Genotype-dependent consequences of traumatic stress in four inbred mouse strains

Genes, Brain and Behavior

Volumn 11, Issue 8, 2012, Pages 977-985

  Szklarczyk, K ^a   Korostynski, M ^a   Golda, S ^a   Solecki, W ^a   Przewlocki, R ^a  

^a INSTITUTE OF PHARMACOLOGY   (Poland)

Author keywords

Amygdala; Fear; Hippocampus; Inbred strains; Mouse models; Nfkbia; Post traumatic stress disorder; Prodynorphin; Stress responsive genes; Tsc22D3

Indexed keywords

MORPHINE; DSIP1 PROTEIN, MOUSE; ENKEPHALIN; I KAPPA B; NF-KAPPAB INHIBITOR ALPHA; PREPROENKEPHALIN; PROTEIN PRECURSOR; TRANSCRIPTION FACTOR;

ADDICTION; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; C57BL 6 MOUSE; CONTROLLED STUDY; CRHR1 GENE; DBA 2 MOUSE; DEPRESSION; FEAR; FOOTSHOCK; GENE; GENE EXPRESSION; GENOTYPE PHENOTYPE CORRELATION; HIPPOCAMPUS; MALE; MOUSE; MOUSE STRAIN; NFKBIA GENE; NONHUMAN; PLAT GENE; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; PSYCHOSOCIAL WITHDRAWAL; REWARD; SENSITIVITY ANALYSIS; STRESS; SWISS WEBSTER MOUSE; TSC22D3 GENE; UPREGULATION; ANIMAL; DISEASE MODEL; ELECTRIC SHOCK; GENETIC PREDISPOSITION; GENETICS; GENOTYPE; INBRED MOUSE STRAIN; METABOLISM; PHENOTYPE; SPECIES DIFFERENCE;

ANIMALIA; MUS;

AMYGDALA; ANIMALS; DISEASE MODELS, ANIMAL; ELECTROSHOCK; ENKEPHALINS; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HIPPOCAMPUS; I-KAPPA B PROTEINS; MICE; MICE, INBRED STRAINS; PHENOTYPE; PROTEIN PRECURSORS; SPECIES SPECIFICITY; STRESS DISORDERS, POST-TRAUMATIC; TRANSCRIPTION FACTORS;

EID: 84876992094     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/j.1601-183X.2012.00850.x     Document Type: Article

References (67)

