Methylation of histone H3 on lysine 4 by the lysine methyltransferase SET1 protein is needed for normal clock gene expression

Journal of Biological Chemistry

Volumn 288, Issue 12, 2013, Pages 8380-8390

  Raduwan, Hamidah ^a   Isola, Allison L ^a   Belden, William J ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN REGULATION; CLOCK GENES; DATA SUPPORT; DNA METHYLATION; FEED-BACK LOOP; HISTONE H3; MAMMALIAN CELLS; METHYLTRANSFERASES;

ALKYLATION; AMINO ACIDS; CHROMOSOMES; DNA SEQUENCES; METHYLATION; STRAIN; TRANSCRIPTION;

CLOCKS;

DNA; FUNGAL PROTEIN; HISTONE H3; HISTONE LYSINE METHYLTRANSFERASE; LYSINE; PROTEIN SET1; TRANSCRIPTION FACTOR CLOCK; UNCLASSIFIED DRUG; WHITE COLLAR 2 PROTEIN;

ARTICLE; CHROMATIN; CIRCADIAN RHYTHM; CLOCK GENE; CONTROLLED STUDY; DNA METHYLATION; FEEDBACK SYSTEM; FREQUENCY GENE; FUNGAL STRAIN; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; HISTONE METHYLATION; NEUROSPORA CRASSA; NONHUMAN; PHOTODYNAMICS; PRIORITY JOURNAL; PROMOTER REGION;

CIRCADIAN RHYTHM; DNA METHYLATION; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENE KNOCKOUT TECHNIQUES; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; LIGHT; METHYLATION; NEUROSPORA CRASSA; PROTEIN PROCESSING, POST-TRANSLATIONAL; SPORES, FUNGAL; TRANSCRIPTION FACTORS;

EUKARYOTA; MAMMALIA; NEUROSPORA;

EID: 84875260336     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.359935     Document Type: Article

References (83)

