CRF Facilitates Calcium Release from Intracellular Stores in Midbrain Dopamine Neurons

Neuron

Volumn 57, Issue 4, 2008, Pages 559-570

  Riegel, Arthur C ^a   Williams, John T ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

MOLNEURO; SIGNALING; SYSNEURO

Indexed keywords

ACETYLCHOLINE; ADENYLATE CYCLASE; BINDING PROTEIN; CALCIUM ACTIVATED POTASSIUM CHANNEL; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR BINDING PROTEIN; CORTICOTROPIN RELEASING FACTOR RECEPTOR 2; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUTAMIC ACID; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; INOSITOL TRISPHOSPHATE RECEPTOR; METABOTROPIC RECEPTOR; RECEPTOR; RYANODINE RECEPTOR; STIMULATORY GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSOL; DENDRITE; DOPAMINERGIC NERVE CELL; ENZYME ACTIVATION; MALE; MESENCEPHALON; MOLECULAR IMAGING; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NONHUMAN; PHOTOLYSIS; PRIORITY JOURNAL; RAT; STRESS;

ANIMALS; CALCIUM; CORTICOTROPIN-RELEASING HORMONE; DOPAMINE; INTRACELLULAR FLUID; MALE; MESENCEPHALON; NEURONS; RATS; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE;

EID: 39449125015     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2007.12.029     Document Type: Article

References (93)

