Development×environment interactions control tph2 mRNA expression

Neuroscience

Volumn 237, Issue , 2013, Pages 139-150

  Lukkes, J L ^a,b   Kopelman, J M ^a   Donner, N C ^a   Hale, M W ^a,c   Lowry, C A ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c LA TROBE UNIVERSITY   (Australia)

Author keywords

Dorsal raphe nucleus; FG 7142; Htr1a; In situ hybridization histochemistry; Isolation rearing; Tph2

Indexed keywords

MESSENGER RNA; N METHYL BETA CARBOLINE 3 CARBOXAMIDE; PROTEIN C FOS;

ADOLESCENT; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; AROUSAL; ARTICLE; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; DRINKING BEHAVIOR; ENVIRONMENTAL FACTOR; FEMALE; GENE; GENE EXPRESSION REGULATION; GENE INTERACTION; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; GROOMING; HTR1A GENE; IN SITU HYBRIDIZATION; LOCOMOTION; MENTAL DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; REARING; RISK FACTOR; SEROTONINERGIC NERVE CELL; SEROTONINERGIC SYSTEM; SLC6A4 GENE; SOCIAL BEHAVIOR; SOCIAL ISOLATION; STRESS; TPH2 GENE; TRANQUILIZING ACTIVITY;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BRAIN; CARBOLINES; DEOXYADENINE NUCLEOTIDES; FEMALE; GABA ANTAGONISTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; RADIOGRAPHY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, SEROTONIN, 5-HT1A; RNA, MESSENGER; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SOCIAL ISOLATION; TRYPTOPHAN HYDROXYLASE;

EID: 84874762775     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.01.070     Document Type: Article

References (80)

