Altered Serotonergic Neurotransmission but Normal Hypothalamic-Pituitary- Adrenocortical Axis Activity in Mice Chronically Treated with the Corticotropin-Releasing Hormone Receptor Type I Antagonist NBI 30775

Neuropsychopharmacology

Volumn 28, Issue 12, 2003, Pages 2148-2159

  Oshima, Akihiko ^a,b   Flachskamm, Cornelia ^a   Reul, Johannes M H M ^a,c   Holsboer, Florian ^a   Linthorst, Astrid C E ^a,c  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^b Tatebayashi Kosei Hospital   (Japan)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Antagonist; Corticosterone; Corticotropin releasing hormone; Mice; Serotonin; Stress

Indexed keywords

3 (6 DIMETHYLAMINO 4 METHYL 3 PYRIDINYL) 7 DIPROPYLAMINO 2,5 DIMETHYLPYRAZOLO[1,5 A]PYRIMIDINE; 5 HYDROXYINDOLEACETIC ACID; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR ANTAGONIST; SEROTONIN; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; CHRONIC DRUG ADMINISTRATION; CIRCADIAN RHYTHM; CLIMBING; CONTROLLED STUDY; CORRELATION ANALYSIS; CORTICOSTERONE BLOOD LEVEL; DRUG EFFECT; DRUG EFFICACY; DRUG TOLERABILITY; FOOD INTAKE; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IN VIVO STUDY; MALE; MENTAL STRESS; MICRODIALYSIS; MOOD DISORDER; MOUSE; MOUSE STRAIN; NEUROTRANSMISSION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PSYCHOPHARMACOLOGY; SEROTONINERGIC SYSTEM; SWIMMING;

EID: 0344983946     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1300267     Document Type: Article

References (74)

1. Aguilera G, Rabadan-Diehl C, Nikodemova M (2001). Regulation of pituitary corticotropin releasing hormone receptors. Peptides 22: 769-774.
2. Arborelius L, Skelton KH, Thrivikraman KV, Plotsky PM, Schulz DW, Owens MJ (2000). Chronic administration of the selective corticotropin-releasing factor 1 receptor antagonist CP-154,526: behavioral, endocrine and neurochemical effects in the rat. J Pharmacol Exp Ther 294: 588-597.
3. Auerbach SB, Minzenberg MJ, Wilkinson LO (1989). Extracellular serotonin and 5-hydroxyindoleacetic acid in hypothalamus of the unanesthetized rat measured by in vivo dialysis coupled to high-performance liquid chromatography with electrochemical detection: dialysate serotonin reflects neuronal release. Brain Res 499: 281-290.
4. Bachmann CG, Linthorst ACE, Holsboer F, Reul JMHM (2003). Effect of chronic administration of selective glucocorticoid receptor antagonists on the rat hypothalamic-pituitary-adrenalcortical axis. Neuropsychopharmacology 28: 1056-1067.
5. Bittencourt JC, Sawchenko PE (2000). Do centrally administered neuropeptides access cognate receptors? An analysis in the central corticotropin-releasing factor system. J Neurosci 20: 1142-1156.
6. Bornstein SR, Webster EL, Torpy DJ, Richman SJ, Mitsiades N, Igel M et al (1998). Chronic effects of a nonpeptide corticotropin-releasing hormone type I receptor antagonist on pituitary-adrenal function, body weight, and metabolic regulation. Endocrinology 139: 1546-1555.
7. Carroll BJ, Feinberg M, Greden JF, Tarika J, Albala AA, Haskett RF et al (1981). A specific laboratory test for the diagnosis of melancholia. Standardization, validation, and clinical utility. Arch Gen Psychiatry 38: 15-22.
8. 1 receptor mRNA expression. J Neurosci 15: 6340-6350.