1. Dunlap, J. C. (1999) Molecular bases for circadian clocks. Cell 96, 271-290 (Pubitemid 29059356)
2. Young, M. W., and Kay, S. A. (2001) Time zones: a comparative genetics of circadian clocks. Nat. Rev. Genet. 2, 702-715 (Pubitemid 33674792)
3. Panda, S., Hogenesch, J. B., and Kay, S. A. (2002) Circadian rhythms from flies to human. Nature 417, 329-335 (Pubitemid 34534720)
4. Bell-Pedersen, D., Cassone, V. M., Earnest, D. J., Golden, S. S., Hardin, P. E., Thomas, T. L., and Zoran, M. J. (2005) Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat. Rev. Genet. 6, 544-556 (Pubitemid 40910431)
5. O'Neill, J. S., and Reddy, A. B. (2011) Circadian clocks in human red blood cells. Nature 469, 498-503
6. Tomita, J., Nakajima, M., Kondo, T., and Iwasaki, H. (2005) No transcription-translation feedback in circadian rhythm of KaiC phosphorylation. Science 307, 251-254 (Pubitemid 40116239)
7. Reppert, S. M., and Weaver, D. R. (2002) Coordination of circadian timing in mammals. Nature 418, 935-941 (Pubitemid 34976023)
8. Schibler, U., and Sassone-Corsi, P. (2002) A web of circadian pacemakers. Cell 111, 919-922 (Pubitemid 36044683)
9. Heintzen, C., and Liu, Y. (2007) The Neurospora crassa circadian clock. Adv. Genet. 58, 25-66
10. Crosthwaite, S. K., Dunlap, J. C., and Loros, J. J. (1997) Neurospora wc-1 and wc-2: transcription, photoresponses, and the origins of circadian rhythmicity. Science 276, 763-769 (Pubitemid 27199850)
11. Darlington, T. K., Wager-Smith, K., Ceriani, M. F., Staknis, D., Gekakis, N., Steeves, T. D., Weitz, C. J., Takahashi, J. S., and Kay, S. A. (1998) Closing the circadian loop: CLOCK-induced transcription of its own inhibitors per and tim. Science 280, 1599-1603 (Pubitemid 28277704)
12. Rutila, J. E., Suri, V., Le, M., So, W. V., Rosbash, M., and Hall, J. C. (1998) CYCLE is a second bHLH-PAS clock protein essential for circadian rhythmicity and transcription of Drosophila period and timeless. Cell 93, 805-814 (Pubitemid 28257586)
13. Allada, R., White, N. E., So, W. V., Hall, J. C., and Rosbash, M. (1998) A mutant Drosophila homolog of mammalian Clock disrupts circadian rhythms and transcription of period and timeless. Cell 93, 791-804 (Pubitemid 28257585)
14. Antoch, M. P., Song, E. J., Chang, A. M., Vitaterna, M. H., Zhao, Y., Wilsbacher, L. D., Sangoram, A. M., King, D. P., Pinto, L. H., and Takahashi, J. S. (1997) Functional identification of the mouse circadian Clock gene by transgenic BAC rescue. Cell 89, 655-667 (Pubitemid 27511775)
15. Gekakis, N., Staknis, D., Nguyen, H. B., Davis, F. C., Wilsbacher, L. D., King, D. P., Takahashi, J. S., and Weitz, C. J. (1998) Role of the CLOCK protein in the mammalian circadian mechanism. Science 280, 1564-1569 (Pubitemid 28277694)
16. Hogenesch, J. B., Gu, Y. Z., Jain, S., and Bradfield, C. A. (1998) The basichelix- loop-helix-PAS orphan MOP3 forms transcriptionally active complexes with circadian and hypoxia factors. Proc. Natl. Acad. Sci. U.S.A. 95, 5474-5479 (Pubitemid 28224118)
17. Bunger, M. K., Wilsbacher, L. D., Moran, S. M., Clendenin, C., Radcliffe, L. A., Hogenesch, J. B., Simon, M. C., Takahashi, J. S., and Bradfield, C. A. (2000) Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 103, 1009-1017 (Pubitemid 32037390)
18. Aronson, B. D., Johnson, K. A., and Dunlap, J. C. (1994) Circadian clock locus frequency: protein encoded by a single open reading frame defines period length and temperature compensation. Proc. Natl. Acad. Sci. U.S.A. 91, 7683-7687 (Pubitemid 24238249)
19. Cheng, P., He, Q., He, Q., Wang, L., and Liu, Y. (2005) Regulation of the Neurospora circadian clock by an RNA helicase. Genes Dev. 19, 234-241 (Pubitemid 40111119)
20. Hardin, P. E., Hall, J. C., and Rosbash, M. (1990) Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 343, 536-540
21. Sehgal, A., Rothenfluh-Hilfiker, A., Hunter-Ensor, M., Chen, Y., Myers, M. P., and Young, M. W. (1995) Rhythmic expression of timeless: a basis for promoting circadian cycles in period gene autoregulation. Science 270, 808-810
22. Shearman, L. P., Zylka, M. J., Weaver, D. R., Kolakowski, L. F., Jr., and Reppert, S. M. (1997) Two period homologs: circadian expression and photic regulation in the suprachiasmatic nuclei. Neuron 19, 1261-1269 (Pubitemid 28030545)
