Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 1986 Nov;50(5):797–803. doi: 10.1016/S0006-3495(86)83520-2

Inositol trisphosphate regulation of photoreceptor membrane currents.

M Sakakibara, D L Alkon, J T Neary, E Heldman, R Gould
PMCID: PMC1329804  PMID: 3491632

Abstract

In previous studies elevation of intracellular Ca2+ was shown to cause prolonged reduction of two voltage-dependent K+ currents (IA and ICa2+-K+) across the membrane of the isolated Hermissenda photoreceptor, the type B cell (Alkon et al., 1982b; Alkon and Sakakibara, 1985). Here we show that iontophoretic injection of inositol trisphosphate (IP3), but not inositol monophosphate, also caused prolonged reduction of IA and ICa2+-K+. IP3 injection also caused reduction of a light-induced K+ current (also ICa2+-K+) but did not affect the voltage-dependent Ca2+ current, ICa2+, or the light-induced inward current, INa+, of the type B cell. IP3 injection caused similar effects on the K+ currents of the other type of Hermissenda photoreceptor, the type A cell. INA+ of the type A cell, unlike that of the type B cell, was, however, markedly increased following IP3 injection. The differences of IP3 effects on the two types of photoreceptors may be related to differences in regulation of ionic currents by endogenous IP3 as reflected by clear differences (before injection) in the magnitude of IA, ICa2+-K+, and INa+ between the two cell types.

