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Nicotine induces intracellular Ca2+ increases in cultured hippocampal astrocytes by nAChR-dependent and -independent pathways

DOI: 10.4236/wjns.2014.41005, PP. 40-46

Keywords: Glial Cells, Hippocampus, Nicotinic Acetylcholine Receptors, Potassium Channels, Calcium Signaling, Astrocytes

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Abstract:

Nicotine, the major addictive substance in tobacco, interacts with nicotinic acetylcholine receptors (nAChRs) located in neuronal and glial cells, modulating synaptic transmission and memory. Here, we show that nAChRs agonists, including nicotine, acetylcholine, and choline, increase the intracellular Ca2+ concentration ([Ca2+]i) in cultured hippocampal astrocytes, indicating the involvement of nAChRs. Interestingly, inhibition of nAChRs, with a cocktail of antagonists (mecamylamine, methyllycaconitine plus dihydro-β- erythroidine), does not prevent the astrocytic [Ca2+]i increases generated by nicotine. This last effect would be attributable to inhibition of K+ currents by nicotine in these cells, as previously we showed using patch- clamp recordings. Furthermore, the application of tetraethylammonium, an inhibitor of K+ currents, also increases the [Ca2+]i. Together, these results indicate that nicotine increases [Ca2+]i in hippocampal astrocytes through two pathways: by activation of nAChRs, and likely by direct inhibition of K+ currents.

