CREB (cAMP response element-binding protein) in the locus coeruleus: Biochemical, physiological, and behavioral evidence for a role in opiate dependence

Journal of Neuroscience

Volumn 17, Issue 20, 1997, Pages 7890-7901

  Lane Ladd, Sarah B ^a   Pineda, Joseba ^a,d   Boundy, Virginia A ^a   Pfeuffer, T ^b   Krupinski, John ^c   Aghajanian, George K ^a   Nestler, Eric J ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Institute of General Psychology I   (Germany)

^c BRISTOL MYERS SQUIBB PHARMACEUTICAL RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

Adenylyl cyclase; cAMP; G proteins; Gene expression; Morphine; Opiate withdrawal; Protein kinase A; Protein phosphorylation; Tyrosine hydroxylase

Indexed keywords

8 BROMO CYCLIC AMP; ADENYLATE CYCLASE; ANTISENSE OLIGONUCLEOTIDE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MORPHINE; OPIATE; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYCLIC AMP RESPONSIVE ELEMENT; DRUG WITHDRAWAL; ENZYME INDUCTION; GENE EXPRESSION; LOCUS CERULEUS; MALE; NONHUMAN; OPIATE ADDICTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

EID: 0030803695     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.17-20-07890.1997     Document Type: Article

References (52)

