Presynaptic c-Jun N-terminal Kinase 2 regulates NMDA receptor-dependent glutamate release

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Nisticò, Robert ^a,g   Florenzano, Fulvio ^a   Mango, Dalila ^a,b   Ferraina, Caterina ^a   Grilli, Massimo ^c   Di Prisco, Silvia ^c   Nobili, Annalisa ^b,d   Saccucci, Stefania ^e   D'Amelio, Marcello ^b,d   Morbin, Michela ^e   Marchi, Mario ^c   Mercuri, Nicola B ^b   Davis, Roger J ^f   Pittaluga, Anna ^c   Feligioni, Marco ^a  

^a EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

^d UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^e DEPARTMENT OF NEUROSURGERY   (Italy)

^f UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^g SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; BIOLOGICAL MARKER; GLUTAMIC ACID; MITOGEN ACTIVATED PROTEIN KINASE 9; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN CORTEX; ENZYME ACTIVATION; EXOCYTOSIS; FEMALE; GENETICS; KNOCKOUT MOUSE; MALE; METABOLISM; MOUSE; PHOSPHORYLATION; SYNAPTOSOME; TIME LAPSE IMAGING; ULTRASTRUCTURE;

ANIMALS; BIOMARKERS; CEREBRAL CORTEX; ENZYME ACTIVATION; EXOCYTOSIS; FEMALE; GLUTAMIC ACID; MALE; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 9; PHOSPHORYLATION; PRESYNAPTIC TERMINALS; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTOSOMES; TIME-LAPSE IMAGING;

EID: 84924866851     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep09035     Document Type: Article

References (59)

