Epigenetic and Posttranslational Modifications in Light Signal Transduction and the Circadian Clock in Neurospora crassa
Abstract
:1. The Neurospora crassa Light Responses
1.1. Light Signal Transduction
1.2. White Collar Complex (WCC) Activation
2. The Neurospora crassa Circadian Cycle
Positive and Negative Feedback Loops in the Neurospora’s Circadian Clock
3. Protein Posttranslational Modifications (PTMs) during the Circadian Clock, and Light Signal Transduction
3.1. Faces and Timing of Frequency (FRQ) Phosphorylation
3.2. Kinases Targeting FRQ
3.2.1. CKIa and CKIb
3.2.2. CKII
3.2.3. CAMK1
3.3. FRQ Stabilization
3.3.1. PKA
3.3.2. PP1, PP2 and PP4
Protein | Target | Activity | Effects | Other Information |
---|---|---|---|---|
FRH | FRQ | Promotes FRQ conformational changes | Ensures proper folding of FRQ | NA |
Masks some residues to CKIa phosphorylation | ||||
frq mRNA | FRH physically interacts with frq mRNA | Exosomal degradation of mRNA | ||
CKIa | FRQ N-terminal domain | Phosphorylation | Conformational changes | Recruited on FRQ FCD domains |
FRQ PEST-1 domain | Phosphorylation | FWD-1 recruitment | NA | |
FRQ S513 | Phosphorylation | FWD-1 recruitment | NA | |
FRQ N-terminal domain | Phosphorylation | FWD-1 recruitment | NA | |
FRQ Central domain | Phosphorylation | FWD-1 recruitment | NA | |
CKII | FRQ N-terminal domain | Phosphorylation | Conformational changes | Recruited on FRQ FCD domains |
FRQ PEST-1 domain | Phosphorylation | FWD-1 recruitment | NA | |
FRQ S513 | Phosphorylation | FWD-1 recruitment | NA | |
FRQ N-terminal domain | Phosphorylation | FWD-1 recruitment | NA | |
FRQ Central domain | Phosphorylation | FWD-1 recruitment | NA | |
CAMK-1 | FRQ N-terminal domain | Phosphorylation | FWD-1 recruitment | NA |
FRQ PEST-1 domain | Phosphorylation | FWD-1 recruitment | NA | |
FRQ S513 | Phosphorylation | FWD-1 recruitment | NA | |
FRQ N-terminal domain | Phosphorylation | FWD-1 recruitment | NA | |
CKIb | FRQ N-terminal domain | Phosphorylation | Conformational changes | Interaction with N-terminal domain demonstrated only in vitro |
PP1 | FRQ PEST-1 domain | Dephosphorylation | Contrasting phosphatase action–FRQ stabilization | NA |
FRQ S513 | Dephosphorylation | Contrasting phosphatase action–FRQ stabilization | NA | |
FRQ N-terminal domain | Dephosphorylation | Contrasting phosphatase action–FRQ stabilization | NA | |
FRQ Central domain | Dephosphorylation | Contrasting phosphatase action–FRQ stabilization | NA | |
PP2A | FRQ PEST-1 domain | Dephosphorylation | Contrasting phosphatase action–FRQ stabilization | NA |
FRQ S513 | Dephosphorylation | Contrasting phosphatase action–FRQ stabilization | NA | |
FRQ N-terminal domain | Dephosphorylation | Contrasting phosphatase action–FRQ stabilization | NA | |
FRQ Central domain | Dephosphorylation | Contrasting phosphatase action–FRQ stabilization | NA | |
PP4 | FRQ PEST-1 domain | Dephosphorylation | Contrasting phosphatase action–FRQ stabilization | NA |
FRQ S513 | Dephosphorylation | Contrasting phosphatase action–FRQ stabilization | NA | |
FRQ N-terminal domain | Dephosphorylation | Contrasting phosphatase action–FRQ stabilization | NA | |
FRQ Central domain | Dephosphorylation | Contrasting phosphatase action–FRQ stabilization | NA | |
FWD-1 | Hyperphosphorylated FRQ | Physical interaction with FRQ | SCF-type ubiquitin E3 ligase recruitment | NA |
SCF-type ubiquitin E3 ligase | Hyperphosphorylated FRQ | Ubiquitination of FRQ | FRQ proteasomal degradation | NA |
3.4. Molecular Mechanisms of FRQ Phosphorylation and Proteasomal Degradation
3.5. White Collar Complex (WCC) Light Dependent Phosphorylation
Protein Name | Protein Target | AA Target | Activity | Effects | Other Information | Other Information |
---|---|---|---|---|---|---|
PKA | WC-1 | S990 S995 | Phosphorylation | Inhibition WCC activity Putative Priming kinase | FRQ independent kinase | Interaction experimentally proven |
PKC | WC-1 | Zn Finger | Phosphorylation | Decreased WC-1 stability | NA | Interaction experimentally proven |
CKIa | WC-1 | S992 S994 S998 | Phosphorylation | Decreased WC-1 activity | Kinases recruited by FRQ | Interaction experimentally proven |
CKII | WC-1 | S992 S994 S998 | Phosphorylation | Decreased WC-1 activity | Kinases recruited by FRQ | Interaction experimentally proven |
GSK | WC-1 | Phosphorylation | NA | Interaction experimentally proven | ||
Unknown | WC-2 | S443 | Phosphorylation | Decreased WCC activity | NA | NA |
3.6. White Collar 1 (WC-1) Light Dependent Acetylation
3.7. The FRQ-Independent WCC Circadian Phosphorylation
3.8. The FRQ-Dependent WCC Circadian Phosphorylation
4. Chromatin Epigenetic Modifications Involved in Circadian Rhythms and Light Signal Transduction
4.1. Chromatin Acetylation
4.2. Chromatin Remodeling Enzymes
Enzyme | Modification | Target | Activation | Deactivation |
---|---|---|---|---|
NGF1 | Acetylation | H3K9–H3K14 | X | - |
DIM-2 | Methylation | Undefined | - | X |
DIM-5 | Methylation | H3K9 | - | X |
CSW-1 | De-Acetylation | Undefined | - | X |
KMT2 | 3Methylation | H3K4 | - | X |
CATP | Demethylation | Undefined | X | - |
CHD1 | Demethylation | Undefined | X | - |
4.3. Chromatin Methylation
5. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Cashmore, A.R.; Jarillo, J.A.; Wu, Y.J.; Liu, D. Cryptochromes: Blue light receptors for plants and animals. Science 1999, 284, 760–765. [Google Scholar] [CrossRef] [PubMed]
- Ahmad, M.; Cashmore, A.R. The HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 1993, 366, 162–166. [Google Scholar] [CrossRef] [PubMed]
- Short, T.W.; Briggs, W.R. The transduction of blue light signals in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1994, 45, 143–171. [Google Scholar] [CrossRef]
