Pathological brain plasticity and cognition in the offspring of males subjected to postnatal traumatic stress

Molecular Psychiatry

Volumn 20, Issue 5, 2015, Pages 621-631

  Bohacek, J ^a   Farinelli, M ^a   Mirante, O ^a   Steiner, G ^b   Gapp, K ^a   Coiret, G ^a   Ebeling, M ^b   Duran Pacheco G ^b   Iniguez, A L ^c   Manuella, F ^a   Moreau, J L ^b   Mansuy, I M ^a  

^a University of Zurich Brain Research Institute   (Switzerland)

^b F HOFFMANN LA ROCHE LTD   (Switzerland)

^c Roche NimbleGen Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE C GAMMA; TRANSCRIPTION FACTOR; PROTEIN KINASE C;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; COGNITION; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; FATHER; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; LONG TERM DEPRESSION; LONG TERM MEMORY; LONG TERM POTENTIATION; MALE; MOUSE; MUTATION; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; PROGENY; PROMOTER REGION; SPERM; ANIMAL; BRAIN; C57BL MOUSE; COGNITION DISORDERS; COMPLICATION; CONDITIONING; CYTOLOGY; FEAR; GENETIC EPIGENESIS; GENETICS; IN VITRO STUDY; METABOLISM; NEWBORN; PATHOLOGY; PHYSIOLOGY; PSYCHOLOGY; RECOGNITION; SWIMMING;

ANIMALS; ANIMALS, NEWBORN; BRAIN; COGNITION DISORDERS; CONDITIONING (PSYCHOLOGY); DNA METHYLATION; EPIGENESIS, GENETIC; FEAR; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; IN VITRO TECHNIQUES; LONG-TERM POTENTIATION; MALE; MICE; MICE, INBRED C57BL; NEURONAL PLASTICITY; PROTEIN KINASE C; RECOGNITION (PSYCHOLOGY); STRESS DISORDERS, TRAUMATIC; SWIMMING;

EID: 84929131136     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2014.80     Document Type: Article

References (79)

