Restraint stress increases hemichannel activity in hippocampal glial cells and neurons

Frontiers in Cellular Neuroscience

Volumn 9, Issue APR, 2015, Pages 1-12

  Orellana, Juan A ^a   Moraga Amaro, Rodrigo ^b   Díaz Galarce, Raúl ^b   Rojas, Sebastián ^b   Maturana, Carola J ^c   Stehberg, Jimmy ^b   Sáez, Juan C ^c,d  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSIDAD ANDRÉS BELLO   (Chile)

^c PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^d Centro Interdisciplinario de Neurociencias de Valparaíso   (Chile)

Author keywords

Connexins; Glia; Hemichannels; Hippocampus; Neuron; Pannexins; Stress

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DEPRESSION; GLIA CELL; HIPPOCAMPUS; IMMOBILIZATION STRESS; MALE; MICROGLIA; MOUSE; NERVE CELL; NONHUMAN; OPEN FIELD TEST;

EID: 84927654466     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2015.00102     Document Type: Article

References (76)

1. Alfarez, D. N., Joels, M., and Krugers, H. J. (2003). Chronic unpredictable stress impairs long-term potentiation in rat hippocampal CA1 area and dentate gyrus in vitro. Eur. J. Neurosci. 17, 1928-1934. doi: 10.1046/j.1460-9568.2003.02622.x
2. Anselmi, F., Hernandez, V. H., Crispino, G., Seydel, A., Ortolano, S., Roper, S. D., et al. (2008). ATP release through connexin hemichannels and gap junction transfer of second messengers propagate Ca2+ signals across the inner ear. Proc. Natl. Acad. Sci. U S A 105, 18770-18775. doi: 10.1073/pnas.0800793105
3. Arbeloa, J., Pérez-Samartín, A., Gottlieb, M., and Matute, C. (2012). P2X7 receptor blockade prevents ATP excitotoxicity in neurons and reduces brain damage after ischemia. Neurobiol. Dis. 45, 954-961. doi: 10.1016/j.nbd.2011.12.014
4. Arsenault-Lapierre, G., Kim, C., and Turecki, G. (2004). Psychiatric diagnoses in 3275 suicides: a meta-analysis. BMC Psychiatry 4:37. doi: 10.1186/1471-244X-4-37
5. Ashpole, N. M., Chawla, A. R., Martin, M. P., Brustovetsky, T., Brustovetsky, N., and Hudmon, A. (2013). Loss of calcium/calmodulin-dependent protein kinase II activity in cortical astrocytes decreases glutamate uptake and induces neurotoxic release of ATP. J. Biol. Chem. 288, 14599-14611. doi: 10.1074/jbc.M113.466235
6. Block, M. L., Zecca, L., and Hong, J. S. (2007). Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 8, 57-69. doi: 10.1038/nrn2038
7. Burkovetskaya, M., Karpuk, N., Xiong, J., Bosch, M., Boska, M. D., Takeuchi, H., et al. (2014). Evidence for aberrant astrocyte hemichannel activity in Juvenile Neuronal Ceroid Lipofuscinosis (JNCL). PLoS One 9:e95023. doi: 10.1371/journal.pone.0095023
8. Contreras, J. E., Sánchez, H. A., Eugenin, E. A., Speidel, D., Theis, M., Willecke, K., et al. (2002). Metabolic inhibition induces opening of unapposed connexin 43 gap junction hemichannels and reduces gap junctional communication in cortical astrocytes in culture. Proc. Natl. Acad. Sci. U S A 99, 495-500. doi: 10.1073/pnas.012589799
9. Crawley, J. N. (1981). Neuropharmacologic specificity of a simple animal model for the behavioral actions of benzodiazepines. Pharmacol. Biochem. Behav. 15, 695-699. doi: 10.1016/0091-3057(81)90007-1
10. Dhabhar, F. S., and McEwen, B. S. (1997). Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: a potential role for leukocyte trafficking. Brain Behav. Immun. 11, 286-306. doi: 10.1006/brbi.1997.0508
11. Elliott, E. M., and Sapolsky, R. M. (1992). Corticosterone enhances kainic acid-induced calcium elevation in cultured hippocampal neurons. J. Neurochem. 59, 1033-1040. doi: 10.1111/j.1471-4159.1992.tb08345.x