- Fankhauser, C. The phytochromes, a family of red/far-red absorbing photoreceptors. J. Biol. Chem. 2001, 276, 11453–11456. [Google Scholar] [CrossRef] [PubMed]
- Linden, H.; Ballario, P.; Macino, G. Blue light regulation in Neurospora crassa. Fungal Genet. Biol. 1997, 3, 141–150. [Google Scholar] [CrossRef] [PubMed]
- Galagan, J.E.; Calvo, S.E.; Borkovich, K.A.; Selker, E.U.; Read, N.D.; Jaffe, D.; FitzHugh, W.; Ma, L.J.; Smirnov, S.; Purcell, S.; et al. The genome sequence of the filamentous fungus Neurospora crassa. Nature 2003, 422, 859–868. [Google Scholar] [CrossRef] [PubMed]
- Froehlich, A.C.; Noh, B.; Vierstra, R.D.; Loros, J.; Dunlap, J.C. Genetic and molecular analysis of phytochromes from the filamentous fungus Neurospora crassa. Eukaryot. Cell 2005, 12, 2140–2152. [Google Scholar] [CrossRef] [PubMed]
- Arpaia, G.; Loros, J.; Dunlap, J.C.; Morelli, G.; Macino, G. The circadian clock-controlled gene ccg-J is induced by light. Mol. Gen. Genet. 1995, 247, 157–163. [Google Scholar] [CrossRef] [PubMed]
- Harding, R.W.; Turner, R.V. Photoregulation of the carotenoid biosynthetic pathways in albino and white collar mutants of Neurospora crassa. Plant Physiol. 1981, 68, 745–749. [Google Scholar] [CrossRef] [PubMed]
- Lauter, F.R.; Russo, V.E. Blue light induction of conidiation-specific genes in Neurospora crassa. Nucleic Acids Res. 1991, 19, 6883–6886. [Google Scholar] [CrossRef] [PubMed]
- Harding, R.W.; Melles, S. Genetic analysis of the phototrophism of Neurospora crassa perithecial beaks using white collar and albino mutants. Plant Physiol. 1984, 72, 996–1000. [Google Scholar] [CrossRef]
- Corrochano, L.M. Fungal photoreceptors: Sensory molecules for fungal development and behaviour. Photochem. Photobiol. Sci. 2007, 7, 725–736. [Google Scholar] [CrossRef] [PubMed]
- Herrera-Estrella, A.; Horwitz, B.A. Looking through the eyes of fungi: Molecular genetics of photoreception. Mol. Microbiol. 2007, 64, 5–15. [Google Scholar] [CrossRef] [PubMed]
- Nelson, M.A.; Morelli, G.; Carattoli, A.; Romano, N.; Macino, G. Molecular cloning of Neurospora crassa carotenoid biosynthetic gene (albino-3) regulated by blue light and the product of the white collar-1 gene. Mol. Cell. Biol. 1989, 9, 1271–1276. [Google Scholar] [PubMed]
- Schmidhauser, T.J.; Lauter, F.R.; Russo, E.A.; Janofsky, C. Cloning, sequence and photoregulation of al-l, a carotenoid biosynthetic gene of Neurospora crassa. Mol. Cell. Biol. 1990, 10, 5064–5070. [Google Scholar] [PubMed]
- Chen, C.H.; Ringelberg, C.S.; Gross, R.H.; Dunlap, J.C.; Loros, J.J. Genome-wide analysis of light-inducible responses reveals hierarchical light signalling in Neurospora. EMBO J. 2009, 28, 1029–1042. [Google Scholar] [CrossRef] [PubMed]
- Chen, C.H.; Dunlap, J.C.; Loros, J.J. Neurospora illuminates fungal photoreception. Fungal Genet. Biol. 2010, 47, 922–929. [Google Scholar] [CrossRef] [PubMed]
- Ballario, P.; Vittorioso, P.; Magrelli, A.; Talora, C.; Cabibbo, A.; Macino, G. White collar-1, a central regulator of blue light responses in Neurospora, is a zinc finger protein. EMBO J. 1996, 15, 1650–1657. [Google Scholar] [PubMed]
- Linden, H.; Macino, G. White collar 2, a partner in blue-light signal transduction, controlling expression of light-regulated genes in Neurospora crassa. EMBO J. 1997, 16, 98–109. [Google Scholar] [CrossRef] [PubMed]
- Ballario, P.; Talora, C.; Galli, D.; Linden, H.; Macino, G. Roles in dimerization and blue light photoresponse of the PAS and LOV domains of Neurospora crassa white collar proteins. Mol. Microbiol. 1998, 29, 719–729. [Google Scholar] [CrossRef] [PubMed]
- Dunlap, J.C.; Loros, J.J. Neurospora photoreceptors. In Handbook of Photosensory Receptors; Briggs, W.R., Spudich, J.L., Eds.; Wiley-VCH Verlag GmbH & Co: Weinheim, Germany, 2005; pp. 371–389. [Google Scholar]
- Christie, J.M.; Salomon, M.; Nozue, K.; Wada, M.; Briggs, W.R. LOV (light, oxygen, or voltage) domains of the blue-light photoreceptor phototropin (nph1): Binding sites for the chromophore flavin mononucleotide. Proc. Natl. Acad. Sci. USA 1999, 96, 8778–8783. [Google Scholar] [CrossRef]
- Schafmeier, T.; Kaldi, K.; Diernfellner, A.; Mohr, C.; Brunner, M. Phosphorylation-dependent maturation of Neurospora circadian clock protein from a nuclear repressor toward a cytoplasmic activator. Genes Dev. 2006, 20, 297–306. [Google Scholar] [CrossRef] [PubMed]
- Froehlich, A.C.; Liu, Y.; Loros, J.J.; Dunlap, J.C. White Collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 2002, 297, 815–819. [Google Scholar] [CrossRef] [PubMed]
- Sancar, C.; Ha, N.; Yilmaz, R.; Tesorero, R.; Fisher, T.; Brunner, M.; Sancar, G. Combinatorial control of light induced chromatin remodeling and gene activation in Neurospora. PLoS Genet. 2015, 3, e1005105. [Google Scholar] [CrossRef] [PubMed]
- Cheng, P.; Yang, Y.; Wang, L.; He, Q.; Liu, Y. WHITE COLLAR-1, a multifunctional Neurospora protein involved in the circadian feedback loops, light sensing, and transcription repression of wc-2. J. Biol. Chem. 2003, 278, 3801–3808. [Google Scholar] [CrossRef] [PubMed]
- He, Q.; Liu, Y. Molecular mechanism of light responses in Neurospora: From light-induced transcription to photoadaptation. Genes Dev. 2005, 19, 2888–2899. [Google Scholar] [CrossRef] [PubMed]
- Sommer, G.J.; Chambers, A.A.; Eberle, J.; Lauter, F.R.; Russo, V.E. Fast light-regulated genes of N. crassa. Nucleic Acids Res. 1989, 17, 5717–5724. [Google Scholar] [CrossRef]
- Arpaia, G.; Loros, J.; Dunlap, J.C.; Morelli, G.; Macino, G. The interplay of light and the circadian clock: Independent dual regulation of clock-controlled gene cg-2(eas). Plant Physiol. 1993, 102, 1299–1305. [Google Scholar] [CrossRef] [PubMed]