1. Augustine G.J., Santamaria F., and Tanaka K. Local calcium signaling in neurons. Neuron 40 (2003) 331-346
2. Balschun D., Wolfer D.P., Bertocchini F., Barone V., Conti A., Zuschratter W., Missiaen L., Lipp H.P., Frey J.U., and Sorrentino V. Deletion of the ryanodine receptor type 3 (RyR3) impairs forms of synaptic plasticity and spatial learning. EMBO J. 18 (1999) 5264-5273
3. Bean B.P. The action potential in mammalian central neurons. Nat. Rev. Neurosci. 8 (2007) 451-465
4. Beene D.L., and Scott J.D. A-kinase anchoring proteins take shape. Curr. Opin. Cell Biol. 19 (2007) 192-198
5. Belmeguenai A., Desrues L., Leprince J., Vaudry H., Tonon M.C., and Louiset E. Neurotensin stimulates both calcium mobilization from inositol trisphosphate-sensitive intracellular stores and calcium influx through membrane channels in frog pituitary melanotrophs. Endocrinology 144 (2003) 5556-5567
6. Berridge M.J., Bootman M.D., and Roderick H.L. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4 (2003) 517-529
7. Bjorklund A., and Dunnett S.B. Dopamine neuron systems in the brain: an update. Trends Neurosci. 30 (2007) 194-202
8. Bond C.T., Maylie J.A., and Adelman J.P. Small-conductance calcium-activated potassium channels. Ann. N Y Acad. Sci. 868 (1999) 370-378
9. Bootman M.D., Thomas D., Tovey S.C., Berridge M.J., and Lipp P. Nuclear calcium signalling. Cell. Mol. Life Sci. 57 (2000) 371-378
10. Bruce J.I., Straub S.V., and Yule D.I. Crosstalk between cAMP and Ca2+ signaling in non-excitable cells. Cell Calcium 34 (2003) 431-444
11. Bugrim A.E. Regulation of Ca2+ release by cAMP-dependent protein kinase. A mechanism for agonist-specific calcium signaling?. Cell Calcium 25 (1999) 219-226
12. Chen R., Lewis K.A., Perrin M.H., and Vale W.W. Expression cloning of a human corticotropin-releasing-factor receptor. Proc. Natl. Acad. Sci. USA 90 (1993) 8967-8971
13. Choi Y.M., Kim S.H., Chung S., Uhm D.Y., and Park M.K. Regional interaction of endoplasmic reticulum Ca2+ signals between soma and dendrites through rapid luminal Ca2+ diffusion. J. Neurosci. 26 (2006) 12127-12136
14. Cui G., Bernier B.E., Harnett M.T., and Morikawa H. Differential regulation of action potential- and metabotropic glutamate receptor-induced Ca2+ signals by inositol 1,4,5-trisphosphate in dopaminergic neurons. J. Neurosci. 27 (2007) 4776-4785
15. Dermitzaki I., Tsatsanis C., Alexaki V.I., Castanas E., and Margioris A.N. Roles of protein kinase A (PKA) and PKC on corticotropin-releasing hormone (CRH)-induced elevation of cytosolic calcium from extra-and intra-cellular sources. Hormones (Athens) 3 (2004) 252-258
16. Dodt H.U., Eder M., Schierloh A., and Zieglgansberger W. Infrared-guided laser stimulation of neurons in brain slices. Sci. STKE 2002 (2002) L2
17. Duridanova D.B., Petkova-Kirova P.S., Lubomirov L.T., Gagov H., and Boev K. Corticotropin-releasing hormone acts on guinea pig ileal smooth muscle via protein kinase A. Pflugers Arch. 438 (1999) 205-212
18. Ellis-Davies G.C., and Kaplan J.H. Nitrophenyl-EGTA, a photolabile chelator that selectively binds Ca2+ with high affinity and releases it rapidly upon photolysis. Proc. Natl. Acad. Sci. USA 91 (1994) 187-191
19. Ellis-Davies G.C., Kaplan J.H., and Barsotti R.J. Laser photolysis of caged calcium: rates of calcium release by nitrophenyl-EGTA and DM-nitrophen. Biophys. J. 70 (1996) 1006-1016
20. Fazal N., Slominski A., Choudhry M.A., Wei E.T., and Sayeed M.M. Effect of CRF and related peptides on calcium signaling in human and rodent melanoma cells. FEBS Lett. 435 (1998) 187-190
21. Fiorillo C.D., and Williams J.T. Glutamate mediates an inhibitory postsynaptic potential in dopamine neurons. Nature 394 (1998) 78-82
22. Fiorillo C.D., and Williams J.T. Cholinergic inhibition of ventral midbrain dopamine neurons. J. Neurosci. 20 (2000) 7855-7860
23. Ford C.P., Mark G.P., and Williams J.T. Properties and opioid inhibition of mesolimbic dopamine neurons vary according to target location. J. Neurosci. 26 (2006) 2788-2797
24. Foskett J.K., White C., Cheung K.H., and Mak D.-O.D. Inositol trisphosphate receptor Ca2+ release channels. Physiol. Rev. 87 (2007) 593-658
25. Furuichi T., Kohda K., Miyawaki A., and Mikoshiba K. Intracellular channels. Curr. Opin. Neurobiol. 4 (1994) 294-303
26. Gaisano H.Y., Wong D., Sheu L., and Foskett J.K. Calcium release by cholecystokinin analogue OPE is IP3 dependent in single rat pancreatic acinar cells. Am. J. Physiol. 267 (1994) C220-C228