1. Schafer I, Fisher HL Childhood trauma and psychosis-what is the evidence?. Dialogues Clin Neurosci 2011; 13: 360-365
2. Norman RE, Byambaa M, De R, Butchart A, Scott J, Vos T The long-Term health consequences of child physical abuse, emotional abuse, and neglect: a systematic review and meta-Analysis. PLoS Med 2012; 9: e1001349
3. U.S. Department of Health and Human Services Administration on Children, Youth and Families, Childrens Bureau. (2012). Child Maltreatment 2011
4. Gilbert R, Widom CS, Browne K, Fergusson D, Webb E, Janson S Burden and consequences of child maltreatment in high-income countries. Lancet 2009; 373: 68-81
5. Lampe A The prevalence of childhood sexual abuse, physical abuse and emotional neglect in Europe. Z Psychosom Med Psychother 2002; 48: 370-380
6. Schönbucher V, Maier T, Held L, Mohler-Kuo M, Schnyder U, Landolt MA Prevalence of child sexual abuse in Switzerland: a systematic review. Swiss Med Wkly 2011; 140: w13123
7. Weiss IC, Franklin TB, Vizi S, Mansuy IM Inheritable effect of unpredictable maternal separation on behavioral responses in mice. Front Behav Neurosci 2011; 5: 3
8. Franklin TB, Russig H, Weiss IC, Gräff J, Linder N, Michalon A, et al. Epigenetic transmission of the impact of early stress across generations. Biol Psychiatry 2010; 68: 408-415
9. Franklin TB, Linder N, Russig H, Thöny B, Mansuy IM Influence of early stress on social abilities and serotonergic functions across generations in mice. PLoS ONE 2011; 6: e21842
10. Gapp K, Jawaid A, Sarkies P, Bohacek J, Pelczar P, Prados J, et al. Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat Neurosci 2014; 17: 667-669
11. Bohacek J, Mansuy IM Epigenetic inheritance of disease and disease risk. Neuropsychopharmacology 2013; 38: 220-236
12. Bohacek J, Gapp K, Saab BJ, Mansuy IM Transgenerational epigenetic effects on brain functions. Biol Psychiatry 2012; 73: 313-320
13. Pechtel P, Pizzagalli DA Effects of early life stress on cognitive and affective function: an integrated review of human literature. Psychopharmacology 2011; 214: 55-70
14. Arts B, Jabben N, Krabbendam L, van Os J Meta-Analyses of cognitive functioning in euthymic bipolar patients and their first-degree relatives. Psychol Med 2008; 38: 771-785
15. McClintock SM, Husain MM, Greer TL, Cullum CM Association between depression severity and neurocognitive function in major depressive disorder: a review and synthesis. Neuropsychology 2010; 24: 9-34
16. Gould F, Clarke J, Heim C, Harvey PD, Majer M, Nemeroff CB The effects of child abuse and neglect on cognitive functioning in adulthood. J Psychiatr Res 2012; 46: 500-506
17. McEwen BS, Gianaros PJ Central role of the brain in stress and adaptation: links to socioeconomic status, health, and disease. Ann NY Acad Sci 2010; 1186: 190-222
18. Kim JJ, Diamond DM The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 2002; 3: 453-462
19. Wang X-D, Rammes G, Kraev I, Wolf M, Liebl C, Scharf SH, et al. Forebrain CRF1 modulates early-life stress-programmed cognitive deficits. J Neurosci 2011; 31: 13625-13634
20. Ivy AS, Rex CS, Chen Y, Dubé C, Maras PM, Grigoriadis DE, et al. Hippocampal dysfunction and cognitive impairments provoked by chronic early-life stress involve excessive activation of CRH receptors. J Neurosci 2010; 30: 13005-13015
21. Murgatroyd C, Patchev AV, Wu Y, Micale V, Bockmühl Y, Fischer D, et al. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci 2009; 12: 1559-1566
22. Abeliovich A, Paylor R, Chen C, Kim JJ, Wehner JM, Tonegawa S.PKC gamma mutant mice exhibit mild deficits in spatial and contextual learning. Cell 1993; 75: 1263-1271
23. Abeliovich A, Chen C, Goda Y, Silva AJ, Stevens CF, Tonegawa S Modified hippocampal long-Term potentiation in PKC gamma-mutant mice. Cell 1993; 75: 1253-1262
24. Hickman DL, Swan MP Effects of age of pups and removal of existing litter on pup survival during cross-fostering between multiparous outbred mice. J Am Assoc Lab Anim Sci 2011; 50: 641-646
25. Bolstad BM, Irizarry RA, Astrand M, Speed TP A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003; 19: 185-193
26. Smyth GK Bioinformatics and Computational Biology Solutions using R and Bioconductor (Gentleman R, Carey V, Dudoit S, Irizarry RA, Huber W). Springer, 2005, pp 397-420
27. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005; 102: 15545-15550
28. Nam D, Kim SY Gene-set approach for expression pattern analysis. Brief Bioinform 2008; 9: 189-197
29. Cerami EG, Gross BE, Demir E, Rodchenkov I, Babur O, Anwar N, et al. Pathway Commons, a web resource for biological pathway data. Nucleic Acids Res 2011; 39: D685-D690
30. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 2007; 35: W71-W74
31. Arvidsson S, Kwasniewski M, Riaño-Pachón DM, Mueller-Roeber B QuantPrime-A flexible tool for reliable high-Throughput primer design for quantitative PCR. BMC Bioinformatics 2008; 9: 465
32. Knobloch M, Farinelli M, Konietzko U, Nitsch RM, Mansuy IM Abeta oligomermediated long-Term potentiation impairment involves protein phosphatase 1-dependent mechanisms. J Neurosci 2007; 27: 7648-7653
33. Humeau Y, Shaban H, Bissiere S, Luthi A Presynaptic induction of heterosynaptic associative plasticity in the mammalian brain. Nature 2003; 426: 841-845
34. Daniel JM, Bohacek J The critical period hypothesis of estrogen effects on cognition: insights from basic research. Biochim Biophys Acta 2010; 1800: 1068-1076
35. Genoux D, Haditsch U, Knobloch M, Michalon A, Storm D, Mansuy IM Protein phosphatase 1 is a molecular constraint on learning and memory. Nature 2002; 418: 970-975
36. Small SA, Schobel SA, Buxton RB, Witter MP, Barnes CA A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat Rev Neurosci 2011; 12: 585-601
37. Gray JD, Rubin TG, Hunter RG, McEwen BS. Hippocampal gene expression changes underlying stress sensitization and recovery. Mol Psychiatry advance online publication, 17 December 2013; doi: 10.1038/mp.2013.175
38. Huang YY, Kandel ER Recruitment of long-lasting and protein kinase A-dependent long-Term potentiation in the CA1 region of hippocampus requires repeated tetanization. Learn Mem 1994; 1: 74-82
39. Schulz PE, Cook EP, Johnston D Changes in paired-pulse facilitation suggest presynaptic involvement in long-Term potentiation. J Neurosci 1994; 14: 5325-5337
40. Takanaga H, Mukai H, Shimakawa M, Konishi H, Kikkawa U, Koizumi T, et al. Functional characterization of the promoter region of the mouse protein kinase C gamma gene. FEBS Lett 1995; 368: 276-278
41. Chen KH, Widen SG, Wilson SH, Huang KP Characterization of the 5'-flanking region of the rat protein kinase C gamma gene. J Biol Chem 1990; 265: 19961-19965
42. Li L, Davie Jr. The role of Sp1 and Sp3 in normal and cancer cell biology. Ann Anat 2010; 192: 275-283
43. Lupien SJ, McEwen BS, Gunnar MR, Heim C Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 2009; 10: 434-445
44. Hedges DW, Woon FL. Early-life stress and cognitive outcome. Psychopharmacology 2011; 214: 121-130
45. Roceri M, Hendriks W, Racagni G, Ellenbroek BA, Riva MA. Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Mol Psychiatry 2002; 7: 609-616
46. Pickering C, Gustafsson L, Cebere A, Nylander I, Liljequist S. Repeated maternal separation of male Wistar rats alters glutamate receptor expression in the hippocampus but not the prefrontal cortex. Brain Res 2006; 1099: 101-108
47. Ryan B, Musazzi L, Mallei A, Tardito D, Gruber SH, El Khoury A, et al. Remodelling by early-life stress of NMDA receptor-dependent synaptic plasticity in a geneenvironment rat model of depression. Int J Neuropsychopharmacol 2009; 12: 553-559
48. Kandel ER. The molecular biology of memory storage: a dialogue between genes and synapses. Science 2001; 294: 1030-1038
49. Lisman J, Yasuda R, Raghavachari S. Mechanisms of CaMKII action in long-Term potentiation. Nat Rev Neurosci 2012; 13: 169-182
50. Li S, Tian X, Hartley DM, Feig LA. Distinct roles for Ras-guanine nucleotidereleasing factor 1 (Ras-GRF1) and Ras-GRF2 in the induction of long-Term potentiation and long-Term depression. J Neurosci 2006; 26: 1721-1729
51. Xu L, Anwyl R, Rowan MJ. Behavioural stress facilitates the induction of long-Term depression in the hippocampus. Nature 1997; 387: 497-500
52. Yang C-H, Huang C-C, Hsu K-S. Behavioral stress enhances hippocampal CA1 longterm depression through the blockade of the glutamate uptake. J Neurosci 2005; 25: 4288-4293
53. Kim JJ, Foy MR, Thompson RF. Behavioral stress modifies hippocampal plasticity through N-methyl-D-Aspartate receptor activation. Proc Natl Acad Sci USA 1996; 93: 4750-4753
