The effect of short-term stress on serotonin gene expression in high and low resilient macaques

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 44, Issue , 2013, Pages 143-153

  Bethea, Cynthia L ^a,b,c   Phu, Kenny ^a   Reddy, Arubala P ^a   Cameron, Judy L ^d  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

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

Author keywords

Amenorrhea; Macaques; Ovulation; Serotonin; Stress; Stress resilient

Indexed keywords

AUTORECEPTOR; DIGOXIGENIN; MESSENGER RNA; PROTEIN C FOS; SEROTONIN; SEROTONIN 1A RECEPTOR; SEROTONIN TRANSPORTER; TRYPTOPHAN HYDROXYLASE 2;

5HT1A GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL ACTIVATION; CELL COUNT; CONTROLLED STUDY; COPING BEHAVIOR; CRANIAL NERVE; DISEASE SEVERITY; DORSAL RAPHE NUCLEUS; FEMALE; FOLLICULAR PHASE; GENE; GENE EXPRESSION; IN SITU HYBRIDIZATION; MACACA; MENSTRUAL CYCLE; MENTAL STRESS; METABOLIC STRESS; NERVE FUNCTION; NEUROBIOLOGY; NONHUMAN; RNA PROBE; SENSITIVITY ANALYSIS; SEROTONINERGIC SYSTEM; SERT GENE; TPH2 GENE;

ANALYSIS OF VARIANCE; ANIMALS; DENSITOMETRY; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION; MACACA FASCICULARIS; MENSTRUAL CYCLE; PROTO-ONCOGENE PROTEINS C-FOS; RAPHE NUCLEI; RECEPTOR, SEROTONIN, 5-HT1A; RNA, MESSENGER; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; STRESS, PSYCHOLOGICAL; TRYPTOPHAN HYDROXYLASE;

EID: 84875273820     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2013.01.013     Document Type: Article

References (69)