References

[1]  Le Houezec, J. (2003) Role of nicotine pharmacokinetics in nicotine addiction and nicotine replacement therapy: A review. The International Journal of Tuberculosis and Lung Disease, 7, 811-819.
[2]  Gotti, C., Zoli, M. and Clementi, F. (2006) Brain nicotinic acetylcholine receptors: Native subtypes and their relevance. Trends in Pharmacological Sciences, 27, 482-491. http://dx.doi.org/10.1016/j.tips.2006.07.004
[3]  Levin, E.D., McClernon, F.J. and Rezvani, A.H. (2006) Nicotinic effects on cognitive function: Behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacology (Berl), 184, 523-539. http://dx.doi.org/10.1007/s00213-005-0164-7
[4]  Satoh, H. (2002) Modulation by nicotine of the ionic currents in guinea pig ventricular cardiomyocytes. Relatively higher sensitivity to IKr and IKl. Vascular Pharmacology, 39, 55-61.
http://dx.doi.org/10.1016/S1537-1891(02)00194-5
[5]  Tang, G., Hanna, S.T. and Wang, R. (1999) Effects of nicotine on K+ channel currents in vascular smooth muscle cells from rat tail arteries. European Journal of Pharmacology, 364, 247-254.
http://dx.doi.org/10.1016/S0014-2999(98)00833-4
[6]  Wang, H., Shi, H. and Wang, Z. (1999) Nicotine depresses the functions of multiple cardiac potassium channels. Life Sciences, 65, PL143-PL149.
http://dx.doi.org/10.1016/S0024-3205(99)00370-7
[7]  Wang, H., Shi, H., Zhang, L., Pourrier, M., Yang, B., Nattel, S. and Wang, Z. (2000) Nicotine is a potent blocker of the cardiac A-type K+ channels. Effects on cloned Kv4.3 channels and native transient outward current. Circulation, 102, 1165-1171.
http://dx.doi.org/10.1161/01.CIR.102.10.1165
[8]  Wang, H., Yang, B., Zhang, L., Xu, D. and Wang, Z. (2000) Direct block of inward rectifier potassium channels by nicotine. Toxicology and Applied Pharmacology, 164, 97-101. http://dx.doi.org/10.1006/taap.2000.8896
[9]  Wang, H.Z., Shi, H., Liao, S.J. and Wang, Z. (1999) Inactivation gating determines nicotine blockade of human HERG channels. American Journal of Physiology, 277, H1081-H1088.
[10]  Hernández-Morales, M. and García-Colunga, J. (2009) Effects of nicotine on K+ currents and nicotinic receptors in astrocytes of the hippocampal CA1 region. Neuropharmacology, 56, 975-983.
http://dx.doi.org/10.1016/j.neuropharm.2009.01.024
[11]  Hosli, L., Hosli, E., Della Briotta. G., Quadri, L. and Heuss L. (1988) Action of acetylcholine, muscarine, nicotine and antagonists on the membrane potential of astrocytes in cultured rat brainstem and spinal cord. Neuroscience Letters, 92, 165-170.
http://dx.doi.org/10.1016/0304-3940(88)90054-7
[12]  Oikawa, H., Nakamichi, N., Kambe, Y., Ogura, M. and Yoneda, Y. (2005) An increase in intracellular free calcium ions by nicotinic acetylcholine receptors in a single cultured rat cortical astrocyte. Journal of Neuroscience Research, 79, 535-544.
http://dx.doi.org/10.1002/jnr.20398
[13]  Levin, E.D., Petro, A., Rezvani, A.H., Pollard, N., Christopher, N.C., Strauss, M., Avery, J., Nicholson, J. and Rose, J.E. (2009) Nicotinic a7or a2-containing receptor knockout: Effects on radial-arm maze learning and longterm nicotine consumption in mice. Behavioural Brain Research, 196, 207-213.
http://dx.doi.org/10.1016/j.bbr.2008.08.048?
[14]  López-Hidalgo, M., Salgado-Puga, K., Alvarado-Martínez, R., Medina, A.C., Prado-Alcalá, R.A. and GarcíaColunga, J. (2012) Nicotine uses neuron-glia communication to enhance hippocampal synaptic transmission and long-term memory. PLoS One, 7, E49998.
http://dx.doi.org/10.1371/journal.pone.0049998
[15]  Delbro, D., Westerlund, A., Bjorklund, U. and Hansson, E. (2009) In inflammatory reactive astrocytes co-cultured with brain endothelial cells nicotine-evoked Ca2+ transients are attenuated due to interleukin-1a release rearrangement of actin filaments. Neuroscience, 159, 770-779.
http://dx.doi.org/10.1016/j.neuroscience.2009.01.005?
[16]  Sharma, G. and Vijayaraghavan, S. (2001) Nicotinic cholinergic signaling in hippocampal astrocytes involves calcium-induced calcium release from intracellular stores. Proceedings of the National Academy of Sciences of the United States of America, 98, 4148-4153.
http://dx.doi.org/10.1073/pnas.071540198
[17]  Shen, J.X. and Yakel, J.L. (2012) Functional a7 nicotinic ACh receptors on astrocytes in rat hippocampal CA1 slices. Journal of Molecular Neuroscience, 48, 14-21.
http://dx.doi.org/10.1007/s12031-012-9719-3
[18]  Takarada, T., Nakamichi, N., Kawagoe, H., Ogura, M., Fukumori, R., Nakazato, R., Fujikawa, K., Kou, M. and Yoneda, Y. (2012) Possible neuroprotective property of nicotinic acetylcholine receptors in association with predominant upregulation of glial cell line-derived neurotrophic factor in astrocytes. Journal of Neuroscience Research, 90, 2074-2085.
http://dx.doi.org/10.1002/jnr.23101
[19]  Lunardi, P., Nardin, P., Guerra, M.C., Abib, R., Leite, M.C. and Gonalves, C.A. (2013) Huperzine A but not tacrine, stimulates S100B secretion in astrocyte cultures. Life Science, 92, 701-707.
http://dx.doi.org/10.1016/j.lfs.2013.01.029
[20]  Araque, A., Martin, E.D., Perea, G., Arellano, J.I. and Buno, W. (2002) Synaptically released acetylcholine evokes Ca2+ elevations in astrocytes in hippocampal slices. Journal of Neuroscience, 22, 2443-2450.
http://dx.doi.org/10.1016/j.bbamcr.2010.09.007
[21]  Lalo, U., Pankratov, Y., Parpura, V. and Verkhratsky, A. (2011) Ionotropic receptors in neuronal-astroglial signalling: What is the role of “excitable” molecules in nonexcitable cells. Biochimica et Biophysica Acta, 1813, 992-1002.
