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Mitochondrial Ca2+ activates a cation current in Aplysia bag cell neurons.

Abstract

Ion channels may be gated by Ca(2+) entering from the extracellular space or released from intracellular stores--typically the endoplasmic reticulum. The present study examines how Ca(2+) impacts ion channels in the bag cell neurons of Aplysia californica. These neuroendocrine cells trigger ovulation through an afterdischarge involving Ca(2+) influx from Ca(2+) channels and Ca(2+) release from both the mitochondria and endoplasmic reticulum. Liberating mitochondrial Ca(2+) with the protonophore, carbonyl cyanide-4-trifluoromethoxyphenyl-hydrazone (FCCP), depolarized bag cell neurons, whereas depleting endoplasmic reticulum Ca(2+) with the Ca(2+)-ATPase inhibitor, cyclopiazonic acid, did not. In a concentration-dependent manner, FCCP elicited an inward current associated with an increase in conductance and a linear current/voltage relationship that reversed near -40 mV. The reversal potential was unaffected by changing intracellular Cl(-), but left-shifted when extracellular Ca(2+) was removed and right-shifted when intracellular K(+) was decreased. Strong buffering of intracellular Ca(2+) decreased the current, although the response was not altered by blocking Ca(2+)-dependent proteases. Furthermore, fura imaging demonstrated that FCCP elevated intracellular Ca(2+) with a time course similar to the current itself. Inhibiting either the V-type H(+)-ATPase or the ATP synthetase failed to produce a current, ruling out acidic Ca(2+) stores or disruption of ATP production as mechanisms for the FCCP response. Similarly, any involvement of reactive oxygen species potentially produced by mitochondrial depolarization was mitigated by the fact that dialysis with xanthine/xanthine oxidase did not evoke an inward current. However, both the FCCP-induced current and Ca(2+) elevation were diminished by disabling the mitochondrial permeability transition pore with the alkylating agent, N-ethylmaleimide. The data suggest that mitochondrial Ca(2+) gates a voltage-independent, nonselective cation current with the potential to drive the afterdischarge and contribute to reproduction. Employing Ca(2+) from mitochondria, rather than the more common endoplasmic reticulum, represents a diversification of the mechanisms that influence neuronal activity.

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    ,

    Queen's University, Department of Physiology, Kingston, ON K7L 3N6, Canada.

    , ,

    Source

    Journal of neurophysiology 103:3 2010 Mar pg 1543-56

    MeSH

    ATP Synthetase Complexes
    Alkylating Agents
    Animals
    Aplysia
    Calcium Signaling
    Calcium-Transporting ATPases
    Carbonyl Cyanide p-Trifluoromethoxyphenylhydrazone
    Cell Membrane
    Electrophysiology
    Endoplasmic Reticulum
    Female
    Hydrogen
    Ion Channels
    Mitochondria
    Neurons
    Nickel
    Ovulation
    Patch-Clamp Techniques
    Uncoupling Agents

    Pub Type(s)

    Journal Article
    Research Support, Non-U.S. Gov't

    Language

    eng

    PubMed ID

    20071622

    Citation

    Hickey, Charlene M., et al. "Mitochondrial Ca2+ Activates a Cation Current in Aplysia Bag Cell Neurons." Journal of Neurophysiology, vol. 103, no. 3, 2010, pp. 1543-56.
    Hickey CM, Geiger JE, Groten CJ, et al. Mitochondrial Ca2+ activates a cation current in Aplysia bag cell neurons. J Neurophysiol. 2010;103(3):1543-56.
    Hickey, C. M., Geiger, J. E., Groten, C. J., & Magoski, N. S. (2010). Mitochondrial Ca2+ activates a cation current in Aplysia bag cell neurons. Journal of Neurophysiology, 103(3), pp. 1543-56. doi:10.1152/jn.01121.2009.
    Hickey CM, et al. Mitochondrial Ca2+ Activates a Cation Current in Aplysia Bag Cell Neurons. J Neurophysiol. 2010;103(3):1543-56. PubMed PMID: 20071622.
    * Article titles in AMA citation format should be in sentence-case
    TY - JOUR T1 - Mitochondrial Ca2+ activates a cation current in Aplysia bag cell neurons. AU - Hickey,Charlene M, AU - Geiger,Julia E, AU - Groten,Chris J, AU - Magoski,Neil S, Y1 - 2010/01/13/ PY - 2010/1/15/entrez PY - 2010/1/15/pubmed PY - 2010/6/12/medline SP - 1543 EP - 56 JF - Journal of neurophysiology JO - J. Neurophysiol. VL - 103 IS - 3 N2 - Ion channels may be gated by Ca(2+) entering from the extracellular space or released from intracellular stores--typically the endoplasmic reticulum. The present study examines how Ca(2+) impacts ion channels in the bag cell neurons of Aplysia californica. These neuroendocrine cells trigger ovulation through an afterdischarge involving Ca(2+) influx from Ca(2+) channels and Ca(2+) release from both the mitochondria and endoplasmic reticulum. Liberating mitochondrial Ca(2+) with the protonophore, carbonyl cyanide-4-trifluoromethoxyphenyl-hydrazone (FCCP), depolarized bag cell neurons, whereas depleting endoplasmic reticulum Ca(2+) with the Ca(2+)-ATPase inhibitor, cyclopiazonic acid, did not. In a concentration-dependent manner, FCCP elicited an inward current associated with an increase in conductance and a linear current/voltage relationship that reversed near -40 mV. The reversal potential was unaffected by changing intracellular Cl(-), but left-shifted when extracellular Ca(2+) was removed and right-shifted when intracellular K(+) was decreased. Strong buffering of intracellular Ca(2+) decreased the current, although the response was not altered by blocking Ca(2+)-dependent proteases. Furthermore, fura imaging demonstrated that FCCP elevated intracellular Ca(2+) with a time course similar to the current itself. Inhibiting either the V-type H(+)-ATPase or the ATP synthetase failed to produce a current, ruling out acidic Ca(2+) stores or disruption of ATP production as mechanisms for the FCCP response. Similarly, any involvement of reactive oxygen species potentially produced by mitochondrial depolarization was mitigated by the fact that dialysis with xanthine/xanthine oxidase did not evoke an inward current. However, both the FCCP-induced current and Ca(2+) elevation were diminished by disabling the mitochondrial permeability transition pore with the alkylating agent, N-ethylmaleimide. The data suggest that mitochondrial Ca(2+) gates a voltage-independent, nonselective cation current with the potential to drive the afterdischarge and contribute to reproduction. Employing Ca(2+) from mitochondria, rather than the more common endoplasmic reticulum, represents a diversification of the mechanisms that influence neuronal activity. SN - 1522-1598 UR - https://www.unboundmedicine.com/medline/citation/20071622/Mitochondrial_Ca2+_activates_a_cation_current_in_Aplysia_bag_cell_neurons_ L2 - http://www.physiology.org/doi/full/10.1152/jn.01121.2009?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub=pubmed DB - PRIME DP - Unbound Medicine ER -