Stress sensitive female macaques have decreased fifth Ewing variant (Fev) and serotonin-related gene expression that is not reversed by citalopram

Neuroscience

Volumn 164, Issue 2, 2009, Pages 676-691

  Lima, F B ^a   Centeno, M L ^a   Costa, M E ^a   Reddy, A P ^a   Cameron, J L ^a,b,c   Bethea, C L ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

5HT1A autoreceptor; citalopram; Fev; serotonin; serotonin reuptake transporter; tryptophan hydroxylase

Indexed keywords

CARRIER PROTEIN; CITALOPRAM; DIGOXIGENIN; MESSENGER RNA; PARAFORMALDEHYDE; SEROTONIN; SEROTONIN 1A RECEPTOR; SEROTONIN REUPTAKE TRANSPORTER; STEROID; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FEV ETS; TRYPTOPHAN HYDROXYLASE 2; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN PERFUSION; CONTROLLED STUDY; DIETARY INTAKE; DORSAL RAPHE NUCLEUS; FEMALE; GENE EXPRESSION; IN SITU HYBRIDIZATION; ISOTOPE LABELING; MACACA; MENSTRUAL CYCLE; MENTAL STRESS; MESENCEPHALON; NERVE FUNCTION; NONHUMAN; OPTICAL DENSITY; OVULATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; RNA PROBE; SEQUENCE ALIGNMENT; SEROTONINERGIC NERVE; STEROID RELEASE;

ANIMALS; ANTIDEPRESSIVE AGENTS, SECOND-GENERATION; CITALOPRAM; FEMALE; GENE EXPRESSION; MACACA FASCICULARIS; PONS; PROTO-ONCOGENE PROTEINS C-ETS; RAPHE NUCLEI; RECEPTOR, SEROTONIN, 5-HT1A; RNA, MESSENGER; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SPECIES SPECIFICITY; STRESS, PSYCHOLOGICAL; TRYPTOPHAN HYDROXYLASE;

EID: 70349738104     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.08.010     Document Type: Article

References (79)

