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. 1995 Jan 15;482(Pt 2):291–307. doi: 10.1113/jphysiol.1995.sp020518

Activation of Ca(2+)-dependent Cl- currents in cultured rat sensory neurones by flash photolysis of DM-nitrophen.

K P Currie 1, J F Wootton 1, R H Scott 1
PMCID: PMC1157729  PMID: 7714823

Abstract

1. Voltage-gated Ca2+ currents (ICa) and Ca(2+)-activated Cl- currents (ICl(Ca)) were recorded from cultured rat dorsal root ganglion (DRG) neurones using the whole-cell configuration of the patch clamp technique. Intracellular photorelease of Ca2+ by flash photolysis of DM-nitrophen elicited transient inward currents only in those cells which possessed Ca(2+)-activated Cl- tail currents following ICa. The reversal potential of the flash responses was hyperpolarized when extracellular Cl- was replaced by SCN-. The flash responses and the Ca(2+)-activated Cl- tail currents were inhibited by the Cl- channel blockers niflumic acid (10-100 microM) and 5-nitro-2-(3-phenylpropylamino)benzoic acid (NPPB) (10 microM). 2. After activation by ICa, the Ca(2+)-activated Cl- current could be reactivated during its decay by photorelease of caged Ca2+. Experiments carried out on neurones held at 0 mV demonstrated that ICl(Ca) could be chronically activated due to residual Ca2+ influx. These data directly demonstrated that the decay of ICl(Ca) is not due to inactivation but rather to deactivation as a result of removal of the Ca2+ load from the cell cytoplasm. 3. Photorelease of caged inositol 1,4,5-trisphosphate (IP3) failed to activate any Ca(2+)-dependent current responses in cultured DRG neurones, although application of caffeine elicited transient inward currents, and responses to photoreleased IP3 could be obtained from freshly dissociated smooth muscle cells. 4. Photorelease of Ca2+ provides a useful method for investigating the properties of ICl(Ca) independently from other physiological parameters. In addition, we have directly demonstrated that ICl(Ca) in DRG neurones does not inactivate, and so may continue to modulate membrane excitability as long as the intracellular Ca2+ concentration ([Ca2+]i) close to the cell membrane is elevated.(ABSTRACT TRUNCATED AT 250 WORDS)