23. Sun, Z. S., Albrecht, U., Zhuchenko, O., Bailey, J., Eichele, G., and Lee, C. C. (1997) RIGUI, a putative mammalian ortholog of the Drosophila period gene. Cell 90, 1003-1011 (Pubitemid 27408514)
24. Tei, H., Okamura, H., Shigeyoshi, Y., Fukuhara, C., Ozawa, R., Hirose, M., and Sakaki, Y. (1997) Circadian oscillation of a mammalian homologue of the Drosophila period gene. Nature 389, 512-516 (Pubitemid 27435329)
25. Kume, K., Zylka, M. J., Sriram, S., Shearman, L. P., Weaver, D. R., Jin, X., Maywood, E. S., Hastings, M. H., and Reppert, S. M. (1999) mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98, 193-205 (Pubitemid 29344907)
26. Kloss, B., Price, J. L., Saez, L., Blau, J., Rothenfluh, A., Wesley, C. S., and Young, M. W. (1998) The Drosophila clock gene double-time encodes a protein closely related to human casein kinase I-. Cell 94, 97-107 (Pubitemid 28347473)
27. Lin, J. M., Kilman, V. L., Keegan, K., Paddock, B., Emery-Le, M., Rosbash, M., and Allada, R. (2002) A role for casein kinase 2' in the Drosophila circadian clock. Nature 420, 816-820 (Pubitemid 36019629)
28. Martinek, S., Inonog, S., Manoukian, A. S., and Young, M. W. (2001)Arole for the segment polarity gene shaggy/GSK-3 in the Drosophila circadian clock. Cell 105, 769-779 (Pubitemid 32635106)
29. Liu, Y., Loros, J., and Dunlap, J. C. (2000) Phosphorylation of the Neurospora clock protein FREQUENCY determines its degradation rate and strongly influences the period length of the circadian clock. Proc. Natl. Acad. Sci. U.S.A. 97, 234-239 (Pubitemid 30055814)
30. Lowrey, P. L., Shimomura, K., Antoch, M. P., Yamazaki, S., Zemenides, P. D., Ralph, M. R., Menaker, M., and Takahashi, J. S. (2000) Positional syntenic cloning and functional characterization of the mammalian circadian mutation tau. Science 288, 483-492
31. Garceau, N. Y., Liu, Y., Loros, J. J., and Dunlap, J. C. (1997) Alternative initiation of translation and time-specific phosphorylation yield multiple forms of the essential clock protein FREQUENCY. Cell 89, 469-476 (Pubitemid 27220891)
32. Chiu, J. C., Vanselow, J. T., Kramer, A., and Edery, I. (2008) The phosphooccupancy of an atypical SLIMB-binding site onPERIODthat is phosphorylated by DOUBLETIME controls the pace of the clock. Genes Dev. 22, 1758-1772 (Pubitemid 351915501)
33. He, Q., Cha, J., He, Q., Lee, H. C., Yang, Y., and Liu, Y. (2006) CKI and CKII mediate the FREQUENCY-dependent phosphorylation of the WHITE COLLAR complex to close the Neurospora circadian negative feedback loop. Genes Dev. 20, 2552-2565 (Pubitemid 44396840)
34. Lee, C., Etchegaray, J. P., Cagampang, F. R., Loudon, A. S., and Reppert, S. M. (2001) Post-translational mechanisms regulate the mammalian circadian clock. Cell 107, 855-867 (Pubitemid 34084977)
35. Ko, H. W., Jiang, J., and Edery, I. (2002) Role for Slimb in the degradation of Drosophila Period protein phosphorylated by Doubletime. Nature 420, 673-678 (Pubitemid 36764499)
36. He, Q., Cheng, P., He, Q., and Liu, Y. (2005) The COP9 signalosome regulates the Neurospora circadian clock by controlling the stability of the SCFFWD-1 complex. Genes Dev. 19, 1518-1531 (Pubitemid 41002996)
37. He, Q., Cheng, P., Yang, Y., He, Q., Yu, H., and Liu, Y. (2003) FWD1- mediated degradation of FREQUENCY in Neurospora establishes a conserved mechanism for circadian clock regulation.EMBOJ. 22, 4421-4430 (Pubitemid 37087196)
38. Querfurth, C., Diernfellner, A. C., Gin, E., Malzahn, E., Höfer, T., and Brunner, M. (2011) Circadian conformational change of the Neurospora clock protein FREQUENCY triggered by clustered hyperphosphorylation of a basic domain. Mol. Cell 43, 713-722
39. Belden, W. J., Lewis, Z. A., Selker, E. U., Loros, J. J., and Dunlap, J. C. (2011) CHD1 remodels chromatin and influences transient DNA methylation at the clock gene frequency. PLoS Genet. 7, e1002166
40. 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 (Pubitemid 46274440)
41. Duong, H. A., Robles, M. S., Knutti, D., and Weitz, C. J. (2011)Amolecular mechanism for circadian clock negative feedback. Science 332, 1436-1439