1. Abrams J.K., Johnson P.L., Hollis J.H., Lowry C.A. Anatomical and functional topography of the dorsal raphe nucleus. Ann N Y Acad Sci 2004, 1018:46-57.
2. Abrams J.K., Johnson P.L., Hay-Schmidt A., Mikkelsen J.D., Shekhar A., Lowry C.A. Serotonergic systems associated with arousal and vigilance behaviors following administration of anxiogenic drugs. Neuroscience 2005, 133:983-997.
3. Andersen S.L. Trajectories of brain development: point of vulnerability or window of opportunity?. Neurosci Biobehav Rev 2003, 27:3-18.
4. Arakawa H. Ontogeny of sex differences in defensive burying behavior in rats: effect of social isolation. Aggress Behav 2007, 33:38-47.
5. Bach-Mizrachi H., Underwood M.D., Kassir S.A., Bakalian M.J., Sibille E., Tamir H., Mann J.J., Arango V. Neuronal tryptophan hydroxylase mRNA expression in the human dorsal and median raphe nuclei: major depression and suicide. Neuropsychopharmacology 2006, 31:814-824.
6. Bach-Mizrachi H., Underwood M.D., Tin A., Ellis S.P., Mann J.J., Arango V. Elevated expression of tryptophan hydroxylase-2 mRNA at the neuronal level in the dorsal and median raphe nuclei of depressed suicides. Mol Psychiatry 2008, 13:507-513.
7. Battaglia M., Bertella S., Politi E., Bernardeschi L., Perna G., Gabriele A., Bellodi L. Age at onset of panic disorder: influence of familial liability to the disease and of childhood separation anxiety disorder. Am J Psychiatry 1995, 152:1362-1364.
8. Blakely R.D., Berson H.E., Fremeau R.T., Caron M.G., Peek M.M., Prince H.K., Bradley C.C. Cloning and expression of a functional serotonin transporter from rat brain. Nature 1991, 354:66-70.
9. Boldrini M., Underwood M.D., Mann J.J., Arango V. More tryptophan hydroxylase in the brainstem dorsal raphe nucleus in depressed suicides. Brain Res 2005, 1041:19-28.
10. Bonkale W.L., Turecki G., Austin M.C. Increased tryptophan hydroxylase immunoreactivity in the dorsal raphe nucleus of alcohol-dependent, depressed suicide subjects is restricted to the dorsal subnucleus. Synapse 2006, 60:81-85.
11. Bueno C.H., Zangrossi H., Nogueira R.L., Soares V.P., Viana M.B. Panicolytic-like effect induced by the stimulation of GABAA and GABAB receptors in the dorsal periaqueductal grey of rats. Eur J Pharmacol 2005, 516:239-246.
12. Bueno C.H., Zangrossi H., Viana M.B. The inactivation of the basolateral nucleus of the rat amygdala has an anxiolytic effect in the elevated T-maze and light/dark transition tests. Braz J Med Biol Res 2005, 38:1697-1701.
13. Bueno C.H., Zangrossi H., Viana M.B. GABA/benzodiazepine receptors in the ventromedial hypothalamic nucleus regulate both anxiety and panic-related defensive responses in the elevated T-maze. Brain Res Bull 2007, 74:134-141.
14. 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. Neuroscience 1990, 10:176-183.
15. Campos S.B., Miranda D.M., Souza B.R., Pereira P.A., Neves F.S., Tramontina J., Kapczinski F., Romano-Silva M.A., Correa H. Association study of tryptophan hydroxylase 2 gene polymorphisms in bipolar disorder patients with panic disorder comorbidity. Psychiatr Genet 2011, 21:106-111.
16. Caspi A., Sugden K., Moffitt T.E., Taylor A., Craig I.W., Harrington H., McClay J., Mill J., Martin J., Braithwaite A., Poulton R. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 2003, 301:386-389.
17. D'Amato F.R., Zanettini C., Lampis V., Coccurello R., Pascucci T., Ventura R., Puglisi-Allegra S., Spatola C.A., Pesenti-Gritti P., Oddi D., Moles A., Battaglia M. Unstable maternal environment, separation anxiety, and heightened CO2 sensitivity induced by gene-by-environment interplay. PLoS ONE 2011, 6:e18637.
18. Deakin J.F.W., Graeff F.G. 5-HT and mechanisms of defence. J Psychopharmacol 1991, 5:305-315.
19. Donner N., Handa R.J. Estrogen receptor beta regulates the expression of tryptophan-hydroxylase 2 mRNA within serotonergic neurons of the rat dorsal raphe nuclei. Neuroscience 2009, 163:705-718.
20. Donner N.C., Johnson P.L., Fitz S.D., Kellen K.E., Shekhar A., Lowry C.A. Elevated tph2 mRNA expression in a rat model of chronic anxiety. Depress Anxiety 2012, 29:307-319.
