Presynaptic GABAB receptors regulate retinohypothalamic tract synaptic transmission by inhibiting voltage-gated Ca2+ channels

Journal of Neurophysiology

Volumn 95, Issue 6, 2006, Pages 3727-3741

  Moldavan, Mykhaylo G ^a   Irwin, Robert P ^a   Allen, Charles N ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOPYRIDINE; BACLOFEN; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL N TYPE; CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; CALCIUM CHANNEL R TYPE; CALCIUM CHANNEL T TYPE; CALCIUM ION; FLUORESCENT DYE; GLUTAMIC ACID; MIBEFRADIL; NIMODIPINE; OMEGA AGATOXIN; OMEGA CONOTOXIN; POTASSIUM CHANNEL; SNX 482; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVATION; ENZYME INHIBITION; EVOKED MUSCLE RESPONSE; EXTRACELLULAR CALCIUM; HYPOTHALAMUS; MALE; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTSYNAPTIC INHIBITION; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; RAT; RETINA; SUPRACHIASMATIC NUCLEUS; SYNAPTIC TRANSMISSION; SYNAPTOSOME; THALAMOCORTICAL TRACT; VOLTAGE CLAMP;

AFFERENT PATHWAYS; ANIMALS; CALCIUM CHANNELS; CELLS, CULTURED; HYPOTHALAMUS; ION CHANNEL GATING; MALE; NEURAL INHIBITION; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-B; RECEPTORS, PRESYNAPTIC; RETINA; SYNAPTIC TRANSMISSION;

EID: 33744920082     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00909.2005     Document Type: Article

References (71)