1. Aghajanian GK (1978) Tolerance to locus coerulcus neurons to morphine and suppression of withdrawal response by clonidine. Nature 267:186-188.
2. Akaoka H, Aston-Jones G (1991) Opiate withdrawal-induced hyperactivity of locus coeruleus neurons is substantially mediated by augmented excitatory amino acid input. J Neurosci 11:3830-3839.
3. Alreja M, Aghajanian GK (1991) Pacemaker activity of locus coeruleus neurons: whole-cell recordings in brain slices show dependence on cAMP and protein kinase A. Brain Res 556:339-343.
4. Alreja M, Aghajanian GK (1993) Opiates suppress a resting sodium-dependent inward current in addition to activating an outward potassium current locus coeruleus neurons. J Neurosci 13:3525-3532.
5. Aston-Jones G, Rajkowski J, Kubiak P, Valentino RJ, Shipley MT (1996) Role of the locus coeruleus in emotional activation. Prog Brain Res 107:379-402.
6. Berhow MT, Hiroi N, Nestler EJ (1996) Regulation of ERK (extracellular signal regulated kinase). part of the neurotrophin signal transduction cascade, in the rat mesolimbic dopamine system by chronic exposure to morphine or cocaine. J Neurosci 16:4707-4715.
7. Cadd G, McKnight GS (1989) Distinct patterns of cAMP-dependent protein kinase gene expression in mouse brain. Neuron 3:71-79.
8. 2 -/calmodulin-stimulated enzyme expressed in discrete regions of rat brain. J Biol Chem 269:12190-12195.
9. 2 -/calmodulin. J Biol Chem 271:1089-1095.
10. Christie MJ, Williams JT, Osborne PB, Bellchambers CE (1997) Where is the locus in opioid withdrawal? Trends Neurosci 18:134-140.
11. Cooper DMF, Mons N, Karpen JW (1995) Adenylyl cyclases and the interaction between calcium and cAMP signalling. Nature 374:421-424.
12. Coven ER, Widnell KL, Chen JS, Walker WH, Habener JF, Nestler EJ (1996) Molecular mechanisms in the cellular specificity of CREB expression. Soc Neurosci Abstr 22:382.
13. Dahlstrom A, Fuxe K (1965) Evidence for the existence of monoamine-containing neurons in the central nervous system, I. Demonstration of monoamines in the cell bodies of brain stem neurons. Acta Physiol Scad 62[Suppl 232]:1-55.
14. Duman RS, Tallman JF, Nestler EJ (1988) Acute and chronic opiate regulation of adenylate cyclase in brain: specific effects in locus coeruleus. J Pharmacol Exp Ther 246:1033-1039.
15. Fitzgerald LW, Ortiz J, Hamedani AG, Nestler EJ (1996) Regulation of glutamate receptor subunit expression by drugs of abuse and stress: common adaptations among cross-sensitizing agents. J Neurosci 16:274-282.
16. Foote SL, Bloom FE, Aston-Jones G (1983) Nucleus locus ceruleus: new evidence of anatomical and physiological specificity. Physiol Rev 63:844-914.
17. Furuyama T, Inagaki S, Takagi H (1993) Distribution of type II adenylyl cyclase mRNA in rat brain. Mol Brain Res 19:165-170.
18. Glatt CF, Snyder SH (1993) Cloning and expression of an adenylyl cyclase localized to the corpus striatum. Nature 361:536-538.
19. Guitart X, Nestler EJ (1989) Identification of morphine- and cyclic AMP-regulated phosphoproteins (MARPPs) in the locus coeruleus and other regions of rat brain: regulation by acute and chronic morphine. J Neurosci 9:4371-4387.
20. Guitart X, Hayward M, Nisebaum LK, Beitner DB, Haycock JW, Nestler EJ (1990) Identification of MARPP-58, a morphine- and cyclic AMP-regulated phosphoprotein of 58 kDa, as tyrosine hydroxy-lase: evidence for regulation of its expression by chronic morphine in the rat locus coeruleus. J Neurosci 10:2635-2645.
21. Guitart X, Thompson MA, Mirante CK, Greenberg ME, Nestler EJ (1992) Regulation of CREB phosphorylation by acute and chronic morphine in the rat locus cocruleus. J Neurochem 58:1168-1171.
22. Guitart X, Kogan JH, Berhow M, Terwilliger RZ, Aghajanian GK, Nestler EJ (1993) Lewis and Fischer rat strains display differences in biochemical, electrophysiol-ogical, and behavioral parameters: studies in the nucleus accumbens and locus coeruleus of drug naive and morphine-treated animals. Brain Res 611:7-17.
23. Hellevuo K, Yoshimura M, Mons N, Hoffman PL, Cooper DMF. Tabakoff B (1995) The characterization of a novel form of adenylyl cyclase which is present in brain and other tissues. J Biol Chem 270:11581-11589.
24. B-induced hyperpolarization of rat dorsal raphe neurons. Brain Res 459:27-36.
25. Kim KS, Park DH, Wessel TC, Song B, Wagner JA, Joh TH (1993) A dual role for the cAMP-dependent protein kinase in tyrosine hydroxylase gene expression. Proc Natl Acad Sci USA 90:3471-3475.
26. Kogan JH, Nestler EJ, Aghajanian GK (1992) Elevated basal firing rates of locus coeruleus neurons in brain slices from opiate-dependent rate association with enhanced responses to 8-Br-cAMP. Eur J Pharmacol 211:47-53.
