Gene expression in amygdala as a function of differential trait anxiety levels in genetically heterogeneous NIH-HS rats

Behavioural Brain Research

Volumn 252, Issue , 2013, Pages 422-431

  Díaz Morán, Sira ^a   Palència, Marta ^a   Mont Cardona, Carme ^a,b   Cañete, Toni ^a   Blázquez, Gloria ^a   Martínez Membrives, Esther ^a   López Aumatell, Regina ^b   Sabariego, Marta ^c   Donaire, Rocío ^c   Morón, Ignacio ^d   Torres, Carmen ^c   Martínez Conejero, José Antonio ^e   Tobeña, Adolf ^a   Esteban, Francisco José ^c   Fernández Teruel, Alberto ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF JAÉN   (Spain)

^d UNIVERSITY OF GRANADA   (Spain)

^e IVIOMICS   (Spain)

Author keywords

Amygdala; Anxiety trait; Fearfulness; Genetically heterogeneous NIH HS rats; HPA axis; Microarray analysis

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARR3 GENE; ARTICLE; AVOIDANCE BEHAVIOR; AVPR1B GENE; BRAIN FUNCTION; BREEDING; CENTRAL NERVOUS SYSTEM; ELECTROENCEPHALOGRAM; FEAR; GENE; GENE ACTIVITY; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE SEQUENCE; GENETIC HETEROGENEITY; GENETIC REGULATION; H2 M9 GENE; MALE; MAZE TEST; NONHUMAN; NUCLEOTIDE SEQUENCE; PR14A1 GENE; PREDICTION; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS MAPPING; RAT; STRESS; TACR3 GENE; UCN3 GENE;

EID: 84880355880     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.05.066     Document Type: Article

References (79)