- Arpaia, G.; Carattoli, A.; Macino, G. Light and development regulate the expression of the albino-3 gene in Neurospora crassa. Dev. Biol. 1995, 170, 626–635. [Google Scholar] [CrossRef] [PubMed]
- Neiss, A.; Schafmeier, T.; Brunner, M. Transcriptional regulation and function of the Neurospora clock gene white collar 2 and its isoforms. EMBO Rep. 2008, 9, 788–794. [Google Scholar] [CrossRef] [PubMed]
- Heintzen, C.; Loros, J.J.; Dunlap, J.C. The PAS protein VIVID defines a clock-associated feedback loop that represses light input, modulates gating, and regulates clock resetting. Cell 2001, 104, 453–464. [Google Scholar] [CrossRef]
- Zoltowski, B.D.; Crane, B.R. Light activation of the LOV protein VIVID generates a rapidly exchanging dimer. Biochemistry 2008, 47, 7012–7019. [Google Scholar] [CrossRef] [PubMed]
- He, Q.; Cheng, P.; Yang, Y.; Wang, L.; Gardner, K.H.; Liu, Y. White collar-1, a DNA binding transcription factor and a light sensor. Science 2002, 297, 840–843. [Google Scholar] [CrossRef] [PubMed]
- Malzahn, E.; Ciprianidis, S.; Kaldi, K.; Schafmeier, T.; Brunner, M. Photoadaptation in Neurospora by competitive interaction of activating and inhibitory LOV domains. Cell 2010, 142, 762–772. [Google Scholar] [CrossRef] [PubMed]
- Schibler, U.; Sassone-Corsi, P. A web of circadian pacemakers. Cell 2002, 111, 919–922. [Google Scholar] [CrossRef]
- Woelfle, M.A.; Ouyang, Y.; Phanvijhitsiri, K.; Johnson, C.H. The adaptive value of circadian clocks: An experimental assessment in cyanobacteria. Curr. Biol. 2004, 14, 1481–1486. [Google Scholar] [CrossRef] [PubMed]
- Dunlap, J.C. Molecular bases for circadian clocks. Cell 1999, 96, 271–290. [Google Scholar] [CrossRef]
- Albrecht, U. Circadian rhythms: A fine c(l)ocktail! Curr. Biol. 2001, 11, 517–519. [Google Scholar] [CrossRef]
- Pittendrigh, C.S. Circadian rhythms and the circadian organization of living systems. Cold Spring Harb. Symp. Quant. Biol. 1960, 25, 159–184. [Google Scholar] [CrossRef] [PubMed]
- Stadler, D.R. Genetic control of a cyclic growth pattern in Neurospora. Nature 1959, 184, 170–171. [Google Scholar] [CrossRef]
- Sussman, A.S.; Durkee, T.L.; Lowry, R.J. A model for rhythmic and temperature-independent growth in “clock” mutants of Neurospora. Mycopathol. Mycol. Appl. 1965, 25, 381–396. [Google Scholar] [CrossRef] [PubMed]
- Sargent, M.L.; Briggs, W.R.; Woodward, D.O. Circadian nature of a rhythm expressed by an invertaseless strain of Neurospora crassa. Plant Physiol. 1966, 41, 1343–1349. [Google Scholar] [CrossRef] [PubMed]
- Berliner, M.D.; Neurath, P.W. The band forming rhythm of Neurospora mutants. J. Cell. Physiol. 1965, 65, 183–193. [Google Scholar] [CrossRef] [PubMed]
- Baker, C.L.; Loros, J.J.; Dunlap, J.C. The circadian clock of Neurospora crassa. FEMS Microbiol. Rev. 2012, 36, 95–110. [Google Scholar] [CrossRef] [PubMed]
- Crosthwaite, S.K.; Dunlap, J.C.; Loros, J.J. Neurospora wc-1 and wc-2: Transcription, photoresponses, and the origins of circadian rhythmicity. Science 1997, 276, 763–769. [Google Scholar] [CrossRef] [PubMed]
- Aronson, B.D.; Johnson, K.A.; Loros, J.J.; Dunlap, J.C. Negative feedback defining a circadian clock: Autoregulation of the clock gene frequency. Science 1994, 263, 1578–1584. [Google Scholar] [CrossRef] [PubMed]
- Gorl, M.; Merrow, M.; Huttner, B.; Johnson, J.; Roenneberg, T.; Brunner, M. A PEST-like element in FREQUENCY determines the length of the circadian period in Neurospora crassa. EMBO J. 2001, 20, 7074–7084. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Loros, J.; Dunlap, J.C. 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. USA 2000, 97, 234–239. [Google Scholar] [CrossRef] [PubMed]
- Cheng, P.; Yang, Y.; Gardner, K.H.; Liu, Y. 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. 2002, 22, 517–524. [Google Scholar] [CrossRef] [PubMed]
- Froehlich, A.C.; Loros, J.J.; Dunlap, J.C. Rhythmic binding of a WHITE COLLAR-containing complex to the frequency promoter is inhibited by FREQUENCY. Proc. Natl. Acad. Sci. USA 2003, 100, 5914–5919. [Google Scholar] [CrossRef] [PubMed]
- Heintzen, C.; Liu, Y. The Neurospora crassa circadian clock. Adv. Genet. 2007, 58, 25–66. [Google Scholar] [PubMed]
- Zhou, M.; Guo, J.; Cha, J.; Chae, M.; Chen, S.; Barral, J.M.; Sachs, M.S.; Liu, Y. Non-optimal codon usage affects expression, structure and function of clock protein FRQ. Nature 2013, 495, 111–115. [Google Scholar] [CrossRef] [PubMed]
- Diernfellner, A.; Colot, H.V.; Dintsis, O.; Loros, J.J.; Dunlap, J.C.; Brunner, M. Long and short isoforms of Neurospora clock protein FRQ support temperature-compensated circadian rhythms. FEBS Lett. 2007, 581, 5759–5764. [Google Scholar] [CrossRef] [PubMed]
- Luo, C.; Loros, J.J.; Dunlap, J.C. Nuclear localization is required for function of the essential clock protein FRQ. EMBO J. 1998, 17, 1228–1235. [Google Scholar] [CrossRef] [PubMed]
- Lewis, M.T.; Morgan, L.W.; Feldman, J.F. Analysis of frequency (frq) clock gene homologs: Evidence for a helix-turn-helix transcription factor. Mol. Gen. Genet. 1997, 4, 401–414. [Google Scholar] [CrossRef]
- Colot, H.V.; Loros, J.J.; Dunlap, J.C. Temperature-modulated alternative splicing and promoter use in the Circadian clock gene frequency. Mol. Biol. Cell 2005, 12, 5563–5571. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Garceau, N.Y.; Loros, J.J.; Dunlap, J.C. Thermally regulated translational control of FRQ mediates aspects of temperature responses in the Neurospora circadian clock. Cell 1997, 89, 477–486. [Google Scholar] [CrossRef]
- Cheng, P.; He, Q.; Wang, L.; Liu, Y. Regulation of the Neurospora circadian clock by an RNA helicase. Genes Dev. 2005, 19, 234–241. [Google Scholar] [CrossRef] [PubMed]
