Neuropeptide regulation of the locus coeruleus and opiate-induced plasticity of stress responses

Advances in Pharmacology

Volumn 68, Issue , 2013, Pages 405-420

  Van Bockstaele, Elisabeth J ^a   Valentino, Rita J ^a,b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

Anxiety; Biological psychiatry; Corticotropin releasing factor; Enkephalin; Hyperarousal; Immunoelectron microscopy; Norepinephrine; Receptor trafficking

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR; DYNORPHIN; ENDORPHIN; ENKEPHALIN; MORPHINE; MU OPIATE RECEPTOR; NALOXONE; NEUROPEPTIDE; NORADRENALIN; OPIATE;

ARTICLE; ATTENTION; BRAIN CORTEX; COGNITION; COPING BEHAVIOR; DEPRESSION; HIPPOCAMPUS; HUMAN; LOCUS CERULEUS; LONG TERM EXPOSURE; NERVE CELL PLASTICITY; NERVE ENDING; NONHUMAN; NORADRENERGIC SYSTEM; NUCLEUS ACCUMBENS; OPIATE ADDICTION; POSTTRAUMATIC STRESS DISORDER; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; SOCIAL STRESS; STRESS;

ANXIETY; BIOLOGICAL PSYCHIATRY; CORTICOTROPIN-RELEASING FACTOR; ENKEPHALIN; HYPERAROUSAL; IMMUNOELECTRON MICROSCOPY; NOREPINEPHRINE; RECEPTOR TRAFFICKING;

ANALGESICS, OPIOID; ANIMALS; LOCUS COERULEUS; NALOXONE; NARCOTIC ANTAGONISTS; NEURONAL PLASTICITY; NEURONS; NEUROPEPTIDES; NOREPINEPHRINE; STRESS, PSYCHOLOGICAL;

EID: 84884302342     PISSN: 10543589     EISSN: 15578925     Source Type: Book Series    
DOI: 10.1016/B978-0-12-411512-5.00019-1     Document Type: Chapter

References (82)

