Neuron-type-specific signaling by the p75NTR death receptor is regulated by differential proteolytic cleavage

Journal of Cell Science

Volumn 128, Issue 8, 2015, Pages 1507-1517

  Vicario, Annalisa ^a,c   Kisiswa, Lilian ^a   Tann, Jason Y ^b   Kelly, Claire E ^a   Ibáñez, Carlos F ^a,b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c UNIVERSITY OF TRIESTE   (Italy)

Author keywords

Cell death; Nerve growth factor; NF B; Presenilin 1; secretase

Indexed keywords

ACTIN; CASPASE 3; GAMMA SECRETASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; JANUS KINASE; NEUROTROPHIN RECEPTOR P75; TRANSCRIPTION FACTOR RELA; CASP3 PROTEIN, MOUSE; NERVE GROWTH FACTOR RECEPTOR; SECRETASE; TNFRSF16 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DEATH; CEREBELLUM GRANULAR LAYER; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HIPPOCAMPAL NEURONAL CULTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; TUNEL ASSAY; UPREGULATION; ANIMAL; CEREBELLUM; CYTOKINESIS; CYTOLOGY; HIPPOCAMPUS; KNOCKOUT MOUSE; METABOLISM; NERVE CELL;

AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CASPASE 3; CELL DEATH; CEREBELLUM; CYTOKINESIS; HIPPOCAMPUS; MICE; MICE, KNOCKOUT; NEURONS; PROTEOLYSIS; RECEPTORS, NERVE GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 84928555294     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.161745     Document Type: Article

References (54)

