The intracellular portion of GITR enhances NGF-promoted neurite growth through an inverse modulation of Erk and NF-κB signalling

Biology Open

Volumn 1, Issue 10, 2012, Pages 1016-1023

  McKelvey, Laura ^a   Gutierrez, Humberto ^b   Nocentini, Giuseppe ^c   Crampton, Sean J ^a   Davies, Alun M ^d   Riccardi, Carlo R ^c   O'Keeffe, Gerard W ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

^c UNIVERSITY OF PERUGIA   (Italy)

^d CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

GITR; Growth; Neurite; Neuron; NF B; NGF

Indexed keywords

EID: 84964836055     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20121024     Document Type: Article

References (37)

1. Armstrong, A., Ryu, Y. K., Chieco, D. and Kuruvilla, R. (2011). Frizzled3 is required for neurogenesis and target innervation during sympathetic nervous system development. J. Neurosci. 31, 2371-2381.
2. Bae, E. M., Kim, W. J., Suk, K., Kang, Y. M., Park, J. E., Kim, W. Y., Choi, E. M., Choi, B. K., Kwon, B. S. and Lee, W. H. (2008). Reverse signaling initiated from GITRL induces NF-κB activation through ERK in the inflammatory activation of macrophages. Mol. Immunol. 45, 523-533.
3. Beinke, S., Robinson, M. J., Hugunin, M. and Ley, S. C. (2004). Lipopolysaccharide activation of the TPL-2/MEK/extracellular signal-regulated kinase mitogen-activated protein kinase cascade is regulated by IκB kinase-induced proteolysis of NF-κB1 p105. Mol. Cell. Biol. 24, 9658-9667.
4. 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.
5. Campenot, R. B. (1994). NGF and the local control of nerve terminal growth. J. Neurobiol. 25, 599-611.
6. Das, S., Cho, J., Lambertz, I., Kelliher, M. A., Eliopoulos, A. G., Du, K. and Tsichlis, P. N. (2005). Tpl2/cot signals activate ERK, JNK, and NF-κB in a cell-type and stimulus-specific manner. J. Biol. Chem. 280, 23748-23757.
7. Edwards, R. H., Rutter, W. J. and Hanahan, D. (1989). Directed expression of NGF to pancreatic β cells in transgenic mice leads to selective hyperinnervation of the islets. Cell 58, 161-170.
8. Eliopoulos, A. G., Wang, C.-C., Dumitru, C. D. and Tsichlis, P. N. (2003). Tpl2 transduces CD40 and TNF signals that activate ERK and regulates IgE induction by CD40. EMBO J. 22, 3855-3864.
9. Esparza, E. M. and Arch, R. H. (2004). TRAF4 functions as an intermediate of GITRinduced NF-κB activation. Cell. Mol. Life Sci. 61, 3087-3092.
10. Esparza, E. M., Lindsten, T., Stockhausen, J. M. and Arch, R. H. (2006). Tumor necrosis factor receptor (TNFR)-associated factor 5 is a critical intermediate of costimulatory signaling pathways triggered by glucocorticoid-induced TNFR in T cells. J. Biol. Chem. 281, 8559-8564.
11. Gallagher, D., Gutierrez, H., Gavalda, N., O'Keeffe, G., Hay, R. and Davies, A. M. (2007). Nuclear factor-κB activation via tyrosine phosphorylation of inhibitor κB-α is crucial for ciliary neurotrophic factor-promoted neurite growth from developing neurons. J. Neurosci. 27, 9664-9669.
12. Gavaldà, N., Gutierrez, H. and Davies, A. M. (2009). Developmental switch in NF-κB signalling required for neurite growth. Development 136, 3405-3412.
13. Glebova, N. O. and Ginty, D. D. (2004). Heterogeneous requirement of NGF for sympathetic target innervation in vivo. J. Neurosci. 24, 743-751.
14. Glebova, N. O. and Ginty, D. D. (2005). Growth and survival signals controlling sympathetic nervous system development. Annu. Rev. Neurosci. 28, 191-222.
15. Grohmann, U., Volpi, C., Fallarino, F., Bozza, S., Bianchi, R., Vacca, C., Orabona, C., Belladonna, M. L., Ayroldi, E., Nocentini, G. et al. (2007). Reverse signaling through GITR ligand enables dexamethasone to activate IDO in allergy. Nat. Med. 13, 579-586.
16. Gutierrez, H. and Davies, A. M. (2007). A fast and accurate procedure for deriving the Sholl profile in quantitative studies of neuronal morphology. J. Neurosci. Methods 163, 24-30.
