Login to MyKarger

New to MyKarger? Click here to sign up.



Login with Facebook

Forgot your password?

Authors, Editors, Reviewers

For Manuscript Submission, Check or Review Login please go to Submission Websites List.

Submission Websites List

Institutional Login
(Shibboleth or Open Athens)

For the academic login, please select your country in the dropdown list. You will be redirected to verify your credentials.

A Crucial Role for cAMP and Protein Kinase A in D1 Dopamine Receptor Regulated Intracellular Calcium Transients

Dai R. · Ali M.K. · Lezcano N. · Bergson C.

Author affiliations

Department of Pharmacology and Toxicology, Medical College of Georgia, Augusta, Ga., USA

Corresponding Author

Clare M. Bergson

Department of Pharmacology and Toxicology, Medical College of Georgia

1459 Laney Walker Blvd

Augusta, GA 30912-2300 (USA)

Tel. +1 706 721 1926, Fax +1 706 721 2347, E-Mail cbergson@mail.mcg.edu

Related Articles for ""

Neurosignals 2008;16:112–123

Do you have an account?

Login Information





Contact Information










I have read the Karger Terms and Conditions and agree.



Abstract

D1-like dopamine receptors stimulate Ca2+ transients in neurons but the effector coupling and signaling mechanisms underlying these responses have not been elucidated. Here we investigated potential mechanisms using both HEK 293 cells that stably express D1 receptors (D1HEK293) and hippocampal neurons in culture. In D1HEK293 cells, the full D1 receptor agonist SKF 81297 evoked a robust dose-dependent increase in Ca2+i following ‘priming’ of endogenous Gq/11-coupled muscarinic or purinergic receptors. The effect of SKF81297 could be mimicked by forskolin or 8-Br-cAMP. Further, cholera toxin and the cAMP-dependent protein kinase (PKA) inhibitors, KT5720 and H89, as well as thapsigargin abrogated the D1 receptor evoked Ca2+ transients. Removal of the priming agonist and treatment with the phospholipase C inhibitor U73122 also blocked the SKF81297-evoked responses. D1R agonist did not stimulate IP3 production, but pretreatment of cells with the D1R agonist potentiated Gq-linked receptor agonist mobilization of intracellular Ca2+ stores. In neurons, SKF81297 and SKF83959, a partial D1 receptor agonist, promoted Ca2+ oscillations in response to Gq/11-coupled metabotropic glutamate receptor (mGluR) stimulation. The effects of both D1R agonists on the mGluR-evoked Ca2+ responses were PKA dependent. Altogether the data suggest that dopamine D1R activation and ensuing cAMP production dynamically regulates the efficiency and timing of IP3-mediated intracellular Ca2+ store mobilization.