1. Beg, A. A. and Baltimore, D. (1996). An essential role for NF-κB in preventing TNF-alpha-induced cell death. Science 274, 782-784.
2. Busuttil, V., Bottero, V., Frelin, C., Imbert, V., Ricci, J.-E., Auberger, P. and Peyron, J.-F. (2002). Blocking NF-κB activation in Jurkat leukemic T cells converts the survival agent and tumor promoter PMA into an apoptotic effector. Oncogene 21, 3213-3224.
3. Carter, B. D., Kaltschmidt, C., Kaltschmidt, B., Offenhäuser, N., Böhm-Matthaei, R., Baeuerle, P. A. and Barde, Y.-A. (1996). Selective activation of NF-k B by nerve growth factor through the neurotrophin receptor p75. Science 272, 542-545.
4. Casademunt, E., Carter, B. D., Benzel, I., Frade, J. M., Dechant, G. and Barde, Y. A. (1999). The zinc finger protein NRIF interacts with the neurotrophin receptor p75(NTR) and participates in programmed cell death. EMBO J. 18, 6050-6061.
5. Ceni, C., Kommaddi, R. P., Thomas, R., Vereker, E., Liu, X., McPherson, P. S., Ritter, B. and Barker, P. A. (2010). The p75NTR intracellular domain generated by neurotrophin-induced receptor cleavage potentiates Trk signaling. J. Cell Sci. 123, 2299-2307.
6. Charalampopoulos, I., Vicario, A., Pediaditakis, I., Gravanis, A., Simi, A. and Ibáñez, C. F. (2012). Genetic dissection of neurotrophin signaling through the p75 neurotrophin receptor. Cell Reports 2, 1563-1570.
7. Chittka, A. and Chao, M. V. (1999). Identification of a zinc finger protein whose subcellular distribution is regulated by serum and nerve growth factor. Proc. Natl. Acad. Sci. USA 96, 10705-10710.
8. 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.
9. Dechant, G. and Barde, Y. A. (2002). The neurotrophin receptor p75(NTR): novel functions and implications for diseases of the nervous system. Nat. Neurosci. 5, 1131-1136.
10. Domeniconi, M., Zampieri, N., Spencer, T., Hilaire, M., Mellado, W., Chao, M. V. and Filbin, M. T. (2005). MAG induces regulated intramembrane proteolysis of the p75 neurotrophin receptor to inhibit neurite outgrowth. Neuron 46, 849-855.
11. Friedman, W. J. (2000). Neurotrophins induce death of hippocampal neurons via the p75 receptor. J. Neurosci. 20, 6340-6346.
12. Guo, T., Marmol, P., Moliner, A., Björnholm, M., Zhang, C., Shokat, K. M. and Ibanez, C. F. (2014). Adipocyte ALK7 links nutrient overload to catecholamine resistance in obesity. eLife 3, e03245.
13. 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. et al. (2003). Regulated intramembrane proteolysis of the p75 neurotrophin receptor modulates its association with the TrkA receptor. J. Biol. Chem. 278, 42161-42169.
14. 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.
15. Karin, M. and Lin, A. (2002). NF-κB at the crossroads of life and death. Nat. Immunol. 3, 221-227.
16. 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.
17. Kenchappa, R. S., Tep, C., Korade, Z., Urra, S., Bronfman, F. C., Yoon, S. O. and Carter, B. D. (2010). p75 neurotrophin receptor-mediated apoptosis in sympathetic neurons involves a biphasic activation of JNK and up-regulation of tumor necrosis factor-alpha-converting enzyme/ADAM17. J. Biol. Chem. 285, 20358-20368.
18. Khursigara, G., Bertin, J., Yano, H., Moffett, H., DiStefano, P. S. and Chao, M. V. (2001). A prosurvival function for the p75 receptor death domain mediated via the caspase recruitment domain receptor-interacting protein 2. J. Neurosci. 21, 5854-5863.
19. Knowles, J. K., Rajadas, J., Nguyen, T.-V. V., Yang, T., LeMieux, M. C., Vander Griend, L., Ishikawa, C., Massa, S. M., Wyss-Coray, T. and Longo, F. M. (2009). The p75 neurotrophin receptor promotes amyloid-beta(1-42)-induced neuritic dystrophy in vitro and in vivo. J. Neurosci. 29, 10627-10637.
20. Kraemer, B. R., Snow, J. P., Vollbrecht, P., Pathak, A., Valentine, W. M., Deutch, A. Y. and Carter, B. D. (2014). A role for the p75 neurotrophin receptor in axonal degeneration and apoptosis induced by oxidative stress. J. Biol. Chem. 289, 21205-21216.
21. Kucharczak, J., Simmons, M. J., Fan, Y. and Gélinas, C. (2003). To be, or not to be: NF-κB is the answer - role of Rel/NF-κB in the regulation of apoptosis. Oncogene 22, 8961-8982.
22. Le Moan, N., Houslay, D. M., Christian, F., Houslay, M. D. and Akassoglou, K. (2011). Oxygen-dependent cleavage of the p75 neurotrophin receptor triggers stabilization of HIF-1a. Mol. Cell 44, 476-490.
23. Lee, R., Kermani, P., Teng, K. K. and Hempstead, B. L. (2001). Regulation of cell survival by secreted proneurotrophins. Science 294, 1945-1948.
24. Lu, B., Pang, P. T. and Woo, N. H. (2005). The yin and yang of neurotrophin action. Nat. Rev. Neurosci. 6, 603-614.
25. Mattson, M. P., Goodman, Y., Luo, H., Fu, W. and Furukawa, K. (1997). Activation of NF-κB protects hippocampal neurons against oxidative stressinduced apoptosis: evidence for induction of manganese superoxide dismutase and suppression of peroxynitrite production and protein tyrosine nitration. J. Neurosci. Res. 49, 681-697.
26. Mi, S., Lee, X., Shao, Z., Thill, G., Ji, B., Relton, J., Levesque, M., Allaire, N., Perrin, S., Sands, B. et al. (2004). LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat. Neurosci. 7, 221-228.
27. Middleton, G., Hamanoue, M., Enokido, Y., Wyatt, S., Pennica, D., Jaffray, E., Hay, R. T. and Davies, A. M. (2000). Cytokine-induced nuclear factor k B activation promotes the survival of developing neurons. J. Cell Biol. 148, 325-332.
28. Nykjaer, A. and Willnow, T. E. (2012). Sortilin: a receptor to regulate neuronal viability and function. Trends Neurosci. 35, 261-270.
