A critical role for dynamic changes in histone H3 methylation at the Bdnf promoter during postnatal thermotolerance acquisition

European Journal of Neuroscience

Volumn 30, Issue 10, 2009, Pages 1909-1922

  Kisliouk, Tatiana ^a   Meiri, Noam ^a  

^a VOLCANI CENTER   (Israel)

Author keywords

Chick; Chromatin modifications; Critical developmental period; EZH2; Hypothalamus; Thermoregulation

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; HISTONE H3; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; GENE SILENCING; GENETIC TRANSCRIPTION; HEAT TOLERANCE; HYPOTHALAMUS; IMMUNOFLUORESCENCE TEST; MALE; NERVE CELL PLASTICITY; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN METHYLATION; PROTEIN MODIFICATION; REAL TIME POLYMERASE CHAIN REACTION; THERMOREGULATION; WESTERN BLOTTING;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANIMALS, NEWBORN; BODY TEMPERATURE REGULATION; BRAIN-DERIVED NEUROTROPHIC FACTOR; CHICKENS; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HYPOTHALAMUS, ANTERIOR; IN SITU NICK-END LABELING; MALE; METHYLATION; OLIGODEOXYRIBONUCLEOTIDES, ANTISENSE; OXIDOREDUCTASES, N-DEMETHYLATING; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; TIME FACTORS;

EID: 70449720612     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2009.06957.x     Document Type: Article

References (46)