21. Dumont F.S., Biancardi V., Kinkead R. Hypercapnic ventilatory response of anesthetized female rats subjected to neonatal maternal separation: insight into the origins of panic attacks?. Respir Physiol Neurobiol 2011, 175:288-295.
22. Evans A.K., Lowry C.A. Pharmacology of the beta-carboline FG-7,142, a partial inverse agonist at the benzodiazepine allosteric site of the GABA A receptor: neurochemical, neurophysiological, and behavioral effects. CNS Drug Rev 2007, 13:475-501.
23. Evans A.K., Abrams J.K., Bouwknecht J.A., Knight D.M., Shekhar A., Lowry C.A. The anxiogenic drug FG-7142 increases serotonin metabolism in the rat medial prefrontal cortex. Pharmacol Biochem Behav 2006, 84:266-274.
24. Fujita M., Shimada S., Maeno H., Nishimura T., Tohyama M. Cellular localization of serotonin transporter mRNA in the rat brain. Neurosci Lett 1993, 162:59-62.
25. Gardner K.L., Thrivikraman K.V., Lightman S.L., Plotsky P.M., Lowry C.A. Early life experience alters behavior during social defeat: focus on serotonergic systems. Neuroscience 2005, 136:181-191.
26. Gardner K.L., Hale M.W., Lightman S.L., Plotsky P.M., Lowry C.A. Adverse early life experience and social stress during adulthood interact to increase serotonin transporter mRNA expression. Brain Res 2009, 1305:47-63.
27. Gardner K.L., Hale M.W., Oldfield S., Lightman S.L., Plotsky P., Lowry C.A. Adverse experience during early life and adulthood ineract to elevate tph2 mRNA expression in serotonergic neurons within the dorsal raphe nucleus. Neuroscience 2009, 163:991-1001.
28. Genest S.E., Balon N., Laforest S., Drolet G., Kinkead R. Neonatal maternal separation and enhancement of the hypoxic ventilatory response in rat: the role of GABAergic modulation within the paraventricular nucleus of the hypothalamus. J Physiol 2007, 583:299-314.
29. Graeff F.G. Neurotransmitters in the dorsal periaqueductal gray and animal models of panic anxiety. New concepts in anxiety 1991, 288-312. MacMillan Press, London. M. Briley, S.E. File (Eds.).
30. Graeff F.G. Serotonin, the periaqueductal gray and panic. Neurosci Biobehav Rev 2004, 28:239-259.
31. Graeff F.G., Guimaraes F.S., De Andrade T.G., Deakin J.F. Role of 5-HT in stress, anxiety, and depression. Pharmacol Biochem Behav 1996, 54:129-141.
32. Grubbs F.E. Procedures for detecting outlying observations in samples. Technometrics 1969, 11:1-21.
33. Hale M.W., Lowry C.A. Functional topography of midbrain and pontine serotonergic systems: implications for synaptic regulation of serotonergic circuits. Psychopharmacology (Berl) 2011, 213:243-264.
34. Hale M.W., Shekhar A., Lowry C.A. Development by environment interactions controlling tryptophan hydroxylase expression. J Chem Neuroanat 2011, 41:219-226.
35. Hale M.W., Shekhar A., Lowry C.A. Stress-related serotonergic systems: implications for symptomatology of anxiety and affective disorders. Cell Mol Neurobiol 2012, 32:695-708.
36. Hansen H.H., Mikkelsen J.D. Long-term effects on serotonin transporter mRNA expression of chronic neonatal exposure to a serotonin reuptake inhibitor. Eur J Pharmacol 1998, 352:307-315.
37. Harbuz M.S., Lightman S.L. Responses of hypothalamic and pituitary mRNA to physical and psychological stress in the rat. J Endocrinol 1989, 122:705-711.
38. Hariri A.R., Holmes A. Genetics of emotional regulation: the role of the serotonin transporter in neural function. Trends Cogn Sci 2006, 10:182-191.
39. Hoefgen B., Schulze T.G., Ohlraun S., von W.O., Hofels S., Gross M., Heidmann V., Kovalenko S., Eckermann A., Kolsch H., Metten M., Zobel A., Becker T., Nothen M.M., Propping P., Heun R., Maier W., Rietschel M. The power of sample size and homogenous sampling: association between the 5-HTTLPR serotonin transporter polymorphism and major depressive disorder. Biol Psychiatry 2005, 57:247-251.
40. Jenck F., Moreau J.L., Martin J.R. Dorsal periaqueductal gray-induced aversion as a simulation of panic anxiety: elements of face and predictive validity. Psychiatry Res 1995, 57:181-191.