27. Gentet L.J., and Williams S.R. Dopamine gates action potential backpropagation in midbrain dopaminergic neurons. J. Neurosci. 27 (2007) 1892-1901
28. Ghosh A., and Greenberg M.E. Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 268 (1995) 239-247
29. Grace A.A., and Onn S.P. Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J. Neurosci. 9 (1989) 3463-3481
30. Grace A.A., Floresco S.B., Goto Y., and Lodge D.J. Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci. 30 (2007) 220-227
31. Guerineau N., Corcuff J.B., Tabarin A., and Mollard P. Spontaneous and corticotropin-releasing factor-induced cytosolic calcium transients in corticotrophs. Endocrinology 129 (1991) 409-420
32. Hagen B.M., Bayguinov O., and Sanders K.M. VIP and PACAP regulate localized Ca2+ transients via cAMP-dependent mechanism. Am. J. Physiol. Cell Physiol. 291 (2006) C375-C385
33. Haug T., and Storm J.F. Protein kinase A mediates the modulation of the slow Ca(2+)-dependent K(+) current, I(sAHP), by the neuropeptides CRF, VIP, and CGRP in hippocampal pyramidal neurons. J. Neurophysiol. 83 (2000) 2071-2079
34. Hauger R.L., Risbrough V., Brauns O., and Dautzenberg F.M. Corticotropin releasing factor (CRF) receptor signaling in the central nervous system: new molecular targets. CNS Neurol. Disord. Drug Targets 5 (2006) 453-479
35. Hausser M., Stuart G., Racca C., and Sakmann B. Axonal initiation and active dendritic propagation of action potentials in substantia nigra neurons. Neuron 15 (1995) 637-647
36. Hsu S.Y., and Hsueh A.J. Human stresscopin and stresscopin-related peptide are selective ligands for the type 2 corticotropin-releasing hormone receptor. Nat. Med. 7 (2001) 605-611
37. Huang Y., Chan F.L., Lau C.W., Tsang S.Y., Chen Z.Y., He G.W., and Yao X. Roles of cyclic AMP and Ca2+-activated K+ channels in endothelium-independent relaxation by urocortin in the rat coronary artery. Cardiovasc. Res. 57 (2003) 824-833
38. Inoue T., Kato K., Kohda K., and Mikoshiba K. Type 1 inositol 1,4,5-trisphosphate receptor is required for induction of long-term depression in cerebellar purkinje neurons. J. Neurosci. 18 (1998) 5366-5373
39. Jahn O., Tezval H., van Werven L., Eckart K., and Spiess J. Three-amino acid motifs of urocortin II and III determine their CRF receptor subtype selectivity. Neuropharmacology 47 (2004) 233-242
40. Kageyama K., Kimura R., Suga S., Ogawa Y., Suda T., and Wakui M. Modulation of Ca2+ influx by corticotropin-releasing factor (CRF) family of peptides via CRF receptors in rat pancreatic beta-cells. Peptides 27 (2006) 1814-1819
41. Kanno T., Suga S., Nakano K., Kamimura N., and Wakui M. Corticotropin-releasing factor modulation of Ca2+ influx in rat pancreatic beta-cells. Diabetes 48 (1999) 1741-1746
42. Kim Y., Park M.K., Uhm D.Y., and Chung S. Modulation of T-type Ca(2+) channels by corticotropin-releasing factor through protein kinase C pathway in MN9D dopaminergic cells. Biochem. Biophys. Res. Commun. 358 (2007) 796-801
43. Korotkova T.M., Brown R.E., Sergeeva O.A., Ponomarenko A.A., and Haas H.L. Effects of arousal- and feeding-related neuropeptides on dopaminergic and GABAergic neurons in the ventral tegmental area of the rat. Eur. J. Neurosci. 23 (2006) 2677-2685
44. Kudoh A., Kudoh E., Katagai H., and Takazawa T. Norepinephrine-induced inositol 1,4,5-trisphosphate formation in atrial myocytes is regulated by extracellular calcium, protein kinase C, and calmodulin. Jpn. Heart J. 44 (2003) 547-556
45. Kuryshev Y.A., Childs G.V., and Ritchie A.K. Corticotropin-releasing hormone stimulates Ca2+ entry through L- and P-type Ca2+ channels in rat corticotropes. Endocrinology 137 (1996) 2269-2277
46. Lavicky J., and Dunn A.J. Corticotropin-releasing factor stimulates catecholamine release in hypothalamus and prefrontal cortex in freely moving rats as assessed by microdialysis. J. Neurochem. 60 (1993) 602-612
47. Lee A.K., and Tse A. Mechanism underlying corticotropin-releasing hormone (CRH) triggered cytosolic Ca2+ rise in identified rat corticotrophs. J. Physiol. 504 (1997) 367-378
48. Lewis K., Li C., Perrin M.H., Blount A., Kunitake K., Donaldson C., Vaughan J., Reyes T.M., Gulyas J., Fischer W., et al. Identification of urocortin III, an additional member of the corticotropin-releasing factor (CRF) family with high affinity for the CRF2 receptor. Proc. Natl. Acad. Sci. USA 98 (2001) 7570-7575
