The potential of epigenetics in stress-enhanced fear learning models of PTSD

Learning and Memory

Volumn 23, Issue 10, 2016, Pages 576-586

  Blouin, Ashley M ^a   Sillivan, Stephanie E ^a   Joseph, Nadine F ^a   Miller, Courtney A ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL MODEL; EPIGENETICS; FEAR; HUMAN; LEARNING; MEMORY; MENTAL STRESS; NEUROMODULATION; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; REVIEW; ANIMAL; DISEASE MODEL; GENETIC EPIGENESIS; GENETICS; METABOLISM;

ANIMALS; DISEASE MODELS, ANIMAL; EPIGENESIS, GENETIC; HUMANS; STRESS DISORDERS, POST-TRAUMATIC;

EID: 84992161348     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.040485.115     Document Type: Review

References (168)

1. Akirav I, Maroun M. 2007. The role of the medial prefrontal cortex-Amygdala circuit in stress effects on the extinction of fear. Neural Plast 2007: 30873.
2. Akirav I, Segev A, Motanis H, Maroun M. 2009. D-cycloserine into the BLA reverses the impairing effects of exposure to stress on the extinction of contextual fear, but not conditioned taste aversion. Learn Memory 16: 682-686.
3. Alberini CM. 2005. Mechanisms of memory stabilization: are consolidation and reconsolidation similar or distinct processes? Trends Neurosci 28: 51-56.
4. Alberini CM, Ledoux JE. 2013. Memory reconsolidation. Curr Biol 23: R746-R750.
5. Albucher RC, Liberzon I. 2002. Psychopharmacological treatment in PTSD: a critical review. J Psychiatr Res 36: 355-367.
6. Andero R, Brothers SP, Jovanovic T, Chen YT, Salah-Uddin H, Cameron M, Bannister TD, Almli L, Stevens JS, Bradley B, et al. 2013. Amygdala-dependent fear is regulated by Oprl1 in mice and humans with PTSD. Sci Transl Med 5: 188ra173.
7. Andero R, Heldt SA, Ye K, Liu X, Armario A, Ressler KJ. 2011. Effect of 7,8-dihydroxyflavone, a small-molecule TrkB agonist, on emotional learning. Am J Psychiatry 168: 163-172.
8. Bahari-Javan S, Maddalena A, Kerimoglu C, Wittnam J, Held T, Bahr M, Burkhardt S, Delalle I, Kugler S, Fischer A, et al. 2012. HDAC1 regulates fear extinction in mice. J Neurosci 32: 5062-5073.
9. Baker-Andresen D, Flavell CR, Li X, Bredy TW. 2013. Activation of BDNF signaling prevents the return of fear in female mice. Learn Memory 20: 237-240.
10. Baratta MV, Kodandaramaiah SB, Monahan PE, Yao J, Weber MD, Lin PA, Gisabella B, Petrossian N, Amat J, Kim K, et al. 2015. Stress enables reinforcement-elicited serotonergic consolidation of fear memory. Biol Psychiatry 79: 814-822.
11. Baumgartel K, Genoux D, Welzl H, Tweedie-Cullen RY, Koshibu K, Livingstone-Zatchej M, Mamie C, Mansuy IM. 2008. Control of the establishment of aversive memory by calcineurin and Zif268. Nat Neurosci 11: 572-578.
12. Bilang-Bleuel A, Ulbricht S, Chandramohan Y, De Carli S, Droste SK, Reul JM. 2005. Psychological stress increases histone H3 phosphorylation in adult dentate gyrus granule neurons: involvement in a glucocorticoid receptor-dependent behavioural response. Eur J Neurosci 22: 1691-1700.
13. Blechert J, Michael T, Vriends N, Margraf J, Wilhelm FH. 2007. Fear conditioning in posttraumatic stress disorder: evidence for delayed extinction of autonomic, experiential, and behavioural responses. Behav Res Ther 45: 2019-2033.
14. Bousiges O, Neidl R, Majchrzak M, Muller MA, Barbelivien A, Pereira de Vasconcelos A, Schneider A, Loeffler JP, Cassel JC, Boutillier AL. 2013. Detection of histone acetylation levels in the dorsal hippocampus reveals early tagging on specific residues of H2B and H4 histones in response to learning. PLoS One 8: e57816.
15. Bouton ME. 2002. Context, ambiguity, and unlearning: sources of relapse after behavioral extinction. Biol Psychiatry 52: 976-986.
16. Bowen MT, Dass SA, Booth J, Suraev A, Vyas A, McGregor IS. 2014. Active coping toward predatory stress is associated with lower corticosterone and progesterone plasma levels and decreased methylation in the medial amygdala vasopressin system. Horm Behav 66: 561-566.
17. Bramham CR, Panja D. 2014. BDNF regulation of synaptic structure, function, and plasticity. Neuropharmacology 76(Pt C): 601-602.
