Differential effects of inescapable stress on locus coeruleus GRK3, alpha2-adrenoceptor and CRF1 receptor levels in learned helpless and non-helpless rats: A potential link to stress resilience

Behavioural Brain Research

Volumn 221, Issue 1, 2011, Pages 25-33

  Taneja, Manish ^a   Salim, Samina ^a   Saha, Kaustuv ^a   Happe, H Kevin ^b   Qutna, Nidal ^b   Petty, Frederick ^b   Bylund, David B ^c   Eikenburg, Douglas C ^a  

^a UNIVERSITY OF HOUSTON   (United States)

^b CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Alpha2A AR; CRF1 receptor; GRK3; Learned helplessness; Resilience; Stress

Indexed keywords

ALPHA 2 ADRENERGIC RECEPTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; G PROTEIN COUPLED RECEPTOR KINASE 2; G PROTEIN COUPLED RECEPTOR KINASE 3; TYROSINE 3 MONOOXYGENASE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN LEVEL; CONTROLLED STUDY; COPING BEHAVIOR; CORPUS STRIATUM; DOWN REGULATION; ENZYME ACTIVITY; ESCAPE BEHAVIOR; LEARNED HELPLESSNESS; LOCUS CERULEUS; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CARBONYLATION; RAT; STRESS;

ANIMALS; BRAIN; CLUSTER ANALYSIS; DOWN-REGULATION; ELECTRIC STIMULATION; G-PROTEIN-COUPLED RECEPTOR KINASE 2; G-PROTEIN-COUPLED RECEPTOR KINASE 3; HELPLESSNESS, LEARNED; LOCUS COERULEUS; MALE; PROTEIN CARBONYLATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, ALPHA-2; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; RESILIENCE, PSYCHOLOGICAL; STRESS, PSYCHOLOGICAL; TYROSINE 3-MONOOXYGENASE;

EID: 79952792916     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.02.018     Document Type: Article

References (45)