Full text

PDF
797

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Acosta-Urquidi J., Alkon D. L., Neary J. T. Ca2+-dependent protein kinase injection in a photoreceptor mimics biophysical effects of associative learning. Science. 1984 Jun 15;224(4654):1254–1257. doi: 10.1126/science.6328653. [DOI] [PubMed] [Google Scholar]
  2. Akon D. L., Fuortes M. G. Responses of photoreceptors in Hermissenda. J Gen Physiol. 1972 Dec;60(6):631–649. doi: 10.1085/jgp.60.6.631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Alkon D. L., Farley J., Sakakibara M., Hay B. Voltage-dependent calcium and calcium-activated potassium currents of a molluscan photoreceptor. Biophys J. 1984 Nov;46(5):605–614. doi: 10.1016/S0006-3495(84)84059-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Alkon D. L., Grossman Y. Long-lasting depolarization and hyperpolarization in eye of Hermissenda. J Neurophysiol. 1978 Sep;41(5):1328–1342. doi: 10.1152/jn.1978.41.5.1328. [DOI] [PubMed] [Google Scholar]
  5. Alkon D. L., Kubota M., Neary J. T., Naito S., Coulter D., Rasmussen H. C-kinase activation prolongs Ca2+-dependent inactivation of K+ currents. Biochem Biophys Res Commun. 1986 Feb 13;134(3):1245–1253. doi: 10.1016/0006-291x(86)90384-0. [DOI] [PubMed] [Google Scholar]
  6. Alkon D. L., Lederhendler I., Shoukimas J. J. Primary changes of membrane currents during retention of associative learning. Science. 1982 Feb 5;215(4533):693–695. doi: 10.1126/science.7058334. [DOI] [PubMed] [Google Scholar]
  7. Alkon D. L. Responses of hair cells to statocyst rotation. J Gen Physiol. 1975 Oct;66(4):507–530. doi: 10.1085/jgp.66.4.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Alkon D. L., Sakakibara M. Calcium activates and inactivates a photoreceptor soma potassium current. Biophys J. 1985 Dec;48(6):983–995. doi: 10.1016/S0006-3495(85)83861-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Alkon D. L., Sakakibara M., Forman R., Harrigan J., Lederhendler I., Farley J. Reduction of two voltage-dependent K+ currents mediates retention of a learned association. Behav Neural Biol. 1985 Sep;44(2):278–300. doi: 10.1016/s0163-1047(85)90296-1. [DOI] [PubMed] [Google Scholar]
  10. Alkon D. L., Shoukimas J. J., Heldman E. Calcium-mediated decrease of a voltage-dependent potassium current. Biophys J. 1982 Dec;40(3):245–250. doi: 10.1016/S0006-3495(82)84479-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Alkon D. L. Voltage-dependent calcium and potassium ion conductances: a contingency mechanism for an associative learning model. Science. 1979 Aug 24;205(4408):810–816. doi: 10.1126/science.223244. [DOI] [PubMed] [Google Scholar]
  12. Berridge M. J., Irvine R. F. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature. 1984 Nov 22;312(5992):315–321. doi: 10.1038/312315a0. [DOI] [PubMed] [Google Scholar]
  13. Brown J. E., Rubin L. J., Ghalayini A. J., Tarver A. P., Irvine R. F., Berridge M. J., Anderson R. E. myo-Inositol polyphosphate may be a messenger for visual excitation in Limulus photoreceptors. Nature. 1984 Sep 13;311(5982):160–163. doi: 10.1038/311160a0. [DOI] [PubMed] [Google Scholar]
  14. Connor J., Alkon D. L. Light- and voltage-dependent increases of calcium ion concentration in molluscan photoreceptors. J Neurophysiol. 1984 Apr;51(4):745–752. doi: 10.1152/jn.1984.51.4.745. [DOI] [PubMed] [Google Scholar]
  15. Eckert R., Lux H. D. Calcium-dependent depression of a late outward current in snail neurons. Science. 1977 Jul 29;197(4302):472–475. doi: 10.1126/science.17921. [DOI] [PubMed] [Google Scholar]
  16. Eckert R., Tillotson D. L., Brehm P. Calcium-mediated control of Ca and K currents. Fed Proc. 1981 Jun;40(8):2226–2232. [PubMed] [Google Scholar]
  17. Eckert R., Tillotson D. L. Calcium-mediated inactivation of the calcium conductance in caesium-loaded giant neurones of Aplysia californica. J Physiol. 1981 May;314:265–280. doi: 10.1113/jphysiol.1981.sp013706. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Eckert R., Tillotson D. Potassium activation associated with intraneuronal free calcium. Science. 1978 Apr 28;200(4340):437–439. doi: 10.1126/science.644308. [DOI] [PubMed] [Google Scholar]
  19. Fein A., Payne R., Corson D. W., Berridge M. J., Irvine R. F. Photoreceptor excitation and adaptation by inositol 1,4,5-trisphosphate. Nature. 1984 Sep 13;311(5982):157–160. doi: 10.1038/311157a0. [DOI] [PubMed] [Google Scholar]
  20. Rasmussen H., Barrett P. Q. Calcium messenger system: an integrated view. Physiol Rev. 1984 Jul;64(3):938–984. doi: 10.1152/physrev.1984.64.3.938. [DOI] [PubMed] [Google Scholar]
  21. Sakakibara M., Alkon D. L., DeLorenzo R., Goldenring J. R., Neary J. T., Heldman E. Modulation of calcium-mediated inactivation of ionic currents by Ca2+/calmodulin-dependent protein kinase II. Biophys J. 1986 Aug;50(2):319–327. doi: 10.1016/S0006-3495(86)83465-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Stensaas L. J., Stensaas S. S., Trujillo-Cenóz O. Some morphological aspects of the visual system of Hermissenda crassicornis (Mollusca: Nudibranchia). J Ultrastruct Res. 1969 Jun;27(5):510–532. doi: 10.1016/s0022-5320(69)80047-x. [DOI] [PubMed] [Google Scholar]
  23. Tillotson D., Horn R. Inactivation without facilitation of calcium conductance in caesium-loaded neurones of Aplysia. Nature. 1978 May 25;273(5660):312–314. doi: 10.1038/273312a0. [DOI] [PubMed] [Google Scholar]
  24. Tillotson D. Inactivation of Ca conductance dependent on entry of Ca ions in molluscan neurons. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1497–1500. doi: 10.1073/pnas.76.3.1497. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES