Kidins220/ARMS downregulation by excitotoxic activation of NMDARs reveals its involvement in neuronal survival and death pathways

Journal of Cell Science

Volumn 122, Issue 19, 2009, Pages 3554-3565

  López Menéndez, Celia ^a,b   Gascón, Sergio ^a,c   Sobrado, Mónica ^a,d   Vidaurre, Oscar G ^a   Higuero, Alonso M ^a,b,e   Rodríguez Peña, Ángeles ^a   Iglesias, Teresa ^a,b   Díaz Guerra, Margarita ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^e HOSPITAL NACIONAL DE PARAPLÉJICOS   (Spain)

Author keywords

Calpain; Eph receptors; ERK; Excitotoxicity; Ischemia; Kidins220 ARMS (ARMS); Neuronal death; Neurotrophins; NMDAR; Survival; Trk receptors

Indexed keywords

ANKYRIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; NEUROTROPHIN AND EPHRIN RECEPTOR SIGNALING IS KINASE D INTERACTING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN CELL; CALCIUM TRANSPORT; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EXCITOTOXICITY; GENE ACTIVATION; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TARGETING; RAT; REGULATORY MECHANISM;

ANIMALS; BRAIN ISCHEMIA; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOWN-REGULATION; HUMANS; MALE; MEMBRANE PROTEINS; NEURONS; PHOSPHOPROTEINS; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 70350365279     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.056473     Document Type: Article

References (43)