- Shi, M.; Collett, M.; Loros, J.J.; Dunlap, J.C. FRQ-interacting RNA helicase mediates negative and positive feedback in the Neurospora circadian clock. Genetics 2010, 267, 414–422. [Google Scholar] [CrossRef] [PubMed]
- Guo, J.; Cheng, P.; Yuan, H.; Liu, Y. The exosome regulates circadian gene expression in a posttranscriptional negative feedback loop. Cell 2009, 138, 1236–1246. [Google Scholar] [CrossRef] [PubMed]
- Hong, C.I.; Ruoff, P.; Loros, J.J.; Dunlap, J.C. Closing the circadian negative feedback loop: FRQ-dependent clearance of WC-1 from the nucleus. Genes Dev. 2008, 22, 3196–3204. [Google Scholar] [CrossRef] [PubMed]
- Hurley, J.M.; Larrondo, L.F.; Loros, J.J.; Dunlap, J.C. Conserved RNA helicase FRH acts nonenzymatically to support the intrinsically disordered Neurospora clock protein FRQ. Mol. Cell 2013, 52, 832–843. [Google Scholar] [CrossRef] [PubMed]
- Lee, K.; Loros, J.J.; Dunlap, J.C. Interconnected feedback loops in the Neurospora circadian system. Science 2000, 289, 107–110. [Google Scholar] [CrossRef] [PubMed]
- Cheng, P.; Yang, Y.; Liu, Y. Interlocked feedback loop contribute to the robustness of the Neurospora circadian clock. Proc. Natl. Acad. Sci. USA 2001, 98, 7408–7413. [Google Scholar] [CrossRef] [PubMed]
- Diernfellner, A.C.; Querfurth, C.; Salazar, C.; Hofer, T.; Brunner, M. Phosphorylation modulates rapid nucleocytoplasmic shuttling and cytoplasmic accumulation of Neurospora clock protein FRQ on a circadian time scale. Genes Dev. 2009, 23, 2192–2200. [Google Scholar] [CrossRef] [PubMed]
- Cha, J.; Yuan, H.; Liu, Y. Regulation of the activity and cellular localization of the circadian clock protein FRQ. J. Biol. Chem. 2011, 286, 11469–11478. [Google Scholar] [CrossRef] [PubMed]
- Hong, C.I.; Jolma, I.W.; Loros, J.J.; Dunlap, J.C.; Ruoff, P. Simulating dark expressions and interactions of frq and wc-1 in the Neurospora circadian clock. Biophys. J. 2008, 15, 1221–1232. [Google Scholar] [CrossRef] [PubMed]
- Van der Steen, T.; Tindall, D.J.; Huang, H. Posttranslational modification of the androgen receptor in prostate cancer. Int. J. Mol. Sci. 2013, 14, 14833–14859. [Google Scholar] [CrossRef] [PubMed]
- Ngounou Wetie, A.G.; Woods, A.G.; Darie, C.C. Mass spectrometric analysis of post-translational modifications (PTMs) and protein-protein interactions (PPIs). Adv. Exp. Med. Biol. 2014, 806, 205–235. [Google Scholar] [PubMed]
- Sabò, A.; Lusic, M.; Cereseto, A.; Giacca, M. Acetylation of conserved lysines in the catalytic core of cyclin-dependent kinase 9 inhibits kinase activity and regulates transcription. Mol. Cell. Biol. 2008, 28, 2201–2212. [Google Scholar] [CrossRef] [PubMed]
- Pegoraro, M.; Tauber, E. Animal clocks: A multitude of molecular mechanisms for circadian timekeeping. Wiley Interdiscip. Rev. RNA 2011, 2, 312–320. [Google Scholar] [CrossRef] [PubMed]
- Weber, F.; Zorn, D.; Rademacher, C.; Hung, H.C. Post-translational timing mechanisms of the Drosophila circadian clock. FEBS Lett. 2011, 10, 1443–1449. [Google Scholar] [CrossRef] [PubMed]
- Kusakina, J.; Dodd, A.N. Phosphorylation in the plant circadian system. Trends Plant Sci. 2012, 17, 575–583. [Google Scholar] [CrossRef] [PubMed]
- Syed, S.; Saez, L.; Young, M.W. Kinetics of Doubletime kinase-dependent degradation of the Drosophila period protein. J. Biol. Chem. 2011, 31, 27654–27662. [Google Scholar] [CrossRef] [PubMed]
- Ko, H.W.; Jiang, J.; Edery, I. Role for Slimb in the degradation of Drosophila Period protein phosphorylated by Doubletime. Nature 2002, 420, 673–678. [Google Scholar] [CrossRef] [PubMed]
- Price, J.L.; Fan, J.Y.; Keightley, A.; Means, J.C. The role of casein kinase I in the Drosophila circadian clock. Methods Enzymol. 2015, 551, 175–195. [Google Scholar] [PubMed]
- Eide, E.J.; Woolf, M.F.; Kang, H.; Woolf, P.; Hurst, W.; Camacho, F.; Vielhaber, E.L.; Giovanni, A.; Virshup, D.M. Control of mammalian circadian rhythm by CKIε-regulated proteasome-mediated PER2 degradation. Mol. Cell. Biol. 2005, 7, 2795–2807. [Google Scholar] [CrossRef] [PubMed]
- Shanware, N.P.; Hutchinson, J.A.; Kim, S.H.; Zhan, L.; Bowler, M.J.; Tibbetts, R.S. Casein kinase 1-dependentphosphorylationof familial advanced sleep phase syndrome-associated residues controls PERIOD 2 stability. J. Biol. Chem. 2011, 14, 12766–12774. [Google Scholar] [CrossRef] [PubMed]
- Mahesh, G.; Jeong, E.; Ng, F.S.; Liu, Y.; Gunawardhana, K.; Houl, J.H.; Yildirim, E.; Jones, R.; Amunugama, R.; Allen, D.L.; et al. Phosphorylation of the transcription activator CLOCK regulates progression through a ~24-h feedback loop to influence the circadian period in Drosophila. J. Biol. Chem. 2014, 289, 19681–19693. [Google Scholar] [CrossRef] [PubMed]
- Kwak, Y.; Jeong, J.; Lee, S.; Park, Y.U.; Lee, S.A.; Han, D.H.; Kim, J.H.; Ohshima, T.; Suh, Y.H.; Mikoshiba, K.; et al. Cyclin-dependent kinase 5 (Cdk5) regulates the function of CLOCK protein by direct phosphorylation. J. Biol. Chem. 2013, 288, 36878–36889. [Google Scholar] [CrossRef] [PubMed]
- Gallego, M.; Virshup, D.M. Post-translational modifications regulate the ticking of the circadian clock. Nat. Rev. Mol. Cell Biol. 2007, 8, 139–148. [Google Scholar] [CrossRef] [PubMed]
- Sanada, K.; Okano, T.; Fukada, Y. Mitogen-activated protein kinase phosphorylates and negatively regulates basic helix-loop-helix-PAS transcription factor BMAL1. J. Biol. Chem. 2002, 277, 267–271. [Google Scholar] [CrossRef] [PubMed]
- Tamaru, T.; Hirayama, J.; Isojima, Y.; Nagai, K.; Norioka, S.; Takamatsu, K.; Sassone-Corsi, P. CK2α phosphorylates BMAL1 to regulate the mammalian clock. Nat. Struct. Mol. Biol. 2009, 16, 446–448. [Google Scholar] [CrossRef] [PubMed]
- Eide, E.J.; Vielhaber, E.L.; Hinz, W.A.; Virshup, D.M. The circadian regulatory proteins BMAL1 and cryptochromes are substrates of casein kinase Iepsilon. J. Biol. Chem. 2002, 277, 17248–17254. [Google Scholar] [CrossRef] [PubMed]