42. DiTacchio, L., Le, H. D., Vollmers, C., Hatori, M., Witcher, M., Secombe, J., and Panda, S. (2011) Histone lysine demethylase JARID1a activates CLOCK-BMAL1 and influences the circadian clock. Science 333, 1881-1885
43. Jones, M. A., Covington, M. F., DiTacchio, L., Vollmers, C., Panda, S., and Harmer, S. L. (2010) Jumonji domain protein JMJD5 functions in both the plant and human circadian systems. Proc. Natl. Acad. Sci. U.S.A. 107, 21623-21628
44. Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389, 251-260 (Pubitemid 27406632)
45. Smith, E., and Shilatifard, A. (2010) The chromatin signaling pathway: diverse mechanisms of recruitment of histone-modifying enzymes and varied biological outcomes. Mol. Cell 40, 689-701
46. Ripperger, J. A., and Schibler, U. (2006) Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions. Nat. Genet. 38, 369-374
47. 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 (Pubitemid 36090986)
48. Curtis, A. M., Seo, S. B., Westgate, E. J., Rudic, R. D., Smyth, E. M., Chakravarti, D., FitzGerald, G. A., and McNamara, P. (2004) Histone acetyltransferase- dependent chromatin remodeling and the vascular clock. J. Biol. Chem. 279, 7091-7097 (Pubitemid 38248855)
49. Doi, M., Hirayama, J., and Sassone-Corsi, P. (2006) Circadian regulator CLOCK is a histone acetyltransferase. Cell 125, 497-508
50. 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 (Pubitemid 38891129)
51. Nakahata, Y., Kaluzova, M., Grimaldi, B., Sahar, S., Hirayama, J., Chen, D., Guarente, L. P., and Sassone-Corsi, P. (2008) The NAD-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell 134, 329-340
52. Asher, G., Gatfield, D., Stratmann, M., Reinke, H., Dibner, C., Kreppel, F., Mostoslavsky, R., Alt, F. W., and Schibler, U. (2008) SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 134, 317-328 (Pubitemid 352024391)
53. Guillaumond, F., Boyer, B., Becquet, D., Guillen, S., Kuhn, L., Garin, J., Belghazi, M., Bosler, O., Franc, J. L., and François-Bellan, A. M. (2011) Chromatin remodeling as a mechanism for circadian prolactin transcription: rhythmic NONO and SFPQ recruitment to HLTF. FASEB J. 25, 2740-2756
54. 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 (Pubitemid 44115460)
55. Katada, S., and Sassone-Corsi, P. (2010) The histone methyltransferase MLL1 permits the oscillation of circadian gene expression. Nat. Struct. Mol. Biol. 17, 1414-1421
56. Lee, H. C., Li, L., Gu, W., Xue, Z., Crosthwaite, S. K., Pertsemlidis, A., Lewis, Z. A., Freitag, M., Selker, E. U., Mello, C. C., and Liu, Y. (2010) Diverse pathways generate microRNA-like RNAs and Dicer-independent small interfering RNAs in fungi. Mol. Cell 38, 803-814
57. Dubruille, R., Murad, A., Rosbash, M., and Emery, P. (2009) A constant light-genetic screen identifies KISMET as a regulator of circadian photoresponses. PLoS Genet. 5, e1000787
58. Belden, W. J., Larrondo, L. F., Froehlich, A. C., Shi, M., Chen, C. H., Loros, J. J., and Dunlap, J. C. (2007) The band mutation in Neurospora crassa is a dominant allele of ras-1 implicating RAS signaling in circadian output. Genes Dev. 21, 1494-1505 (Pubitemid 46955722)
59. Gooch, V. D., Mehra, A., Larrondo, L. F., Fox, J., Touroutoutoudis, M., Loros, J. J., and Dunlap, J. C. (2008) Fully codon-optimized luciferase uncovers novel temperature characteristics of the Neurospora clock. Eukaryot. Cell 7, 28-37 (Pubitemid 351959591)
60. Edelstein, A., Amodaj, N., Hoover, K., Vale, R., and Stuurman, N. (2010) Computer control of microscopes using -Manager. Curr. Protoc. Mol. Biol. Chapter 14, Unit 14.20.1-14.20.17
61. Lee, K., Loros, J. J., and Dunlap, J. C. (2000) Interconnected feedback loops in the Neurospora circadian system. Science 289, 107-110 (Pubitemid 30463301)
62. Luo, C., Loros, J. J., and Dunlap, J. C. (1998) Nuclear localization is required for function of the essential clock protein FRQ. EMBO J. 17, 1228-1235 (Pubitemid 28105502)
63. Komarnitsky, P., Cho, E. J., and Buratowski, S. (2000) Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev. 14, 2452-2460
64. Kuras, L., and Struhl, K. (1999) Binding of TBP to promoters in vivo is stimulated by activators and requires Pol II holoenzyme. Nature 399, 609-613
