Glutamate-induced NFκB activation in the retina

Investigative Ophthalmology and Visual Science

Volumn 50, Issue 2, 2009, Pages 917-925

  Fan, Wei ^a   Cooper, Nigel G F ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOCAMTIDE 2 RELATED INHIBITORY PEPTIDE; CALCIUM ION; EGTAZIC ACID; GLUTAMIC ACID; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITOR PROTEIN; MEMANTINE; TRANSCRIPTION FACTOR REL; UNCLASSIFIED DRUG; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; RELB PROTEIN, RAT; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CONTROLLED STUDY; EXPLANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RAT; RETINA; RETINA GANGLION CELL; SIGNAL TRANSDUCTION; ANIMAL; CULTURE TECHNIQUE; DRUG ANTAGONISM; DRUG EFFECT; FLUORESCENT ANTIBODY TECHNIQUE; GEL MOBILITY SHIFT ASSAY; METABOLISM; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL CULTURE TECHNIQUES; EGTAZIC ACID; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GLUTAMIC ACID; MEMANTINE; NF-KAPPA B; NF-KAPPA B P50 SUBUNIT; NF-KAPPA B P52 SUBUNIT; ORGAN CULTURE TECHNIQUES; PROTO-ONCOGENE PROTEINS C-REL; RATS; RATS, SPRAGUE-DAWLEY; RETINA; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB;

EID: 59449094331     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.08-2555     Document Type: Article

References (75)

1. Mattson MP, Camandola S. NF-κB in neuronal plasticity and neurodegenerative disorders. J Clin Invest. 2001;107:247-254.
2. Hayden MS, Ghosh S. Signaling to NF-κB. Genes Dev. 2004;18: 2195-2224.
3. Mattson MP, Culmsee C, Yu Z, Camandola S. Roles of nuclear factor κB in neuronal survival and plasticity. J Neurochem. 2000; 74:443-456.
4. de Erausquin GA, Hyrc K, Dorsey DA, et al. Nuclear translocation of nuclear transcription factor-kappa B by alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid receptors leads to transcription of p53 and cell death in dopaminergic neurons. Mol Pharmacol. 2003;63:784-790.
5. Pizzi M, Goffi F, Boroni F, et al. Opposing roles for NF-κB/Rel factors p65 and c-Rel in the modulation of neuron survival elicited by glutamate and interleukin-1β. J Biol Chem. 2002;277:20717-20723.
6. Osborne NN, Casson RJ, Wood JPM, Chidlow G, Graham M, Melena J. Retinal ischemia: mechanisms of damage and potential therapeutic strategies. Prog Retinal Eye Res. 2004;23:91-147.
7. Otori Y, Wei JY, Barnstable CJ. Neurotoxic effects of low doses of glutamate on purified rat retinal ganglion cells. Invest Ophthalmol Vis Sci. 1998;39:972-981.
8. Sucher NJ, Lipton SA, Dreyer EB. Molecular basis of glutamate toxicity in retinal ganglion cells. Vision Res. 1997;37:3483-3493.
9. Low HC, Gionfriddo JR, Madl JE. Assessment of glutamate loss from the ganglion cell layer of young DBA/2J mice with glaucoma. Am J Vet Res. 2006;67:302-309.
10. Hirooka K, Miyamoto O, Jinming P, et al. Neuroprotective effects of D-allose against retinal ischemia-reperfusion injury. Invest Ophthalmol Vis Sci. 2006;47:1653-1657.
11. Okuno T, Oku H, Sugiyama T, Ikeda T. Glutamate level in optic nerve head is increased by artificial elevation of intraocular pressure in rabbits. Exp Eye Res. 2006;82:465-470.
12. Wakabayashi Y, Yagihashi T, Kezuka J, Muramatsu D, Usui M, Iwasaki T. Glutamate levels in aqueous humor of patients with retinal artery occlusion. Retina. 2006;26:432-436.
13. Uckermann O, Vargova L, Ulbricht E, et al. Glutamate-evoked alterations of glial and neuronal cell morphology in the guinea pig retina. J Neurosci. 2004;24:10149-10158.
14. Harada T, Harada C, Watanabe M, et al. Functions of the two glutamate transporters GLAST and GLT-1 in the retina. Proc Natl Acad Sci U S A. 1998;95:4663-4666.
