Does stress remove the HDAC brakes for the formation and persistence of long-term memory?

Neurobiology of Learning and Memory

Volumn 112, Issue , 2014, Pages 61-67

  White, André O ^a,b   Wood, Marcelo A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Center for the Neurobiology of Learning and Memory   (United States)

Author keywords

Chromatin; Epigenetics; Gene expression; Histone acetylation; Histone deacetylases (HDACs); Long term memory; Stress

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLUCOCORTICOID RECEPTOR; HISTONE DEACETYLASE; HYDROCORTISONE; NORADRENALIN; HISTONE DEACETYLASE INHIBITOR;

CELL FUNCTION; CHROMATIN; EMOTIONALITY; ENZYME INHIBITION; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; HYDROCORTISONE RELEASE; LEARNING; LONG TERM MEMORY; MEMORY CONSOLIDATION; NONHUMAN; NORADRENALIN RELEASE; POSTTRAUMATIC STRESS DISORDER; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; STRESS; ANIMAL; GENE EXPRESSION REGULATION; HUMAN; MENTAL STRESS; METABOLISM; PHYSIOLOGY;

ANIMALS; GENE EXPRESSION REGULATION; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; MEMORY, LONG-TERM; STRESS, PSYCHOLOGICAL;

EID: 84901918412     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2013.10.007     Document Type: Review

References (66)