1. Hack, N. & Balázs, R. Selective stimulation of excitatory amino acid receptor subtypes and the survival of granule cells in culture: effect of quisqualate and AMPA. Neurochem. Int. 25, 235-41 (1994).
2. Yang, X.-R. et al . Involvement of MAPK pathways in NMDA-induced apoptosis of rat cortical neurons. Sheng Li Xue Bao 64, 609-16 (2012).
3. Collingridge, G. L.&Lester, R. A. Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacol. Rev. 41, 143-210 (1989).
4. Headley, P. M. & Grillner, S. Excitatory amino acids and synaptic transmission: the evidence for a physiological function. Trends Pharmacol. Sci. 11, 205-11 (1990).
5. Rothman, S. M. &Olney, J. W. Excitotoxicity and theNMDA receptor - still lethal after eight years. Trends Neurosci. 18, 57-8 (1995).
6. Choi, D. W. & Rothman, S. M. The role of glutamate neurotoxicity in hypoxicischemic neuronal death. Annu. Rev. Neurosci. 13, 171-82 (1990).
7. Meldrum, B. & Garthwaite, J. Excitatory amino acid neurotoxicity and neurodegenerative disease. Trends Pharmacol. Sci. 11, 379-87 (1990).
8. Corlew, R., Brasier, D. J., Feldman, D. E. & Philpot, B. D. Presynaptic NMDA receptors: newly appreciated roles in cortical synaptic function and plasticity. Neuroscientist 14, 609-625 (2008).
9. Feligioni, M., Holman, D., Haglerod, C., Davanger, S. & Henley, J. M. Ultrastructural localisation and differential agonist-induced regulation of AMPA and kainate receptors present at the presynaptic active zone and postsynaptic density. J. Neurochem. 99, 549-60 (2006).
10. Pinheiro, P. S. et al. Presynaptic kainate receptors are localized close to release sites in rat hippocampal synapses. Neurochem. Int. 47, 309-16 (2005).
11. Grilli, M. et al. In vitro exposure to nicotine induces endocytosis of presynaptic AMPA receptors modulating dopamine release in rat nucleus accumbens nerve terminals. Neuropharmacology 63, 916-26 (2012).
12. Musante, V. et al. Presynaptic mGlu1 and mGlu5 autoreceptors facilitate glutamate exocytosis from mouse cortical nerve endings. Neuropharmacology 55, 474-82 (2008).
13. Pittaluga, A., Feligioni, M., Longordo, F., Luccini, E. & Raiteri, M. Trafficking of presynaptic AMPA receptors mediating neurotransmitter release: neuronal selectivity and relationships with sensitivity to cyclothiazide. Neuropharmacology 50, 286-96 (2006).
14. Perkins, D., Gyure, K. A., Pereira, E. F. R. & Aurelian, L. Herpes simplex virus type 1-induced encephalitis has an apoptotic component associated with activation of c-Jun N-terminal kinase. J. Neurovirol. 9, 101-11 (2003).
15. Sclip, A. et al . c-Jun N-terminal kinase regulates soluble A β oligomers and cognitive impairment in AD mouse model. J. Biol. Chem. 286, 43871-80 (2011).
16. La Rosa, L. R. et al. Age-related changes of hippocampal synaptic plasticity in AβPP-null mice are restored by NGF through p75NTR. J. Alzheimers. Dis. 33, 265-72 (2013).
17. Davis, R. J. Signal transduction by the JNK group of MAP kinases. Cell 103, 239-52 (2000).
18. Gupta, S. et al. Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J. 15, 2760-70 (1996).
19. Kuan, C. Y. et al. The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron 22, 667-76 (1999).
20. Weston, C. R.&Davis, R. J. The JNK signal transduction pathway. Curr. Opin. Cell Biol. 19, 142-9 (2007).
21. Brecht, S. et al. Specific pathophysiological functions of JNK isoforms in the brain. Eur. J. Neurosci. 21, 363-77 (2005).
22. Yamasaki, T., Kawasaki, H. & Nishina, H. Diverse Roles of JNK and MKK Pathways in the Brain. J. Signal Transduct. 2012, 459265 (2012).
23. Borsello, T., Croquelois, K., Hornung, J.-P. & Clarke, P. G. H. N-methyl-d-aspartate- triggered neuronal death in organotypic hippocampal cultures is endocytic, autophagic and mediated by the c-Jun N-terminal kinase pathway. Eur. J. Neurosci. 18, 473-85 (2003).
24. Luccini, E., Musante, V., Neri, E., Raiteri, M. & Pittaluga, A. N-methyl-Daspartate autoreceptors respond to low and high agonist concentrations by facilitating, respectively, exocytosis and carrier-mediated release of glutamate in rat hippocampus. J. Neurosci. Res. 85, 3657-65 (2007).
25. Grilli, M., Raiteri, L. & Pittaluga, A. Somatostatin inhibits glutamate release from mouse cerebrocortical nerve endings through presynaptic sst2 receptors linked to the adenylyl cyclase-protein kinase A pathway. Neuropharmacology 46, 388-96 (2004).
26. Pittaluga, A., Feligioni, M., Longordo, F., Arvigo, M. & Raiteri, M. Somatostatin-induced activation and up-regulation of N-methyl-D-aspartate receptor function: mediation through calmodulin-dependent protein kinase II, phospholipase C, protein kinase C, and tyrosine kinase in hippocampal noradrenergic nerve endings. J. Pharmacol. Exp. Ther. 313, 242-9 (2005).
27. Feligioni, M., Nishimune, A. & Henley, J. M. Protein SUMOylation modulates calcium influx and glutamate release from presynaptic terminals. Eur. J. Neurosci. 29, 1348-56 (2009).
28. Kennedy, N. J. et al. Requirement of JIP scaffold proteins for NMDA-mediated signal transduction. Genes Dev. 21, 2336-46 (2007).
29. Bonny, C., Oberson, A., Negri, S., Sauser, C. & Schorderet, D. F. Cell-permeable peptide inhibitors of JNK: novel blockers of beta-cell death. Diabetes 50, 77-82 (2001).
