Sex-biased stress signaling: The corticotropin-releasing factor receptor as a model

Molecular Pharmacology

Volumn 83, Issue 4, 2013, Pages 737-745

  Valentino, Rita J ^a   Bangasser, Debra ^b   Van Bockstaele, Elisabeth J ^c  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b TEMPLE UNIVERSITY   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ARRESTIN 2; CORTICOTROPIN RELEASING FACTOR RECEPTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; G PROTEIN COUPLED RECEPTOR; NORADRENALIN; STIMULATORY GUANINE NUCLEOTIDE BINDING PROTEIN;

ALCOHOL ABUSE; BRAIN NERVE CELL; CELL MIGRATION; CELLULAR STRESS SIGNAL; CHRONIC STRESS; CLINICAL FEATURE; COPING BEHAVIOR; DISEASE ASSOCIATION; DRUG ABUSE; FEMALE; HUMAN; INTERNALIZATION; LOCUS CERULEUS; MALE; MENTAL DISEASE; NEUROTRANSMISSION; PATHOLOGY; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; SIGNAL TRANSDUCTION; STRESS;

ANIMALS; CORTICOTROPIN-RELEASING HORMONE; FEMALE; HUMANS; MALE; MENTAL DISORDERS; MODELS, CHEMICAL; MODELS, MOLECULAR; PROTEIN TRANSPORT; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; SEX CHARACTERISTICS; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL;

EID: 84875470081     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.112.083550     Document Type: Review

References (104)

1. Alonso J, Petukhova M, Vilagut G, Chatterji S, Heeringa S, Üstün TB, Alhamzawi AO, Viana MC, Angermeyer M, and Bromet E et al. (2011) Days out of role due to common physical and mental conditions: results from the WHO World Mental Health surveys. Mol Psychiatry 16:1234-1246.
2. Anisman H, Prakash P, Merali Z, and Poulter MO (2007) Corticotropin releasing hormone receptor alterations elicited by acute and chronic unpredictable stressor challenges in stressor-susceptible and resilient strains of mice. Behav Brain Res 181:180-190.
3. Arborelius L, Owens MJ, Plotsky PM, and Nemeroff CB (1999) The role of corticotropin-releasing factor in depression and anxiety disorders. J Endocrinol 160:1-12.
4. Aston-Jones G and Cohen JD (2005) An integrative theory of locus coeruleusnorepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci 28:403-450.
5. Aston-Jones G, Rajkowski J, and Cohen J (1999) Role of locus coeruleus in attention and behavioral flexibility. Biol Psychiatry 46:1309-1320.
6. Aston-Jones G, Shipley MT, and Grzanna R (1995) The locus coeruleus, A5 and A7 noradrenergic cell groups, in The Rat Brain (Paxinos G, ed, ed) pp 183-213, Academic Press, San Diego, CA.
7. Austin MC, Janosky JE, and Murphy HA (2003) Increased corticotropin-releasing hormone immunoreactivity in monoamine-containing pontine nuclei of depressed suicide men. Mol Psychiatry 8:324-332.
8. Baker DG, West SA, Nicholson WE, Ekhator NN, Kasckow JW, Hill KK, Bruce AB, Orth DN, and Geracioti TD, Jr (1999) Serial CSF corticotropin-releasing hormone levels and adrenocortical activity in combat veterans with posttraumatic stress disorder. Am J Psychiatry 156:585-588.
9. Bale TL, Contarino A, Smith GW, Chan R, Gold LH, Sawchenko PE, Koob GF, ValeWW, and Lee KF (2000) Mice deficient for corticotropin-releasing hormone receptor-2 display anxiety-like behaviour and are hypersensitive to stress. Nat Genet 24:410-414.
10. Bale TL and Vale WW (2004) CRF and CRF receptors: role in stress responsivity and other behaviors. Annu Rev Pharmacol Toxicol 44:525-557.
11. Bangasser DA, Curtis A, Reyes BA, Bethea TT, Parastatidis I, Ischiropoulos H, Van Bockstaele EJ, and Valentino RJ (2010) Sex differences in corticotropin-releasing factor receptor signaling and trafficking: potential role in female vulnerability to stress-related psychopathology. Mol Psychiatry 15:877-, 896-904.
12. Bangasser DA, Reyes BA, Piel D, Garachh V, Zhang XY, Plona ZM, Van Bockstaele EJ, Beck SG, and Valentino RJ (2012) Increased vulnerability of the brain norepinephrine system of females to corticotropin-releasing factor overexpression. Mol Psychiatry doi: 10.1038/mp.2012.24. [Epub ahead of print].