- Choudhary, C.; Kumar, C.; Gnad, F.; Nielsen, M.L.; Rehman, M.; Walther, T.C.; Olsen, J.V.; Mann, M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325, 834–840. [Google Scholar] [CrossRef] [PubMed]
- Hirayama, J.; Sahar, S.; Grimaldi, B.; Tamaru, T.; Takamatsu, K.; Nakahata, Y.; Sassone-Corsi, P. CLOCK-mediated acetylation of BMAL1 controls circadian function. Nature 2007, 450, 1086–1090. [Google Scholar] [CrossRef] [PubMed]
- Nakahata, Y.; Kaluzova, M.; Grimaldi, B.; Sahar, S.; Hirayama, J.; Chen, D.; Guarente, L.P.; Sassone-Corsi, P. The NAD+-dependent deacetylaseSIRT1modulates CLOCK-mediated chromatin remodeling andcircadian control. Cell 2008, 134, 329–340. [Google Scholar] [CrossRef] [PubMed]
- Asher, G.; Gatfield, D.; Stratmann, M.; Reinke, H.; Dibner, C.; Kreppel, F.; Mostoslavsky, R.; Alt, F.W.; Schibler, U. SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 2008, 134, 17–28. [Google Scholar] [CrossRef] [PubMed]
- Garceau, N.Y.; Liu, Y.; Loros, J.J.; Dunlap, J.C. Alternative initiation of translation and time-specific phosphorylation yield multiple forms of the essential clock protein FREQUENCY. Cell 1997, 89, 469–476. [Google Scholar] [CrossRef]
- Yang, Y.; Cheng, P.; Zhi, G.; Liu, Y. Identification of a calcium/calmodulin-dependent protein kinase that phosphorylates the Neurospora circadian clock protein FREQUENCY. J. Biol. Chem. 2001, 276, 41064–41072. [Google Scholar] [CrossRef] [PubMed]
- Querfurth, C.; Diernfellner, A.; Heise, F.; Lauinger, L.; Neiss, A.; Tataroglu, O.; Brunner, M.; Schafmeier, T. Posttranslational regulation of Neurospora circadian clock by CK1a-dependent phosphorylation. Cold Spring Harb. Symp. Quant. Biol. 2007, 72, 177–183. [Google Scholar] [CrossRef] [PubMed]
- Baker, C.L.; Kettenbach, A.N.; Loros, J.J.; Gerber, S.A.; Dunlap, J.C. Quantitative proteomics reveals a dynamic interactome and phase-specific phosphorylation in the Neurospora circadian clock. Mol. Cell 2009, 34, 354–363. [Google Scholar] [CrossRef] [PubMed]
- Merrow, M.W.; Dunlap, J.C. Intergenic complementation of a circadian rhythmicity defect: Phylogenetic conservation of structure and function of the clock gene frequency. EMBO J. 1994, 13, 2257–2566. [Google Scholar] [PubMed]
- Roth, A.F.; Davis, N.G. Ubiquitination of the PEST-like endocytosis signal of the yeast a-factor receptor. J. Biol. Chem. 2000, 17, 8143–8153. [Google Scholar] [CrossRef]
- Diernfellner, A.C.; Schafmeier, T. Phosphorylations: Making the Neurospora crassa circadian clock tick. FEBS Lett. 2011, 585, 1461–1466. [Google Scholar] [CrossRef] [PubMed]
- Guo, J.; Cheng, P.; Liu, Y. Functional significance of FRH in regulating the phosphorylation and stability of Neurospora circadian clock protein FRQ. J. Biol. Chem. 2010, 285, 11508–11515. [Google Scholar] [CrossRef] [PubMed]
- He, Q.; Cha, J.; Lee, H.C.; Yang, Y.; Liu, Y. CKI and CKII mediate the FREQUENCY-dependent phosphorylation of the WHITE COLLAR complex to close the Neurospora circadian negative feedback loop. Genes Dev. 2006, 20, 2552–2565. [Google Scholar] [CrossRef] [PubMed]
- Kloss, B.; Price, J.L.; Saez, L.; Blau, J.; Rothenfluh, A.; Wesley, C.S.; Young, M.W. The Drosophila clock gene double-time encodes a protein closely related to human casein kinase I epsilon. Cell 1998, 94, 97–107. [Google Scholar] [CrossRef]
- Lauinger, L.; Diernfellner, A.; Falk, S.; Brunner, M. The RNA helicase FRH is an ATP-dependent regulator of CK1a in the circadian clock of Neurospora crassa. Nat. Commun. 2014, 5, 3598. [Google Scholar] [CrossRef] [PubMed]
- Tang, C.T.; Li, S.; Long, C.; Cha, J.; Huang, G.; Li, L.; Chen, S; Liu, Y. Setting the pace of the Neurospora circadian clock by multiple independent FRQ phosphorylation events. Proc. Natl. Acad. Sci. USA 2009, 106, 10722–10727. [Google Scholar] [CrossRef] [PubMed]
- Yang, Y.; Cheng, P.; He, Q.; Wang, L.; Liu, Y. Phosphorylation of FREQUENCY protein by casein kinase II is necessary for the function of the Neurospora circadian clock. Mol. Cell. Biol. 2003, 23, 6221–6228. [Google Scholar] [CrossRef] [PubMed]
- Yang, Y.; Cheng, P.; Liu, Y. Regulation of the Neurospora circadian clock by casein kinase II. Genes Dev. 2002, 16, 994–1006. [Google Scholar] [CrossRef] [PubMed]
- Cheng, P.; Yang, Y.; Heintzen, C.; Liu, Y. Coiled-coil domain-mediated FRQ-FRQ interaction is essential for its circadian clock function in Neurospora. EMBO J. 2001, 20, 101–108. [Google Scholar] [CrossRef] [PubMed]
- Nakashima, H. Phase shifting of the circadian conidiation rhythm in Neurospora crassa by calmodulin antagonists. J. Biol. Rhythm. 1986, 2, 163–169. [Google Scholar] [CrossRef]
- Sadakane, Y.; Nakashima, H. Light-induced phase shifting of the circadian conidiation rhythm is inhibited by calmodulin antagonists in Neurospora crassa. J. Biol. Rhythm. 1996, 11, 234–240. [Google Scholar] [CrossRef]
- Huang, G.; Chen, S.; Li, S.; Long, C.; Li, L.; He, Q.; Liu, Y. Protein kinase A and casein kinases mediate sequential phosphorylation events in the circadian negative feedback loop. Genes Dev. 2007, 21, 3283–3295. [Google Scholar] [CrossRef] [PubMed]
- Vanselow, K.; Vanselow, J.T.; Westermark, P.O.; Reischl, S.; Maier, B.; Korte, T.; Herrmann, A.; Herzel, H.; Schlosser, A.; Kramer, A. Differential effects of PER2 phosphorylation: Molecular basis for the human familial advanced sleep phase syndrome (FASPS). Genes Dev. 2006, 20, 2660–2672. [Google Scholar] [CrossRef] [PubMed]
- Xu, Y.; Toh, K.L.; Jones, C.R.; Shin, J.Y.; Fu, Y.H.; Ptácek, L.J. Modeling of a human circadian mutation yields insights into clock regulation by PER2. Cell 2007, 128, 59–70. [Google Scholar] [CrossRef] [PubMed]