1. Maier S.F. Learned helplessness and animal models of depression. Prog Neuropsychopharmacol Biol Psychiatry 1984, 8:435-446.
2. Charney D.S. Psychobiological mechanisms of resilience and vulnerability: implications for successful adaptation to extreme stress. Am J Psychiatry 2004, 161:195-216.
3. Southwick S.M., Vythilingam M., Charney D.S. The psychobiology of depression and resilience to stress: implications for prevention and treatment. Annu Rev Clin Psychol 2005, 1:255-291.
4. Ahmed M.R., Bychkov E., Gurevich V.V., Benovic J.L., Gurevich E.V. Altered expression and subcellular distribution of GRK subtypes in the dopamine-depleted rat basal ganglia is not normalized by l-DOPA treatment. J Neurochem 2008, 104:1622-1636.
5. Dinieri J.A., Nemeth C.L., Parsegian A., Carle T., Gurevich V.V., Gurevich E., et al. Altered sensitivity to rewarding and aversive drugs in mice with inducible disruption of cAMP response element-binding protein function within the nucleus accumbens. J Neurosci 2009, 29:1855-1859.
6. Hauger R.L., Risbrough V., Oakley R.H., Olivares-Reyes J.A., Dautzenberg F.M. Role of CRF receptor signaling in stress vulnerability, anxiety, and depression. Ann N Y Acad Sci 2009, 1179:120-143.
7. Grange-Midroit M., Garcia-Sevilla J.A., Ferrer-Alcon M., La Harpe R., Huguelet P., Guimon J. Regulation of GRK 2 and 6, beta-arrestin-2 and associated proteins in the prefrontal cortex of drug-free and antidepressant drug-treated subjects with major depression. Brain Res Mol Brain Res 2003, 111:31-41.
8. Ertley R.N., Bazinet R.P., Lee H.J., Rapoport S.I., Rao J.S. Chronic treatment with mood stabilizers increases membrane GRK3 in rat frontal cortex. Biol Psychiatry 2007, 61:246-249.
9. Barrett T.B., Emberton J.E., Nievergelt C.M., Liang S.G., Hauger R.L., Eskin E., et al. Further evidence for association of GRK3 to bipolar disorder suggests a second disease mutation. Psychiatr Genet 2007, 17:315-322.
10. Cryan J.F., Mombereau C., Vassout A. The tail suspension test as a model for assessing antidepressant activity: review of pharmacological and genetic studies in mice. Neurosci Biobehav Rev 2005, 29:571-625.
11. Chourbaji S., Zacher C., Sanchis-Segura C., Dormann C., Vollmayr B., Gass P. Learned helplessness: validity and reliability of depressive-like states in mice. Brain Res Brain Res Protoc 2005, 16:70-78.
12. Bawa-Khalfe T., Altememi G.F., Mandyam C.D., Schwarz L.A., Eikenburg D.C., Standifer K.M. The presence of beta2-adrenoceptors sensitizes alpha2A-adrenoceptors to desensitization after chronic epinephrine treatment. BMC Pharmacol 2007, 7:16.
13. Desai A.N., Standifer K.M., Eikenburg D.C. Cellular G protein-coupled receptor kinase levels regulate sensitivity of the {alpha}2b-adrenergic receptor to undergo agonist-induced down-regulation. J Pharmacol Exp Ther 2005, 312:767-773.
14. Salim S., Hite B., Eikenburg D.C. Activation of the CRF(1) receptor causes ERK1/2 mediated increase in GRK3 expression in CATH.a cells. FEBS Lett 2007, 581:3204-3210.
15. Dautzenberg F.M., Braun S., Hauger R.L. GRK3 mediates desensitization of CRF1 receptors: a potential mechanism regulating stress adaptation. Am J Physiol Regul Integr Comp Physiol 2001, 280:R935-R946.
16. Hauger R.L., Smith R.D., Braun S., Dautzenberg F.M., Catt K.J. Rapid agonist-induced phosphorylation of the human CRF receptor, type 1: a potential mechanism for homologous desensitization. Biochem Biophys Res Commun 2000, 268:572-576.
17. Gold P.W., Chrousos G.P. Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs low CRH/NE states. Mol Psychiatry 2002, 7:254-275.
18. Zhu M.Y., Klimek V., Dilley G.E., Haycock J.W., Stockmeier C., Overholser J.C., et al. Elevated levels of tyrosine hydroxylase in the locus coeruleus in major depression. Biol Psychiatry 1999, 46:1275-1286.
19. Weiss J.M., Simson P.G. Depression in an animal model: focus on the locus ceruleus. Ciba Found Symp 1986, 123:191-215.
20. Erdtmann-Vourliotis M., Mayer P., Ammon S., Riechert U., Hollt V. Distribution of G-protein-coupled receptor kinase (GRK) isoforms 2, 3, 5 and 6 mRNA in the rat brain. Brain Res Mol Brain Res 2001, 95:129-137.
21. 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. J Pharmacol Exp Ther 1997, 281:163-172.
22. Berridge C.W., Abercrombie E.D. Relationship between locus coeruleus discharge rates and rates of norepinephrine release within neocortex as assessed by in vivo microdialysis. Neuroscience 1999, 93:1263-1270.
23. Petty F., Chae Y., Kramer G., Jordan S., Wilson L. Learned helplessness sensitizes hippocampal norepinephrine to mild restress. Biol Psychiatry 1994, 35:903-908.