41. Johnson P.L., Lightman S.L., Lowry C.A. A functional subset of serotonergic neurons in the rat ventrolateral periaqueductal gray implicated in the inhibition of sympathoexcitation and panic. Ann N Y Acad Sci 2004, 1018:58-64.
42. Johnson P.L., Hollis J.H., Moratalla R., Lightman S.L., Lowry C.A. Acute hypercarbic gas exposure reveals functionally distinct subpopulations of serotonergic neurons in rats. J Psychopharmacol 2005, 19:327-341.
43. Johnson P.L., Truitt W.A., Fitz S.D., Lowry C.A., Shekhar A. Neural pathways underlying lactate-induced panic. Neuropsychopharmacology 2007, 33:2093-2107.
44. Johnson P.L., Lowry C.A., Truitt W., Shekhar A. Disruption of GABAergic tone in the dorsomedial hypothalamus attenuates responses in a subset of serotonergic neurons in the dorsal raphe nucleus following lactate-induced panic. J Psychopharmacol 2008, 22:642-645.
45. Johnson P.L., Fitz S.D., Hollis J.H., Moratalla R., Lightman S.L., Shekhar A., Lowry C.A. Induction of c-Fos in 'panic/defence'-related brain circuits following brief hypercarbic gas exposure. J Psychopharmacol 2011, 25:26-36.
46. Kim Y.K., Lee H.J., Yang J.C., Hwang J.A., Yoon H.K. A tryptophan hydroxylase 2 gene polymorphism is associated with panic disorder. Behav Genet 2009, 39:170-175.
47. Kirby L.G., Pernar L., Valentino R.J., Beck S.G. Distinguishing characteristics of serotonin and nonserotonin-containing cells in the dorsal raphe nucleus: electrophysiological and immunohistochemical studies. Neuroscience 2003, 116:669-683.
48. Klein R.G. Is panic disorder associated with childhood separation anxiety disorder?. Clin Neuropharmacol 1995, 18(suppl 2):S7-S14.
49. Lesch K.P., Gutknecht L. Focus on the 5-HT1A receptor: emerging role of a gene regulatory variant in psychopathology and pharmacogenetics. Int J Neuropsychopharmacol 2004, 7:381-385.
50. Lesch K.P., Bengel D., Heils A., Sabol S.Z., Greenberg B.D., Petri S., Benjamin J., Muller C.R., Hamer D.H., Murphy D.L. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 1996, 274:1527-1531.
51. Leussis M.P., Andersen S.L. Is adolescence a sensitive period for depression? Behavioral and neuroanatomical findings from a social stress model. Synapse 2008, 62:22-30.
52. Lowry C.A., Hale M.W., Evans A.K., Heerkens J., Staub D.R., Gasser P.J., Shekhar A. Serotonergic systems, anxiety, and affective disorder: focus on the dorsomedial part of the dorsal raphe nucleus. Ann N Y Acad Sci 2008, 1148:86-94.
53. Lowry C.A., Johnson P.L., Hay-Schmidt A., Mikkelsen J., Shekhar A. Modulation of anxiety circuits by serotonergic systems. Stress 2005, 8:233-246.
54. Lukkes J., Vuong S., Scholl J., Oliver H., Forster G. Corticotropin-releasing factor receptor antagonism within the dorsal raphe nucleus reduces social anxiety-like behavior after early-life social isolation. J Neurosci 2009, 29:9955-9960.
55. Lukkes J.L., Mokin M.V., Scholl J.L., Forster G.L. Adult rats exposed to early-life social isolation exhibit increased anxiety and conditioned fear behavior, and altered hormonal stress responses. Horm Behav 2009, 55:248-256.
56. Lukkes J.L., Watt M.J., Lowry C.A., Forster G.L. Consequences of post-weaning social isolation on anxiety behavior and related neural circuits in rodents. Front Behav Neurosci 2009, 3:18.
57. Lukkes J.L., Burke A.R., Zelin N.S., Hale M.W., Lowry C.A. Post-weaning social isolation attenuates c-Fos expression in GABAergic interneurons in the basolateral amygdala of adult female rats. Physiol Behav 2012, 107:719-725.
58. Lukkes J.L., Engelman G.H., Zelin N.S., Hale M.W., Lowry C.A. Post-weaning social isolation of female rats, anxiety-related behavior, and serotonergic systems. Brain Res 2012, 1443:1-17.
59. 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.
60. Maron E., Toru I., Must A., Tasa G., Toover E., Vasar V., Lang A., Shlik J. Association study of tryptophan hydroxylase 2 gene polymorphisms in panic disorder. Neurosci Lett 2007, 411:180-184.
61. Maron E., Toru I., Tasa G., Must A., Toover E., Lang A., Vasar V., Shlik J. Association testing of panic disorder candidate genes using CCK-4 challenge in healthy volunteers. Neurosci Lett 2008, 446:88-92.
