Maintenance of Cell Fates and Regulation of the Histone Variant H3.3 by TLK Kinase in

Overview

Journal Biol Open

Specialty Biology

Date 2019 Jan 13

PMID 30635266

Citations 1

Authors

Yukimasa Shibata

Yoshiyuki Seki

Kiyoji Nishiwaki

Affiliations

Soon will be listed here.

Abstract

Cell-fate maintenance is important to preserve the variety of cell types that are essential for the formation and function of tissues. We previously showed that the acetylated histone-binding protein BET-1 maintains cell fate by recruiting the histone variant H2A.z. Here, we report that TLK-1 and the histone H3 chaperone CAF1 prevent the accumulation of histone variant H3.3. In addition, TLK-1 and CAF1 maintain cell fate by repressing ectopic expression of transcription factors that induce cell-fate specification. Genetic analyses suggested that TLK-1 and BET-1 act in parallel pathways. In mutants, the loss of SIN-3, which promotes histone acetylation, suppressed a defect in cell-fate maintenance in a manner dependent on MYST family histone acetyltransferase MYS-2 and BET-1. mutation also suppressed abnormal H3.3 incorporation. Thus, we propose a hypothesis that the regulation and interaction of histone variants play crucial roles in cell-fate maintenance through the regulation of selector genes.

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References

Kamath R, Martinez-Campos M, Zipperlen P, Fraser A, Ahringer J . Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2001; 2(1):RESEARCH0002. PMC: 17598. DOI: 10.1186/gb-2000-2-1-research0002. View

Nass R, Hall D, Miller 3rd D, Blakely R . Neurotoxin-induced degeneration of dopamine neurons in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2002; 99(5):3264-9. PMC: 122507. DOI: 10.1073/pnas.042497999. View

Kamath R, Fraser A, Dong Y, Poulin G, Durbin R, Gotta M . Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature. 2003; 421(6920):231-7. DOI: 10.1038/nature01278. View

Clark S, Chiu C . C. elegans ZAG-1, a Zn-finger-homeodomain protein, regulates axonal development and neuronal differentiation. Development. 2003; 130(16):3781-94. DOI: 10.1242/dev.00571. View

Toker A, Teng Y, Ferreira H, Emmons S, Chalfie M . The Caenorhabditis elegans spalt-like gene sem-4 restricts touch cell fate by repressing the selector Hox gene egl-5 and the effector gene mec-3. Development. 2003; 130(16):3831-40. DOI: 10.1242/dev.00398. View

Kostic I, Li S, Roy R . cki-1 links cell division and cell fate acquisition in the C. elegans somatic gonad. Dev Biol. 2003; 263(2):242-52. DOI: 10.1016/j.ydbio.2003.07.001. View

Han Z, Saam J, Adams H, Mango S, Schumacher J . The C. elegans Tousled-like kinase (TLK-1) has an essential role in transcription. Curr Biol. 2003; 13(22):1921-9. DOI: 10.1016/j.cub.2003.10.035. View

Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y . Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell. 2004; 116(1):51-61. DOI: 10.1016/s0092-8674(03)01064-x. View

Chase D, Pepper J, Koelle M . Mechanism of extrasynaptic dopamine signaling in Caenorhabditis elegans. Nat Neurosci. 2004; 7(10):1096-103. DOI: 10.1038/nn1316. View

10.

Ringrose L, Paro R . Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu Rev Genet. 2004; 38:413-43. DOI: 10.1146/annurev.genet.38.072902.091907. View

11.

Han Z, Riefler G, Saam J, Mango S, Schumacher J . The C. elegans Tousled-like kinase contributes to chromosome segregation as a substrate and regulator of the Aurora B kinase. Curr Biol. 2005; 15(10):894-904. PMC: 2653428. DOI: 10.1016/j.cub.2005.04.019. View

12.

Wirbelauer C, Bell O, Schubeler D . Variant histone H3.3 is deposited at sites of nucleosomal displacement throughout transcribed genes while active histone modifications show a promoter-proximal bias. Genes Dev. 2005; 19(15):1761-6. PMC: 1182337. DOI: 10.1101/gad.347705. View

13.

Lam N, Chesney M, Kimble J . Wnt signaling and CEH-22/tinman/Nkx2.5 specify a stem cell niche in C. elegans. Curr Biol. 2006; 16(3):287-95. PMC: 1637041. DOI: 10.1016/j.cub.2005.12.015. View

14.

Ooi S, Priess J, Henikoff S . Histone H3.3 variant dynamics in the germline of Caenorhabditis elegans. PLoS Genet. 2006; 2(6):e97. PMC: 1484599. DOI: 10.1371/journal.pgen.0020097. View

15.

Wang Y, Liu J, Xia R, Wang J, Shen J, Cao R . The protein kinase TOUSLED is required for maintenance of transcriptional gene silencing in Arabidopsis. EMBO Rep. 2006; 8(1):77-83. PMC: 1796745. DOI: 10.1038/sj.embor.7400852. View

16.

Grigsby I, Finger F . UNC-85, a C. elegans homolog of the histone chaperone Asf1, functions in post-embryonic neuroblast replication. Dev Biol. 2008; 319(1):100-9. DOI: 10.1016/j.ydbio.2008.04.013. View

17.

Hobert O . Regulatory logic of neuronal diversity: terminal selector genes and selector motifs. Proc Natl Acad Sci U S A. 2008; 105(51):20067-71. PMC: 2629285. DOI: 10.1073/pnas.0806070105. View

18.

Grigsby I, Rutledge E, Morton C, Finger F . Functional redundancy of two C. elegans homologs of the histone chaperone Asf1 in germline DNA replication. Dev Biol. 2009; 329(1):64-79. DOI: 10.1016/j.ydbio.2009.02.015. View

19.

Ooi S, Henikoff J, Henikoff S . A native chromatin purification system for epigenomic profiling in Caenorhabditis elegans. Nucleic Acids Res. 2009; 38(4):e26. PMC: 2831312. DOI: 10.1093/nar/gkp1090. View

20.

Shibata Y, Takeshita H, Sasakawa N, Sawa H . Double bromodomain protein BET-1 and MYST HATs establish and maintain stable cell fates in C. elegans. Development. 2010; 137(7):1045-53. DOI: 10.1242/dev.042812. View