Mechanism of the Neurospora circadian clock, a FREQUENCY-centric view

Biochemistry

Volumn 54, Issue 2, 2015, Pages 150-156

  Cha, Joonseok ^a   Zhou, Mian ^a   Liu, Yi ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY;

CIRCADIAN CLOCK; CORE CLOCK; FILAMENTOUS FUNGI; NEUROSPORA; NEUROSPORA CIRCADIAN CLOCK; NEUROSPORA CRASSA; REGULATORY MECHANISM;

CLOCKS;

PROTEIN FRQ; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR WHITE COLLAR COMPLEX; UNCLASSIFIED DRUG; FRQ PROTEIN, NEUROSPORA CRASSA; FUNGAL PROTEIN;

ARTICLE; CHROMATIN; CIRCADIAN RHYTHM; CODON USAGE; GENE EXPRESSION; GENE LOCUS; MOLECULAR DYNAMICS; NEGATIVE FEEDBACK; NEUROSPORA CRASSA; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN STABILITY; REGULATORY MECHANISM; TRANSCRIPTION REGULATION; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

EUKARYOTA; FUNGI; NEUROSPORA; NEUROSPORA CRASSA;

CIRCADIAN CLOCKS; FEEDBACK, PHYSIOLOGICAL; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; NEUROSPORA CRASSA;

EID: 84922476122     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi5005624     Document Type: Article

References (91)

