Gene and stress history interplay in emergence of PTSD-like features

Behavioural Brain Research

Volumn 292, Issue , 2015, Pages 266-277

  Chakraborty, Nabarun ^a   Meyerhoff, James ^a   Gautam, Aarti ^a   Muhie, Seid ^a   Jibitu, Meskerem ^a   De Lima, Thereza C M ^b   Hammamieh, Rasha ^a   Jett, Marti ^a  

^a US Army Center for Environmental Health Research   (United States)

^b FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

Author keywords

Aggressor exposed model; Gene environment model; Mouse behavior; Mouse strain differences; Post traumatic stress disorder (PTSD)

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CHOLECYSTOKININ B RECEPTOR; FK 506 BINDING PROTEIN; FK 506 BINDING PROTEIN 5; NERVE GROWTH FACTOR; SEROTONIN TRANSPORTER; UNCLASSIFIED DRUG;

AGGRESSION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; BDNF GENE; BRAIN TISSUE; C57BL 6 MOUSE; CARDIOMYOPATHY; CCKBR GENE; CLINICAL FEATURE; CONTROLLED STUDY; DBA 2 MOUSE; DISEASE PREDISPOSITION; ENVIRONMENTAL EXPOSURE; FKBP5 GENE; GENETIC ASSOCIATION; GENETIC HETEROGENEITY; GENOTYPE ENVIRONMENT INTERACTION; HISTOPATHOLOGY; HYPOXIA; MALE; MOUSE; MURINE MODEL; NERVE CELL PLASTICITY; NGF GENE; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; SLC6A4 GENE; STRESS; ZWINT GENE; ANIMAL; DISEASE MODEL; GENE EXPRESSION; GENETICS; MEMORY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; GENE EXPRESSION; MALE; MEMORY; MICE; NEURONAL PLASTICITY; PHENOTYPE; STRESS DISORDERS, POST-TRAUMATIC;

EID: 84947778365     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2015.05.038     Document Type: Article

References (78)