1. Bannister, A.J. Kouzarides, T. (2005) Reversing histone methylation. Nature, 436, 1103 1106.
2. Barco, A., Patterson, S., Alarcon, J.M., Gromova, P., Mata-Roig, M., Morozov, A. Kandel, E.R. (2005) Gene expression profiling of facilitated L-LTP in VP16-CREB mice reveals that BDNF is critical for the maintenance of LTP and its synaptic capture. Neuron, 48, 123 137.
3. Berger, S.L. (2007) The complex language of chromatin regulation during transcription. Nature, 447, 407 412.
4. Boulant, J.A. (2006) Neuronal basis of Hammel's model for set-point thermoregulation. J. Appl. Physiol., 100, 1347 1354.
5. Bredy, T.W., Wu, H., Crego, C., Zellhoefer, J., Sun, Y.E. 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.
6. Cao, R. Zhang, Y. (2004a) SUZ12 is required for both the histone methyltransferase activity and the silencing function of the EED-EZH2 complex. Mol. Cell, 15, 57 67.
7. Cao, R. Zhang, Y. (2004b) The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr. Opin. Genet. Dev., 14, 155 164.
8. Cao, R., Wang, L., Wang, H., Xia, L., Erdjument-Bromage, H., Tempst, P., Jones, R.S. Zhang, Y. (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science, 298, 1039 1043.
9. Chandramohan, Y., Droste, S.K. Reul, J.M. (2007) 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. J. Neurochem., 101, 815 828.
10. Chang, S. Aune, T.M. (2007) Dynamic changes in histone-methylation 'marks' across the locus encoding interferon-gamma during the differentiation of T helper type 2 cells. Nat. Immunol., 8, 723 731.
11. Chwang, W.B., O'Riordan, K.J., Levenson, J.M. Sweatt, J.D. (2006) ERK/MAPK regulates hippocampal histone phosphorylation following contextual fear conditioning. Learn. Mem., 13, 322 328.
12. Erhardt, S., Su, I.H., Schneider, R., Barton, S., Bannister, A.J., Perez-Burgos, L., Jenuwein, T., Kouzarides, T., Tarakhovsky, A. Surani, M.A. (2003) Consequences of the depletion of zygotic and embryonic enhancer of zeste 2 during preimplantation mouse development. Development, 130, 4235 4248.
13. Fischer, A., Sananbenesi, F., Wang, X., Dobbin, M. Tsai, L.H. (2007) Recovery of learning and memory is associated with chromatin remodelling. Nature, 447, 178 182.
14. Guan, Z., Giustetto, M., Lomvardas, S., Kim, J.H., Miniaci, M.C., Schwartz, J.H., Thanos, D. Kandel, E.R. (2002) Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell, 111, 483 493.
15. Huang, Z.J., Kirkwood, A., Pizzorusso, T., Porciatti, V., Morales, B., Bear, M.F., Maffei, L. Tonegawa, S. (1999) BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell, 98, 739 755.
16. Kang, H. Schuman, E.M. (1995) Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science, 267, 1658 1662.
17. Katz, A. Meiri, N. (2006) Brain-derived neurotrophic factor is critically involved in thermal-experience-dependent developmental plasticity. J. Neurosci., 26, 3899 3907.
18. Kim, S.Y., Levenson, J.M., Korsmeyer, S., Sweatt, J.D. Schumacher, A. (2007) Developmental regulation of Eed complex composition governs a switch in global histone modification in brain. J. Biol. Chem., 282, 9962 9972.
19. Kouzarides, T. (2007) Chromatin modifications and their function. Cell, 128, 693 705.
20. Kuzmichev, A., Jenuwein, T., Tempst, P. Reinberg, D. (2004) Different EZH2-containing complexes target methylation of histone H1 or nucleosomal histone H3. Mol. Cell, 14, 183 193.
21. Labunskay, G. Meiri, N. (2006) R-Ras3/(M-Ras) is involved in thermal adaptation in the critical period of thermal control establishment. J. Neurobiol., 66, 56 70.
22. Lachner, M. Jenuwein, T. (2002) The many faces of histone lysine methylation. Curr. Opin. Cell Biol., 14, 286 298.
23. Lee, M.G., Villa, R., Trojer, P., Norman, J., Yan, K.P., Reinberg, D., Croce, L.D. Shiekhattar, R. (2007) Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science, 318, 447 450.
24. Levenson, J.M. Sweatt, J.D. (2005) Epigenetic mechanisms in memory formation. Nat. Rev. Neurosci., 6, 108 118.
25. Levenson, J.M., O'Riordan, K.J., Brown, K.D., Trinh, M.A., Molfese, D.L. Sweatt, J.D. (2004) Regulation of histone acetylation during memory formation in the hippocampus. J. Biol. Chem., 279, 40545 40559.
26. Levin, B.E. (2007) Neurotrophism and energy homeostasis: perfect together. Am. J. Physiol. Regul. Integr. Comp. Physiol., 293, R988 R991.
27. Metzger, E., Wissmann, M., Yin, N., Muller, J.M., Schneider, R., Peters, A.H., Gunther, T., Buettner, R. Schule, R. (2005) LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature, 437, 436 439.
28. Naert, G., Ixart, G., Tapia-Arancibia, L. Givalois, L. (2006) Continuous i.c.v. infusion of brain-derived neurotrophic factor modifies hypothalamic-pituitary-adrenal axis activity, locomotor activity and body temperature rhythms in adult male rats. Neuroscience, 139, 779 789.
29. Nicholson, J.R., Peter, J.C., Lecourt, A.C., Barde, Y.A. Hofbauer, K.G. (2007) Melanocortin-4 receptor activation stimulates hypothalamic brain-derived neurotrophic factor release to regulate food intake, body temperature and cardiovascular function. J. Neuroendocrinol., 19, 974 982.
30. O'Carroll, D., Erhardt, S., Pagani, M., Barton, S.C., Surani, M.A. Jenuwein, T. (2001) The polycomb-group gene Ezh2 is required for early mouse development. Mol. Cell. Biol., 21, 4330 4336.
31. Pasini, D., Bracken, A.P., Hansen, J.B., Capillo, M. Helin, K. (2007) The polycomb group protein Suz12 is required for embryonic stem cell differentiation. Mol. Cell. Biol., 27, 3769 3779.
32. Patterson, S.L., Abel, T., Deuel, T.A., Martin, K.C., Rose, J.C. Kandel, E.R. (1996) Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron, 16, 1137 1145.
33. Roh, T.Y., Cuddapah, S., Cui, K. Zhao, K. (2006) The genomic landscape of histone modifications in human T cells. Proc. Natl Acad. Sci. USA, 103, 15782 15787.
34. Rothwell, N.J. (1990) Central effects of CRF on metabolism and energy balance. Neurosci. Biobehav. Rev., 14, 263 271.
35. Soshnikova, N. Duboule, D. (2008) Epigenetic regulation of Hox gene activation: the waltz of methyls. BioEssays, 30, 199 202.
36. Trewick, S.C., McLaughlin, P.J. Allshire, R.C. (2005) Methylation: lost in hydroxylation? EMBO Rep., 6, 315 320.
37. Trojer, P. Reinberg, D. (2006) Histone lysine demethylases and their impact on epigenetics. Cell, 125, 213 217.
38. Tsankova, N.M., Kumar, A. Nestler, E.J. (2004) Histone modifications at gene promoter regions in rat hippocampus after acute and chronic electroconvulsive seizures. J. Neurosci., 24, 5603 5610.
39. 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. Nat. Neurosci., 9, 519 525.
40. Tzschentke, B. Basta, D. (2002) Early development of neuronal hypothalamic thermosensitivity in birds: influence of epigenetic temperature adaptation. Comp. Biochem. Physiol. A. Mol. Integr. Physiol., 131, 825 832.
41. Vakoc, C.R., Mandat, S.A., Olenchock, B.A. Blobel, G.A. (2005) Histone H3 lysine 9 methylation and HP1gamma are associated with transcription elongation through mammalian chromatin. Mol. Cell, 19, 381 391.
42. Vakoc, C.R., Sachdeva, M.M., Wang, H. Blobel, G.A. (2006) Profile of histone lysine methylation across transcribed mammalian chromatin. Mol. Cell. Biol., 26, 9185 9195.
43. Weaver, I.C., Cervoni, N., Champagne, F.A., D'Alessio, A.C., Sharma, S., Seckl, J.R., Dymov, S., Szyf, M. Meaney, M.J. (2004) Epigenetic programming by maternal behavior. Nat. Neurosci., 7, 847 854.
44. Yahav, S. McMurtry, J.P. (2001) Thermotolerance acquisition in broiler chickens by temperature conditioning early in life - the effect of timing and ambient temperature. Poult. Sci., 80, 1662 1666.
45. Yossifoff, M., Kisliouk, T. Meiri, N. (2008) Dynamic changes in DNA methylation during thermal control establishment affect CREB binding to the brain-derived neurotrophic factor promoter. Eur. J. Neurosci., 28, 2267 2277.
46. Zhang, Y. Reinberg, D. (2001) Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev., 15, 2343 2360.