18. Bredy TW, Barad M. 2008. The histone deacetylase inhibitor valproic acid enhances acquisition, extinction, and reconsolidation of conditioned fear. Learn Mem 15: 39-45.
19. Bredy TW, Wu H, Crego C, Zellhoefer J, Sun YE, Barad M. 2007. Histone modifications around individual BDNF gene promoters in prefrontal cortex are associated with extinction of conditioned fear. Learn Mem 14: 268-276.
20. Brennan FX, Beck KD, Ross RJ, Servatius RJ. 2005. Stress-induced increases in avoidance responding: an animal model of post-traumatic stress disorder behavior? Neuropsychiatr Dis Treat 1: 69-72.
21. Brennan FX, Beck KD, Servatius RJ. 2006. Predator odor exposure facilitates acquisition of a leverpress avoidance response in rats. Neuropsychiatr Dis Treat 2: 65-69.
22. Breslau N, Koenen KC, Luo Z, Agnew-Blais J, Swanson S, Houts RM, Poulton R, Moffitt TE. 2014. Childhood maltreatment, juvenile disorders and adult post-traumatic stress disorder: a prospective investigation. Psychol Med 44: 1937-1945.
23. Callaghan BL, Graham BM, Li S, Richardson R. 2013. From resilience to vulnerability: mechanistic insights into the effects of stress on transitions in critical period plasticity. Front Psychiatry 4: 90.
24. Chauveau F, Lange MD, Jungling K, Lesting J, Seidenbecher T, Pape HC. 2012. Prevention of stress-impaired fear extinction through neuropeptide s action in the lateral amygdala. Neuropsychopharmacology 37: 1588-1599.
25. Chertkow-Deutsher Y, Cohen H, Klein E, Ben-Shachar D. 2010. DNA methylation in vulnerability to post-traumatic stress in rats: evidence for the role of the post-synaptic density protein Dlgap2. Int J Neuropsychopharmacol 13: 347-359.
26. Cordero MI, Venero C, Kruyt ND, Sandi C. 2003. Prior exposure to a single stress session facilitates subsequent contextual fear conditioning in rats. Evidence for a role of corticosterone. Horm Behav 44: 338-345.
27. Dalla C, Shors TJ. 2009. Sex differences in learning processes of classical and operant conditioning. Physiol Behav 97: 229-238.
28. Daskalakis NP, Bagot RC, Parker KJ, Vinkers CH, de Kloet ER. 2013. The three-hit concept of vulnerability and resilience: toward understanding adaptation to early-life adversity outcome. Psychoneuroendocrinology 38: 1858-1873.
29. Debiec J, Ledoux JE. 2004. Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala. Neuroscience 129: 267-272.
30. de Kleine RA, Smits JA, Hendriks GJ, Becker ES, van Minnen A. 2015. Extinction learning as a moderator of d-cycloserine efficacy for enhancing exposure therapy in posttraumatic stress disorder. J Anxiety Disord 34: 63-67.
31. Dell'Osso L, Carmassi C, Del Debbio A, Catena Dell'Osso M, Bianchi C, da Pozzo E, Origlia N, Domenici L, Massimetti G, Marazziti D, et al. 2009. Brain-derived neurotrophic factor plasma levels in patients suffering from post-traumatic stress disorder. Prog Neuropsychopharmacol Biol Psychiatry 33: 899-902.
32. Dubreucq S, Matias I, Cardinal P, Haring M, Lutz B, Marsicano G, Chaouloff F. 2012. Genetic dissection of the role of cannabinoid type-1 receptors in the emotional consequences of repeated social stress in mice. Neuropsychopharmacology 37: 1885-1900.
33. Forcato C, Rodriguez ML, Pedreira ME. 2011. Repeated labilization-reconsolidation processes strengthen declarative memory in humans. PLoS One 6: e23305.
34. Fuchikami M, Yamamoto S, Morinobu S, Takei S, Yamawaki S. 2010. Epigenetic regulation of BDNF gene in response to stress. Psychiatry Investig 7: 251-256.
35. Fukada M, Hanai A, Nakayama A, Suzuki T, Miyata N, Rodriguiz RM, Wetsel WC, Yao TP, Kawaguchi Y. 2012. Loss of deacetylation activity of Hdac6 affects emotional behavior in mice. PLoS One 7: e30924.
36. Furukawa-Hibi Y, Nagai T, Yun J, Yamada K. 2015. Stress increases DNA methylation of the neuronal PAS domain 4 (Npas4) gene. Neuroreport 26: 827-832.
37. Garfinkel SN, Abelson JL, King AP, Sripada RK, Wang X, Gaines LM, Liberzon I. 2014. Impaired contextual modulation of memories in PTSD: an fMRI and psychophysiological study of extinction retention and fear renewal. J Neurosci 34: 13435-13443.
38. Glover EM, Jovanovic T, Norrholm SD. 2015. Estrogen and extinction of fear memories: implications for posttraumatic stress disorder treatment. Biol Psychiatry 78: 178-185.
