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Purinergic modulation of neuronal gap junction circuits in the CNS of the leech.
J Neurosci Res. 2020 Jun; 98(6):1232-1249.JN

Abstract

Gap junctions (GJs) are widely distributed in brains across the animal kingdom. To visualize the GJ- coupled networks of two major mechanosensory neurons in the ganglia of medicinal leeches, we injected these cells with the GJ-permeable tracer Neurobiotin. When diffusion time was limited to only 30 min, tracer coupling was highly variable for both cells, suggesting a possible modulation of GJ permeability. In invertebrates the innexins (homologs of vertebrate pannexins) form the GJs. Because extracellular adenosine triphosphate (ATP) modulates pannexin and leech innexin hemichannel permeability and is released by leech glial cells following injury, we tested the effects of bath application of ATP after the injection of Neurobiotin and observed a significant increase in the number of neurons tracer coupled to the sensory neurons. This effect required the elevation of intracellular Ca2+ and could be produced by bath application of caffeine. Conversely, scavenging endogenous extracellular ATP with the ATPase apyrase decreased the number of coupled cells. ATP also increased electrical conductance and tracer permeability between the bilateral Retzius neurons. This modulatory effect of ATP on GJ coupling was blocked by siRNA knockdown of a P1-like adenosine receptor. Finally, exposure of leech ganglia to extracellular ATP induced a characteristic low frequency (<0.3 Hz) rhythmic bursting activity that was roughly synchronous among multiple neurons, a behavior that was significantly attenuated by the GJ blocker octanol. These findings highlight the mediation by ATP of a robust physiological mechanism for modifying neuronal circuits by rapidly recruiting neurons into active networks and entraining synchronized bursting activity.

Authors+Show Affiliations

Division of Biological Sciences, University of California San Diego, La Jolla, CA, USA.Division of Biological Sciences, University of California San Diego, La Jolla, CA, USA.Division of Biological Sciences, University of California San Diego, La Jolla, CA, USA.Division of Biological Sciences, University of California San Diego, La Jolla, CA, USA.Division of Biological Sciences, University of California San Diego, La Jolla, CA, USA.Division of Biological Sciences, University of California San Diego, La Jolla, CA, USA. Department of Psychology, Mount Saint Vincent University, Halifax, Nova Scotia, Canada.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

32096570

Citation

Segura, Oliva Mota, et al. "Purinergic Modulation of Neuronal Gap Junction Circuits in the CNS of the Leech." Journal of Neuroscience Research, vol. 98, no. 6, 2020, pp. 1232-1249.
Segura OM, Abdulnoor L, Hua VV, et al. Purinergic modulation of neuronal gap junction circuits in the CNS of the leech. J Neurosci Res. 2020;98(6):1232-1249.
Segura, O. M., Abdulnoor, L., Hua, V. V., Solano, M. J., Macagno, E. R., & Baker, M. W. (2020). Purinergic modulation of neuronal gap junction circuits in the CNS of the leech. Journal of Neuroscience Research, 98(6), 1232-1249. https://doi.org/10.1002/jnr.24599
Segura OM, et al. Purinergic Modulation of Neuronal Gap Junction Circuits in the CNS of the Leech. J Neurosci Res. 2020;98(6):1232-1249. PubMed PMID: 32096570.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Purinergic modulation of neuronal gap junction circuits in the CNS of the leech. AU - Segura,Oliva Mota, AU - Abdulnoor,Lina, AU - Hua,Vinh-Vincent, AU - Solano,Martha J, AU - Macagno,Eduardo R, AU - Baker,Michael W, Y1 - 2020/02/25/ PY - 2019/09/16/received PY - 2020/01/25/revised PY - 2020/02/05/accepted PY - 2020/2/26/pubmed PY - 2020/2/26/medline PY - 2020/2/26/entrez KW - ATP KW - RRID:AB_10374301 KW - RRID:AB_1501343 KW - RRID:AB_2336606 KW - RRID:AB_2536190 KW - RRID:AB_514497 KW - gap junction KW - modulation KW - neuronal circuit KW - permeability KW - synaptic plasticity SP - 1232 EP - 1249 JF - Journal of neuroscience research JO - J. Neurosci. Res. VL - 98 IS - 6 N2 - Gap junctions (GJs) are widely distributed in brains across the animal kingdom. To visualize the GJ- coupled networks of two major mechanosensory neurons in the ganglia of medicinal leeches, we injected these cells with the GJ-permeable tracer Neurobiotin. When diffusion time was limited to only 30 min, tracer coupling was highly variable for both cells, suggesting a possible modulation of GJ permeability. In invertebrates the innexins (homologs of vertebrate pannexins) form the GJs. Because extracellular adenosine triphosphate (ATP) modulates pannexin and leech innexin hemichannel permeability and is released by leech glial cells following injury, we tested the effects of bath application of ATP after the injection of Neurobiotin and observed a significant increase in the number of neurons tracer coupled to the sensory neurons. This effect required the elevation of intracellular Ca2+ and could be produced by bath application of caffeine. Conversely, scavenging endogenous extracellular ATP with the ATPase apyrase decreased the number of coupled cells. ATP also increased electrical conductance and tracer permeability between the bilateral Retzius neurons. This modulatory effect of ATP on GJ coupling was blocked by siRNA knockdown of a P1-like adenosine receptor. Finally, exposure of leech ganglia to extracellular ATP induced a characteristic low frequency (<0.3 Hz) rhythmic bursting activity that was roughly synchronous among multiple neurons, a behavior that was significantly attenuated by the GJ blocker octanol. These findings highlight the mediation by ATP of a robust physiological mechanism for modifying neuronal circuits by rapidly recruiting neurons into active networks and entraining synchronized bursting activity. SN - 1097-4547 UR - https://www.unboundmedicine.com/medline/citation/32096570/Purinergic_modulation_of_neuronal_gap_junction_circuits_in_the_CNS_of_the_leech L2 - https://doi.org/10.1002/jnr.24599 DB - PRIME DP - Unbound Medicine ER -
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