Enhanced NMDA receptor tyrosine phosphorylation and increased brain injury following neonatal hypoxia-ischemia in mice with neuronal Fyn overexpression

Neurobiology of Disease

Volumn 51, Issue , 2013, Pages 113-119

  Knox, Renatta ^a,b   Zhao, Chong ^a   Miguel Perez, Dario ^a   Wang, Steven ^a   Yuan, Jinwei ^c   Ferriero, Donna ^a,b   Jiang, Xiangning ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ICON CLINICAL RESEARCH   (United States)

Author keywords

Fyn; Hypoxia ischemia; Neonatal brain; NR2B

Indexed keywords

CALPAIN; CRESYL VIOLET; DYE; IRON; MEMBRANE PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PROTEIN KINASE FYN; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN INJURY; BRAIN TISSUE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE FUNCTION; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MORTALITY; MOUSE; NERVE CELL; NERVE CELL NECROSIS; NEUROPATHOLOGY; NEWBORN; NONHUMAN; PERINATAL PERIOD; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SYNAPTIC MEMBRANE; TISSUE SECTION; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; HYPOXIA-ISCHEMIA, BRAIN; IMMUNOPRECIPITATION; MICE; MICE, TRANSGENIC; NEURONS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-FYN; RECEPTORS, N-METHYL-D-ASPARTATE; TYROSINE;

EID: 84872760247     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.10.024     Document Type: Article

References (42)

