CCL2-ethanol interactions and hippocampal synaptic protein expression in a transgenic mouse model

Frontiers in Integrative Neuroscience

Volumn 8, Issue APR, 2014, Pages

  Gruol, Donna L ^a   Vo, Khanh ^a   Bray, Jennifer G ^a,b   Roberts, Amanda J ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WISCONSIN STEVENS POINT   (United States)

Author keywords

Alcohol use disorders; Astrocyte; Chemokine; Chronic treatment; Neuroimmune; Western blot

Indexed keywords

ALCOHOL; MONOCYTE CHEMOTACTIC PROTEIN 1;

ADAPTATION; ALCOHOL BLOOD LEVEL; ALCOHOL CONSUMPTION; ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN LEVEL; CONTROLLED STUDY; CYTOKINE PRODUCTION; EXPOSURE; FEMALE; HIPPOCAMPUS; MALE; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE; VAPOR;

EID: 84897934569     PISSN: 16625145     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnint.2014.00029     Document Type: Article

References (60)

1. Banisadr, G., Gosselin, R. D., Mechighel, P., Rostene, W., Kitabgi, P., and Melik Parsadaniantz, S. (2005). Constitutive neuronal expression of CCR2 chemokine receptor and its colocalization with neurotransmitters in normal rat brain: functional effect of MCP-1/CCL2 on calcium mobilization in primary cultured neurons. J. Comp. Neurol. 492, 178-192. doi: 10.1002/cne.20729
2. Becker, H. C., and Lopez, M. F. (2004). Increased ethanol drinking after repeated chronic ethanol exposure and withdrawal experience in C57BL/6 mice. Alcohol. Clin. Exp. Res. 28, 1829-1838. doi: 10.1097/01.ALC.0000149977.95306.3A
3. Belkouch, M., Dansereau, M. A., Reaux-Le Goazigo, A., Van Steenwinckel, J., Beaudet, N., Chraibi, A., et al. (2011). The chemokine CCL2 increases Nav1.8 sodium channel activity in primary sensory neurons through a Gbetagamma-dependent mechanism. J. Neurosci. 31, 18381-18390. doi: 10.1523/JNEUROSCI.3386-11.2011
4. Ben Achour, S., and Pascual, O. (2010). Glia: the many ways to modulate synaptic plasticity. Neurochem. Int. 57, 440-445. doi: 10.1016/j.neuint.2010.02.013
5. Bessis, A., Bechade, C., Bernard, D., and Roumier, A. (2007). Microglial control of neuronal death and synaptic properties. Glia 55, 233-238. doi: 10.1002/glia.20459
6. Blanco, A. M., and Guerri, C. (2007). Ethanol intake enhances inflammatory mediators in brain: role of glial cells and TLR4/IL-1RI receptors. Front. Biosci. 12, 2616-2630. doi: 10.2741/2259
7. Blednov, Y. A., Bergeson, S. E., Walker, D., Ferreira, V. M., Kuziel, W. A., and Harris, R. A. (2005). Perturbation of chemokine networks by gene deletion alters the reinforcing actions of ethanol. Behav. Brain Res. 165, 110-125. doi: 10.1016/j.bbr.2005.06.026
8. Blednov, Y. A., Ponomarev, I., Geil, C., Bergeson, S., Koob, G. F., and Harris, R. A. (2012). Neuroimmune regulation of alcohol consumption: behavioral validation of genes obtained from genomic studies. Addict. Biol. 17, 108-120. doi: 10.1111/j.1369-1600.2010.00284.x
9. Bray, J. G., Reyes, K. C., Roberts, A. J., Ransohoff, R., and Gruol, D. L. (2013a). Synaptic plasticity in the hippocampus shows resistance to acute ethanol exposure in transgenic mice with astrocyte-targeted enhanced CCL2 expression. Neuropharmacology 67, 115-125. doi: 10.1016/j.neuropharm.2012.11.007
10. Bray, J. G., Roberts, A. J., Nadav, T., Cates, L. N., Ransohoff, R. M., and Gruol, D. L. (2013b). Ethanol drinking and cognitive performance in dependent and non-dependent CCL2 overexpressing mice. Alcohol. Clin. Exp. Res. 35(SUPPL.), 177A.
11. Breese, G. R., Knapp, D. J., Overstreet, D. H., Navarro, M., Wills, T. A., and Angel, R. A. (2008). Repeated lipopolysaccharide (LPS) or cytokine treatments sensitize ethanol withdrawal-induced anxiety-like behavior. Neuropsychopharmacology 33, 867-876. doi: 10.1038/sj.npp.1301468
