Logo of pnasPNASInfo for AuthorsSubscriptionsAboutThis Article
Proc Natl Acad Sci U S A. Jun 1983; 80(11): 3522–3525.
PMCID: PMC394077

Serotonin increases an anomalously rectifying K+ current in the Aplysia neuron R15.

Abstract

Previous work has shown that serotonin causes an increase in K+ conductance in the identified Aplysia neuron R15. This response is mediated by cAMP-dependent protein phosphorylation. The results presented here show that the K+ channel modulated by serotonin is an anomalous or inward rectifier (designated IR) that is present in R15 together with the three other distinct K+ channels previously described for this cell. Several lines of evidence indicate that this inward rectifier is partially activated in the resting cell and is further activated by serotonin. Voltage clamp analysis of resting and serotonin-evoked membrane currents at various external K+ concentrations shows that both currents have reversal potentials close to the potassium equilibrium potential, exhibit similar dependences in magnitude on external K+ concentration, and display marked anomalous rectification. The effects of particular monovalent and divalent cations are also similar on the resting and serotonin-evoked currents. Rb+, Cs+, and Ba2+ block both currents while Tl+ can substitute for K+ as a charge carrier and channel activator in both. These properties are characteristics of anomalous rectifiers in other systems. Furthermore, measurement of the voltage dependence of inactivation for the fast transient K+ current shows that this current cannot account for the anomalously rectifying K+ conductance in R15. The inward rectifier is therefore a separate current mediated by its own channels, the activity of which can be modulated by serotonin.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (680K), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Adrian RH. Rectification in muscle membrane. Prog Biophys Mol Biol. 1969;19(2):339–369. [PubMed]
  • ADRIAN RH, FREYGANG WH. Potassium conductance of frog muscle membrane under controlled voltage. J Physiol. 1962 Aug;163:104–114. [PMC free article] [PubMed]
  • Noble SJ. Potassium accumulation and depletion in frog atrial muscle. J Physiol. 1976 Jul;258(3):579–613. [PMC free article] [PubMed]
  • Dudel J, Peper K, Rüdel R, Trautwein W. The potassium component of membrane current in Purkinje fibers. Pflugers Arch Gesamte Physiol Menschen Tiere. 1967;296(4):308–327. [PubMed]
  • Cleemann L, Morad M. Potassium currents in frog ventricular muscle: evidence from voltage clamp currents and extracellular K accumulation. J Physiol. 1979 Jan;286:113–143. [PMC free article] [PubMed]
  • Clay JR, Shrier A. Analysis of subthreshold pace-maker currents in chick embryonic heart cells. J Physiol. 1981 Mar;312:471–490. [PMC free article] [PubMed]
  • Ohmori H. Inactivation kinetics and steady-state current noise in the anomalous rectifier of tunicate egg cell membranes. J Physiol. 1978 Aug;281:77–99. [PMC free article] [PubMed]
  • Hagiwara S, Takahashi K. The anomalous rectification and cation selectivity of the membrane of a starfish egg cell. J Membr Biol. 1974;18(1):61–80. [PubMed]
  • Kandel ER, Tauc L. Anomalous rectification in the metacerebral giant cells and its consequences for synaptic transmission. J Physiol. 1966 Mar;183(2):287–304. [PMC free article] [PubMed]
  • Ochs AL. Changes in membrane properties with hyperpolarization in snail neurons. Am J Physiol. 1967 Jul;213(1):16–20. [PubMed]
  • Nelson PG, Frank K. Anomalous rectification in cat spinal motoneurons and effect of polarizing currents on excitatory postsynaptic potential. J Neurophysiol. 1967 Sep;30(5):1097–1113. [PubMed]
  • Hotson JR, Prince DA, Schwartzkroin PA. Anomalous inward rectification in hippocampal neurons. J Neurophysiol. 1979 May;42(3):889–895. [PubMed]
  • Eckert R, Lux HD. A non-inactivating inward current recorded during small depolarizing voltage steps in snail pacemaker neurons. Brain Res. 1975 Jan 17;83(3):486–489. [PubMed]
  • HAGIWARA S, KUSANO K, SAITO N. Membrane changes of Onchidium nerve cell in potassium-rich media. J Physiol. 1961 Mar;155:470–489. [PMC free article] [PubMed]
  • Neher E. Two fast transient current components during voltage clamp on snail neurons. J Gen Physiol. 1971 Jul;58(1):36–53. [PMC free article] [PubMed]
  • Gola M, Romey G. Responses anomales a des courants sous-liminaires de certaines membranes somatiques (neurones géants d'Helix pomatia). Analyse par la methode du voltage impose. Pflugers Arch. 1971;327(2):105–131. [PubMed]