1. Arevalo, J. C., Yano, H., Teng, K. K. and Chao, M. V. (2004). A unique pathway for sustained neurotrophin signaling through an ankyrin-rich membrane-spanning protein. EMBO J. 23, 2358-2368.
2. Arevalo, J. C., Pereira, D. B., Yano, H., Teng, K. K. and Chao, M. V. (2006). Identification of a switch in neurotrophin signaling by selective tyrosine phosphorylation. J. Biol. Chem. 281, 1001-1007.
3. Bano, D., Young, K. W., Guerin, C. J., Lefeuvre, R., Rothwell, N. J., Naldini, L., Rizzuto, R., Carafoli, E. and Nicotera, P. (2005). Cleavage of the plasma membrane Na+/Ca2+ exchanger in excitotoxicity. Cell 120, 275-285.
4. Cabrera-Poch, N., Sanchez-Ruiloba, L., Rodriguez-Martinez, M. and Iglesias, T. (2004). Lipid raft disruption triggers protein kinase C and Src-dependent protein kinase D activation and Kidins220 phosphorylation in neuronal cells. J. Biol. Chem. 279, 28592-28602.
5. Choi, D. W. (1988). Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623-634.
6. Cortes, R. Y., Arevalo, J. C., Magby, J. P., Chao, M. V. and Plummer, M. R. (2007). Developmental and activity-dependent regulation of ARMS/Kidins220 in cultured rat hippocampal neurons. Dev. Neurobiol. 67, 1687-1698.
7. Cui, H., Hayashi, A., Sun, H. S., Belmares, M. P., Cobey, C., Phan, T., Schweizer, J., Salter, M. W., Wang, Y. T., Tasker, R. A. et al. (2007). PDZ protein interactions underlying NMDA receptor-mediated excitotoxicity and neuroprotection by PSD-95 inhibitors. J. Neurosci. 27, 9901-9915.
8. Dalva, M. B., Takasu, M. A., Lin, M. Z., Shamah, S. M., Hu, L., Gale, N. W. and Greenberg, M. E. (2000). EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 103, 945-956.
9. Gascon, S., Deogracias, R., Sobrado, M., Roda, J. M., Renart, J., Rodriguez-Pena, A. and Diaz-Guerra, M. (2005). Transcription of the NR1 subunit of the N-methyl-Daspartate receptor is down-regulated by excitotoxic stimulation and cerebral ischemia. J. Biol. Chem. 280, 35018-35027.
10. Gascon, S., Sobrado, M., Roda, J. M., Rodriguez-Pena, A. and Diaz-Guerra, M. (2008). Excitotoxicity and focal cerebral ischemia induce truncation of the NR2A and NR2B subunits of the NMDA receptor and cleavage of the scaffolding protein PSD-95. Mol. Psychiatry 13, 99-114.
11. Gouix, E., Leveille, F., Nicole, O., Melon, C., Had-Aissouni, L. and Buisson, A. (2009). Reverse glial glutamate uptake triggers neuronal cell death through extrasynaptic NMDA receptor activation. Mol. Cell Neurosci. 40, 463-473.
12. Hardingham, G. E., Fukunaga, Y. and Bading, H. (2002). Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat. Neurosci. 5, 405-414.
13. Henderson, J. T., Georgiou, J., Jia, Z., Robertson, J., Elowe, S., Roder, J. C. and Pawson, T. (2001). The receptor tyrosine kinase EphB2 regulates NMDA-dependent synaptic function. Neuron 32, 1041-1056.
14. Hirao, K., Hata, Y., Ide, N., Takeuchi, M., Irie, M., Yao, I., Deguchi, M., Toyoda, A., Sudhof, T. C. and Takai, Y. (1998). A novel multiple PDZ domain-containing molecule interacting with N-methyl-D-aspartate receptors and neuronal cell adhesion proteins. J. Biol. Chem. 273, 21105-21110.
15. Hirao, K., Hata, Y., Yao, I., Deguchi, M., Kawabe, H., Mizoguchi, A. and Takai, Y. (2000). Three isoforms of synaptic scaffolding molecule and their characterization. Multimerization between the isoforms and their interaction with N-methyl-D-aspartate receptors and SAP90/ PSD-95-associated protein. J. Biol. Chem. 275, 2966-2972.
16. Hisata, S., Sakisaka, T., Baba, T., Yamada, T., Aoki, K., Matsuda, M. and Takai, Y. (2007). Rap1-PDZ-GEF1 interacts with a neurotrophin receptor at late endosomes, leading to sustained activation of Rap1 and ERK and neurite outgrowth. J. Cell Biol. 178, 843-860.
17. Hong, S. C., Lanzino, G., Goto, Y., Kang, S. K., Schottler, F., Kassell, N. F. and Lee, K. S. (1994). Calcium-activated proteolysis in rat neocortex induced by transient focal ischemia. Brain Res. 661, 43-50.
18. Husi, H., Ward, M. A., Choudhary, J. S., Blackstock, W. P. and Grant, S. G. (2000). Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat. Neurosci. 3, 661-669.
19. Iglesias, T., Caubin, J., Stunnenberg, H. G., Zaballos, A., Bernal, J. and Munoz, A. (1996). Thyroid hormone-dependent transcriptional repression of neural cell adhesion molecule during brain maturation. EMBO J. 15, 4307-4316.
20. Iglesias, T., Cabrera-Poch, N., Mitchell, M. P., Naven, T. J., Rozengurt, E. and Schiavo, G. (2000). Identification and cloning of Kidins220, a novel neuronal substrate of protein kinase D. J. Biol. Chem. 275, 40048-40056.