39. Gräff J, Joseph NF, Horn ME, Samiei A, Meng J, Seo J, Rei D, Bero AW, Phan TX, Wagner F, et al. 2014. Epigenetic priming of memory updating during reconsolidation to attenuate remote fear memories. Cell 156: 261-276.
40. Grillon C. 2002. Startle reactivity and anxiety disorders: aversive conditioning, context, and neurobiology. Biol Psychiatry 52: 958-975.
41. Guan JS, Haggarty SJ, Giacometti E, Dannenberg JH, Joseph N, Gao J, Nieland TJ, Zhou Y, Wang X, Mazitschek R, et al. 2009. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459: 55-60.
42. Gudsnuk K, Champagne FA. 2012. Epigenetic influence of stress and the social environment. ILAR J 53: 279-288.
43. Guo JU, Su Y, Zhong C, Ming GL, Song H. 2011. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 145: 423-434.
44. Gupta S, Kim SY, Artis S, Molfese DL, Schumacher A, Sweatt JD, Paylor RE, Lubin FD. 2010. Histone methylation regulates memory formation. J Neurosci 30: 3589-3599.
45. Halder R, Hennion M, Vidal RO, Shomroni O, Rahman RU, Rajput A, Centeno TP, van Bebber F, Capece V, Garcia Vizcaino JC, et al. 2016. DNA methylation changes in plasticity genes accompany the formation and maintenance of memory. Nat Neurosci 19: 102-110.
46. Han A, Sung YB, Chung SY, Kwon MS. 2014. Possible additional antidepressant-like mechanism of sodium butyrate: targeting the hippocampus. Neuropharmacology 81: 292-302.
47. Hauck S, Kapczinski F, Roesler R, de Moura Silveira E Jr., Magalhaes PV, Kruel LR, Schestatsky SS, Ceitlin LH. 2010. Serum brain-derived neurotrophic factor in patients with trauma psychopathology. Prog Neuropsychopharmacol Biol Psychiatry 34: 459-462.
48. Herzog CJ, Miot S, Mansuy IM, Giros B, Tzavara ET. 2008. Chronic valproate normalizes behavior in mice overexpressing calcineurin. Eur J Pharmacol 580: 153-160.
49. Hodes GE, Pfau ML, Purushothaman I, Ahn HF, Golden SA, Christoffel DJ, Magida J, Brancato A, Takahashi A, Flanigan ME, et al. 2015. Sex differences in nucleus accumbens transcriptome profiles associated with susceptibility versus resilience to subchronic variable stress. J Neurosci 35: 16362-16376.
50. Hunter RG, McCarthy KJ, Milne TA, Pfaff DW, McEwen BS. 2009. Regulation of hippocampal H3 histone methylation by acute and chronic stress. Proc Natl Acad Sci 106: 20912-20917.
51. Ieraci A, Mallei A, Musazzi L, Popoli M. 2015. Physical exercise and acute restraint stress differentially modulate hippocampal brain-derived neurotrophic factor transcripts and epigenetic mechanisms in mice. Hippocampus 25: 1380-1392.
52. Ishii D, Matsuzawa D, Matsuda S, Tomizawa H, Sutoh C, Shimizu E. 2014. Methyl donor-deficient diet during development can affect fear and anxiety in adulthood in C57BL/6J mice. PLoS One 9: e105750.
53. Iwamoto Y, Morinobu S, Takahashi T, Yamawaki S. 2007. Single prolonged stress increases contextual freezing and the expression of glycine transporter 1 and vesicle-Associated membrane protein 2 mRNA in the hippocampus of rats. Prog Neuropsychopharmacol Biol Psychiatry 31: 642-651.
54. Izquierdo A, Wellman CL, Holmes A. 2006. Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice. J Neurosci 26: 5733-5738.
55. Jones CE, Monfils M-H. 2016. Fight, flight, or freeze? The answer may depend on your sex. Trends Neurosci 39: 51-53.
56. Jones ME, Lebonville CL, Barrus D, Lysle DT. 2015. The role of brain interleukin-1 in stress-enhanced fear learning. Neuropsychopharmacology 40: 1289-1296.
57. Kaas GA, Zhong C, Eason DE, Ross DL, Vachhani RV, Ming GL, King JR, Song H, Sweatt JD. 2013. TET1 controls CNS 5-methylcytosine hydroxylation, active DNA demethylation, gene transcription, and memory formation. Neuron 79: 1086-1093.
58. Karpova NN. 2014. Role of BDNF epigenetics in activity-dependent neuronal plasticity. Neuropharmacology 76(Pt C): 709-718.
59. Kessler RC, Chiu WT, Demler O, Merikangas KR, Walters EE. 2005. Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 62: 617-627.
60. Khan S, Liberzon I. 2004. Topiramate attenuates exaggerated acoustic startle in an animal model of PTSD. Psychopharmacology (Berl) 172: 225-229.