29. Nykjaer, A., Lee, R., Teng, K. K., Jansen, P., Madsen, P., Nielsen, M. S., Jacobsen, C., Kliemannel, M., Schwarz, E., Willnow, T. E. et al. (2004). Sortilin is essential for proNGF-induced neuronal cell death. Nature 427, 843-848.
30. Park, K. J., Grosso, C. A., Aubert, I., Kaplan, D. R. and Miller, F. D. (2010). p75NTR-dependent, myelin-mediated axonal degeneration regulates neural connectivity in the adult brain. Nat. Neurosci. 13, 559-566.
31. Perini, G., Della-Bianca, V., Politi, V., Della Valle, G., Dal-Pra, I., Rossi, F. and Armato, U. (2002). Role of p75 neurotrophin receptor in the neurotoxicity by beta-amyloid peptides and synergistic effect of inflammatory cytokines. J. Exp. Med. 195, 907-918.
32. Perkins, N. D. (2007). Integrating cell-signalling pathways with NF-κB and IKK function. Nat. Rev. Mol. Cell Biol. 8, 49-62.
33. Powell, J. C., Twomey, C., Jain, R. and McCarthy, J. V. (2009). Association between Presenilin-1 and TRAF6 modulates regulated intramembrane proteolysis of the p75NTR neurotrophin receptor. J. Neurochem. 108, 216-230.
34. Reichardt, L. F. (2006). Neurotrophin-regulated signalling pathways. Philos. Trans. R. Soc. B 361, 1545-1564.
35. Roux, P. P. and Barker, P. A. (2002). Neurotrophin signaling through the p75 neurotrophin receptor. Prog. Neurobiol. 67, 203-233.
36. Salehi, A. H., Roux, P. P., Kubu, C. J., Zeindler, C., Bhakar, A., Tannis, L. L., Verdi, J. M. and Barker, P. A. (2000). NRAGE, a novel MAGE protein, interacts with the p75 neurotrophin receptor and facilitates nerve growth factor-dependent apoptosis. Neuron 27, 279-288.
37. Shin, H.-M., Kim, M.-H., Kim, B. H., Jung, S.-H., Kim, Y. S., Park, H. J., Hong, J. T., Min, K. R. and Kim, Y. (2004). Inhibitory action of novel aromatic diamine compound on lipopolysaccharide-induced nuclear translocation of NF-κB without affecting IkB degradation. FEBS Lett. 571, 50-54.
38. Skeldal, S., Sykes, A. M., Glerup, S., Matusica, D., Palstra, N., Autio, H., Boskovic, Z., Madsen, P., Castrén, E., Nykjaer, A. et al. (2012). Mapping of the interaction site between sortilin and the p75 neurotrophin receptor reveals a regulatory role for the sortilin intracellular domain in p75 neurotrophin receptor shedding and apoptosis. J. Biol. Chem. 287, 43798-43809.
39. Sotthibundhu, A., Sykes, A. M., Fox, B., Underwood, C. K., Thangnipon, W. and Coulson, E. J. (2008). Beta-amyloid(1-42) induces neuronal death through the p75 neurotrophin receptor. J. Neurosci. 28, 3941-3946.
40. 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 c-secretase. J. Biol. Chem. 287, 43810-43824.
41. Tuffereau, C., Bénéjean, J., Blondel, D., Kieffer, B. and Flamand, A. (1998). Low-affinity nerve-growth factor receptor (P75NTR) can serve as a receptor for rabies virus. EMBO J. 17, 7250-7259.
42. Underwood, C. K. and Coulson, E. J. (2008). The p75 neurotrophin receptor. Int. J. Biochem. Cell Biol. 40, 1664-1668.
43. Underwood, C. K., Reid, K., May, L. M., Bartlett, P. F. and Coulson, E. J. (2008). Palmitoylation of the C-terminal fragment of p75(NTR) regulates death signaling and is required for subsequent cleavage by gamma-secretase. Mol. Cell. Neurosci. 37, 346-358.
44. Urra, S., Escudero, C. A., Ramos, P., Lisbona, F., Allende, E., Covarrubias, P., Parraguez, J. I., Zampieri, N., Chao, M. V., Annaert, W. et al. (2007). TrkA receptor activation by nerve growth factor induces shedding of the p75 neurotrophin receptor followed by endosomal gamma-secretase-mediated release of the p75 intracellular domain. J. Biol. Chem. 282, 7606-7615.
45. Vilar, M., Murillo-Carretero, M., Mira, H., Magnusson, K., Besset, V. and Ibáñez, C. F. (2006). Bex1, a novel interactor of the p75 neurotrophin receptor, links neurotrophin signaling to the cell cycle. EMBO J. 25, 1219-1230.
46. Volosin, M., Trotter, C., Cragnolini, A., Kenchappa, R. S., Light, M., Hempstead, B. L., Carter, B. D. and Friedman, W. J. (2008). Induction of proneurotrophins and activation of p75NTR-mediated apoptosis via neurotrophin receptor-interacting factor in hippocampal neurons after seizures. J. Neurosci. 28, 9870-9879.
47. Wang, C. Y., Mayo, M. W., Korneluk, R. G., Goeddel, D. V. and Baldwin, A. S., Jr (1998). NF-κB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281, 1680-1683.
48. Wang, K. C., Kim, J. A., Sivasankaran, R., Segal, R. and He, Z. (2002). P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420, 74-78.
49. Wong, S. T., Henley, J. R., Kanning, K. C., Huang, K.-H., Bothwell, M. and Poo, M.-M. (2002). A p75(NTR) and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat. Neurosci. 5, 1302-1308.
50. Yamashita, T. and Tohyama, M. (2003). The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. Nat. Neurosci. 6, 461-467.
51. Yamashita, T., Tucker, K. L. and Barde, Y. A. (1999). Neurotrophin binding to the p75 receptor modulates Rho activity and axonal outgrowth. Neuron 24, 585-593.
52. Yoon, S. O., Casaccia-Bonnefil, P., Carter, B. and Chao, M. V. (1998). Competitive signaling between TrkA and p75 nerve growth factor receptors determines cell survival. J. Neurosci. 18, 3273-3281.
53. Zhang, T., Inesta-Vaquera, F., Niepel, M., Zhang, J., Ficarro, S. B., Machleidt, T., Xie, T., Marto, J. A., Kim, N., Sim, T. et al. (2012). Discovery of potent and selective covalent inhibitors of JNK. Chem. Biol. 19, 140-154.
54. Zhang, Y., Huang, H., Zhou, H., Du, T., Zeng, L., Cao, Y., Chen, J., Lai, Y., Li, J., Wang, G. et al. (2014). Activation of nuclear factor κB pathway and downstream targets survivin and livin by SHARPIN contributes to the progression and metastasis of prostate cancer. Cancer 120, 3208-3218.