1. Jaffee S.R., Price T.S. Gene-environment correlations: a review of the evidence and implications for prevention of mental illness. Mol. Psychiatry 2007, 12(5):432-442.
2. Kendler K.S., Eaves L.J. Models for the joint effect of genotype and environment on liability to psychiatric illness. Am. J. Psychiatry 1986, 143(3):279-289.
3. Stein M.B., Jang K.L., Taylor S., Vernon P.A., Livesley W.J. Genetic and environmental influences on trauma exposure and posttraumatic stress disorder symptoms: a twin study. Am. J. Psychiatry 2002, 159(10):1675-1681.
4. Goldberg J., True W.R., Eisen S.A., Henderson W.G. A twin study of the effects of the Vietnam War on posttraumatic stress disorder. JAMA 1990, 263(9):1227-1232.
5. Sartor C.E., et al. Common genetic and environmental contributions to post-traumatic stress disorder and alcohol dependence in young women. Psychol. Med. 2011, 41(7):1497-1505.
6. Yehuda R., et al. Parental posttraumatic stress disorder as a vulnerability factor for low cortisol trait in offspring of holocaust survivors. Arch. Gen. Psychiatry 2007, 64(9):1040-1048.
7. Berkowitz S.J., Stover C.S., Marans S.R. The Child and Family Traumatic Stress Intervention: secondary prevention for youth at risk of developing PTSD. J. Child Psychol. Psychiatry Allied Discip. 2011, 52(6):676-685.
8. Gauderman W.J. Sample size requirements for matched case-control studies of gene-environment interaction. Stat. Med. 2002, 21(1):35-50.
9. Hetherington M.M., Cecil J.E. Gene-environment interactions in obesity. Forum Nutr. 2010, 63:195-203.
10. Lau J.Y., Eley T.C. Gene-environment interactions and correlations in psychiatric disorders. Curr. Psychiatry Rep. 2004, 6(2):119-124.
11. Kolassa I.T., et al. Association study of trauma load and SLC6A4 promoter polymorphism in posttraumatic stress disorder: evidence from survivors of the Rwandan genocide. J. Clin. Psychiatry 2010, 71(5):543-547.
12. Siegmund A., Wotjak C.T. Toward an animal model of posttraumatic stress disorder. Ann. N.Y. Acad. Sci. 2006, 1071:324-334.
13. Wimer R.E., Wimer C.C., Roderick T.H. Genetic variability in forebrain structures between inbred strains of mice. Brain Res. 1969, 16(1):257-264.
14. Ammassari-Teule M., Passino E., Restivo L., de Marsanich B. Fear conditioning in C57/BL/6 and DBA/2 mice: variability in nucleus accumbens function according to the strain predisposition to show contextual- or cue-based responding. Eur. J. Neurosci. 2000, 12(12):4467-4474.
15. Airey D.C., Robbins A.I., Enzinger K.M., Wu F., Collins C.E. Variation in the cortical area map of C57BL/6J and DBA/2J inbred mice predicts strain identity. BMC Neurosci. 2005, 6:18.
16. Mandel P., Ayad G., Hermetet J.C., Ebel A. Correlation between choline acetyltransferase activity and learning ability in different mice strains and their offspring. Brain Res. 1974, 72(1):65-70.
17. Good R.L., Liang L.P., Patel M., Radcliffe R.A. Mouse strain- and age-dependent effects of binge methamphetamine on dopaminergic signaling. Neurotoxicology 2011, 32(6):751-759.
18. Fairless A.H., et al. Sociability and brain development in BALB/cJ and C57BL/6J mice. Behav. Brain Res. 2012, 228(2):299-310.
19. Papaleo F., Lipska B.K., Weinberger D.R. Mouse models of genetic effects on cognition: relevance to schizophrenia. Neuropharmacology 2012, 62(3):1204-1220.
20. Hammamieh R., et al. Murine model of repeated exposures to conspecific trained aggressors simulates features of post-traumatic stress disorder. Behav. Brain Res. 2012, 235(1):55-66.
21. Cho J.H., et al. Molecular evidence of stress-induced acute heart injury in a mouse model simulating posttraumatic stress disorder. Proc. Natl. Acad. Sci. U. S. A. 2014.
22. Seid Muhie A.G., James Meyerhoff, Nabarun Chakraborty, Rasha Hammamieh, Marti Jett Brain transcriptome profiles in mouse model simulating features of post-traumatic stress disorder. Mol. Brain 2015, 8.1:14. PMID: 25888136.
23. Gautam A., et al. Acute and chronic plasma metabolomic and liver transcriptomic stress effects in a mouse model with features of post-traumatic stress disorder. PLOS ONE 2015, 10(1):e0117092.
24. Krishnan V., et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 2007, 131(2):391-404.
25. Razzoli M., Carboni L., Andreoli M., Ballottari A., Arban R. Different susceptibility to social defeat stress of BalbC and C57BL6/J mice. Behav. Brain Res. 2011, 216(1):100-108.
26. Siegmund A., Wotjak C.T. A mouse model of posttraumatic stress disorder that distinguishes between conditioned and sensitised fear. J. Psychiatr. Res. 2007, 41(10):848-860.
