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히스톤 3 아세틸화(H3Ac)를 통한 De-Etiolated 1 (DET1)의 애기장대 생체시계 조절

Regulation of Arabidopsis Circadian Clock by De-Etiolated 1 (DET1) Possibly via Histone 3 Acetylation (H3Ac)

  • 송해룡 (국립환경과학원 바이오안전연구팀)
  • Song, Hae-Ryong (Biosafety Research Team, National Institute of Environmental Research (NIER))
  • 투고 : 2012.06.07
  • 심사 : 2012.07.11
  • 발행 : 2012.08.30

초록

자기 현가적(self-sustaining) 조절 장치인 생체시계는 24시간 주기의 생체리듬을 조절하며 또한 생물체로 하여금 매일 변화하는 자연환경의 외부 신호를 인지할 수 있도록 해준다. 생체시계 유전자의 발현 조절은 전사/해독의 역환류 기작을 통해 이루어진다. 애기장대 LATE ELONGATED HYPOCOTYL (LHY)와 CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1)는 아침에 최고조로 발현되며 해독된 LHY and CCA1는 저녁에 최고로 발현되는 TIMING OF CAB EXPRESSION1 (TOC1)의 발현을 억제한다. TOC1단백질은 LHY와 CCA1 발현을 촉진시킴으로써 생체시계의 핵심 진자(oscillator)를 형성한다. 동물에서 생체시계의 주요 전사 인자인CLOCK은 아세틸화효소 활성 기능을 가지며, 이는 생체시계의 기능 유지에 아세틸화의 중요함을 의미한다. 하지만 애기장대 생체시계에 아세틸화를 담당하는 인자에 대한 정보는 현재 보고된 바가 없다. 본 연구에서 DET1 (De-Etiolated1)는 암조건하에서 애기장대 생체시계 관련 핵심인자 중 하나인 LHY발현을 억제하는데 필요하며 이의 억제는 H3Ac 조절을 통해 이루어짐을 증명하였다. 하지만 LHY 아세틸화를 담당하는 효소의 발굴 및 이들 효소와 DET1과의 연결을 찾는 문제는 여전히 미재로 남아있다.

The circadian clock is a self-sustaining 24-hour timekeeper that allows organisms to anticipate daily-changing environmental time cues. Circadian clock genes are regulated by a transcriptional-translational feedback loop. In Arabidopsis, LATE ELONGATED HYPOCOTYL (LHY) and CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1) transcripts are highly expressed in the morning. Translated LHY and CCA1 proteins repress the expression of the TIMING OF CAB EXPRESSION 1 (TOC1) transcripts, which peaks in the evening. The TOC1 protein elevates the expression of the LHY and CCA1 transcripts, forming a negative feedback loop that is believed to constitute the oscillatory mechanism of the clock. In mammals, the transcription factor protein CLOCK, which is a central component of the circadian clock, was reported to have an intrinsic histone acetyltransferase (HAT) activity, suggesting that histone acetylation is important for core clock mechanisms. However, little is known about the components necessary for the histone acetylation of the Arabidopsis clock-related genes. Here, I report that DET1 (De-Etiolated1) functions as a negative regulator of a key component of the Arabidopsis circadian clock gene LHY in constant dark phases (DD) and is required for the down-regulation of LHY expression through the acetylation of histone 3 (H3Ac). However, the HATs directly responsible for the acetylation of H3 within LHY chromatin need to be identified, and a link connecting the HATs and DET1 protein is still absent.