1. Acheson, D.T., Gresack, J.E. & Risbrough, V.B. (2011) Hippocampal dysfunction effects on context memory: possible etiology for posttraumatic stress disorder. Neuropharmacology 62, 674-685.
2. Adamec, R., Holmes, A. & Blundell, J. (2008) Vulnerability to lasting anxiogenic effects of brief exposure to predator stimuli: sex, serotonin and other factors-relevance to PTSD. Neurosci Biobehav Rev 32, 1287-1292.
3. Amstadter, A.B., Nugent, N.R., Yang, B.Z., Miller, A., Siburian, R., Moorjani, P., Haddad, S., Basu, A., Fagerness, J., Saxe, G., Smoller, J.W. & Koenen, K.C. (2011) Corticotrophin-releasing hormone type 1 receptor gene (CRHR1) variants predict posttraumatic stress disorder onset and course in pediatric injury patients. Dis Markers 30, 89-99.
4. Ayroldi, E. & Riccardi, C. (2009) Glucocorticoid-induced leucine zipper (GILZ): a new important mediator of glucocorticoid action. FASEB J 23, 3649-3658.
5. Belzung, C., El Hage, W.,Moindrot, N. & Griebel, G. (2001) Behavioral and neurochemical changes following predatory stress in mice. Neuropharmacology 41, 400-408.
6. Bilkei-Gorzo, A., Erk, S., Schurmann, B., Mauer, D., Michel, K., Boecker, H., Scheef, L., Walter, H. & Zimmer, A. (2012) Dynorphins regulate fear memory: from mice to men. J Neurosci 32, 9335-9343.
7. Binder, E.B. (2009) The role of FKBP5, a co-chaperone of the glucocorticoid receptor in the pathogenesis and therapy of affective and anxiety disorders. Psychoneuroendocrinology 34 (Suppl. 1), S186-S195.
8. Bonini, S.A., Ferrari-Toninelli, G., Uberti, D., Montinaro, M., Buizza, L., Lanni, C., Grilli, M., Memo, M. (2011) Nuclear factor κBdependent neurite remodeling is mediated by notch pathway. J Neurosci 31, 11697-11705.
9. Camp, M., Norcross, M., Whittle, N., Feyder, M., D'Hanis, W., Yilmazer-Hanke, D., Singewald, N. & Holmes, A. (2009) ImpairedPavlovian fear extinction is a common phenotype across genetic lineages of the 129 inbred mouse strain. Genes Brain Behav 8, 744-752.
10. Chilcoat, H.D. & Breslau, N. (1998) Posttraumatic stress disorder and drug disorders: testing causal pathways. Arch Gen Psychiatry 55, 913-917.
11. Cohen, H., Geva, A.B.,Matar,M.A., Zohar, J. & Kaplan, Z. (2008) Posttraumatic stress behavioural responses in inbred mouse strains: can genetic predisposition explain phenotypic vulnerability? Int J Neuropsychopharmacol 11, 331-349.
12. Cohen, H., Kozlovsky, N., Alona, C., Matar, M.A. & Joseph, Z. (2011). Animal model for PTSD: from clinical concept to translational research. Neuropharmacology 62, 715-724.
13. Fenoglio, K.A., Chen, Y. & Baram, T.Z. (2006) Neuroplasticity of the hypothalamic-pituitary-adrenal axis early in life requires recurrent recruitment of stress-regulating brain regions. J Neurosci 26, 2434-2442.
14. Gubner, N.R., Wilhelm, C.J., Phillips, T.J. & Mitchell, S.H. (2010) Strain differences in behavioral inhibition in a Go/No-go task demonstrated using 15 inbred mouse strains. Alcohol Clin Exp Res 34, 1353-1362.
15. Hurd, Y.L. (2002) Subjects with major depression or bipolar disorder show reduction of prodynorphin mRNA expression in discrete nuclei of the amygdaloid complex. Mol Psychiatry 7, 75-81.
16. Jacobsen, L.K., Southwick, S.M., Kosten, T.R. (2001) Substance use disorders in patients with posttraumatic stress disorder: a review of the literature. Am J Psychiatry 158, 1184-1190.
17. Kamprath, K. & Wotjak, C.T. (2004) Nonassociative learning processes determine expression and extinction of conditioned fear in mice. Learn Mem 11, 770-786.
18. Kaouane, N., Porte, Y., Vallee, M., Brayda-Bruno, L., Mons, N., Calandreau, L., Marighetto, A., Piazza, P.V. & Desmedt, A. (2012) Glucocorticoids can induce PTSD-like memory impairments in mice. Science 335, 1510-1513.
19. Kest, B., Hopkins, E., Palmese, C.A., Adler, M. & Mogil, J.S. (2002a) Genetic variation in morphine analgesic tolerance: a survey of 11 inbred mouse strains. Pharmacol Biochem Behav 73, 821-828.
20. Kest, B., Palmese, C.A., Hopkins, E., Adler, M., Juni, A. & Mogil, J.S. (2002b) Naloxone-precipitated withdrawal jumping in 11 inbred mouse strains: evidence for common genetic mechanisms in acute and chronic morphine physical dependence. Neuroscience 115, 463-469.
21. Knoll, A.T. & Carlezon, W.A. Jr. (2010) Dynorphin, stress, and depression. Brain Res 1314, 56-73.
22. Korostynski, M., Kaminska-Chowaniec, D., Piechota, M. & Przewlocki, R. (2006) Gene expression profiling in the striatum of inbred mouse strains with distinct opioid-related phenotypes. BMC Genomics 7, 146.