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Selected References

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  1. Akasu T., Nishimura T., Tokimasa T. Calcium-dependent chloride current in neurones of the rabbit pelvic parasympathetic ganglia. J Physiol. 1990 Mar;422:303–320. doi: 10.1113/jphysiol.1990.sp017985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Amédée T., Large W. A., Wang Q. Characteristics of chloride currents activated by noradrenaline in rabbit ear artery cells. J Physiol. 1990 Sep;428:501–516. doi: 10.1113/jphysiol.1990.sp018224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bader C. R., Bertrand D., Schlichter R. Calcium-activated chloride current in cultured sensory and parasympathetic quail neurones. J Physiol. 1987 Dec;394:125–148. doi: 10.1113/jphysiol.1987.sp016863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benham C. D., Evans M. L., McBain C. J. Ca2+ efflux mechanisms following depolarization evoked calcium transients in cultured rat sensory neurones. J Physiol. 1992 Sep;455:567–583. doi: 10.1113/jphysiol.1992.sp019316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boton R., Singer D., Dascal N. Inactivation of calcium-activated chloride conductance in Xenopus oocytes: roles of calcium and protein kinase C. Pflugers Arch. 1990 Apr;416(1-2):1–6. doi: 10.1007/BF00370214. [DOI] [PubMed] [Google Scholar]
  6. Currie K. P., Scott R. H. Calcium-activated currents in cultured neurones from rat dorsal root ganglia. Br J Pharmacol. 1992 Jul;106(3):593–602. doi: 10.1111/j.1476-5381.1992.tb14381.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Currie K. P., Swann K., Galione A., Scott R. H. Activation of Ca(2+)-dependent currents in cultured rat dorsal root ganglion neurones by a sperm factor and cyclic ADP-ribose. Mol Biol Cell. 1992 Dec;3(12):1415–1425. doi: 10.1091/mbc.3.12.1415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Delaney K. R., Zucker R. S. Calcium released by photolysis of DM-nitrophen stimulates transmitter release at squid giant synapse. J Physiol. 1990 Jul;426:473–498. doi: 10.1113/jphysiol.1990.sp018150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Deschenes M., Feltz P., Lamour Y. A model for an estimate in vivo of the ionic basis of presynaptic inhibition: an intracellular analysis of the GABA-induced depolarization in rat dorsal root ganglia. Brain Res. 1976 Dec 24;118(3):486–493. doi: 10.1016/0006-8993(76)90318-8. [DOI] [PubMed] [Google Scholar]
  10. Dolphin A. C., Wootton J. F., Scott R. H., Trentham D. R. Photoactivation of intracellular guanosine triphosphate analogues reduces the amplitude and slows the kinetics of voltage-activated calcium channel currents in sensory neurones. Pflugers Arch. 1988 Jun;411(6):628–636. doi: 10.1007/BF00580858. [DOI] [PubMed] [Google Scholar]
  11. Fryer M. W., Zucker R. S. Ca(2+)-dependent inactivation of Ca2+ current in Aplysia neurons: kinetic studies using photolabile Ca2+ chelators. J Physiol. 1993 May;464:501–528. doi: 10.1113/jphysiol.1993.sp019648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gola M., Crest M. Colocalization of active KCa channels and Ca2+ channels within Ca2+ domains in helix neurons. Neuron. 1993 Apr;10(4):689–699. doi: 10.1016/0896-6273(93)90170-v. [DOI] [PubMed] [Google Scholar]
  13. Gurney A. M., Tsien R. Y., Lester H. A. Activation of a potassium current by rapid photochemically generated step increases of intracellular calcium in rat sympathetic neurons. Proc Natl Acad Sci U S A. 1987 May;84(10):3496–3500. doi: 10.1073/pnas.84.10.3496. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  15. Hogg R. C., Wang Q., Large W. A. Time course of spontaneous calcium-activated chloride currents in smooth muscle cells from the rabbit portal vein. J Physiol. 1993 May;464:15–31. doi: 10.1113/jphysiol.1993.sp019622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ivanenko A., Baring M. D., Airey J. A., Sutko J. L., Kenyon J. L. A caffeine- and ryanodine-sensitive Ca2+ store in avian sensory neurons. J Neurophysiol. 1993 Aug;70(2):710–722. doi: 10.1152/jn.1993.70.2.710. [DOI] [PubMed] [Google Scholar]