1. Agler HL, Evans J, Colecraft HM, and Yue DT. Custom distinctions in the interaction of G-protein beta subunits with N-type (CaV2.2) versus P/Q-type (CaV2.1) calcium channels. J Gen Physiol 121: 495-510, 2003.
2. Andrade R, Malenka RC, and Nicoll RA. A G-protein couples serotonin and GABAB receptors to the same channels in hippocampus. Science 234: 1261-1265, 1986.
3. Barnes-Davies M and Forsythe ID. Pre- and postsynaptic glutamate receptors at a giant excitatory synapse in rat auditory brainstem slices. J Physiol 488: 387-406, 1995.
4. Berson DM, Dunn FA, and Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science 295: 1070-1073, 2002.
5. Bertram R, Swanson J, Yousef M, Feng ZP, and Zamponi GW. A minimal model for G protein-mediated synaptic facilitation and depression. J Neurophysiol 90: 1643-1653, 2003.
6. Bettler B, Kaupmann K, Mosbacher J, and Gassmann M. Molecular structure and physiological functions of GABA(B) receptors. Physiol Rev 84: 835-867, 2004.
7. 2+ channel antagonist mibefradil (Ro 40-5967). Mol Pharmacol 48: 540-549, 1995.
8. Bramley JR, Sollars PJ, Pickard GE, and Dudek FE. 5-HT1B receptormediated presynaptic inhibition of GABA release in the suprachiasmatic nucleus. J Neurophysiol 93: 3157-3164, 2005.
9. 2+ channels and anoxic injury in rat CNS white matter. J Neurophysiol 85: 900-911, 2001.
10. Card JP and Moore RY. The organization of visual circuits influencing the circadian activity of the suprachiasmatic nucleus. In: Suprachiasmatic Nucleus - The Mind's Clock, edited by Klein DC, Moore RY, and Reppert SM. Oxford, UK: Oxford Univ. Press, 1991, p. 51-76.
11. Castel M, Belenky M, Cohen S, Ottersen OP, and Storm-Mathisen J. Glutamate-like immunoreactivity in retinal terminals of the mouse suprachiasmatic nucleus. Eur J Neurosci 5: 368-381, 1993.
12. Chen G and Van den Pol AN. Presynaptic GABAB autoreceptor modulation of P/Q-type calcium channels and GABA release in rat suprachiasmatic nucleus neurons. Neuroscience 18: 1913-1922, 1998.
13. Chen L, Yu YC, Zhao JW, and Yang XL. Inwardly rectifying potassium channels in rat retinal ganglion cells. Eur J Neurosci 20: 956-964, 2004.
14. Childers SR, Pacheco MA, Bennett BA, Edwards TA, Hampson RE, Mu J, and Deadwyler SA. Cannabinoid receptors: G-protein-mediated signal transduction mechanisms. Biochem Soc Symp 59: 27-50, 1993.
15. Colwell CS. Circadian modulation of calcium levels in cells in the suprachiasmatic nucleus. Eur J Neurosci 12: 571-576, 2000.
16. Colwell CS, Kaufman CM, and Menaker M. Photic induction of Fos in the hamster suprachiasmatic nucleus is inhibited by baclofen but not by diazepam or bicuculline. Neurosci Lett 163: 177-181, 1993.
17. Cui LN, Coderre E, and Renaud LP. GABA(B) presynaptically modulates suprachiasmatic input to hypothalamic paraventricular magnocellular neurons. Am J Physiol Regul Integr Comp Physiol 278: R1210-R1216, 2000.
18. De Jeu M, Geurtsen A, and Pennartz C. A Ba(2+)-sensitive K(+) current contributes to the resting membrane potential of neurons in rat suprachiasmatic nucleus. J Neurophysiol 88: 869-878, 2002.
19. Dittman JS and Regehr WG. Contributions of calcium-dependent and calcium-independent mechanisms to presynaptic inhibition at a cerebellar synapse. Neuroscience 16: 1623-1633, 1996.
20. Forsythe ID. Direct patch recording from identified presynaptic terminals mediating glutamatergic EPSCs in the rat CNS, in vitro. J Physiol 479: 381-387, 1994.
21. 2+ signals and calcium channels in axons of developing rat cerebellar interneurones. J Physiol 527: 33-48, 2000.
22. Gannon RL, Cato MJ, Kelley KH, Armstrong DL, and Rea MA. GABAergic modulation of optic nerve-evoked field potentials in the rat suprachiasmatic nucleus. Brain Res 694: 264-270, 1995.
23. Gillespie CF, Mintz EM, Marvel CL, Huhman KL, and Albers HE. GABAA and GABAB agonists and antagonists alter the phase-shifting effects of light when microinjected into the suprachiasmatic region. Brain Res 759: 181-189, 1997.