[22]  Nedergaard, M., Rodriguez, J.J. and Verkhratsky, A. (2010) Glial calcium and diseases of the nervous system. Cell Calcium, 47, 140-149.
http://dx.doi.org/10.1016/j.ceca.2009.11.010
[23]  Takata, N., Mishima, T., Hisatsune, C., Nagai, T., Ebisui, E., Mikoshiba, K. and Hirase, H. (2011) Astrocyte calcium signaling transforms cholinergic modulation to cortical plasticity in vivo. Journal of Neuroscience, 31, 18155-18165. http://dx.doi.org/10.1523/JNEUROSCI.5289-11.2011
[24]  Zorec, R., Araque, A., Carmignoto, G., Haydon, P.G., Verkhratsky, A. and Parpura, V. (2012) Astroglial excitability and gliotransmission: An appraisal of Ca2+ as a signalling route. ASN Neuro, 4, E00080.
http://dx.doi.org/10.1042/AN20110061
[25]  Fucile, S. (2004) Ca2+ permeability of nicotinic acetylcholine receptors. Cell Calcium, 35, 1-8.
http://dx.doi.org/10.1016/j.ceca.2003.08.006
[26]  Yaguchi, T. and Nishizaki, T. (2010) Extracellular high K+ stimulates vesicular glutamate release from astrocytes by activating voltage-dependent calcium channels. Journal of Cellular Physiology, 225, 512-518.
http://dx.doi.org/10.1002/jcp.22231
[27]  Hille, B. (1992) Ion channels of Excitable Membranes. 2nd Edition, Sinauer Associates, Inc., Massachusetts.
[28]  Dwoskin, L.P. and Crooks, P.A. (2001) Competitive neuronal nicotinic receptor antagonists: A new direction for drug discovery. Journal of Pharmacology and Experimental Therapeutics, 298, 395-402.
[29]  Dickinson, J.A., Hanrott, K.E., Mok, M.H., Kew, J.N. and Wonnacott, S. (2007) Differential coupling of a7 and non-a7 nicotinic acetylcholine receptors to calcium-induced calcium release and voltage-operated calcium channels in PC12 cells. Journal of Neurochemistry, 100, 1089-1096.
http://dx.doi.org/10.1111/j.1471-4159.2006.04273.x
[30]  Burgos, M., Pastor, M.D., Gonzalez, J.C., Martinez-Galan, J.R., Vaquero, C.F., Fradejas, N., Benavides, A., Hernandez-Guijo, J.M., Tranque, P. and Calvo, S. (2007) PKC? upregulates voltage-dependent calcium channels in cultured astrocytes. Glia, 55, 1437-1448.
http://dx.doi.org/10.1002/glia.20555
[31]  Latour, I., Hamid, J., Beedle, A.M., Zamponi, G.W. and Macvicar, B.A. (2003) Expression of voltage-gated Ca2+ channel subtypes in cultured astrocytes. Glia, 41, 347-353. http://dx.doi.org/10.1002/glia.20555
[32]  Duffy, A.M., Fitzgerald, M.L., Chan, J., Robinson, D.C., Milner, T.A., Mackie, K. and Pickel, V.M. (2011) Acetylcholine a7 nicotinic and dopamine D2 receptors are targeted to many of the same postsynaptic dendrites and astrocytes in the rodent prefrontal cortex. Synapse, 65 1350-1367. http://dx.doi.org/10.1002/syn.20977
[33]  Gahring, L.C., Persiyanov, K., Dunn, D., Weiss, R., Meyer, E.L. and Rogers, S.W. (2004) Mouse strain-specific nicotinic acetylcholine receptor expression by inhibitory interneurons and astrocytes in the dorsal hippocampus. Journal of Comparative Neurology, 468, 334346. http://dx.doi.org/10.1002/cne.10943
[34]  Gahring, L.C., Persiyanov, K. and Rogers, S.W. (2004) Neuronal and astrocyte expression of nicotinic receptor subunit a4 in the adult mouse brain. Journal of Comparative Neurology, 468, 322-333.
http://dx.doi.org/10.1002/cne.10942
[35]  Graham, A.J., Ray, M.A., Perry, E.K., Jaros, E., Perry, R.H., Volsen, S.G., Bose, S., Evans, N., Lindstrom, J. and Court, J.A. (2003) Differential nicotinic acetylcholine receptor subunit expression in the human hippocampus. Chemical Neuroanatomy, 25, 97-113.
http://dx.doi.org/10.1016/S0891-0618(02)00100-X
[36]  Shytle, R.D., Mori, T., Townsend, K., Vendrame, M., Sun, N., Zeng, J., Ehrhart, J., Silver, A.A., Sanberg, P.R. and Tan, J. (2004) Cholinergic modulation of microglial activation by a7 nicotinic receptors. Journal of Neurochemistry, 89, 337-343.
http://dx.doi.org/10.1046/j.1471-4159.2004.02347.x
[37]  Gu, Z. and Yakel, J.L. (2011) Timing-dependent septal cholinergic induction of dynamic hippocampal synaptic plasticity. Neuron, 71, 155-165.
http://dx.doi.org/10.1016/j.neuron.2011.04.026
[38]  Ji, D., Lape, R. and Dani, J.A. (2001) Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity. Neuron, 31, 131-141.
http://dx.doi.org/10.1016/S0896-6273(01)00332-4
[39]  Parri, H.R., Hernandez, C.M. and Dineley, K.T. (2011) Research update: Alpha7 nicotinic acetylcholine receptor mechanisms in Alzheimer’s disease. Biochemical Pharmacology, 82, 931-942.
http://dx.doi.org/10.1016/j.bcp.2011.06.039
[40]  Benowitz, N.L. (2008) Neurobiology of nicotine addiction: Implications for smoking cessation treatment. American Journal of Medicine, 121, S3-S10.
http://dx.doi.org/10.1016/j.amjmed.2008.01.015
[41]  Griguoli, M., Maul, A., Nguyen, C., Giorgetti, A., Carloni, P. and Cherubini, E. (2010) Nicotine blocks the hyperpolarization-activated current Ih and severely impairs the oscillatory behavior of oriens-lacunosum moleculare interneurons. Journal of Neuroscience, 30, 10773-10783.
http://dx.doi.org/10.1523/JNEUROSCI.2446-10.2010
[42]  Kuchibhotla, K.V., Lattarulo, C.R., Hyman, B.T. and Bacskai, B. (2009) Synchronous hyperactivity and intercellular calcium waves in astrocytes in Alzheimer mice. Science, 323, 1211-1215.
http://dx.doi.org/10.1126/science.1169096
[43]  Zhang, Z., Gong, N., Wang, W., Xu, L. and Xu, T.L. (2008) Bell-shaped D-serine actions on hippocampal long-term depression and spatial memory retrieval. Cerebral Cortex, 18, 2391-2401. http://dx.doi.org/10.1093/cercor/bhn008

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