- Hino, S.; Tanji, C.; Nakayama, K.; Kikuchi, A. Phosphorylation of beta-catenin by cyclic AMP-dependent protein kinase stabilizes beta-catenin through inhibition of its ubiquitination. Mol. Cell. Biol. 2005, 25, 9063–9072. [Google Scholar] [CrossRef] [PubMed]
- Van Veelen, W.; Le, N.H.; Helvensteijn, W.; Blonden, L.; Theeuwes, M.; Bakker, E.R.; Franken, P.F.; van Gurp, L.; Meijlink, F.; van der Valk, M.A.; et al. β-catenin tyrosine 654 phosphorylation increases Wnt signalling and intestinal tumorigenesis. Gut 2011, 60, 1204–1212. [Google Scholar] [CrossRef] [PubMed]
- Yang, Y.; He, Q.; Cheng, P.; Wrage, P.; Yarden, O.; Liu, Y. Distinct roles for PP1 and PP2A in the Neurospora circadian clock. Genes Dev. 2004, 18, 255–260. [Google Scholar] [CrossRef] [PubMed]
- Cha, J.; Chang, S.S.; Huang, G.; Cheng, P.; Liu, Y. Control of WHITE COLLAR localization by phosphorylation is a critical step in the circadian negative feedback process. EMBO J. 2008, 27, 3246–3255. [Google Scholar] [CrossRef] [PubMed]
- Cohen, P.T.; Philp, A.; Vázquez-Martin, C. Protein phosphatase 4—From obscurity to vital functions. FEBS Lett. 2005, 13, 3278–3286. [Google Scholar] [CrossRef] [PubMed]
- Querfurth, C.; Diernfellner, A.C.; Gin, E.; Malzahn, E.; Höfer, T.; Brunner, M. Circadian Conformational change of the Neurospora clock protein FREQUENCY triggered by clustered hyperphosphorylation of a Basic Domain. Mol. Cell 2011, 43, 713–722. [Google Scholar] [CrossRef] [PubMed]
- Cha, J.; Huang, G.; Guo, J.; Liu, Y. Posttranslational control of the Neurospora circadian clock. Cold Spring Harb. Symp. Quant. Biol. 2007, 72, 185–191. [Google Scholar] [CrossRef] [PubMed]
- Leung, P.C.; Taylor, W.A.; Wang, J.H.; Tipton, C.L. Ophiobolin A. A natural product inhibitor of calmodulin. J. Biol. Chem. 1984, 10, 2742–2747. [Google Scholar]
- He, Q.; Cheng, P.; Yang, Y.; Yu, H.; Liu, Y. FWD1-mediated degradation of FREQUENCY in Neurospora establishes a conserved mechanism for circadian clock regulation. EMBO J. 2003, 22, 4421–4430. [Google Scholar] [CrossRef] [PubMed]
- Lauter, F.R.; Russo, V.A. Light-induced dephosphorylation of a 33 kDa protein in the wild-type strain of Neurospora crassa. The regulatory mutants wc-1 and wc-2 are abnormal. J. Photochem. Photobiol. 1990, 5, 95–103. [Google Scholar] [CrossRef]
- Oda, K.; Hasunuma, K. Light signals are transduced to the phosphorylation of 15 kDa proteins in Neurospora crassa. FEBS Lett. 1994, 345, 162–166. [Google Scholar] [CrossRef]
- Talora, C.; Franchi, L.; Linden, H.; Ballario, P.; Macino, G. Role of a white collar-1-white collar-2 complex in blue-light signal transduction. EMBO J. 1999, 18, 4961–4968. [Google Scholar] [CrossRef] [PubMed]
- Schwerdtfeger, C.; Linden, H. Localization and light-dependent phosphorylation of WHITE COLLAR1 and 2, the two central components of blue light signaling in Neurospora crassa. Eur. J. Biochem. 2003, 22, 4846–4855. [Google Scholar]
- Arpaia, G.; Cerri, F.; Baima, S.; Macino, G. Involvement of protein kinase C in the response of Neurospora crassa to blue light. Mol. Gen. Genet. 1999, 262, 314–322. [Google Scholar] [CrossRef] [PubMed]
- Franchi, L.; Fulci, V.; Macino, G. Protein kinase C modulates light responses in Neurospora by regulating the blue light photoreceptor WC-1. Mol. Microbiol. 2005, 56, 334–345. [Google Scholar] [CrossRef] [PubMed]
- Franchi, L.; Macino, G. In vitro phosphorylation and kinase assays in Neurospora crassa. Methods Mol. Biol. 2007, 362, 407–412. [Google Scholar] [PubMed]
- Schafmeier, T.; Haase, A.; Kaldi, K.; Scholz, J.; Fuchs, M.; Brunner, M. Transcriptional feedback of Neurospora circadian clock gene by phosphorylation-dependent inactivation of its transcription factor. Cell 2005, 122, 235–246. [Google Scholar] [CrossRef] [PubMed]
- Sancar, G.; Sancar, C.; Brunner, M.; Schafmeier, T. Activity of the circadian transcription factor White Collar Complex is modulated by phosphorylation of SP-motifs. FEBS Lett. 2009, 583, 1833–1840. [Google Scholar] [CrossRef] [PubMed]
- Roux, P.P.; Blenis, J. ERK and p38 MAPK-activated protein kinases: A family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev. 2004, 68, 320–344. [Google Scholar] [CrossRef] [PubMed]
- Brenna, A.; Grimaldi, B.; Filetici, P.; Ballario, P. Physical association of the WC-1 photoreceptor and the histone acetyltransferase NGF-1 is required for blue light signal transduction in Neurospora crassa. Mol. Biol. Cell 2012, 23, 3863–3872. [Google Scholar] [CrossRef] [PubMed]
- Grimaldi, B.; Coiro, P.; Filetici, P.; Berge, E.; Dobosy, J.R.; Freitag, M.; Selker, E.U.; Ballario, P. The Neurospora crassa White Collar-1 dependent blue light response requires acetylation of histone H3 lysine 14 by NGF-1. Mol. Biol. Cell 2006, 17, 4576–4583. [Google Scholar] [CrossRef] [PubMed]
- He, Q.; Shu, H.; Cheng, P.; Chen, S.; Wang, L.; Liu, Y. Light-independent phosphorylation of WHITE COLLAR-1 regulates its function in the Neurospora circadian negative feedback loop. J. Biol. Chem. 2005, 280, 17526–17532. [Google Scholar] [CrossRef] [PubMed]
- Townsend, R.R.; Lipniunas, P.H.; Tulk, B.M.; Verkman, A.S. Identification of protein kinase A phosphorylation sites on NBD1 and R domains of CFTR using electrospray mass spectrometry with selective phosphate ion monitoring. Protein Sci. 1996, 5, 1865–1873. [Google Scholar] [CrossRef] [PubMed]
- Tataroğlu, Ö.; Lauinger, L.; Sancar, G.; Jakob, K.; Brunner, M.; Diernfellner, A.C. Glycogen synthase kinase is a regulator of the circadian clock of Neurospora crassa. J. Biol. Chem. 2012, 287, 36936–36943. [Google Scholar] [CrossRef] [PubMed]