24. Reed A.L., Anderson J.C., Bylund D.B., Petty F., El Refaey H., Happe H.K. Treatment with escitalopram but not desipramine decreases escape latency times in a learned helplessness model using juvenile rats. Psychopharmacology (Berl) 2009, 205:249-259.
25. Petty F., Kramer G., Wilson L. Prevention of learned helplessness: in vivo correlation with cortical serotonin. Pharmacol Biochem Behav 1992, 43:361-367.
26. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., et al. Measurement of protein using bicinchoninic acid. Anal Biochem 1985, 150:76-85.
27. Goto S., Nakamura A., Radak Z., Nakamoto H., Takahashi R., Yasuda K., et al. Carbonylated proteins in aging and exercise: immunoblot approaches. Mech Ageing Dev 1999, 107:245-253.
28. Takase L.F., Nogueira M.I., Bland S.T., Baratta M., Watkins L.R., Maier S.F., et al. Effect of number of tailshocks on learned helplessness and activation of serotonergic and noradrenergic neurons in the rat. Behav Brain Res 2005, 162:299-306.
29. Simson P.G., Weiss J.M., Hoffman L.J., Ambrose M.J. Reversal of behavioral depression by infusion of an alpha-2 adrenergic agonist into the locus coeruleus. Neuropharmacology 1986, 25:385-389.
30. Weiss J.M., Boss-Williams K.A., Moore J.P., Demetrikopoulos M.K., Ritchie J.C., West C.H. Testing the hypothesis that locus coeruleus hyperactivity produces depression-related changes via galanin. Neuropeptides 2005, 39:281-287.
31. Bangasser D.A., Curtis A., Reyes B.A., Bethea T.T., Parastatidis I., Ischiropoulos H., et al. Sex differences in corticotropin-releasing factor receptor signaling and trafficking: potential role in female vulnerability to stress-related psychopathology. Mol Psychiatry 2010.
32. 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 Res 2010, 1314:162-174.
33. Premont R.T. Once and future signaling: G protein-coupled receptor kinase control of neuronal sensitivity. Neuromol Med 2005, 7:129-147.
34. Ribas C., Penela P., Murga C., Salcedo A., Garcia-Hoz C., Jurado-Pueyo M., et al. The G protein-coupled receptor kinase (GRK) interactome: role of GRKs in GPCR regulation and signaling. Biochim Biophys Acta 2007, 1768:913-922.
35. Valentino R.J., Foote S.L., Aston-Jones G. Corticotropin-releasing factor activates noradrenergic neurons of the locus coeruleus. Brain Res 1983, 270:363-367.
36. Mateo Y., Pineda J., Meana J.J. Somatodendritic alpha2-adrenoceptors in the locus coeruleus are involved in the in vivo modulation of cortical noradrenaline release by the antidepressant desipramine. J Neurochem 1998, 71:790-798.
37. Bruchas M.R., Land B.B., Aita M., Xu M., Barot S.K., Li S., et al. Stress-induced p38 mitogen-activated protein kinase activation mediates kappa-opioid-dependent dysphoria. J Neurosci 2007, 27:11614-11623.
38. McLaughlin J.P., Land B.B., Li S., Pintar J.E., Chavkin C. Prior activation of kappa opioid receptors by U50,488 mimics repeated forced swim stress to potentiate cocaine place preference conditioning. Neuropsychopharmacology 2006, 31:787-794.
39. Xu M., Petraschka M., McLaughlin J.P., Westenbroek R.E., Caron M.G., Lefkowitz R.J., et al. Neuropathic pain activates the endogenous kappa opioid system in mouse spinal cord and induces opioid receptor tolerance. J Neurosci 2004, 24:4576-4584.
40. Dautzenberg F.M., Wille S., Braun S., Hauger R.L. GRK3 regulation during CRF- and urocortin-induced CRF1 receptor desensitization. Biochem Biophys Res Commun 2002, 298:303-308.
41. Thakker D.R., Standifer K.M. Induction of G protein-coupled receptor kinases 2 and 3 contributes to the cross-talk between mu and ORL1 receptors following prolonged agonist exposure. Neuropharmacology 2002, 43:979-990.
42. Salim S., Eikenburg D.C. Role of 90-kDa heat shock protein (Hsp 90) and protein degradation in regulating neuronal levels of G protein-coupled receptor kinase 3. J Pharmacol Exp Ther 2007, 320:1106-1112.
43. Greenwood B.N., Foley T.E., Day H.E., Campisi J., Hammack S.H., Campeau S., et al. Freewheel running prevents learned helplessness/behavioral depression: role of dorsal raphe serotonergic neurons. J Neurosci 2003, 23:2889-2898.
44. Salim S., Sarraj N., Taneja M., Saha K., Tejada-Simon M.V., Chugh G. Moderate treadmill exercise prevents oxidative stress-induced anxiety-like behavior in rats. Behav Brain Res 2010.
45. Butler P.D., Weiss J.M., Stout J.C., Nemeroff C.B. Corticotropin-releasing factor produces fear-enhancing and behavioral activating effects following infusion into the locus coeruleus. J Neurosci 1990, 10:176-183.