12. Elliott, E. M., and Sapolsky, R. M. (1993). Corticosterone impairs hippocampal neuronal calcium regulation-possible mediating mechanisms. Brain Res. 602, 84-90. doi: 10.1016/0006-8993(93)90245-i
13. Fields, R. D., and Burnstock, G. (2006). Purinergic signalling in neuron-glia interactions. Nat. Rev. Neurosci. 7, 423-436. doi: 10.1038/nrn1928
14. Frank, M. G., Baratta, M. V., Sprunger, D. B., Watkins, L. R., and Maier, S. F. (2007). Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain Behav. Immun. 21, 47-59. doi: 10.1016/j.bbi.2006.03.005
15. Garré, J. M., Retamal, M. A., Cassina, P., Barbeito, L., Bukauskas, F. F., Sáez, J. C., et al. (2010). FGF-1 induces ATP release from spinal astrocytes in culture and opens pannexin and connexin hemichannels. Proc. Natl. Acad. Sci. U S A 107, 22659-22664. doi: 10.1073/pnas.1013793107
16. Gilad, G. M., Gilad, V. H., Wyatt, R. J., and Tizabi, Y. (1990). Region-selective stress-induced increase of glutamate uptake and release in rat forebrain. Brain Res. 525, 335-338. doi: 10.1016/0006-8993(90)90886-g
17. 7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nat. Med. 18, 600-604. doi: 10.1038/nm.2679
18. Hammen, C. (2005). Stress and depression. Annu. Rev. Clin. Psychol. 1, 293-319. doi: 10.1146/annurev.clinpsy.1.102803.143938
19. Hammen, C., Kim, E. Y., Eberhart, N. K., and Brennan, P. A. (2009). Chronic and acute stress and the prediction of major depression in women. Depress. Anxiety 26, 718-723. doi: 10.1002/da.20571
20. Huckstepp, R. T. R., Id Bihi, R., Eason, R., Spyer, K. M., Dicke, N., Willecke, K., et al. (2010). Connexin hemichannel-mediated CO2-dependent release of ATP in the medulla oblongata contributes to central respiratory chemosensitivity. J. Physiol. 588, 3901-3920. doi: 10.1113/jphysiol.2010.192088
21. Iglesias, R., Dahl, G., Qiu, F., Spray, D. C., and Scemes, E. (2009). Pannexin 1: the molecular substrate of astrocyte "hemichannels." J. Neurosci. 29, 7092-7097. doi: 10.1523/JNEUROSCI.6062-08.2009
22. Ito, K., and Ito, M. (2011). Sedative effects of vapor inhalation of the essential oil of Microtoena patchoulii and its related compounds. J. Nat. Med. 65, 336-343. doi: 10.1007/s11418-010-0502-x
23. Karpuk, N., Burkovetskaya, M., Fritz, T., Angle, A., and Kielian, T. (2011). Neuroinflammation leads to region-dependent alterations in astrocyte gap junction communication and hemichannel activity. J. Neurosci. 31, 414-425. doi: 10.1523/JNEUROSCI.5247-10.2011
24. Kendler, K. S. (1998). Anna-Monika-Prize paper. Major depression and the environment: a psychiatric genetic perspective. Pharmacopsychiatry 31, 5-9. doi: 10.1055/s-2007-979287
25. Kessler, R. C. (1997). The effects of stressful life events on depression. Annu. Rev. Psychol. 48, 191-214. doi: 10.1146/annurev.psych.48.1.191
26. Kleen, J. K., Sitomer, M. T., Killeen, P. R., and Conrad, C. D. (2006). Chronic stress impairs spatial memory and motivation for reward without disrupting motor ability and motivation to explore. Behav. Neurosci. 120, 842-851. doi: 10.1037/0735-7044.120.4.842
27. Kwon, M. S., Seo, Y. J., Lee, J. K., Lee, H. K., Jung, J. S., Jang, J. E., et al. (2008). The repeated immobilization stress increases IL-1beta immunoreactivities in only neuron, but not astrocyte or microglia in hippocampal CA1 region, striatum and paraventricular nucleus. Neurosci. Lett. 430, 258-263. doi: 10.1016/j.neulet.2007.11.006