23. Korostynski, M., Piechota, M., Kaminska, D., Solecki, W. & Przewlocki, R. (2007) Morphine effects on striatal transcriptome in mice. Genome Biol 8, R128.
24. Mahan, A.L. & Ressler, K.J. (2011). Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder. Trends Neurosci.
25. Maren, S. (1996) Synaptic transmission and plasticity in the amygdala. An emerging physiology of fear conditioning circuits.Mol Neurobiol 13, 1-22.
26. Matsuyama, S., Namgung, U., Routtenberg, A. (1997) Longterm potentiation persistence greater in C57BL/6 than DBA/2 mice: predicted on basis of protein kinase C levels and learning performance. Brain Res 763, 127-130.
27. Mattson, M.P., Culmsee, C., Yu, Z. & Camandola, S. (2000) Roles of nuclear factor kappaB in neuronal survival and plasticity. J Neurochem 74, 443-456.
28. McEwen, B.S., Eiland, L., Hunter, R.G. & Miller, M.M. (2011). Stress and anxiety: structural plasticity and epigenetic regulation as a consequence of stress. Neuropharmacology 62, 3-12.
29. Memet, S. (2006) NF-kappaB functions in the nervous system: from development to disease. Biochem Pharmacol 72, 1180-1195.
30. Mikics, E., Baranyi, J., Haller, J. (2008) Rats exposed to traumatic stress bury unfamiliar objects--a novel measure of hyper-vigilance in PTSD models? Physiol Behav 94, 341-348.
31. Milner, L.C. & Crabbe, J.C. (2008) Three murine anxiety models: results from multiple inbred strain comparisons. Genes Brain Behav 7, 496-505.
32. Moy, S.S., Nadler, J.J., Young, N.B., Nonneman, R.J., Segall, S.K., Andrade, G.M., Crawley, J.N. & Magnuson, T.R. (2008) Social approach and repetitive behavior in eleven inbred mouse strains. Behav Brain Res 191, 118-129.
33. Nemeroff, C.B., Bremner, J.D., Foa, E.B., Mayberg, H.S., North, C.S. & Stein, M.B. (2006) Posttraumatic stress disorder: a state-of-thescience review. J Psychiatr Res 40, 1-21.
34. Olff, M., Langeland, W. & Gersons, B.P. (2005) The psychobiology of PTSD: coping with trauma. Psychoneuroendocrinology 30, 974-982.
35. Ottoni, E.B. (2000) EthoLog 2.2: a tool for the transcription and timing of behavior observation sessions. Behav Res Methods Instrum Comput 32, 446-449.
36. Pang, P.T., Teng, H.K., Zaitsev, E., Woo, N.T., Sakata, K., Zhen, S., Teng, K.K., Yung, W.H., Hempstead, B.L., Lu, B. (2004) Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 306, 487-491.
37. Paulus,M.P., Dulawa, S.C., Ralph, R.J. & Mark, A.G. (1999) Behavioral organization is independent of locomotor activity in 129 and C57 mouse strains. Brain Res 835, 27-36.
38. Pawlak, R., Magarinos, A.M., Melchor, J., McEwen, B., Strickland, S. (2003) Tissue plasminogen activator in the amygdala is critical for stress-induced anxiety-like behavior. Nat Neurosci 6, 168-174.
39. Philbert, J., Pichat, P., Beeske, S., Decobert, M., Belzung, C. & Griebel, G. (2011) Acute inescapable stress exposure induces long-term sleep disturbances and avoidance behavior: a mouse model of post-traumatic stress disorder (PTSD). Behav Brain Res 221, 149-154.
40. Piechota, M., Korostynski, M., Solecki, W., Gieryk, A., Slezak, M., Bilecki, W., Ziolkowska, B., Kostrzewa, E., Cymerman, I., Swiech, L., Jaworski, J. & Przewlocki, R. (2010) The dissection of transcriptional modules regulated by various drugs of abuse in the mouse striatum. Genome Biol 11, R48.
41. Pittenger, C. & Duman, R.S. (2008) Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology 33, 88-109.
42. Radley, J.J., Kabbaj, M., Jacobson, L., Heydendael, W., Yehuda, R., Herman, J.P. (2011) Stress risk factors and stress-related pathology: Neuroplasticity, epigenetics and endophenotypes. Stress 14, 481-497.
43. Radulovic, J., Kammermeier, J. & Spiess, J. (1998) Generalization of fear responses in C57BL/6N mice subjected to one-trial foreground contextual fear conditioning. Behav Brain Res 95, 179-189.
44. Romano, A., Freudenthal, R., Merlo, E. & Routtenberg, A. (2006) Evolutionarily-conserved role of the NF-kappaB transcription factor in neural plasticity and memory. Eur J Neurosci 24, 1507-1516.
45. Rozeske, R.R., Der-Avakian, A., Bland, S.T., Beckley, J.T., Watkins, L.R. & Maier, S.F. (2009) The medial prefrontal cortex regulates the differential expression of morphine-conditioned place preference following a single exposure to controllable or uncontrollable stress. Neuropsychopharmacology 34, 834-843.
46. Salomons, A.R., van Luijk, J.A., Reinders, N.R., Kirchhoff, S., Arndt, S.S. & Ohl, F. (2010) Identifying emotional adaptation: behavioural habituation to novelty and immediate early gene expression in two inbred mouse strains. Genes Brain Behav 9, 1-10.