키워드

참고문헌

  1. Alabadí, D., Oyama, T., Yanovsky, M. J., Harmon, F. G., Más, P. and Kay, S. A. 2001. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293, 880-883. https://doi.org/10.1126/science.1061320
  2. Belden, W. J., Loros, J. J. and Dunlap, J. C. 2007. Execution of the circadian negative feedback loop in Neurospora requires the ATP-dependent chromatin-remodeling enzyme CLOCKSWITCH. Mol. Cell 25, 587-600. https://doi.org/10.1016/j.molcel.2007.01.010
  3. Benvenuto, G., Formiggini, F., Laflamme, P., Malakhov, M. and Bowler, C. 2002. The photomorphogenesis regulator DET1 binds the amino-terminal tail of histone H2B in a nucleosome context. Curr. Biol. 12, 1529-1534. https://doi.org/10.1016/S0960-9822(02)01105-3
  4. Berloco, M., Fanti, L., Breiling, A., Orlando, V. and Pimpinelli, V. 2001. The maternal effect gene, abnormal oocyte (abo), of Drosophila melanogaster encodes a specific negative regulator of histones. Proc. Natl. Acad. Sci. USA 98, 12126-12131. https://doi.org/10.1073/pnas.211428798
  5. Brown, S. A., Ripperger, J., Kadener, S., Fleury-Olela, F., Vilbois, F., Rosbash, M. and Schibler, U. 2005. PERIOD1-associated proteins modulate the negative limb of the mammalian circadian oscillator. Science 308, 693-696. https://doi.org/10.1126/science.1107373
  6. Castells, E., Molinier, J., Benvenuto, G., Bourbousse, C., Zabulon, G., Zalc, A., Cazzaniga, S., Genschik, P., Barneche, F. and Bowler, C. 2011. The conserved factor DEETIOLATED 1 cooperates with CUL4-DDB1DDB2 to maintain genome integrity upon UV stress. EMBO J. 30, 1162-1172. https://doi.org/10.1038/emboj.2011.20
  7. Chen, H., Shen, Y., Tang, X., Yu, L., Wang, J., Guo, L., Zhang, Y., Zhang, H., Feng, S., Strickland, E., Zheng, N. and Deng, X. W. 2006. Arabidopsis CULLIN4 forms an E3 ubiquitin ligase with RBX1 and the CDD complex in mediating light control of development. Plant Cell 18, 1991-2004. https://doi.org/10.1105/tpc.106.043224
  8. Chen, Z. J. and Tian, L. 2007. Roles of dynamic and reversible histone acetylation in plant development and polyploidy. Biochim. Biophys. Acta. 1769, 295-307. https://doi.org/10.1016/j.bbaexp.2007.04.007
  9. Chory, J., Peto, C., Feinbaum, R., Pratt, L. and Ausubel, F. 1989. Arabidopsis thaliana mutant that develops as a light-grown plant in the absence of light. Cell 58, 991-999. https://doi.org/10.1016/0092-8674(89)90950-1
  10. Covington, M. F., Maloof, J. N., Straume, M., Kay, S. A. and Harmer, S. L. 2008. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol. 9, R130. https://doi.org/10.1186/gb-2008-9-8-r130
  11. Dodd, A. N., Salathia, N., Hall, A., Kevei, E., Toth, R., Nagy, F., Hibberd, J. M., Millar, A. J. and Webb, A. A. 2005. Plant circadian clocks increase photosynthesis, growth, survival and competitive advantage. Science 309, 630-633. https://doi.org/10.1126/science.1115581
  12. Doi, M., Hirayama, J. and Sassone-Corsi, P. 2006. Circadian regulator CLOCK is a histone acetyltransferase. Cell 125, 497-508. https://doi.org/10.1016/j.cell.2006.03.033
  13. Dowson-Day, M. J. and Millar, A. J. 1999. Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis. Plant J. 17, 63-71. https://doi.org/10.1046/j.1365-313X.1999.00353.x
  14. Dunlap, J. C. 1990. Closely watched clocks: molecular analysis of circadian rhythms in Neurospora and Drosophila. Trends Genet. 6, 159-165. https://doi.org/10.1016/0168-9525(90)90151-U