1. Abumaria N., Rygula R., Hiemke C., Fuchs E., Havemann-Reinecke U., Ruther E., et al. Effect of chronic citalopram on serotonin-related and stress-regulated genes in the dorsal raphe nucleus of the rat. Eur Neuropsychopharmacol 2007, 17:417-429.
2. Adamec R., Toth M., Haller J., Halasz J., Blundell J. Activation patterns of cells in selected brain stem nuclei of more and less stress responsive rats in two animal models of PTSD - predator exposure and submersion stress. Neuropharmacology 2012, 62:725-736.
3. Adams J.H., Wigg K.G., King N., Burcescu I., Vetro A., Kiss E., et al. Association study of neurotrophic tyrosine kinase receptor type 2 (NTRK2) and childhood-onset mood disorders. Am J Med Genet B Neuropsychiatr Genet 2005, 132:90-95.
4. Alfonso J., Frasch A.C., Flugge G. Chronic stress, depression and antidepressants: effects on gene transcription in the hippocampus. Rev Neurosci 2005, 16:43-56.
5. Apparsundaram S., Sung U., Price R.D., Blakely R.D. Trafficking-dependent and -independent pathways of neurotransmitter transporter regulation differentially involving p38 mitogen-activated protein kinase revealed in studies of insulin modulation of norepinephrine transport in SK-N-SH cells. J Pharmacol Exp Ther 2001, 299(2):666-677.
6. Azmitia E.C., Gannon P.J. The primate serotonergic system: a review of human and animal studies and a report on Macaca fascicularis. Adv Neurol 1986, 43:407-468.
7. Berga S.L., Girton L.G. The psychoneuroendocrinology of functional hypothalamic amenorrhea. Psychiatr Clin North Am 1989, 12:105-116.
8. Berga S.L., Daniels T.L., Giles D.E. Women with functional hypothalamic amenorrhea but not other forms of anovulation display amplified cortisol concentrations. Fertil Steril 1997, 67:1024-1030.
9. Berga S.L., Marcus M.D., Loucks T.L., Hlastala S., Ringham R., Krohn M.A. Recovery of ovarian activity in women with functional hypothalamic amenorrhea who were treated with cognitive behavior therapy. Fertil Steril 2003, 80:976-981.
10. Berg-von der Emde K., Dees W.L., Hiney J.K., Hill D.F., Dissen G.A., Costa M.E., et al. Neurotrophins and the neuroendocrine brain: different neurotrophins sustain anatomically and functionally segregated subsets of hypothalamic dopaminergic neurons. J Neurosci 1995, 15:4223-4237.
11. Berod A., Hartman B.K., Pujol J.F. Importance of fixation in immunohistochemisty: use of formaldehyde solutions at variable pH for the localization of tyrosine hydroxylase. J Histochem Cytochem 1981, 29:844-850.
12. Berton O., Durand M., Aguerre S., Mormede P., Chaouloff F. Behavioral, neuroendocrine and serotonergic consequences of single social defeat and repeated fluoxetine pretreatment in the Lewis rat strain. Neuroscience 1999, 92:327-341.
13. Bethea C.L., Pau F.K., Fox S., Hess D.L., Berga S.L., Cameron J.L. Sensitivity to stress-induced reproductive dysfunction linked to activity of the serotonin system. Fertil Steril 2005, 83:148-155.
14. Bethea C.L., Streicher J.M., Mirkes S.J., Sanchez R.L., Reddy A.P., Cameron J.L. Serotonin-related gene expression in female monkeys with individual sensitivity to stress. Neuroscience 2005, 132:151-166.
15. Bethea C.L., Centeno M.L., Cameron J.L. Neurobiology of stress-induced reproductive dysfunction in female macaques. Mol Neurobiol 2008, 38:199-230.
16. Bethea C.L., Lima F.B., Centeno M.L., Weissheimer K.V., Senashova O., Reddy A.P., et al. Effects of citalopram on serotonin and CRF systems in the midbrain of primates with differences in stress sensitivity. J Chem Neuroanat 2011, 41:200-218.
17. Bethea C.L., Kim A., Cameron J.L. Function and innervation of the locus ceruleus in a macaque model of Functional Hypothalamic Amenorrhea. Neurobiol Dis 2012, 50:96-106.
18. Bethea C.L., Smith A.W., Centeno M.L., Reddy A.P. Long-term ovariectomy decreases serotonin neuron number and gene expression in free ranging macaques. Neuroscience 2012, 49:251-262.
19. Bhagwagar Z., Whale R., Cowen P.J. State and trait abnormalities in serotonin function in major depression. Br J Psychiatry 2002, 180:24-28.
20. Biller B.M.K., Federoff H.J., Koenig J.I., Klibanski A. Abnormal cortisol secretion and responses to corticotropin-releasing hormone in women with hypothalamic amenorrhea. J Clin Endocrinol Metab 1990, 70:311-317.
21. Botchin M.B., Kaplan J.R., Manuck S.B., Mann J.J. Neuroendocrine responses to fenfluramine challenge are influcenced by exposure to chronic social stress in adult male cynomolgus macaques. Psychoneuroendocrinology 1994, 19:1-11.
22. Briski K., Gillen E. Differential distribution of Fos expression within the male rat preoptic area and hypothalamus in response to physical vs. psychological stress. Brain Res Bull 2001, 55:401-408.