9. Chaouloff F (2000). Serotonin, stress and corticoids. J Psychopharmacol 14: 139-151.
10. Crespi F, Garratt JC, Sleight AJ, Marsden CA (1990). In vivo evidence that 5-hydroxytryptamine (5-HT) neuronal firing and release are not necessarily correlated with 5-HT metabolism. Neuroscience 35: 139-144.
11. Cryan JF, Markou A, Lucki I (2002). Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 23: 238-245.
12. Deak T, Nguyen KT, Ehrlich AL, Watkins LR, Spencer RL, Maier SF et al (1999). The impact of the nonpeptide corticotropin-releasing hormone antagonist antalarmin on behavioral and endocrine responses to stress. Endocrinology 140: 79-86.
13. Detke MJ, Rickels M, Lucki I (1995). Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology 121: 66-72.
14. Deuschle M, Schweiger U, Weber B, Gotthardt U, Korner A, Schmider J et al (1997). Diurnal activity and pulsatility of the hypothalamus-pituitary- adrenal system in male depressed patients and healthy controls. J Clin Endocrinol Metab 82: 234-238.
15. Dunn AJ (2000). Footshock-induced changes in brain catecholamines and indoleamines are not mediated by CRF or ACTH. Neurochem Int 37: 61-69.
16. Garcia-Lecumberri C, Ambrosio E (1998). Role of corticotropin-releasing factor in forced swimming test. Eur J Pharm 343: 17-26.
17. Grahame-Smith DG (1974). How important is the synthesis of brain 5-hydroxytryptamine in the physiological control of its central function? Adv Biochem Psychopharmacol 10: 83-91.
18. Griebel G, Perrault G, Sanger DJ (1998). Characterization of the behavioral profile of the non-peptide CRF receptor antagonist CP-154,526 in anxiety models in rodents. Comparison with diazepam and buspirone. Psychopharmacology 138: 55-66.
19. Griebel G, Simiand J, Steinberg R, Jung M, Gully D, Roger P et al (2002). 4-(2-Chloro-4-methoxy-5-methylphenyl)-N-[(1S)-2-cyclopropyl-1-(3-fluoro-4- methylphenyl)ethyl]5-methyl-N-(2-propynyl)-1,3-thiazol-2-amine hydrochloride (SSR125543A), a potent and selective corticotrophin-releasing factor(1) receptor antagonist. II. Characterization in rodent models of stress-related disorders. J Pharmacol Exp Ther 301: 333-345.
20. 1 receptor antagonist R121919 attenuates the behavioral and endocrine responses to stress. J Pharmacol Exp Ther 304: 874-880.
21. Heinrichs SC, De Souza EB, Schulteis G, Lapsansky JL, Grigoriadis DE (2002). Brain penetrance, receptor occupancy and antistress in vivo efficacy of a small molecule corticotropin releasing factor type I receptor selective antagonist. Neuropsychopharmacology 27: 194-202.
22. Holsboer F (1999). The rationale for corticotropin-releasing hormone receptor (CRH-R) antagonists to treat depression and anxiety. J Psychiatr Res 33: 181-214.
23. Isogawa K, Akiyoshi J, Hikichi T, Yamamoto Y, Tsutsumi T, Nagayama H (2000). Effect of corticotropin releasing factor receptor 1 antagonist on extracellular norepinephrine, dopamine and serotonin in hippocampus and prefrontal cortex of rats in vivo. Neuropeptides 34: 234-239.
24. Keck ME, Welt T, Wigger A, Renner U, Engelmann M, Holsboer F et al (2001). The anxiolytic effect of the CRH(1) receptor antagonist R121919 depends on innate emotionality in rats. EurJ Neurosci 13: 373-380.
25. Kirby LG, Rice KC, Valentino RJ (2000). Effects of corticotropin- releasing factor on neuronal activity in the serotonergic dorsal raphe nucleus. Neuropsychopharmacology 22: 148-162.
26. Kizer JS, Palkovits M, Kopin IJ, Saavedra JM, Brownstein MJ (1976). Lack of effect of various endocrine manipulations on tryptophan hydroxylase activity of individual nuclei of the hypothalamus, limbic system, and midbrain of the rat. Endocrinology 98: 743-747.