1. Gray J., McNaughton N. The neuropsychology of anxiety 2000, Oxford University Press, New York.
2. Davis M. Neurobiology of fear responses: the role of the amygdala. Journal of Neuropsychiatry and Clinical Neurosciences 1997, 9:382-402.
3. LeDoux J.E. Emotion circuits in the brain. Annual Review of Neuroscience 2000, 23:155-184.
4. López-Aumatell R., Guitart-Masip M., Vicens-Costa E., Gimenez-Llort L., Valdar W., Johannesson M., et al. Fearfulness in a large N/Nih genetically heterogeneous rat stock: differential profiles of timidity and defensive flight in males and females. Behavioural Brain Research 2008, 188:41-55.
5. Kertes E., László K., Berta B., Lénárd L. Effects of substance P microinjections into the globus pallidus and central nucleus of amygdala on passive avoidance learning in rats. Behavioural Brain Research 2009, 198:397-403.
6. Morón I., Gómezb M.J., Escarabajal D., Torre L., Cándido A., Maldonado A., et al. One-way avoidance learning in female inbred Roman high- and low-avoidance rats: effects of bilateral electrolytic central amygdala lesions. Neuroscience Letters 2010, 474:32-36.
7. Gómez M.J., Morón I., Torres C., Esteban F.J., de la Torre L., Cándido A., et al. One-way avoidance acquisition and cellular density in the basolateral amygdala: strain differences in Roman high- and low-avoidance rats. Neuroscience Letters 2009, 450:317-320.
8. Guitart-Masip M., Johansson B., Cañete T., Fernández-Teruel A., Tobeña A., Terenius A., et al. Regional adaptations in PSD-95, NGFI-A and secretogranin gene transcripts related to vulnerability to behavioral sensitization to amphetamine in the Roman rat strains. Neuroscience 2008, 151:195-208.
9. López-Aumatell R., Vicens-Costa E., Guitart-Masip M., Martínez-Membrives E., Valdar W., Johannesson M., et al. Unlearned anxiety predicts learned fear: a comparison among heterogeneous rats and the Roman rat strains. Behavioural Brain Research 2009, 202:92-101.
10. Yilmazer-Hanke D.M., Faber-Zuschratter H., Linke R., Schwegler H. Contribution of amygdala neurons containing peptides and calcium-binding proteins to fear-potentiated startle and exploration-related anxiety in inbred Roman high- and low-avoidance rats. European Journal of Neuroscience 2002, 15:1206-1218.
11. Mei B., Li C., Dong S., Jiang C., Huimin W., Hu Y. Distinct gene expression profiles in hippocampus and amygdala after fear conditioning. Brain Research Bulletin 2005, 67:1-12.
12. Ploski J.E., Park K.W., Ping J., Monsey M.S., Schafe G.E. Identification of plasticity-associated genes regulated by Pavlovian fear conditioning in the lateral amygdala. Journal of Neurochemistry 2010, 112:636-650.
13. Hansen C., Spuhler K. Development of the National Institutes of Health genetically heterogeneous stock. Alcoholism, Clinical and Experimental Research 1984, 8:477-479.
14. Johannesson M., López-Aumatell R., Stridh P., Diez M., Tuncel J., Blázquez G., et al. A resource for the simultaneous high-resolution mapping of multiple quantitative trait loci in rats: the NIH heterogeneous stock. Genome Research 2009, 19:150-158.
15. Díaz-Morán S., Palencia M., Mont C., Cañete T., Blázquez G., Martínez-Membrives E., et al. Coping style and stress hormone responses in genetically heterogeneous rats: comparison with the Roman rat strains. Behavioural Brain Research 2012, 228:203-210.
16. Vicens-Costa E., Martínez-Membrives E., López-Aumatell R., Guitart-Masip M., Cañete T., Blázquez G., et al. Two-way avoidance acquisition is negatively related to conditioned freezing and positively associated with startle reactions: a dissection of anxiety and fear in genetically heterogeneous rats. Physiology and Behavior 2011, 103:148-156.
17. Alam I., Koller D.L., Sun Q., Roeder R.K., Cañete T., Blázquez G., et al. Heterogeneous stock rat: a unique animal model for mapping genes influencing bone fragility. Bone 2011, 48:1169-1177.
18. Solberg L.C., Holl K., Tschannen M., Valdar W. Fine-mapping a locus for glucose tolerance using heterogeneous stock rats. Physiological Genomics 2010, 41:102-108.
19. Fernández-Teruel A., Escorihuela R.M., Núñez J.F., Zapata A., Boix F., Salazar W., et al. The early acquisition of two-way (shuttle-box) avoidance as an anxiety-mediated behavior: psychopharmacological validation. Brain Research Bulletin 1991, 26:173-176.
