Tetrahymena thermophila JMJD3 Homolog Regulates H3K27 Methylation and Nuclear Differentiation

Chung, Pei-Han; Yao, Meng-Chao

doi:10.1128/ec.05290-11

Cited by 19 publications

(26 citation statements)

References 81 publications

(98 reference statements)

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“…Acetylation levels of H3 appeared to be essentially unchanged in both ⌬TXR1 and ⌬EZL2 cells. (24,25), Ezl2p is one of the homologues of the Drosophila enhancer of zeste, which is specific for H3K27 methylation. We applied the same strategy used for ⌬TXR1 to ⌬EZL2 for analysis of the global PTM profile changes in histone H3.…”

Section: Resultsmentioning

confidence: 99%

“…1), all of which are consistent with its being a bona fide member of the ATXR5/ATXR6 subfamily of HMTs. In Tetrahymena, there are also three homologues of the canonical H3K27-specific HMT enhancer of zeste, referred to as EZL1, EZL2, and EZL3, respectively (24,25). Only EZL2 is expressed at significant levels (24,25) and required for H3K27 di-and trimethylation in asexually dividing cells (see below).…”

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confidence: 99%

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Quantitative Proteomics Reveals That the Specific Methyltransferases Txr1p and Ezl2p Differentially Affect the Mono-, Di- and Trimethylation States of Histone H3 Lysine 27 (H3K27)

Zhang

Molascon

Gao

et al. 2013

Molecular & Cellular Proteomics

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Nuclear DNA in eukaryotic cells is assembled into the hierarchical chromatin structure via a process that is dynamically affected by the combinatorial set of post-translational modifications (PTMs) of histones in a dynamic manner responsive to physiological and environmental changes. The precise quantification of these complex modifications is challenging. Here we present a robust MS-based quantitative proteomics method for studying histone PTMs using 15 N metabolically labeled histones as the internal reference. Using this approach, we identified Tetrahymena trithorax related 1 (Txr1p) as a histone methyltransferase in Tetrahymena thermophila and characterized the relationships of the Txr1p and Ezl2p methyltransferases to histone H3 modification. We identified 32 PTMs in more than 60 tryptic peptides from histone H3 of the ciliate model organism Tetrahymena thermophila, and we quantified them (average coefficient of variation: 13%). We examined perturbations to histone modification patterns in two knockout strains of SET-domain-containing histone methyltransferases (HMT). Knockout of TXR1 led to progressively decreased mono-, di-, and tri-methylation of H3K27 and apparent reduced monomethylation of H3K36 in vivo. In contrast, EZL2 knockout resulted in dramatic reductions in both di-and tri-methylation of H3K27 in vivo, whereas the levels of monomethylation of H3K27 increased significantly. This buildup of monomethyl H3K27 is consistent with its role as a substrate for Ezl2p. These results were validated via immunoblotting using modification site-specific antibodies. Taken together, our studies define Txr1p as an H3K27 monomethylation-specific HMT that facilitates the buildup of H3K27 di-and trimethylation by the canonical H3K27-specific HMT, Ezl2p. Our studies also delineate some of the interdependences between various H3 modifications, as compensatory increases in monomethylation at H3K4, H3K23, and H3K56 were also observed for both TXR1 and ELZ2

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

Quantitative Proteomics Reveals That the Specific Methyltransferases Txr1p and Ezl2p Differentially Affect the Mono-, Di- and Trimethylation States of Histone H3 Lysine 27 (H3K27)

Zhang

Molascon

Gao

et al. 2013

Molecular & Cellular Proteomics

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“…It is partially responsible for the removal of H3K27me3 in the developing macronucleus. It has only a minor role in DNA deletion since knockdown mutants showed only slight defects in DNA deletion but were unable to complete macronucleus development beyond DNA deletion (60).…”

Section: Histone Modificationsmentioning

confidence: 99%

Programmed Genome Rearrangements in Tetrahymena

2014

Self Cite

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Ciliates are champions in programmed genome rearrangements. They carry out extensive restructuring during differentiation to drastically alter the complexity, relative copy number, and arrangement of sequences in the somatic genome. This chapter focuses on the model ciliate Tetrahymena, perhaps the simplest and best-understood ciliate studied. It summarizes past studies on various genome rearrangement processes and describes in detail the remarkable progress made in the past decade on the understanding of DNA deletion and other processes. The process occurs at thousands of specific sites to remove defined DNA segments that comprise roughly one-third of the genome including all transposons. Interestingly, this DNA rearranging process is a special form of RNA interference. It involves the production of double-stranded RNA and small RNA that guides the formation of heterochromatin. A domesticated piggyBac transposase is believed to cut off the marked chromatin, and the retained sequences are joined together through nonhomologous end-joining processes. Many of the proteins and DNA players involved have been analyzed and are described. This link provides possible explanations for the evolution, mechanism, and functional roles of the process. The article also discusses the interactions between parental and progeny somatic nuclei that affect the selection of sequences for deletion, and how the specific deletion boundaries are determined after heterochromatin marking.