1. Agranoff B.W., Davis R.E., Casola L., Lim R. Actinomycin D blocks formation of memory of shock-avoidance in goldfish. Science 1967, 158:1600-1601.
2. Alarcón J.M., Malleret G., Touzani K., Vronskaya S., Ishii S., Kandel E.R., et al. Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice. A model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 2004, 42:947-959.
3. Alberini C.M. Transcription factors in long-term memory and synaptic plasticity. Physiological Reviews 2009, 89:121-145.
4. Bahari-Javan S., Maddalena A., Kerimoglu C., Wittnam J., Held T., et al. HDAC1 regulates fear extinction in mice. Journal of Neuroscience 2012, 2(15):5062-5073.
5. Bale T.L. Sex differences in prenatal epigenetic programming of stress pathways. Stress 2011, 14(4):348-356.
6. Barrett R.M., Malvaez M., Kramar E., Matheos D.P., Arrizon A., Cabrera S.M., et al. Hippocampal focal knockout of CBP affects specific histone modifications, long-term potentiation, and long-term memory. Neuropsychopharmacology 2011, 36:1545-1556.
7. Barrett R.M., Wood M.A. Beyond transcription factors: The role of chromatin modifying enzymes in regulating transcription required for memory. Learning & Memory 2008, 15:460-467.
8. Beato M., Sánchez-Pacheco A. Interaction of steroid hormone receptors with the transcription initiation complex. Endocrine Reviews 1996, 17:587-609.
9. Bilang Bleuel A., Ulbricht S., Chandramohan Y., De Carli S., Droste S.K., Reul J.M.H.M. Psychological stress increases histone H3 phosphorylation in adult dentate gyrus granule neurons: Involvement in a glucocorticoid receptor-dependent behavioural response. European Journal of Neuroscience 2005, 22:1691-1700.
10. Bouton M.E. Context, time, and memory retrieval in the interference paradigms of Pavlovian learning. Psychological Bulletin 1993, 114:80-99.
11. Bredy T.W., Barad M. The histone deacetylase inhibitor valproic acid enhances acquisition, extinction, and reconsolidation of conditioned fear. Learning & Memory 2008, 15(1):39-45.
12. Bredy T.W., Wu H., Crego C., Zellhoefer J., Sun Y.E., Barad M. Histone modifications around individual BDNF gene promoters in prefrontal cortex are associated with extinction of conditioned fear. Learning & Memory 2007, 14:268-276.
13. Broide R.S., Redwine J.M., Aftahi N., Young W., Bloom F.E., Winrow C.J. Distribution of histone deacetylases 1-11 in the rat brain. Journal of Molecular Neuroscience 2007, 31:47-58.
14. Chandramohan Y., Droste S.K., Reul J.M.H.M. Novelty stress induces phospho-acetylation of histone H3 in rat dentate gyrus granule neurons through coincident signalling via the N-methyl-D-aspartate receptor and the glucocorticoid receptor: Relevance for c-fos induction. Journal of Neurochemistry 2007, 101:815-828.
15. Chen Y., Bender R.A., Frotscher M., Baram T.Z. Novel and transient populations of corticotropin-releasing hormone-expressing neurons in developing hippocampus suggest unique functional roles: A quantitative spatiotemporal analysis. Journal of Neuroscience 2001, 21:7171-7181.
16. Davis M., Ressler K., Rothbaum B.O., Richardson R. Effects of D-cycloserine on extinction: Translation from preclinical to clinical work. Biological Psychiatry 2006, 60(4):369-375.
17. Day J.J., Sweatt J.D. Epigenetic mechanisms in cognition. Neuron 2011, 70:813-829.
18. de Kloet E.R., Oitzl M.S., Joëls M. Stress and cognition: Are corticosteroids good or bad guys?. Trends in Neurosciences 1999, 22:422-426.
19. de Quervain D.J.-F., Roozendaal B., McGaugh J.L. Stress and glucocor- ticoids impair retrieval of long-term spatial memory. Nature 1998, 394:787-790.
20. Fischer A., Sananbenesi F., Wang X., Dobbin M., Tsai L.H. Recovery of learning and memory is associated with chromatin remodeling. Nature 2007, 447:178-182.
21. Guan Z., Giustetto M., Lomvardas S., Kim J.H., Miniaci M.C., Schwartz J.H., et al. Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell 2002, 111:483-493.
22. Guan J.S., Haggarty S.J., Giacometti E., Dannenberg J.H., Joseph N., Gao J., et al. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 2009, 459:55-60.
23. Gutièrrez-Mecinas M., Trollope A.F., Collins A., Monfett H., Hesketh S.A., Kersanté F., et al. Long-lasting behavioral responses to stress involve a direct interaction of glucocorticoid receptors with ERK1/2-MSK1-Elk-1 signaling. Proceedings of the National Academy Sciences of the United States of America 2011, 108(33):13806-13811.
24. Haettig J., Stefanko D.P., Multani M.L., Figueroa D.X., McQuown S.C., Wood M.A. HDAC inhibition modulates hippocampus-dependent long-term memory for object location in a CBP-dependent manner. Learning & Memory 2011, 18:71-79.
25. Hargreaves D.C., Crabtree G.R. ATP-dependent chromatin remodeling: Genetics, genomics and mechanisms. Cell Research 2011, 21:396-420.
26. Hawk J.D., Florian C., Abel T. Post-training intrahippocampal inhibition of class I histone deacetylases enhances long-term object-location memory. Learning & Memory 2011, 18:367-370.
27. Joëls M., Baram T.Z. The neuro-symphony of stress. Nature Reviews Neuroscience 2009, 10(6):459-466.
28. Joëls M., Fernandez G., Roozendaal B. Stress and emotional memory: A matter of timing. Trends in Cognitive Sciences 2011, 15:280-288.
29. Karsten C.A., Baram T.Z. How Does a Neuron "know" to modulate its epigenetic machinery in response to early-life environment/experience? Front. Psychiatry 2013, 4:89.
30. Kilgore M., Miller C.A., Fass D.M., Hennig K.M., Haggarty S.J., Sweatt J.D., et al. Inhibitors of class1 histone deacetylases reverse contextual memory deficits in a mouse model of Alzheimer's disease. Neuropsychopharmacology 2010, 35:870-880.
31. Kim M.S., Akhtar M.W., Adachi M., Mahgoub M., Bassel-Duby R., Kavalali E.T., et al. An essential role for histone deacetylase 4 in Synaptic plasticity and memory formation. Journal of Neuroscience 2012, 32(32):10879-10886.
32. Kim J., Kwon J.T., Kim H.S., Han J.H. CREB and neuronal selection for memory trace. Front Neural Circuits 2013, 7:44.
33. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