1. Dunlap, J. C. (1999) Molecular bases for circadian clocks Cell 96, 271-290
2. Young, M. W. and Kay, S. A. (2001) Time zones: A comparative genetics of circadian clocks Nat. Rev. Genet. 2, 702-715
3. Heintzen, C. and Liu, Y. (2007) The Neurospora crassa circadian clock Adv. Genet. 58, 25-66
4. Cha, J., Huang, G., Guo, J., and Liu, Y. (2007) Posttranslational control of the Neurospora circadian clock Cold Spring Harbor Symp. Quant. Biol. 72, 185-191
5. Lakin-Thomas, P. L., Bell-Pedersen, D., and Brody, S. (2011) The genetics of circadian rhythms in Neurospora Adv. Genet. 74, 55-103
6. Sargent, M. L., Briggs, W. R., and Woodward, D. O. (1966) Circadian nature of a rhythm expressed by an invertaseless strain of Neurospora crassa Plant Physiol. 41, 1343-1349
7. 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 Eukaryotic Cell 7, 28-37
8. 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
9. Aronson, B. D., Johnson, K. A., Loros, J. J., and Dunlap, J. C. (1994) Negative feedback defining a circadian clock: Autoregulation of the clock gene frequency Science 263, 1578-1584
10. Cheng, P., He, Q., Wang, L., and Liu, Y. (2005) Regulation of the Neurospora circadian clock by an RNA helicase Genes Dev. 19, 234-241
11. 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
12. Cheng, P., Yang, Y., Gardner, K. H., and Liu, Y. (2002) PAS domain-mediated WC-1/WC-2 interaction is essential for maintaining the steady-state level of WC-1 and the function of both proteins in circadian clock and light responses of Neurospora Mol. Cell. Biol. 22, 517-524
13. Cheng, P., Yang, Y., Wang, L., He, Q., and Liu, Y. (2003) WHITE COLLAR-1, a multifunctional neurospora protein involved in the circadian feedback loops, light sensing, and transcription repression of wc-2 J. Biol. Chem. 278, 3801-3808
14. Froehlich, A. C., Loros, J. J., and Dunlap, J. C. (2003) Rhythmic binding of a WHITE COLLAR-containing complex to the frequency promoter is inhibited by FREQUENCY Proc. Natl. Acad. Sci. U.S.A. 100, 5914-5919
15. 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
16. 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
17. 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
18. Gorl, M., Merrow, M., Huttner, B., Johnson, J., Roenneberg, T., and Brunner, M. (2001) A PEST-like element in FREQUENCY determines the length of the circadian period in Neurospora crassa EMBO J. 20, 7074-7084
19. 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 EMBO J. 22, 4421-4430
20. Yang, Y., Cheng, P., He, Q., Wang, L., and Liu, Y. (2003) Phosphorylation of FREQUENCY protein by casein kinase II is necessary for the function of the Neurospora circadian clock Mol. Cell. Biol. 23, 6221-6228
21. He, Q., Cha, J., 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
22. Tang, C. T., Li, S., Long, C., Cha, J., Huang, G., Li, L., Chen, S., and Liu, Y. (2009) Setting the pace of the Neurospora circadian clock by multiple independent FRQ phosphorylation events Proc. Natl. Acad. Sci. U.S.A. 106, 10722-10727
23. Cheng, P., Yang, Y., and Liu, Y. (2001) Interlocked feedback loops contribute to the robustness of the Neurospora circadian clock Proc. Natl. Acad. Sci. U.S.A. 98, 7408-7413
24. Schafmeier, T., Kaldi, K., Diernfellner, A., Mohr, C., and Brunner, M. (2006) Phosphorylation-dependent maturation of Neurospora circadian clock protein from a nuclear repressor toward a cytoplasmic activator Genes Dev. 20, 297-306
25. McClung, C. R., Fox, B. A., and Dunlap, J. C. (1989) The Neurospora clock gene frequency shares a sequence element with the Drosophila clock gene period Nature 339, 558-562
26. Cheng, P., Yang, Y., Heintzen, C., and Liu, Y. (2001) Coiled-coil domain-mediated FRQ-FRQ interaction is essential for its circadian clock function in Neurospora EMBO J. 20, 101-108
27. 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