1. Alfonso J., Frasch A.C., and Flugge G. Chronic stress, depression and antidepressants: effects on gene transcription in the hippocampus. Rev Neurosci 16 (2005) 43-56
2. Alfonso J., Pollevick G.D., Van Der Hart M.G., Flugge G., Fuchs E., and Frasch A.C. Identification of genes regulated by chronic psychosocial stress and antidepressant treatment in the hippocampus. Eur J Neurosci 19 (2004) 659-666
3. Arango V., Underwood M.D., and Mann J.J. Serotonin brain circuits involved in major depression and suicide. Prog Brain Res 136 (2002) 443-453
4. Artigas F., Perez V., and Alvarez E. Pindolol induces a rapid improvement of depressed patients treated with serotonin reuptake inhibitors. Arch Gen Psychiatry 51 (1994) 248-251
5. Asan E., Yilmazer-Hanke D.M., Eliava M., Hantsch M., Lesch K.P., and Schmitt A. The corticotropin-releasing factor (CRF)-system and monoaminergic afferents in the central amygdala: investigations in different mouse strains and comparison with the rat. Neuroscience 131 (2005) 953-967
6. Bassett J.L., and Foote S.L. Distribution of corticotropin-releasing factor-like immunoreactivity in squirrel monkey (Saimiri sciureus) amygdala. J Comp Neurol 323 (1992) 91-102
7. Berga S.L., and Girton L.G. The psychoneuroendocrinology of functional hypothalamic amenorrhea. Psychiatr Clin North Am 12 (1989) 105-116
8. Berga S.L., and Loucks T.L. Use of cognitive behavior therapy for functional hypothalamic amenorrhea. Ann N Y Acad Sci 1092 (2006) 114-129
9. Berga S.L., Marcus M.D., Loucks T.L., Hlastala S., Ringham R., and Krohn M.A. Recovery of ovarian activity in women with functional hypothalamic amenorrhea who were treated with cognitive behavior therapy. Fertil Steril 80 (2003) 976-981
10. Berg-von der Emde K., Dees W.L., Hiney J.K., Hill D.F., Dissen G.A., Costa M.E., Moholt-Siebert M., and Ojeda S.R. Neurotrophins and the neuroendocrine brain: different neurotrophins sustain anatomically and functionally segregated subsets of hypothalamic dopaminergic neurons. J Neurosci 15 (1995) 4223-4237
11. Berod A., Hartman B.K., and Pujol J.F. Importance of fixation in immunohistochemisty: use of formaldehyde solutions at variable pH for the localization of tyrosine hydroxylase. J Histochem Cytochem 29 (1981) 844-850
12. Bethea C.L., Centeno M.L., and Cameron J.L. Neurobiology of stress-induced reproductive dysfunction in female macaques. Mol Neurobiol 38 (2008) 199-230
13. Bethea C.L., Pau F.K., Fox S., Hess D.L., Berga S.L., and Cameron J.L. Sensitivity to stress-induced reproductive dysfunction linked to activity of the serotonin system. Fertil Steril 83 (2005) 148-155
14. Bethea C.L., Reddy A.P., Pedersen D., and Tokuyama Y. Expression profile of differentiating serotonin neurons derived from rhesus embryonic stem cells and comparison to adult serotonin neurons. Gene Expr Patterns 9 (2009) 94-108
15. Bethea C.L., Streicher J.M., Coleman K., Pau F.K., Moessner R., and Cameron J.L. Anxious behavior and fenfluramine-induced prolactin secretion in young rhesus macaques with different alleles of the serotonin reuptake transporter polymorphism (5HTTLPR). Behav Genet 34 (2004) 295-307
16. Bethea C.L., Streicher J.M., Mirkes S.J., Sanchez R.L., Reddy A.P., and Cameron J.L. Serotonin-related gene expression in female monkeys with individual sensitivity to stress. Neuroscience 132 (2005) 151-166
17. Biederman J., Rosenbaum J.F., Hirshfeld D.R., Faraone S.V., Bolduc E.A., Gersten M., Meminger S.R., Kagan J., Snidman N., and Reznick J.S. Psychiatric correlates of behavioral inhibition in young children of parents with and without psychiatric disorders. Arch Gen Psychiatry 47 (1990) 21-26
18. Bondy B., Erfurth A., De Jonge S., Kruger M., and Meyer H. Possible association of the short allele of the serotonin transporter promoter gene polymorphism (5-HTTLPR) with violent suicide. Mol Psychiatry 5 (2000) 193-195
19. Cameron J.L. Reproductive dysfunction in primates, behaviorally induced. In: Fink G. (Ed). Encyclopedia of stress (2000), Academic Press, New York 366-372