27. Matar M.A., Zohar J., Cohen H. Translationally relevant modeling of PTSD in rodents. Cell Tissue Res. 2013, 354(1):127-139.
28. Szklarczyk K., Korostynski M., Golda S., Solecki W., Przewlocki R. Genotype-dependent consequences of traumatic stress in four inbred mouse strains. Genes Brain Behav. 2012.
29. Belzung C., El Hage W., Moindrot N., Griebel G. Behavioral and neurochemical changes following predatory stress in mice. Neuropharmacology 2001, 41(3):400-408.
30. Tang X., Orchard S.M., Sanford L.D. Home cage activity and behavioral performance in inbred and hybrid mice. Behav. Brain Res. 2002, 136(2):555-569.
31. Podhorna J., Brown R.E. Strain differences in activity and emotionality do not account for differences in learning and memory performance between C57BL/6 and DBA/2 mice. Genes Brain Behav. 2002, 1(2):96-110.
32. Hammamieh R., et al. Transcriptomic analysis of the effects of a fish oil enriched diet on murine brains. PLOS ONE 2014, 9(3):e90425.
33. Lumley L.A., Sipos M.L., Charles R.C., Charles R.F., Meyerhoff J.L. Social stress effects on territorial marking and ultrasonic vocalizations in mice. Physiol. Behav. 1999, 67(5):769-775.
34. Carola V., D'Olimpio F., Brunamonti E., Mangia F., Renzi P. Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Behav. Brain Res. 2002, 134(1-2):49-57.
35. Clement Y., et al. Anxiety in mice: a principal component analysis study. Neural Plas. 2007, 2007:35457.
36. Moura P.J., Meirelles S.T., Xavier G.F. Long-term social recognition memory in adult male rats: factor analysis of the social and non-social behaviors. Braz. J. Med. Biol. Res.=Revista brasileira de pesquisas medicas e biologicas/Sociedade Brasileira de Biofisica. . . [et al.] 2010, 43(7):663-676.
37. O'Leary T.P., Gunn R.K., Brown R.E. What are we measuring when we test strain differences in anxiety in mice?. Behav. Genet. 2013, 43(1):34-50.
38. Kanari K., Kikusui T., Takeuchi Y., Mori Y. Multidimensional structure of anxiety-related behavior in early-weaned rats. Behav. Brain Res. 2005, 156(1):45-52.
39. Tanaka S., Young J.W., Halberstadt A.L., Masten V.L., Geyer M.A. Four factors underlying mouse behavior in an open field. Behav. Brain Res. 2012, 233(1):55-61.
40. Lassance-Soares R.M., et al. Chronic stress impairs collateral blood flow recovery in aged mice. J. Cardiovasc. Transl. Res. 2014, 7(8):749-755.
41. Logan R.W., Nicole Edgar, Gillman A.G., Daniel Hoffman, Xiyu Zhu, McClung C.A. Chronic stress induces brain region specific alterations of molecular rhythms in mice that correlate with depression-like behavior. Biol. Psychiatry 2015, PMID: 25771506, (Epub ahead of print).
42. Koolhaas J.M., et al. Stress revisited: a critical evaluation of the stress concept. Neurosci. Biobehav. Rev. 2011, 35(5):1291-1301.
43. Philbert J., et al. Acute inescapable stress exposure induces long-term sleep disturbances and avoidance behavior: a mouse model of post-traumatic stress disorder (PTSD). Behav. Brain Res. 2011, 221(1):149-154.
44. Sankoorikal G.M., Kaercher K.A., Boon C.J., Lee J.K., Brodkin E.S. A mouse model system for genetic analysis of sociability: C57BL/6J versus BALB/cJ inbred mouse strains. Biol. Psychiatry 2006, 59(5):415-423.
45. Tucci V., et al. Gene-environment interactions differentially affect mouse strain behavioral parameters. Mamm. Genome 2006, 17(11):1113-1120.
46. Holmes A., et al. Early life genetic, epigenetic and environmental factors shaping emotionality in rodents. Neurosci. Biobehav. Rev. 2005, 29(8):1335-1346.
47. Barnabei M.S., Palpant N.J., Metzger J.M. Influence of genetic background on ex vivo and in vivo cardiac function in several commonly used inbred mouse strains. Physiol. Genomics 2010, 42A(2):103-113.
48. Takano T., et al. Cortical spreading depression causes and coincides with tissue hypoxia. Nat. Neurosci. 2007, 10(6):754-762.
49. Rasmusson A.M., Schnurr P.P., Zukowska Z., Scioli E., Forman D.E. Adaptation to extreme stress: post-traumatic stress disorder, neuropeptide Y and metabolic syndrome. Exp. Biol. Med. 2010, 235(10):1150-1162.
50. Kubzansky L.D., Koenen K.C. Is post-traumatic stress disorder related to development of heart disease?. Future Cardiol. 2007, 3(2):153-156.
51. Association AP Diagnostic Criteria from DSM-IV 1994, The Association, Washington, DC.
52. Pamplona F.A., et al. Prolonged fear incubation leads to generalized avoidance behavior in mice. J. Psychiatr. Res. 2011, 45(3):354-360.
53. Kalueff A.V., Tuohimaa P. Experimental modeling of anxiety and depression. Acta Neurobiol. Exp. (Wars.) 2004, 64(4):439-448.
54. Golub Y., et al. Reduced hippocampus volume in the mouse model of posttraumatic stress disorder. J. Psychiatr. Res. 2011, 45(5):650-659.