20. Shepherd J.K., Grewal S.S., Fletcher A., Bill D.J., Dourishmm C.T. Behavioural and pharmacological characterisation of the elevated zero-maze as an animal model of anxiety. Psychopharmacology 1994, 116:56-64.
21. Escorihuela R.M., Fernández-Teruel A., Zapata A., Núñez J.F., Tobeña A. Flumazenil prevents the anxiolytic effects diazepam, alprazolam and adinazolam on the early acquisition of two-way active avoidance. Pharmacological Research 1993, 28:53-58.
22. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1997, Academic Press, Sydney. 4th ed.
23. Schroeder A., Mueller O., Stocker S., Salowsky R., Leiber M., Gassmann M., et al. The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Molecular Biology 2006, 31:3-7.
24. Wang H., Zhu Y.Z., Wong P.T.H., Farook J.M., Teo A.L., Lee L.K.H., et al. cDNA microarray analysis of gene expression in anxious PVG and SD rats after cat-freezing test. Experimental Brain Research 2003, 149:413-421.
25. Kabbaj M., Evans S., Watson S.J., Akil H. The search for the neurobiological basis of vulnerability to drug abuse: using microarrays to investigate the role of stress and individual differences. Neuropharmacology 2004, 47:111-122.
26. Zhang S., Amstein T., Shen J., Brush R.F., Gershenfeld H.K. Molecular correlates of emotional learning using genetically selected rat lines. Genes, Brain and Behavior 2005, 4:99-109.
27. Sabariego M., Gómez M.J., Morón I., Torres C., Fernández-Teruel A., Tobeña A., et al. Differential gene expression between inbred Roman high- (RHA-I) and low- (RLA-I) avoidance rats. Neuroscience Letters 2011, 504:265-270.
28. Andrus B.M., Blizinsky K., Vedell P.T., Dennis K., Shukla P.K., Schaffer D.J., et al. Gene expression patterns in the hippocampus and amygdale of endogeneous depression and chronic stress models. Molecular Psychiatry 2010, 17:49-61.
29. Kim K.S., Han P.L. Optimization of chronic stress paradigms using anxiety- and depression-like behavioral parameters. Journal of Neuroscience Research 2006, 83:497-507.
30. Ain R., Tash J., Soares M. Prolactin-like protein-A is a functional modulator of natural killer cells at the maternal-fetal interface. Molecular and Cellular Endocrinology 2003, 204:65-74.
31. Castanon N., Pérez-Díaz F., Mormede P. Genetic analysis of the relationship between behavioral and neuroendocrine traits in Roman high and low avoidance rat lines. Behavior Genetics 1995, 25:371-383.
32. Steimer T., Driscoll P. Divergent stress responses and coping styles in psychogenetically selected Roman high-(RHA) and low-(RLA) avoidance rats: behavioral, neuroendocrine and developmental aspects. Stress 2003, 6:87-100.
33. Lewis K., Li C., Perrin M.H., Blount A., Kunitake K., Donaldson C., et al. Identification of urocortin III, an additional member of the corticotropin-releasing factor (CRF) family with high affinity for the CRF2 receptor. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:7570-7575.
34. Li C., Vaughan J., Sawchenko P.E., Vale W.W. Urocortin III-immunoreactive projections in rat brain: partial overlap with sites of type 2 corticotrophin-releasing factor receptor expression. Journal of Neuroscience 2002, 22:991-1001.
35. Jamieson P.M., Li C., Kukura C., Vaughan J., Vale W. Urocortin 3 modulates the neuroendocrine stress response and is regulated in rat amygdala and hypothalamus by stress and glucocorticoids. Endocrinology 2006, 147:4578-4588.
36. Venihaki M., Sakihara S., Subramanian S., Dikkes P., Weninger S.C., Liapakis G., et al. Urocortin III, a brain neuropeptide of the corticotropin-releasing hormone family: modulation by stress and attenuation of some anxiety-like behaviours. Journal of Neuroendocrinology 2004, 16:411-422.
37. Skutella T., Criswell H., Moy S., Probst J.C., Breese G.R., Jirikowski G.F., et al. Corticotropin-releasing hormone (CRH) antisense oligodeoxynucleotide induces anxiolytic effects in rat. Neuroreport 1994, 5:2181-2185.
38. Krajewski S.J., Anderson M.J., Iles-Shih L., Chen K.J., Urbanski H.F., Rance N.E. Morphologic evidence that neurokinin B modulates gonadotropin-releasing hormone secretion via neurokinin 3 receptors in the rat median eminence. Journal of Comparative Neurology 2005, 89:372-386.