17. Gutierrez, H. and Davies, A. M. (2011). Regulation of neural process growth, elaboration and structural plasticity by NF-κB. Trends Neurosci. 34, 316-325.
18. Gutierrez, H., Hale, V. A., Dolcet, X. and Davies, A. (2005). NF-κB signalling regulates the growth of neural processes in the developing PNS and CNS. Development 132, 1713-1726.
19. Gutierrez, H., O'Keeffe, G. W., Gavaldà, N., Gallagher, D. and Davies, A. M. (2008). Nuclear factor κB signaling either stimulates or inhibits neurite growth depending on the phosphorylation status of p65/RelA. J. Neurosci. 28, 8246-8256.
20. Hauer, J., Püschner, S., Ramakrishnan, P., Simon, U., Bongers, M., Federle, C. and Engelmann, H. (2005). TNF receptor (TNFR)-associated factor (TRAF) 3 serves as an inhibitor of TRAF2/5-mediated activation of the noncanonical NF-κB pathway by TRAF-binding TNFRs. Proc. Natl. Acad. Sci. USA 102, 2874-2879.
21. Hoffmann, A., Natoli, G. and Ghosh, G. (2006). Transcriptional regulation via the NF-κB signaling module. Oncogene 25, 6706-6716.
22. Honma, Y., Araki, T., Gianino, S., Bruce, A., Heuckeroth, R., Johnson, E. and Milbrandt, J. (2002). Artemin is a vascular-derived neurotropic factor for developing sympathetic neurons. Neuron 35, 267-282.
23. Krausz, L. T., Bianchini, R., Ronchetti, S., Fettucciari, K., Nocentini, G. and Riccardi, C. (2007). GITR-GITRL system, a novel player in shock and inflammation. Scientific World Journal 7, 533-566.
24. Levi-Montalcini, R. (1987). The nerve growth factor 35 years later. Science 237, 1154-1162
25. Markus, A., Patel, T. D. and Snider, W. D. (2002). Neurotrophic factors and axonal growth. Curr. Opin. Neurobiol. 12, 523-531.
26. Mettouchi, A., Cabon, F., Montreau, N., Dejong, V., Vernier, P., Gherzi, R., Mercier, G. and Binétruy, B. (1997). The c-Jun-induced transformation process involves complex regulation of tenascin-C expression. Mol. Cell. Biol. 17, 3202-3209.
27. Nolan, A. M., Nolan, Y. M. and O'Keeffe, G. W. (2011). IL-1β inhibits axonal growth of developing sympathetic neurons. Mol. Cell. Neurosci. 48, 142-150.
28. O'Keeffe, G. W., Gutierrez, H., Pandolfi, P. P., Riccardi, C. and Davies, A. M. (2008). NGF-promoted axon growth and target innervation requires GITRL-GITR signaling. Nat. Neurosci. 11, 135-142.
29. Roff, M., Thompson, J., Rodriguez, M. S., Jacque, J.-M., Baleux, F., Arenzana-Seisdedos, F. and Hay, R. T. (1996). Role of IκBα ubiquitination in signal-induced activation of NFκB in vivo. J. Biol. Chem. 271, 7844-7850.
30. Ronchetti, S., Zollo, O., Bruscoli, S., Agostini, M., Bianchini, R., Nocentini, G., Ayroldi, E. and Riccardi, C. (2004). GITR, a member of the TNF receptor superfamily, is costimulatory to mouse T lymphocyte subpopulations. Eur. J. Immunol. 34, 613-622.
31. Sholl, D. A. (1953). Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat. 87, 387-406.
32. Simpson, C. S. and Morris, B. J. (2000). Regulation of neuronal cell adhesion molecule expression by NF-κB. J. Biol. Chem. 275, 16879-16884.
33. Thompson, J., Dolcet, X., Hilton, M., Tolcos, M. and Davies, A. M. (2004). HGF promotes survival and growth of maturing sympathetic neurons by PI-3 kinase- and MAP kinase-dependent mechanisms. Mol. Cell. Neurosci. 27, 441-452.
34. Vizard, T. N., O'Keeffe, G. W., Gutierrez, H., Kos, C. H., Riccardi, D. and Davies, A. M. (2008). Regulation of axonal and dendritic growth by the extracellular calciumsensing receptor. Nat. Neurosci. 11, 285-291.
35. 1 integrin-dependent mechanism. J. Immunol. 170, 795-804.
36. Waterfield, M. R., Zhang, M., Norman, L. P. and Sun, S.-C. (2003). NF-κB1/p105 regulates lipopolysaccharide-stimulated MAP kinase signaling by governing the stability and function of the Tpl2 kinase. Mol. Cell 11, 685-694.
37. Zhou, Z., Tone, Y., Song, X., Furuuchi, K., Lear, J. D., Waldmann, H., Tone, M., Greene, M. I. and Murali, R. (2008). Structural basis for ligand-mediated mouse GITR activation. Proc. Natl. Acad. Sci. USA 105, 641-645.