28. Lau, A., and Tymianski, M. (2010). Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch. 460, 525-542. doi: 10.1007/s00424-010-0809-1
29. Levinstein, M. R., and Samuels, B. A. (2014). Mechanisms underlying the antidepressant response and treatment resistance. Front. Behav. Neurosci. 8:208. doi: 10.3389/fnbeh.2014.00208
30. Lin, J. H., Lou, N., Kang, N., Takano, T., Hu, F., Han, X., et al. (2008). A central role of connexin 43 in hypoxic preconditioning. J. Neurosci. 28, 681-695. doi: 10.1523/JNEUROSCI.3827-07.2008
31. Locovei, S., Wang, J., and Dahl, G. (2006). Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett. 580, 239-244. doi: 10.1016/j.febslet.2005.12.004
32. Lowy, M. T., Gault, L., and Yamamoto, B. K. (1993). Adrenalectomy attenuates stress-induced elevations in extracellular glutamate concentrations in the hippocampus. J. Neurochem. 61, 1957-1960. doi: 10.1111/j.1471-4159.1993.tb09839.x
33. Luine, V., Villegas, M., Martinez, C., and McEwen, B. S. (1994). Repeated stress causes reversible impairments of spatial memory performance. Brain Res. 639, 167-170. doi: 10.1016/0006-8993(94)91778-7
34. Magariños, A. M., and McEwen, B. S. (1995). Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 69, 89-98. doi: 10.1016/0306-4522(95)00259-l
35. Magariños, A. M., Verdugo, J. M., and McEwen, B. S. (1997). Chronic stress alters synaptic terminal structure in hippocampus. Proc. Natl. Acad. Sci. U S A 94, 14002-14008. doi: 10.1073/pnas.94.25.14002
36. Mathis, C., Neumann, P. E., Gershenfeld, H., Paul, S. M., and Crawley, J. N. (1995). Genetic analysis of anxiety-related behaviors and responses to benzodiazepine-related drugs in AXB and BXA recombinant inbred mouse strains. Behav. Genet. 25, 557-568. doi: 10.1007/bf02327579
37. McEwen, B. S. (1999). Stress and hippocampal plasticity. Annu. Rev. Neurosci. 22, 105-122. doi: 10.1146/annurev.neuro.22.1.105
38. Millán, S., González-Quijano, M. I., Giordano, M., Soto, L., Martín, A. I., and López-Calderón, A. (1996). Short and long restraint differentially affect humoral and cellular immune functions. Life Sci. 59, 1431-1442. doi: 10.1016/0024-3205(96)00471-7
39. Moghaddam, B. (1993). Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: comparison to hippocampus and basal ganglia. J. Neurochem. 60, 1650-1657. doi: 10.1111/j.1471-4159.1993.tb13387.x
40. Moghaddam, B., Bolinao, M. L., Stein-Behrens, B., and Sapolsky, R. (1994). Glucocorticoids mediate the stress-induced extracellular accumulation of glutamate. Brain Res. 655, 251-254. doi: 10.1016/0006-8993(94)91622-5
41. Mozhui, K., Karlsson, R. M., Kash, T. L., Ihne, J., Norcross, M., Patel, S., et al. (2010). Strain differences in stress responsivity are associated with divergent amygdala gene expression and glutamate-mediated neuronal excitability. J. Neurosci. 30, 5357-5367. doi: 10.1523/JNEUROSCI.5017-09.2010
42. Nair, A., and Bonneau, R. H. (2006). Stress-induced elevation of glucocorticoids increases microglia proliferation through NMDA receptor activation. J. Neuroimmunol. 171, 72-85. doi: 10.1016/j.jneuroim.2005.09.012
43. Orellana, J. A., Froger, N., Ezan, P., Jiang, J. X., Bennett, M. V., Naus, C. C., et al. (2011a). ATP and glutamate released via astroglial connexin 43 hemichannels mediate neuronal death through activation of pannexin 1 hemichannels. J. Neurochem. 118, 826-840. doi: 10.1111/j.1471-4159.2011.07210.x
44. Orellana, J. A., Montero, T. D., and von Bernhardi, R. (2013). Astrocytes inhibit nitric oxide- dependent Ca(2+) dynamics in activated microglia: involvement of ATP released via pannexin 1 channels. Glia 61, 2023-2037. doi: 10.1002/glia.22573