39. Nussdorfer G., Malendowicz L. Role of tachykinins in the regulation of the hypothalamo-pituitary-adrenal axis. Peptides 1998, 19:949-968.
40. Sladek C.D., Stevens W., Levinson S.R., Song Z., Jensen D.D., Flynn F.W. Characterization of nuclear neurokinin 3 receptor expression in rat brain. Neuroscience 2011, 196:35-48.
41. Lessard A., Campos M.M., Neugebauer W., Couture R. Implication of nigral tachykinin NK3 receptors in the maintenance of hypertension in spontaneously hypertensive rats: a pharmacologic and autoradiographic study. British Journal of Pharmacology 2003, 138:554-563.
42. De Souza Silva M.A., Mello E.L., Muller C.P., Jocham G., Maior R.S., Huston J.P., et al. The tachykinin NK3 receptor antagonist SR142801 blocks the behavioral effects of cocaine in marmoset monkeys. European Journal of Pharmacology 2006, 536:269-278.
43. Stoessl A.J., Dourish C.T., Iversen S.D. The NK-3 tachykinin receptor agonist senktide elicits 5-HT-mediated behaviour following central or peripheral administration in mice and rats. British Journal of Pharmacology 1988, 94:285-287.
44. Hurt P., Walter L., Sudbrak R., Klages S., Müller I., Shiina T., et al. The genomic sequence and comparative analysis of the rat major histocompatibility complex. Genome Research 2004, 14:631-639.
45. Craft C.M., Whitmore D.H., Wiechmann A.F. Cone arrestin identified by targeting expression of a functional family. Journal of Biological Chemistry 1994, 269:4613-4619.
46. Macey T.A., Gurevich V.V., Neve K.A. Preferential interaction between the dopamine D2 receptor and Arrestin2 in neostriatal neurons. Molecular Pharmacology 2004, 66:1635-1642.
47. Engin E., Treit D. Dissociation of the anxiolytic-like effects of Avpr1a and Avpr1b receptor antagonists in the dorsal and ventral hippocampus. Neuropeptides 2008, 242:411-421.
48. Landgraf R., Keßler M., Bunk M., Murgatroyd C., Spengler D., Zimbelmann M., et al. Candidate genes of anxiety-related behavior in HAB/LAB rats and mice: focus on vasopressin and glycoxalase-I. Neuroscience and Biobehavioral Reviews 2007, 31:89-102.
49. Serradeil-Le Gal C., Wagnon J., Tonnerre B., Roux R., Garcia G., Griebel G., et al. An overview of SSR149415, a selective nonpeptide vasopressin V(1b) receptor antagonist for the treatment of stress-related disorders. CNS Drug Reviews 2005, 11:53-68.
50. 2+ concentration in hippocampal and cortical astrocytes through two distinct receptors. Journal of Neurochemistry 2007, 103:229-237.
51. Zhao D.K., Ai H.B. Oxytocin and vasopressin involved in restraint water-immersion stress mediated by oxytocin receptor and vasopressin 1b receptor in rat brain. PLoS ONE 2011, 6:e23362. 10.1371/journal.pone.0023362.
52. Bradesi S., Martinez V., Lao L., Larsson H., Mayer E.A. Involvement of vasopressin 3 receptors in chronic psychological stress-induced visceral hyperalgesia in rats. American Journal of Physiology - Gastrointestinal and Liver Physiology 2009, 296:G302-G309.
53. Lolait S.J., O'Carroll A.M., Mahan L.C., Felder C.C., Button D.C., Young W.S., et al. Extrapituitary expression of the rat V1b vasopressin receptor gene. Proceedings of the National Academy of Sciences of the United States of America 1995, 92:6783-6787.
54. Driscoll P., Fernández-Teruel A., Corda M.G., Giorgi O., Steimer T. Some guidelines for defining personality differences in rats. Handbook of Behavior Genetics 2009, 281-300. Springer, USA. Yong-Kyu Kim (Ed.).
55. Roozendaal B., Wierma A., Driscoll P., Koolhaas J.M., Bohus B. Vasopressinergic modulation of stress responses in the central amygdale of the Roman high-avoidance and low-avoidance rat. Brain Research 1992, 596:35-40.
56. Pimpinelli F., Parenti M., Guzzi F., Piva F., Hokfelt T., Maggi R. Presence of delta opioid receptors on a subset of hypothalamic gonadotropin releasing hormone (GnRH) neurons. Brain Research 2006, 1070:15-23.
57. Wu Y., Chen R., Zhao X., Li Z., Zhou J. JWA regulates chronic morphine dependence via the delta opioid receptor. Biochemical and Biophysical Research Communications 2011, 409:520-525.
58. Zhu Y., King M., Schuller A., Nitsche J., Reidl M., Elde R., et al. Retention of supraspinal delta-like analgesia and loss of morphine tolerance in δ opioid receptor knockout mice. Neuron 1999, 24:243-252.