1. Aghajanian G.K., Alreja M., Nestler E.J., Kogan J.H. Dual mechanisms of opiate dependence in the locus coeruleus. Clinical Neuropharmacology 1992, 15(Suppl. 1Pt A):143A-144A.
2. Akaoka H., Aston-Jones G. Opiate withdrawal-induced hyperactivity of locus coeruleus neurons is substantially mediated by augmented excitatory amino acid input. Journal of Neuroscience 1991, 11(12):3830-3839.
3. Angulo J.A., Printz D., Ledoux M., McEwen B.S. Isolation stress increases tyrosine hydroxylase mRNA in the locus coeruleus and midbrain and decreases proenkephalin mRNA in the striatum and nucleus accumbens. Brain Research. Molecular Brain Research 1991, 11(3-4):301-308.
4. Aston-Jones G., Bloom F.E. Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. Journal of Neuroscience 1981, 1(8):876-886.
5. Aston-Jones G., Bloom F.E. Norepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli. Journal of Neuroscience 1981, 1(8):887-900.
6. Aston-Jones G., Cohen J.D. An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance. Annual Review of Neuroscience 2005, 28:403-450.
7. Barr J., Van Bockstaele E.J. Vesicular glutamate transporter-1 colocalizes with endogenous opioid peptides in axon terminals of the rat locus coeruleus. The Anatomical Record. Part A, Discoveries in Molecular, Cellular, and Evolutionary Biology 2005, 284(1):466-474.
8. Butler R.K., Finn D.P. Stress-induced analgesia. Progress in Neurobiology 2009, 88(3):184-202. 10.1016/j.pneurobio.2009.04.003.
9. Carr G.V., Bangasser D.A., Bethea T., Young M., Valentino R.J., Lucki I. Antidepressant-like effects of kappa-opioid receptor antagonists in Wistar Kyoto rats. Neuropsychopharmacology 2010, 35(3):752-763. 10.1038/npp.2009.183.
10. Covington H.E., Miczek K.A. Repeated social-defeat stress, cocaine or morphine. Effects on behavioral sensitization and intravenous cocaine self-administration "binges". Psychopharmacology 2001, 158(4):388-398. 10.1007/s002130100858.
11. Curtis A.L., Bello N.T., Connolly K.R., Valentino R.J. Corticotropin-releasing factor neurones of the central nucleus of the amygdala mediate locus coeruleus activation by cardiovascular stress. Journal of Neuroendocrinology 2002, 14(8):667-682.
12. Curtis A.L., Bello N.T., Valentino R.J. Evidence for functional release of endogenous opioids in the locus coeruleus during stress termination. Journal of Neuroscience 2001, 21(RC152):1-5.
13. Curtis A.L., Lechner S.M., Pavcovich L.A., Valentino R.J. Activation of the locus coeruleus noradrenergic system by intracoerulear microinfusion of corticotropin-releasing factor: Effects on discharge rate, cortical norepinephrine levels and cortical electroencephalographic activity. Journal of Pharmacology and Experimental Therapeutics 1997, 281(1):163-172.
14. Curtis A.L., Leiser S.C., Snyder K., Valentino R.J. Predator stress engages corticotropin-releasing factor and opioid systems to alter the operating mode of locus coeruleus norepinephrine neurons. Neuropharmacology 2012, 62(4):1737-1745. 10.1016/j.neuropharm.2011.11.020.
15. Detke M.J., Rickels M., Lucki I. Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology 1995, 121(1):66-72.
16. Drolet G., Van Bockstaele E.J., Aston-Jones G. Robust enkephalin innervation of the locus coeruleus from the rostral medulla. Journal of Neuroscience 1992, 12(8):3162-3174.
17. Dumont E.C., Kinkead R., Trottier J.F., Gosselin I., Drolet G. Effect of chronic psychogenic stress exposure on enkephalin neuronal activity and expression in the rat hypothalamic paraventricular nucleus. Journal of Neurochemistry 2000, 75(5):2200-2211.
18. Ennis M., Aston-Jones G. Activation of locus coeruleus from nucleus paragigantocellularis: A new excitatory amino acid pathway in brain. Journal of Neuroscience 1988, 8(10):3644-3657.
19. Haney M., Maccari S., Le Moal M., Simon H., Piazza P.V. Social stress increases the acquisition of cocaine self-administration in male and female rats. Brain Research 1995, 698(1-2):46-52.
20. Hebb A.L., Zacharko R.M., Gauthier M., Trudel F., Laforest S., Drolet G. Brief exposure to predator odor and resultant anxiety enhances mesocorticolimbic activity and enkephalin expression in CD-1 mice. European Journal of Neuroscience 2004, 20(9):2415-2429. 10.1111/j.1460-9568.2004.03704.x.
21. Hyman S.M., Fox H., Hong K.I., Doebrick C., Sinha R. Stress and drug-cue-induced craving in opioid-dependent individuals in naltrexone treatment. Experimental and Clinical Psychopharmacology 2007, 15(2):134-143. 10.1037/1064-1297.15.2.134.
22. Ishimatsu M., Williams J.T. Synchronous activity in locus coeruleus results from dendritic interactions in pericoerulear regions. Journal of Neuroscience 1996, 16(16):5196-5204.