47. Schimanski, L.A., Ali, D.W., Baker, G.B. & Nguyen, P.V. (2007) Impaired hippocampal LTP in inbred mouse strains can be rescued by beta-adrenergic receptor activation. Eur J Neurosci 25, 1589-1598.
48. Shibuya, N., Suzuki, A., Sadahiro, R., Kamata, M., Matsumoto, Y., Goto, K., Hozumi, Y. & Otani, K. (2010) Association study between a functional polymorphism of FK506-binding protein 51 (FKBP5) gene and personality traits in healthy subjects. Neurosci Lett 485, 194-197.
49. Shiosaka, S. (2004) Serine proteases regulating synaptic plasticity. Anat Sci Int 79, 137-144.
50. Siegmund, A., Wotjak, C.T. (2006) Toward an animal model of posttraumatic stress disorder. Ann N Y Acad Sci 1071, 324-334.
51. Siegmund, A. & Wotjak, C.T. (2007a) Hyperarousal does not depend on trauma-related contextual memory in an animal model of posttraumatic stress disorder. Physiol Behav 90, 103-107.
52. Siegmund, A. & Wotjak, C.T. (2007b) Amousemodel of posttraumatic stress disorder that distinguishes between conditioned and sensitised fear. J Psychiatr Res 41, 848-860.
53. Siegmund, A., Langnaese, K., Wotjak, C.T. (2005) Differences in extinction of conditioned fear in C57BL/6 substrains are unrelated to expression of alpha-synuclein. Behav Brain Res 157, 291-298.
54. Skrzypiec, A.E., Buczko, W. & Pawlak, R. (2008) Tissue plasminogen activator in the amygdala: a new role for an old protease. J Physiol Pharmacol 59 (Suppl. 8), 135-146.
55. Solecki, W., Turek, A., Kubik, J. & Przewlocki, R. (2009) Motivational effects of opiates in conditioned place preference and aversion paradigm--a study in three inbred strains of mice. Psychopharmacology (Berl) 207, 245-255.
56. Tang, X., Orchard, S.M. & Sanford, L.D. (2002) Home cage activity and behavioral performance in inbred and hybridmice. Behav Brain Res 136, 555-569.
57. Thoeringer, C.K., Henes, K., Eder, M., Dahlhoff, M., Wurst, W., Holsboer, F., Deussing, J.M., Moosmang, S. & Wotjak, C.T. (2012) Consolidation of remote fear memories involves Corticotropin- Releasing Hormone (CRH) receptor type 1-mediated enhancement of AMPA receptor GluR1 signaling in the dentate gyrus. Neuropsychopharmacology 37, 787-796.
58. Touma, C., Gassen, N.C., Herrmann, L., Cheung-Flynn, J., Bull, D.R., Ionescu, I.A., Heinzmann, J.M., Knapman, A., Siebertz, A., Depping, A.M., Hartmann, J., Hausch, F., Schmidt, M.V., Holsboer, F., Ising, M., Cox, M.B., Schmidt, U. & Rein, T. (2011) FK506 binding protein 5 shapes stress responsiveness: modulation of neuroendocrine reactivity and coping behavior. Biol Psychiatry 70, 928-936.
59. Tzschentke, T.M. (2007) Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict Biol 12, 227-462.
60. Uchiumi, K., Aoki, M., Kikusui, T., Takeuchi, Y., Mori, Y. (2008) Wheel-running activity increases with social stress in male DBA mice. Physiol Behav 93, 1-7.
61. Wang, X.D., Rammes, G., Kraev, I., Wolf, M., Liebl, C., Scharf, S.H., Rice, C.J., Wurst, W., Holsboer, F., Deussing, J.M., Baram, T.Z., Stewart, M.G., Muller, M.B. & Schmidt, M.V. (2011) Forebrain CRF(1) modulates early-life stress-programmed cognitive deficits. J Neurosci 31, 13625-13634.
62. Wang, X.D., Labermaier, C., Holsboer, F., Wurst, W., Deussing, J.M., Muller, M.B. & Schmidt, M.V. (2012). Early-life stress-induced anxiety-related behavior in adult mice partially requires forebrain corticotropin-releasing hormone receptor 1. Eur J Neurosci 36, 2360-2367.
63. Wittmann, W., Schunk, E., Rosskothen, I., Gaburro, S., Singewald, N., Herzog, H. & Schwarzer, C. (2009) Prodynorphin-derived peptides are critical modulators of anxiety and regulate neurochemistry and corticosterone. Neuropsychopharmacology 34, 775-785.
64. Yachi, K., Inoue, K., Tanaka, H., Yoshikawa, H. & Tohyama, M. (2007) Localization of glucocorticoid-induced leucine zipper (GILZ) expressing neurons in the central nervous system and its relationship to the stress response. Brain Res 1159, 141-147.
65. Yang, N., Zhang, W. & Shi, X.M. (2008) Glucocorticoid-induced leucine zipper (GILZ) mediates glucocorticoid action and inhibits inflammatory cytokine-induced COX-2 expression. J Cell Biochem 103, 1760-1771.
66. Yeh, S.H., Lin, C.H. & Gean, P.W. (2004) Acetylation of nuclear factorkappaB in rat amygdala improves long-term but not short-term retention of fear memory. Mol Pharmacol 65, 1286-1292.
67. Yehuda, R. & LeDoux, J. (2007) Response variation following trauma: a translational neuroscience approach to understanding PTSD. Neuron 56, 19-32.