54. Artola A, von Frijtag JC, Fermont PC, Gispen WH, Schrama LH, Kamal A, et al. Long-lasting modulation of the induction of LTD and LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment. Eur J Neurosci 2006; 23: 261-272
55. Rioult-Pedotti MS, Donoghue JP, Dunaevsky A. Plasticity of the synaptic modification range. J Neurophysiol 2007; 98: 3688-3695
56. Dudek SM, Bear MF. Homosynaptic long-Term depression in area CA1 of hippocampus and effects of N-methyl-D-Aspartate receptor blockade. Proc Natl Acad Sci USA 1992; 89: 4363-4367
57. Bienenstock EL, Cooper LN, Munro PW. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 1982; 2: 32-48
58. Danielewicz J, Hess G. Early life stress alters synaptic modification range in the rat lateral amygdala. Behav Brain Res 2014; 265C: 32-37
59. Rodgers AB, Morgan CP, Bronson SL, Revello S, Bale TL. Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. J Neurosci 2013; 33: 9003-9012
60. Aisa B, Tordera R, Lasheras B, Del Río J, Ramírez MJ. Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 2007; 32: 256-266
61. Batalha VL, Pego JM, Fontinha BM, Costenla AR, Valadas JS, Baqi Y, et al. Adenosine A2A receptor blockade reverts hippocampal stress-induced deficits and restores corticosterone circadian oscillation. Mol Psychiatry 2012; 18: 320-331
62. Saavedra-Rodríguez L, Feig LA. Chronic social instability induces anxiety and defective social interactions across generations. Biol Psychiatry 2013; 73: 44-53
63. Arai JA, Li S, Hartley DM, Feig LA. Transgenerational rescue of a genetic defect in long-Term potentiation and memory formation by juvenile enrichment. J Neurosci 2009; 29: 1496-1502
64. Dunn GA, Morgan CP, Bale TL. Sex-specificity in transgenerational epigenetic programming. Horm Behav 2011; 59: 290-295
65. Morgan CP, Bale TL. Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage. J Neurosci 2011; 31: 11748-11755
66. Dietz DM, Laplant Q, Watts EL, Hodes GE, Russo SJ, Feng J, et al. Paternal transmission of stress-induced pathologies. Biol Psychiatry 2011; 70: 408-414
67. Guerrero-Bosagna C, Settles M, Lucker B, Skinner MK. Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS ONE 2010; 5: e13100
68. Wolstenholme JT, Edwards M, Shetty SR, Gatewood JD, Taylor JA, Rissman EF, et al. Gestational exposure to bisphenol a produces transgenerational changes in behaviors and gene expression. Endocrinology 2012; 153: 3828-3838
69. Dunn GA, Bale TL. Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 2011; 152: 2228-2236
70. Carone BR, Fauquier L, Habib N, Shea JM, Hart CE, Li R, et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 2010; 143: 1084-1096
71. Vassoler FM, White SL, Schmidt HD, Sadri-Vakili G, Pierce RC. Epigenetic inheritance of a cocaine-resistance phenotype. Nat Neurosci 2013; 16: 42-47
72. Gapp K, von Ziegler L, Tweedie-Cullen RY, Mansuy IM. Early life epigenetic programming and transmission of stress-induced traits in mammals: how and when can environmental factors influence traits and their transgenerational inheritance? Bioessays 2014; 36: 491-502
73. Curley JP, Mashoodh R. Parent-of-origin and trans-generational germline influences on behavioral development: the interacting roles of mothers, fathers, and grandparents. Dev Psychobiol 2010; 52: 312-330
74. Gowaty PA, Anderson WW, Bluhm CK, Drickamer LC, Kim YK, Moore AJ, et al. The hypothesis of reproductive compensation and its assumptions about mate preferences and offspring viability. Proc Natl Acad Sci USA 2007; 104: 15023-15027
75. Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet 2007; 8: 253-262
76. Davies G, Tenesa A, Payton A, Yang J, Harris SE, Liewald D, et al. Genome-wide association studies establish that human intelligence is highly heritable and polygenic. Mol Psychiatry 2011; 16: 996-1005
77. Nisbett RE, Aronson J, Blair C, Dickens W, Flynn J, Halpern DF, et al. Intelligence: new findings and theoretical developments. Am Psychol 2012; 67: 130-159
78. Deary I, Johnson W, Houlihan LM. Genetic foundations of human intelligence. Hum Genet 2009; 126: 215-232
79. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, et al. Finding the missing heritability of complex diseases. Nature 2009; 461: 747-753