23. Kalivas P.W., Abhold R. Enkephalin release into the ventral tegmental area in response to stress: Modulation of mesocorticolimbic dopamine. Brain Research 1987, 414(2):339-348.
24. Kawahara H., Kawahara Y., Westerink B.H. The role of afferents to the locus coeruleus in the handling stress-induced increase in the release of noradrenaline in the medial prefrontal cortex: A dual-probe microdialysis study in the rat brain. European Journal of Pharmacology 2000, 387(3):279-286.
25. Kreek M.J., Koob G.F. Drug dependence: Stress and dysregulation of brain reward pathways. Drug and Alcohol Dependence 1998, 51(1-2):23-47.
26. Kreibich A., Reyes B.A., Curtis A.L., Ecke L., Chavkin C., Van Bockstaele E.J., et al. Presynaptic inhibition of diverse afferents to the locus ceruleus by kappa-opiate receptors: A novel mechanism for regulating the central norepinephrine system. Journal of Neuroscience 2008, 28(25):6516-6525. 10.1523/JNEUROSCI.0390-08.2008.
27. Krystal J.H., Neumeister A. Noradrenergic and serotonergic mechanisms in the neurobiology of posttraumatic stress disorder and resilience. Brain Research 2009, 1293:13-23. 10.1016/j.brainres.2009.03.044.
28. Kulling P., Frischknecht H.R., Pasi A., Waser P.G., Siegfried B. Social conflict-induced changes in nociception and beta-endorphin-like immunoreactivity in pituitary and discrete brain areas of C57BL/6 and DBA/2 mice. Brain Research 1988, 450(1-2):237-246.
29. Lucas L.R., Celen Z., Tamashiro K.L., Blanchard R.J., Blanchard D.C., Markham C., et al. Repeated exposure to social stress has long-term effects on indirect markers of dopaminergic activity in brain regions associated with motivated behavior. Neuroscience 2004, 124(2):449-457. 10.1016/j.neuroscience.2003.12.009.
30. Maderdrut J.L., Merchenthaler I., Sundberg D.K., Okado N., Oppenheim R.W. Distribution and development of proenkephalin-like immunoreactivity in the lumbar spinal cord of the chicken. Brain Research 1986, 377(1):29-40.
31. Mansi J.A., Laforest S., Drolet G. Effect of stress exposure on the activation pattern of enkephalin-containing perikarya in the rat ventral medulla. Journal of Neurochemistry 2000, 74(6):2568-2575.
32. Mansi J.A., Rivest S., Drolet G. Effect of immobilization stress on transcriptional activity of inducible immediate-early genes, corticotropin-releasing factor, its type 1 receptor, and enkephalin in the hypothalamus of borderline hypertensive rats. Journal of Neurochemistry 1998, 70(4):1556-1566.
33. Merchenthaler I., Maderdrut J.L., Altschuler R.A., Petrusz P. Immunocytochemical localization of proenkephalin-derived peptides in the central nervous system of the rat. Neuroscience 1986, 17(2):325-348.
34. Miczek K.A. Tolerance to the analgesic, but not discriminative stimulus effects of morphine after brief social defeat in rats. Psychopharmacology 1991, 104(2):181-186.
35. Miczek K.A., Thompson M.L., Shuster L. Analgesia following defeat in an aggressive encounter: Development of tolerance and changes in opioid receptors. Annals of the New York Academy of Sciences 1986, 467:14-29.
36. Mills K.L., Lynskey M., Teesson M., Ross J., Darke S. Post-traumatic stress disorder among people with heroin dependence in the Australian treatment outcome study (ATOS): Prevalence and correlates. Drug and Alcohol Dependence 2005, 77(3):243-249. 10.1016/j.drugalcdep.2004.08.016.
37. Mills K.L., Teesson M., Ross J., Peters L. Trauma, PTSD, and substance use disorders: Findings from the Australian National Survey of Mental Health and Well-Being. The American Journal of Psychiatry 2006, 163(4):652-658. 10.1176/appi.ajp.163.4.652.
38. Nankova B., Kvetnansky R., Hiremagalur B., Sabban B., Rusnak M., Sabban E.L. Immobilization stress elevates gene expression for catecholamine biosynthetic enzymes and some neuropeptides in rat sympathetic ganglia: Effects of adrenocorticotropin and glucocorticoids. Endocrinology 1996, 137(12):5597-5604.
39. Nestler E.J., Alreja M., Aghajanian G.K. Molecular and cellular mechanisms of opiate action: Studies in the rat locus coeruleus. Brain Research Bulletin 1994, 35(5-6):521-528.
40. O'Donnell T., Hegadoren K.M., Coupland N.C. Noradrenergic mechanisms in the pathophysiology of post-traumatic stress disorder. Neuropsychobiology 2004, 50(4):273-283. 10.1159/000080952.
41. O'Mahony C.M., Clarke G., Gibney S., Dinan T.G., Cryan J.F. Strain differences in the neurochemical response to chronic restraint stress in the rat: Relevance to depression. Pharmacology, Biochemistry, and Behavior 2011, 97(4):690-699. 10.1016/j.pbb.2010.11.012.
