Early stress evokes dysregulation of histone modifiers in the medial prefrontal cortex across the life span

Developmental Psychobiology

Volumn 58, Issue 2, 2016, Pages 198-210

  Pusalkar, Madhavi ^a   Suri, Deepika ^a   Kelkar, Ashwin ^b   Bhattacharya, Amrita ^a   Galande, Sanjeev ^b   Vaidya, Vidita A ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH   (India)

Author keywords

Histone acetyltransferase; Histone deacetylase; Histone demethylase; Histone methyltransferase; Maternal separation; Sirtuin

Indexed keywords

HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; HISTONE LYSINE METHYLTRANSFERASE; SIRTUIN;

ACETYLATION; ANIMAL; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HISTONE CODE; MALE; MATERNAL DEPRIVATION; MENTAL STRESS; METABOLISM; METHYLATION; PREFRONTAL CORTEX; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

ACETYLATION; ANIMALS; BLOTTING, WESTERN; DOWN-REGULATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONE ACETYLTRANSFERASES; HISTONE CODE; HISTONE DEACETYLASES; HISTONE-LYSINE N-METHYLTRANSFERASE; MALE; MATERNAL DEPRIVATION; METHYLATION; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIRTUINS; STRESS, PSYCHOLOGICAL;

EID: 84958762178     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.21365     Document Type: Article

References (63)