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“…More cryptic species were subsequently discovered and currently the T. pyriformis complex comprises 18 micronucleate and 4 amicronucleate species (Feng et al 1988;Jerome et al 1996;Nanney et al 1980;Nyberg 1981;Simon et al 1985). Species in the T. pyriformis complex, such as Tetrahymena thermophila, are now used as model organisms for research in a wide range of fields including cell biology, epigenetics, and molecular ecology (Been and Cech 1986;Cervantes et al 2015;Cherry and Blackburn 1985;Chung and Yao 2012;Gao et al 2013;Liu et al 2007;Mochizuki et al 2002;Nanney 1953). The former Syngen 11 of the T. pyriformis complex was designated Tetrahymena australis, mainly according to its geographical distribution (Elliott 1970(Elliott , 1973, although it was subsequently found to be globally distributed (Simon et al 1985(Simon et al , 2008.…”

Section: Introductionmentioning

confidence: 99%

Tetrahymena australis (Protozoa, Ciliophora): A Well‐Known But “Non‐Existing” Taxon – Consideration of Its Identification, Definition and Systematic Position

Liu

Fan

Gao

et al. 2016

J Eukaryotic Microbiology

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A cryptic species of the Tetrahymena pyriformis complex, Tetrahymena australis, has been known for a long time but never properly diagnosed based on taxonomic methods. The species name is thus invalid according to the International Code of Zoological Nomenclature. Recently, a population isolated from a freshwater lake in Wuhan, China was investigated using live observations, silver staining methods and gene sequence data. This organism can be separated from other described species of the T. pyriformis complex by its relatively small body size, the number of somatic kineties and differences in sequences of two genes, namely the small subunit ribosomal RNA (SSU rRNA) and the mitochondrial cytochrome c oxidase subunit I (cox1). We compared the SSU rRNA gene sequences of all available Tetrahymena species to reveal the nucleotide differences within this genus. The sequence of the Wuhan population is identical to two sequences of a previously isolated strain of T. australis (ATCC #30831). Phylogenetic analyses indicate that these three sequences (X56167, M98015, KT334373) cluster with Tetrahymena shanghaiensis (EF070256) in a polytomy. However, sequence divergence of the cox1 gene between the Wuhan population and another strain of T. australis (ATCC #30271) is 1.4%, suggesting that these may represent different subspecies.A wide variety of protists, including hymenostome ciliates, have relatively simple body structures with few morphological characters for species circumscription, which makes them difficult to separate from each other (Borden et al. 1977;Simon et al. 2008). Early taxonomists identified and classified such organisms based only on morphological and cell cycle characters. As a consequence, independent species were sometimes misidentified as morphologically similar species within a morphospecies complex (for instance, Paramecium aurelia). The development of modern methods, especially gene sequencing and phylogenetic analyses, has improved this situation and the taxonomic positions of several such species have been clarified in recent years (Quintela-Alonso et al. 2013;Zhao et al. 2016).Cryptic species of ciliates were first discovered by Sonneborn (1939) for the model organism P. aurelia Ehrenberg, 1838. Cryptic species have since been found in a variety of ciliate genera including Aspidisca, Colpidium, Euplotes, Glaucoma, Oxytricha, Paramecium, Pseudourostyla, Stylonychia, Tetrahymena, Tokophrya, and Uronychia (Dini and Nyberg 1993;Przybos 1986;Simon et al. 2008). The probable wide occurrence of cryptic speciation has been cited as evidence for the underestimation of ciliate species diversity (Foissner et al. 2007).Tetrahymena pyriformis (Ehrenberg, 1830) Lwoff, 1947 is another example now known to be a species complex (Nanney and McCoy 1976). Species of Tetrahymena were previously assigned to the genera Leucophyrs or Glaucoma until the establishment of the genus Tetrahymena by Furgason (1940). Using mating type tests, Gruchy (1955) first discovered the heterogeneity of T. pyriformis by describin...

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Tetrahymena thermophila JMJD3 Homolog Regulates H3K27 Methylation and Nuclear Differentiation

Cited by 19 publications

References 81 publications

Quantitative Proteomics Reveals That the Specific Methyltransferases Txr1p and Ezl2p Differentially Affect the Mono-, Di- and Trimethylation States of Histone H3 Lysine 27 (H3K27)

Quantitative Proteomics Reveals That the Specific Methyltransferases Txr1p and Ezl2p Differentially Affect the Mono-, Di- and Trimethylation States of Histone H3 Lysine 27 (H3K27)

Programmed Genome Rearrangements in Tetrahymena

Tetrahymena australis (Protozoa, Ciliophora): A Well‐Known But “Non‐Existing” Taxon – Consideration of Its Identification, Definition and Systematic Position

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