Synaptic plasticity in the hippocampus shows resistance to acute ethanol exposure in transgenic mice with astrocyte-targeted enhanced CCL2 expression

Neuropharmacology

Volumn 67, Issue , 2013, Pages 115-125

  Bray, Jennifer G ^a   Reyes, Kenneth C ^a   Roberts, Amanda J ^a   Ransohoff, Richard M ^b   Gruol, Donna L ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

Author keywords

CCL2; Chemokine; Electrophysiology; Hippocampal slice; Long term potentiation; Synaptic plasticity

Indexed keywords

ALCOHOL; MONOCYTE CHEMOTACTIC PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN DEPTH RECORDING; BRAIN LEVEL; BRAIN SLICE; CONDITIONING; CONTROLLED STUDY; FEAR; FEMALE; HIPPOCAMPUS; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE;

ANIMALS; ASTROCYTES; CHEMOKINE CCL2; ETHANOL; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONAL PLASTICITY; SYNAPSES;

EID: 84873386607     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.11.007     Document Type: Article

References (75)

1. C. Allgaier Ethanol sensitivity of NMDA receptors Neurochem. Int. 41 2002 377 382
2. E. Ambrosini, and F. Aloisi Chemokines and glial cells: a complex network in the central nervous system Neurochem. Res. 29 2004 1017 1038
3. C. Bertollini, D. Ragozzino, C. Gross, C. Limatola, and F. Eusebi Fractalkine/CX3CL1 depresses central synaptic transmission in mouse hippocampal slices Neuropharmacology 51 2006 816 821
4. Y.A. Blednov, S.E. Bergeson, D. Walker, V.M. Ferreira, W.A. Kuziel, and R.A. Harris Perturbation of chemokine networks by gene deletion alters the reinforcing actions of ethanol Behav. Brain Res. 165 2005 110 125
5. R.D. Blitzer, O. Gil, and E.M. Landau Long-term potentiation in rat hippocampus is inhibited by low concentrations of ethanol Brain Res. 537 1990 203 208
6. V. Bruno, A. Copani, G. Besong, G. Scoto, and F. Nicoletti Neuroprotective activity of chemokines against N-methyl-D-aspartate or beta-amyloid-induced toxicity in culture Eur. J. Pharmacol. 399 2000 117 121
7. A.E. Cardona, M. Li, L. Liu, C. Savarin, and R.M. Ransohoff Chemokines in and out of the central nervous system: much more than chemotaxis and inflammation J. Leukoc. Biol. 84 2008 587 594
8. L. Cartier, O. Hartley, M. Dubois-Dauphin, and K.H. Krause Chemokine receptors in the central nervous system: role in brain inflammation and neurodegenerative diseases Brain Res. Brain Res. Rev. 48 2005 16 42
9. A. Celerier, R. Ognard, L. Decorte, and D. Beracochea Deficits of spatial and non-spatial memory and of auditory fear conditioning following anterior thalamic lesions in mice: comparison with chronic alcohol consumption Eur. J. Neurosci. 12 2000 2575 2584
10. J. Cho, and D.L. Gruol The chemokine CCL2 activates p38 mitogen-activated protein kinase pathway in cultured rat hippocampal cells J. Neuroimmunol. 199 2008 94 103
11. G. Conductier, N. Blondeau, A. Guyon, J.L. Nahon, and C. Rovere The role of monocyte chemoattractant protein MCP1/CCL2 in neuroinflammatory diseases J. Neuroimmunol. 224 2010 93 100
12. F.T. Crews, R. Bechara, L.A. Brown, D.M. Guidot, P. Mandrekar, S. Oak, L. Qin, G. Szabo, M. Wheeler, and J. Zou Cytokines and alcohol Alcohol Clin. Exp. Res. 30 2006 720 730
13. A.H. de Haas, H.R. van Weering, E.K. de Jong, H.W. Boddeke, and K.P. Biber Neuronal chemokines: versatile messengers in central nervous system cell interaction Mol. Neurobiol. 36 2007 137 151
14. M.A. Erickson, L.A. Maramara, and J. Lisman A single brief burst induces GluR1-dependent associative short-term potentiation: a potential mechanism for short-term memory J. Cogn. Neurosci. 22 2010 2530 2540