  15. Etchegaray, J. P., Lee, C., Wade, P. A. and Reppert, S. M. 2003. Rhythmic histone acetylation underlies transcription in the mammalian circadian clock. Nature 421, 177-182. https://doi.org/10.1038/nature01314
  16. Etchegaray, J. P., Yang, X., DeBruyne, J. P., Peters, A. H., Weaver, D. R., Jenuwein, T. and Reppert, S. M. 2006. The polycomb group protein EZH2 is required for mammalian circadian clock function. J. Biol. Chem. 281, 21209-21215. https://doi.org/10.1074/jbc.M603722200
  17. Han, S. K., Song, J. D., Noh, Y. S. and B. Noh, B. 2007. Role of plant CBP/p300-like genes in the regulation of flowering time. Plant J. 49, 103-114.
  18. Harmer, S. L. 2009. The circadian system in higher plants. Annu. Rev. Plant Biol. 60, 357-377. https://doi.org/10.1146/annurev.arplant.043008.092054
  19. Hirayama, J., Sahar, S., Grimaldi, B., Tamaru, T., Takamatsu, K., Nakahata, Y. and Sassone-Corsi, P. 2007. CLOCK-mediated acetylation of BMAL1 controls circadian function. Nature 450, 1086-1090. https://doi.org/10.1038/nature06394
  20. Hollender, C. and Liu, Z. 2008. Histone deacetylase genes in Arabidopsis development. Integr. Plant Biol. 50, 875-885. https://doi.org/10.1111/j.1744-7909.2008.00704.x
  21. Imaizumi, T. and Kay, S. A. 2006. Photoperiodic control of flowering: not only by coincidence. Trends Plant Sci. 11, 550-558. https://doi.org/10.1016/j.tplants.2006.09.004
  22. Lau, O. S., Huang, X., Charron, J. B., Lee, J. H., Li, G. and Deng, X. W. 2011. Interaction of Arabidopsis DET1 with CCA1 and LHY in mediating transcriptional repression in the plant circadian clock. Mol. Cell. 43, 703-712. https://doi.org/10.1016/j.molcel.2011.07.013
  23. Locke, J. C., Kozma-Bognar, L., Gould, P. D., Feher, B., Kevei, E., Nagy, F., Turner, M. S., Hall, A. and Millar, A. J. 2006. Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Mol. Syst. Biol. 2, 59.
  24. McClung, C. R. and Gutiérrez, R. A. 2010. Network news: prime time for systems biology of the plant circadian clock. Curr. Opin. Genet. Dev. 20, 588-598. https://doi.org/10.1016/j.gde.2010.08.010
  25. Millar, A. J., Short, S. R., Hiratsuka, K., Chua, N. -H. and Kay, S. A. 1992. Firefly luciferase as a reporter of regulated gene expression in higher plants. Plant Mol. Biol. Rep. 10, 324-337. https://doi.org/10.1007/BF02668909
  26. Millar, A. J., Straume, M., Chory, J., Chua, N. H. and Kay, S. A. 1995. The regulation of circadian period by phototransduction pathways in Arabidopsis. Science 267, 1163-1166. https://doi.org/10.1126/science.7855596
  27. Moore, R. Y. 1997. Circadian rhythms: basic neurobiology and clinical applications. Annu. Rev. Med. 48, 253-266. https://doi.org/10.1146/annurev.med.48.1.253
  28. Naruse, Y., Oh-hashi, K., Iijima, N., Naruse, M., Yoshioka, H. and Tanaka, M. 2004. Circadian and light-induced transcription of clock gene Per1 depends on histone acetylation and deacetylation. Mol. Cell. Biol. 24, 6278-6287. https://doi.org/10.1128/MCB.24.14.6278-6287.2004
  29. Niwa, Y., Ito, S., Nakamichi, N., Mizoguchi, T., Niinuma, K., Yamashino, T. and Mizuno, T. 2007. Genetic linkages of the circadian clock-associated genes, TOC1, CCA1 and LHY, in the photoperiodic control of flowering time in Arabidopsis thaliana. Plant Cell Physiol. 48, 925-937. https://doi.org/10.1093/pcp/pcm067