24. Gillespie CF, Van der Beek EM, Mintz EM, Mickley NC, Jasnow AM, Huhman KL, and Albers HE. GABAergic regulation of light-induced c-Fos immunoreactivity within the suprachiasmatic nucleus. J Comp Neurol 411: 683-692, 1999.
25. Gompf HS, Moldavan MG, Irwin RP, and Allen CN. Nociceptin/orphanin FQ (N/OFQ) inhibits excitatory and inhibitory synaptic signaling in the suprachiasmatic nucleus (SCN). J Neurosci Methods 132: 955-965, 2005.
26. Gooley JJ, Lu J, Fischer D, and Saper CB. A broad role for melanopsin in nonvisual photoreception. Neuroscience 23: 7093-7106, 2003.
27. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450, 1985.
28. Guenther E, Rothe T, Taschenberger H, and Grantyn R. Separation of calcium currents in retinal ganglion cells from postnatal rat. Brain Res 633: 223-235, 1994.
29. Hoss W and Labkovsky B. Inactivation of depolarization-induced calcium uptake in rat brain synaptosomes. Neurochem Res 11: 1361-1372, 1986.
30. Isaacson JS. GABAB receptor-mediated modulation of presynaptic currents and excitatory transmission at a fast central synapse. J Neurophysiol 80: 1571-1576, 1998.
31. Ishikawa T, Nakamura Y, Saitoh N, Li WB, Iwasaki S, and Takahashi T. Distinct roles of Kv1 and Kv3 potassium channels at the calyx of Held presynaptic terminal. Neuroscience 23: 10445-10453, 2003.
32. Jiang Z-G, Allen CN, and North RA. Presynatic inhibition by baclofen of retinohypothalamic excitatory synaptic transmission in rat suprachiasmatic nucleus. J Neurosci Methods 64: 813-819, 1995.
33. Kajikawa Y, Saitoh N, and Takahashi T. GTP-binding protein beta gamma subunits mediate presynaptic calcium current inhibition by GABA(B) receptor. Proc Natl Acad Sci USA 98: 8054-8058, 2001.
34. Kirsch GE and Drewe JA. Gating-dependent mechanism of 4-aminopyridine block in two related potassium channels. J Gen Physiol 102: 797-816, 1993.
35. Kishimoto K, Koyama S, and Akaike N. Synergistic mu-opioid and 5-HT1A presynaptic inhibition of GABA release in rat periaqueductal gray neurons. Neuropharmacology 41: 529-538, 2001.
36. Lacinova L. Pharmacology of recombinant low-voltage activated calcium channels. Curr Drug Targets CNS Neurol Disord 33: 105-111, 2004.
37. Lewy AJ, Sack RL, Miller LS, and Hoban TM. Antidepressant and circadian phase-shifting effects of light. Science 235: 352-354, 1987.
38. Liang Y, Yuan L-Y, Johnston D, and Gray R. Calcium signaling at single mossy fiber presynaptic terminals in the rat hippocampus. J Neurophysiol 87: 1132-1137, 2002.
39. Liou SY, Shibata S, Iwasaki K, and Ueki S. Optic nerve stimulation-induced increase of release of 3H-glutamate and 3H-aspartate but not 3H-GABA from the suprachiasmatic nucleus in slices of rat hypothalamus. Brain Res Bull 16: 527-531, 1986.
40. + currents in human fusion-competent myoblasts. Br J Pharmacol 126: 245-250, 1999.
41. Luebke JI, Dunlap K, and Turner TJ. Multiple calcium channel types control glutamatergic synaptic transmission in the hippocampus. Neuron 11: 895-902, 1993.
42. + channels (GIRKs) mediate postsynaptic but not presynaptic transmitter actions in hippocampal neurons. Neuron 19: 687-695, 1997.
43. Mintz IM, Sabatini BL, and Regehr WG. Calcium control of transmitter release at a central synapse. Neuron 15: 675-688, 1995.
44. Moore RY, Speh JC, and Card JP. The retinohypothalamic tract originates from a distinct subset of retinal ganglion cells. J Comp Neurol 352: 351-366, 1995.
45. Morin LP, Blanchard JH, and Provencio I. Retinal ganglion cell projections to the hamster suprachiasmatic nucleus, intergeniculate leaflet, and visual midbrain: bifurcation and melanopsin immunoreactivity. J Comp Neurol 465: 401-416, 2003.
46. Pickard GE and Rea MA. TFMPP, a 5HT1B receptor agonist, inhibits light-induced phase shifts of the circadian activity rhythm and c-fos expression in the mouse suprachiasmatic nucleus. Neurosci Lett 231: 95-98, 1997.
47. Pickard GE, Smith BN, Belenky M, Rea MA, Dudek FE, and Sollars PJ. 5-HT1B receptor-mediated presynaptic inhibition of retinal input to the suprachiasmatic nucleus. Neuroscience 19: 4034-4045, 1999.