13. Bangasser DA, Zhang X, Garachh V, Hanhauser E, and Valentino RJ (2011) Sexual dimorphism in locus coeruleus dendritic morphology: a structural basis for sex differences in emotional arousal. Physiol Behav 103:342-351.
14. Bayatti N, Hermann H, Lutz B, and Behl C (2005) Corticotropin-releasing hormonemediated induction of intracellular signaling pathways and brain-derived neurotrophic factor expression is inhibited by the activation of the endocannabinoid system. Endocrinology 146:1205-1213.
15. Berridge CW and Waterhouse BD (2003) The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Brain Res Rev 42:33-84.
16. Bijlsma EY, van Leeuwen ML, Westphal KG, Olivier B, and Groenink L (2011) Local repeated corticotropin-releasing factor infusion exacerbates anxiety- and fearrelated behavior: differential involvement of the basolateral amygdala and medial prefrontal cortex. Neuroscience 173:82-92.
17. Bissette G, Klimek V, Pan J, Stockmeier C, and Ordway G (2003) Elevated concentrations of CRF in the locus coeruleus of depressed subjects. Neuropsychopharmacology 28:1328-1335.
18. Bohn LM and McDonald PH (2010) Seeking ligand bias: assessing GPCR coupling to beta-arrestins for drug discovery. Drug Discov Today Technol 7:e37-e42.
19. Bremner JD, Licinio J, Darnell A, Krystal JH, Owens MJ, Southwick SM, Nemeroff CB, and Charney DS (1997) Elevated CSF corticotropin-releasing factor concentrations in posttraumatic stress disorder. Am J Psychiatry 154:624-629.
20. Breslau N (2001) The epidemiology of posttraumatic stress disorder: what is the extent of the problem? J Clin Psychiatry 62 (Suppl 17):16-22.
21. Breslau N (2002) Gender differences in trauma and posttraumatic stress disorder. J Gend Specif Med 5:34-40.
22. Breslau N (2009) The epidemiology of trauma, PTSD, and other posttrauma disorders. Trauma Violence Abuse 10:198-210.
23. Breslau N, Chilcoat HD, Kessler RC, and Davis GC (1999) Previous exposure to trauma and PTSD effects of subsequent trauma: results from the Detroit Area Survey of Trauma. Am J Psychiatry 156:902-907.
24. Bromet E, Andrade LH, Hwang I, Sampson NA, Alonso J, de Girolamo G, de Graaf R, Demyttenaere K, Hu C, and Iwata N et al. (2011) Cross-national epidemiology of DSM-IV major depressive episode. BMC Med 9:90.
25. Bychkov E, Ahmed MR, and Gurevich EV (2011) Sex differences in the activity of signalling pathways and expression of G-protein-coupled receptor kinases in the neonatal ventral hippocampal lesion model of schizophrenia. Int J Neuropsychopharmacol 14:1-15.
26. Chalmers DT, Lovenberg TW, Grigoriadis DE, Behan DP, and De Souza EB (1996) Corticotrophin-releasing factor receptors: from molecular biology to drug design. Trends Pharmacol Sci 17:166-172.
27. Chen A, Perrin M, Brar B, Li C, Jamieson P, Digruccio M, Lewis K, and Vale W (2005) Mouse corticotropin-releasing factor receptor type 2alpha gene: isolation, distribution, pharmacological characterization and regulation by stress and glucocorticoids. Mol Endocrinol 19:441-458.
28. Cibelli G, Corsi P, Diana G, Vitiello F, and Thiel G (2001) Corticotropin-releasing factor triggers neurite outgrowth of a catecholaminergic immortalized neuron via cAMP and MAP kinase signalling pathways. Eur J Neurosci 13:1339-1348.
29. Csernansky JG, Dong H, Fagan AM, Wang L, Xiong C, Holtzman DM, and Morris JC (2006) Plasma cortisol and progression of dementia in subjects with Alzheimertype dementia. Am J Psychiatry 163:2164-2169.
30. Curtis AL, Bello NT, and Valentino RJ (2001) Endogenous opioids in the locus coeruleus function to limit the noradrenergic response to stress. J Neurosci 21:RC152.
31. Curtis AL, Bethea T, and Valentino RJ (2006) Sexually dimorphic responses of the brain norepinephrine system to stress and corticotropin-releasing factor. Neuropsychopharmacology 31:544-554.