27. Kuhn DM, Wolf WA, Youdim MB (1986). Serotonin neurochemistry revisited: a new look at some old axioms. Neurochem Int 8: 141-154.
28. Laaris N, Hajdahmane S, Hamon M, Lanfumey L (1995). Glucocorticoid receptor-mediated inhibition by corticosterone of 5-HT1A autoreceptor functioning in the rat dorsal raphe nucleus. Neuropharmacology 34: 1201-1210.
29. Linkowski P, Mendlewicz J, Leclercq R, Brasseur M, Hubain P, Golstein J et al (1985). The 24-h profile of adrenocorticotropin and cortisol in major depressive illness. J Clin Endocrinol Metab 61: 429-438.
30. Linthorst ACE, Flachskamm C, Barden N, Holsboer F, Reul JMHM (2000). Glucocorticoid receptor impairment alters CNS responses to a psychological stressor: an in vivo microdialysis study in transgenic mice. Eur J Neurosci 12: 283-291.
31. Linthorst ACE, Flachskamm C, Holsboer F, Reul JMHM (1994). Local administration of recombinant human interleukin-1 beta in the rat hippocampus increases serotonergic neurotransmission, hypothalamic-pituitary-adrenocortical axis activity, and body temperature. Endocrinology 135: 520-532.
32. Linthorst ACE, Flachskamm C, Hopkins SJ, Hoadley ME, Labeur MS, Holsboer F et al (1997). Long-term intracerebroventricular infusion of corticotropin-releasing hormone alters neuroendocrine, neurochemical, autonomic, behavioral, and cytokine responses to a systemic inflammatory challenge. J Neurosci 17: 4448-4460.
33. Linthorst ACE, Flachskamm C, Müller-Preuss P, Holsboer F, Reul JMHM (1995). Effect of bacterial endotoxin and interleukin-1 beta on hippocampal serotonergic neurotransmission, behavioral activity, and free corticosterone levels: an in vivo microdialysis study. J Neurosci 15: 2920-2934.
34. Linthorst ACE, Karanth S, Barden N, Holsboer F, Reul JMHM (1999). Impaired glucocorticoid receptor function evolves in aberrant physiological responses to bacterial endotoxin. Eur J Neurosci 11: 178-186.
35. Linthorst ACE, Peñalva RG, Flachskamm C, Holsboer F, Reul JMHM (2002). Forced swim stress activates rat hippocampal serotonergic neurotransmission involving a corticotropin-releasing hormone receptor-dependent mechanism. Eur J Neurosci 16: 2441-2452.
36. Lowry CA, Johnson PL, Hathway NJA, Lightman SL (2002). Distribution of corticotropin-releasing factor receptor 1-(CRFR1) and CRFR2-immunoreactivity in limbic and caudal brainstem raphe nuclei. Program No 867 6 2002 Abstract Viewer/Itinerary Planner Washington, DC: Society for Neuroscience, 2002 CD-ROM.
37. Lowry CA, Rodda JE, Lightman SL, Ingram CD (2000). Corticotropin- releasing factor increases in vitro firing rates of serotonergic neurons in the rat dorsal raphe nucleus: evidence for activation of a topographically organized mesolimbocortical serotonergic system. J Neurosci 20: 7728-7736.
38. Lundkvist J, Chai Z, Teheranian R, Hasanvan H, Bartfai T, Jenck F et al (1996). A non peptidic corticotropin releasing factor receptor antagonist attenuates fever and exhibits anxiolytic-like activity. Eur J Pharmacol 309: 195-200.
39. Maes M, Meltzer HY (1995). The serotonin hypothesis of major depression. In: Bloom FE, Kupfer DJ (eds) Psychopharmacology: The Fourth Generation of Progress pp 933-944.