20. Cameron J.L. Stress and reproduction. In: Henry H.L., and Norman A.W. (Eds). The encyclopedia of hormones (2003), Elsevier Science, New York 433-438
21. Cameron J.L., Bytheway J.A., Guay S., Bethea C.L., Kerr D.I., Rockcastle N., Perel J.M., and Axelson D.A. Treatment with a serotonin reuptake inhibitor increases reproductive hormone secretion in stress sensitive monkeys. Program No. 192.18. San Diego, CA: 34th Annual Meeting of the Society for Neuroscience, October 23-27 (2004)
22. Centeno M.L., Sanchez R.L., Cameron J.L., and Bethea C.L. Hypothalamic expression of serotonin 1A, 2A and 2C receptors and GAD67 in female cynomolgus monkeys with different sensitivity to stress. Brain Res 1142 (2007) 1-12
23. Centeno M.L., Sanchez R.L., Cameron J.L., and Bethea C.L. Hypothalamic gonadotrophin-releasing hormone expression in female monkeys with different sensitivity to stress. J Neuroendocrinol 19 (2007) 594-604
24. Centeno M.L., Sanchez R.L., Reddy A.P., Cameron J.L., and Bethea C.L. Corticotropin-releasing hormone and pro-opiomelanocortin gene expression in female monkeys with differences in sensitivity to stress. Neuroendocrinology 86 (2007) 277-288
25. Clark M.S., McDevitt R.A., Hoplight B.J., and Neumaier J.F. Chronic low dose ovine corticotropin releasing factor or urocortin II into the rostral dorsal raphe alters exploratory behavior and serotonergic gene expression in specific subregions of the dorsal raphe. Neuroscience 146 (2007) 1888-1905
26. Conti B., Maier R., Barr A.M., Morale M.C., Lu X., Sanna P.P., Bilbe G., Hoyer D., and Bartfai T. Region-specific transcriptional changes following the three antidepressant treatments electro convulsive therapy, sleep deprivation and fluoxetine. Mol Psychiatry 12 (2007) 167-189
27. Drevets W.C., Frank E., Price J.C., Kupfer D.J., Greer P.J., and Mathis C. Serotonin type-1A receptor imaging in depression. Nucl Med Biol 27 (2000) 499-507
28. Drevets W.C., Videen T.O., Price J.L., Preskorn S.H., Carmichael S.T., and Raichle M.E. A functional anatomical study of unipolar depression. J Neurosci 12 (1992) 3628-3641
29. Ferin M. Neuropeptides, the stress response, and the hypothalamo-pituitary-gonadal axis in the female rhesus monkey. Ann N Y Acad Sci 697 (1993) 106-116
30. Ferin M. The antireproductive role of corticotropin releasing hormone and interleukin-1 in the female rhesus monkey. Ann Endocrinol (Paris) 56 (1995) 181-186
31. Fioroni L., Fava M., Genazzani A.D., Facchinetti F., and Genazzani A.R. Life events impact in patients with secondary amenorrhoea. J Psychosom Res 38 (1994) 617-622
32. Flugge G., Kramer M., Rensing S., and Fuchs E. 5HT1A-receptors and behaviour under chronic stress: selective counteraction by testosterone. Eur J Neurosci 10 (1998) 2685-2693
33. Fox N.A. Temperament and early experience form social behavior. Ann N Y Acad Sci 1038 (2004) 171-178
34. Giles D.E., and Berga S.L. Cognitive and psychiatric correlates of functional hypothalamic amenorrhea: a controlled comparison. Fertil Steril 60 (1993) 486-492
35. Hasler G., Drevets W.C., Manji H.K., and Charney D.S. Discovering endophenotypes for major depression. Neuropsychopharmacology 29 (2004) 1765-1781
36. Hendricks T., Francis N., Fyodorov D., and Deneris E.S. The ETS domain factor Pet-1 is an early and precise marker of central serotonin neurons and interacts with a conserved element in serotonergic genes. J Neurosci 19 (1999) 10348-10356
37. Hendricks T.J., Fyodorov D.V., Wegman L.J., Lelutiu N.B., Pehek E.A., Yamamoto B., Silver J., Weeber E.J., Sweatt J.D., and Deneris E.S. Pet-1 ETS gene plays a critical role in 5-HT neuron development and is required for normal anxiety-like and aggressive behavior. Neuron 37 (2003) 233-247
38. Herod S.M., Bytheway J., Dolney R., and Cameron J.L. Female monkeys who are sensitive to stress-induced reproductive dysfunction show increases in certain forms of anxious behavior. Program No. 257.22. Atlanta, GA: 36th Annual Meeting of the Society for Neuroscience, October 14, 18 (2006)