34. Lahm A., Paolini C., Pallaoro M., Nardi M.C., Jones P., Neddermann P., et al. Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases. Proceedings of the National Academy Sciences of the United States of America 2007, 104:17335-17340.
35. Lattal K.M., Barrett R.M., Wood M.A. Systemic or intrahippocampal delivery of histone deacetylase inhibitors facilitates fear extinction. Behavioral Neuroscience 2007, 121:1125-1131.
36. Lattal K.M., Wood M.A. Epigenetics and persistent memory: Implications for reconsolidation and silent extinction beyond the zero. Nature Neuroscience 2013, 16:124-129.
37. Levenson J.M., O'Riordan K.J., Brown K.D., Trinh M.A., Molfese D.L., Sweatt J.D. Regulation of histone acetylation during memory formation in the hippocampus. Journal of Biological Chemistry 2004, 279:40545-40559.
38. Li X., Wei W., Ratnu V.S., Bredy T.W. On the potential role of active DNA demethylation in establishing epigenetic states associated with neural plasticity and memory. Neurobiology of Learning and Memory 2013, 105:125-132.
39. Liang K.C., Lee E.H. Intra-amygdala injections of corticotropin releasing factor facilitate inhibitory avoidance learning and reduce exploratory behavior in rats. Psychopharmacology 1988, 96:232-236.
40. Malvaez M., McQuown S.C., Rogge G.A., Astarabadi M., Jacques V., Carreiro S., et al. HDAC3-selective inhibitor enhances extinction of cocaine-seeking behavior in a persistent manner. Proceedings of the National Academy Sciences of the United States of America 2013, 110:2647-2652.
41. Malvaez M., Sanchis-Segura C., Vo D., Lattal K.M., Wood M.A. Modulation of chromatin modification facilitates extinction of cocaine-induced conditioned place preference. Biological Psychiatry 2010, 67:36-43.
42. Maras P.M., Baram T.Z. Sculpting the hippocampus from within: Stress, spines, and CRH. Cell 2012, 35(5):315-324.
43. McClelland S., Korosi A., Cope J., Ivy A., Baram T.Z. Emerging roles of epigenetic mechanisms in the enduring effects of early-life stress and experience on learning and memory. Neurobiology of Learning and Memory 2011, 96:79-88.
44. McGaugh J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annual Review of Neuroscience 2004, 27:1-28.
45. McQuown S.C., Barrett R.M., Matheos D.P., Post R.J., Rogge G.R., Alenghat T., et al. HDAC3 is a critical negative regulator of long-term memory formation. Journal of Neuroscience 2011, 31:764-774.
46. McQuown S., Wood M.A. HDAC3 and the molecular brake pad hypothesis. Neurobiology of Learning and Memory 2011, 96:27-34.
47. Morris M.J., Mahgoub M., Na E.S., Pranav H., Monteggia L.M. Loss of histone deacetylase 2 improves working memory and accelerates extinction learning. Journal of Neuroscience 2013, 33(15):6401-6411.
48. Okuda S., Roozendaal B., McGaugh J.L. Glucocorticoid effects on object recognition memory require training-associated emotional arousal. Proceedings of the National Academy Sciences of the United States of America 2004, 101:853-858.
49. Pearce J.M. A model for stimulus generalization in Pavlovian conditioning. Psychological Review 1987, 94:61-73.
50. Peixoto L., Abel T. The role of histone acetylation in memory formation and cognitive impairments. Neuropsychopharmacology 2013, 38(1):62-76.
51. Revollo J.R., Cidlowski J.A. Mechanisms generating diversity in glucocorticoid receptor signaling. Annals of New York Academy of Sciences 2009, 1179:167-178.
52. Rodgers A.B., Morgan C.P., Bronson S.L., Revello S., Bale T.L. Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. Journal of Neuroscience 2013, 33(21):9003-9012.
53. Rogge G.A., Singh H., Dang R., Wood M.A. HDAC3 is a negative regulator of cocaine-context-associated memory formation. Journal of Neuroscience 2013, 33(15):6623-6632.
54. Roozendaal B., Barsegyan A., Lee S. Adrenal stress hormones, amygdala activation, and memory for emotionally arousing experiences. Progress in Brain Research 2008, 167:79-97.
55. Roozendaal B., Hernandez A., Cabrera S.M., Hagewoud R., Malvaez M., Stefanko D.P., Haettig J., Wood M.A. Membrane-associated glucocorticoid activity is necessary for modulation of long-term memory via chromatin modification. Journal of Neuroscience 2010, 30(14):5037-5046.
56. Roozendaal B., Okuda S., Van der Zee E.A., McGaugh J.L. Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proceedings of the National Academy Sciences of the United States of America 2006, 103:6741-6746.
57. Roozendaal B., Quirarte G. Glucocorticoids interact with the basolateral amygdala β-adrenoceptor-cAMP/cAMP/PKA system in influencing memory consolidation. European Journal of Neuroscience 2002, 15:553-560.
58. Sandi C., Pinelo-Nava M.T. Stress and memory: Behavioral effects and neurobiological mechanisms. Neural Plasticity 2007, 2007:78970.
59. Sando R., Gounko N., Pieraut S., Liao L., Yates J., Maximov A. HDAC4 governs a transcriptional program essential for synaptic plasticity and memory. Cell 2012, 151(4):821-834.
60. Stafford J.M., Raybuck J.D., Ryabinin A.E., Lattal K.M. Increasing histone acetylation in the hippocampus- infralimbic network enhances fear extinction. Biological Psychiatry 2012, 72:25-33.
61. Stefanko D.P., Barrett R.M., Ly A.R., Reolon G.K., Wood M.A. Modulation of long-term memory for object recognition via HDAC inhibition. Proceedings of the National Academy Sciences of the United States of America 2009, 106:9447-9452.
62. Turner B.M. Cellular memory and the histone code. Cell 2002, 111:285-291.
63. Vecsey C.G., Hawk J.D., Lattal K.M., Stein J.M., Fabian S.A., Attner M.A., et al. Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. Journal of Neuroscience 2007, 27:6128-6140.
64. Vogel-Ciernia A., Matheos D.P., Barrett R.M., Kramár E.A., Wood M.A., et al. The neuron-specific chromatin regulatory subunit BAF53b is necessary for synaptic plasticity and memory. Nature Neuroscience 2013, 16(5):552-561.
65. Wood M.A., Attner M.A., Oliveira A.M.M., Brindle P.K., Abel T. A transcription factor-binding domain of the coactivator CBP is essential for long-term memory and the expression of specific target genes. Learning & Memory 2006, 13:609-617.
66. kB in rat amygdala improves long-term but not short-term retention of fear memory. Molecular Pharmacology 2004, 65:1286-1292.