  17. Kaplan J. H., Ellis-Davies G. C. Photolabile chelators for the rapid photorelease of divalent cations. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6571–6575. doi: 10.1073/pnas.85.17.6571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kleene S. J., Gesteland R. C. Calcium-activated chloride conductance in frog olfactory cilia. J Neurosci. 1991 Nov;11(11):3624–3629. doi: 10.1523/JNEUROSCI.11-11-03624.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Komori S., Bolton T. B. Calcium release induced by inositol 1,4,5-trisphosphate in single rabbit intestinal smooth muscle cells. J Physiol. 1991 Feb;433:495–517. doi: 10.1113/jphysiol.1991.sp018440. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Korn S. J., Bolden A., Horn R. Control of action potentials and Ca2+ influx by the Ca(2+)-dependent chloride current in mouse pituitary cells. J Physiol. 1991 Aug;439:423–437. doi: 10.1113/jphysiol.1991.sp018674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Korn S. J., Weight F. F. Patch-clamp study of the calcium-dependent chloride current in AtT-20 pituitary cells. J Neurophysiol. 1987 Dec;58(6):1431–1451. doi: 10.1152/jn.1987.58.6.1431. [DOI] [PubMed] [Google Scholar]
  22. Mayer M. L. A calcium-activated chloride current generates the after-depolarization of rat sensory neurones in culture. J Physiol. 1985 Jul;364:217–239. doi: 10.1113/jphysiol.1985.sp015740. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Miller R. J. The control of neuronal Ca2+ homeostasis. Prog Neurobiol. 1991;37(3):255–285. doi: 10.1016/0301-0082(91)90028-y. [DOI] [PubMed] [Google Scholar]
  24. Morad M., Davies N. W., Kaplan J. H., Lux H. D. Inactivation and block of calcium channels by photo-released Ca2+ in dorsal root ganglion neurons. Science. 1988 Aug 12;241(4867):842–844. doi: 10.1126/science.2457253. [DOI] [PubMed] [Google Scholar]
  25. Nishimura T., Akasu T., Tokimasa T. A slow calcium-dependent chloride current in rhythmic hyperpolarization in neurones of the rabbit vesical pelvic ganglia. J Physiol. 1991 Jun;437:673–690. doi: 10.1113/jphysiol.1991.sp018618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ogden D. C., Capiod T., Walker J. W., Trentham D. R. Kinetics of the conductance evoked by noradrenaline, inositol trisphosphate or Ca2+ in guinea-pig isolated hepatocytes. J Physiol. 1990 Mar;422:585–602. doi: 10.1113/jphysiol.1990.sp018002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Owen D. G., Segal M., Barker J. L. A Ca-dependent Cl- conductance in cultured mouse spinal neurones. Nature. 1984 Oct 11;311(5986):567–570. doi: 10.1038/311567a0. [DOI] [PubMed] [Google Scholar]
  28. Pacaud P., Loirand G., Lavie J. L., Mironneau C., Mironneau J. Calcium-activated chloride current in rat vascular smooth muscle cells in short-term primary culture. Pflugers Arch. 1989 Apr;413(6):629–636. doi: 10.1007/BF00581813. [DOI] [PubMed] [Google Scholar]
  29. Partridge L. D., Swandulla D. Calcium-activated non-specific cation channels. Trends Neurosci. 1988 Feb;11(2):69–72. doi: 10.1016/0166-2236(88)90167-1. [DOI] [PubMed] [Google Scholar]
  30. Schlichter R., Bader C. R., Bertrand D., Dubois-Dauphin M., Bernheim L. Expression of substance P and of a Ca2+-activated Cl- current in quail sensory trigeminal neurons. Neuroscience. 1989;30(3):585–594. doi: 10.1016/0306-4522(89)90153-x. [DOI] [PubMed] [Google Scholar]
  31. Scott R. H., McGuirk S. M., Dolphin A. C. Modulation of divalent cation-activated chloride ion currents. Br J Pharmacol. 1988 Jul;94(3):653–662. doi: 10.1111/j.1476-5381.1988.tb11572.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Stapleton S. R., Currie K. P., Scott R. H., Bell B. A. Palmitoyl-DL-carnitine has calcium-dependent effects on cultured neurones from rat dorsal root ganglia. Br J Pharmacol. 1992 Dec;107(4):1192–1197. doi: 10.1111/j.1476-5381.1992.tb13427.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Stapleton S. R., Scott R. H., Bell B. A. Effects of metabolic blockers on Ca(2+)-dependent currents in cultured sensory neurones from neonatal rats. Br J Pharmacol. 1994 Jan;111(1):57–64. doi: 10.1111/j.1476-5381.1994.tb14023.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Thayer S. A., Perney T. M., Miller R. J. Regulation of calcium homeostasis in sensory neurons by bradykinin. J Neurosci. 1988 Nov;8(11):4089–4097. doi: 10.1523/JNEUROSCI.08-11-04089.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Walker J. W., Feeney J., Trentham D. R. Photolabile precursors of inositol phosphates. Preparation and properties of 1-(2-nitrophenyl)ethyl esters of myo-inositol 1,4,5-trisphosphate. Biochemistry. 1989 Apr 18;28(8):3272–3280. doi: 10.1021/bi00434a023. [DOI] [PubMed] [Google Scholar]

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