42. Page M.E., Berridge C.W., Foote S.L., Valentino R.J. Corticotropin-releasing factor in the locus coeruleus mediates EEG activation associated with hypotensive stress. Neuroscience Letters 1993, 164(1-2):81-84.
43. Pearson K.A., Stephen A., Beck S.G., Valentino R.J. Identifying genes in monoamine nuclei that may determine stress vulnerability and depressive behavior in Wistar-Kyoto rats. Neuropsychopharmacology 2006, 31(11):2449-2461. 10.1038/sj.npp.1301100.
44. Rasmussen K. The role of the locus coeruleus and N-methyl-D-aspartic acid (NMDA) and AMPA receptors in opiate withdrawal. Neuropsychopharmacology 1995, 13(4):295-300. 10.1016/0893-133X(95)00082-O.
45. Rasmussen K., Aghajanian G.K. Withdrawal-induced activation of locus coeruleus neurons in opiate-dependent rats: Attenuation by lesions of the nucleus paragigantocellularis. Brain Research 1989, 505(2):346-350.
46. Rasmussen K., Beitner-Johnson D.B., Krystal J.H., Aghajanian G.K., Nestler E.J. Opiate withdrawal and the rat locus coeruleus: Behavioral, electrophysiological, and biochemical correlates. Journal of Neuroscience 1990, 10(7):2308-2317.
47. Reyes B.A., Carvalho A.F., Vakharia K., Van Bockstaele E.J. Amygdalar peptidergic circuits regulating noradrenergic locus coeruleus neurons: Linking limbic and arousal centers. Experimental Neurology 2011, 230(1):96-105.
48. Reyes B.A., Chavkin C., Van Bockstaele E.J. Subcellular targeting of kappa-opioid receptors in the rat nucleus locus coeruleus. The Journal of Comparative Neurology 2009, 512(3):419-431.
49. Reyes B.A., Chavkin C., Van Bockstaele E.J. Agonist-induced internalization of kappa-opioid receptors in noradrenergic neurons of the rat locus coeruleus. Journal of Chemical Neuroanatomy 2010, 40(4):301-309.
50. Reyes B.A., Drolet G., Van Bockstaele E.J. Dynorphin and stress-related peptides in rat locus coeruleus: Contribution of amygdalar efferents. The Journal of Comparative Neurology 2008, 508(4):663-675.
51. Reyes B.A., Glaser J.D., Van Bockstaele E.J. Ultrastructural evidence for co-localization of corticotropin-releasing factor receptor and mu-opioid receptor in the rat nucleus locus coeruleus. Neuroscience Letters 2007, 413(3):216-221.
52. Reyes B.A.S., Johnson A.D., Glaser J.D., Commons K.G., Van Bockstaele E.J. Dynorphin-containing axons directly innervate noradrenergic neurons in the rat nucleus locus coeruleus. Neuroscience 2007, 145:1077-1086.
53. Rodgers R.J., Randall J.I. Social conflict analgesia: Studies on naloxone antagonism and morphine cross-tolerance in male DBA/2 mice. Pharmacology, Biochemistry, and Behavior 1985, 23(5):883-887.
54. Rouzade-Dominguez M.L., Curtis A.L., Valentino R.J. Role of Barrington's nucleus in the activation of rat locus coeruleus neurons by colonic distension. Brain Research 2001, 917(2):206-218.
55. Schluger J.H., Bart G., Green M., Ho A., Kreek M.J. Corticotropin-releasing factor testing reveals a dose-dependent difference in methadone maintained vs control subjects. Neuropsychopharmacology 2003, 28(5):985-994.
56. Sinha R. The role of stress in addiction relapse. Current Psychiatry Reports 2007, 9(5):388-395.
57. Stewart J. Stress and relapse to drug seeking: Studies in laboratory animals shed light on mechanisms and sources of long-term vulnerability. The American Journal on Addictions/American Academy of Psychiatrists in Alcoholism and Addictions 2003, 12(1):1-17.
58. Strawn J.R., Geracioti T.D. Noradrenergic dysfunction and the psychopharmacology of posttraumatic stress disorder. Depression and Anxiety 2008, 25(3):260-271. 10.1002/da.20292.
59. Thompson M.L., Miczek K.A., Noda K., Shuster L., Kumar M.S. Analgesia in defeated mice: Evidence for mediation via central rather than pituitary or adrenal endogenous opioid peptides. Pharmacology, Biochemistry, and Behavior 1988, 29(3):451-456.
60. Tidey J.W., Miczek K.A. Acquisition of cocaine self-administration after social stress: Role of accumbens dopamine. Psychopharmacology 1997, 130(3):203-212.
61. Tjoumakaris S.I., Rudoy C., Peoples J., Valentino R.J., Van Bockstaele E.J. Cellular interactions between axon terminals containing endogenous opioid peptides or corticotropin-releasing factor in the rat locus coeruleus and surrounding dorsal pontine tegmentum. The Journal of Comparative Neurology 2003, 466(4):445-456.
62. Valentino R.J., Curtis A.L., Page M.E., Pavcovich L.A., Florin-Lechner S.M. Activation of the locus ceruleus brain noradrenergic system during stress: Circuitry, consequences, and regulation. Advances in Pharmacology 1998, 42:781-784.