12. Chandler, L. J., Norwood, D., and Sutton, G. (1999). Chronic ethanol upregulates NMDA and AMPA, but not kainate receptor subunit proteins in rat primary cortical cultures. Alcohol. Clin. Exp. Res. 23, 363-370. doi: 10.1111/j.1530-0277.1999.tb04123.x
13. Clapp, P., Gibson, E. S., Dell'Acqua, M. L., and Hoffman, P. L. (2010). Phosphorylation regulates removal of synaptic N-methyl-D-aspartate receptors after withdrawal from chronic ethanol exposure. J. Pharmacol. Exp. Ther. 332, 720-729. doi: 10.1124/jpet.109.158741
14. Crews, F. T. (2012). Immune function genes, genetics, and the neurobiology of addiction. Alcohol Res. 34, 355-361.
15. Crews, F. T., Morrow, A. L., Criswell, H., and Breese, G. (1996). Effects of ethanol on ion channels. Int. Rev. Neurobiol. 39, 283-367. doi: 10.1016/S0074-7742(08)60670-4
16. Dolin, S., Little, H., Hudspith, M., Pagonis, C., and Littleton, J. (1987). Increased dihydropyridine-sensitive calcium channels in rat brain may underlie ethanol physical dependence. Neuropharmacology 26, 275-279. doi: 10.1016/0028-3908(87)90220-6
17. Finn, D. A., Snelling, C., Fretwell, A. M., Tanchuck, M. A., Underwood, L., Cole, M., et al. (2007). Increased drinking during withdrawal from intermittent ethanol exposure is blocked by the CRF receptor antagonist D-Phe-CRF(12-41). Alcohol. Clin. Exp. Res. 31, 939-949. doi: 10.1111/j.1530-0277.2007.00379.x
18. Flora, G., Pu, H., Lee, Y. W., Ravikumar, R., Nath, A., Hennig, B., et al. (2005). Proinflammatory synergism of ethanol and HIV-1 Tat protein in brain tissue. Exp. Neurol. 191, 2-12. doi: 10.1016/j.expneurol.2004.06.007
19. Foltran, F., Gregori, D., Franchin, L., Verduci, E., and Giovannini, M. (2011). Effect of alcohol consumption in prenatal life, childhood, and adolescence on child development. Nutr. Rev. 69, 642-659. doi: 10.1111/j.1753-4887.2011. 00417.x
20. Ge, S., Murugesan, N., and Pachter, J. S. (2009). Astrocyte and endothelial-targeted CCL2 conditional knockout mice: critical tools for studying the pathogenesis of neuroinflammation. J. Mol. Neurosci. 39, 269-283. doi: 10.1007/s12031-009-9197-4
21. Gilpin, N. W., Richardson, H. N., Cole, M., and Koob, G. F. (2008). Vapor inhalation of alcohol in rats. Curr. Protoc. Neurosci. Chapter 9, Unit 9.29. doi: 10.1002/0471142301.ns0929s44
22. Glabinski, A. R., Balasingam, V., Tani, M., Kunkel, S. L., Strieter, R. M., Yong, V. W., et al. (1996). Chemokine monocyte chemoattractant protein-1 is expressed by astrocytes after mechanical injury to the brain. J. Immunol. 156, 4363-4368.
23. Gosselin, R. D., Varela, C., Banisadr, G., Mechighel, P., Rostene, W., Kitabgi, P., et al. (2005). Constitutive expression of CCR2 chemokine receptor and inhibition by MCP-1/CCL2 of GABA-induced currents in spinal cord neurones. J. Neurochem. 95, 1023-1034. doi: 10.1111/j.1471-4159.2005.03431.x
24. Griffin, W. C. IIIrd., Lopez, M. F., and Becker, H. C. (2009). Intensity and duration of chronic ethanol exposure is critical for subsequent escalation of voluntary ethanol drinking in mice. Alcohol. Clin. Exp. Res. 33, 1893-1900. doi: 10.1111/j.1530-0277.2009.01027.x
25. Gruol, D. L. (2013). "Alcohol-chemokine interaction and neurotransmission," in Neural-Immune Interactions in Brain Function and Alcohol Related Disorders, eds C. Cui, L. Grandison, and A. Noronha (New York, NY: Springer), 387-424. doi: 10.1007/978-1-4614-4729-0_12
26. Gulya, K., Grant, K. A., Valverius, P., Hoffman, P. L., and Tabakoff, B. (1991). Brain regional specificity and time-course of changes in the NMDA receptor-ionophore complex during ethanol withdrawal. Brain Res. 547, 129-134. doi: 10.1016/0006-8993(91)90125-F