62. Mossner R., Freitag C.M., Gutknecht L., Reif A., Tauber R., Franke P., Fritze J., Wagner G., Peikert G., Wenda B., Sand P., Rietschel M., Garritsen H., Jacob C., Lesch K.P., Deckert J. The novel brain-specific tryptophan hydroxylase-2 gene in panic disorder. J Psychopharmacol 2006, 20:547-552.
63. Otter M.H., Matto V., Soukand R., Skrebuhhova T., Allikmets L., Harro J. Characterization of rat exploratory behavior using the exploration box test. Methods Find Exp Clin Pharmacol 1997, 19:683-691.
64. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, San Diego. Fourth Edition.
65. Peyron C., Petit J.-M., Rampon C., Jouvet M., Luppi P.-H. Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods. Neuroscience 1998, 82:443-468.
66. Rainnie D.G., Bergeron R., Sajdyk T.J., Patil M., Gehlert D.R., Shekhar A. Corticotrophin releasing factor-induced synaptic plasticity in the amygdala translates stress into emotional disorders. J Neurosci 2004, 24:3471-3479.
67. Reznikov L.R., Reagan L.P., Fadel J.R. Activation of phenotypically distinct neuronal subpopulations in the anterior subdivision of the rat basolateral amygdala following acute and repeated stress. J Comp Neurol 2008, 508:458-472.
68. Rothe C., Gutknecht L., Freitag C., Tauber R., Mossner R., Franke P., Fritze J., Wagner G., Peikert G., Wenda B., Sand P., Jacob C., Rietschel M., Nothen M.M., Garritsen H., Fimmers R., Deckert J., Lesch K.P. Association of a functional 1019C>G 5-HT1A receptor gene polymorphism with panic disorder with agoraphobia. Int J Neuropsychopharmacol 2004, 7:189-192.
69. Sajdyk T.J., Schober D.A., Gehlert D.R., Shekhar A. Role of corticotropin-releasing factor and urocortin within the basolateral amygdala of rats in anxiety and panic responses. Behav Brain Res 1999, 100:207-215.
70. Salchner P., Sartori S.B., Sinner C., Wigger A., Frank E., Landgraf R., Singewald N. Airjet and FG-7142-induced Fos expression differs in rats selectively bred for high and low anxiety-related behavior. Neuropharmacology 2006, 50:1048-1058.
71. Singewald N., Sharp T. Neuroanatomical targets of anxiogenic drugs in the hindbrain as revealed by Fos immunocytochemistry. Neuroscience 2000, 98:759-770.
72. Singewald N., Salchner P., Sharp T. Induction of c-Fos expression in specific areas of the fear circuitry in rat forebrain by anxiogenic drugs. Biol Psychiatry 2003, 53:275-283.
73. Strobel A., Gutknecht L., Rothe C., Reif A., Mossner R., Zeng Y., Brocke B., Lesch K.P. Allelic variation in 5-HT1A receptor expression is associated with anxiety- and depression-related personality traits. J Neural Transm 2003, 110:1445-1453.
74. Teicher M.H., Samson J.A., Polcari A., McGreenery C.E. Sticks, stones, and hurtful words: relative effects of various forms of childhood maltreatment. Am J Psychiatry 2006, 163:993-1000.
75. Underwood M.D., Khaibulina A.A., Ellis S.P., Moran A., Rice P.M., Mann J.J., Arango V. Morphometry of the dorsal raphe nucleus serotonergic neurons in suicide victims. Biol Psychiatry 1999, 46:473-483.
76. Weiss I.C., Pryce C.R., Jongen-Relo A.L., Nanz-Bahr N.I., Feldon J. Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat. Behav Brain Res 2004, 152:279-295.
77. Yoon H.K., Yang J.C., Lee H.J., Kim Y.K. The association between serotonin-related gene polymorphisms and panic disorder. J Anxiety Disord 2008, 22:1529-1534.
78. Yu Y.W., Tsai S.J., Chen T.J., Lin C.H., Hong C.J. Association study of the serotonin transporter promoter polymorphism and symptomatology and antidepressant response in major depressive disorders. Mol Psychiatry 2002, 7:1115-1119.
79. Zhang K., Xu Q., Xu Y., Yang H., Luo J., Sun Y., Sun N., Wang S., Shen Y. The combined effects of the 5-HTTLPR and 5-HTR1A genes modulates the relationship between negative life events and major depressive disorder in a Chinese population. J Affect Disord 2009, 114:224-231.
80. Zill P., Buttner A., Eisenmenger W., Moller H.J., Bondy B., Ackenheil M. Single nucleotide polymorphism and haplotype analysis of a novel tryptophan hydroxylase isoform (TPH2) gene in suicide victims. Biol Psychiatry 2004, 56:581-586.