40. Millan MJ, Brocco M, Gobert A, Dorey G, Casara P, Dekeyne A (2001). Anxiolytic properties of the selective, non-peptidergic CRF(1) antagonists, CP154,526 and DMP695: a comparison to other classes of anxiolytic agent. Neuropsychopharmacology 25: 585-600.
41. Montkowski A, Barden N, Wotjak C, Stec I, Ganster J, Meaney M et al (1995). Long-term antidepressant treatment reduces behavioural deficits in transgenic mice with impaired glucocorticoid receptor function. J Neuroendocrinol 7: 841-845.
42. Nemeroff CB (1996). The corticotropin-releasing factor (CRF) hypothesis of depression: new findings and new directions. Mol Psychiatry 1: 336-342.
43. Nemeroff CB, Owens MJ, Bissette G, Andorn AC, Stanley M (1988). Reduced corticotropin releasing factor binding sites in the frontal cortex of suicide victims. Arch Gen Psychiatry 45: 577-579.
44. Nemeroff CB, Widerlov E, Bissette G, Walleus H, Karlsson I, Eklund K et al (1984). Elevated concentrations of CSF corticotropin-releasing factor-like immunoreactivity in depressed patients. Science 226: 1342-1344.
45. Owens MJ, Nemeroff CB (1991). Physiology and pharmacology of corticotropin-releasing factor. Pharmacol Rev 43: 425-473.
46. Peñalva RG, Flachskamm C, Zimmermann S, Wurst W, Holsboer F, Reul JMHM et al (2002). Corticotropin-releasing hormone receptor type 1-deficiency enhances hippocampal serotonergic neurotransmission: an in vivo microdialysis study in mutant mice. Neuroscience 109: 253-266.
47. Porsolt RD, Bertin A, Jalfre M (1977a). Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 229: 327-336.
48. Porsolt RD, Le Pichon M, Jalfre M (1977b). Depression: a new animal model sensitive to antidepressant treatments. Nature 266: 730-732.
49. Price ML, Curtis AL, Kirby LG, Valentino RJ, Lucki I (1998). Effects of corticotropin-releasing factor on brain serotonergic activity. Neuropsychopharmacology 18: 492-502.
50. Price ML, Kirby LG, Valentino RJ, Lucki I (2002). Evidence for corticotropin-releasing factor regulation of serotonin in the lateral septum during acute swim stress: adaptation produced by repeated swimming. Psychopharmacology 162: 406-414.
51. Price ML, Lucki I (2001). Regulation of serotonin release in the lateral septum and striatum by corticotropin-releasing factor. J Neurosci 21: 2833-2841.
52. Raadsheer FC, Hoogendijk WJG, Stam FC, Tilders FJH, Swaab DF (1994). Increased numbers of corticotropin-releasing hormone expressing neurons in the hypothalamic paraventricular nucleus of depressed patients. Neuroendocrinology 60: 436-444.
53. Raadsheer FC, Van Heerikhuize JJ, Lucassen PJ, Hoogendijk WJG, Tilders FJH, Swaab DF (1995). Corticotropin-releasing hormone mRNA levels in the paraventricular nucleus of patients with Alzheimer's disease and depression. Am J Psychiatry 152: 1372-1376.
54. Ressler KJ, Nemeroff CB (2000). Role of serotonergic and noradrenergic systems in the pathophysiology of depression and anxiety disorders. Depression Anxiety 12: 2-19.
55. Reul JMHM, Holsboer F (2002). Corticotropin-releasing hormone receptors 1 and 2 in anxiety and depression. Curr Opin Pharmacol 2: 23-33.
56. Reul JMHM, Labeur MS, Grigoriadis DE, De Souza EB, Holsboer F (1994). Hypothalamic-pituitary-adrenocortical axis changes in the rat after long-term treatment with the reversible monoamine oxidase-A inhibitor moclobemide. Neuroendocrinology 60: 509-519.
57. Reul JMHM, Stec I, Söder M, Holsboer F (1993). Chronic treatment of rats with the antidepressant amitriptyline attenuates the activity of the hypothalamic-pituitary-adrenocortical system. Endocrinology 133: 312-320.