28. Guo, J., Cheng, P., and Liu, Y. (2010) Functional significance of FRH in regulating the phosphorylation and stability of Neurospora circadian clock protein FRQ J. Biol. Chem. 285, 11508-11515
29. Guo, J., Cheng, P., Yuan, H., and Liu, Y. (2009) The exosome regulates circadian gene expression in a posttranscriptional negative feedback loop Cell 138, 1236-1246
30. Shi, M., Collett, M., Loros, J. J., and Dunlap, J. C. (2010) FRQ-interacting RNA helicase mediates negative and positive feedback in the Neurospora circadian clock Genetics 184, 351-361
31. Hurley, J. M., Larrondo, L. F., Loros, J. J., and Dunlap, J. C. (2013) Conserved RNA helicase FRH acts nonenzymatically to support the intrinsically disordered Neurospora clock protein FRQ Mol. Cell 52, 832-843
32. Yang, Y., He, Q., Cheng, P., Wrage, P., Yarden, O., and Liu, Y. (2004) Distinct roles for PP1 and PP2A in the Neurospora circadian clock Genes Dev. 18, 255-260
33. Schafmeier, T., Haase, A., Kaldi, K., Scholz, J., Fuchs, M., and Brunner, M. (2005) Transcriptional feedback of Neurospora circadian clock gene by phosphorylation-dependent inactivation of its transcription factor Cell 122, 235-246
34. He, Q., Shu, H., Cheng, P., Chen, S., Wang, L., and Liu, Y. (2005) Light-independent phosphorylation of WHITE COLLAR-1 regulates its function in the Neurospora circadian negative feedback loop J. Biol. Chem. 280, 17526-17532
35. Zhou, Z., Liu, X., Hu, Q., Zhang, N., Sun, G., Cha, J., Wang, Y., Liu, Y., and He, Q. (2013) Suppression of WC-independent frequency transcription by RCO-1 is essential for Neurospora circadian clock Proc. Natl. Acad. Sci. U.S.A. 110, E4867-E4874
36. Yang, Y., Cheng, P., Zhi, G., and Liu, Y. (2001) Identification of a calcium/calmodulin-dependent protein kinase that phosphorylates the Neurospora circadian clock protein FREQUENCY J. Biol. Chem. 276, 41064-41072
37. 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
38. He, Q. and Liu, Y. (2005) Degradation of the Neurospora circadian clock protein FREQUENCY through the ubiquitin-proteasome pathway Biochem. Soc. Trans. 33, 953-956
39. Pregueiro, A. M., Liu, Q., Baker, C. L., Dunlap, J. C., and Loros, J. J. (2006) The Neurospora checkpoint kinase 2: A regulatory link between the circadian and cell cycles Science 313, 644-649
40. Huang, G., Chen, S., Li, S., Cha, J., Long, C., Li, L., He, Q., and Liu, Y. (2007) Protein kinase A and casein kinases mediate sequential phosphorylation events in the circadian negative feedback loop Genes Dev. 21, 3283-3295
41. Cha, J., Chang, S. S., Huang, G., Cheng, P., and Liu, Y. (2008) Control of WHITE COLLAR localization by phosphorylation is a critical step in the circadian negative feedback process EMBO J. 27, 3246-3255
42. Baker, C. L., Kettenbach, A. N., Loros, J. J., Gerber, S. A., and Dunlap, J. C. (2009) Quantitative proteomics reveals a dynamic interactome and phase-specific phosphorylation in the Neurospora circadian clock Mol. Cell 34, 354-363
43. Schafmeier, T., Diernfellner, A., Schafer, A., Dintsis, O., Neiss, A., and Brunner, M. (2008) Circadian activity and abundance rhythms of the Neurospora clock transcription factor WCC associated with rapid nucleo-cytoplasmic shuttling Genes Dev. 22, 3397-3402
44. 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
45. Cha, J., Zhou, M., and Liu, Y. (2013) CATP is a critical component of the Neurospora circadian clock by regulating the nucleosome occupancy rhythm at the frequency locus EMBO Rep. 14, 923-930
46. Lee, K., Loros, J. J., and Dunlap, J. C. (2000) Interconnected feedback loops in the Neurospora circadian system Science 289, 107-110
47. Merrow, M., Franchi, L., Dragovic, Z., Gorl, M., Johnson, J., Brunner, M., Macino, G., and Roenneberg, T. (2001) Circadian regulation of the light input pathway in Neurospora crassa EMBO J. 20, 307-315
48. Glossop, N. R., Lyons, L. C., and Hardin, P. E. (1999) Interlocked feedback loops within the Drosophila circadian oscillator Science 286, 766-768