15. E.A. Eugenin, T.G. D'Aversa, L. Lopez, T.M. Calderon, and J.W. Berman MCP-1 (CCL2) protects human neurons and astrocytes from NMDA or HIV-tat-induced apoptosis J. Neurochem. 85 2003 1299 1311
16. G. Flora, H. Pu, Y.W. Lee, R. Ravikumar, A. Nath, B. Hennig, and M. Toborek Proinflammatory synergism of ethanol and HIV-1 Tat protein in brain tissue Exp. Neurol. 191 2005 2 12
17. A. Flugel, G. Hager, A. Horvat, C. Spitzer, G.M. Singer, M.B. Graeber, G.W. Kreutzberg, and F.W. Schwaiger Neuronal MCP-1 expression in response to remote nerve injury J. Cereb. Blood Flow Metab. 21 2001 69 76
18. D. Galimberti, N. Schoonenboom, P. Scheltens, C. Fenoglio, F. Bouwman, E. Venturelli, I. Guidi, M.A. Blankenstein, N. Bresolin, and E. Scarpini Intrathecal chemokine synthesis in mild cognitive impairment and Alzheimer disease Arch. Neurol. 63 2006 538 543
19. B. Givens, and K. McMahon Ethanol suppresses the induction of long-term potentiation in vivo Brain Res. 688 1995 27 33
20. T.J. Gould Ethanol disrupts fear conditioning in C57BL/6 mice J. Psychopharmacol. 17 2003 77 81
21. D. Gulick, and T.J. Gould Acute ethanol has biphasic effects on short- and long-term memory in both foreground and background contextual fear conditioning in C57BL/6 mice Alcohol Clin. Exp. Res. 31 2007 1528 1537
22. J.K. Harrison, Y. Jiang, S. Chen, Y. Xia, D. Maciejewski, R.K. McNamara, W.J. Streit, M.N. Salafranca, S. Adhikari, D.A. Thompson, P. Botti, K.B. Bacon, and L. Feng Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia Proc. Natl. Acad. Sci. U. S. A. 95 1998 10896 10901
23. J. He, and F.T. Crews Increased MCP-1 and microglia in various regions of the human alcoholic brain Exp. Neurol. 210 2008 349 358
24. D. Huang, M. Tani, J. Wang, Y. Han, T.T. He, J. Weaver, I.F. Charo, V.K. Tuohy, B.J. Rollins, and R.M. Ransohoff Pertussis toxin-induced reversible encephalopathy dependent on monocyte chemoattractant protein-1 overexpression in mice J. Neurosci. 22 2002 10633 10642
25. D. Huang, J. Wujek, G. Kidd, T.T. He, A. Cardona, M.E. Sasse, E.J. Stein, J. Kish, M. Tani, I.F. Charo, A.E. Proudfoot, B.J. Rollins, T. Handel, and R.M. Ransohoff Chronic expression of monocyte chemoattractant protein-1 in the central nervous system causes delayed encephalopathy and impaired microglial function in mice FASEB J. 19 2005 761 772
26. K. Ishizuka, T. Kimura, R. Igata-yi, S. Katsuragi, J. Takamatsu, and T. Miyakawa Identification of monocyte chemoattractant protein-1 in senile plaques and reactive microglia of Alzheimer's disease Psychiatry Clin. Neurosci. 51 1997 135 138
27. Y. Izumi, K. Nagashima, K. Murayama, and C.F. Zorumski Acute effects of ethanol on hippocampal long-term potentiation and long-term depression are mediated by different mechanisms Neuroscience 136 2005 509 517
28. H. Jung, P.T. Toth, F.A. White, and R.J. Miller Monocyte chemoattractant protein-1 functions as a neuromodulator in dorsal root ganglia neurons J. Neurochem. 104 2008 254 263
29. T. Kiyota, M. Yamamoto, H. Xiong, M.P. Lambert, W.L. Klein, H.E. Gendelman, R.M. Ransohoff, and T. Ikezu CCL2 accelerates microglia-mediated Abeta oligomer formation and progression of neurocognitive dysfunction PLoS One 4 2009 e6197
30. C.F. Landry, G.O. Ivy, and I.R. Brown Developmental expression of glial fibrillary acidic protein mRNA in the rat brain analyzed by in situ hybridization J. Neurosci. Res. 25 1990 194 203
31. J. Larson, D. Wong, and G. Lynch Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation Brain Res. 368 1986 347 350
32. C. Lauro, A.S. Di, R. Cipriani, F. Sobrero, L. Antonilli, V. Brusadin, D. Ragozzino, and C. Limatola Activity of adenosine receptors type 1 is required for CX3CL1-mediated neuroprotection and neuromodulation in hippocampal neurons J. Immunol. 180 2008 7590 7596