32. Curtis AL, Lechner SM, Pavcovich LA, and Valentino RJ (1997) 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 281: 163-172.
33. Curtis AL, Leiser SC, Snyder K, and Valentino RJ (2012) Predator stress engages corticotropin-releasing factor and opioid systems to alter the operating mode of locus coeruleus norepinephrine neurons. Neuropharmacology 62:1737-1745.
34. de Kloet ER, Joëls M, and Holsboer F (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6:463-475.
35. Dirks A, Groenink L, Bouwknecht JA, Hijzen TH, Van Der Gugten J, Ronken E, Verbeek JS, Veening JG, Dederen PJ, and Korosi A et al. (2002) Overexpression of corticotropin-releasing hormone in transgenic mice and chronic stress-like autonomic and physiological alterations. Eur J Neurosci 16:1751-1760.
36. Figueira ML and Ouakinin S (2010) Gender-related endocrinological dysfunction and mental disorders. Curr Opin Psychiatry 23:369-372.
37. Gaub M and Carlson CL (1997) Gender differences in ADHD: a meta-analysis and critical review. J Am Acad Child Adolesc Psychiatry 36:1036-1045.
38. Gold PW and Chrousos GP (2002) Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs low CRH/NE states. Mol Psychiatry 7:254-275.
39. Gold PW, Goodwin FK, and Chrousos GP (1988a) Clinical and biochemical manifestations of depression: relationship to the neurobiology of stress (Part 1). N Engl J Med 316:348-353.
40. Gold PW, Goodwin FK, and Chrousos GP (1988b) Clinical and biochemical manifestations of depression. Relation to the neurobiology of stress (2). N Engl J Med 319:413-420.
41. Grammatopoulos DK and Chrousos GP (2002) Functional characteristics of CRH receptors and potential clinical applications of CRH-receptor antagonists. Trends Endocrinol Metab 13:436-444.
42. Grigoriadis DE and De Souza EB (1989) Heterogeneity between brain and pituitary corticotropin-releasing factor receptors is due to differential glycosylation. Endocrinology 125:1877-1888.
43. Groenink L, Pattij T, De Jongh R, Van der Gugten J, Oosting RS, Dirks A, and Olivier B (2003) 5-HT1A receptor knockout mice and mice overexpressing corticotropin-releasing hormone in models of anxiety. Eur J Pharmacol 463:185-197.
44. Hammack SE, Schmid MJ, LoPresti ML, Der-Avakian A, Pellymounter MA, Foster AC, Watkins LR, and Maier SF (2003) Corticotropin releasing hormone type 2 receptors in the dorsal raphe nucleus mediate the behavioral consequences of uncontrollable stress. J Neurosci 23:1019-1025.
45. Hauger RL, Grigoriadis DE, Dallman MF, Plotsky PM, Vale WW, and Dautzenberg FM (2003) International Union of Pharmacology. XXXVI. Current status of the nomenclature for receptors for corticotropin-releasing factor and their ligands. Pharmacol Rev 55:21-26.
46. Hauger RL, Risbrough V, Brauns O, and Dautzenberg FM (2006) Corticotropin releasing factor (CRF) receptor signaling in the central nervous system: new molecular targets. CNS Neurol Disord Drug Targets 5:453-479.
47. Hauger RL, Risbrough V, Oakley RH, Olivares-Reyes JA, and Dautzenberg FM (2009) Role of CRF receptor signaling in stress vulnerability, anxiety, and depression. Ann N Y Acad Sci 1179:120-143.
48. Heinrichs SC, Min H, Tamraz S, Carmouché M, Boehme SA, and Vale WW (1997) Anti-sexual and anxiogenic behavioral consequences of corticotropin-releasing factor overexpression are centrally mediated. Psychoneuroendocrinology 22: 215-224.
49. Hillhouse EW and Grammatopoulos DK (2006) The molecular mechanisms underlying the regulation of the biological activity of corticotropin-releasing hormone receptors: implications for physiology and pathophysiology. Endocr Rev 27: 260-286.
50. Hiroi N, Wong ML, Licinio J, Park C, Young M, Gold PW, Chrousos GP, and Bornstein SR (2001) Expression of corticotropin releasing hormone receptors type I and type II mRNA in suicide victims and controls. Mol Psychiatry 6: 540-546.