- Schafmeier, T.; Diernfellner, A.; Schafer, A.; Dintsis, O.; Neiss, A.; Brunner, M. Circadian activity and abundance rhythms of the Neurospora clock transcription factor WCC associated with rapid nucleo-cytoplasmic shuttling. Genes Dev. 2008, 22, 3397–3402. [Google Scholar] [CrossRef] [PubMed]
- Edmondson, D.G.; Roth, S.Y. Chromatinand transcription. FASEB J. 1996, 10, 1173–1182. [Google Scholar] [PubMed]
- Narlikar, G.J.; Fan, H.Y.; Kingston, R.E. Cooperation between complexes that regulate chromatin structure and transcription. Cell 2002, 108, 475–487. [Google Scholar] [CrossRef]
- Allis, C.D.; Berger, S.L.; Cote, J.; Dent, S.; Jenuwien, T.; Kouzarides, T.; Pillus, L.; Reinberg, D.; Shi, Y.; Shiekhattar, R.; et al. New nomenclature for chromatin-modifying enzymes. Cell 2007, 131, 633–636. [Google Scholar] [CrossRef] [PubMed]
- Fischle, W.; Wang, Y.; Jacobs, S.A.; Kim, Y.; Allis, C.D.; Khorasanizadeh, S. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev. 2003, 17, 1870–1881. [Google Scholar] [CrossRef] [PubMed]
- Strahl, B.D.; Allis, C.D. The language of covalent histone modifications. Nature 2000, 403, 41–45. [Google Scholar] [CrossRef] [PubMed]
- Jenuwein, T.; Allis, C.D. Translating the histone code. Science 2001, 293, 1074–1080. [Google Scholar] [CrossRef] [PubMed]
- Naruse, Y.; Oh-hashi, K.; Iijima, N.; Naruse, M.; Yoshioka, H.; Tanaka, M. Circadian and light-induced transcription of clock gene Per1 depends on histone acetylation and deacetylation. Mol. Cell. Biol. 2004, 14, 6278–6287. [Google Scholar] [CrossRef] [PubMed]
- Etchegaray, J.P.; Yang, X.; de Bruyne, J.P.; Peters, A.H.; Weaver, D.R.; Jenuwein, T.; Reppert, S.M. The polycomb group protein EZH2 is required for mammalian circadian clock function. J. Biol. Chem. 2006, 281, 21209–21215. [Google Scholar] [CrossRef] [PubMed]
- Fu, H.; Maunakea, A.K.; Martin, M.M.; Huang, L.; Zhang, Y.; Ryan, M.; Kim, R.; Lin, C.M.; Zhao, K.; Aladjem, M.I. Methylation of histone H3 on lysine 79 associates with a group of replication origins and helps limit DNA replication once per cell cycle. PLoS Genet. 2013, 9, e1003542. [Google Scholar] [CrossRef] [PubMed]
- Crosio, C.; Cermakian, N.; Allis, C.D.; Sassone-Corsi, P. Light induces chromatin modification in cells of the mammalian circadian clock. Nat. Neurosci. 2000, 3, 1241–1247. [Google Scholar] [PubMed]
- Katada, S.; Sassone-Corsi, P. The histone methyltransferase MLL1 permits the oscillation of circadian gene expression. Nat. Struct. Mol. Biol. 2010, 17, 1414–1421. [Google Scholar] [CrossRef] [PubMed]
- Jones, M.A.; Covington, M.F.; DiTacchio, L.; Vollmers, C.; Panda, S.; Harmer, S.L. Jumonji domain protein JMJD5 functions in both the plant and human circadian systems. Proc. Natl. Acad. Sci. USA 2010, 107, 21623–21628. [Google Scholar] [CrossRef] [PubMed]
- Jones, M.A.; Harmer, S. JMJD5 Functions in concert with TOC1 in the Arabidopsis circadian system. Plant Signal. Behav. 2011, 6, 6445–6448. [Google Scholar] [CrossRef]
- Perales, M.; Más, P. A functional link between rhythmic changes in chromatin structure and the Arabidopsis biological clock. Plant Cell 2007, 19, 2111–2123. [Google Scholar] [CrossRef] [PubMed]
- Feng, B.; Marzluf, A. Interaction between major nitrogen regulatory protein NIT2 and pathways-specific regulatory factor NIT4 is required for their synergistic activation of gene expression in Neurospora crassa. Mol. Cell. Biol. 1998, 18, 3983–3990. [Google Scholar] [PubMed]
- Baima, S.; Macino, G.; Morelli, G. Photoregulation of the albino-3 gene in Neurospora crassa. J. Photochem. Photobiol. 1991, 11, 107–115. [Google Scholar] [CrossRef]
- Etchegaray, J.P.; Lee, C.; Wade, P.A.; Reppert, S.M. Rhythmic histone acetylation underlies transcription in the mammalian circadian clock. Nature 2003, 421, 177–182. [Google Scholar] [CrossRef] [PubMed]
- Carrozza, M.J.; Utley, R.T.; Workman, J.L.; Cote, J. The diverse functions of histone acetyltransferase complexes. Trends Genet. 2003, 19, 321–329. [Google Scholar] [CrossRef]
- Belden, W.J.; Loros, J.J.; Dunlap, J.C. Execution of the circadian negative feedback loop in Neurospora requires the ATP-dependent chromatin-remodeling enzyme CLOCK SWITCH. Mol. Cell 2007, 25, 587–600. [Google Scholar] [CrossRef] [PubMed]
- Crosson, S.; Moffat, K. Photoexcited structure of a plant photoreceptor domain reveals a light-driven molecular switch. Plant Cell 2002, 14, 1067–1075. [Google Scholar] [CrossRef] [PubMed]
- Savkur, R.S.; Burris, T.P. The coactivator LXXLL nuclear receptor recognition motif. J. Pept. Res. 2004, 63, 207–212. [Google Scholar] [CrossRef] [PubMed]
- Schmutz, I.; Ripperger, J.A.; Baeriswyl-Aebischer, S.; Albrecht, U. The mammalian clock component PERIOD2 coordinates circadian output by interaction with nuclear receptors. Genes Dev. 2010, 24, 345–357. [Google Scholar] [CrossRef] [PubMed]
- Näär, A.M.; Thakur, J.K. Nuclear receptor-like transcription factors in fungi. Genes Dev. 2009, 23, 419–432. [Google Scholar] [CrossRef] [PubMed]
- Belden, W.J.; Lewis, Z.A.; Selker, E.U.; Loros, J.J.; Dunlap, J.C. CHD1 remodels chromatin and influences transient DNA methylation at the clock gene frequency. PLoS Genet. 2011, 7, e1002166. [Google Scholar] [CrossRef] [PubMed]
- Ruesch, C.E.; Ramakrishnan, M.; Park, J.; Li, N.; Chong, H.S.; Zaman, R.; Joska, T.M.; Belden, W.J. The histone H3 lysine 9 methyltransferase DIM-5 modifies chromatin at frequency and represses light-activated gene expression. Genes Genomes Genet. 2014, 1, 93–101. [Google Scholar] [CrossRef] [PubMed]
- Selker, E.U.; Tountas, N.A.; Cross, S.H.; Margolin, B.S.; Murphy, J.G.; Bird, A.P.; Freitag, M. The methylated component of the Neurospora crassa genome. Nature 2003, 422, 893–897. [Google Scholar] [CrossRef] [PubMed]