63. Valentino R.J., Foote S.L. Corticotropin-releasing factor disrupts sensory responses of brain noradrenergic neurons. Neuroendocrinology 1987, 45(1):28-36.
64. Valentino R.J., Foote S.L., Aston-Jones G. Corticotropin-releasing factor activates noradrenergic neurons of the locus coeruleus. Brain Research 1983, 270(2):363-367.
65. Valentino R.J., Page M.E., Curtis A.L. Activation of noradrenergic locus coeruleus neurons by hemodynamic stress is due to local release of corticotropin-releasing factor. Brain Research 1991, 555(1):25-34.
66. Valentino R.J., Rudoy C., Saunders A., Liu X.B., Van Bockstaele E.J. Corticotropin-releasing factor is preferentially colocalized with excitatory rather than inhibitory amino acids in axon terminals in the peri-locus coeruleus region. Neuroscience 2001, 106(2):375-384.
67. Valentino R.J., Van Bockstaele E. Opposing regulation of the locus coeruleus by corticotropin-releasing factor and opioids. Potential for reciprocal interactions between stress and opioid sensitivity. Psychopharmacology 2001, 158(4):331-342. 10.1007/s002130000673.
68. Valentino R.J., Van Bockstaele E.J. Functional interactions between stress neuromediators and the locus-coeruleus noradrenaline system. Handbook of stress and the brain 2005, 465-486. Elsevier, Amsterdam. N. Kalin, T. Steckler, J.M.H.M. Reul (Eds.).
69. Valentino R.J., Wehby R.G. Corticotropin-releasing factor: Evidence for a neurotransmitter role in the locus ceruleus during hemodynamic stress. Neuroendocrinology 1988, 48(6):674-677.
70. Van Bockstaele E.J., Bajic D., Proudfit H., Valentino R.J. Topographic architecture of stress-related pathways targeting the noradrenergic locus coeruleus. Physiology and Behavior 2001, 73(3):273-283.
71. Van Bockstaele E.J., Chan J., Pickel V.M. Input from central nucleus of the amygdala efferents to pericoerulear dendrites, some of which contain tyrosine hydroxylase immunoreactivity. Journal of Neuroscience Research 1996, 45(3):289-302.
72. Van Bockstaele E.J., Colago E.E.O., Valentino R.J. Corticotropin-releasing factor-containing axon terminals synapse onto catecholamine dendrites and may presynaptically modulate other afferents int he rostral pole of the nucleus locus coeruleus in the rat brain. The Journal of Comparative Neurology 1996, 364:523-534.
73. Van Bockstaele E.J., Colago E.E.O., Valentino R.J. Amygdaloid corticotropin-releasing factor targets locus coeruleus dendrites: Substrate for the co-ordination of emotional and cognitive limbs of the stress response. Journal of Neuroendocrinology 1998, 10:743-757.
74. Van Bockstaele E.J., Menko A.S., Drolet G. Neuroadaptive responses in brainstem noradrenergic nuclei following chronic morphine exposure. Molecular Neurobiology 2001, 23(2-3):155-171.
75. Van Bockstaele E.J., Peoples J., Menko A.S., McHugh K., Drolet G. Decreases in endogenous opioid peptides in the rat medullo-coerulear pathway after chronic morphine treatment. Journal of Neuroscience 2000, 20(23):8659-8666.
76. Van Bockstaele E.J., Peoples J., Valentino R.J. A.E. Bennett Research Award. Anatomic basis for differential regulation of the rostrolateral peri-locus coeruleus region by limbic afferents. Biological Psychiatry 1999, 46(10):1352-1363.
77. Van Bockstaele E.J., Reyes B.A., Valentino R.J. The locus coeruleus: A key nucleus where stress and opioids intersect to mediate vulnerability to opiate abuse. Brain Research 2010, 1314:162-174.
78. Van Bockstaele E.J., Saunders A., Commons K.G., Liu X.B., Peoples J. Evidence for coexistence of enkephalin and glutamate in axon terminals and cellular sites for functional interactions of their receptors in the rat locus coeruleus. The Journal of Comparative Neurology 2000, 417(1):103-114.
79. Waterhouse B.D., Lin C.S., Burne R.A., Woodward D.J. The distribution of neocortical projection neurons in the locus coeruleus. The Journal of Comparative Neurology 1983, 217(4):418-431.
80. Wiedenmayer C.P., Noailles P.A., Angulo J.A., Barr G.A. Stress-induced preproenkephalin mRNA expression in the amygdala changes during early ontogeny in the rat. Neuroscience 2002, 114(1):7-11.
81. Xu G., Van Bockstaele E.J., Reyes B., Bethea T., Valentino R.J. Chronic morphine sensitizes the brain norepinephrine system to stress. Journal of Neuroscience 2004, 24:8193-8197.
82. Zachariou V., Liu R., LaPlant Q., Xiao G., Renthal W., Chan G.C., et al. Distinct roles of adenylyl cyclases 1 and 8 in opiate dependence: Behavioral, electrophysiological, and molecular studies. Biological Psychiatry 2008, 63(11):1013-1021. 10.1016/j.biopsych.2007.11.021.