51. Hoare SR, Sullivan SK, Schwarz DA, Ling N, Vale WW, Crowe PD, and Grigoriadis DE (2004) Ligand affinity for amino-terminal and juxtamembrane domains of the corticotropin releasing factor type I receptor: regulation by G-protein and nonpeptide antagonists. Biochemistry 43:3996-4011.
52. Holmes KD, Babwah AV, Dale LB, Poulter MO, and Ferguson SS (2006) Differential regulation of corticotropin releasing factor 1alpha receptor endocytosis and trafficking by beta-arrestins and Rab GTPases. J Neurochem 96:934-949.
53. Holsboer F (1999) The rationale for corticotropin-releasing hormone receptor (CRHR) antagonists to treat depression and anxiety. J Psychiatr Res 33:181-214.
54. Jaferi A and Bhatnagar S (2007) Corticotropin-releasing hormone receptors in the medial prefrontal cortex regulate hypothalamic-pituitary-adrenal activity and anxiety-related behavior regardless of prior stress experience. Brain Res 1186:212-223.
55. Jedema HP and Grace AA (2004) Corticotropin-releasing hormone directly activates noradrenergic neurons of the locus ceruleus recorded in vitro. J Neurosci 24: 9703-9713.
56. Kendler KS, Kessler RC, Walters EE, MacLean C, Neale MC, Heath AC, and Eaves LJ (1995) Stressful life events, genetic liability, and onset of an episode of major depression in women. Am J Psychiatry 152:833-842.
57. Kessler RC (2003) Epidemiology of women and depression. J Affect Disord 74:5-13.
58. Kessler RC, McGonagle KA, Nelson CB, Hughes M, Swartz M, and Blazer DG (1994) Sex and depression in the National Comorbidity Survey. II: Cohort effects. J Affect Disord 30:15-26.
59. Kohout TA and Lefkowitz RJ (2003) Regulation of G protein-coupled receptor kinases and arrestins during receptor desensitization. Mol Pharmacol 63:9-18.
60. Leake A, Perry EK, Perry RH, Fairbairn AF, and Ferrier IN (1990) Cortical concentrations of corticotropin-releasing hormone and its receptor in Alzheimer type dementia and major depression. Biol Psychiatry 28:603-608.
61. Lefkowitz RJ and Shenoy SK (2005) Transduction of receptor signals by betaarrestins. Science 308:512-517.
62. Lovenberg TW, Liaw CW, Grigoriadis DE, Clevenger W, Chalmers DT, De Souza EB, and Oltersdorf T (1995) Cloning and characterization of a functionally distinct corticotropin-releasing factor receptor subtype from rat brain. Proc Natl Acad Sci USA 92:836-840.
63. Lu A, Steiner MA, Whittle N, Vogl AM, Walser SM, Ableitner M, Refojo D, Ekker M, Rubenstein JL, and Stalla GK et al. (2008) Conditional mouse mutants highlight mechanisms of corticotropin-releasing hormone effects on stress-coping behavior. Mol Psychiatry 13:1028-1042.
64. Magalhaes AC, Holmes KD, Dale LB, Comps-Agrar L, Lee D, Yadav PN, Drysdale L, Poulter MO, Roth BL, and Pin JP et al. (2010) CRF receptor 1 regulates anxiety behavior via sensitization of 5-HT2 receptor signaling. Nat Neurosci 13:622-629.
65. Merali Z, Du L, Hrdina P, Palkovits M, Faludi G, Poulter MO, and Anisman H (2004) Dysregulation in the suicide brain: mRNA expression of corticotropin-releasing hormone receptors and GABA(A) receptor subunits in frontal cortical brain region. J Neurosci 24:1478-1485.
66. Million M, Wang L, Stenzel-Poore MP, Coste SC, Yuan PQ, Lamy C, Rivier J, Buffington T, and Taché Y (2007) Enhanced pelvic responses to stressors in female CRF-overexpressingmice. Am J Physiol Regul Integr Comp Physiol 292:R1429-R1438.
67. Nemeroff CB, Widerlöv E, Bissette GT, Walléus H, Karlsson I, Eklund K, Kilts CD, Loosen PT, and ValeW(1984) Elevated concentrations of CSF corticotropin-releasing factor-like immunoreactivity in depressed patients. Science 226:1342-1344.
68. Oakley RH, Olivares-Reyes JA, Hudson CC, Flores-Vega F, Dautzenberg FM, and Hauger RL (2007) Carboxyl-terminal and intracellular loop sites for CRF1 receptor phosphorylation and beta-arrestin-2 recruitment: a mechanism regulating stress and anxiety responses. Am J Physiol Regul Integr Comp Physiol 293: R209-R222.