65. Smith, K. M., Sancar, G., Dekhang, R., Sullivan, C. M., Li, S., Tag, A. G., Sancar, C., Bredeweg, E. L., Priest, H. D., McCormick, R. F., Thomas, T. L., Carrington, J. C., Stajich, J. E., Bell-Pedersen, D., Brunner, M., and Freitag, M. (2010) Transcription factors in light and circadian clock signaling networks revealed by genome-wide mapping of direct targets for Neurospora white collar complex. Eukaryot. Cell 9, 1549-1556
66. Denault, D. L., Loros, J. J., and Dunlap, J. C. (2001) WC-2 mediates WC- 1-FRQ interaction within the PAS protein-linked circadian feedback loop of Neurospora. EMBO J. 20, 109-117 (Pubitemid 32099107)
67. Colot, H. V., Park, G., Turner, G. E., Ringelberg, C., Crew, C. M., Litvinkova, L., Weiss, R. L., Borkovich, K. A., and Dunlap, J. C. (2006) A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl. Acad. Sci. U.S.A. 103, 10352-10357 (Pubitemid 44051170)
68. Sims, R. J., 3rd, Chen, C. F., Santos-Rosa, H., Kouzarides, T., Patel, S. S., and Reinberg, D. (2005) Human but not yeast CHD1 binds directly and selectively to histone H3 methylated at lysine 4 via its tandem chromodomains. J. Biol. Chem. 280, 41789-41792 (Pubitemid 43023146)
69. Sims, R. J., 3rd, Millhouse, S., Chen, C. F., Lewis, B. A., Erdjument-Bromage, H., Tempst, P., Manley, J. L., and Reinberg, D. (2007) Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Mol. Cell 28, 665-676 (Pubitemid 350137805)
70. Flanagan, J. F., Blus, B. J., Kim, D., Clines, K. L., Rastinejad, F., and Khorasanizadeh, S. (2007) Molecular implications of evolutionary differences in CHD double chromodomains. J. Mol. Biol. 369, 334-342 (Pubitemid 46678044)
71. Miller, T., Krogan, N. J., Dover, J., Erdjument-Bromage, H., Tempst, P., Johnston, M., Greenblatt, J. F., and Shilatifard, A. (2001) COMPASS: a complex of proteins associated with a trithorax-related SET domain protein. Proc. Natl. Acad. Sci. U.S.A. 98, 12902-12907 (Pubitemid 33051292)
72. Briggs, S. D., Bryk, M., Strahl, B. D., Cheung, W. L., Davie, J. K., Dent, S. Y., Winston, F., and Allis, C. D. (2001) Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev. 15, 3286-3295 (Pubitemid 34008193)
73. Krogan, N. J., Dover, J., Khorrami, S., Greenblatt, J. F., Schneider, J., Johnston, M., and Shilatifard, A. (2002) COMPASS, a histone H3 (lysine 4) methyltransferase required for telomeric silencing of gene expression. J. Biol. Chem. 277, 10753-10755 (Pubitemid 34952826)
74. Liu, C. L., Kaplan, T., Kim, M., Buratowski, S., Schreiber, S. L., Friedman, N., and Rando, O. J. (2005) Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol. 3, e328
75. Barski, A., Cuddapah, S., Cui, K., Roh, T. Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I., and Zhao, K. (2007) High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837 (Pubitemid 46802390)
76. Collins, G. A., and Tansey, W. P. (2006) The proteasome: a utility tool for transcription? Curr. Opin. Genet. Dev. 16, 197-202 (Pubitemid 43376068)
77. Stratmann, M., Suter, D. M., Molina, N., Naef, F., and Schibler, U. (2012) Circadian Dbp transcription relies on highly dynamic BMAL1-CLOCK interaction with E boxes and requires the proteasome. Mol. Cell 48, 277-287
78. Talora, C., Franchi, L., Linden, H., Ballario, P., and Macino, G. (1999) Role of a white collar-1-white collar-2 complex in blue-light signal transduction. EMBO J. 18, 4961-4968 (Pubitemid 29443798)
79. Thomson, J. P., Skene, P. J., Selfridge, J., Clouaire, T., Guy, J., Webb, S., Kerr, A. R., Deaton, A., Andrews, R., James, K. D., Turner, D. J., Illingworth, R., and Bird, A. (2010) CpG islands influence chromatin structure via the CpG-binding protein Cfp1. Nature 464, 1082-1086
80. Tamaru, H., and Selker, E. U. (2001) A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414, 277-283 (Pubitemid 33097798)
81. Venkatasubrahmanyam, S., Hwang, W. W., Meneghini, M. D., Tong, A. H., and Madhani, H. D. (2007) Genome-wide, as opposed to local, antisilencing is mediated redundantly by the euchromatic factors Set1 and H2A.Z. Proc. Natl. Acad. Sci. U.S.A. 104, 16609-16614 (Pubitemid 350211064)
82. 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 (Pubitemid 40594390)
83. Loros, J. J., Richman, A., and Feldman, J. F. (1986) A recessive circadian clock mutation at the frq locus of Neurospora crassa. Genetics 114, 1095-1110 (Pubitemid 17219785)