45. Orellana, J. A., Sáez, P. J., Cortés-Campos, C., Elizondo, R. J., Shoji, K. F., Contreras-Duarte, S., et al. (2012). Glucose increases intracellular free Ca2+ in tanycytes via ATP released through connexin 43 hemichannels. Glia 60, 53-68. doi: 10.1002/glia.21246
46. Orellana, J. A., Sáez, P. J., Shoji, K. F., Schalper, K. A., Palacios-Prado, N., Velarde, V., et al. (2009). Modulation of brain hemichannels and gap junction channels by pro-inflammatory agents and their possible role in neurodegeneration. Antioxid. Redox. Signal. 11, 369-399. doi: 10.1089/ars.2008.2130
47. Orellana, J. A., Shoji, K. F., Abudara, V., Ezan, P., Amigou, E., Sáez, P. J., et al. (2011b). Amyloid β-induced death in neurons involves glial and neuronal hemichannels. J. Neurosci. 31, 4962-4977. doi: 10.1523/JNEUROSCI.6417-10.2011
48. Orellana, J. A., and Stehberg, J. (2014). Hemichannels: new roles in astroglial function. Front. Physiol. 5:193. doi: 10.3389/fphys.2014.00193
49. Pavlides, C., Nivón, L. G., and McEwen, B. S. (2002). Effects of chronic stress on hippocampal long- term potentiation. Hippocampus 12, 245-257. doi: 10.1002/hipo.1116
50. 7 receptor. EMBO J. 25, 5071-5082. doi: 10.1038/sj.emboj.7601378
51. Perea, G., and Araque, A. (2010). GLIA modulates synaptic transmission. Brain Res. Rev. 63, 93-102. doi: 10.1016/j.brainresrev.2009.10.005
52. Perea, G., Navarrete, M., and Araque, A. (2009). Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci. 32, 421-431. doi: 10.1016/j.tins.2009.05.001
53. Popoli, M., Yan, Z., McEwen, B. S., and Sanacora, G. (2011). The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat. Rev. Neurosci. 13, 22-37. doi: 10.1038/nrn3138
54. Rouach, N., Avignone, E., Même, W., Koulakoff, A., Venance, L., Blomstrand, F., et al. (2002). Gap junctions and connexin expression in the normal and pathological central nervous system. Biol. Cell 94, 457-475. doi: 10.1016/s0248-4900(02)00016-3
55. Sáez, J. C., and Leybaert, L. (2014). Hunting for connexin hemichannels. FEBS Lett. 588, 1205-1211. doi: 10.1016/j.febslet.2014.03.004
56. Sáez, P. J., Shoji, K. F., Retamal, M. A., Harcha, P. A., Ramírez, G., Jiang, J. X., et al. (2013). ATP is required and advances cytokine-induced gap junction formation in microglia in vitro. Mediators Inflamm. 2013:216402. doi: 10.1155/2013/216402
57. Sahu, G., Sukumaran, S., and Bera, A. K. (2014). Pannexins form gap junctions with electrophysiological and pharmacological properties distinct from connexins. Sci. Rep. 4:4955. doi: 10.1038/srep04955
58. Schalper, K. A., Palacios-Prado, N., Orellana, J. A., and Sáez, J. C. (2008). Currently used methods for identification and characterization of hemichannels. Cell Commun. Adhes. 15, 207-218. doi: 10.1080/15419060802014198
59. Schock, S. C., Leblanc, D., Hakim, A. M., and Thompson, C. S. (2008). ATP release by way of connexin 36 hemichannels mediates ischemic tolerance in vitro. Biochem. Biophys. Res. Commun. 368, 138-144. doi: 10.1016/j.bbrc.2008.01.054
60. Shestopalov, V. I., and Slepak, V. Z. (2014). Molecular pathways of pannexin1-mediated neurotoxicity. Front. Physiol. 5:23. doi: 10.3389/fphys.2014.00023
61. Shijie, J., Takeuchi, H., Yawata, I., Harada, Y., Sonobe, Y., Doi, Y., et al. (2009). Blockade of glutamate release from microglia attenuates experimental autoimmune encephalomyelitis in mice. Tohoku. J. Exp. Med. 217, 87-92. doi: 10.1620/tjem.217.87