61. Kim JK, Samaranayake M, Pradhan S. 2009. Epigenetic mechanisms in mammals. Cell Mol Life Sci 66: 596-612.
62. Knox D, Nault T, Henderson C, Liberzon I. 2012. Glucocorticoid receptors and extinction retention deficits in the single prolonged stress model. Neuroscience 223: 163-173.
63. Koenen KC, Moffitt TE, Poulton R, Martin J, Caspi A. 2007. Early childhood factors associated with the development of post-traumatic stress disorder: results from a longitudinal birth cohort. Psychol Med 37: 181-192.
64. Kohda K, Harada K, Kato K, Hoshino A, Motohashi J, Yamaji T, Morinobu S, Matsuoka N, Kato N. 2007. Glucocorticoid receptor activation is involved in producing abnormal phenotypes of single-prolonged stress rats: a putative post-traumatic stress disorder model. Neuroscience 148: 22-33.
65. Korzus E, Rosenfeld MG, Mayford M. 2004. CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 42: 961-972.
66. Koshibu K, Gräff J, Mansuy IM. 2011. Nuclear protein phosphatase-1: an epigenetic regulator of fear memory and amygdala long-term potentiation. Neuroscience 173: 30-36.
67. Kriaucionis S, Heintz N. 2009. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324: 929-930.
68. Kudler H, Day K, Schnurr PP. 2016. Treatment options for veterans with posttraumatic stress disorder. JAMA Psychiatry 73: 756-757.
69. Kumar A, Choi KH, Renthal W, Tsankova NM, Theobald DE, Truong HT, Russo SJ, Laplant Q, Sasaki TS, Whistler KN, et al. 2005. Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 48: 303-314.
70. Kwapis JL, Wood MA. 2014. Epigenetic mechanisms in fear conditioning: implications for treating post-traumatic stress disorder. Trends Neurosci 37: 706-720.
71. Labonte B, Azoulay N, Yerko V, Turecki G, Brunet A. 2014. Epigenetic modulation of glucocorticoid receptors in posttraumatic stress disorder. Transl Psychiatry 4: e368.
72. Lattal KM, Barrett RM, Wood MA. 2007. Systemic or intrahippocampal delivery of histone deacetylase inhibitors facilitates fear extinction. Behav Neurosci 121: 1125-1131.
73. Lee JL. 2008. Memory reconsolidation mediates the strengthening of memories by additional learning. Nat Neurosci 11: 1264-1266.
74. Levenson JM, O'Riordan KJ, Brown KD, Trinh MA, Molfese DL, Sweatt JD. 2004. Regulation of histone acetylation during memory formation in the hippocampus. J Biol Chem 279: 40545-40559.
75. Li S, Murakami Y, Wang M, Maeda K, Matsumoto K. 2006. The effects of chronic valproate and diazepam in a mouse model of posttraumatic stress disorder. Pharmacol Biochem Behav 85: 324-331.
76. Li X,WeiW, Ratnu VS, BredyTW. 2013. On the potential role of active DNA demethylation in establishing epigenetic states associated with neural plasticity and memory. Neurobiol Learn Mem 105: 125-132.
77. Li X, Wei W, Zhao QY, Widagdo J, Baker-Andresen D, Flavell CR, D'Alessio A, Zhang Y, Bredy TW. 2014. Neocortical Tet3-mediated accumulation of 5-hydroxymethylcytosine promotes rapid behavioral adaptation. Proc Natl Acad Sci 111: 7120-7125.
78. Li S, Papale LA, Kintner DB, Sabat G, Barrett-Wilt GA, Cengiz P, Alisch RS. 2015. Hippocampal increase of 5-hmC in the glucocorticoid receptor gene following acute stress. Behav Brain Res 286: 236-240.
79. Li S, Papale LA, Zhang Q, Madrid A, Chen L, Chopra P, Keles S, Jin P, Alisch RS. 2016. Genome-wide alterations in hippocampal 5-hydroxymethylcytosine links plasticity genes to acute stress. Neurobiol Dis 86: 99-108.
80. Liberzon I, Krstov M, Young EA. 1997. Stress-restress: effects on ACTH and fast feedback. Psychoneuroendocrinology 22: 443-453.
81. Lu B, Nagappan G, Lu Y. 2014. BDNF and synaptic plasticity, cognitive function, and dysfunction. Handb Exp Pharmacol 220: 223-250.
82. Lubin FD, Sweatt JD. 2007. The IkB kinase regulates chromatin structure during reconsolidation of conditioned fear memories. Neuron 55: 942-957.
83. Lubin FD, Roth TL, Sweatt JD. 2008. Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. J Neurosci 28: 10576-10586.
84. Maddox SA, Schafe GE. 2011. Epigenetic alterations in the lateral amygdala are required for reconsolidation of a Pavlovian fear memory. Learn Mem 18: 579-593.