© 2008 S. Karger AG, Basel


References

  1. Missale C, Nash SR, Robinson SW, Jaber M, Caron MG: Dopamine receptors: from structure to function. Physiol Rev 1998;78:189–225.
  2. Smiley JF, Levey AI, Ciliax BJ, Goldman-Rakic PS: D1 dopamine receptor immunoreactivity in human and monkey cerebral cortex: predominant and extrasynaptic localization in dendritic spines. Proc Natl Acad Sci USA 1994;91:5720–5724.
  3. Paspalas CD, Goldman-Rakic PS: Presynaptic D1 dopamine receptors in primate prefrontal cortex: target-specific expression in the glutamatergic synapse. J Neurosci 2005;25:1260–1267.
  4. Goldman-Rakic PS, Muly EC, III, Williams GV: D(1) receptors in prefrontal cells and circuits. Brain Res Brain Res Rev 2000;31:295–301.
  5. Bergson C, Mrzljak L, Smiley JF, Pappy M, Levenson R, Goldman-Rakic PS: Regional, cellular, and subcellular variations in the distribution of D1 and D5 dopamine receptors in primate brain. J Neurosci 1995;15:7821–7836.
  6. Arnt J, Hyttel J, Sanchez C: Partial and full dopamine D1 receptor agonists in mice and rats: relation between behavioural effects and stimulation of adenylate cyclase activity in vitro. Eur J Pharmacol 1992;213:259–267.
  7. Tang TS, Bezprozvanny I: Dopamine receptor-mediated Ca(2+) signaling in striatal medium spiny neurons. J Biol Chem 2004;279:42082–42094.
  8. Lezcano N, Bergson C: D1/D5 dopamine receptors stimulate intracellular calcium release in primary cultures of neocortical and hippocampal neurons. J Neurophysiol 2002;87:2167–2175.
  9. Rashid AJ, So CH, Kong MM, et al: D1-D2 dopamine receptor heterooligomers with unique pharmacology are coupled to rapid activation of Gq/11 in the striatum. Proc Natl Acad Sci USA 2007;104:654–659.
  10. Mahan LC, Burch RM, Monsma FJ Jr, Sibley DR: Expression of striatal D1 dopamine receptors coupled to inositol phosphate production and Ca2+ mobilization in Xenopus oocytes. Proc Natl Acad Sci USA 1990;87:2196–2200.
  11. Ming Y, Zhang H, Long L, Wang F, Chen J, Zhen X: Modulation of Ca2+ signals by phosphatidylinositol-linked novel D1 dopamine receptor in hippocampal neurons. J Neurochem 2006;98:1316–1323.
  12. Redmond L, Kashani AH, Ghosh A: Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron 2002;34:999–1010.
  13. Malinow R, Malenka RC: AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 2002;25:103–126.
  14. Roussel C, Erneux T, Schiffmann SN, Gall D: Modulation of neuronal excitability by intracellular calcium buffering: from spiking to bursting. Cell Calcium 2006;39:455–466.
  15. Sudhof TC: The synaptic vesicle cycle. Annu Rev Neurosci 2004;27:509–547.
  16. West AE, Chen WG, Dalva MB, et al: Calcium regulation of neuronal gene expression. Proc Natl Acad Sci USA 2001;98:11024–11031.
  17. Calderon DP, Leverkova N, Peinado A: Gq/11-induced and spontaneous waves of coordinated network activation in developing frontal cortex. J Neurosci 2005;25:1737–1749.
  18. Otani S, Auclair N, Desce JM, Roisin MP, Crepel F: Dopamine receptors and groups I and II mGluRs cooperate for long-term depression induction in rat prefrontal cortex through converging postsynaptic activation of MAP kinases. J Neurosci 1999;19:9788–9802.
  19. Jin LQ, Goswami S, Cai G, Zhen X, Friedman E: SKF83959 selectively regulates phosphatidylinositol-linked D1 dopamine receptors in rat brain. J Neurochem 2003;85:378–386.
  20. Panchalingam S, Undie AS: Physicochemical modulation of agonist-induced [35s] GTPgammaS binding: implications for coexistence of multiple functional conformations of dopamine D1-like receptors. J Recept Signal Transduct Res 2005;25:125–146.
  21. Ali MK, Bergson C: Elevated intracellular calcium triggers recruitment of the receptor cross-talk accessory protein calcyon to the plasma membrane. J Biol Chem 2003;278:51654–51663.
  22. Islam M, Akhtar RA: Epidermal growth factor stimulates phospholipase cgamma1 in cultured rabbit corneal epithelial cells. Exp Eye Res 2000;70:261–269.
  23. Wang Q, Mullah BK, Robishaw JD: Ribozyme approach identifies a functional association between the G protein beta1gamma7 subunits in the beta-adrenergic receptor signaling pathway. J Biol Chem 1999;274:17365–17371.
  24. Mundell SJ, Benovic JL: Selective regulation of endogenous G protein-coupled receptors by arrestins in HEK293 cells. J Biol Chem 2000;275:12900–12908.
  25. Tovey SC, Goraya TA, Taylor CW: Parathyroid hormone increases the sensitivity of inositol trisphosphate receptors by a mechanism that is independent of cyclic AMP. Br J Pharmacol 2003;138:81–90.
  26. Short AD, Taylor CW: Parathyroid hormone controls the size of the intracellular Ca(2+) stores available to receptors linked to inositol trisphosphate formation. J Biol Chem 2000;275:1807–1813.
  27. Buckley KA, Wagstaff SC, McKay G, et al: Parathyroid hormone potentiates nucleotide-induced [Ca2+]i release in rat osteoblasts independently of Gq activation or cyclic monophosphate accumulation. A mechanism for localizing systemic responses in bone. J Biol Chem 2001;276:9565–9571.