62. Siller-Jackson, A. J., Burra, S., Gu, S., Xia, X., Bonewald, L. F., Sprague, E., et al. (2008). Adaptation of connexin 43-hemichannel prostaglandin release to mechanical loading. J. Biol. Chem. 283, 26374-26382. doi: 10.1074/jbc.M803136200
63. Silverman, W., Locovei, S., and Dahl, G. (2008). Probenecid, a gout remedy, inhibits pannexin 1 channels. Am. J. Physiol. Cell Physiol. 295, C761-C767. doi: 10.1152/ajpcell.00227.2008
64. Simard, M., Couldwell, W. T., Zhang, W., Song, H., Liu, S., Cotrina, M. L., et al. (1999). Glucocorticoids-potent modulators of astrocytic calcium signaling. Glia 28, 1-12. doi: 10.1002/(sici)1098-1136(199910)28:1<1::aid-glia1>3.0.co;2-4
65. Sorrells, S. F., Caso, J. R., Munhoz, C. D., and Sapolsky, R. M. (2009). The stressed CNS: when glucocorticoids aggravate inflammation. Neuron 64, 33-39. doi: 10.1016/j.neuron.2009.09.032
66. Sosinsky, G. E., Boassa, D., Dermietzel, R., Duffy, H. S., Laird, D. W., MacVicar, B., et al. (2011). Pannexin channels are not gap junction hemichannels. Channels (Austin) 5, 193-197. doi: 10.4161/chan.5.3.15765
67. Stehberg, J., Moraga-Amaro, R., Salazar, C., Becerra, A., Echeverría, C., Orellana, J. A., et al. (2012). Release of gliotransmitters through astroglial connexin 43 hemichannels is necessary for fear memory consolidation in the basolateral amygdala. FASEB J. 26, 3649-3657. doi: 10.1096/fj.11-198416
68. Sugama, S., Fujita, M., Hashimoto, M., and Conti, B. (2007). Stress induced morphological microglial activation in the rodent brain: involvement of interleukin-18. Neuroscience 146, 1388-1399. doi: 10.1016/j.neuroscience.2007.02.043
69. Takemoto, H., Ito, M., Shiraki, T., Yagura, T., and Honda, G. (2008). Sedative effects of vapor inhalation of agarwood oil and spikenard extract and identification of their active components. J. Nat. Med. 62, 41-46. doi: 10.1007/s11418-007-0177-0
70. Takeuchi, H., Jin, S., Wang, J., Zhang, G., Kawanokuchi, J., Kuno, R., et al. (2006). Tumor necrosis factor-alpha induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. J. Biol. Chem. 281, 21362-21368. doi: 10.1074/jbc.m600504200
71. Thompson, R. J., Jackson, M. F., Olah, M. E., Rungta, R. L., Hines, D. J., Beazely, M. A., et al. (2008). Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus. Science 322, 1555-1559. doi: 10.1126/science.1165209
72. Thompson, R. J. R., Zhou, N. N., and Macvicar, B. A. B. (2006). Ischemia opens neuronal gap junction hemichannels. Science 312, 924-927. doi: 10.1126/science.1126241
73. Torres, A., Wang, F., Xu, Q., Fujita, T., Dobrowolski, R., Willecke, K., et al. (2012). Extracellular Ca2+ acts as a mediator of communication from neurons to glia. Sci. Signal. 5:ra8. doi: 10.1126/scisignal.2002160
74. Tynan, R. J., Naicker, S., Hinwood, M., Nalivaiko, E., Buller, K. M., Pow, D. V., et al. (2010). Chronic stress alters the density and morphology of microglia in a subset of stress-responsive brain regions. Brain Behav. Immun. 24, 1058-1068. doi: 10.1016/j.bbi.2010.02.001
75. Wang, N., De Bock, M., Decrock, E., Bol, M., Gadicherla, A., Bultynck, G., et al. (2013a). Connexin targeting peptides as inhibitors of voltage- and intracellular Ca2+- triggered Cx43 hemichannel opening. Neuropharmacology 75, 506-516. doi: 10.1016/j.neuropharm.2013.08.021
76. Wang, N., De Bock, M., Decrock, E., Bol, M., Gadicherla, A., Vinken, M., et al. (2013b). Paracrine signaling through plasma membrane hemichannels. Biochim. Biophys. Acta 1828, 35-50. doi: 10.1016/j.bbamem.2012.07.002