1. Atkinson E.A., et al. A physical interaction between the cell death protein Fas and the tyrosine kinase p59fynT. J. Biol. Chem. 1996, 271:5968-5971.
2. Boehm S.L., et al. Deletion of the fyn-kinase gene alters sensitivity to GABAergic drugs: dependence on beta2/beta3 GABAA receptor subunits. J. Pharmacol. Exp. Ther. 2004, 309:1154-1159.
3. Choi D.W. Ionic dependence of glutamate neurotoxicity. J. Neurosci. 1987, 7:369-379.
4. Choi U.B., et al. Effect of Src kinase phosphorylation on disordered C-terminal domain of N-methyl-d-aspartic acid (NMDA) receptor subunit GluN2B protein. J. Biol. Chem. 2011, 286:29904-29912.
5. Cuaycong M., et al. A novel approach to the study of hypoxia-ischemia-induced clinical and subclinical seizures in the neonatal rat. Dev. Neurosci. 2011, 33:241-250.
6. DeRidder M.N., et al. Traumatic mechanical injury to the hippocampus in vitro causes regional caspase-3 and calpain activation that is influenced by NMDA receptor subunit composition. Neurobiol. Dis. 2006, 22:165-176.
7. Du C.P., et al. Fyn kinases play a critical role in neuronal apoptosis induced by oxygen and glucose deprivation or amyloid-β peptide treatment. CNS Neurosci. Ther. 2012, 18:754-761.
8. Ferriero D.M. Neonatal brain injury. N. Engl. J. Med. 2004, 351:1985-1995.
9. Ferriero D.M., et al. Selective destruction of nitric oxide synthase neurons with quisqualate reduces damage after hypoxia-ischemia in the neonatal rat. Pediatr. Res. 1995, 38:912-918.
10. Fox C.J., et al. Tyrosine phosphorylation of the GluR2 subunit is required for long-term depression of synaptic efficacy in young animals in vivo. Hippocampus 2007, 17:600-605.
11. Goebel-Goody S.M., et al. Phospho-regulation of synaptic and extrasynaptic N-methyl-d-aspartate receptors in adult hippocampal slices. Neuroscience 2009, 158:1446-1459.
12. Gurd J.W., et al. Hypoxia-ischemia in perinatal rat brain induces the formation of a low molecular weight isoform of striatal enriched tyrosine phosphatase (STEP). J. Neurochem. 1999, 73:1990-1994.
13. Hayashi T., Huganir R.L. Tyrosine phosphorylation and regulation of the AMPA receptor by SRC family tyrosine kinases. J. Neurosci. 2004, 24:6152-6160.
14. Hisatsune C., et al. Phosphorylation-dependent interaction of the N-methyl-d-aspartate receptor epsilon 2 subunit with phosphatidylinositol 3-kinase. Genes Cells 1999, 4:657-666.
15. Ikonomidou C., et al. Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 1999, 283:70-74.
16. Jiang X., et al. Neonatal hypoxia-ischemia differentially upregulates MAGUKs and associated proteins in PSD-93-deficient mouse brain. Stroke 2003, 34:2958-2963.
17. Jiang X., et al. Activated Src kinases interact with the N-methyl-d-aspartate receptor after neonatal brain ischemia. Ann. Neurol. 2008, 63:632-641.
18. Jiang X., et al. Developmental localization of NMDA receptors, Src and MAP kinases in mouse brain. Neurosci. Lett. 2011, 503:215-219.
19. Jurd R., et al. Fyn kinase contributes to tyrosine phosphorylation of the GABA(A) receptor gamma2 subunit. Mol. Cell. Neurosci. 2010, 44:129-134.
20. Köhr G., Seeburg P.H. Subtype-specific regulation of recombinant NMDA receptor-channels by protein tyrosine kinases of the src family. J. Physiol. (Lond.) 1996, 492:445-452.
21. Kojima N., et al. Rescuing impairment of long-term potentiation in fyn-deficient mice by introducing Fyn transgene. Proc. Natl. Acad. Sci. U. S. A. 1997, 29:4761-4765.
22. Kojima N., et al. Higher seizure susceptibility and enhanced tyrosine phosphorylation of N-methyl-d-aspartate receptor subunit 2B in fyn transgenic mice. Learn. Mem. 1998, 5:429-445.
23. Lu Y.F., et al. Enhanced synaptic transmission and reduced threshold for LTP induction in fyn-transgenic mice. Eur. J. Neurosci. 1999, 11:75-82.
24. McDonald J.W., et al. MK-801 protects the neonatal brain from hypoxic-ischemic damage. Eur. J. Pharmacol. 1987, 140:359-361.
25. Nakazawa T., et al. Characterization of Fyn-mediated tyrosine phosphorylation sites on GluR epsilon 2 (NR2B) subunit of the N-methyl-d-aspartate receptor. J. Biol. Chem. 2001, 276:693-699.
26. Nakazawa T., et al. NR2B tyrosine phosphorylation modulates fear learning as well as amygdaloid synaptic plasticity. EMBO J. 2006, 25:2867-2877.
27. Nath R., et al. Non-erythroid alpha-spectrin breakdown by calpain and interleukin 1 beta-converting-enzyme-like protease(s) in apoptotic cells: contributory roles of both protease families in neuronal apoptosis. Biochem. J. 1996, 319:683-690.
28. Nath R., et al. Evidence for activation of caspase-3-like protease in excitotoxin- and hypoxia/hypoglycemia-injured neurons. J. Neurochem. 1998, 71:186-195.
29. Olney J.W. Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate. Science 1969, 164:719-721.
30. Olney J.W., et al. Cytotoxic effects of acidic and sulphur containing amino acids on the infant mouse central nervous system. Exp. Brain Res. 1971, 14:61-76.
31. Prybylowski K., et al. The synaptic localization of NR2B-containing NMDA receptors is controlled by interactions with PDZ proteins and AP-2. Neuron 2005, 47:845-857.
32. Rice J.E., et al. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol. 1981, 9:131-141.
33. Roche K.W., et al. Molecular determinants of NMDA receptor internalization. Nat. Neurosci. 2001, 4:794-802.
34. Rong Y., et al. Tyrosine phosphorylation of ionotropic glutamate receptors by Fyn or Src differentially modulates their susceptibility to calpain and enhances their binding to spectrin and PSD-95. J. Neurochem. 2001, 79:382-390.
35. Sheldon R.A., et al. Strain-related brain injury in neonatal mice subjected to hypoxia-ischemia. Brain Res. 1998, 810:114-122.
36. Takagi N., et al. The effect of transient global ischemia on the interaction of Src and Fyn with the N-methyl-D-aspartate receptor and postsynaptic densities: possible involvement of Src homology 2 domains. J. Cereb. Blood Flow Metab. 1999, 19:880-888.
37. Takagi N., et al. Transient ischemia enhances tyrosine phosphorylation and binding of the NMDA receptor to the Src homology 2 domain of phosphatidylinositol 3-kinase in the rat hippocampus. J. Neurochem. 2003, 84:67-76.
38. Vanderklish P.W., Bahr B.A. The pathogenic activation of calpain: a marker and mediator of cellular toxicity and disease states. Int. J. Exp. Pathol. 2000, 81:323-339.
39. Vexler Z.S., Ferriero D.M. Molecular and biochemical mechanisms of perinatal brain injury. Semin. Neonatol. 2001, 6:99-108.
40. Wang K. Calpain and caspase: can you tell the difference?. Trends Neurosci. 2000, 23:20-26.
41. Waxman E.A., Lynch D.R. N-methyl-d-aspartate receptor subtype mediated bidirectional control of p38 mitogen-activated protein kinase. J. Biol. Chem. 2005, 280:29322-29333.
42. Wu H., et al. Fyn-mediated phosphorylation of NR2B Tyr-1336 controls calpain-mediated NR2B cleavage in neurons and heterologous systems. J. Biol. Chem. 2007, 282:20075-20087.