WC-1 Recruits SWI/SNF to Remodel and Initiate a Circadian Cycle

English version České info

Circadian clocks govern behavior in a wide variety of organisms. These clocks are assembled in such a way that proteins encoded by a few dedicated “clock genes” form a complex that acts to reduce their own expression. That is, the genes and proteins participate in a negative feedback loop, and so long as the feedback has delays built in, this system will oscillate. The feedback loops that underlie circadian rhythms in fungi and animals are quite similar in many ways, and while much is known about the proteins themselves, both those that activate the dedicated clock genes and the clock proteins that repress their own expression, relatively little is known about how the initial expression of the clock genes is activated. In Neurospora, a fungal model for these clocks, the proteins that activate expression of the clock gene “frequency” bind to DNA far away from where the coding part of the gene begins, and a mystery has been how this action-at-a-distance works. The answer revealed here is that the activating proteins recruit other proteins to unwrap the DNA and bring the distal site close to the place where the coding part of the gene begins.

Vyšlo v časopise: WC-1 Recruits SWI/SNF to Remodel and Initiate a Circadian Cycle. PLoS Genet 10(9): e32767. doi:10.1371/journal.pgen.1004599
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004599

Souhrn

Zdroje

1. FroehlichAC, LorosJJ, DunlapJC (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.

2. FroehlichAC, LiuY, LorosJJ, DunlapJC (2002) White Collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297: 815–819.

3. LeeK, LorosJJ, DunlapJC (2000) Interconnected feedback loops in the Neurospora circadian system. Science 289: 107–110.

4. ShiM, CollettM, LorosJJ, DunlapJC (2010) FRQ-interacting RNA helicase mediates negative and positive feedback in the Neurospora circadian clock. Genetics 184: 351–361.

5. ChengP, HeQ, WangL, LiuY (2005) Regulation of the Neurospora circadian clock by an RNA helicase. Genes Dev 19: 234–241.

6. AronsonBD, JohnsonKA, LorosJJ, DunlapJC (1994) Negative feedback defining a circadian clock: autoregulation of the clock gene frequency. Science 263: 1578–1584.

7. SchafmeierT, HaaseA, KaldiK, ScholzJ, FuchsM, et al. (2005) Transcriptional feedback of Neurospora circadian clock gene by phosphorylation-dependent inactivation of its transcription factor. Cell 122: 235–246.

8. HeQ, ChaJ, LeeHC, YangY, LiuY (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.

9. HeQ, ChengP, YangY, WangL, GardnerKH, et al. (2002) White collar-1, a DNA binding transcription factor and a light sensor. Science 297: 840–843.

10. ChengP, YangY, WangL, HeQ, LiuY (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.

11. BallarioP, VittoriosoP, MagrelliA, TaloraC, CabibboA, et al. (1996) White collar-1, a central regulator of blue light responses in Neurospora, is a zinc finger protein. Embo Journal 15: 1650–1657.

12. VignaliM, HassanAH, NeelyKE, WorkmanJL (2000) ATP-dependent chromatin-remodeling complexes. Mol Cell Biol 20: 1899–1910.

13. FlausA, Owen-HughesT (2001) Mechanisms for ATP-dependent chromatin remodelling. Curr Opin Genet Dev 11: 148–154.

14. ClapierCR, CairnsBR (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78: 273–304.

15. de la SernaIL, OhkawaY, ImbalzanoAN (2006) Chromatin remodelling in mammalian differentiation: lessons from ATP-dependent remodellers. Nat Rev Genet 7: 461–473.

16. SudarsanamP, IyerVR, BrownPO, WinstonF (2000) Whole-genome expression analysis of snf/swi mutants of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 97: 3364–3369.

17. LaurentBC, TreichI, CarlsonM (1993) The yeast SNF2/SWI2 protein has DNA-stimulated ATPase activity required for transcriptional activation. Genes Dev 7: 583–591.

18. DrorV, WinstonF (2004) The Swi/Snf chromatin remodeling complex is required for ribosomal DNA and telomeric silencing in Saccharomyces cerevisiae. Mol Cell Biol 24: 8227–8235.

19. SternM, JensenR, HerskowitzI (1984) Five SWI genes are required for expression of the HO gene in yeast. J Mol Biol 178: 853–868.

20. PetersonCL, HerskowitzI (1992) Characterization of the yeast SWI1, SWI2, and SWI3 genes, which encode a global activator of transcription. Cell 68: 573–583.

21. ZhaoJ, Herrera-DiazJ, GrossDS (2005) Domain-wide displacement of histones by activated heat shock factor occurs independently of Swi/Snf and is not correlated with RNA polymerase II density. Mol Cell Biol 25: 8985–8999.