23. Browne C.A., Clarke G., Dinan T.G., Cryan J.F. Differential stress-induced alterations in tryptophan hydroxylase activity and serotonin turnover in two inbred mouse strains. Neuropharmacology 2011, 60:683-691.
24. Cameron J.L. Reproductive dysfunction in primates, behaviorally induced. Encyclopedia of stress 2000, 366-372. Academic Press, New York. G. Fink (Ed.).
25. Cameron J.L., Bridges M.W., Graham R.E., Bench L., Berga S.L., Matthews K. Basal heart rate predicts development of reproductive dysfunction in response to psychological stress. Annual Meeting of the Endocrine Society 1998, P1-P76. [abstract].
26. Cameron J.L., Bytheway J.A., Guay S., Bethea C.L., Kerr D.I., Rockcastle N., et al. Treatment with a serotonin reuptake inhibitor increases reproductive hormone secretion in stress sensitive monkeys. Annual Meeting of the Society for Neuroscience 2004, [abstract 192.18].
27. Drevets W.C., Frank E., Price J.C., Kupfer D.J., Holt D., Greer P.J., et al. PET imaging of serotonin 1A receptor binding in depression. Biol Psychiatry 1999, 46:1375-1387.
28. Filipenko M.L., Beilina A.G., Alekseyenko O.V., Dolgov V.V., Kudryavtseva N.N. Increase in expression of brain serotonin transporter and monoamine oxidase genes induced by repeated experience of social defeats in male mice. Biochemistry 2002, 67:451-455.
29. Gardner K.L., Hale M.W., Oldfield S., Lightman S.L., Plotsky P.M., Lowry C.A. Adverse experience during early life and adulthood interact to elevate TPH2 mRNA expression in serotonergic neurons within the dorsal raphe nucleus. Neuroscience 2009, 163:991-1001.
30. Giles D.E., Berga S.L. Cognitive and psychiatric correlates of functional hypothalamic amenorrhea: a controlled comparison. Fertil Steril 1993, 60:486-492.
31. Golovatscka V., Ennes H., Mayer E.A., Bradesi S. Chronic stress-induced changes in pro-inflammatory cytokines and spinal glia markers in the rat: a time course study. Neuroimmunomodulation 2012, 19:367-376.
32. Hendricks T., Francis N., Fyodorov D., 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 1999, 19:10348-10356.
33. Herod S.M., Dettmer A.M., Novak M.A., Meyer J.S., Cameron J.L. Sensitivity to stress-induced reproductive dysfunction is associated with a selective but not a generalized increase in activity of the adrenal axis. Am J Physiol Endocrinol Metab 2011, 300:E28-E36.
34. Herod S.M., Pohl C.R., Cameron J.L. Treatment with a CRH-R1 antagonist prevents stress-induced suppression of the central neural drive to the reproductive axis in female macaques. Am J Physiol Endocrinol Metab 2011, 300:E19-E27.
35. Jacobs B.L., Azmitia E.C. Structure and function of the brain serotonin system. Physiol Rev 1992, 72:165-231.
36. Kondoh Y., Uemura T., Murase M., Yokoi N., Ishikawa M., Hirahara F. A longitudinal study of disturbances of the hypothalamic-pituitary-adrenal axis in women with progestin-negative functional hypothalamic amenorrhea. Fertil Steril 2001, 76:748-752.
37. Laughlin G.A., Dominguez C.E., Yen S.S. Nutritional and endocrine-metabolic aberrations in women with functional hypothalamic amenorrhea. J Clin Endocrinol Metabol 1998, 83:25-32.
38. Lima F.B., Centeno M.L., Costa M.E., Reddy A.P., Cameron J.L., Bethea C.L. Stress sensitive female macaques have decreased fifth Ewing variant (Fev) and serotonin-related gene expression that is not reversed by citalopram. Neuroscience 2009, 164:676-691.
39. Lino-de-Oliveira C., Sales A.J., Del Bel E.A., Silveira M.C., Guimaraes F.S. Effects of acute and chronic fluoxetine treatments on restraint stress-induced Fos expression. Brain Res Bull 2001, 55:747-754.
40. Lira A., Zhou M., Castanon N., Ansorge M.S., Gordon J.A., Francis J.H., et al. Altered depression-related behaviors and functional changes in the dorsal raphe nucleus of serotonin transporter-deficient mice. Biol Psychiatry 2003, 54:960-971.
41. Maier S.F., Watkins L.R. Stressor controllability and learned helplessness: the roles of the dorsal raphe nucleus, serotonin, and corticotropin-releasing factor. Neurosci Biobehav Rev 2005, 29:829-841.
42. Malison R.T., Price L.H., Berman R., van Dyck C.H., Pelton G.H., Carpenter L., et al. Reduced brain serotonin transporter availability in major depression as measured by [123I]-2beta-carbomethoxy-3beta-(4-iodophenyl)tropane and single photon emission computed tomography. Biol Psychiatry 1998, 44:1090-1098.
43. Mann J.J., Malone K.M., Diehl D.J., Perel J., Cooper T.B., Mintun M.A. Demonstration in vivo of reduced serotonin responsivity in the brain of untreated depressed patients. Am J Psychiatry 1996, 153:174-182.
44. Martinez M., Phillips P.J., Herbert J. Adaptation in patterns of c-fos expression in the brain associated with exposure to either single or repeated social stress in male rats. Eur J Neurosci 1998, 10:20-33.
