Interleukin-1β enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases

Journal of Neuroscience

Volumn 23, Issue 25, 2003, Pages 8692-8700

  Viviani, Barbara ^a   Bartesaghi, S ^a   Gardoni, F ^a   Vezzani, A ^b   Behrens, M M ^c   Bartfai, T ^c   Binaglia, M ^a   Corsini, E ^a   Di Luca, M ^a   Galli, C L ^a   Marinovich, M ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Cytokines; Excitotoxicity; Hippocampal neurons; IL 1 receptor type I; NR2A B subunits; Tyrosine kinase

Indexed keywords

2 AMINOETHOXYDIPHENYLBORANE; 4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; BORIC ACID; CALCIUM ION; DANTROLENE; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; LAVENDUSTIN A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRENDIPINE; PROTEIN TYROSINE KINASE; PYRIMIDINE DERIVATIVE; RECEPTOR SUBUNIT; TETRODOTOXIN; UNCLASSIFIED DRUG; AMINO ACID RECEPTOR STIMULATING AGENT; CALCIUM; ENZYME INHIBITOR; INTERLEUKIN 1; N METHYLASPARTIC ACID; NR2A NMDA RECEPTOR; NR2B NMDA RECEPTOR; SIALOGLYCOPROTEIN;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; FETUS; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; CELL CULTURE; CELL DEATH; CYTOLOGY; DOSE RESPONSE; DRUG EFFECT; DRUG POTENTIATION; INTRACELLULAR FLUID; METABOLISM; NERVE CELL; PHOSPHORYLATION;

ANIMALS; CALCIUM; CELL DEATH; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; ENZYME ACTIVATION; ENZYME INHIBITORS; EXCITATORY AMINO ACID AGONISTS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1; INTRACELLULAR FLUID; N-METHYLASPARTATE; NEURONS; PHOSPHORYLATION; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; SIALOGLYCOPROTEINS; SRC-FAMILY KINASES;

EID: 0141535180     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-25-08692.2003     Document Type: Article

References (40)