22. AbramsE, NeigebornL, CarlsonM (1986) Molecular analysis of SNF2 and SNF5, genes required for expression of glucose-repressible genes in Saccharomyces cerevisiae. Mol Cell Biol 6: 3643–3651.

23. LaurentBC, TreitelMA, CarlsonM (1990) The SNF5 protein of Saccharomyces cerevisiae is a glutamine- and proline-rich transcriptional activator that affects expression of a broad spectrum of genes. Mol Cell Biol 10: 5616–5625.

24. CoteJ, PetersonCL, WorkmanJL (1998) Perturbation of nucleosome core structure by the SWI/SNF complex persists after its detachment, enhancing subsequent transcription factor binding. Proc Natl Acad Sci U S A 95: 4947–4952.

25. QuinnJ, FyrbergAM, GansterRW, SchmidtMC, PetersonCL (1996) DNA-binding properties of the yeast SWI/SNF complex. Nature 379: 844–847.

26. SudarsanamP, WinstonF (2000) The Swi/Snf family nucleosome-remodeling complexes and transcriptional control. Trends Genet 16: 345–351.

27. NeelyKE, HassanAH, WallbergAE, StegerDJ, CairnsBR, et al. (1999) Activation domain-mediated targeting of the SWI/SNF complex to promoters stimulates transcription from nucleosome arrays. Mol Cell 4: 649–655.

28. KingstonRE, NarlikarGJ (1999) ATP-dependent remodeling and acetylation as regulators of chromatin fluidity. Genes Dev 13: 2339–2352.

29. PetersonCL, WorkmanJL (2000) Promoter targeting and chromatin remodeling by the SWI/SNF complex. Curr Opin Genet Dev 10: 187–192.

30. EtchegarayJP, LeeC, WadePA, ReppertSM (2003) Rhythmic histone acetylation underlies transcription in the mammalian circadian clock. Nature 421: 177–182.

31. BeldenWJ, LorosJJ, DunlapJC (2007) Execution of the circadian negative feedback loop in Neurospora requires the ATP-dependent chromatin-remodeling enzyme CLOCKSWITCH. Mol Cell 25: 587–600.

32. BeldenWJ, LewisZA, SelkerEU, LorosJJ, DunlapJC (2011) CHD1 remodels chromatin and influences transient DNA methylation at the clock gene frequency. PLoS Genet 7: e1002166.

33. GarceauNY, LiuY, LorosJJ, DunlapJC (1997) Alternative initiation of translation and time-specific phosphorylation yield multiple forms of the essential clock protein FREQUENCY. Cell 89: 469–476.

34. LeeK, DunlapJC, LorosJJ (2003) Roles for WHITE COLLAR-1 in circadian and general photoperception in Neurospora crassa. Genetics 163: 103–114.

35. NatarajanK, JacksonBM, ZhouH, WinstonF, HinnebuschAG (1999) Transcriptional activation by Gcn4p involves independent interactions with the SWI/SNF complex and the SRB/mediator. Mol Cell 4: 657–664.

36. Owen-HughesT, UtleyRT, CoteJ, PetersonCL, WorkmanJL (1996) Persistent site-specific remodeling of a nucleosome array by transient action of the SWI/SNF complex. Science 273: 513–516.

37. YudkovskyN, LogieC, HahnS, PetersonCL (1999) Recruitment of the SWI/SNF chromatin remodeling complex by transcriptional activators. Genes Dev 13: 2369–2374.

38. NeelyKE, HassanAH, BrownCE, HoweL, WorkmanJL (2002) Transcription activator interactions with multiple SWI/SNF subunits. Mol Cell Biol 22: 1615–1625.

39. BeldenWJ, LarrondoLF, FroehlichAC, ShiM, ChenCH, et al. (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.

40. LarrondoLF, LorosJJ, DunlapJC (2012) High-resolution spatiotemporal analysis of gene expression in real time: in vivo analysis of circadian rhythms in Neurospora crassa using a FREQUENCY-luciferase translational reporter. Fungal Genet Biol 49: 681–683.

41. BurnsLG, PetersonCL (1997) The yeast SWI-SNF complex facilitates binding of a transcriptional activator to nucleosomal sites in vivo. Mol Cell Biol 17: 4811–4819.

42. GregoryPD, SchmidA, ZavariM, MunsterkotterM, HorzW (1999) Chromatin remodelling at the PHO8 promoter requires SWI-SNF and SAGA at a step subsequent to activator binding. Embo Journal 18: 6407–6414.

