Molecular Turnover, the H3.3 Dilemma and Organismal Aging (hypothesis)

Overview

Journal Aging Cell

Specialties Cell Biology
Geriatrics

Date 2015 Feb 28

PMID 25720734

Citations 6

Authors

Evelyne Saade

Iryna Pirozhkova

Rakhan Aimbetov

Marc Lipinski

Vasily Ogryzko

Affiliations

Soon will be listed here.

Abstract

The H3.3 histone variant has been a subject of increasing interest in the field of chromatin studies due to its two distinguishing features. First, its incorporation into chromatin is replication independent unlike the replication-coupled deposition of its canonical counterparts H3.1/2. Second, H3.3 has been consistently associated with an active state of chromatin. In accordance, this histone variant should be expected to be causally involved in the regulation of gene expression, or more generally, its incorporation should have downstream consequences for the structure and function of chromatin. This, however, leads to an apparent paradox: In cells that slowly replicate in the organism, H3.3 will accumulate with time, opening the way to aberrant effects on heterochromatin. Here, we review the indications that H3.3 is expected both to be incorporated in the heterochromatin of slowly replicating cells and to retain its functional downstream effects. Implications for organismal aging are discussed.

Citing Articles

Histones and their chaperones: Adaptive remodelers of an ever-changing chromatinic landscape.

Torres-Arciga K, Flores-Leon M, Ruiz-Perez S, Trujillo-Pineda M, Gonzalez-Barrios R, Herrera L Front Genet. 2022; 13:1057846.

PMID: 36468032 PMC: 9709290. DOI: 10.3389/fgene.2022.1057846.

Remodeling of the H3 nucleosomal landscape during mouse aging.

Chen Y, Bravo J, Son J, Lee C, Benayoun B Transl Med Aging. 2020; 4:22-31.

PMID: 32462102 PMC: 7252472. DOI: 10.1016/j.tma.2019.12.003.

Histone variant H3.3-mediated chromatin remodeling is essential for paternal genome activation in mouse preimplantation embryos.

Kong Q, Banaszynski L, Geng F, Zhang X, Zhang J, Zhang H J Biol Chem. 2018; 293(10):3829-3838.

PMID: 29358330 PMC: 5846143. DOI: 10.1074/jbc.RA117.001150.

Accumulation of histone variant H3.3 with age is associated with profound changes in the histone methylation landscape.

Tvardovskiy A, Schwammle V, Kempf S, Rogowska-Wrzesinska A, Jensen O Nucleic Acids Res. 2017; 45(16):9272-9289.

PMID: 28934504 PMC: 5766163. DOI: 10.1093/nar/gkx696.

Replication-Independent Histone Variant H3.3 Controls Animal Lifespan through the Regulation of Pro-longevity Transcriptional Programs.

Piazzesi A, Papic D, Bertan F, Salomoni P, Nicotera P, Bano D Cell Rep. 2016; 17(4):987-996.

PMID: 27760329 PMC: 5081402. DOI: 10.1016/j.celrep.2016.09.074.

References

Fernandez-Capetillo O, Mahadevaiah S, Celeste A, Romanienko P, Camerini-Otero R, Bonner W . H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell. 2003; 4(4):497-508. DOI: 10.1016/s1534-5807(03)00093-5. View

Creyghton M, Markoulaki S, Levine S, Hanna J, Lodato M, Sha K . H2AZ is enriched at polycomb complex target genes in ES cells and is necessary for lineage commitment. Cell. 2008; 135(4):649-61. PMC: 2853257. DOI: 10.1016/j.cell.2008.09.056. View

Ogryzko V . Erwin Schroedinger, Francis Crick and epigenetic stability. Biol Direct. 2008; 3:15. PMC: 2413215. DOI: 10.1186/1745-6150-3-15. View

Howitz K, Bitterman K, Cohen H, Lamming D, Lavu S, Wood J . Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature. 2003; 425(6954):191-6. DOI: 10.1038/nature01960. View