15. Lagreze WA, Knorle R, Bach M, Feuerstein TJ. Memantine is neuroprotective in a rat model of pressure-induced retinal ischemia. Invest Ophthalmol Vis Sci. 1998;39:1063-1066.
16. Romano C, Price MT, Almli T, Olney JW. Excitotoxic neurodegeneration induced by deprivation of oxygen and glucose in isolated retina. Invest Ophthalmol Vis Sci. 1998;39:416-423.
17. Gorovits R, Avidan N, Avisar N, Shaked I, Vardimon L. Glutamine synthetase protects against neuronal degeneration in injured retinal tissue. Proc Natl Acad Sci U S A. 1997;94:7024-7029.
18. Louzada-Junior P, Dias JJ, Santos WF, Lachat JJ, Bradford HF, Coutinho-Netto J. Glutamate release in experimental ischaemia of the retina: an approach using microdialysis. J Neurochem. 1992; 59:358-363.
19. Neal MJ, Cunningham JR, Hutson PH, Hogg J. Effects of ischaemia on neurotransmitter release from the isolated retina. J Neurochem. 1994;62:1025-1033.
20. Joo CK, Choi JS, Ko HW, et al. Necrosis and apoptosis after retinal ischemia: involvement of NMDA-mediated excitotoxicity and p53. Invest Ophthalmol Vis Sci. 1999;40:713-720.
21. Guerrini L, Blasi F, Denis-Donini S. Synaptic activation of NF-κB by glutamate in cerebellar granule neurons in vitro. Proc Natl Acad Sci U S A. 1995;92:9077-9081.
22. Kaltschmidt C, Kaltschmidt B, Baeuerle PA. Stimulation of ionotropic glutamate receptors activates transcription factor NF-κB in primary neurons 72. Proc Natl Acad Sci U S A. 1995;92:9618-9622.
23. Scholzke MN, Potrovita I, Subramaniam S, Prinz S, Schwaninger M. Glutamate activates NF-κB through calpain in neurons. Eur J Neurosci. 2003;18:3305-3310.
24. Kaltschmidt B, Widera D, Kaltschmidt C. Signaling via NF-[kappa]B in the nervous system. Biochim Biophys Acta. 2005;1745:287-299.
25. Schneider A, Martin-Villalba A, Weih F, Vogel J, Wirth T, Schwaninger M. NF-κB is activated and promotes cell death in focal cerebral ischemia. Nat Med. 1999;5:554 -559.
26. Schwaninger M, Inta I, Herrmann O. NF-κB signalling in cerebral ischaemia. Biochem Soc Trans. 2006;34:1291-1294.
27. Wang J, Jiang S, Kwong JM, Sanchez RN, Sadun AA, Lam TT. Nuclear factor-κB p65 and upregulation of interleukin-6 in retinal ischemia/reperfusion injury in rats. Brain Res. 2006;1081:211-218.
28. Kitaoka Y, Kumai T, Kitaoka Y, et al. Nuclear factor-kappa B p65 in NMDA-induced retinal neurotoxicity. Mol Brain Res. 2004;131: 8-16.
29. Kitaoka Y, Munemasa Y, Nakazawa T, Ueno S. NMDA-induced interleukin-1beta expression is mediated by nuclear factor-kappa B p65 in the retina. Brain Res. 2007;1142:247-255.
30. Chen YG, Zhang C, Chiang SK, Wu T, Tso MO. Increased nuclear factor-kappa B p65 immunoreactivity following retinal ischemia and reperfusion injury in mice. J Neurosci Res. 2003;72:125-131.
31. Zheng L, Howell SJ, Hatala DA, Huang K, Kern TS. Salicylate-based anti-inflammatory drugs inhibit the early lesion of diabetic retinopathy. Diabetes. 2007;56:337-345.
32. Choi JS, Kim J, Kim DH, et al. Failure to activate NF-[kappa]B promotes apoptosis of retinal ganglion cells following optic nerve transection. Brain Res. 2000;883:60-68.
33. Choi JS, Sungjoo KY, Joo CK. NF-kappa B activation following optic nerve transection. Korean J Ophthalmol. 1998;12:19 -24.
34. 2+-mediated activation of c-Jun N-terminal kinase and nuclear factor kappa B by NMDA in cortical cell cultures. J Neurochem. 1998;71:1390-1395.
35. Meffert MK, Chang JM, Wiltgen BJ, Fanselow MS, Baltimore D. NF-kappa B functions in synaptic signaling and behavior. Nat Neurosci. 2003;6:1072-1078.