39. Hirshfeld D.R., Rosenbaum J.F., Biederman J., Bolduc E.A., Faraone S.V., Snidman N., Reznick J.S., and Kagan J. Stable behavioral inhibition and its association with anxiety disorder. J Am Acad Child Adolesc Psychiatry 31 (1992) 103-111
40. Hjorth S., Bengtsson H.J., Kullberg A., Carlzon D., Peilot H., and Auerbach S.B. Serotonin autoreceptor function and antidepressant drug action. J Psychopharmacol 14 (2000) 177-185
41. Hrdina P.D., Demeter E., Vu T.B., Sotonyi P., and Palkovits M. 5-HT uptake sites and 5-HT2 receptors in brain of antidepressant-free suicide victims/depressives: increase in 5-HT2 sites in cortex and amygdala. Brain Res 614 (1993) 37-44
42. Julius D. Molecular biology of serotonin receptors. Annu Rev Neurosci 14 (1991) 335-360
43. Kalin N.H., and Shelton S.E. Nonhuman primate models to study anxiety, emotion regulation, and psychopathology. Ann N Y Acad Sci 1008 (2003) 189-200
44. Kelly J.P., Wrynn A.S., and Leonard B.E. The olfactory bulbectomized rat as a model of depression: an update. Pharmacol Ther 74 (1997) 299-316
45. Kirby L.G., Rice K.C., and Valentino R.J. Effects of corticotropin-releasing factor on neuronal activity in the serotonergic dorsal raphe nucleus. Neuropsychopharmacology 22 (2000) 148-162
46. Laflamme N., Feuvrier E., Richard D., and Rivest S. Involvement of serotonergic pathways in mediating the neuronal activity and genetic transcription of neuroendocrine corticotropin-releasing factor in the brain of systemically endotoxin-challenged rats. Neuroscience 88 (1999) 223-240
47. Laughlin G.A., Dominguez C.E., and Yen S.S. Nutritional and endocrine-metabolic aberrations in women with functional hypothalamic amenorrhea. J Clin Endocrinol Metab 83 (1998) 25-32
48. Lawrence K.M., De Paermentier F., Cheetham S.C., Crompton M.R., Katona C.L., and Horton R.W. Brain 5-HT uptake sites, labelled with [3H]paroxetine, in antidepressant-free depressed suicides. Brain Res 526 (1990) 17-22
49. Lindenmayer J.P. The pathophysiology of agitation. J Clin Psychiatry 61 Suppl 14 (2000) 5-10
50. Lu N.Z., and Bethea C.L. Ovarian steroid regulation of 5HT1A receptor binding and G protein activation in female monkeys. Neuropsychopharmacology 27 (2002) 12-24
51. Manji H.K., Quiroz J.A., Sporn J., Payne J.L., Denicoff K., Gray A.N., Zarate Jr. C.A., and Charney D.S. Enhancing neuronal plasticity and cellular resilience to develop novel, improved therapeutics for difficult-to-treat depression. Biol Psychiatry 53 (2003) 707-742
52. Marcus M.D., Loucks T.L., and Berga S.L. Psychological correlates of functional hypothalamic amenorrhea. Fertil Steril 76 (2001) 310-316
53. McEwen B.S. The end of stress as we know it (2002), Joseph Henry Press, Washington, DC
54. Myers K.M., and Davis M. Mechanisms of fear extinction. Mol Psychiatry 12 (2007) 120-150
55. Pare W.P., and Tejani-Butt S.M. Effect of stress on the behavior and 5-HT system in Sprague-Dawley and Wistar Kyoto rat strains. Integr Physiol Behav Sci 31 (1996) 112-121
56. Pecins-Thompson M., and Bethea C.L. Ovarian steroid regulation of 5HT1A autoreceptor messenger ribonucleic acid expression in the dorsal raphe of rhesus macaques. Neuroscience 89 (1998) 267-277
57. Pecins-Thompson M., Brown N.A., and Bethea C.L. Regulation of serotonin re-uptake transporter mRNA expression by ovarian steroids in rhesus macaques. Mol Brain Res 53 (1998) 120-129
58. Polkowska J., and Przekop F. The effect of corticotropin-releasing factor (CRF) on the gonadotropin hormone releasing hormone (GnRH) hypothalamic neuronal system during preovulatory period in the ewe. Acta Neurobiol Exp (Wars) 57 (1997) 91-99
59. Reifenstein Jr. E.C. Psychogenic or "hypothalamic" amenorrhea. Med Clin North Am 30 (1946) 1103-1114
60. Reindollar R.H., Novak M., Tho S.P., and McDonough P.G. Adult-onset amenorrhea: a study of 262 patients. Am J Obstet Gynecol 155 (1986) 531-543
61. Romero L., and Artigas F. Preferential potentiation of the effects of serotonin uptake inhibitors by 5HT1A receptor antagonists in the dorsal raphe pathway: role of somatodendritic autoreceptors. J Neurochem 68 (1997) 2593-2603
