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Capsaicin-induced currents with distinct desensitization and Ca2+ dependence in rat trigeminal ganglion cells
1Department of Neurobiology and Anesthesiology, Duke University Medical Center, Durham, North Carolina 27710, USA.
Abstract:
1. Whole cell patch-clamp records from cultured rat trigeminal ganglion cells having soma diameters ranging from 20 to 50 microM revealed that capsaicin activated two inward currents and an outward current. At -60 mV, the inward currents could be distinguished by their different peak times, which were 4.2 +/- 3.1 and 41.4 +/- 16.4 (SD) s. 2. Cells with the smallest soma diameters had the largest current densities. 3. The more rapidly activating current had a linear current-voltage relation and a reversal potential near 0 mV. 4. The more slowly activating current is not a Ca(2+)-activated Cl- current. 5. The peak of the rapid current (Ip)-capsaicin concentration (C) relationship was characterized by Ip/Ipmax = [1 + (C/Kd)n]-1, where n = 1.2 and the dissociation constant (Kd) = 0.68 microM. 6. The rapidly activating current was heterogeneous in regards to both its rate of activation and extent of desensitization. In cells bathed in buffer containing calcium and held at -60 mV, most of the capsaicin-activated currents desensitized. Removal of extracellular Ca2+ could reduce, eliminate, or have no effect on desensitization. 7. At positive holding potentials the currents very slowly desensitized, even in the presence of Ca2+. 8. Repeated 30-s applications of 1 microM capsaicin separated by 0.5, 2.5, and 5.5 min all induced tachyphylaxis. Tachyphylaxis decreased exponentially until the current remained approximately constant. Decreasing the time between capsaicin applications increased the extent of tachyphylaxis, whereas elimination of extracellular Ca2+ markedly reduced tachyphylaxis.
Insights
Capsaicin activates distinct inward currents in rat trigeminal ganglion cells, with smaller cells showing higher current densities. Desensitization and tachyphylaxis are influenced by calcium and application frequency.
Area of Science:
- Neuroscience
- Molecular Biology
- Electrophysiology
Background:
- The trigeminal ganglion (TG) is crucial for sensory processing, including pain and chemosensation.
- Capsaicin, the active component of chili peppers, is a well-known activator of transient receptor potential vanilloid 1 (TRPV1) channels, which are expressed in TG neurons.
Purpose of the Study:
- To characterize the electrophysiological responses of cultured rat trigeminal ganglion cells to capsaicin.
- To investigate the properties of capsaicin-activated currents, including their kinetics, voltage dependence, and desensitization mechanisms.
Main Methods:
- Whole-cell patch-clamp recordings were performed on cultured rat trigeminal ganglion (TG) cells.
- Cells were exposed to varying concentrations of capsaicin.
- Currents were analyzed at different holding potentials, and the effects of extracellular calcium and repeated applications were examined.
Main Results:
- Capsaicin activated two distinct inward currents with different activation times (4.2 ± 3.1 s and 41.4 ± 16.4 s) and an outward current.
- Current density was inversely correlated with soma diameter; smaller cells exhibited larger current densities.
- The rapidly activating current displayed linear current-voltage relationship and a reversal potential near 0 mV, with a dissociation constant (Kd) of 0.68 µM.
- Desensitization and tachyphylaxis were observed, influenced by extracellular calcium levels and the frequency of capsaicin application.
Conclusions:
- Cultured rat TG cells exhibit complex capsaicin-evoked currents, suggesting the involvement of multiple ion channels.
- Cell size influences current density, potentially indicating distinct neuronal populations within the TG.
- Calcium ions play a significant role in the desensitization and tachyphylaxis of capsaicin-activated currents, providing insights into neuronal adaptation mechanisms.