59. Randall-Thompson J., Pescatore K., Unterwald E. A role for delta opioid receptors in the central nucleus of the amygdala in anxiety-like behaviors. Psychopharmacology 2010, 212:585-595.
60. Babygirija R., Bülbül M., Yoshimoto S., Ludwig K., Takahashi T. Central and peripheral release of oxytocin following chronic homotypic stress in rats. Autonomic Neuroscience - Basic and Clinical 2012, 167:56-60.
61. Windler R.J., Kershaw Y.M., Shanks N., Wood S.A., Lightman S.L., Ingram C.D. Oxytocin attenuates stress-induced c-fos mRNA expression in specific forebrain regions associated with modulation of hypothalamo-pituitary-adrenal activity. Journal of Neuroscience 2004, 24:2974-2982.
62. Uvnäs-Mosberg K., Eklund M., Hillegaart V., Ahlenius S. Improved conditioned avoidance learning by ocytocin administration in high-emotional male Sprague-Dawley rats. Regulatory Peptides 2000, 88:27-32.
63. Laguna-Abreu M.T., Germano C., Moreira A.C., Antunes-Rodrigues J., Elias L., Castro M. Changes in prolactin secretion in the short- and long-term after adrenalectomy. Arquivos Brasileiros de Endocrinologia e Metabologia 2012, 56:244-249.
64. Bertoglio L.J., Zangrossi J.H. Involvement of dorsolateral periaqueductal gray cholecystokinin-2 receptors in the regulation of a panic-related behavior in rats. Brain Research 2005, 1059:46-51.
65. Faris P.L., Komisaruk B.R., Watkins L.R., Mayer D.J. Evidence for the neuropeptide cholecystokinin as an antagonist of opiate analgesia. Science 1983, 219:310-312.
66. Lovick T.A. Pro-nociceptive action of cholecystokinin in the periaqueductal grey: a role in neuropathic and anxiety-induced hyperalgesic states. Neuroscience and Biobehavioral Reviews 2008, 32:852-862.
67. Greisen M.H., Bolwig T.G., Wörtwein G. Cholecystokinin tetrapeptide effects on HPA axis function and elevated plus maze behaviour in maternally separated and handled rats. Behavioural Brain Research 2005, 161:204-212.
68. Deng P., Xiao Z., Jha A., Ramonet D., Matsui T., Leitges M., et al. Cholecystokinin facilitates glutamate release by increasing the number of readily releasable vesicles and releasing probability. Journal of Neuroscience 2010, 30:5136-5148.
69. Vanessa A.M., Jeong H., Drew G., Vaughan C.W. Cholecystokinin exerts an effect via the endocannabinoid system to inhibit GABAergic transmission in midbrain periaqueductal gray. Neuropsychopharmacology 2011, 36:1801-1810.
70. Lang C.H., Nystrom G.J., Frost R.A. Burn-induced changes in IGF-I and IGF-binding proteins are partially glucocorticoid dependent. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2002, 282:R207-R215.
71. Pereira R.C., Blanquaert F., Canalis E. Cortisol enhances the expression of mac25/insulin-like growth factor-binding protein-related protein-1 in cultured osteoblasts. Endocrinology 1999, 140:228-232.
72. Nakakura T., Soda A., Unno K., Suzuki M., Tanaka S. Expression of IGFBP7 mRNA in corticotrophs in the anterior pituitary of adrenalectomized rats. Journal of Histochemistry and Cytochemistry 2010, 58:969-978.
73. Goddard A.W., Ball S.G., Martinez J., Robinson M.J., Yang C.R., Russell J.M., et al. Current perspectives of the roles of the central norepinephrine system in anxiety and depression. Depression and Anxiety 2010, 27:339-350.
74. Kvetnanky R., Sabban E.L., Palkovits M. Catecholaminergic systems in stress: structural and molecular. Genetic approaches. Physiological Reviews 2009, 89:535-606.
75. Huang da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols 2009, 4:44.
76. Huang da W., Sherman B.T., Lempicki R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research 2009, 37:1.
77. Gimsa U., Kanitz E., Otten W., Tuchscherer M., Tuchscherer A., Ibrahim S.M. Tumour necrosis factor receptor deficiency alters anxiety-like behavioural and neuroendocrine stress responses of mice. Cytokine 2012, 59:72-78.
78. Bailey M.T., Kinsey S.G., Padgett D.A., Sheridan J.F., Leblebici B. Social stress enhances IL-1β and TNF-α production by Porphyromonas gingivalis lipopolysaccharide-stimulated CD11b+ cells. Physiology and Behavior 2009, 98:351-358.
79. Chen J., Song Y., Yang J., Zhang Y., Zhao P., Zhu X., et al. The contribution of TNF-α in the amygdala to anxiety in mice with persistent inflammatory pain. Neuroscience Letters 2013, in press.