48. Pickard GE, Weber ET, Scott PA, Riberdy AF, and Rea MA. 5HT1B receptor agonists inhibit light-induced phase shifts of behavioral circadian rhythms and expression of the immediate-early gene c-fos in the suprachiasmatic nucleus. Neuroscience 16: 8208-8220, 1996.
49. Ralph MR and Menaker M. GABA regulation of circadian responses to light. I. Involvement of GABAA-benzodiazepine and GABAB receptors. Neuroscience 9: 2858-2865, 1989.
50. Regehr WG and Mintz IM. Participation of multiple calcium channel types in transmission at single climbing fiber to Purkinje cell synapses. Neuron 12: 605-613, 1994.
51. 2+ channels mediate transmitter release with a similar cooperativity at rat hippocampal autapses. Neuroscience 18: 2849-2855, 1998.
52. 2+ channels: a functional patchwork. Trends Neurosci 26: 683-687, 2003.
53. Reiff DF and Guenther E. Developmental changes in voltage-activated potassium currents of rat retinal ganglion cells. J Neurosci Methods 92: 1103-1117, 1999.
54. Saint DA, Thomas T, and Gage PW. GABAB agonists modulate a transient potassium current in cultured mammalian hippocampal neurons. Neurosci Lett 118: 9-13, 1990.
55. Sakaba T and Neher E. Direct modulation of synaptic vesicle priming by GABA(B) receptor activation at a glutamatergic synapse. Nature 424: 775-778, 2003.
56. Scholz KP and Miller RJ. Developmental changes in presynaptic calcium channels coupled to glutamate release in cultured rat hippocampal neurons. Neuroscience 15: 4612-4617, 1995.
57. Slaughter MM. GABAb receptors in the vertebrate retina. Prog Retin Eye Res 14: 293-312, 1995.
58. Sodickson DL and Bean BP. GABAB receptor-activated inwardly rectifying potassium current in dissociated hippocampal CA3 neurons. Neuroscience 16: 6374-6385, 1996.
59. 1B receptor knockout mouse. J Biol Rhythm 21: 1-12, 2006.
60. Sollars PJ, Smeraski CA, Kaufman JD, Ogilvie MD, Provencio I, and Pickard GE. Melanopsin and non-melanopsin expressing retinal ganglion cells innervate the hypothalamic suprachiasmatic nucleus. Vis Neurosci 20: 601-610, 2003.
61. Sun BB and Chiu SY. N-type calcium channels and their regulation by GABAB receptors in axons of neonatal rat optic nerve. Neuroscience 19: 5185-5194, 1999.
62. Takahashi T, Kajikawa Y, and Tsujimoto T. G-protein-coupled modulation of presynaptic calcium currents and transmitter release by a GABAB receptor. Neuroscience 18: 3138-3146, 1998.
63. Takeda M, Tanimoto T, Ikeda M, Kadoi J, and Matsumoto S. Activaton of GABAB receptor inhibits the excitability of rat small diameter trigeminal root ganglion neurons. Neuroscience 123: 491-505, 2004.
64. Thompson SM and Gahwiler BH. Comparison of the actions of baclofen at pre- and postsynaptic receptors in the rat hippocampus in vitro. J Physiol 451: 329-345, 1992.
65. Tottene A, Volsen S, and Pietrobon D. alpha(1E) subunits form the pore of three cerebellar R-type calcium channels with different pharmacological and permeation properties. Neuroscience 20: 171-178, 2000.
66. Verbny Y, Zhang CL, and Chiu SY. Coupling of calcium homeostasis to axonal sodium in axons of mouse optic nerve. J Neurophysiol 88: 802-816, 2002.
67. Viana F, Van den Bosch L, Missiaen L, Vandenberghe W, Droogmans G, Nilius B, and Robberecht W. Mibefradil (Ro 40-5967) blocks multiple types of voltage-gated calcium channels in cultured rat spinal motoneurones. Cell Calcium 22: 299-311, 1997.
68. 2+ channels in rat hippocampus. Neuroscience 16: 2226-2237, 1996.
69. Wu LG and Saggau P. Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci 20: 204-212, 1997.
70. Yuste R. Loading brain slices with AM esters of calcium indicators. In: Imaging Neurons: A Laboratory Manual, edited by Yuste R, Lanni R, and Konnerth A. Plainview, NY: Cold Spring Harbor Laboratory Press, 2000, p. 34.
71. Zamponi GW and Snutch TP. Modulation of voltage-dependent calcium channels by G proteins. Curr Opin Neurobiol 8: 351-356, 1998.