  30. Pepper, A., Delaney, T., Washburn, T., Poole, D. and Chory, J. 1994. DET1, a negative regulator of light-mediated development and gene expression in Arabidopsis, encodes a novel nuclear-localized protein. Cell 78, 109-116. https://doi.org/10.1016/0092-8674(94)90577-0
  31. Perales, M. and Más, P. 2007. A functional link between rhythmic changes in chromatin structure and the Arabidopsis biological clock. Plant Cell 19, 2111-2123. https://doi.org/10.1105/tpc.107.050807
  32. Pick, E., Lau, O. S., Tsuge, T., Menon, S., Tong, Y., Dohmae, N., Plafker, S. M., Deng, X. W. and Wei, N. 2007. Mammalian DET1 regulates Cul4A activity and forms stable complexes with E2 ubiquitin-conjugating enzymes. Mol. Cell. Biol. 27, 4708-4719. https://doi.org/10.1128/MCB.02432-06
  33. Pruneda-Paz, J. L., Breton, G., Para, A. and Kay, S. A. 2009. A functional genomics approach reveals CHE as a component of the Arabidopsis circadian clock. Science 323, 1481-1485. https://doi.org/10.1126/science.1167206
  34. Ripperger, J. A. and Schibler, U. 2006. Rhythmic CLOCKBMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions. Nat. Genet. 38, 369-374. https://doi.org/10.1038/ng1738
  35. Roden, L. C., Song, H.-R., Jackson, S., Morris, K. and Carré, I. A. 2002 Floral responses to photoperiod are correlated with the timing of rhythmmic gene expression relative to dawn and dusk, in Arabidopsis. Proc. Natl. Acad. Sci. USA 99, 13313-13318. https://doi.org/10.1073/pnas.192365599
  36. Schaffer, R., Ramsay, N., Samach, A., Corden, S., Putterill, J., Carré, I. A. and Coupland, G. 1998. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93, 1219-1229. https://doi.org/10.1016/S0092-8674(00)81465-8
  37. Schroeder, D. F., Gahrtz, M., Maxwell, B. B., Cook, R. K., Kan, J. M., Alonso, J. M., Ecker, J. R. and Chory, J. 2002. De-etiolated 1 (DET1) and Damaged DNA Binding Protein 1 (DDB1) interact to regulate Arabidopsis photomorphogenesis. Curr. Biol. 12, 1462-1472. https://doi.org/10.1016/S0960-9822(02)01106-5
  38. Song, H.-R. and Noh, Y.-S. 2007. Plants measure the time. J. Plant Biol. 50, 257-265. https://doi.org/10.1007/BF03030653
  39. Wang, Z.-Y. and Tobin, E. M. 1998. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93, 1207-1217. https://doi.org/10.1016/S0092-8674(00)81464-6
  40. Wenden, B., Kozma-Bognar, L., Edwards, K. D., Hall, A. J., Locke, J. C. and Millar, A. J. 2011. Light inputs shape the Arabidopsis circadian system. Plant J. 66, 480-491. https://doi.org/10.1111/j.1365-313X.2011.04505.x
  41. Yamashino, T., Ito, S., Niwa, Y., Kunihiro, A., Nakamichi, N. and Mizuno, T. 2008. Involvement of Arabidopsis clock-associated pseudo-response regulators in diurnal oscillations of gene expression in the presence of environmental time cues. Plant Cell Physiol. 49, 1839-1850. https://doi.org/10.1093/pcp/pcn165
  42. Yanagawa, Y., Sullivan, J. A., Komatsu, S., Gusmaroli, G., Suzuki, G., Yin, J., Ishibashi, T., Saijo, Y., Rubio, V., Kimura, S., Wang, J. and Deng, X. W. 2004. Arabidopsis COP10 forms a complex with DDB1 and DET1 in vivo and enhances the activity of ubiquitin conjugating enzymes. Genes Dev. 18, 2172-2181. https://doi.org/10.1101/gad.1229504
  43. Yerushalmi, S., Yakir, E. and Green, R. M. 2011. Circadian clocks and adaptation in Arabidopsis. Mol. Ecol. 20, 1155-1165. https://doi.org/10.1111/j.1365-294X.2010.04962.x
  44. Zhang, E. E. and Kay, S. A. 2010. Clocks not winding down: unraveling circadian networks. Nat. Rev. Mol. Cell Biol. 11, 764-776. https://doi.org/10.1038/nrm2995