69. Perrin MH, Donaldson CJ, Chen R, Lewis KA, and Vale WW (1993) Cloning and functional expression of a rat brain corticotropin releasing factor (CRF) receptor. Endocrinology 133:3058-3061.
70. Rajagopal S, Ahn S, Rominger DH, Gowen-MacDonald W, Lam CM, Dewire SM, Violin JD, and Lefkowitz RJ (2011) Quantifying ligand bias at seven-transmembrane receptors. Mol Pharmacol 80:367-377.
71. Ramtekkar UP, Reiersen AM, Todorov AA and Todd RD (2010) Sex and age differences in attention-deficit/hyperactivity disorder symptoms and diagnoses: implications for DSM-V and ICD-11. J Am Acad Child Adolesc Psychiatry 49:217-228, e211-213.
72. Reyes BA, Fox K, Valentino RJ, and Van Bockstaele EJ (2006) Agonist-induced internalization of corticotropin-releasing factor receptors in noradrenergic neurons of the rat locus coeruleus. Eur J Neurosci 23:2991-2998.
73. Reyes BA, Valentino RJ, and Van Bockstaele EJ (2008) Stress-induced intracellular trafficking of corticotropin-releasing factor receptors in rat locus coeruleus neurons. Endocrinology 149:122-130.
74. Ruitenberg A, Ott A, van Swieten JC, Hofman A, and Breteler MM (2001) Incidence of dementia: does gender make a difference? Neurobiol Aging 22:575-580.
75. Sánchez MM, Young LJ, Plotsky PM, and Insel TR (1999) Autoradiographic and in situ hybridization localization of corticotropin- releasing factor 1 and 2 receptors in nonhuman primate brain. J Comp Neurol 408:365-377.
76. Sautter FJ, Bissette G, Wiley J, Manguno-Mire G, Schoenbachler B, Myers L, Johnson JE, Cerbone A, and Malaspina D (2003) Corticotropin-releasing factor in posttraumatic stress disorder (PTSD) with secondary psychotic symptoms, nonpsychotic PTSD, and healthy control subjects. Biol Psychiatry 54:1382-1388.
77. Sheng H, Sun T, Cong B, He P, Zhang Y, Yan J, Lu C, and Ni X (2008) Corticotropinreleasing hormone stimulates SGK-1 kinase expression in cultured hippocampal neurons via CRH-R1. Am J Physiol Endocrinol Metab 295:E938-E946.
78. Shipley MT, Fu L, Ennis M, Liu WL, and Aston-Jones G (1996) Dendrites of locus coeruleus neurons extend preferentially into two pericoerulear zones. J Comp Neurol 365:56-68.
79. Snyder K, Wang WW, Han R, McFadden K, and Valentino RJ (2012) Corticotropinreleasing factor in the norepinephrine nucleus, locus coeruleus, facilitates behavioral flexibility. Neuropsychopharmacology 37:520-530.
80. Southwick SM, Bremner JD, Rasmusson A, Morgan CA, 3rd, Arnsten A, and Charney DS (1999) Role of norepinephrine in the pathophysiology and treatment of posttraumatic stress disorder. Biol Psychiatry 46:1192-1204.
81. Stenzel-Poore MP, Heinrichs SC, Rivest S, Koob GF, and Vale WW (1994) Overproduction of corticotropin-releasing factor in transgenic mice: a genetic model of anxiogenic behavior. J Neurosci 14:2579-2584.
82. Swinny JD and Valentino RJ (2006) Corticotropin-releasing factor promotes growth of brain norepinephrine neuronal processes through Rho GTPase regulators of the actin cytoskeleton in rat. Eur J Neurosci 24:2481-2490.
83. Tolin DF and Foa EB (2006) Sex differences in trauma and posttraumatic stress disorder: a quantitative review of 25 years of research. Psychol Bull 132:959-992.
84. Traver S, Marien M, Martin E, Hirsch EC, and Michel PP (2006) The phenotypic differentiation of locus ceruleus noradrenergic neurons mediated by brain-derived neurotrophic factor is enhanced by corticotropin releasing factor through the activation of a cAMP-dependent signaling pathway. Mol Pharmacol 70:30-40.
85. Vale W, Spiess J, Rivier C, and Rivier J (1981) Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science 213:1394-1397.