Elsaesser S, Goldberg A, Allis C . New functions for an old variant: no substitute for histone H3.3. Curr Opin Genet Dev. 2010; 20(2):110-7. PMC: 2860041. DOI: 10.1016/j.gde.2010.01.003. View

Li A, Maffey A, Abbott W, Conde E Silva N, Prunell A, Siino J . Characterization of nucleosomes consisting of the human testis/sperm-specific histone H2B variant (hTSH2B). Biochemistry. 2005; 44(7):2529-35. DOI: 10.1021/bi048061n. View

CARTER D, Chae C . Composition of liver histones in aging rat and mouse. J Gerontol. 1975; 30(1):28-32. DOI: 10.1093/geronj/30.1.28. View

Luger K, Dechassa M, Tremethick D . New insights into nucleosome and chromatin structure: an ordered state or a disordered affair?. Nat Rev Mol Cell Biol. 2012; 13(7):436-47. PMC: 3408961. DOI: 10.1038/nrm3382. View

Kaeberlein M, McVey M, Guarente L . The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev. 1999; 13(19):2570-80. PMC: 317077. DOI: 10.1101/gad.13.19.2570. View

10.

de Magalhaes J, Chainiaux F, DE Longueville F, Mainfroid V, Migeot V, Marcq L . Gene expression and regulation in H2O2-induced premature senescence of human foreskin fibroblasts expressing or not telomerase. Exp Gerontol. 2004; 39(9):1379-89. DOI: 10.1016/j.exger.2004.06.004. View

11.

Pchelintsev N, McBryan T, Rai T, van Tuyn J, Ray-Gallet D, Almouzni G . Placing the HIRA histone chaperone complex in the chromatin landscape. Cell Rep. 2013; 3(4):1012-9. PMC: 3974909. DOI: 10.1016/j.celrep.2013.03.026. View

12.

Tachiwana H, Kagawa W, Osakabe A, Kawaguchi K, Shiga T, Hayashi-Takanaka Y . Structural basis of instability of the nucleosome containing a testis-specific histone variant, human H3T. Proc Natl Acad Sci U S A. 2010; 107(23):10454-9. PMC: 2890842. DOI: 10.1073/pnas.1003064107. View

13.

Serrano M, Lin A, McCurrach M, Beach D, Lowe S . Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell. 1997; 88(5):593-602. DOI: 10.1016/s0092-8674(00)81902-9. View

14.

Skene P, Henikoff S . Histone variants in pluripotency and disease. Development. 2013; 140(12):2513-24. DOI: 10.1242/dev.091439. View

15.

Mito Y, Henikoff J, Henikoff S . Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet. 2005; 37(10):1090-7. DOI: 10.1038/ng1637. View

16.

Dimri G, Lee X, Basile G, Acosta M, Scott G, Roskelley C . A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A. 1995; 92(20):9363-7. PMC: 40985. DOI: 10.1073/pnas.92.20.9363. View

17.

Campisi J . Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell. 2005; 120(4):513-22. DOI: 10.1016/j.cell.2005.02.003. View

18.

Guo R, Zheng L, Park J, Lv R, Chen H, Jiao F . BS69/ZMYND11 reads and connects histone H3.3 lysine 36 trimethylation-decorated chromatin to regulated pre-mRNA processing. Mol Cell. 2014; 56(2):298-310. PMC: 4363072. DOI: 10.1016/j.molcel.2014.08.022. View

19.

Behjati S, Tarpey P, Presneau N, Scheipl S, Pillay N, Van Loo P . Distinct H3F3A and H3F3B driver mutations define chondroblastoma and giant cell tumor of bone. Nat Genet. 2013; 45(12):1479-82. PMC: 3839851. DOI: 10.1038/ng.2814. View

20.

Gamble M, Frizzell K, Yang C, Krishnakumar R, Kraus W . The histone variant macroH2A1 marks repressed autosomal chromatin, but protects a subset of its target genes from silencing. Genes Dev. 2009; 24(1):21-32. PMC: 2802188. DOI: 10.1101/gad.1876110. View