30. Antoniou, X. et al. JNK contributes to Hif-1alpha regulation in hypoxic neurons. Molecules 15, 114-27 (2010).
31. Yan, J. & Hales, B. F. p38 and c-Jun N-terminal kinase mitogen-activated protein kinase signaling pathways play distinct roles in the response of organogenesisstage embryos to a teratogen. J. Pharmacol. Exp. Ther. 326, 764-72 (2008).
32. Sakaba, T., Stein, A., Jahn, R. & Neher, E. Distinct kinetic changes in neurotransmitter release after SNARE protein cleavage. Science 309, 491-4 (2005).
33. Silinsky, E. M. Modulation of calcium currents is eliminated after cleavage of a strategic component of themammalian secretory apparatus. J. Physiol. 566, 681-8 (2005).
34. Berretta, N. & Jones, R. S. Tonic facilitation of glutamate release by presynaptic N-methyl- D-aspartate autoreceptors in the entorhinal cortex. Neuroscience 75, 339-44 (1996).
35. Dong, C. et al. Defective T cell differentiation in the absence of Jnk1. Science 282, 2092-5 (1998).
36. Tsuiki, H. et al . Constitutively Active Forms of c-Jun NH2-terminal Kinase Are Expressed in Primary Glial Tumors. Cancer Res. 63, 250-255 (2003).
37. Groffen, A. J. et al. Doc2b is a high-affinity Ca21 sensor for spontaneous neurotransmitter release. Science 327, 1614-8 (2010).
38. Liang, B., Kiessling, V. & Tamm, L. K. Prefusion structure of syntaxin-1A suggests pathway for folding into neuronal trans-SNARE complex fusion intermediate. Proc. Natl. Acad. Sci. U. S. A. 110, 19384-9 (2013).
39. Centeno, C. et al . Role of the JNK pathway in NMDA-mediated excitotoxicity of cortical neurons. Cell Death Differ. 14, 240-53 (2007).
40. Musante, V., Summa, M., Cunha, R. A., Raiteri, M. & Pittaluga, A. Pre-synaptic glycine GlyT1 transporter - NMDA receptor interaction: relevance to NMDA autoreceptor activation in the presence of Mg2 1 ions. J. Neurochem. 117, 516-27 (2011).
41. Mori, Y., Higuchi, M., Hirabayashi, Y., Fukuda, M. & Gotoh, Y. JNK phosphorylates synaptotagmin-4 and enhances Ca21-evoked release. EMBO J. 27, 76-87 (2008).
42. Wu, Y. E., Huo, L., Maeder, C. I., Feng, W.&Shen, K. The balance between capture and dissociation of presynaptic proteins controls the spatial distribution of synapses. Neuron 78, 994-1011 (2013).
43. Feligioni, M. et al. Crosstalk between JNK and SUMO Signaling Pathways: deSUMOylation Is Protective against H(2)O(2)-Induced Cell Injury. PLoS One 6, e28185 (2011).
44. Borsello, T. et al. A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nat. Med. 9, 1180-6 (2003).
45. Lin, T. Y., Lu, C. W., Huang, S. K. & Wang, S. J. Curcumin inhibits glutamate release from rat prefrontal nerve endings by affecting vesicle mobilization. Int. J. Mol. Sci. 13, 9097-109 (2012).
46. Tuz, K., Peña-Segura, C., Franco, R. & Pasantes-Morales, H. Depolarization, exocytosis and amino acid release evoked by hyposmolarity from cortical synaptosomes. Eur. J. Neurosci. 19, 916-924 (2004).
47. Song, L., Nath, A., Geiger, J. D., Moore, A. & Hochman, S. Human immunodeficiency virus type 1 Tat protein directly activates neuronal N-methyl- D-aspartate receptors at an allosteric zinc-sensitive site. J. Neurovirol. 9, 399-403 (2003).
48. Longordo, F. et al. The human immunodeficiency virus-1 protein transactivator of transcription up-regulates N-methyl-D-aspartate receptor function by acting at metabotropic glutamate receptor 1 receptors coexisting on human and rat brain noradrenergic neurones. J. Pharmacol. Exp. Ther. 317, 1097-105 (2006).
49. Feligioni, M. et al. The human immunodeficiency virus-1 protein Tat and its discrete fragments evoke selective release of acetylcholine from human and rat cerebrocortical terminals through species-specific mechanisms. J. Neurosci. 23, 6810-8 (2003).
50. Repici, M. et al. Time-course of c-Jun N-terminal kinase activation after cerebral ischemia and effect of D-JNKI1 on c-Jun and caspase-3 activation. Neuroscience 150, 40-9 (2007).
51. Yang, D. D. et al. Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature 389, 865-70 (1997).
52. Kuan, C.-Y. et al . A critical role of neural-specific JNK3 for ischemic apoptosis. Proc. Natl. Acad. Sci. U. S. A. 100, 15184-9 (2003).
53. Kim, M. J. et al. Synaptic accumulation of PSD-95 and synaptic function regulated by phosphorylation of serine-295 of PSD-95. Neuron 56, 488-502 (2007).
54. Coffey, E. T. Nuclear and cytosolic JNK signalling in neurons. Nat. Rev. Neurosci. 15, 285-99 (2014).
55. Cui, J., Zhang, M., Zhang, Y.-Q. & Xu, Z.-H. JNK pathway: diseases and therapeutic potential. Acta Pharmacol. Sin. 28, 601-8 (2007).
56. Yang,D.D. et al.Differentiation of CD41 T cells to Th1 cells requiresMAPkinase JNK2. Immunity 9, 575-85 (1998).
57. Pittaluga, A., Segantini, D., Feligioni, M. & Raiteri, M. Extracellular protons differentially potentiate the responses of native AMPA receptor subtypes regulating neurotransmitter release. Br. J. Pharmacol. 144, 293-9 (2005).
58. Jones, R. S. & Heinemann, U. Synaptic and intrinsic responses of medical entorhinal cortical cells in normal and magnesium-free medium in vitro. J. Neurophysiol. 59, 1476-96 (1988).
59. Nisticò, R. et al. Inflammation subverts hippocampal synaptic plasticity in experimental multiple sclerosis. PLoS One 8, e54666 (2013).