27. Guyon, A., Skrzydelski, D., De Giry, I., Rovere, C., Conductier, G., Trocello, J. M., et al. (2009). Long term exposure to the chemokine CCL2 activates the nigrostri-atal dopamine system: a novel mechanism for the control of dopamine release. Neuroscience 162, 1072-1080. doi: 10.1016/j.neuroscience.2009.05.048
28. Halassa, M. M., Fellin, T., and Haydon, P. G. (2007). The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol. Med. 13, 54-63. doi: 10.1016/j.molmed.2006.12.005
29. He, J., and Crews, F. T. (2008). Increased MCP-1 and microglia in various regions of the human alcoholic brain. Exp. Neurol. 210, 349-358. doi: 10.1016/j.expneurol.2007.11.017
30. Hingson, R. W., Heeren, T., and Winter, M. R. (2006). Age at drinking onset and alcohol dependence: age at onset, duration, and severity. Arch. Pediatr. Adolesc. Med. 160, 739-746. doi: 10.1001/archpedi.160.7.739
31. Hoffman, P. L. (2003). NMDA receptors in alcoholism. Int. Rev. Neurobiol. 56, 35-82. doi: 10.1016/S0074-7742(03)56002-0
32. Holmes, A., Spanagel, R., and Krystal, J. H. (2013). Glutamatergic targets for new alcohol medications. Psychopharmacology 229, 539-554. doi: 10.1007/s00213-013-3226-2
33. Huang, D., Tani, M., Wang, J., He, T. T., Weaver, J., Charo, I. F., et al. (2002). Pertussis toxin-induced encephalopathy dependent on monocyte chemoattrac-tant protein-1 overexpression in mice. J. Neurosci. 22, 10633-10642.
34. Kane, C. J., Phelan, K. D., Douglas, J. C., Wagoner, G., Johnson, J. W., Xu, J., et al. (2013a). Effects of ethanol on immune response in the brain: region-specific changes in aged mice. J. Neuroinflammation 10:66. doi: 10.1186/1742-209 4-10-66
35. Kane, C. J., Phelan, K. D., Douglas, J. C., Wagoner, G., Johnson, J. W., Xu, J., et al. (2013b). Effects of ethanol on immune response in the brain: region-specific changes in adolescent versus adult mice. Alcohol. Clin. Exp. Res. 38, 384-391. doi: 10.1111/acer.12244
36. Kim, J. S., Kim, J., Kim, Y., Yang, M., Jang, H., Kang, S., et al. (2011). Differential patterns of nestin and glial fibrillary acidic protein expression in mouse hippocampus during postnatal development. J. Vet. Sci. 12, 1-6. doi: 10.4142/jvs.2011.12.1.1
37. Lee, H. K., Takamiya, K., He, K., Song, L., and Huganir, R. L. (2010). Specific roles of AMPA receptor subunit GluR1 (GluA1) phosphorylation sites in regulating synaptic plasticity in the CA1 region of hippocampus. J. Neurophysiol. 103, 479-489. doi: 10.1152/jn.00835.2009
38. Lomo, T. (2003). The discovery of long-term potentiation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 617-620. doi: 10.1098/rstb.2002.1226
39. Lopez, M. F., and Becker, H. C. (2005). Effect of pattern and number of chronic ethanol exposures on subsequent voluntary ethanol intake in C57BL/6J mice. Psychopharmacology 181, 688-696. doi: 10.1007/s00213-005-0026-3
40. Nagy, J. (2008). Alcohol related changes in regulation of NMDA receptor functions. Curr. Neuropharmacol. 6, 39-54. doi: 10.2174/157015908783769662
41. Nelson, T. E., Hao, C., Manos, J., Ransohoff, R. M., and Gruol, D. L. (2011). Altered hippocampal synaptic transmission in transgenic mice with astrocyte-targeted enhanced CCL2 expression. Brain Behav. Immun. 25(SUPP
42. Nelson, T. E., Ur, C. L., and Gruol, D. L. (2005). Chronic intermittent ethanol exposure enhances NMDA-receptor-mediated synaptic responses and NMDA receptor expression in hippocampal CA1 region. Brain Res. 1048, 69-79. doi: 10.1016/j.brainres.2005.04.041