45. Meczekalski B., Tonetti A., Monteleone P., Bernardi F., Luisi S., Stomati M., et al. Hypothalamic amenorrhea with normal body weight: ACTH, allopregnanolone and cortisol responses to corticotropin-releasing hormone test. Eur J Endocrinol 2000, 142:280-285.
46. Mo B., Feng N., Renner K., Forster G. Restraint stress increases serotonin release in the central nucleus of the amygdala via activation of corticotropin-releasing factor receptors. Brain Res Bull 2008, 76:493-498.
47. Moses-Kolko E.L., Wisner K.L., Price J.C., Berga S.L., Drevets W.C., Hanusa B.H., et al. Serotonin 1A receptor reductions in postpartum depression: a positron emission tomography study. Fertil Steril 2008, 83:685-692.
48. Palkovits M., Brownstein M., Kizer J.S., Saavedra J.M., Kopin I.J. Effect of stress on serotonin concentration and tryptophan hydroxylase activity of brain nuclei. Neuroendocrinology 1976, 22:298-304.
49. Pare W.P., 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 1996, 31:112-121.
50. Parsey R.V., Hastings R.S., Oquendo M.A., Huang Y.Y., Simpson N., Arcement J., et al. Lower serotonin transporter binding potential in the human brain during major depressive episodes. Am J Psychiatry 2006, 163:52-58.
51. Perkins R.B., Hall J.E., Martin K.A. Aetiology, previous menstrual function and patterns of neuro-endocrine disturbance as prognostic indicators in hypothalamic amenorrhea. Hum Reprod 2001, 16:2198-2205.
52. Priyadarshini S., Aich P. Effects of psychological stress on innate immunity and metabolism in humans: a systematic analysis. PLoS One 2012, 7:e43232.
53. Ramamoorthy S., Blakely R.D. Phosphorylation and sequestration of serotonin transporters differentially modulated by psychostimulants. Science 1999, 285:763-766.
54. Ramamoorthy S., Giovanetti E., Qian Y., Blakely R.D. Phosphorylation and regulation of antidepressant-sensitive serotonin transporters. J Biol Chem 1998, 273:2458-2466.
55. Richardson-Jones J.W., Craige C.P., Guiard B.P., Stephen A., Metzger K.L., Kung H.F., et al. 5-HT1A autoreceptor levels determine vulnerability to stress and response to antidepressants. Neuron 2010, 65:40-52.
56. Sanchez R.L., Reddy A.P., Centeno M.L., Henderson J.A., 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 2005, 135:194-203.
57. Savitz J., Lucki I., Drevets W.C. 5-HT(1A) receptor function in major depressive disorder. Prog Neurobiol 2009, 88:17-31.
58. Shively C.A., Fontenot M.B., Kaplan J.R. Social status, behavior, and central serotonergic responsivity in female cynomolgus monkeys. Am J Primatol 1995, 37:333-339.
59. Short K. Uncontrollable social defeat, like inescapable shock, causes and anxiety increase and down-regulation of dorsal raphe serotonin 1A receptors with the same time course; both are prevented by a 5-HT1AR antagonist. Annual Meeting of the Society for Neuroscience 2003, [abstract 713.16].
60. Simmons D.M., Arriza J.L., 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 1989, 12:169-181.
61. Singh V.B., Corley K.C., Phan T.H., Boadle-Biber M.C. 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 1990, 516:66-76.
62. Tancer M.E., Mailman R.B., Stein M.F., Mason G.A., Carson S.W., Golden R.N. Neuroendocrine responsivity to monoaminergic system probes in generalized social phobia. Anxiety 1994, 1:216-223.
63. Van de Kar L. Neuroendocrine pharmacology of serotonergic (5HT) neurons. Annu Rev Pharmacol Toxicol 1991, 31:289-320.
64. Warren M.P., Fried J.L. Hypothalamic amenorrhea. The effects of environmental stresses on the reproductive system: a central effect of the central nervous system. Endocrinol Metab Clin North Am 2001, 30:611-629.
65. Warren M.P., Stiehl A.L. Exercise and female adolescents: effects on the reproductive and skeletal systems. J Am Med Womens Assoc 1999, 54:115-120. [38].
66. Watanabe Y., Sakai R.R., McEwen B.S., Mendelson S. Stress and antidepressant effects on hippocampal and cortical 5-HT1A and 5-HT2 receptors and transport sites for serotonin. Brain Res 1993, 615:87-94.
67. Williams N.I., Berga S.L., Cameron J.L. Mild metabolic stress potentiates the suppressive effect of psychological stress on reproductive function in female cynomolgus monkeys. Annual Meeting of the Endocrine Society 1997, [abstract PI-367].
68. Williams N.I., Helmreich D.L., Parfitt D.B., Caston-Balderrama A., Cameron J.L. Evidence for a causal role of low energy availability in the induction of menstrual cycle disturbances during strenuous exercise training. J Clin Endocrinol Metab 2001, 86:5184-5193.
69. Xiao E., Xia-Zhang L., 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 Metabol 1999, 84:623-626.