49. Lodge D.J., and Grace A.A. Acute and chronic corticotropin-releasing factor 1 receptor blockade inhibits cocaine-induced dopamine release: correlation with dopamine neuron activity. J. Pharmacol. Exp. Ther. 314 (2005) 201-206
50. Lu L., Liu Z., Huang M., and Zhang Z. Dopamine-dependent responses to cocaine depend on corticotropin-releasing factor receptor subtypes. J. Neurochem. 84 (2003) 1378-1386
51. Luini A., Lewis D., Guild S., Corda D., and Axelrod J. Hormone secretagogues increase cytosolic calcium by increasing cAMP in corticotropin-secreting cells. Proc. Natl. Acad. Sci. USA 82 (1985) 8034-8038
52. Manzoni O.J., and Williams J.T. Presynaptic regulation of glutamate release in the ventral tegmental area during morphine withdrawal. J. Neurosci. 19 (1999) 6629-6636
53. Marino M.J., Wittmann M., Bradley S.R., Hubert G.W., Smith Y., and Conn P.J. Activation of group I metabotropic glutamate receptors produces a direct excitation and disinhibition of GABAergic projection Neurons in the substantia nigra pars reticulata. J. Neurosci. 21 (2001) 7001-7012
54. Marx S.O., Reiken S., Hisamatsu Y., Jayaraman T., Burkhoff D., Rosemblit N., and Marks A.R. PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101 (2000) 365-376
55. Mignery G.A., Newton C.L., Archer III B.T., and Sudhof T.C. Structure and expression of the rat inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 265 (1990) 12679-12685
56. Morikawa H., Khodakhah K., and Williams J.T. Two intracellular pathways mediate metabotropic glutamate receptor-induced Ca2+ mobilization in dopamine neurons. J. Neurosci. 23 (2003) 149-157
57. Nakamura T., Barbara J.G., Nakamura K., and Ross W.N. Synergistic release of Ca2+ from IP3-sensitive stores evoked by synaptic activation of mGluRs paired with backpropagating action potentials. Neuron 24 (1999) 727-737
58. Neher E., and Zucker R.S. Multiple calcium-dependent processes related to secretion in bovine chromaffin cells. Neuron 10 (1993) 21-30
59. Orozco-Cabal L., Pollandt S., Liu J., Shinnick-Gallagher P., and Gallagher J.P. Regulation of synaptic transmission by CRF receptors. Rev. Neurosci. 17 (2006) 279-307
60. Paladini C.A., Mitchell J.M., Williams J.T., and Mark G.P. Cocaine self-administration selectively decreases noradrenergic regulation of metabotropic glutamate receptor-mediated inhibition in dopamine neurons. J. Neurosci. 24 (2004) 5209-5215
61. Paladini C.A., and Williams J.T. Noradrenergic inhibition of midbrain dopamine neurons. J. Neurosci. 24 (2004) 4568-4575
62. Pedarzani P., McCutcheon J.E., Rogge G., Jensen B.S., Christophersen P., Hougaard C., Strobaek D., and Stocker M. Specific enhancement of SK channel activity selectively potentiates the afterhyperpolarizing current I(AHP) and modulates the firing properties of hippocampal pyramidal neurons. J. Biol. Chem. 280 (2005) 41404-41411
63. Petersen O.H., Petersen C.C., and Kasai H. Calcium and hormone action. Annu. Rev. Physiol. 56 (1994) 297-319
64. Petkova-Kirova P.S., Gagov H.S., and Duridanova D.B. Urocortin hyperpolarizes stomach smooth muscle via activation of Ca2+-sensitive K+ currents. J. Muscle Res. Cell Motil. 21 (2000) 639-645
65. Pologruto T.A., Sabatini B.L., and Svoboda K. ScanImage: flexible software for operating laser scanning microscopes. Biomed. Eng. Online 2 (2003) 13
66. Sabatini B.L., Oertner T.G., and Svoboda K. The life cycle of Ca2+ ions in dendritic spines. Neuron 33 (2002) 439-452
67. Sarnyai Z., Shaham Y., and Heinrichs S.C. The role of corticotropin-releasing factor in drug addiction. Pharmacol. Rev. 53 (2001) 209-243
68. Scott J.D., Fischer E.H., Demaille J.G., and Krebs E.G. Identification of an inhibitory region of the heat-stable protein inhibitor of the cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. USA 82 (1985) 4379-4383
69. Scott J.D., Glaccum M.B., Fischer E.H., and Krebs E.G. Primary-structure requirements for inhibition by the heat-stable inhibitor of the cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. USA 83 (1986) 1613-1616
70. Smith F.D., Langeberg L.K., and Scott J.D. The where's and when's of kinase anchoring. Trends Biochem. Sci. 31 (2006) 316-323
71. Spada A., Reza-Elahi F., Lania A., Bassetti M., and Atti E. Inhibition of basal and corticotropin-releasing hormone-stimulated adenylate cyclase activity and cytosolic Ca2+ levels by somatostatin in human corticotropin-secreting pituitary adenomas. J. Clin. Endocrinol. Metab. 70 (1990) 1262-1268