1. Aguilar-Valles, A., Vaissière, T., Griggs, E. M., Mikaelsson, M. A., Takács, I. F., Young, E. J., ... & Miller, C. A. ( 2014). Methamphetamine-associated memory is regulated by a writer and eraser of permissive histone methylation. Biological Psychiatry, 76, 57-65.
2. Bagot, R. C., Labonté, B., Peña, C. J., & Nestler, E. J. ( 2014). Epigenetic signaling in psychiatric disorders: Stress and depression. Dialogues in Clinical Neuroscience, 16, 281-295.
3. Baumgart, M., Groth, M., Priebe, S., Savino, A., Testa, G., Dix, A., ... & Cellerino, A. ( 2014). RNA-seq of the aging brain in the short-lived fish N. Furzeri-Conserved pathways and novel genes associated with neurogenesis. Aging Cell, 13, 965-974.
4. Bedford, D. C., & Brindle, P. K. ( 2012). Is histone acetylation the most important physiological function for CBP and P300? Aging, 4, 247-255.
5. Benekareddy, M., Goodfellow, N., Lambe, E. K., & Vaidya, V. A. ( 2010). Enhanced function of prefrontal serotonin 5-HT(2) receptors in a rat model of psychiatric vulnerability. Journal of Neuroscience, 30, 12138-12150.
6. Bharadwaj, R., Peter, C. J., Jiang, Y., Roussos, P., Vogel-Ciernia, A., Shen, E. Y., ... & Akbarian, S. ( 2014). Conserved high-order chromatin regulates NMDA receptor gene expression and cognition. Neuron, 84, 997-1008.
7. Blackledge, N. P., Zhou, J. C., Tolstorukov, M. Y., Farcas, A. M., Parl, P. J., & Klose, R. J. ( 2010). CpG Islands recruit a histone H3 lysine 36 demethylase. Molecular Cell, 38, 179-190.
8. Blaze, J., & Roth, T. L. ( 2013). Exposure to caregiver maltreatment alters expression levels of epigenetic regulators in the medial prefrontal cortex. International Journal of Developmental Neuroscience, 31, 804-810.
9. Bookout, A. L., & Mangelsdorf, D. J. ( 2003). Quantitative real-time PCR protocol for analysis of nuclear receptor signaling pathways. Nuclear Receptor Signaling, 1, e012.
10. Cedar, H., & Bergman, Y. ( 2009). Linking DNA methylation and histone modification: Patterns and paradigms. Nature Reviews Genetics, 10, 295-304.
11. Chalkiadaki, A., & Guarente, L. ( 2012). Sirtuins mediate mammalian metabolic responses to nutrient availability. Nature Reviews in Endocrinology, 8, 287-296.
12. Chase, K. A., & Sharma, R. P. ( 2013). Nicotine induces chromatin remodeling through decrease in the methyltransferases GLP, G9a, Setdb1 and levels of H3K9me2. International Journal of Neurpsychopharmacology, 16, 1129-1138.
13. Chocyk, A., Bobula, B., Dudys, D., Przyborowska, A., Majcher-Maślanka, I., Hess, G., & Wedzony, K. ( 2013). Early-life stress affects the structural and functional plasticity of the medial prefrontal cortex in adolescent rats. European Journal of Neuroscience, 38, 2089-2107.
14. Choi, J. E., & Mastoslavsky, R. ( 2014). Sirtuins, metabolism and DNA repair. Current Opinion in Genetics and Development, 26, 24-32.
15. Chudasama, Y. ( 2011). Animal models of prefrontal-executive function. Behavioural Neuroscience, 125(3), 327-343.
16. Covington, H. E. 3rd, Maze, I., LaPlant, Q. C., Vialou, V. F., Ohnishi, Y. N, Berton, O., ... & Nestler, E. J. ( 2009). Antidepressant actions of histone deacetylase inhibitors. The Journal of Neuroscience, 29, 11451-11460.
17. Dai, Y., & Faller, D. V. ( 2008). Transcription regulation by class III histone deacetylases (HDACs)- Sirtuins. Translational oncogenomics, 3, 53-65.
18. Daniels, W. M., Pieterson, C. Y., Carstens, M. E., & Stein, D. J. ( 2004). Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metabolism and Brain Disorders, 19, 3-14.
19. Dong, E., Dzitoyeva, S. G., Matrisciano, F., Tueting, P., Grayson, D. R., & Guidotti, A. ( 2015). Brain-derived neurotrophic factor epigenetic modifications associated with Schizophrenia-like phenotype induced by prenatal stress in mice. Biological Psychiatry, 77, 589-596.
20. Felitti, V. J., Anda, R. F., Nordenberg, D., Williamson, D. F., Spitz, A. M., Edwards, V., ... & Marks, J. S. ( 1998). Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults: The Adverse Childhood Experiences (ACE) Study. American Journal of Preventive Medicine, 14, 245-258.
21. Hashimoto, H., Vertino, P. M., & Cheng, X. ( 2010). Molecular coupling of DNA methylation and histone methylation. Epigenomics, 2, 657-669.
22. Herskovits, A. Z., & Guarente, L. ( 2014). SIRT1 in neurodevelopment and brain senescence. Neuron, 81, 471-483.