1. Allan SM, Rothwell NJ (2001) Cylokines and acute neurodegeneration. Nat Rev Neurosci 2:734-744.
2. Allan SM, Parker LC, Collins B, Davies R, Luheshi GN, Rothwell NJ (2000) Cortical cell death induced by IL-1 is mediated via actions in the hypothalamus of the rat. Proc Natl Acad Sci USA 97:5580-5585.
3. Chatterton JE, Awobuluyi M, Premkumar LS, Takahashi H, Talantova M, Shin Y, Cul J, Tu S, Sevarino KA, Nakanishi N, Tong G, Lipton SA, Zhang D (2002) Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 415:793-798.
4. Coogan A, O'Connor JJ (1997) Inhibition of NMDA receptor-mediated synaptic transmission in the rat dentate gyrus in vitro by IL-1 beta. NeuroReport 8:2107-2110.
5. Cooper JA, MacAuley A (1998) Potential positive and negative autoregulation of p60-src by intermolecular autophosphorylation. Proc Natl Acad Sci USA 85:4232-4236.
6. Denizot F, Lang R (1986) Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods 89:271-277.
7. Dinarello CA (1996) Biologic basis for interleukin-1 in disease. Blood 87:2095-2147.
8. Gardoni F, Caputi A, Cimino M, Pastorino L, Cattabeni F, Di Luca M (1998) Calcium/calmodulin-dependent protein kinase II is associated with NR2A/B subunits of NMDA receptor in postsynaptic densities. J Neurochem 71:1733-1741.
9. Gardoni F, Kamal A, Bellone C, Biessels GJ, Ramakers GM, Cattabeni F, Gispent WH, Di Luca M (2002) Effects of streptozotocin-diabetes on the hippocampal NMDA receptor complex in rats. J Neurochem 80:438-447.
10. Grazia de Simoni M, Imeri L (1998) Cytokine-neurotransmitter interactions in the brain. Biol Signals Receptors 7:33-44.
11. Grosshans DR, Browning MD (2001) Protein kinase C activation induces tyrosine phosphorylation of the NR2A and NR2B subunits of the NMDA receptor. J Neurochem 76:737-744.
12. Hagan P, Poole S, Bristow AF, Tilders F, Silverstein FS (1996) Intracerebral NMDA injection stimulates production of interleukin-1beta in perinatal rat brain. J Neurochem 67:2215-2218.
13. Hardingham GE, Fukunaga Y, Bading H (2002) Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 5:405-414.
14. Haughey NJ, Nath A, Mattson MP, Slevin JT, Geiger JD (2001) HIV-1 Tat through phosphorylation of NMDA receptors potentiates glutamate excitotoxicity. J Neurochem 78:457-467.
15. Hazeki K, Masuda N, Funami K, Sukenobu N, Matsumoto M, Akira S, Takeda K, Seya T, Hazeki O (2003) Toll-like receptor-mediated tyrosine phosphorylation of paxillin via MyD88-dependent and -independent pathways. Eur J Immunol 33:740-747.
16. Hollmann M, Heinemann S (1994) Cloned glutamate receptors. Annu Rev Neurosci 17:31-108.
17. Kohr G, Seeburg PH (1996) Subtype-specific regulation of recombinant NMDA receptor-channels by protein tyrosine kinases of the src family. J Physiol (Lond) 492:445-452.
18. Lau LF, Huganir RL (1995) Differential tyrosine phosphorylation of N-methyl-D-aspartate receptor subunits. J Biol Chem 270:20036-20041.
19. Leonard AS, Hell JW (1997) Cyclic AMP-dependent protein kinase and protein kinase C phosphorylate N-methyl-D-aspartate receptors at different sites. J Biol Chem 272:12107-12115.
20. Loddick SA, Rothwell NJ (1996) Neuroprotective effects of human recombinant interleukin-1 receptor antagonist in focal cerebral ischaemia in the rat. J Cereb Blood Flow Metab 16:932-940.
21. Lu WY, Xiong ZG, Lei S, Orser BA, Dudek E, Browning MD, MacDonald JF (1999) G-protein-coupled receptors act via protein kinase C and Src to regulate NMDA receptors. Nat Neurosci 2:331-338.
22. Manzerra P, Behrens MM, Canzoniero LM, Wang XQ, Heidinger V, Ichinose T, Yu SP, Choi DW (2001) Zinc induces a Src family kinase-mediated up-regulation of NMDA receptor activity and excitotoxicity. Proc Natl Acad Sci USA 98:11055-11061.
23. Moon IS, Apperson ML, Kennedy MB (1994) The major tyrosine-phosphorylated protein in the postsynaptic density fraction is N-methyl-D-aspartate receptor subunit 2B. Proc Natl Acad Sci USA 91:3954-3958.
24. Nakazawa T, Komai S, Tezuka T, Hisatsune C, Umemori H, Semba K, Mishina M, Manabe T, Yamamoto T (2001) Characterization of Fyn mediated tyrosine phosphorylation sites on GluR epsilon 2 (NR2B) subunit of the N-methyl-D-aspartate receptor. J Biol Chem 276:693-699.
25. Omkumar RV, Kiely MJ, Rosenstein AJ, Min KT, Kennedy MB (1996) Identification of a phosphorylation site for calcium/calmodulin-dependent protein kinase II in the NR2B subunit of the N-methyl-D-aspartate receptor. J Biol Chem 271:31670-31678.
26. Pringle AK, Niyadurupola N, Johns P, Anthony DC, Iannotti F (2001) Interleukin-1beta exacerbates hypoxia-induced neuronal damage, but attenuates toxicity produced by simulated ischaemia and excitotoxicity in rat organotypic hippocampal slice cultures. Neurosci Lett 305:29-32.
27. Rothwell NJ, Hopkins SJ (1995) Cytokines and the nervous system II: actions and mechanisms of action. Trends Neurosci 18:130-136.
28. Salter MW (1998) Src, N-methyl-D-aspartate (NMDA) receptors, and synaptic plasticity. Biochem Pharmacol 56:789-798.
29. Schneider H, Pitossi F, Balschun D, Wagner A, del Rey A, Besedovsky HO (1998) A neuromodulatory role of interleukin-1beta in the hippocampus. Proc Natl Acad Sci USA 95:7778-7783.
30. Strijbos PJ, Rothwell NJ (1995) Interleukin-1 beta attenuates excitatory amino acid-induced neurodegeneration in vitro: involvement of nerve growth factor. J Neurosci 15:3468-3474.
31. Taishi P, Bredow S, Guha-Thakurta N, Obal Jr F, Krueger JM (1997) Diurnal variations of interleukin-1 beta mRNA and beta-actin mRNA in rat brain. J Neuroimmunol 75:69-74.
32. Takagi N, Shinno K, Teves L, Bissoon N, Wallace MC, Gurd JW (1997) Transient ischemia differentially increases tyrosine phosphorylation of NMDA receptor subunits 2A and 2B. J Neurochem 69:1060-1065.
33. Takahashi S, Kapas L, Fang J, Seyer JM, Wang Y, Krueger JM (1996) An interleukin-1 receptor fragment inhibits spontaneous sleep and muramyl dipeptide-induced sleep in rabbits. Am J Physiol 271:R1O1-108.
34. Takasu MA, Dalva MB, Zigmond RE, Greenberg ME (2002) Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 295:491-495.
35. Vezzani A, Conti M, De Luigi A, Ravizza T, Moneta D, Marchesi F, De Simoni MG (1999) Interleukin-1beta immunoreactivity and microglia are enhanced in the rat hippocampus by focal kainate application: functional evidence for enhancement of electrographic seizures. J Neurosci 19:5054-5065.
36. Vezzani A, Moneta D, Conti M, Richichi C, Ravizza T, De Luigi A, De Simoni MG, Sperk G, Andell-Jonsson S, Lundkvist J, Iverfeldt K, Bartfai T (2000) Powerful anticonvulsant action of IL-1 receptor antagonist on intracerebral injection and astrocytic overexpression in mice. Proc Natl Acad Sci USA 97:11534-11539.
37. Viviani B, Corsini E, Binaglia M, Galli CL, Marinovich M (2001) Reactive oxygen species generated by glia are responsible for neuron death induced by human immunodeficiency virus-glycoprotein 120 in vitro. Neuroscience 107:51-58.
38. Wang YT, Salter MW (1994) Regulation of NMDA receptors by tyrosine kinases and phosphatases. Nature 369:233-235.
39. Yamasaki Y, Matsuura N, Shozuhara H, Onodera H, Itoyama Y, Kogure K (1995) Interleukin-1 as a pathogenetic mediator of ischemic brain damage in rats. Stroke 26:676-680.
40. Yu XM, Askalan R, Keil II GJ, Salter MW (1997) NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science 275:674-678.