33. S.A. Lewis, and N.J. Cowan Temporal expression of mouse glial fibrillary acidic protein mRNA studied by a rapid in situ hybridization procedure J. Neurochem. 45 1985 913 919
34. C. Limatola, A. Giovannelli, L. Maggi, D. Ragozzino, L. Castellani, M.T. Ciotti, F. Vacca, D. Mercanti, A. Santoni, and F. Eusebi SDF-1alpha-mediated modulation of synaptic transmission in rat cerebellum Eur. J. Neurosci. 12 2000 2497 2504
35. J. Losy, and J. Zaremba Monocyte chemoattractant protein-1 is increased in the cerebrospinal fluid of patients with ischemic stroke Stroke 32 2001 2695 2696
36. S.F. Logue, R. Paylor, and J.M. Wehner Hippocampal lesions cause learning deficits in inbred mice in the Morris water maze and conditioned-fear task Behav. Neurosci. 111 1997 104 113
37. D.M. Lovinger, G. White, and F.F. Weight Ethanol inhibits NMDA-activated ion current in hippocampal neurons Science 243 1989 1721 1724
38. M.A. Lynch Long-term potentiation and memory Physiol. Rev. 84 2004 87 136
39. J.L. Madrigal, J.C. Leza, P. Polak, S. Kalinin, and D.L. Feinstein Astrocyte-derived MCP-1 mediates neuroprotective effects of noradrenaline J. Neurosci. 29 2009 263 267
40. J.L. Madrigal, B. Garcia-Bueno, A.E. Hinojosa, P. Polak, D.L. Feinstein, and J.C. Leza Regulation of MCP-1 production in brain by stress and noradrenaline-modulating drugs J. Neurochem. 113 2010 543 551
41. D.J. Mahad, and R.M. Ransohoff The role of MCP-1 (CCL2) and CCR2 in multiple sclerosis and experimental autoimmune encephalomyelitis (EAE) Semin. Immunol. 15 2003 23 32
42. S.J. Martin, P.D. Grimwood, and R.G. Morris Synaptic plasticity and memory: an evaluation of the hypothesis Annu. Rev. Neurosci. 23 2000 649 711
43. D.B. Matthews, and J.R. Silvers The use of acute ethanol administration as a tool to investigate multiple memory systems Neurobiol. Learn. Mem. 82 2004 299 308
44. B.A. McCool Ethanol modulation of synaptic plasticity Neuropharmacology 61 2011 1097 1108
45. C. McManus, J.W. Berman, F.M. Brett, H. Staunton, M. Farrell, and C.F. Brosnan MCP-1, MCP-2 and MCP-3 expression in multiple sclerosis lesions: an immunohistochemical and in situ hybridization study J. Neuroimmunol. 86 1998 20 29
46. K.R. Melia, A.E. Ryabinin, K.P. Corodimas, M.C. Wilson, and J.E. LeDoux Hippocampal-dependent learning and experience-dependent activation of the hippocampus are preferentially disrupted by ethanol Neuroscience 74 1996 313 322
47. S.Z. Meng, A. Oka, and S. Takashima Developmental expression of monocyte chemoattractant protein-1 in the human cerebellum and brainstem Brain Dev. 21 1999 30 35
48. E. Miyamoto Molecular mechanism of neuronal plasticity: induction and maintenance of long-term potentiation in the hippocampus J. Pharm. Sci. 100 2006 433 442
49. T.E. Nelson, C. Hao, J. Manos, R.M. Ransohoff, and D.L. Gruol Altered hippocampal synaptic transmission in transgenic mice with astrocyte-targeted enhanced CCL2 expression Brain Behav. Immun. 25 Suppl. 1 2011 S106 S119
50. T. Otto, H. Eichenbaum, S.I. Wiener, and C.G. Wible Learning-related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long-term potentiation Hippocampus 1 1991 181 192
51. R.G. Phillips, and J.E. LeDoux Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning Behav. Neurosci. 106 1992 274 285
52. G.K. Pyapali, D.A. Turner, W.A. Wilson, and H.S. Swartzwelder Age and dose-dependent effects of ethanol on the induction of hippocampal long-term potentiation Alcohol 19 1999 107 111
53. L. Qin, J. He, R.N. Hanes, O. Pluzarev, J.S. Hong, and F.T. Crews Increased systemic and brain cytokine production and neuroinflammation by endotoxin following ethanol treatment J. Neuroinflamm. 5 2008 10