  • Farber DS, Klee MR. Membrane characteristics of bursting pacemaker neurones in Aplysia. Nat New Biol. 1972 Nov 1;240(96):29–31. [PubMed]
  • Drummond AH, Benson JA, Levitan IB. Serotonin-induced hyperpolarization of an indentified Aplysia neuron is mediated by cyclic AMP. Proc Natl Acad Sci U S A. 1980 Aug;77(8):5013–5017. [PMC free article] [PubMed]
  • Leech CA, Stanfield PR. Inward rectification in frog skeletal muscle fibres and its dependence on membrane potential and external potassium. J Physiol. 1981;319:295–309. [PMC free article] [PubMed]
  • Meunier JM, Tauc L. Participation d'une pompe métabolique au potentiel de repos de neurones d'aplysie. J Physiol (Paris) 1970;62 (Suppl 1):192–193. [PubMed]
  • Marmor MF. The effects of temperature and ions on the current-voltage relation and electrical characteristics of a molluscan neurone. J Physiol. 1971 Nov;218(3):573–598. [PMC free article] [PubMed]
  • Standen NB, Stanfield PR. A potential- and time-dependent blockade of inward rectification in frog skeletal muscle fibres by barium and strontium ions. J Physiol. 1978 Jul;280:169–191. [PMC free article] [PubMed]
  • Hagiwara S, Miyazaki S, Moody W, Patlak J. Blocking effects of barium and hydrogen ions on the potassium current during anomalous rectification in the starfish egg. J Physiol. 1978 Jun;279:167–185. [PMC free article] [PubMed]
  • Reuter H, Stevens CF. Ion conductance and ion selectivity of potassium channels in snail neurones. J Membr Biol. 1980 Dec 15;57(2):103–118. [PubMed]
  • Standen NB, Stanfield PR. Rubidium block and rubidium permeability of the inward rectifier of frog skeletal muscle fibres. J Physiol. 1980 Jul;304:415–435. [PMC free article] [PubMed]
  • Isenberg G. Cardiac Purkinje fibers: cesium as a tool to block inward rectifying potassium currents. Pflugers Arch. 1976 Sep 30;365(2-3):99–106. [PubMed]
  • Landowne D. A comparison of radioactive thallium and potassium fluxes in the giant axon of the squid. J Physiol. 1975 Oct;252(1):79–96. [PMC free article] [PubMed]
  • Hagiwara S, Miyazaki S, Krasne S, Ciani S. Anomalous permeabilities of the egg cell membrane of a starfish in K+-Tl+ mixtures. J Gen Physiol. 1977 Sep;70(3):269–281. [PMC free article] [PubMed]
  • Stanfield PR, Ashcroft FM, Plant TD. Gating of a muscle K+ channel and its dependence on the permeating ion species. Nature. 1981 Feb 5;289(5797):509–511. [PubMed]
  • Adams WB, Levitan IB. Intracellular injection of protein kinase inhibitor blocks the serotonin-induced increase in K+ conductance in Aplysia neuron R15. Proc Natl Acad Sci U S A. 1982 Jun;79(12):3877–3880. [PMC free article] [PubMed]
  • Lemos JR, Novak-Hofer I, Levitan IB. Serotonin alters the phosphorylation of specific proteins inside a single living nerve cell. Nature. 1982 Jul 1;298(5869):64–65. [PubMed]
  • Kaczmarek LK, Jennings KR, Strumwasser F, Nairn AC, Walter U, Wilson FD, Greengard P. Microinjection of catalytic subunit of cyclic AMP-dependent protein kinase enhances calcium action potentials of bag cell neurons in cell culture. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7487–7491. [PMC free article] [PubMed]
  • Castellucci VF, Kandel ER, Schwartz JH, Wilson FD, Nairn AC, Greengard P. Intracellular injection of t he catalytic subunit of cyclic AMP-dependent protein kinase simulates facilitation of transmitter release underlying behavioral sensitization in Aplysia. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7492–7496. [PMC free article] [PubMed]
  • de Peyer JE, Cachelin AB, Levitan IB, Reuter H. Ca2+ -activated K+ conductance in internally perfused snail neurons is enhanced by protein phosphorylation. Proc Natl Acad Sci U S A. 1982 Jul;79(13):4207–4211. [PMC free article] [PubMed]
  • Gorman AL, Hermann A, Thomas MV. Ionic requirements for membrane oscillations and their dependence on the calcium concentration in a molluscan pace-maker neurone. J Physiol. 1982 Jun;327:185–217. [PMC free article] [PubMed]
  • HUTTER OF, NOBLE D. Rectifying properties of heart muscle. Nature. 1960 Nov 5;188:495–495. [PubMed]
  • Carmeliet E, Ramon J. Effect of acetylcholine on time-independent currents in sheep cardiac Purkinje fibers. Pflugers Arch. 1980 Sep;387(3):207–216. [PubMed]
  • Ojeda C, Rougier O, Tourneur Y. Effects of Cs on acetylcholine induced current. Is ik1 increased by acetylcholine in frog atrium? Pflugers Arch. 1981 Jul;391(1):57–59. [PubMed]
  • Ohmori H, Yoshida S, Hagiwara S. Single K+ channel currents of anomalous rectification in cultured rat myotubes. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4960–4964. [PMC free article] [PubMed]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...