NR2B phosphorylation at tyrosine 1472 contributes to brain injury in a rodent model of neonatal hypoxia-ischemia

Stroke

Volumn 45, Issue 10, 2014, Pages 3040-3047

  Knox, Renatta ^a,b   Brennan Minnella, Angela M ^a,b   Lu, Fuxin ^a   Yang, Diana ^a   Nakazawa, Takanobu ^c   Yamamoto, Tadashi ^c   Swanson, Raymond A ^a,b   Ferriero, Donna M ^a,b   Jiang, Xiangning ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

brain; Fyn tyrosine kinase; hypoxia ischemia; NR2B NMDA receptor

Indexed keywords

CALCIUM; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PHENYLALANINE; PROTEIN KINASE FYN; PROTEIN P47; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SUPEROXIDE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NR2B NMDA RECEPTOR; TYROSINE;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BRAIN CELL; BRAIN DAMAGE; BRAIN INJURY; CONTROLLED STUDY; ENZYME ACTIVITY; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; DISEASE MODEL; FLUORESCENT ANTIBODY TECHNIQUE; GENE TARGETING; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; PHOSPHORYLATION;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE; GENE KNOCK-IN TECHNIQUES; HYPOXIA-ISCHEMIA, BRAIN; IMMUNOPRECIPITATION; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; PHOSPHORYLATION; RECEPTORS, N-METHYL-D-ASPARTATE; TYROSINE;

EID: 84922480115     PISSN: 00392499     EISSN: 15244628     Source Type: Journal    
DOI: 10.1161/STROKEAHA.114.006170     Document Type: Article

References (25)

1. Ferriero DM. Neonatal brain injury. N Engl J Med. 2004;351:1985-1995.
2. Jiang X, Mu D, Biran V, Faustino J, Chang S, Rincón CM, et al. Activated Src kinases interact with the N-methyl-D-aspartate receptor after neonatal brain ischemia. Ann Neurol. 2008;63:632-641.
3. Knox R, Zhao C, Miguel-Perez D, Wang S, Yuan J, Ferriero D, et al. Enhanced NMDA receptor tyrosine phosphorylation and increased brain injury following neonatal hypoxia-ischemia in mice with neuronal Fyn overexpression. Neurobiol Dis. 2013;51:113-119.
4. Nakazawa T, Komai S, Tezuka T, Hisatsune C, Umemori H, Semba K, 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.
5. Zhang F, Guo A, Liu C, Comb M, Hu B. Phosphorylation and assembly of glutamate receptors after brain ischemia. Stroke. 2013;44:170-176.
6. Gurd JW, Bissoon N, Beesley PW, Nakazawa T, Yamamoto T, Vannucci SJ. Differential effects of hypoxia-ischemia on subunit expression and tyrosine phosphorylation of the NMDA receptor in 7-and 21-day-old rats. J Neurochem. 2002;82:848-856.
7. Rostas JA, Brent VA, Voss K, Errington ML, Bliss TV, Gurd JW. Enhanced tyrosine phosphorylation of the 2B subunit of the N-methyl-D-aspartate receptor in long-term potentiation. Proc Natl Acad Sci U S A. 1996;93:10452-10456.
8. Nakazawa T, Komai S, Watabe AM, Kiyama Y, Fukaya M, Arima-Yoshida F, et al. NR2B tyrosine phosphorylation modulates fear learning as well as amygdaloid synaptic plasticity. EMBO J. 2006;25:2867-2877.
9. Prybylowski K, Chang K, Sans N, Kan L, Vicini S, Wenthold RJ. The synaptic localization of NR2B-containing NMDA receptors is controlled by interactions with PDZ proteins and AP-2. Neuron. 2005;47:845-857.
10. Goebel-Goody SM, Davies KD, Alvestad Linger RM, Freund RK, Browning MD. Phospho-regulation of synaptic and extrasynaptic N-methyl-d-aspartate receptors in adult hippocampal slices. Neuroscience. 2009;158:1446-1459.
11. Matsumura S, Kunori S, Mabuchi T, Katano T, Nakazawa T, Abe T, et al. Impairment of CaMKII activation and attenuation of neuropathic pain in mice lacking NR2B phosphorylated at Tyr1472. Eur J Neurosci. 2010;32:798-810.
12. Brennan AM, Suh SW, Won SJ, Narasimhan P, Kauppinen TM, Lee H, et al. NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation. Nat Neurosci. 2009;12:857-863.
13. Girouard H, Wang G, Gallo EF, Anrather J, Zhou P, Pickel VM, et al. NMDA receptor activation increases free radical production through nitric oxide and NOX2. J Neurosci. 2009;29:2545-2552.
14. Brennan AM, Shen Y, Swanson RA. Phosphoinositide 3-kinase couples NMDA receptors to superoxide release in excitotoxic neuronal death. Cell Death Dis. 2013;4:e580.
15. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev. 2007;87:245-313.
16. Sheldon RA, Sedik C, Ferriero DM. Strain-related brain injury in neonatal mice subjected to hypoxia-ischemia. Brain Res. 1998;810:114-122.
17. Lu Q, Wainwright MS, Harris VA, Aggarwal S, Hou Y, Rau T, et al. Increased NADPH oxidase-derived superoxide is involved in the neuronal cell death induced by hypoxia-ischemia in neonatal hippocampal slice cultures. Free Radic Biol Med. 2012;53:1139-1151.
18. Doverhag C, Keller M, Karlsson A, Hedtjarn M, Nilsson U, Kapeller E, et al. Pharmacological and genetic inhibition of NADPH oxidase does not reduce brain damage in different models of perinatal brain injury in newborn mice. Neurobiol Dis. 2008;31:133-144.
19. Kaindl AM, Degos V, Peineau S, Gouadon E, Chhor V, Loron G, et al. Activation of microglial N-methyl-D-aspartate receptors triggers inflammation and neuronal cell death in the developing and mature brain. Ann Neurol. 2012;72:536-549.
20. Hisatsune C, Umemori H, Mishina M, Yamamoto T. Phosphorylationdependent interaction of the N-methyl-D-aspartate receptor epsilon 2 subunit with phosphatidylinositol 3-kinase. Genes Cells. 1999;4:657-666.
21. Jiang X, Knox R, Pathipati P, Ferriero D. Developmental localization of NMDA receptors, Src and MAP kinases in mouse brain. Neurosci Lett. 2011;503:215-219.
22. Hardingham GE, Bading H. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci. 2010;11:682-696.
23. Papouin T, Ladépêche L, Ruel J, Sacchi S, Labasque M, Hanini M, et al. Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists. Cell. 2012;150:633-646.
24. Wroge CM, Hogins J, Eisenman L, Mennerick S. Synaptic NMDA receptors mediate hypoxic excitotoxic death. J Neurosci. 2012;32:6732-6742.
25. Martel MA, Ryan TJ, Bell KF, Fowler JH, McMahon A, Al-Mubarak B, et al. The subtype of GluN2 C-terminal domain determines the response to excitotoxic insults. Neuron. 2012;74:543-556.