36. Cuschieri J, Bulger E, Garcia I, Jelacic S, Maier RV. Calcium/ calmodulin-dependent kinase II is required for platelet-activating factor priming. Shock. 2005;23:99 -106.
37. Mishra S, Mishra JP, Gee K, McManus DC, LaCasse EC, Kumar A. Distinct role of calmodulin and calmodulin-dependent protein kinase-II in lipopolysaccharide and tumor necrosis factor-alpha-mediated suppression of apoptosis and antiapoptotic c-IAP2 gene expression in human monocytic cells. J Biol Chem. 2005;280: 37536-37546.
38. 2+/calmodulin- dependent protein kinase II is required for microcystin-induced apoptosis. J Biol Chem. 2002;277:2804-2811.
39. Hajimohammadreza I, Probert AW, Coughenour LL, et al. A specific inhibitor of calcium/calmodulin-dependent protein kinase-II provides neuroprotection against NMDA- and hypoxia/hypoglycemia-induced cell death. J Neurosci. 1995;15:4093-4101.
40. Takano H, Fukushi H, Morishima Y, Shirasaki Y. Calmodulin and calmodulin-dependent kinase II mediate neuronal cell death induced by depolarization. Brain Res. 2003;962:41-47.
41. Wright SC, Schellenberger U, Ji L, Wang H, Larrick JW. Calmodulin-dependent protein kinase II mediates signal transduction in apoptosis. FASEB J. 1997;11:843-849.
42. Laabich A, Cooper NG. Neuroprotective effect of AIP on N-methyl-D-aspartate-induced cell death in retinal neurons. Brain Res Mol Brain Res. 2000;85:32-40.
43. Caffe AR, Visser H, Jansen HG, Sanyal S. Histotypic differentiation of neonatal mouse retina in organ culture. Curr Eye Res. 1989;8: 1083-1092.
44. McKernan DP, Caplis C, Donovan M, O'Brien CJ, Cotter TG. Age-dependent susceptibility of the retinal ganglion cell layer to cell death. Invest Ophthalmol Vis Sci. 2006;47:807-814.
45. Chen TA, Yang F, Cole GM, Chan SO. Inhibition of caspase-3-like activity reduces glutamate induced cell death in adult rat retina. Brain Res. 2001;904:177-188.
46. Rocha M, Martins RAP, Linden R. Activation of NMDA receptors protects against glutamate neurotoxicity in the retina: evidence for the involvement of neurotrophins. Brain Res. 1999;827:79-92.
47. Barres BA, Silverstein BE, Corey DP, Chun LL. Immunological, morphological, and electrophysiological variation among retinal ganglion cells purified by panning. Neuron. 1988;1:791-803.
48. Meyer-Franke A, Kaplan MR, Pfrieger FW, Barres BA. Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron. 1995;15:805-819.
49. Fan W, Li X, Cooper NGF. CaMKIIαB mediates a survival response in retinal ganglion cells subjected to a glutamate stimulus. Invest Ophthalmol Vis Sci. 2007;48:3854-3863.
50. Kaltschmidt C, Kaltschmidt B, Neumann H, Wekerle H, Baeuerle PA. Constitutive NF-kappa B activity in neurons. Mol Cell Biol. 1994;14:3981-3992.
51. O'Neill LA, Kaltschmidt C. NF-kappa B: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci. 1997; 20:252-258.
52. Bhakar AL, Tannis LL, Zeindler C, et al. Constitutive nuclear factorkappa B activity is required for central neuron survival. J Neurosci. 2002;22:8466-8475.
53. Dobrzanski P, Ryseck RP, Bravo R. Differential interactions of Rel-NF-kappa B complexes with I kappa B alpha determine pools of constitutive and inducible NF-kappa B activity. EMBO J. 1994; 13:4608-4616.
54. Lernbecher T, Kistler B, Wirth T. Two distinct mechanisms contribute to the constitutive activation of RelB in lymphoid cells. EMBO J. 1994;13:4060-4069.
55. Lernbecher T, Muller U, Wirth T. Distinct NF-kappa B/Rel transcription factors are responsible for tissue-specific and inducible gene activation. Nature. 1993;365:767-770.
56. Weih F, Carrasco D, Durham SK, et al. Multiorgan inflammation and hematopoietic abnormalities in mice with a targeted disruption of RelB, a member of the NF-[kappa]B/Rel family. Cell. 1995; 80:331-340.