21. Ivanov, A., Pellegrino, C., Rama, S., Dumalska, I., Salyha, Y., Ben-Ari, Y. and Medina, I. (2006). Opposing role of synaptic and extrasynaptic NMDA receptors in regulation of the extracellular signal-regulated kinases (ERK) activity in cultured rat hippocampal neurons. J. Physiol. 572, 789-798.
22. Kong, H., Boulter, J., Weber, J. L., Lai, C. and Chao, M. V. (2001). An evolutionarily conserved transmembrane protein that is a novel downstream target of neurotrophin and ephrin receptors. J. Neurosci. 21, 176-185.
23. Kornau, H. C., Schenker, L. T., Kennedy, M. B. and Seeburg, P. H. (1995). Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269, 1737-1740.
24. Leveille, F., El Gaamouch, F., Gouix, E., Lecocq, M., Lobner, D., Nicole, O. and Buisson, A. (2008). Neuronal viability is controlled by a functional relation between synaptic and extrasynaptic NMDA receptors. FASEB J. 22, 4258-4271.
25. Li, J. H., Wang, Y. H., Wolfe, B. B., Krueger, K. E., Corsi, L., Stocca, G. and Vicini, S. (1998). Developmental changes in localization of NMDA receptor subunits in primary cultures of cortical neurons. Eur. J. Neurosci. 10, 1704-1715.
26. Luo, S., Chen, Y., Lai, K. O., Arevalo, J. C., Froehner, S. C., Adams, M. E., Chao, M. V. and Ip, N. Y. (2005). {alpha}-Syntrophin regulates ARMS localization at the neuromuscular junction and enhances EphA4 signaling in an ARMS-dependent manner. J. Cell Biol. 169, 813-824.
27. Miyamoto, Y., Chen, L., Sato, M., Sokabe, M., Nabeshima, T., Pawson, T., Sakai, R. and Mori, N. (2005). Hippocampal synaptic modulation by the phosphotyrosine adapter protein ShcC/N-Shc via interaction with the NMDA receptor. J. Neurosci. 25, 1826-1835.
28. Neumar, R. W., Xu, Y. A., Gada, H., Guttmann, R. P. and Siman, R. (2003). Cross-talk between calpain and caspase proteolytic systems during neuronal apoptosis. J. Biol. Chem. 278, 14162-14167.
29. Papadia, S., Soriano, F. X., Leveille, F., Martel, M. A., Dakin, K. A., Hansen, H. H., Kaindl, A., Sifringer, M., Fowler, J., Stefovska, V. et al. (2008). Synaptic NMDA receptor activity boosts intrinsic antioxidant defenses. Nat. Neurosci. 11, 476-487.
30. Park, J. S., Bateman, M. C. and Goldberg, M. P. (1996). Rapid alterations in dendrite morphology during sublethal hypoxia or glutamate receptor activation. Neurobiol. Dis. 3, 215-227.
31. Rubinson, D. A., Dillon, C. P., Kwiatkowski, A. V., Sievers, C., Yang, L., Kopinja, J., Rooney, D. L., Zhang, M., Ihrig, M. M., McManus, M. T. et al. (2003). A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat. Genet. 33, 401-406.
32. Sanchez-Ruiloba, L., Cabrera-Poch, N., Rodriguez-Martinez, M., Lopez-Menendez, C., Jean-Mairet, R. M., Higuero, A. M. and Iglesias, T. (2006). Protein kinase D intracellular localization and activity control kinase D-interacting substrate of 220-kDa traffic through a postsynaptic density-95/discs large/zonula occludens-1-binding motif. J. Biol. Chem. 281, 18888-18900.
33. Siman, R. and Noszek, J. C. (1988). Excitatory amino acids activate calpain I and induce structural protein breakdown in vivo. Neuron 1, 279-287.
34. Simpkins, K. L., Guttmann, R. P., Dong, Y., Chen, Z., Sokol, S., Neumar, R. W. and Lynch, D. R. (2003). Selective activation induced cleavage of the NR2B subunit by calpain. J. Neurosci. 23, 11322-11331.
35. Takasu, M. A., Dalva, M. B., Zigmond, R. E. and Greenberg, M. E. (2002). Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 295, 491-495.
36. Tezuka, T., Umemori, H., Akiyama, T., Nakanishi, S. and Yamamoto, T. (1999). PSD-95 promotes Fyn-mediated tyrosine phosphorylation of the N-methyl-D-aspartate receptor subunit NR2A. Proc. Natl. Acad. Sci. USA 96, 435-440.
37. Thomas, C. G., Miller, A. J. and Westbrook, G. L. (2006). Synaptic and extrasynaptic NMDA receptor NR2 subunits in cultured hippocampal neurons. J. Neurophysiol. 95, 1727-1734.
38. Thomas, G. M. and Huganir, R. L. (2004). MAPK cascade signalling and synaptic plasticity. Nat. Rev. Neurosci. 5, 173-183.
39. Vanderklish, P. W. and Bahr, B. A. (2000). The pathogenic activation of calpain: a marker and mediator of cellular toxicity and disease states. Int. J. Exp. Pathol. 81, 323-339.
40. Vosler, P. S., Brennan, C. S. and Chen, J. (2008). Calpain-mediated signaling mechanisms in neuronal injury and neurodegeneration. Mol. Neurobiol. 38, 78-100.
41. Walton, M. R. and Dragunow, I. (2000). Is CREB a key to neuronal survival? Trends Neurosci. 23, 48-53.
42. Williams, K. (1993). Ifenprodil discriminates subtypes of the N-methyl-D-aspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors. Mol. Pharmacol. 44, 851-859.
43. Yamada, K. and Nabeshima, T. (2004). Interaction of BDNF/TrkB signaling with NMDA receptor in learning and memory. Drug News Perspect. 17, 435-438.