49. Shearman, L. P., Sriram, S., Weaver, D. R., Maywood, E. S., Chaves, I., Zheng, B., Kume, K., Lee, C. C., van der Horst, G. T., Hastings, M. H., and Reppert, S. M. (2000) Interacting molecular loops in the mammalian circadian clock Science 288, 1013-1019
50. 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
51. 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
52. He, Q., Cheng, P., Yang, Y., Wang, L., Gardner, K. H., and Liu, Y. (2002) White collar-1, a DNA binding transcription factor and a light sensor Science 297, 840-843
53. Yu, W., Zheng, H., Houl, J. H., Dauwalder, B., and Hardin, P. E. (2006) PER-dependent rhythms in CLK phosphorylation and E-box binding regulate circadian transcription Genes Dev. 20, 723-733
54. Kim, E. Y., Ko, H. W., Yu, W., Hardin, P. E., and Edery, I. (2007) A DOUBLETIME kinase binding domain on the Drosophila PERIOD protein is essential for its hyperphosphorylation, transcriptional repression, and circadian clock function Mol. Cell. Biol. 27, 5014-5028
55. Menet, J. S., Abruzzi, K. C., Desrochers, J., Rodriguez, J., and Rosbash, M. (2010) Dynamic PER repression mechanisms in the Drosophila circadian clock: From on-DNA to off-DNA Genes Dev. 24, 358-367
56. Yoshitane, H., Takao, T., Satomi, Y., Du, N. H., Okano, T., and Fukada, Y. (2009) Roles of CLOCK phosphorylation in suppression of E-box-dependent transcription Mol. Cell. Biol. 29, 3675-3686
57. Tamaru, T., Hirayama, J., Isojima, Y., Nagai, K., Norioka, S., Takamatsu, K., and Sassone-Corsi, P. (2009) CK2α phosphorylates BMAL1 to regulate the mammalian clock Nat. Struct. Mol. Biol. 16, 446-448
58. Hunt, S. M., Thompson, S., Elvin, M., and Heintzen, C. (2010) VIVID interacts with the WHITE COLLAR complex and FREQUENCY-interacting RNA helicase to alter light and clock responses in Neurospora Proc. Natl. Acad. Sci. U.S.A. 107, 16709-16714
59. Chen, C. H., DeMay, B. S., Gladfelter, A. S., Dunlap, J. C., and Loros, J. J. (2010) Physical interaction between VIVID and white collar complex regulates photoadaptation in Neurospora Proc. Natl. Acad. Sci. U.S.A. 107, 16715-16720
60. Huang, G., He, Q., Guo, J., Cha, J., and Liu, Y. (2013) The Ccr4-not protein complex regulates the phase of the Neurospora circadian clock by controlling white collar protein stability and activity J. Biol. Chem. 288, 31002-31009
61. He, Q. and Liu, Y. (2005) Molecular mechanism of light responses in Neurospora: From light-induced transcription to photoadaptation Genes Dev. 19, 2888-2899
62. Hong, C. I., Ruoff, P., Loros, J. J., and Dunlap, J. C. (2008) Closing the circadian negative feedback loop: FRQ-dependent clearance of WC-1 from the nucleus Genes Dev. 22, 3196-3204
63. Berger, S. L. (2007) The complex language of chromatin regulation during transcription Nature 447, 407-412
64. 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
65. 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
66. 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
67. 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
68. Koike, N., Yoo, S. H., Huang, H. C., Kumar, V., Lee, C., Kim, T. K., and Takahashi, J. S. (2012) Transcriptional architecture and chromatin landscape of the core circadian clock in mammals Science 338, 349-354
69. Zou, J. X., Revenko, A. S., Li, L. B., Gemo, A. T., and Chen, H. W. (2007) ANCCA, an estrogen-regulated AAA+ ATPase coactivator for ERα, is required for coregulator occupancy and chromatin modification Proc. Natl. Acad. Sci. U.S.A. 104, 18067-18072
70. Gradolatto, A., Smart, S. K., Byrum, S., Blair, L. P., Rogers, R. S., Kolar, E. A., Lavender, H., Larson, S. K., Aitchison, J. D., Taverna, S. D., and Tackett, A. J. (2009) A noncanonical bromodomain in the AAA ATPase protein Yta7 directs chromosomal positioning and barrier chromatin activity Mol. Cell. Biol. 29, 4604-4611
71. Revenko, A. S., Kalashnikova, E. V., Gemo, A. T., Zou, J. X., and Chen, H. W. (2010) Chromatin loading of E2F-MLL complex by cancer-associated coregulator ANCCA via reading a specific histone mark Mol. Cell. Biol. 30, 5260-5272
