CXCL12 inhibits expression of the NMDA receptor's NR2B subunit through a histone deacetylasedependent pathway contributing to neuronal survival

Cell Death and Disease

Volumn 1, Issue 4, 2010, Pages

  Nicolai, J ^a   Burbassi, S ^a   Rubin, J ^b   Meucci, O ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calcium; Cell death; Chemokine; CXCR4; Neuron

Indexed keywords

CALCIUM; CHEMOKINE RECEPTOR CXCR4; GLUTAMIC ACID; HISTONE DEACETYLASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; SYNAPSE RECEPTOR; CXCR4 PROTEIN, RAT; HISTONE DEACETYLASE INHIBITOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYLASPARTIC ACID; NEUROTOXIN; NEUROTRANSMITTER RECEPTOR; NR2B NMDA RECEPTOR; PROTEIN SUBUNIT; STROMAL CELL DERIVED FACTOR 1;

ANIMAL CELL; ARTICLE; BRAIN DEVELOPMENT; CELL SURVIVAL; CONTROLLED STUDY; EPIGENETICS; GENE CONTROL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STIMULATION; ANIMAL; CELL CULTURE; CELL NUCLEUS; CELL PROTECTION; CYTOLOGY; DOWN REGULATION; DRUG EFFECT; ENZYMOLOGY; METABOLISM; NERVE CELL; SIGNAL TRANSDUCTION; TIME;

ANIMALS; CELL NUCLEUS; CELL SURVIVAL; CELLS, CULTURED; CHEMOKINE CXCL12; CYTOPROTECTION; DOWN-REGULATION; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; N-METHYLASPARTATE; NEURONS; NEUROTOXINS; PROTEIN SUBUNITS; RATS; RECEPTORS, CXCR4; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, NEUROTRANSMITTER; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 79251637647     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2010.10     Document Type: Article

References (41)