43. Pannasch, U., Vargova, L., Reingruber, J., Ezan, P., Holcman, D., Giaume, C., et al. (2011). Astroglial networks scale synaptic activity and plasticity. Proc. Natl. Acad. Sci. U.S.A. 108, 8467-8472. doi: 10.1073/pnas.1016650108
44. Pian, J. P., Criado, J. R., Milner, R., and Ehlers, C. L. (2010). N-methyl-D-aspartate receptor subunit expression in adult and adolescent brain following chronic ethanol exposure. Neuroscience 170, 645-654. doi: 10.1016/j.neuroscience.2010.06.065
45. Qiang, M., Denny, A. D., and Ticku, M. K. (2007). Chronic intermittent ethanol treatment selectively alters N-methyl-D-aspartate receptor subunit surface expression in cultured cortical neurons. Mol. Pharmacol. 72, 95-102. doi: 10.1124/mol.106.033043
46. Qin, L., He, J., Hanes, R. N., Pluzarev, O., Hong, J. S., and Crews, F. T. (2008). Increased systemic and brain cytokine production and neuroinflammation by endotoxin following ethanol treatment. J. Neuroinflammation 5, 10. doi: 10.1186/1742-2094-5-10
47. Roberto, M., Bajo, M., Crawford, E., Madamba, S. G., and Siggins, G. R. (2006). Chronic ethanol exposure and protracted abstinence alter NMDA receptors in central amygdala. Neuropsychopharmacology 31, 988-996. doi: 10.1038/sj.npp.1300840
48. Sanderson, D. J., Good, M. A., Seeburg, P. H., Sprengel, R., Rawlins, J. N., and Bannerman, D. M. (2008). The role of the GluR-A (GluR1) AMPA receptor subunit in learning and memory. Prog. Brain Res. 169, 159-178. doi: 10.1016/S0079-6123(07)00009-X
49. Soderling, T. R., and Derkach, V. A. (2000). Postsynaptic protein phosphorylation and LTP. Tr e n d s Ne u r o s c i. 23, 75-80. doi: 10.1016/S0166-2236(99)01490-3
50. Suk, K. (2007). Microglial signal transduction as a target of alcohol action in the brain. Curr. Neurovasc. Res. 4, 131-142. doi: 10.2174/156720207780637261
51. Tremblay, M. E., and Majewska, A. K. (2011). A role for microglia in synaptic plasticity? Commun. Integr. Biol. 4, 220-222. doi: 10.4161/cib.4.2. 14506
52. 2+ dynamics and electrophysiological properties of cultured cerebellar Purkinje neurons. Eur. J. Neurosci. 21, 2949-2957. doi: 10.1111/j.1460-9568.2005.04113.x
53. Vendruscolo, L. F., and Roberts, A. J. (2013). Operant alcohol self-administration in dependent rats: Focus on the vapor model. Alcohol. doi: 10.1016/j.alcohol.2013.08.006. [Epub ahead of print].
54. Whitman, B. A., Knapp, D. J., Werner, D. F., Crews, F. T., and Breese, G. R. (2013). The Cytokine mRNA increase induced by withdrawal from chronic ethanol in the sterile environment of brain is mediated by CRF and HMGB1 release. Alcohol. Clin. Exp. Res. 37, 2086-2097. doi: 10.1111/acer.12189
55. Whittington, M. A., Lambert, J. D., and Little, H. J. (1995). Increased NMDA receptor and calcium channel activity underlying ethanol withdrawal hyperex-citability. Alcohol Alcohol. 30, 105-114.
56. Yoneyama, N., Crabbe, J. C., Ford, M. M., Murillo, A., and Finn, D. A. (2008). Voluntary ethanol consumption in 22 inbred mouse strains. Alcohol 42, 149-160. doi: 10.1016/j.alcohol.2007.12.006
57. You, H., Altier, C., and Zamponi, G. W. (2010). CCR2 receptor ligands inhibit Cav3.2 T-type calcium channels. Mol. Pharmacol. 77, 211-217. doi: 10.1124/mol.109.059022
58. Zhou, Y., Tang, H., Liu, J., Dong, J., and Xiong, H. (2011). Chemokine CCL2 modulation of neuronal excitability and synaptic transmission in rat hip-pocampal slices. J. Neurochem. 116, 406-414. doi: 10.1111/j.1471-4159.2010. 07121.x
59. Zink, M., and Spanagel, R. (2005). Ethanol induces GAD67 and VGAT in slice cultures of newborn rat cerebral cortex. Neuroreport 16, 377-380. doi: 10.1097/00001756-200503150-00014
60. Zou, J., and Crews, F. (2010). 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, 777-789. doi: 10.1111/j.1530-0277.2010.01150.x