72. Lombardi, L. M., Ellahi, A., and Rine, J. (2011) Direct regulation of nucleosome density by the conserved AAA-ATPase Yta7 Proc. Natl. Acad. Sci. U.S.A. 108, E1302-E1311
73. Raduwan, H., Isola, A. L., and Belden, W. J. (2013) Methylation of histone H3 on lysine 4 by the lysine methyltransferase SET1 protein is needed for normal clock gene expression J. Biol. Chem. 288, 8380-8390
74. Bobrowicz, P., Pawlak, R., Correa, A., Bell-Pedersen, D., and Ebbole, D. J. (2002) The Neurospora crassa pheromone precursor genes are regulated by the mating type locus and the circadian clock Mol. Microbiol. 45, 795-804
75. Sancar, G., Sancar, C., Brugger, B., Ha, N., Sachsenheimer, T., Gin, E., Wdowik, S., Lohmann, I., Wieland, F., Hofer, T., Diernfellner, A., and Brunner, M. (2011) A global circadian repressor controls antiphasic expression of metabolic genes in Neurospora Mol. Cell 44, 687-697
76. Wang, L., Kim, J., and Somers, D. E. (2013) Transcriptional corepressor TOPLESS complexes with pseudoresponse regulator proteins and histone deacetylases to regulate circadian transcription Proc. Natl. Acad. Sci. U.S.A. 110, 761-766
77. Sharp, P. M., Tuohy, T. M. F., and Mosurski, K. R. (1986) Codon usage in yeast: Cluster analysis clearly differentiates highly and lowly expressed genes Nucleic Acids Res. 14, 5125-5143
78. Sørensen, M. A., Kurland, C. G., and Pedersen, S. (1989) Codon usage determines translation rate in Escherichia coli J. Mol. Biol. 207, 365-377
79. Lavner, Y. and Kotlar, D. (2005) Codon bias as a factor in regulating expression via translation rate in the human genome Gene 345, 127-138
80. Brocca, S., Schmidt-Dannert, C., Schmid, R. D., Lotti, M., and Alberghina, L. (1998) Design, total synthesis, and functional overexpression of the Candida rugosa lipl gene coding for a major industrial lipase Protein Sci. 7, 1415-1422
81. Zhang, G., Hubalewska, M., and Ignatova, Z. (2009) Transient ribosomal attenuation coordinates protein synthesis and co-translational folding Nat. Struct. Mol. Biol. 16, 274-280
82. Siller, E., DeZwaan, D. C., Anderson, J. F., Freeman, B. C., and Barral, J. M. (2010) Slowing Bacterial Translation Speed Enhances Eukaryotic Protein Folding Efficiency J. Mol. Biol. 396, 1310-1318
83. Spencer, P. S., Siller, E., Anderson, J. F., and Barral, J. M. (2012) Silent Substitutions Predictably Alter Translation Elongation Rates and Protein Folding Efficiencies J. Mol. Biol. 422, 328-335
84. Akashi, H. (1994) Synonymous codon usage in Drosophila melanogaster: Natural selection and translational accuracy Genetics 136, 927-935
85. Drummond, D. A. and Wilke, C. O. (2008) Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution Cell 134, 341-352
86. Zhou, M., Guo, J., Cha, J., Chae, M., Chen, S., Barral, J. M., Sachs, M. S., and Liu, Y. (2013) Non-optimal codon usage affects expression, structure and function of clock protein FRQ Nature 495, 111-115
87. Xu, Y., Ma, P., Shah, P., Rokas, A., Liu, Y., and Johnson, C. H. (2013) Non-optimal codon usage is a mechanism to achieve circadian clock conditionality Nature 495, 116-120
88. Wu, G., Xu, G., Schulman, B. A., Jeffrey, P. D., Harper, J. W., and Pavletich, N. P. (2003) Structure of a β-TrCP1-Skp1-β-catenin complex: Destruction motif binding and lysine specificity of the SCF(β-TrCP1) ubiquitin ligase Mol. Cell 11, 1445-1456
89. Querfurth, C., Diernfellner, A. C., Gin, E., Malzahn, E., Hofer, 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
90. Diernfellner, A. C., Querfurth, C., Salazar, C., Hofer, T., and Brunner, M. (2009) Phosphorylation modulates rapid nucleocytoplasmic shuttling and cytoplasmic accumulation of Neurospora clock protein FRQ on a circadian time scale Genes Dev. 23, 2192-2200
91. Cha, J., Yuan, H., and Liu, Y. (2011) Regulation of the activity and cellular localization of the circadian clock protein FRQ J. Biol. Chem. 286, 11469-11478