85. Maddox SA, Watts CS, Doyere V, Schafe GE. 2013a. A naturally-occurring histone acetyltransferase inhibitor derived from Garcinia indica impairs newly acquired and reactivated fear memories. PLoS One 8: e54463.
86. Maddox SA, Watts CS, Schafe GE. 2013b. p300/CBP histone acetyltransferase activity is required for newly acquired and reactivated fear memories in the lateral amygdala. Learn Memory 20: 109-119.
87. Maddox SA, Watts CS, Schafe GE. 2014. DNA methyltransferase activity is required for memory-related neural plasticity in the lateral amygdala. Neurobiol Learn Mem 107: 93-100.
88. Mahan AL, Mou L, Shah N, Hu JH, Worley PF, Ressler KJ. 2012. Epigenetic modulation of Homer1a transcription regulation in amygdala and hippocampus with pavlovian fear conditioning. J Neurosci 32: 4651-4659.
89. Malan-Muller S, Seedat S, Hemmings SM. 2014. Understanding posttraumatic stress disorder: insights from the methylome. Genes Brain Behav 13: 52-68.
90. Marek R, Coelho CM, Sullivan RK, Baker-Andresen D, Li X, Ratnu V, Dudley KJ, Meyers D, Mukherjee C, Cole PA, et al. 2011. Paradoxical enhancement of fear extinction memory and synaptic plasticity by inhibition of the histone acetyltransferase p300. J Neurosci 31: 7486-7491.
91. MarenS,HolmesA.2016. Stressandfearextinction.Neuropsychopharmacology 41: 58-79.
92. Maren S, De Oca B, Fanselow MS. 1994. Sex differences in hippocampal long-term potentiation (LTP) and Pavlovian fear conditioning in rats: positive correlation between LTP and contextual learning. Brain Res 661: 25-34.
93. Maroun M, Ioannides PJ, Bergman KL, Kavushansky A, Holmes A, Wellman CL. 2013. Fear extinction deficits following acute stress associate with increased spine density and dendritic retraction in basolateral amygdala neurons. Eur J Neurosci 38: 2611-2620.
94. Matsumoto Y, Morinobu S, Yamamoto S, Matsumoto T, Takei S, Fujita Y, Yamawaki S. 2013. Vorinostat ameliorates impaired fear extinction possibly via the hippocampal NMDA-CaMKII pathway in an animal model of posttraumatic stress disorder. Psychopharmacology (Berl) 229: 51-62.
95. McGaugh JL. 2000. Memory-A century of consolidation. Science 287: 248-251.
96. Meyer RM, Burgos-Robles A, Liu E, Correia SS, Goosens KA. 2014. A ghrelin-growth hormone axis drives stress-induced vulnerability to enhanced fear. Mol Psychiatry 19: 1284-1294.
97. Meyer-Lindenberg A, Domes G, Kirsch P, Heinrichs M. 2011. Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat Rev Neurosci 12: 524-538.
98. Milad MR, Pitman RK, Ellis CB, Gold AL, Shin LM, Lasko NB, Zeidan MA, Handwerger K, Orr SP, Rauch SL. 2009. Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biol Psychiatry 66: 1075-1082.
99. Milekic MH, Alberini CM. 2002. Temporally graded requirement for protein synthesis following memory reactivation. Neuron 36: 521-525.
100. Miller CA, Sweatt JD. 2006. Amnesia or retrieval deficit? Implications of a molecular approach to the question of reconsolidation. Learn Memory 13: 498-505.
101. Miller CA, Sweatt JD. 2007. Covalent modification of DNA regulates memory formation. Neuron 53: 857-869.
102. Miller CA, Campbell SL, Sweatt JD. 2008. DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity. Neurobiol Learn Mem 89: 599-603.
103. Miller CA, Gavin CF, White JA, Parrish RR, Honasoge A, Yancey CR, Rivera IM, Rubio MD, Rumbaugh G, Sweatt JD. 2010. Cortical DNA methylation maintains remote memory. Nat Neurosci 13: 664-666.
104. Miracle AD, Brace MF, Huyck KD, Singler SA, Wellman CL. 2006. Chronic stress impairs recall of extinction of conditioned fear. Neurobiol Learn Mem 85: 213-218.
105. Miyagawa K, Tsuji M, Takeda H. 2012. [Possible involvement of histone acetylation in the development of emotional resistance to stress stimuli]. Nihon Shinkei Seishin Yakurigaku Zasshi 32: 263-267.
106. Monfils MH, Cowansage KK, Klann E, LeDoux JE. 2009. Extinction-reconsolidation boundaries: key to persistent attenuation of fear memories. Science 324: 951-955.
107. Monsey MS, Ota KT, Akingbade IF, Hong ES, Schafe GE. 2011. Epigenetic alterations are critical for fear memory consolidation and synaptic plasticity in the lateral amygdala. PLoS One 6: e19958.