- Lewis, Z.A.; Honda, S.; Khlafallah, T.K.; Jeffress, J.K.; Freitag, M.; Mohn, F.; Schübeler, D.; Selker, E.U. Relics of repeat-induced point mutation direct heterochromatin formation in Neurospora crassa. Genome Res. 2009, 19, 427–437. [Google Scholar] [CrossRef] [PubMed]
- Cha, J.; Zhou, M.; Liu, Y. CATP is a critical component of the Neurospora circadian clock by regulating the nucleosome occupancy rhythm at the frequency locus. EMBO Rep. 2013, 14, 923–930. [Google Scholar] [CrossRef] [PubMed]
- Raduwan, H.; Isola, A.L.; Belden, W.J. Methylation of histone H3 on lysine 4 by the lysine methyltransferase SET1 protein is needed for normal clock gene expression. J. Biol. Chem. 2013, 288, 8380–8390. [Google Scholar] [CrossRef] [PubMed]
- Miller, T.; Krogan, N.J.; Dover, J.; Erdjument-Bromage, H.; Tempst, P.; Johnston, M.; Greenblatt, J.F.; Shilatifard, A. COMPASS: A complex of proteins associated with a trithorax-related SET domain protein. Proc. Natl. Acad. Sci. USA 2001, 98, 12902–12907. [Google Scholar] [CrossRef] [PubMed]
- Barski, A.; Cuddapah, S.; Cui, K.; Roh, T.Y.; Schones, D.E.; Wang, Z.; Wei, G.; Chepelev, I.; Zhao, K. High-resolution profiling of histone methylations in the human genome. Cell 2007, 129, 823–837. [Google Scholar] [CrossRef] [PubMed]
- Lee, C.; Etchegaray, J.P.; Cagampang, F.R.; Loudon, A.S.; Reppert, S.M. Posttranslational mechanisms regulate the mammalian circadian clock. Cell 2001, 107, 855–867. [Google Scholar] [CrossRef]
- Brunner, M.; Kaldi, K. Interlocked feedback loops of the circadian clock of Neurospora crassa. Mol. Microbiol. 2008, 68, 255–262. [Google Scholar] [CrossRef] [PubMed]
- Wang, B.; Kettenbach, A.N.; Gerber, S.A.; Loros, J.J; Dunlap, J.C. Neurospora WC-1 recruits SWI/SNF to remodel frequency and initiate a circadian cycle. PLoS Genet. 2014, 9, e1004599. [Google Scholar] [CrossRef] [PubMed]
- Clapier, C.R.; Cairns, B.R. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 2009, 78, 273–304. [Google Scholar] [CrossRef] [PubMed]
- De la Serna, I.L.; Ohkawa, Y.; Imbalzano, A.N. Chromatin remodelling in mammalian differentiation: Lessons from ATP-dependent remodellers. Nat. Rev. Genet. 2006, 6, 461–473. [Google Scholar] [CrossRef] [PubMed]
- Nishiwaki, T.; Iwasaki, H.; Ishiura, M.; Kondo, T. Nucleotide binding and autophosphorylation of the clock protein KaiC as a circadian timing process of cyanobacteria. Proc. Natl. Acad. Sci. USA 2000, 97, 495–498. [Google Scholar] [CrossRef] [PubMed]
- Nakajima, M.; Imai, K.; Ito, H.; Nishiwaki, T.; Murayama, Y.; Iwasaki, H.; Oyama, T.; Kondo, T. Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 2005, 15, 414–415. [Google Scholar] [CrossRef] [PubMed]
- Iwasaki, H.; Nishiwaki, T.; Kitayama, Y.; Nakajimam, M.; Kondo, T. KaiA-stimulated KaiC phosphorylation in circadian timing loops in cyanobacteria. Proc. Natl. Acad. Sci. USA 2002, 99, 15788–15793. [Google Scholar] [CrossRef] [PubMed]
- Edery, I.; Zwiebel, L.J.; Dembinska, M.E.; Rosbash, M. Temporal phosphorylation of the Drosophila period protein. Proc. Natl. Acad. Sci. USA 1994, 91, 2260–2264. [Google Scholar] [CrossRef] [PubMed]
- Lin, J.M.; Schroeder, A.; Allada, R. In vivo circadian function of casein kinase 2 phosphorylation sites in Drosophila PERIOD. J. Neurosci. 2005, 25, 11175–11183. [Google Scholar] [CrossRef] [PubMed]
- Baker, C.L.; Dunlap, J.C. Circadian rhythms: Phosphorylating the CLOCK. Cell Cycle 2010, 9, 231–232. [Google Scholar] [CrossRef] [PubMed]
- Kondratov, R.V.; Chernov, M.V.; Kondratova, A.A.; Gorbacheva, V.Y.; Gudkov, A.V.; Antoch, M.P. BMAL1-dependent circadian oscillation of nuclear CLOCK: Posttranslational events induced by dimerization of transcriptional activators of the mammalian clock system. Genes Dev. 2003, 17, 1921–1932. [Google Scholar] [CrossRef] [PubMed]
- Spengler, M.L.; Kuropatwinski, K.K.; Schumer, M.; Antoch, M.P. A serine cluster mediates BMAL1-dependent CLOCK phosphorylation and degradation. Cell Cycle 2009, 8, 4138–4146. [Google Scholar] [CrossRef] [PubMed]
- Yoshitane, H.; Takao, T.; Satomi, Y.; Du, N.H.; Okano, T.; Fukada, Y. Roles of CLOCK phosphorylation in suppression of E-box-dependent transcription. Mol. Cell. Biol. 2009, 29, 3675–3686. [Google Scholar] [CrossRef] [PubMed]
- Vanselow, K.; Kramer, A. Role of phosphorylation in the mammalian circadian clock. Cold Spring Harb. Symp. Quant. Biol. 2007, 72, 167–176. [Google Scholar] [CrossRef] [PubMed]
- Dardente, H.; Fortier, E.E.; Martineau, V.; Cermakian, N. Cryptochromes impair phosphorylation of transcriptional activators in the clock: A general mechanism for circadian repression. Biochem. J. 2007, 402, 525–536. [Google Scholar] [PubMed]
- Vollmers, C.; Schmitz, R.J.; Nathanson, J.; Yeo, G.; Ecker, J.R.; Panda, S. Circadian oscillations of protein-coding and regulatory RNAs in a highly dynamic mammalian liver epigenome. Cell Metab. 2012, 16, 833–845. [Google Scholar] [CrossRef] [PubMed]
© 2015 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Proietto, M.; Bianchi, M.M.; Ballario, P.; Brenna, A. Epigenetic and Posttranslational Modifications in Light Signal Transduction and the Circadian Clock in Neurospora crassa. Int. J. Mol. Sci. 2015, 16, 15347-15383. https://doi.org/10.3390/ijms160715347
Proietto M, Bianchi MM, Ballario P, Brenna A. Epigenetic and Posttranslational Modifications in Light Signal Transduction and the Circadian Clock in Neurospora crassa. International Journal of Molecular Sciences. 2015; 16(7):15347-15383. https://doi.org/10.3390/ijms160715347
Chicago/Turabian StyleProietto, Marco, Michele Maria Bianchi, Paola Ballario, and Andrea Brenna. 2015. "Epigenetic and Posttranslational Modifications in Light Signal Transduction and the Circadian Clock in Neurospora crassa" International Journal of Molecular Sciences 16, no. 7: 15347-15383. https://doi.org/10.3390/ijms160715347