62. Ruggiero D.A., Underwood M.D., Rice P.M., Mann J.J., and Arango V. Corticotropic-releasing hormone and serotonin interact in the human brainstem: behavioral implications. Neuroscience 91 (1999) 1343-1354
63. Sanchez R.L., Reddy A.P., Centeno M.L., Henderson J.A., and Bethea C.L. A second tryptophan hydroxylase isoform, TPH-2 mRNA, is increased by ovarian steroids in the raphe region of macaques. Brain Res Mol Brain Res 135 (2005) 194-203
64. Schulkin J., Gold P.W., and McEwen B.S. Induction of corticotropin-releasing hormone gene expression by glucocorticoids: implication for understanding the states of fear and anxiety and allostatic load. Psychoneuroendocrinology 23 (1998) 219-243
65. Shishkina G.T., Kalinina T.S., and Dygalo N.N. Up-regulation of tryptophan hydroxylase-2 mRNA in the rat brain by chronic fluoxetine treatment correlates with its antidepressant effect. Neuroscience 150 (2007) 404-412
66. Shroff H., Reba L., Thornton L.M., Tozzi F., Klump K.L., Berrettini W.H., Brandt H., Crawford S., Crow S., Fichter M.M., Goldman D., Halmi K.A., Johnson C., Kaplan A.S., Keel P., LaVia M., Mitchell J., Rotondo A., Strober M., Treasure J., Woodside D.B., Kaye W.H., and Bulik C.M. Features associated with excessive exercise in women with eating disorders. Int J Eat Disord 39 (2006) 454-461
67. Simmons D.M., Arriza J.L., and Swanson L.W. A complete protocol for in situ hybridization of messenger RNAs in brain and other tissues with radio-labeled single-stranded RNA probes. J Histotechnol 12 (1989) 169-181
68. Singh A., and Lucki I. Antidepressant-like activity of compounds with varying efficacy at 5HT1A receptors. Neuropharmacology 32 (1993) 331-340
69. Sit D.K., Perel J.M., Helsel J.C., and Wisner K.L. Changes in antidepressant metabolism and dosing across pregnancy and early postpartum. J Clin Psychiatry 69 (2008) 652-658
70. Smith T.D., Kuczenski R., George-Griedman K., Malley J.D., and Foote S.L. In vivo microdialysis assessment of extracellular serotonin and dopamine levels in awake monkeys during sustained fluoxetine administration. Synapse 38 (2000) 460-470
71. Spurlock G., Buckland P., O'Donovan M., and McGuffin P. Lack of effect of antidepressant drugs on the levels of mRNAs encoding serotonergic receptors, synthetic enzymes and 5HT transporter. Neuropharmacology 33 (1994) 433-440
72. Strekalova T., Spanagel R., Dolgov O., and Bartsch D. Stress-induced hyperlocomotion as a confounding factor in anxiety and depression models in mice. Behav Pharmacol 16 (2005) 171-180
73. Turner C.A., Akil H., Watson S.J., and Evans S.J. The fibroblast growth factor system and mood disorders. Biol Psychiatry 59 (2006) 1128-1135
74. Wang R., and Millam J.R. Corticotropin-releasing hormone-immunopositive nerve elements in apposition to chicken gonadotropin-releasing hormone I-containing perikarya in Japanese quail (Coturnix coturnix japonica) brain. Cell Tissue Res 297 (1999) 223-228
75. Watanabe Y., Sakai R.R., McEwen B.S., and Mendelson S. Stress and antidepressant effects on hippocampal and cortical 5-HT1A and 5-HT2 receptors and transport sites for serotonin. Brain Res 615 (1993) 87-94
76. Williams N.I., Berga S.L., and Cameron J.L. Mild metabolic stress potentiates the suppressive effect of psychological stress on reproductive function in female cynomolgus monkeys. Abstract PI-367. Minneapolis, MN: 79th Annual Meeting of the Endocrine Society, June 11-14 (1997)
77. Williams N.I., Berga S.L., and Cameron J.L. Synergism between psychosocial and metabolic stressors: impact on reproductive function in cynomolgus monkeys. Am J Physiol Endocrinol Metab 293 (2007) E270-E276
78. Xiao E., Xia-Zhang L., and Ferin M. Stress and the menstrual cycle: short- and long-term response to a five-day endotoxin challenge during the luteal phase in the rhesus monkey. J Clin Endocrinol Metab 84 (1999) 623-626
79. Yatham L.N. Is 5HT1A receptor subsensitivity a trait marker for late luteal phase dysphoric disorder?. A pilot study. Can J Psychiatry 38 (1993) 662-664