108. Nader K, Schafe GE, Le Doux JE. 2000. Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406: 722-726.
109. Nasca C, Zelli D, Bigio B, Piccinin S, Scaccianoce S, Nistico R, McEwen BS. 2015. Stress dynamically regulates behavior and glutamatergic gene expression in hippocampus by opening a window of epigenetic plasticity. Proc Natl Acad Sci 112: 14960-14965.
110. Norrholm SD, Jovanovic T, Olin IW, Sands LA, Karapanou I, Bradley B, Ressler KJ. 2011. Fear extinction in traumatized civilians with posttraumatic stress disorder: relation to symptom severity. Biol Psychiatry 69: 556-563.
111. Norrholm SD, Jovanovic T, Smith AK, Binder E, Klengel T, Conneely K, Mercer KB, Davis JS, Kerley K,Winkler J, et al. 2013. Differential genetic and epigenetic regulation of catechol-O-methyltransferase is associated with impaired fear inhibition in posttraumatic stress disorder. Front Behav Neurosci 7: 30.
112. Pedreira ME, Maldonado H. 2003. Protein synthesis subserves reconsolidation or extinction depending on reminder duration. Neuron 38: 863-869.
113. Peleg S, Sananbenesi F, Zovoilis A, Burkhardt S, Bahari-Javan S, Agis-Balboa RC, Cota P, Wittnam JL, Gogol-Doering A, Opitz L, et al. 2010. Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 328: 753-756.
114. Perusini JN, Meyer EM, Long VA, Rau V, Nocera N, Avershal J, Maksymetz J, Spigelman I, Fanselow MS. 2016. Induction and expression of fear sensitization caused by acute traumatic stress. Neuropsychopharmacology 41: 45-57.
115. Peters J, Dieppa-Perea LM, Melendez LM, Quirk GJ. 2010. Induction of fear extinction with hippocampal-infralimbic BDNF. Science 328: 1288-1290.
116. Pitman RK, Rasmusson AM, Koenen KC, Shin LM, Orr SP, Gilbertson MW, Milad MR, Liberzon I. 2012. Biological studies of post-traumatic stress disorder. Nat Rev Neurosci 13: 769-787.
117. Quinn JJ, Skipper RA, Claflin DI. 2014. Infant stress exposure produces persistent enhancement of fear learning across development. Dev Psychobiol 56: 1008-1016.
118. Ragu Varman D, Rajan KE. 2015. Environmental enrichment reduces anxiety by differentially activating serotonergic and neuropeptide Y (NPY)-ergic system in indian field mouse (Mus booduga): an animal model of post-traumatic stress disorder. PLoS One 10: e0127945.
119. Rampp C, Binder EB, Provencal N. 2014. Epigenetics in posttraumatic stress disorder. Prog Mol Biol Transl Sci 128: 29-50.
120. Rau V, DeCola JP, Fanselow MS. 2005. Stress-induced enhancement of fear learning: an animal model of posttraumatic stress disorder. Neurosci Biobehav Rev 29: 1207-1223.
121. Ressler KJ, Mercer KB, Bradley B, Jovanovic T, Mahan A, Kerley K, Norrholm SD, Kilaru V, Smith AK, Myers AJ, et al. 2011. Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor. Nature 470: 492-497.
122. Rodrigues GM Jr., Toffoli LV, Manfredo MH, Francis-Oliveira J, Silva AS, Raquel HA, Martins-Pinge MC, Moreira EG, Fernandes KB, Pelosi GG, et al. 2015. Acute stress affects the global DNA methylation profile in rat brain: modulation by physical exercise. Behav Brain Res 279: 123-128.
123. Rodriguez Manzanares PA, Isoardi NA, Carrer HF, Molina VA. 2005. Previous stress facilitates fear memory, attenuates GABAergic inhibition, and increases synaptic plasticity in the rat basolateral amygdala. J Neurosci 25: 8725-8734.
124. Rosas-Vidal LE, Do-Monte FH, Sotres-Bayon F, Quirk GJ. 2014. Hippocampal-prefrontal BDNF and memory for fear extinction. Neuropsychopharmacology 39: 2161-2169.
125. Roth TL, Roth ED, Sweatt JD. 2010. Epigenetic regulation of genes in learning and memory. Essays Biochem 48: 263-274.
126. Roth TL, Zoladz PR, Sweatt JD, Diamond DM. 2011. Epigenetic modification of hippocampal Bdnf DNA in adult rats in an animal model of post-traumatic stress disorder. J Psychiatr Res 45: 919-926.
127. Rotllant D, Pastor-Ciurana J, Armario A. 2013. Stress-induced brain histone H3 phosphorylation: contribution of the intensity of stressors and length of exposure. J Neurochem 125: 599-609.
128. Rougemont-Bucking A, Linnman C, Zeffiro TA, Zeidan MA, Lebron-Milad K, Rodriguez-Romaguera J, Rauch SL, Pitman RK, Milad MR. 2011. Altered processing of contextual information during fear extinction in PTSD: an fMRI study. CNS Neurosci Ther 17: 227-236.