72. Spira M.E., Oren R., Dormann A., Ilouz N., and Lev S. Calcium, protease activation, and cytoskeleton remodeling underlie growth cone formation and neuronal regeneration. Cell. Mol. Neurobiol. 21 (2001) 591-604
73. Stenzel P., Kesterson R., Yeung W., Cone R.D., Rittenberg M.B., and Stenzel-Poore M.P. Identification of a novel murine receptor for corticotropin-releasing hormone expressed in the heart. Mol. Endocrinol. 9 (1995) 637-645
74. Stocker M. Ca2+-activated K+ channels: molecular determinants and function of the SK family. Nat. Rev. Neurosci. 5 (2004) 758-770
75. Strobaek D., Teuber L., Jorgensen T.D., Ahring P.K., Kjaer K., Hansen R.S., Olesen S.P., Christophersen P., and Skaaning-Jensen B. Activation of human IK and SK Ca2+ -activated K+ channels by NS309 (6,7-dichloro-1H-indole-2,3-dione 3-oxime). Biochim. Biophys. Acta 1665 (2004) 1-5
76. Sudhof T.C., Newton C.L., Archer III B.T., Ushkaryov Y.A., and Mignery G.A. Structure of a novel InsP3 receptor. EMBO J. 10 (1991) 3199-3206
77. Swanson L.W., Sawchenko P.E., Rivier J., and Vale W.W. Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 36 (1983) 165-186
78. Takuma K., Matsuda T., Yoshikawa T., Kitanaka J., Gotoh M., Hayata K., and Baba A. Corticotropin-releasing factor stimulates Ca2+ influx in cultured rat astrocytes. Biochem. Biophys. Res. Commun. 199 (1994) 1103-1107
79. Tao J., Zhang Y., Soong T.W., and Li S. Expression of urocortin 2 and its inhibitory effects on intracellular ca2+ via L-type voltage-gated calcium channels in rat pheochromocytoma (PC12) cells. Neuropsychopharmacol 31 (2006) 2600-2609
80. Taufiq A.M., Fujii S., Yamazaki Y., Sasaki H., Kaneko K., Li J., Kato H., and Mikoshiba K. Involvement of IP3 receptors in LTP and LTD induction in guinea pig hippocampal CA1 neurons. Learn. Mem. 12 (2005) 594-600
81. Tse A., and Lee A.K. Arginine vasopressin triggers intracellular calcium release, a calcium-activated potassium current and exocytosis in identified rat corticotropes. Endocrinology 139 (1998) 2246-2252
82. Tu J.C., Xiao B., Yuan J.P., Lanahan A.A., Leoffert K., Li M., Linden D.J., and Worley P.F. Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Neuron 21 (1998) 717-726
83. Ungless M.A., Singh V., Crowder T.L., Yaka R., Ron D., and Bonci A. Corticotropin-releasing factor requires CRF binding protein to potentiate NMDA receptors via CRF receptor 2 in dopamine neurons. Neuron 39 (2003) 401-407
84. Van Pett K., Viau V., Bittencourt J.C., Chan R.K., Li H.Y., Arias C., Prins G.S., Perrin M., Vale W., and Sawchenko P.E. Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J. Comp. Neurol. 428 (2000) 191-212
85. Verkhratsky A. Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons. Physiol. Rev. 85 (2005) 201-279
86. West A.E., Chen W.G., Dalva M.B., Dolmetsch R.E., Kornhauser J.M., Shaywitz A.J., Takasu M.A., Tao X., and Greenberg M.E. Calcium regulation of neuronal gene expression. Proc. Natl. Acad. Sci. USA 98 (2001) 11024-11031
87. Wise R.A. Dopamine, learning and motivation. Nat. Rev. Neurosci. 5 (2004) 483-494
88. Wolfart J., and Roeper J. Selective coupling of T-type calcium channels to SK potassium channels prevents intrinsic bursting in dopaminergic midbrain neurons. J. Neurosci. 22 (2002) 3404-3413
89. Wolfart J., Neuhoff H., Franz O., and Roeper J. Differential expression of the small-conductance, calcium-activated potassium channel SK3 is critical for pacemaker control in dopaminergic midbrain neurons. J. Neurosci. 21 (2001) 3443-3456
90. Womack M.D., Chevez C., and Khodakhah K. Calcium-activated potassium channels are selectively coupled to P/Q-type calcium channels in cerebellar Purkinje neurons. J. Neurosci. 24 (2004) 8818-8822
91. Yamamori E., Iwasaki Y., Oki Y., Yoshida M., Asai M., Kambayashii M., Oiso Y., and Nakashima N. Possible involvement of ryanodine receptor-mediated intracellular calcium release in the effect of corticotropin-releasing factor on adrenocorticotropin secretion. Endocrinology 145 (2004) 36-38
92. Ziff E.B. TARPs and the AMPA receptor trafficking paradox. Neuron 53 (2007) 627-633
93. Zimmermann B., Somlyo A.V., Ellis-Davies G.C., Kaplan J.H., and Somlyo A.P. Kinetics of prephosphorylation reactions and myosin light chain phosphorylation in smooth muscle. Flash photolysis studies with caged calcium and caged ATP. J. Biol. Chem. 270 (1995) 23966-23974