54. R.M. Ransohoff Chemokines and chemokine receptors: standing at the crossroads of immunobiology and neurobiology Immunity 31 2009 711 721
55. A.J. Roberts, T. Krucker, C.L. Levy, K.A. Slanina, J.G. Sutcliffe, and P.B. Hedlund Mice lacking 5-HT receptors show specific impairments in contextual learning Eur. J. Neurosci. 19 2004 1913 1922
56. R.B. Rock, S. Hu, W.S. Sheng, and P.K. Peterson Morphine stimulates CCL2 production by human neurons J. Neuroinflamm. 3 2006 32
57. B.J. Rollins Chemokines Blood 90 1997 909 928
58. D. Rossi, and A. Zlotnik The biology of chemokines and their receptors Annu. Rev. Immunol. 18 2000 217 242
59. J.A. Sánchez-Alcañiz, S. Haege, W. Mueller, R. Pla, F. Mackay, S. Schulz, G. Lopez-Bendito, R. Stumm, and O. Marin Cxcr7 controls neuronal migration by regulating chemokine responsiveness Neuron 69 2011 77 90
60. V.J. Sanders, C.A. Pittman, M.G. White, G. Wang, C.A. Wiley, and C.L. Achim Chemokines and receptors in HIV encephalitis AIDS 12 1998 1021 1026
61. C. Savarin-Vuaillat, and R.M. Ransohoff Chemokines and chemokine receptors in neurological disease: raise, retain, or reduce? Neurotherapeutics 4 2007 590 601
62. J. Schummers, and M.D. Browning Evidence for a role for GABA(A) and NMDA receptors in ethanol inhibition of long-term potentiation Brain Res. Mol. Brain Res. 94 2001 9 14
63. B.D. Semple, T. Kossmann, and M.C. Morganti-Kossmann Role of chemokines in CNS health and pathology: a focus on the CCL2/CCR2 and CXCL8/CXCR2 networks J. Cereb. Blood Flow Metab. 30 2010 459 473
64. J.E. Simpson, J. Newcombe, M.L. Cuzner, and M.N. Woodroofe Expression of monocyte chemoattractant protein-1 and other beta-chemokines by resident glia and inflammatory cells in multiple sclerosis lesions J. Neuroimmunol. 84 1998 238 249
65. J.G. Sinclair, and G.F. Lo Ethanol blocks tetanic and calcium-induced long-term potentiation in the hippocampal slice Gen. Pharmacol. 17 1986 231 233
66. A. Sokolova, M.D. Hill, F. Rahimi, L.A. Warden, G.M. Halliday, and C.E. Shepherd Monocyte chemoattractant protein-1 plays a dominant role in the chronic inflammation observed in Alzheimer's disease Brain Pathol. 19 2009 392 398
67. E.E. Ubogu, M.B. Cossoy, and R.M. Ransohoff The expression and function of chemokines involved in CNS inflammation Trends Pharmacol. Sci. 27 2006 48 55
68. 2+ dynamics and electrophysiological properties of cultured cerebellar Purkinje neurons Eur. J. Neurosci. 21 2005 2949 2957
69. R. Vlkolinský, G.R. Siggins, I.L. Campbell, and T. Krucker Acute exposure to CXC chemokine ligand 10, but not its chronic astroglial production, alters synaptic plasticity in mouse hippocampal slices J. Neuroimmunol. 150 2004 37 47
70. J.L. Weiner, and C.F. Valenzuela Ethanol modulation of GABAergic transmission: the view from the slice Pharmacol. Ther. 111 2006 533 554
71. J.J. Woodward Ethanol and NMDA receptor signaling Crit. Rev. Neurobiol. 14 2000 69 89
72. H. Xiong, J. Boyle, M. Winkelbauer, S. Gorantla, J. Zheng, A. Ghorpade, Y. Persidsky, K.A. Carlson, and H.E. Gendelman Inhibition of long-term potentiation by interleukin-8: implications for human immunodeficiency virus-1-associated dementia J. Neurosci. Res. 71 2003 600 607
73. R. Yaka, K. Phamluong, and D. Ron Scaffolding of Fyn kinase to the NMDA receptor determines brain region sensitivity to ethanol J. Neurosci. 23 2003 3623 3632
74. Y. Zhou, H. Tang, J. Liu, J. Dong, and H. Xiong Chemokine CCL2 modulation of neuronal excitability and synaptic transmission in rat hippocampal slices J. Neurochem. 116 2011 406 414
75. J. Zou, and F. Crews Induction of innate immune gene expression cascades in brain slice cultures by ethanol: key role of NF-kappaB and proinflammatory cytokines Alcohol Clin. Exp. Res. 34 2010 777 789