Effects of the cell type-specific ablation of the cAMP-responsive transcription factor in noradrenergic neurons on locus coeruleus firing and withdrawal behavior after chronic exposure to morphine

Journal of Neurochemistry

Volumn 115, Issue 3, 2010, Pages 563-573

  Parlato, Rosanna ^a   Cruz, Hans ^b   Otto, Christiane ^a,e   Murtra, Patricia ^b,f   Parkitna, Jan Rodriguez ^a,g   Martin, Miquel ^c   Bura, Simona A ^c   Begus Nahrmann, Yvonne ^a,h   Von Bohlen Und Halbach, Oliver ^d,i   Maldonado, Rafael ^c   Schütz, Günther ^a   Lüscher, Christian ^b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c UNIVERSITAT POMPEU FABRA   (Spain)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e BAYER PHARMA AG   (Germany)

^f INSTITUT DE NEUROCIÈNCIES   (Spain)

^g INSTITUTE OF PHARMACOLOGY   (Poland)

^h UNIVERSITY OF ULM   (Germany)

ⁱ UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

Cre LoxP; Cyclic AMP; Locus coeruleus; Morphine dependence

Indexed keywords

CELL MARKER; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT MODULATOR; MORPHINE; NALOXONE; PROTEIN C FOS; TYROSINE 3 MONOOXYGENASE;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; CELL SPECIFICITY; CELL TYPE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION REGULATION; JUMPING; LOCUS CERULEUS; LONG TERM EXPOSURE; MALE; MASTICATION; MORPHINE ADDICTION; MOUSE; NERVE CELL EXCITABILITY; NONHUMAN; NORADRENERGIC NERVE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; TREMOR; UPREGULATION; WITHDRAWAL SYNDROME;

MUS;

EID: 78651331814     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06709.x     Document Type: Article

References (42)