23. Hobara, T., Uchida, S., Otsuki, K., Matsubara, T., Funato, H., Matsuo, K., ... & Watanabe, Y. ( 2010). Altered gene expression of histone deacetylases in mood disorder patients. Journal of Psychiatric Research, 44, 263-270.
24. Huang, H. S., Matevossian, A., Whittle, C., Kim, S. Y., Schumacher, A., Baker, S. P., & Akbarian, S. ( 2007). Prefrontal dysfunction in schizophrenia involves mixed-lineage leukemia 1-regulated histone methylation at GABAergic gene promoters. Journal of Neuroscience, 27, 11254-11262.
25. Huang, C., Xu, M., & Zhu, B. ( 2013). Epigenetic inheritance mediated by histone lysine methylation: Maintaining transcriptional states without the precise restoration of marks? Philosophical Transactions of the Royal Society B, 368, 1-6.
26. Iwahara, T., Bonasio, R., Narendra, V., & Reinberg, D. ( 2012). Sirt 3 functions in the nucleus in the control of stress-related gene expression. Molecular and Cellular Biology, 32, 5022-5034.
27. Kanfi, Y., Naiman, S., Amir, G., Peshti, V., Zinman, G., Nahum, L., ... & Cohen, H. Y. ( 2012). The Sirtuin Sirt6 regulates life-span in male mice. Nature, 483, 218-221.
28. Karsten, C. A., & Baram, T. Z. ( 2013). How does a neuron "know" to modulate its epigenetic machinery in response to early-life environment/experience? Frontiers in Psychiatry, 4, 1-5.
29. Kenworthy, C. A., Sengupta, A., Luz, S. M., Ver Hoeve, E. S., Meda, K., Bhatnagar, S., & Abel, T ( 2014). Social defeat induces changes in histone acetylation and expression of histone modifying enzymes in the ventral hippocampus, prefrontal cortex and dorsal raphe nucleus. Neuroscience, 264, 88-98.
30. Khare, S. P., Habib, F., Sharma, R., Gadewal, N., Gupta, S., & Galande, S. ( 2011). Histome: A relational knowledgebase of human histone proteins and histone modifying enzymes. Nucleic Acids Research, 40, D337-342.
31. Kim, M. S., Akhtar, M. W., Adachi, M., Mahgoub, M., Bassel-Duby, R., Kavalali, E. T., ... & Monteggia, L. M. ( 2012). An essential role for histone deacetylase 4 in synaptic plasticity and memory formation. Journal of Neuroscience, 32, 10879-10886.
32. Kumar, S., Black, S. J., Hultman, R., Szabo, S. T., DeMaio, K. D., Du, J., ... & Dzirasa, K ( 2013). Cortical control of affective networks. Journal of Neuroscience, 33, 1116-1129.
33. Larsson, S., Aas, M., Klungsøyr, O., Agartz, I., Mork, E., Steen, N. E., ... & Lorentzen, S. ( 2013). Patterns of childhood adverse events are associated with clinical characteristics of bipolar disorder. BMC Psychiatry, 13, 97.
34. Levine, S. ( 1967). Maternal and environmental influences on the adrenocortical response to stress in weanlings rats. Science, 156, 258-260.
35. Levine, A., Worrell, T. R., Zimnisky, R., & Schmauss, C. ( 2012). Early life stress triggers sustained changes in histone deacetylase expression and histone H4 modifications that alter responsiveness to adolescent antidepressant treatment. Neurobiology of Disease, 45, 488-498.
36. Lippmann, M., Bress, A., Nemeroff, C., Plotsky, P., & Monteggia, L. ( 2007). Long term behavioural and molecular alterations associated with maternal separation in rats. European Journal of Neuroscience, 25, 3091-3098.
37. Maćkowiak, M., Bator, E., Latusz, J., Mordalska, P., & Wedzony, K. ( 2014). Prenatal MAM administration affects histone H3 methylation in postnatal life in the rat medial prefrontal cortex. European Journal of Neuropsychopharmacology, 24, 271-289.
38. McClelland, S., Korosi, A., Cope, J., Ivy, A., & Baram, T. Z. ( 2011). Emerging roles of epigenetic mechanisms in the enduring effects of early-life stress and experience on learning and memory. Neurobiology of Learning and Memory, 96, 79-88.
39. Meaney, M. J. ( 2001). Maternal care, gene expression and the transmission of individual differences in stress reactivity across generations. Annual Reviews in Neuroscience, 24, 1161-1192.
40. Muhammad, A., Carrol, C., & Kolb, B. ( 2012). Stress during development alters dendritic morphology in the nucleus accumbens and prefrontal cortex. Neuroscience, 216, 103-109.
41. Nanni, V., Uher, R., & Danese, A. ( 2012). Childhood maltreatment predicts unfavorable course of illness and treatment outcome in depression: A meta-analysis. American Journal of Psychiatry, 169, 141-151.
42. Nemeroff, C. B. ( 2004). Neurobiological consequences of childhood trauma. Journal of Clinical Psychiatry, 65, 18-28.