43. KingstonRE, BunkerCA, ImbalzanoAN (1996) Repression and activation by multiprotein complexes that alter chromatin structure. Genes & Development 10: 905–920.

44. CosmaMP, TanakaT, NasmythK (1999) Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle- and developmentally regulated promoter. Cell 97: 299–311.

45. KwonH, ImbalzanoAN, KhavariPA, KingstonRE, GreenMR (1994) Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex. Nature 370: 477–481.

46. WangW, CoteJ, XueY, ZhouS, KhavariPA, et al. (1996) Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. EMBO J 15: 5370–5382.

47. NieZ, XueY, YangD, ZhouS, DerooBJ, et al. (2000) A specificity and targeting subunit of a human SWI/SNF family-related chromatin-remodeling complex. Mol Cell Biol 20: 8879–8888.

48. XueYT, CanmanJC, LeeCS, NieZQ, YangDF, et al. (2000) The human SWI/SNF-B chromatin-remodeling complex is related to yeast Rsc and localizes at kinetochores of mitotic chromosomes. Proceedings of the National Academy of Sciences of the United States of America 97: 13015–13020.

49. LemonB, InouyeC, KingDS, TjianR (2001) Selectivity of chromatin-remodelling cofactors for ligand-activated transcription. Nature 414: 924–928.

50. ProchassonP, NeelyKE, HassanAH, LiB, WorkmanJL (2003) Targeting activity is required for SWI/SNF function in vivo and is accomplished through two partially redundant activator-interaction domains. Molecular Cell 12: 983–990.

51. Bazett-JonesDP, CoteJ, LandelCC, PetersonCL, WorkmanJL (1999) The SWI/SNF complex creates loop domains in DNA and polynucleosome arrays and can disrupt DNA-histone contacts within these domains. Mol Cell Biol 19: 1470–1478.

52. ZhangY, SmithCL, SahaA, GrillSW, MihardjaS, et al. (2006) DNA translocation and loop formation mechanism of chromatin remodeling by SWI/SNF and RSC. Mol Cell 24: 559–568.

53. LiG, RuanX, AuerbachRK, SandhuKS, ZhengM, et al. (2012) Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell 148: 84–98.

54. CaiS, LeeCC, Kohwi-ShigematsuT (2006) SATB1 packages densely looped, transcriptionally active chromatin for coordinated expression of cytokine genes. Nat Genet 38: 1278–1288.

55. NiZ, Abou El HassanM, XuZ, YuT, BremnerR (2008) The chromatin-remodeling enzyme BRG1 coordinates CIITA induction through many interdependent distal enhancers. Nat Immunol 9: 785–793.

56. ToyotaK, OnaiK, NakashimaH (2002) A new wc-1 mutant of Neurospora crassa shows unique light sensitivity in the circadian conidiation rhythm. Molecular Genetics and Genomics 268: 56–61.

57. ChenCH, DeMayBS, GladfelterAS, DunlapJC, LorosJJ (2010) Physical interaction between VIVID and white collar complex regulates photoadaptation in Neurospora. Proceedings of the National Academy of Sciences of the United States of America 107: 16715–16720.

58. MalzahnE, CiprianidisS, KaldiK, SchafmeierT, BrunnerM (2010) Photoadaptation in Neurospora by competitive interaction of activating and inhibitory LOV domains. Cell 142: 762–772.

59. BrennaA, GrimaldiB, FileticiP, BallarioP (2012) Physical association of the WC-1 photoreceptor and the histone acetyltransferase NGF-1 is required for blue light signal transduction in Neurospora crassa. Molecular Biology of the Cell 23: 3863–3872.

60. MichaelTP, ParkS, KimTS, BoothJ, ByerA, et al. (2007) Simple sequence repeats provide a substrate for phenotypic variation in the Neurospora crassa circadian clock. PLoS One 2: e795.

61. ChaJ, ZhouM, LiuY (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.

62. CrosthwaiteSK, LorosJJ, DunlapJC (1995) Light-induced resetting of a circadian clock is mediated by a rapid increase in frequency transcript. Cell 81: 1003–1012.

63. ColotHV, ParkG, TurnerGE, RingelbergC, CrewCM, et al. (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.

64. BakerCL, KettenbachAN, LorosJJ, GerberSA, DunlapJC (2009) Quantitative proteomics reveals a dynamic interactome and phase-specific phosphorylation in the Neurospora circadian clock. Mol Cell 34: 354–363.

65. HongCI, RuoffP, LorosJJ, DunlapJC (2008) Closing the circadian negative feedback loop: FRQ-dependent clearance of WC-1 from the nucleus. Genes Dev 22: 3196–3204.