27. Konradi C, Cole RL, Heckers S, Hyman SE (1994) Amphetamine regulates gene expression in rat striatum via transcription factor CREB, J Neurosci 14:5623-5634.
28. Koob GF, Maldonado R, Stinus L (1992) Neural substrates of opiate withdrawal. Trends Neurosci 15:186-191.
29. Lane SB, Pineda J, Boundy VA, Widnell KL, Aghajanian GK, Nestler EJ (1996) Role of CREB in chronic morphine-induced adaptation is locus coeruleus neurons. Soc Neurosci Abstr 22:382.
30. Lazaroff M, Patankar S, Yoon SO, Chikaraishi DM (1995) The cyclic AMP response element directs tyrosine hydroxylase expression is catecholaminergic central and peripheral nervous system cell lines from transgenic mice. J Biol Chem 270:21579-21589.
31. Maldonado R, Koob GF (1993) Destruction of the locus coeruleus decreases physical signs of opiate withdrawal. Brain Res 605:128-138.
32. Maldonado R, Valverde O, Garbay C, Roques BP (1995) Protein kinases in the locus coeruleus and periaqueductal gray matter arc involved in the expression of opiate withdrawal. Naunyn Schmiedebergs Arch Pharmacol 352:565-575.
33. Maldonado R, Blendy JA, Tzavara E, Gass P, Roques BP, Hanoune (1996) Reduction of morphine abstinence in mice with a mutation in the gene encoding CREB. Science 273:657-659.
34. Matsuoka I, Maldonado R, Defer N, Noel F, Hanoune J, Roques BP (1994) Chronic morphine administration causes region-specific increase of brain type VIII adenylyl cyclase mRNA. Eur J Pharmacol 268:215-221.
35. Nestler EJ (1992) Molecular mechanisms of drug addiction. J Neurosci 12:2439-2450.
36. Nestler EJ (1996) Under seige: the brain on opiates. Neuron 16:897-900.
37. Nestler EJ. Greengard P (1994) Protein phosphorylation and the regulation of neuronal function. In: Basic neurochemistry: molecular, cellular, and medical aspects, Ed 5 (Siegel GJ, Albers RW, Agranoff BW, Molinoff P, eds), pp 449-474. Boston: Little, Brown.
38. Nestler EJ, Tallman JF (1988) Chronic morphine treatment increases cyclic AMP-dependent protein kinase activity in the rat locus coeruleus. Mol Pharmacol 33:127-132.
39. Nestler EJ, Erdos JJ, Terwilliger R, Duman RS, Tallman JF (1989) Regulation of G-proteins by chronic morphine in the rat locus coeruleus. Brain Res 476:230-239.
40. Nestler EJ, Terwilliger RZ, Walker J, Sevarino KA, Duman RS (1990) Chronic cocaine decreases levels of the G-protein subunits Giα and Goα in discrete regions of rat brain. J Neurochem 55:1079-1082.
41. Nestler EJ, Hope BT, Widnell KL (1993) Drug addiction: a model for the molecular basis of neural plasticity. Neuron 11:995-1006.
42. Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. New York: Academic.
43. Punch L, Self DW, Nestler EJ, Taylor JR (1997) Opposite modulation of opiate withdrawal behaviors upon microinfusion of a protein kinase A inhibitor versus activator into the locus coeruleus or periaqueductal gray. J Neurosci, in press.
44. Rasmussen K., Aghajanian GK (1989) Withdrawal-induced activation of locus coerulcus neurons in opiate-dependent rats: attenuation by lesions of the nucleus paragigantocellularis. Brain Res 505:346-350.
45. Rasmussen K, Beitner-Johnson DB, Krystal JH, Aghajanian GK, Nestler EJ (1490) Opiate withdrawal and the rat locus coeruleus: Behavioral, electrophysiological, and biochemical correlates. J Neurosci 10:2308-2317.
46. Russell DS, Widnell KL, Nestler EJ (1996) Antisense oligonucleotides: New tools for the study of brain function. Neuroscientist 2:79-82.
47. Sunahara RK, Dessauer CW, Gilman AG (1995) Complexity and diversity of mammalian adenylyl cyclases. Annu Rev Pharmacol Toxicol 36:461-480.
48. Wallach J, Droste M, Kluxen FW, Pfeuffer T, Frank R (1994) Molecular cloning and expression of a novel type V adenylyl cyclasc from rabbit myocardium. FEBS Lett 338:257-263.
49. Widnell KL, Russell D, Nestler EJ (1994) Regulation of cAMP response element binding protein in the locus coeruleus in vivo and in a locus coeruleus-like (CATH.a) cell line in vitro. Proc Natl Acad Sci USA 91:10947-10951.
50. Widnell KL, Self DW, Lane SB, Russell DS, Vaidya V, Miserendino MJD, Rubin CS, Duman RS, Nestler EJ (1996a) Regulation of CREB expression: in vivo evidence for a functional role in morphine action in the nucleus accumbens. J Pharmacol Exp Ther 276:306-315.
51. Widnell KL, Chen J-S, Iredale PA, Walker WH, Duman RS, Habener JF, Nestler EJ (1996b) Transcriptional regulation of CREB (cAMP response element-binding protein) expression in CATH.a cells. J Neurochem 66:1770-1773.
52. Xia Z, Choi E-J, Wang F, Blazynski C, Storm DR (1993) Type I calmodulin-sensitive adenylyl cyclase is neural specific. J Neurochem 60:305-311.