86. Valentino RJ, Bangasser D, Plona Z, Ding H, and Seeholzer SH (2012) The sex biased phosphoproteome: a novel approach towards understanding the molecular basis for sex differences in neuropsychiatric diseases. Neuropsychopharmacology 38: S272-273. DOI: 10.1038/npp.2012.220
87. Valentino RJ and Commons KG (2005) Peptides that fine-tune the serotonin system. Neuropeptides 39:1-8.
88. Valentino RJ and Foote SL (1987) Corticotropin-releasing factor disrupts sensory responses of brain noradrenergic neurons. Neuroendocrinology 45:28-36.
89. Valentino RJ and Foote SL (1988) Corticotropin-releasing hormone increases tonic but not sensory-evoked activity of noradrenergic locus coeruleus neurons in unanesthetized rats. J Neurosci 8:1016-1025.
90. Valentino RJ, Page M, Van Bockstaele E, and Aston-Jones G (1992) Corticotropin-releasing factor innervation of the locus coeruleus region: distribution of fibers and sources of input. Neuroscience 48:689-705.
91. Valentino RJ, Page ME, and Curtis AL (1991) Activation of noradrenergic locus coeruleus neurons by hemodynamic stress is due to local release of corticotropin-releasing factor. Brain Res 555:25-34.
92. Valentino RJ, Rudoy C, Saunders A, Liu XB, and Van Bockstaele EJ (2001) Corticotropin-releasing factor is preferentially colocalized with excitatory rather than inhibitory amino acids in axon terminals in the peri-locus coeruleus region. Neuroscience 106:375-384.
93. Valentino RJ and Van Bockstaele E (2008) Convergent regulation of locus coeruleus activity as an adaptive response to stress. Eur J Pharmacol 583:194-203.
94. Van Bockstaele EJ, Bajic D, Proudfit H, and Valentino RJ (2001) Topographic architecture of stress-related pathways targeting the noradrenergic locus coeruleus. Physiol Behav 73:273-283.
95. Van Bockstaele EJ, Colago EE, and Valentino RJ (1996) Corticotropin-releasing factor-containing axon terminals synapse onto catecholamine dendrites and may presynaptically modulate other afferents in the rostral pole of the nucleus locus coeruleus in the rat brain. J Comp Neurol 364:523-534.
96. Van Bockstaele EJ, Colago EEO, and Valentino RJ (1998) Amygdaloid corticotropinreleasing factor targets locus coeruleus dendrites: substrate for the co-ordination of emotional and cognitive limbs of the stress response. J Neuroendocrinol 10: 743-757.
97. Van Bockstaele EJ, Peoples J, and Valentino RJ (1999) A.E. Bennett Research Award. Anatomic basis for differential regulation of the rostrolateral peri-locus coeruleus region by limbic afferents. Biol Psychiatry 46:1352-1363.
98. Van Pett K, Viau V, Bittencourt JC, Chan RK, Li HY, Arias C, Prins GS, Perrin M, Vale W, and Sawchenko PE (2000) Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J Comp Neurol 428:191-212.
99. Violin JD and Lefkowitz RJ (2007) Beta-arrestin-biased ligands at seventransmembrane receptors. Trends Pharmacol Sci 28:416-422.
100. Waterhouse BD, Devilbiss D, Fleischer D, Sessler FM, and Simpson KL (1998) New perspectives on the functional organization and postsynaptic influences of the locus ceruleus efferent projection system. Adv Pharmacol 42:749-754.
101. Whalen EJ, Rajagopal S, and Lefkowitz RJ (2011) Therapeutic potential of β-arrestin- and G protein-biased agonists. Trends Mol Med 17:126-139.
102. Wilson RS, Arnold SE, Schneider JA, Kelly JF, Tang Y, and Bennett DA (2006) Chronic psychological distress and risk of Alzheimer's disease in old age. Neuroepidemiology 27:143-153.
103. Xing G, Carlton J, Zhang L, Jiang X, Fullerton C, Li H, and Ursano R (2011) Cannabinoid receptor expression and phosphorylation are differentially regulated between male and female cerebellum and brain stem after repeated stress: implication for PTSD and drug abuse. Neurosci Lett 502:5-9.
104. Zeng J, Kitayama I, Yoshizato H, Zhang K, and Okazaki Y (2003) Increased expression of corticotropin-releasing factor receptor mRNA in the locus coeruleus of stress-induced rat model of depression. Life Sci 73:1131-1139.