavage by γ-secretase. Mol. Cell Neurosci. 37, 346-358.
32. Arevalo, J. C., Conde, B., Hempstead, B. I., Chao, M. V., Martín-Zanca, D., and Pérez, P. (2001) A novel mutation within the extracellular domain of TrkA causes constitutive receptor activation. Oncogene 20, 1229-1234.
33. Ho, A., Schwarze, S. R., Mermelstein, S. J., Waksman, G., and Dowdy, S. F. (2001) Synthetic protein transduction domains: enhanced transduction potential in vitro and in vivo. Cancer Res. 61, 474-477.
34. Bodmer, D., Levine-Wilkinson, S., Richmond, A., Hirsh, S., and Kuruvilla, R. (2009) Wnt5a mediates nerve growth factor-dependent axonal branching and growth in developing sympathetic neurons. J. Neurosci. 29, 7569-7581.
35. Zareen, N., and Greene, L. A. (2009) Protocol for culturing sympathetic neurons from rat superior cervical ganglia (SCG). J. Vis. Exp. 32, e988.
36. Greene, L. A., and Tischler, A. S. (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. U.S.A. 73, 2424-2428.
37. Shaw, G., Morse, S., Ararat, M., and Graham, F. L. (2002) Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK 293 cells. FASEB J. 16, 869-871.
38. Weible, M. W., 2nd, Bartlett, S. E., Reynolds, A. J., and Hendry, I. A. (2001) Prolonged recycling of internalized neurotrophins in the nerve terminal. Cytometry 43, 182-188.
39. Weible, M. W., 2nd, Ozsarac, N., Grimes, M. L., and Hendry, I. A. (2004) Comparison of nerve terminal events in vivo effecting retrograde transport of vesicles containing neurotrophins or synaptic vesicle components. J. Neurosci. Res. 75, 771-781.
40. Kaplan, D. R., and Miller, F. D. (2000) Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 10, 381-391.
41. Traverse, S., Gomez, N., Paterson, H., Marshall, C., and Cohen, P. (1992) Sustained activation of the mitogen-activated protein (MAP) kinase cascade may be required for differentiation of PC12 cells. Comparison of the effects of nerve growth factor and epidermal growth factor. Biochem. J. 288, 351-355.
42. Vaudry, D., Stork, P. J., Lazarovici, P., and Eiden, L. E. (2002) Signaling pathways for PC12 cell differentiation: making the right connections. Science 296, 1648-1649.
43. Fukuda, M., Gotoh, Y., Tachibana, T., Dell, K., Hattori, S., Yoneda, Y., and Nishida, E. (1995) Induction of neurite outgrowth by MAP kinase in PC12 cells. Oncogene 11, 239-244.
44. Kim, Y., Seger, R., Suresh Babu, C. V., Hwang, S. Y., and Yoo, Y. S. (2004) A positive role of the PI3-K/Akt signaling pathway in PC12 cell differentiation. Mol. Cells 18, 353-359.
45. NTR is positively promiscuous: novel partners and new insights. Neuron 42, 529-533.
46. Barrett, G. L., and Georgiou, A. (1996) The low-affinity nerve growth factor receptor p75NGFR mediates death of PC12 cells after nerve growth factor withdrawal. J. Neurosci. Res. 45, 117-128.
47. Huber, L. J., and Chao, M. V. (1995) A potential interaction of p75 and trkA NGF receptors revealed by affinity crosslinking and immunoprecipitation. J. Neurosci. Res. 40, 557-563.
48. Wolf, D. E., McKinnon, C. A., Daou, M. C., Stephens, R. M., Kaplan, D. R., and Ross, A. H. (1995) Interaction with TrkA immobilizes gp75 in the high affinity nerve growth factor receptor complex. J. Biol. Chem. 270, 2133-2138.
49. Fay, S. P., Posner, R. G., Swann, W. N., and Sklar, L. A. (1991) Real-time analysis of the assembly of ligand, receptor, and G protein by quantitative fluorescence flow cytometry. Biochemistry 30, 5066-5075.
50. Sklar, L. A., Edwards, B. S., Graves, S. W., Nolan, J. P., and Prossnitz, E. R. (2002) Flow cytometric analysis of ligand-receptor interactions and molecular assemblies. Annu. Rev. Biophys. Biomol. Struct. 31, 97-119.
51. Zaccaro, M. C., Ivanisevic, L., Perez, P., Meakin, S. O., and Saragovi, H. U. (2001) p75 Co-receptors regulate ligand-dependent and ligand-independent Trk receptor activation, in part by altering Trk docking subdomains. J. Biol. Chem. 276, 31023-31029.
52. Roux, P. P., and Barker, P. A. (2002) Neurotrophin signaling through the p75 neurotrophin receptor. Prog. Neurobiol. 67, 203-233.
53. Kenchappa, R. S., Zampieri, N., Chao, M. V., Barker, P. A., Teng, H. K., Hempstead, B. L., and Carter, B. D. (2006) Ligand-dependent cleavage of the p75 neurotrophin receptor is necessary for NRIF nuclear translocation and apoptosis in sympathetic neurons. Neuron 50, 219-232.
54. Sotthibundhu, A., Sykes, A. M., Fox, B., Underwood, C. K., Thangnipon, W., and Coulson, E. J. (2008) β-amyloid1-42 induces neuronal death through the p75 neurotrophin receptor. J. Neurosci. 28, 3941-3946.
55. Coulson, E. J., May, L. M., Osborne, S. L., Reid, K., Underwood, C. K., Meunier, F. A., Bartlett, P. F., and Sah, P. (2008) p75 neurotrophin receptor mediates neuronal cell death by activating GIRK channels through phosphatidylinositol 4, 5-bisphosphate. J. Neurosci. 28, 315-324.
56. Ibáñez, C. F. (1994) Structure-function relationships in the neurotrophin family. J. Neurobiol. 25, 1349-1361.
57. Margadant, C., Monsuur, H. N., Norman, J. C., and Sonnenberg, A. (2011) Mechanisms of integrin activation and trafficking. Curr. Opin. Cell Biol. 23, 607-614.
58. Liepinsh, E., Ilag, L. L., Otting, G., and Ibáñez, C. F. (1997) NMR structure of the death domain of the p75 neurotrophin receptor. EMBO J. 16, 4999-5005.