1. Kaul M, Lipton SA. Mechanisms of neuronal injury and death in HIV-1 associated dementia. Curr HIV Res 2006;4:307-318. (Pubitemid 44027720)
2. Greenwood SM, Connolly CN. Dendritic and mitochondrial changes during glutamate excitotoxicity. Neuropharmacology 2007;53:891-898. (Pubitemid 350137396)
3. Waxman EA, Lynch DR. N-methyl-D-aspartate receptor subtypes: multiple roles in excitotoxicity and neurological disease. Neuroscientist 2005;11:37-49. (Pubitemid 40223089)
4. Wollmuth LP, Sobolevsky AI. Structure and gating of the glutamate receptor ion channel. Trends Neurosci 2004;27:321-328. (Pubitemid 38692413)
5. Burnashev N. Calcium permeability of glutamate-gated channels in the central nervous system. Curr Opin Neurobiol 1996;6:311-317. (Pubitemid 26235678)
6. Sattler R, Tymianski M. Molecular mechanisms of glutamate receptor-mediated excitotoxic neuronal cell death. Mol Neurobiol 2001;24:107-129. (Pubitemid 34066681)
7. Villmann C, Becker CM. On the hypes and falls in neuroprotection: targeting the NMDA receptor. Neuroscientist 2007;13:594-615. (Pubitemid 350077310)
8. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 1994;12:529-540. (Pubitemid 24100885)
9. Tovar KR, Westbrook GL. Mobile NMDA receptors at hippocampal synapses. Neuron 2002;34:255-264. (Pubitemid 34442568)
10. Miwa H, Fukaya M, Watabe AM, Watanabe M, Manabe T. Functional contributions of synaptically localized NR2B subunits of the NMDA receptor to synaptic transmission and long-term potentiation in the adult mouse CNS. J Physiol 2008;586:2539-2550. (Pubitemid 351689811)
11. Leveille F, El Gaamouch F, Gouix E, Lecocq M, Lobner D, Nicole O et al. Neuronal viability is controlled by a functional relation between synaptic and extrasynaptic NMDA receptors. FASEB J 2008;22:4258-4271.
12. Bading H, Ginty DD, Greenberg ME. Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 1993;260:181-186. (Pubitemid 23140883)
13. Hardingham GE, Fukunaga Y, Bading H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 2002;5:405-414. (Pubitemid 34454245)
14. Massey PV, Johnson BE, Moult PR, Auberson YP, Brown MW, Molnar E et al. Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J Neurosci 2004;24:7821-7828. (Pubitemid 39215685)
15. Ivanov A, Pellegrino C, Rama S, Dumalska I, Salyha Y, Ben-Ari Y et al. Opposing role of synaptic and extrasynaptic NMDA receptors in regulation of the extracellular signalregulated kinases (ERK) activity in cultured rat hippocampal neurons. J Physiol 2006;572(Part 3):789-798.
16. Li M, Ransohoff RM. Multiple roles of chemokine CXCL12 in the central nervous system: a migration from immunology to neurobiology. Prog Neurobiol 2008;84:116-131.
17. Bezzi P, Domercq M, Brambilla L, Galli R, Schols D, De Clercq E et al. CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nat Neurosci 2001;4:702-710. (Pubitemid 32595408)
18. Bhattacharyya BJ, Banisadr G, Jung H, Ren D, Cronshaw DG, Zou Y et al. The chemokine stromal cell-derived factor-1 regulates GABAergic inputs to neural progenitors in the postnatal dentate gyrus. J Neurosci 2008;28:6720-6730.
19. Khan MZ, Brandimarti R, Shimizu S, Nicolai J, Crowe E, Meucci O. The chemokine CXCL12 promotes survival of postmitotic neurons by regulating Rb protein. Cell Death Differ 2008;15:1663-1672.
20. Shimizu S, Khan MZ, Hippensteel RL, Parkar A, Raghupathi R, Meucci O. Role of the transcription factor E2F1 in CXCR4-mediated neurotoxicity and HIV neuropathology. Neurobiol Dis 2007;25:17-26. (Pubitemid 44765213)
21. Qiu Z, Ghosh A. A calcium-dependent switch in a CREST-BRG1 complex regulates activity-dependent gene expression. Neuron 2008;60:775-787.
22. Meucci O, Miller RJ. gp120-induced neurotoxicity in hippocampal pyramidal neuron cultures: protective action of TGF-beta1. J Neurosci 1996;16:4080-4088. (Pubitemid 26192404)
23. Oh SB, Endoh T, Simen AA, Ren D, Miller RJ. Regulation of calcium currents by chemokines and their receptors. J Neuroimmunol 2002;123:66-75. (Pubitemid 34195608)
24. Sattler R, Charlton MP, Hafner M, Tymianski M. Distinct influx pathways, not calcium load, determine neuronal vulnerability to calcium neurotoxicity. J Neurochem 1998;71:2349-2364. (Pubitemid 28531245)
25. Papadia S, Hardingham GE. The dichotomy of NMDA receptor signaling. Neuroscientist 2007;13:572-579. (Pubitemid 350077306)
26. Saha RN, Pahan K. HATs and HDACs in neurodegeneration: a tale of disconcerted acetylation homeostasis. Cell Death Differ 2006;13:539-550.
27. Burbassi S, Aloyo VJ, Simansky KJ, Meucci O. GTPgammaS incorporation in the rat brain: a study on mu-opioid receptors and CXCR4. J Neuroimmune Pharmacol 2008;3:26-34.
28. Sengupta R, Burbassi S, Shimizu S, Cappello S, Vallee RB, Rubin JB et al. Morphine increases brain levels of ferritin heavy chain leading to inhibition of CXCR4-mediated survival signaling in neurons. J Neurosci 2009;29:2534-2544.
29. Woerner BM, Warrington NM, Kung AL, Perry A, Rubin JB. Widespread CXCR4 activation in astrocytomas revealed by phospho-CXCR4-specific antibodies. Cancer Res 2005;65:11392-11399. (Pubitemid 41821696)
30. Lynch DR, Guttmann RP. NMDA receptor pharmacology: perspectives from molecular biology. Curr Drug Targets 2001;2:215-231. (Pubitemid 32821467)
31. Zhang SJ, Steijaert MN, Lau D, Schutz G, Delucinge-Vivier C, Descombes P et al. Decoding NMDA receptor signaling: identification of genomic programs specifying neuronal survival and death. Neuron 2007;53:549-562. (Pubitemid 46216756)
32. Kim MJ, Dunah AW, Wang YT, Sheng M. Differential roles of NR2A-and NR2B-containing NMDA receptors in Ras-ERK signaling and AMPA receptor trafficking. Neuron 2005;46:745-760. (Pubitemid 40733130)
33. Stocca G, Vicini S. Increased contribution of NR2A subunit to synaptic NMDA receptors in developing rat cortical neurons. J Physiol 1998;507(Part 1):13-24. (Pubitemid 28102672)
34. Bonni A, Brunet A, West AE, Datta SR, Takasu MA, Greenberg ME. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and-independent mechanisms. Science 1999;286:1358-1362.
35. Hardingham GE, Arnold FJ, Bading H. A calcium microdomain near NMDA receptors: on switch for ERK-dependent synapse-to-nucleus communication. Nat Neurosci 2001;4:565-566. (Pubitemid 32507368)
36. Miller RJ, Rostene W, Apartis E, Banisadr G, Biber K, Milligan ED et al. Chemokine action in the nervous system. J Neurosci 2008;28:11792-11795.
37. Melik-Parsadaniantz S, Rostene W. Chemokines and neuromodulation. J Neuroimmunol 2008;198:62-68.
38. Thomas GM, Huganir RL. MAPK cascade signalling and synaptic plasticity. Nat Rev Neurosci 2004;5:173-183. (Pubitemid 38252474)
39. Liu Y, Wong TP, Aarts M, Rooyakkers A, Liu L, Lai TW et al. NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo. J Neurosci 2007;27:2846-2857. (Pubitemid 46438991)
40. Langley B, D'Annibale MA, Suh K, Ayoub I, Tolhurst A, Bastan B et al. Pulse inhibition of histone deacetylases induces complete resistance to oxidative death in cortical neurons without toxicity and reveals a role for cytoplasmic p21 (waf1/cip1) in cell cycle-independent neuroprotection. J Neurosci 2008;28:163-176.
41. Salminen A, Tapiola T, Korhonen P, Suuronen T. Neuronal apoptosis induced by histone deacetylase inhibitors. Brain Res Mol Brain Res 1998;61:203-206. (Pubitemid 28511364)