129. Rudenko A, Tsai LH. 2014. Epigenetic regulation in memory and cognitive disorders. Neuroscience 264: 51-63.
130. Rudenko A, Dawlaty MM, Seo J, Cheng AW, Meng J, Le T, Faull KF, Jaenisch R, Tsai LH. 2013. Tet1 is critical for neuronal activity-regulated gene expression and memory extinction. Neuron 79: 1109-1122.
131. Sawamura T, Klengel T, Armario A, Jovanovic T, Norrholm SD, Ressler KJ, Andero R. 2016. Dexamethasone treatment leads to enhanced fear extinction and dynamic Fkbp5 regulation in amygdala. Neuropsychopharmacology 41: 832-846.
132. Shors TJ, Weiss C, Thompson RF. 1992. Stress-induced facilitation of classical conditioning. Science 257: 537-539.
133. Sierra-Mercado D, Padilla-Coreano N, Quirk GJ. 2011. Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 36: 529-538.
134. Soeter M, Kindt M. 2012. Stimulation of the noradrenergic system during memory formation impairs extinction learning but not the disruption of reconsolidation. Neuropsychopharmacology 37: 1204-1215.
135. Soliman F, Glatt CE, Bath KG, Levita L, Jones RM, Pattwell SS, Jing D, Tottenham N, Amso D, Somerville LH, et al. 2010. A genetic variant BDNF polymorphism alters extinction learning in both mouse and human. Science 327: 863-866.
136. Stafford JM, Raybuck JD, Ryabinin AE, Lattal KM. 2012. Increasing histone acetylation in the hippocampus-infralimbic network enhances fear extinction. Biol Psychiatry 72: 25-33.
137. Stankiewicz AM, Swiergiel AH, Lisowski P. 2013. Epigenetics of stress adaptations in the brain. Brain Res Bull 98: 76-92.
138. Steenen SA, vanWijk AJ, van der Heijden GJ, vanWestrhenen R, de Lange J, de Jongh A. 2016. Propranolol for the treatment of anxiety disorders: Systematic review and meta-Analysis. J Psychopharmacol 30: 128-139.
139. Steenkamp MM. 2016a. Treatment options for veterans with posttraumatic stress disorder-reply. JAMA Psychiatry 73: 757-758.
140. Steenkamp MM. 2016b. True evidence-based care for posttraumatic stress disorder in military personnel and veterans. JAMA Psychiatry 73: 431-432.
141. Stevens JS, Almli LM, Fani N, Gutman DA, Bradley B, Norrholm SD, Reiser E, Ely TD, Dhanani R, Glover EM, et al. 2014. PACAP receptor gene polymorphism impacts fear responses in the amygdala and hippocampus. Proc Natl Acad Sci 111: 3158-3163.
142. Stevenson CW, Meredith JP, Spicer CH, Mason R, Marsden CA. 2009. Early life programming of innate fear and fear learning in adult female rats. Behav Brain Res 198: 51-57.
143. Suvrathan A, Bennur S, Ghosh S, Tomar A, Anilkumar S, Chattarji S. 2014. Stress enhances fear by forming new synapses with greater capacity for long-term potentiation in the amygdala. Philos Trans R Soc Lond B Biol Sci 369: 20130151.
144. Suzuki A, Josselyn SA, Frankland PW, Masushige S, Silva AJ, Kida S. 2004. Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J Neurosci 24: 4787-4795.
145. Szczytkowski-Thomson JL, Lebonville CL, Lysle DT. 2013. Morphine prevents the development of stress-enhanced fear learning. Pharmacol Biochem Behav 103: 672-677.
146. Takahashi T, Morinobu S, Iwamoto Y, Yamawaki S. 2006. Effect of paroxetine on enhanced contextual fear induced by single prolonged stress in rats. Psychopharmacology (Berl) 189: 165-173.
147. Takei S, Morinobu S, Yamamoto S, Fuchikami M, Matsumoto T, Yamawaki S. 2011. Enhanced hippocampal BDNF/TrkB signaling in response to fear conditioning in an animal model of posttraumatic stress disorder. J Psychiatr Res 45: 460-468.
148. Toda H, Boku S, Nakagawa S, Inoue T, Kato A, Takamura N, Song N, Nibuya M, Koyama T, Kusumi I. 2014. Maternal separation enhances conditioned fear and decreases the mRNA levels of the neurotensin receptor 1 gene with hypermethylation of this gene in the rat amygdala. PLoS One 9: e97421.
149. Tronson NC, Guzman YF, Guedea AL, Huh KH, Gao C, Schwarz MK, Radulovic J. 2010. Metabotropic glutamate receptor 5/Homer interactions underlie stress effects on fear. Biol Psychiatry 68: 1007-1015.