  28. Werry TD, Wilkinson GF, Willars GB: Mechanisms of cross-talk between G-protein-coupled receptors resulting in enhanced release of intracellular Ca2+. Biochem J 2003;374:281–296.
  29. Werry TD, Christie MI, Dainty IA, Wilkinson GF, Willars GB: Ca(2+) signalling by recombinant human CXCR2 chemokine receptors is potentiated by P2Y nucleotide receptors in HEK cells. Br J Pharmacol 2002;135:1199–1208.
  30. Quitterer U, Lohse MJ: Crosstalk between Galpha(i)- and Galpha(q)-coupled receptors is mediated by Gbetagamma exchange. Proc Natl Acad Sci USA 1999;96:10626–10631.
  31. Yeo A, Samways DS, Fowler CE, Gunn-Moore F, Henderson G: Coincident signalling between the Gi/Go-coupled delta-opioid receptor and the Gq-coupled m3 muscarinic receptor at the level of intracellular free calcium in SH-SY5Y cells. J Neurochem 2001;76:1688–1700.
  32. Chan JS, Lee JW, Ho MK, Wong YH: Preactivation permits subsequent stimulation of phospholipase C by G(i)-coupled receptors. Mol Pharmacol 2000;57:700–708.
  33. Zaccolo M, Pozzan T: CAMP and Ca2+ interplay: a matter of oscillation patterns. Trends Neurosci 2003;26:53–55.
  34. Gorbunova YV, Spitzer NC: Dynamic interactions of cyclic AMP transients and spontaneous Ca(2+) spikes. Nature 2002;418:93–96.
  35. Schmidt M, Evellin S, Weernink PA, et al: A new phospholipase-C-calcium signalling pathway mediated by cyclic AMP and a Rap GTPase. Nat Cell Biol 2001;3:1020–1024.
  36. Tang TS, Tu H, Wang Z, Bezprozvanny I: Modulation of type 1 inositol (1,4,5)-trisphosphate receptor function by protein kinase a and protein phosphatase 1alpha. J Neurosci 2003;23:403–415.
  37. Bruce JI, Straub SV, Yule DI: Crosstalk between cAMP and Ca2+ signaling in non-excitable cells. Cell Calcium 2003;34:431–444.
  38. Tu H, Tang TS, Wang Z, Bezprozvanny I: Association of type 1 inositol 1,4,5-trisphosphate receptor with AKAP9 (Yotiao) and protein kinase A. J Biol Chem 2004;279:19375–19382.
  39. Jacob SN, Choe CU, Uhlen P, DeGray B, Yeckel MF, Ehrlich BE: Signaling microdomains regulate inositol 1,4,5-trisphosphate-mediated intracellular calcium transients in cultured neurons. J Neurosci 2005;25:2853–2864.
  40. Wojcikiewicz RJ, Luo SG: Phosphorylation of inositol 1,4,5-trisphosphate receptors by cAMP-dependent protein kinase: type I, II, and III receptors are differentially susceptible to phosphorylation and are phosphorylated in intact cells. J Biol Chem 1998;273:5670–5677.
  41. Wagner LE, Li WH, Joseph SK, Yule DI: Functional consequences of phosphomimetic mutations at key cAMP-dependent protein kinase phosphorylation sites in the type 1 inositol 1,4,5-trisphosphate receptor. J Biol Chem 2004;279:46242–46252.
  42. Brown DA, Bruce JI, Straub SV, Yule DI: cAMP potentiates ATP-evoked calcium signaling in human parotid acinar cells. J Biol Chem 2004;279:39485–39494.
  43. Sneyd J, Tsaneva-Atanasova K, Yule DI, Thompson JL, Shuttleworth TJ: Control of calcium oscillations by membrane fluxes. Proc Natl Acad Sci USA 2004;101:1392–1396.
  44. Chatton JY, Cao Y, Liu H, Stucki JW: Permissive role of cAMP in the oscillatory Ca2+ response to inositol 1,4,5-trisphosphate in rat hepatocytes. Biochem J 1998;330:1411–1416.
  45. Bezprozvanny I: The inositol 1,4,5-trisphosphate receptors. Cell Calcium 2005;38:261–272.
  46. Nash MS, Schell MJ, Atkinson PJ, Johnston NR, Nahorski SR, Challiss RA: Determinants of metabotropic glutamate receptor-5-mediated Ca2+ and inositol 1,4,5-trisphosphate oscillation frequency: receptor density versus agonist concentration. J Biol Chem 2002;277:35947–35960.
  47. Tateyama M, Kubo Y: Dual signaling is differentially activated by different active states of the metabotropic glutamate receptor 1alpha. Proc Natl Acad Sci USA 2006;103:1124–1128.
  48. Wang HY, Undie AS, Friedman E: Evidence for the coupling of Gq protein to D1-like dopamine sites in rat striatum: possible role in dopamine-mediated inositol phosphate formation. Mol Pharmacol 1995;48:988–994.
  49. Lee SP, So CH, Rashid AJ, et al: Dopamine D1 and D2 receptor Co-activation generates a novel phospholipase C-mediated calcium signal. J Biol Chem 2004;279:35671–35678.
  50. Cordeaux Y, Hill SJ: Mechanisms of cross-talk between G-protein-coupled receptors. Neurosignals 2002;11:45–57.
  51. Dolmetsch RE, Xu K, Lewis RS: Calcium oscillations increase the efficiency and specificity of gene expression. Nature 1998;392:933–936.
  52. Konradi C, Cole RL, Heckers S, Hyman SE: Amphetamine regulates gene expression in rat striatum via transcription factor CREB. J Neurosci 1994;14:5623–5634.
  53. Koob GF, Nestler EJ: The neurobiology of drug addiction. J Neuropsychiatry Clin Neurosci 1997;9:482–497.
  54. Kalivas PW, Volkow ND: The neural basis of addiction: pathology of motivation and choice. Am J Psychiatry 2005;162:1403–1413.

Article / Publication Details

First-Page Preview
Abstract of Paper

Published online: February 05, 2008
Issue release date: February 2008

Number of Print Pages: 12
Number of Figures: 5
Number of Tables: 0

ISSN: 1424-862X (Print)
eISSN: 1424-8638 (Online)

For additional information: https://www.karger.com/NSG


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.