57. Weih F, Durham SK, Barton DS, Sha WC, Baltimore D, Bravo R. p50-NF-kappa B complexes partially compensate for the absence of RelB: severely increased pathology in p50-/-/RelB-/- double-knockout mice. J Exp Med. 1997;185:1359-1370.
58. Massa PT, Aleyasin H, Park DS, Mao X, Barger SW. NFκB in neurons? The uncertainty principle in neurobiology. J Neurochem. 2006;97:607-618.
59. Streilein JW. Immune privilege as the result of local tissue barriers and immunosuppressive microenvironments. Curr Opin Immunol. 1993;5:428-432.
60. Shen W, Zhang C, Zhang G. Nuclear factor κB activation is mediated by NMDA and non-NMDA receptor and L-type voltage-gated Ca(2+) channel following severe global ischemia in rat hippocampus. Brain Res. 2002;933:23-30.
61. Ishige K, Tanaka M, Arakawa M, Saito H, Ito Y. Distinct nuclear factor-κB/Rel proteins have opposing modulatory effects in glutamate-induced cell death in HT22 cells. Neurochem Int. 2005;47: 545-555.
62. Cruise L, Ho LK, Veitch K, Fuller G, Morris BJ. Kainate receptors activate NF-κB via MAP kinase in striatal neurones. Neuroreport. 2000;11:395-398.
63. Lilienbaum A, Israel A. From calcium to NF-κB signaling pathways in neurons. Mol Cell Biol. 2003;23:2680-2698.
64. Hughes K, Edin S, Antonsson A, Grundstrom T. Calmodulin-dependent kinase II mediates T cell receptor/CD3- and phorbol esterinduced activation of IκB kinase. J Biol Chem. 2001;276:36008-36013.
65. Liu AM, Wong YH. Activation of nuclear factor κB by somatostatin type 2 receptor in pancreatic acinar AR42J cells involves Gα14 and multiple signaling components: a mechanism requiring protein kinase C, calmodulin-dependent kinase II, ERK, and c-Src. J Biol Chem. 2005;280:34617-34625.
66. Grilli M, Memo M. Possible role of NF-κB and p53 in the glutamate-induced pro-apoptotic neuronal pathway. Cell Death Differ. 1999; 6:22-27.
67. Qin ZH, Chen RW, Wang Y, Nakai M, Chuang DM, Chase TN. Nuclear factor kappa B nuclear translocation upregulates c-Myc and p53 expression during NMDA receptor-mediated apoptosis in rat striatum. J Neurosci. 1999;19:4023-4033.
68. Chen C, Edelstein LC, Gelinas C. The Rel/NF-kappa B family directly activates expression of the apoptosis inhibitor Bcl-xL. Mol Cell Biol. 2000;20:2687-2695.
69. Grumont RJ, Rourke IJ, Gerondakis S. Rel-dependent induction of A1 transcription is required to protect B cells from antigen receptor ligation-induced apoptosis. Genes Dev. 1999;13:400-411.
70. Zong WX, Edelstein LC, Chen C, Bash J, Gelinas C. The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-κB that blocks TNFα-induced apoptosis. Genes Dev. 1999;13:382-387.
71. Bernard D, Quatannens B, Begue A, Vandenbunder B, Abbadie C. Antiproliferative and antiapoptotic effects of cRel may occur within the same cells via the up-regulation of manganese superoxide dismutase. Cancer Res. 2001;61:2656-2664.
72. Qiu J, Grafe MR, Schmura SM, et al. Differential NF-κB regulation of bcl-x gene expression in hippocampus and basal forebrain in response to hypoxia. J Neurosci Res. 2001;64:223-234.
73. Pizzi M, Sarnico I, Boroni F, Benetti A, Benarese M, Spano PF. Inhibition of IκBα phosphorylation prevents glutamate-induced NF-κB activation and neuronal cell death. Acta Neurochir Suppl. 2005;93:59-63.
74. Pizzi M, Spano P. Distinct roles of diverse nuclear factor-[kappa]B complexes in neuropathological mechanisms. Eur J Pharmacol. 2006;545:22-28.
75. Charles I, Khalyfa A, Kumar DM, et al. Serum deprivation induces apoptotic cell death of transformed rat retinal ganglion cells via mitochondrial signaling pathways. Invest Ophthalmol Vis Sci. 2005;46:1330-1338.