150. Vaiserman AM. 2015. Epigenetic programming by early-life stress: evidence from human populations. Dev Dyn 244: 254-265.
151. Vaissiere T, Sawan C, Herceg Z. 2008. Epigenetic interplay between histone modifications and DNA methylation in gene silencing. Mutat Res 659: 40-48.
152. Valvassori SS, Varela RB, Arent CO, Dal-Pont GC, Bobsin TS, Budni J, Reus GZ, Quevedo J. 2014. Sodium butyrate functions as an antidepressant and improves cognition with enhanced neurotrophic expression in models of maternal deprivation and chronic mild stress. Curr Neurovasc Res 11: 359-366.
153. Valvassori SS, Resende WR, Budni J, Dal-Pont GC, Bavaresco DV, Reus GZ, Carvalho AF, Goncalves CL, Furlanetto CB, Streck EL, et al. 2015. Sodium butyrate, a histone deacetylase inhibitor, reverses behavioral and mitochondrial alterations in animal models of depression induced by early-or late-life stress. Curr Neurovasc Res 12: 312-320.
154. Vialou V, Feng J, Robison AJ, Nestler EJ. 2013. Epigenetic mechanisms of depression and antidepressant action. Annu Rev Pharmacol Toxicol 53: 59-87.
155. Vogel-Ciernia A, Matheos DP, Barrett RM, Kramar EA, Azzawi S, Chen Y, Magnan CN, Zeller M, Sylvain A, Haettig J, et al. 2013. The neuron-specific chromatin regulatory subunit BAF53b is necessary for synaptic plasticity and memory. Nat Neurosci 16: 552-561.
156. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ. 2004. Epigenetic programming by maternal behavior. Nat Neurosci 7: 847-854.
157. Wei W, Coelho CM, Li X, Marek R, Yan S, Anderson S, Meyers D, Mukherjee C, Sbardella G, Castellano S, et al. 2012. p300/CBP-Associated factor selectively regulates the extinction of conditioned fear. J Neurosci 32: 11930-11941.
158. Wilson CB, McLaughlin LD, Ebenezer PJ, Nair AR, Francis J. 2014. Valproic acid effects in the hippocampus and prefrontal cortex in an animal model of post-traumatic stress disorder. Behav Brain Res 268: 72-80.
159. Wood MA, Kaplan MP, Park A, Blanchard EJ, Oliveira AM, Lombardi TL, Abel T. 2005. Transgenic mice expressing a truncated form of CREB-binding protein (CBP) exhibit deficits in hippocampal synaptic plasticity and memory storage. Learn Mem 12: 111-119.
160. Yamamoto S, Morinobu S, Fuchikami M, Kurata A, Kozuru T, Yamawaki S. 2008. Effects of single prolonged stress and D-cycloserine on contextual fear extinction and hippocampal NMDA receptor expression in a rat model of PTSD. Neuropsychopharmacology 33: 2108-2116.
161. Yamamoto S, Morinobu S, Takei S, Fuchikami M, Matsuki A, Yamawaki S, Liberzon I. 2009. Single prolonged stress: toward an animal model of posttraumatic stress disorder. Depress Anxiety 26: 1110-1117.
162. Yamawaki Y, Fuchikami M, Morinobu S, Segawa M, Matsumoto T, Yamawaki S. 2012. Antidepressant-like effect of sodium butyrate (HDAC inhibitor) and its molecular mechanism of action in the rat hippocampus. World J Biol Psychiatry 13: 458-467.
163. Yehuda R, Hoge CW. 2016. Treatment options for veterans with posttraumatic stress disorder-reply. JAMA Psychiatry 73: 758.
164. Yehuda R, Cai G, Golier JA, Sarapas C, Galea S, Ising M, Rein T, Schmeidler J, Muller-Myhsok B, Holsboer F, et al. 2009. Gene expression patterns associated with posttraumatic stress disorder following exposure to the World Trade Center attacks. Biol Psychiatry 66: 708-711.
165. Yehuda R, Daskalakis NP, Bierer LM, Bader HN, Klengel T, Holsboer F, Binder EB. 2015a. Holocaust exposure induced intergenerational effects on FKBP5 methylation. Biol Psychiatry, in press. doi: 10.1016/j.biopsych.2015.08.005.
166. Yehuda R, Flory JD, Bierer LM, Henn-Haase C, Lehrner A, Desarnaud F, Makotkine I, Daskalakis NP, Marmar CR, Meaney MJ. 2015b. Lower methylation of glucocorticoid receptor gene promoter 1F in peripheral blood of veterans with posttraumatic stress disorder. Biol Psychiatry 77: 356-364.
167. Zhou VW, Goren A, Bernstein BE. 2011. Charting histone modifications and the functional organization of mammalian genomes. Nat Rev Genet 12: 7-18.
168. Zovkic IB, Guzman-Karlsson MC, Sweatt JD. 2013. Epigenetic regulation of memory formation and maintenance. Learn Mem 20: 61-74.