58. Roche M, Commons KG, Peoples A, Valentino RJ (2003). Circuitry underlying regulation of the serotonergic system by swim stress. J Neurosci 23: 970-977.
59. Rueter LE, Fornal CA, Jacobs BL (1997). A critical review of 5-HT brain microdialysis and behavior. Rev Neurosci 8: 117-137.
60. Rueter LE, Jacobs BL (1996). Changes in forebrain serotonin at the light-dark transition: correlation with behaviour. Neuroreport 7: 1107-1111.
61. Ruggiero DA, Underwood MD, Rice PM, Mann JJ, Arango V (1999). Corticotropic-releasing hormone and serotonin interact in the human brainstem: behavioral implications. Neuroscience 91: 1343-1354.
62. Sakanaka M, Shibasaki T, Lederis K (1987). Corticotropin releasing factor-like immunoreactivity in the rat brain as revealed by a modified cobalt-glucose oxidase-diaminobenzidine method. J Comp Neurol 260: 256-298.
63. Schulz DW, Mansbach RS, Sprouse J, Braselton JP, Collins J, Corman M et al (1996). CP-154,526: a potent and selective nonpeptide antagonist of corticotropin releasing factor receptors. Proc Natl Acad Sci USA 93: 10477-10482.
64. Singh VB, Corley KC, Phan TH, Boadle-Biber MC (1990). Increases in the activity of tryptophan hydroxylase from rat cortex and midbrain in response to acute or repeated sound stress are blocked by adrenalectomy and restored by dexamethasone treatment. Brain Res 516: 66-76.
65. Smith GW, Aubry JM, Dellu F, Contarino A, Bilezikjian LM, Gold LH et al (1998). Corticotropin releasing factor receptor 1-deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development. Neuron 20: 1093-1102.
66. Swanson LW, Sawchenko PE, Rivier J, Vale WW (1983). Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 36: 165-186.
67. Sze PY, Neckers L, Towle AC (1976). Glucocorticoids as a regulatory factor for brain tryptophan hydroxylase. J Neurochem 26: 169-173.
68. Timpl P, Spanagel R, Sillaber I, Kresse A, Reul JMHM, Stalla GK et al (1998). Impaired stress response and reduced anxiety in mice lacking a functional corticotropin-releasing hormone receptor 1. Nat Genet 19: 162-166.
69. Valentino RJ, Liouterman L, Van Bockstaele EJ (2001). Evidence for regional heterogeneity in corticotropin-releasing factor interactions in the dorsal raphe nucleus. J Comp Neurol 435: 450-463.
70. Van Pett K, Viau V, Bittencourt JC, Chan RKW, Li HY, Arias C et al (2000). Distribution of mRNAs encoding CRF receptors in brain and pituitary of bat and mouse. J Comp Neurol 428: 191-212.
71. Von Bardeleben U, Holsboer F (1989). Cortisol response to a combined dexamethasone-hCRH challenge in patients with depression. J Neuroendocrinol 1: 485-488.
72. Wong ML, Webster EL, Spokes H, Phu P, Ehrhart-Bornstein M, Bornstein S et al (1999). Chronic administration of the non-peptide CRH type 1 receptor antagonist antalarmin does not blunt hypothalamic-pituitary-adrenal axis responses to acute immobilization stress. Life Sci 65: L53-L58.
73. Wright IK, Upton N, Marsden CA (1992). Effect of established and putative anxiolytics on extracellular 5-HT and 5-HIAA in the ventral hippocampus of rats during behaviour on the elevated X-maze. Psychopharmacology 109: 338-346.
74. Zobel AW, Nickel T, Künzel HE, Ackl N, Sonntag A, Ising M et al (2000). Effects of the high-affinity corticotropin-releasing hormone receptor 1 antagonist R121919 in major depression: the first 20 patients treated. J Psychiatr Res 34: 171-181.