1. Aghajanian G. K. (1978) Tolerance of locus coeruleus neurones to morphine and suppression of withdrawal response by clonidine. Nature 276, 186-188.
2. Aston-Jones G. and Harris G. C. (2004) Brain substrates for increased drug seeking during protracted withdrawal. Neuropharmacology 47(Suppl 1), 167-179.
3. Bajic D., Proudfit H. K. and Van Bockstaele E. J. (2000) Periaqueductal gray neurons monosynaptically innervate extranuclear noradrenergic dendrites in the rat pericoerulear region. J. Comp. Neurol. 427, 649-662.
4. 2+/ calmodulin-dependent protein kinase type IV in dopaminoceptive neurons enhances behavioral effects of cocaine. Proc. Natl. Acad. Sci. USA 105, 17549-17554.
5. Bleckmann S. C., Blendy J. A., Rudolph D., Monaghan A. P., Schmid W. and Schutz G. (2002) Activating transcription factor 1 and CREB are important for cell survival during early mouse development. Mol. Cell. Biol. 22, 1919-1925.
6. Blendy J. A., Kaestner K. H., Schmid W., Gass P. and Schutz G. (1996) Targeting of the CREB gene leads to up-regulation of a novel CREB mRNA isoform. EMBO J. 15, 1098-1106.
7. von Bohlen und Halbach O. and Unsicker K. (2003) Age-related decline in the tyrosine hydroxylase-immunoreactive innervation of the amygdala and dentate gyrus in mice. Cell Tissue Res. 311, 139-143.
8. Caille S., Espejo E. F., Reneric J. P., Cador M., Koob G. F. and Stinus L. (1999) Total neurochemical lesion of noradrenergic neurons of the locus ceruleus does not alter either naloxone-precipitated or spontaneous opiate withdrawal nor does it influence ability of clonidine to reverse opiate withdrawal. J. Pharmacol. Exp. Ther. 290, 881-892.
9. Carlezon W. A., Jr, Olson V. G., Lane-Ladd S. B., Brodkin E. S., Hiroi N., Duman R. S., Neve R. L. and Nestler E. J. (1998) Regulation of cocaine reward by CREB. Science 282, 2272-2275.
10. Chieng B. and Christie M. J. (2009) Chronic morphine treatment induces functional delta-opioid receptors in amygdala neurons that project to periaqueductal grey. Neuropharmacology 57, 430-437.
11. Christie M. J. (2008) Cellular neuroadaptations to chronic opioids: Tolerance, withdrawal and addiction. Br. J. Pharmacol. 154, 384-396.
12. Christie M. J., Williams J. T., Osborne P. B. and Bellchambers C. E. (1997) Where is the locus in opioid withdrawal? Trends Pharmacol. Sci. 18, 134-140.
13. Cruz H. G., Berton F., Sollini M., Blanchet C., Pravetoni M., Wickman K. and Luscher C. (2008) Absence and rescue of morphine withdrawal in GIRK/Kir3 knock-out mice. J. Neurosci. 28, 4069-4077.
14. Curran E. J., Akil H. and Watson S. J. (1996) Psychomotor stimulant - and opiate-induced c-fos mRNA expression patterns in the rat forebrain: Comparisons between acute drug treatment and a drug challenge in sensitized animals. Neurochem. Res. 21, 1425-1435.
15. Delfs J. M., Zhu Y., Druhan J. P. and Aston-Jones G. (2000) Noradrenaline in the ventral forebrain is critical for opiate withdrawalinduced aversion. Nature 403, 430-434.
16. Dong Y., Green T., Saal D., Marie H., Neve R., Nestler E. J. and Malenka R. C. (2006) CREB modulates excitability of nucleus accumbens neurons. Nat. Neurosci. 9, 475-477.
17. Guitart X., Thompson M. A., Mirante C. K., Greenberg M. E. and Nestler E. J. (1992) Regulation of cyclic AMP response elementbinding protein (CREB) phosphorylation by acute and chronic morphine in the rat locus coeruleus. J. Neurochem. 58, 1168-1171.
18. Han M. H., Bolanos C. A., Green T. A., Olson V. G., Neve R. L., Liu R. J., Aghajanian G. K. and Nestler E. J. (2006) Role of cAMP response element-binding protein in the rat locus ceruleus: Regulation of neuronal activity and opiate withdrawal behaviors. J. Neurosci. 26, 4624-4629.
19. Hayward M. D., Duman R. S. and Nestler E. J. (1990) Induction of the cfos proto-oncogene during opiate withdrawal in the locus coeruleus and other regions of rat brain. Brain Res. 525, 256-266.
20. Hogan B., Beddington R., Costantini F. and Lacy E. (1994) Manipulating the mouse embryo; A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
21. Ivanov A. and Aston-Jones G. (2001) Local opiate withdrawal in locus coeruleus neurons in vitro. J. Neurophysiol. 85, 2388-2397.
22. Koob G. F., Maldonado R. and Stinus L. (1992) Neural substrates of opiate withdrawal. Trends Neurosci. 15, 186-191.
23. Lane-Ladd S. B., Pineda J., Boundy V. A., Pfeuffer T., Krupinski J., Aghajanian G. K. and Nestler E. J. (1997) CREB (cAMP response element-binding protein) in the locus coeruleus: Biochemical, physiological, and behavioral evidence for a role in opiate dependence. J. Neurosci. 17, 7890-7901.
24. Lemberger T., Parkitna J. R., Chai M., Schutz G. and Engblom D. (2008) CREB has a context-dependent role in activity-regulated transcription and maintains neuronal cholesterol homeostasis. FASEB J. 22, 2872-2879.
25. Lonze B. E. and Ginty D. D. (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35, 605-623.
26. Maldonado R. and Koob G. F. (1993) Destruction of the locus coeruleus decreases physical signs of opiate withdrawal. Brain Res. 605, 128-138.
27. Maldonado R., Negus S. and Koob G. F. (1992a) Precipitation of morphine withdrawal syndrome in rats by administration of mu-, deltaand kappa-selective opioid antagonists. Neuropharmacology 31, 1231-1241.
28. Maldonado R., Stinus L., Gold L. H. and Koob G. F. (1992b) Role of different brain structures in the expression of the physical morphine withdrawal syndrome. J. Pharmacol. Exp. Ther. 261, 669-677.
29. Maldonado R., Blendy J. A., Tzavara E., Gass P., Roques B. P., Hanoune J. and Schutz G. (1996) Reduction of morphine abstinence in mice with a mutation in the gene encoding CREB. Science 273, 657-659.
30. Mantamadiotis T., Lemberger T., Bleckmann S. C. et al. (2002) Disruption of CREB function in brain leads to neurodegeneration. Nat. Genet. 31, 47-54.
31. McClung C. A., Nestler E. J. and Zachariou V. (2005) Regulation of gene expression by chronic morphine and morphine withdrawal in the locus ceruleus and ventral tegmental area. J. Neurosci. 25, 6005-6015.
32. Nestler E. J. (2004) Molecular mechanisms of drug addiction. Neuropharmacology 47(Suppl 1), 24-32.
33. Nestler E. J. and Aghajanian G. K. (1997) Molecular and cellular basis of addiction. Science 278, 58-63.
34. Otto D. and Unsicker K. (1990) Basic FGF reverses chemical and morphological deficits in the nigrostriatal system of MPTP-treated mice. J. Neurosci. 10, 1912-1921.
35. Parlato R., Rieker C., Turiault M., Tronche F. and Schutz G. (2006) Survival of DA neurons is independent of CREM upregulation in absence of CREB. Genesis 44, 454-464.
36. Parlato R., Otto C., Begus Y., Stotz S. and Schutz G. (2007) Specific ablation of the transcription factor CREB in sympathetic neurons surprisingly protects against developmentally regulated apoptosis. Development 134, 1663-1670.
37. Rasmussen K. (1995) The role of the locus coeruleus and N-methyl-Daspartic acid (NMDA) and AMPA receptors in opiate withdrawal. Neuropsychopharmacology 13, 295-300.
38. Rudolph D., Tafuri A., Gass P., Hammerling G. J., Arnold B. and Schutz G. (1998) Impaired fetal T cell development and perinatal lethality in mice lacking the cAMP response element binding protein. Proc. Natl. Acad. Sci. USA 95, 4481-4486.
39. Shaw-Lutchman T. Z., Barrot M., Wallace T., Gilden L., Zachariou V., Impey S., Duman R. S., Storm D. and Nestler E. J. (2002) Regional and cellular mapping of cAMP response element-mediated transcription during naltrexone-precipitated morphine withdrawal. J. Neurosci. 22, 3663-3672.
40. Soriano P. (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
41. Valverde O., Mantamadiotis T., Torrecilla M. et al. (2004) Modulation of anxiety-like behavior and morphine dependence in CREB-deficient mice. Neuropsychopharmacology 29, 1122-1133.
42. Zechel S., Jarosik J., Kiprianova I., Schober A., Unsicker K. and von Bohlen und Halbach O. (2006) FGF-2 deficiency does not alter vulnerability of the dopaminergic nigrostriatal system towards MPTP intoxication in mice. Eur. J. Neurosci. 23, 1671-1675.