55. Hauck S., et al. Serum brain-derived neurotrophic factor in patients with trauma psychopathology. Prog. Neuro-psychopharmacol. Biol. Psychiatry 2010, 34(3):459-462.
56. Binder E.B., et al. Association of FKBP5 polymorphisms and childhood abuse with risk of posttraumatic stress disorder symptoms in adults. JAMA 2008, 299(11):1291-1305.
57. Boscarino J.A., Erlich P.M., Hoffman S.N., Zhang X. Higher FKBP5, COMT, CHRNA5, and CRHR1 allele burdens are associated with PTSD and interact with trauma exposure: implications for neuropsychiatric research and treatment. Neuropsychiatr. Dis. Treat. 2012, 8:131-139.
58. Kilpatrick D.G., et al. The serotonin transporter genotype and social support and moderation of posttraumatic stress disorder and depression in hurricane-exposed adults. Am. J. Psychiatry 2007, 164(11):1693-1699.
59. Muinos-Gimeno M., et al. Human microRNAs miR-22, miR-138-2, miR-148a, and miR-488 are associated with panic disorder and regulate several anxiety candidate genes and related pathways. Biol. Psychiatry 2011, 69(6):526-533.
60. Zagrebelsky M., et al. The p75 neurotrophin receptor negatively modulates dendrite complexity and spine density in hippocampal neurons. J. Neurosci. 2005, 25(43):9989-9999.
61. Woo N.H., et al. Activation of p75NTR by proBDNF facilitates hippocampal long-term depression. Nat. Neurosci. 2005, 8(8):1069-1077.
62. Alzoubi K.H., Khabour O.F., Salah H.A., Abu Rashid B.E. The combined effect of sleep deprivation and Western diet on spatial learning and memory: role of BDNF and oxidative stress. J. Mol. Neurosci. 2013, 50(1):124-133.
63. Kozlovsky N., et al. Long-term down-regulation of BDNF mRNA in rat hippocampal CA1 subregion correlates with PTSD-like behavioural stress response. Int. J. Neuropsychopharmacol. 2007, 10(6):741-758.
64. Pizarro J.M., et al. Acute social defeat reduces neurotrophin expression in brain cortical and subcortical areas in mice. Brain Res. 2004, 1025(1-2):10-20.
65. Berry A., et al. Social deprivation stress is a triggering factor for the emergence of anxiety- and depression-like behaviours and leads to reduced brain BDNF levels in C57BL/6J mice. Psychoneuroendocrinology 2012, 37(6):762-772.
66. Takei S., et al. Enhanced hippocampal BDNF/TrkB signaling in response to fear conditioning in an animal model of posttraumatic stress disorder. J. Psychiatr. Res. 2011, 45(4):460-468.
67. Terry A.V., Kutiyanawalla A., Pillai A. Age-dependent alterations in nerve growth factor (NGF)-related proteins, sortilin, and learning and memory in rats. Physiol. Behav. 2011, 102(2):149-157.
68. Yee B.K., Zhu S.W., Mohammed A.H., Feldon J. Levels of neurotrophic factors in the hippocampus and amygdala correlate with anxiety- and fear-related behaviour in C57BL6 mice. J. Neural Transm. 2007, 114(4):431-444.
69. Endo H., Ikeda K., Urano T., Horie-Inoue K., Inoue S. Terf/TRIM17 stimulates degradation of kinetochore protein ZWINT and regulates cell proliferation. J. Biochem. 2012, 151(2):139-144.
70. Dai C., et al. Functional identification of neuroprotective molecules. PLoS ONE 2010, 5(11):e15008.
71. Binder E.B. The role of FKBP5, a co-chaperone of the glucocorticoid receptor in the pathogenesis and therapy of affective and anxiety disorders. Psychoneuroendocrinology 2009, 34(Suppl. 1):S186-S195.
72. Hartmann J., et al. The involvement of FK506-binding protein 51 (FKBP5) in the behavioral and neuroendocrine effects of chronic social defeat stress. Neuropharmacology 2012, 62(1):332-339.
73. Gale G.D., et al. A genome-wide panel of congenic mice reveals widespread epistasis of behavior quantitative trait loci. Mol. Psychiatry 2009, 14(6):631-645.
74. Han H.J., et al. Strain background influences neurotoxicity and behavioral abnormalities in mice expressing the tetracycline transactivator. J. Neurosci. 2012, 32(31):10574-10586.
75. Vergnes M., Depaulis A., Boehrer A. Parachlorophenylalanine-induced serotonin depletion increases offensive but not defensive aggression in male rats. Physiol. Behav. 1986, 36(4):653-658.
76. Miyasaka K., et al. Anxiety-related behaviors in cholecystokinin-A, B, and AB receptor gene knockout mice in the plus-maze. Neurosci. Lett. 2002, 335(2):115-118.
77. Chen Q., Nakajima A., Meacham C., Tang Y.P. Elevated cholecystokininergic tone constitutes an important molecular/neuronal mechanism for the expression of anxiety in the mouse. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(10):3881-3886.
78. Bartolomucci A., et al. Increased vulnerability to psychosocial stress in heterozygous serotonin transporter knockout mice. Dis. Model. Mech. 2010, 3(7-8):459-470.