43. Peter, C. J., & Akbarian, S. ( 2011). Balancing histone methylation activities in psychiatric disorders. Trends in Molecular Medicine, 17, 372-379.
44. Rincón-Cortés, M., & Sullivan, R. M. ( 2014). Early life trauma and attachment: Immediate and enduring effects on neurobehavioral and stress axis development. Frontiers in Endocrinology, 5, 33.
45. Rosenberg, S. D., Lu, W., Mueser, K. T., Jankowski, M. K., & Cournos, F. ( 2007). Correlates of adverse childhood events among adults with schizophrenia spectrum disorders. Psychiatric Services, 58, 245-253.
46. Roth, T. L., Lubin, F. D., Funk, A. J., & Sweatt, J. D. ( 2009). Lasting epigenetic influence of early-life adversity on the BDNF gene. Biological Psychiatry, 65, 760-769.
47. Sailaja, B. S., Cohen-Carmon, D., Zimmerman, G., Soreq, H., & Meshorer, E. ( 2012). Stress-induced epigenetic transcriptional memory of acetylcholinetransferase by HDAC4. Proceedings of National Academy of Science, 109, E3687-E3695.
48. Sando, R 3rd, Gounko, N., Pieraut, S., Liao, L., Yates, J 3rd, & Maximov, A. ( 2012). HDAC4 governs a transcriptional program essential for synaptic plasticity and memory. Cell, 151, 821-834.
49. Satoh, A., & Imai, S. ( 2014). Systemic regulation of mammalian ageing and longevity by brain sirtuins. Nature communications, 5, 1-11.
50. Shih, J., Liu, L., Mason, A., Higashimori, H., & Donmez, G. ( 2014). Loss of Sirt4 decreases GLT-1-dependent glutamate uptake and increases sensitivity to kainic acid. Journal of Neurochemistry, 131, 573-581.
51. Soztutar, E., Colak, E., & Ulupinar, E. ( 2015). Gender- and anxiety level-dependent effects of perinatal stress exposure on medial prefrontal cortex. Experimental Neurology pii: S0014-4886(15)30016-9. doi: 10.1016/2015.06.005 (In press).
52. Stevenson, C. W., Halliday, D. M., Marsden, C. A., & Mason, R. ( 2008). Early life programming of hemispheric lateralization and synchronization in the adult medial prefrontal cortex. Neuroscience, 155, 852-863.
53. Stilling, R. M., Rönicke, R., Benito, E., Urbanke, H., Capece, V., Burkhardt, S., ... & Fischer, A. ( 2014). K-lysine acetyltransferase 2a regulates a hippocampal gene expression network linked to memory formation. The EMBO Journal, 33, 1912-1927.
54. Suri, D., Bhattacharya, A., & Vaidya, V. A. ( 2014). Early stress evokes temporally distinct consequences on the hippocampal transcriptome, anxiety and cognitive behaviour. International Journal of Neuropsychopharmacology, 17, 289-301.
55. Suri, D., Veenit, V., Sarkar, A., Thiagarajan, D., Kumar, A., Nestler, E., ... & Vaidya, V. ( 2013). Early stress evokes age-dependent biphasic changes in hippocampal neurogenesis, BDNF expression and cognition. Biological Psychiatry, 37, 658-666.
56. Sweatt, J. D. ( 2013). The emerging field of neuroepigenetics. Neuron, 80, 624-632.
57. Tordera, R. M., Garcia-García, A. L., Elizalde, N., Segura, V., Aso, E., Venzala, E., ... & Del Rio, J. ( 2011). Chronic stress and impaired glutamate function elicit a depressive-like phenotype and common changes in gene expression in the mouse frontal cortex. European Neuropsychopharmacology, 21(1), 23-32.
58. Tsankova, N. M., Berton, O., Renthal, W., Kumar, A., Neve, R. L., & Nestler, E. J. ( 2006). Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nature Neuroscience, 9, 519-525.
59. Wang, J., Hevi, S., Kurash, J. K., Lei, H., Gay, F., Bajko, J., ... & Chen, T. ( 2009). The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation. Nature Genetics, 41, 125-129.
60. Weiss, I. C., Franklin, T. B., Wizi, S., & Mansuy, I. M. ( 2011). Inheritable effect of unpredictable maternal separation on behavioural responses in mice. Frontiers in Behavioural Neuroscience, 3, 1-12.
61. Wieck, A., Andersen, S. L., & Brenhouse, H. C. ( 2013). Evidence for a neuroinflammatory mechanism in delayed effects of early life adversity in rats: Relationship to cortical NMDA receptor expression. Brain, Behaviour and Immunity, 28, 218-226.
62. Wu, Y. T., Wu, S. B., & Wei, Y. H. ( 2014). Roles of sirtuins in the regulation of antioxidant defense and bioenergetic function of mitochondria under oxidative stress. Free Radical Research, 48, 1070-1084.
63. Zhang, T. Y., Labonté, B., Wen, Z. L., Turecki, G., & Meaney, M. J. ( 2013). Epigenetic mechanisms for the early environmental regulation of hippocampal glucocorticoid receptor gene expression in rodents and humans. Neuropsychopharmacology, 38, 111-123.