Programmed nuclear death: Apoptotic-like degradation of specific nuclei in conjugating Tetrahymena

Davis, Maria C.; Ward, Jacob; Herrick, Glenn; Allis, C. David

doi:10.1016/0012-1606(92)90080-z

Cited by 111 publications

(90 citation statements)

References 24 publications

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“…However, during the sexual pathway known as conjugation, macronuclei, now known as "old macronuclei," are selectively eliminated by an apoptosis-like process (44). It will be interesting to determine if phosphorylation of H2B also correlates with the pronounced chromatin changes that accompany the elimination of this nucleus.…”

Section: Discussionmentioning

confidence: 99%

Characterization of Tetrahymena Histone H2B Variants and Posttranslational Populations by Electron Capture Dissociation (ECD) Fourier Transform Ion Cyclotron Mass Spectrometry (FT-ICR MS)

Medzihradszky

Zhang

Chalkley

et al. 2004

Molecular & Cellular Proteomics

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This work describes the nature and sequence information content of the electron capture dissociation mass spectra for the intact Tetrahymena histone H2B. Two major variants of this protein were present bearing nominal modifications of both ؉42 and ؉84 Da. This work describes identification of the nature of these two modifications. For example, using gas-phase selection and isolation of the ؉42-Da modified species, from a background of two H2B variants each present in six or more posttranslationally modified isoforms, we were able to determine that this ؉42-Da modification isoform bears trimethylation rather than acetylation. LC-CIDMS analysis was also employed on digested preparations to obtain complementary detail of the nature of site-specific posttranslational modifications. This study establishes that integration of the information from these two datasets provides a comprehensive map of posttranslational occupancy for each particular covalent assemblage selected for structural investigation. Molecular & Cellular Proteomics 3: 872-886, 2004.

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Section: Discussionmentioning

confidence: 99%

Characterization of Tetrahymena Histone H2B Variants and Posttranslational Populations by Electron Capture Dissociation (ECD) Fourier Transform Ion Cyclotron Mass Spectrometry (FT-ICR MS)

Medzihradszky

Zhang

Chalkley

et al. 2004

Molecular & Cellular Proteomics

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“…Ten years ago, it was reported that a machinery similar to that inducing the nuclear features of apoptosis in cells from multicellular organisms (the nuclear chromatin condensation and the DNA fragmentation into multiples of oligonucleosome length fragments) was present and operational in the unicellular ciliated eukaryote Tetrahymena. 156 This nuclear execution machinery and program was reported, however, not to be involved in the induction of cell death, but in the elimination of supernumerary old macronuclei during Tetrahymena conjugation, a situation in which these supernumerary nuclei are destroyed, but the cell survives. This finding led to the proposal that programmed cell death, in multicellular organisms evolved from genetic programs that were originally involved, in single-celled eukaryote organisms, in the elimination of supernumerary macronuclei.…”

Section: On Paradigms`anomalies' And`retrorecognition'mentioning

confidence: 99%

On the origin, evolution, and nature of programmed cell death: a timeline of four billion years

2002

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Programmed cell death is a genetically regulated process of cell suicide that is central to the development, homeostasis and integrity of multicellular organisms. Conversely, the dysregulation of mechanisms controlling cell suicide plays a role in the pathogenesis of a wide range of diseases. While great progress has been achieved in the unveiling of the molecular mechanisms of programmed cell death, a new level of complexity, with important therapeutic implications, has begun to emerge, suggesting (i) that several different selfdestruction pathways may exist and operate in parallel in our cells, and (ii) that molecular effectors of cell suicide may also perform other functions unrelated to cell death induction and crucial to cell survival. In this review, I will argue that this new level of complexity, implying that there may be no such thing as a`bona fide' genetic death program in our cells, might be better understood when considered in an evolutionary context. And a new view of the regulated cell suicide pathways emerges when one attempts to ask the question of when and how they may have become selected during evolution, at the level of ancestral single-celled organisms.

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“…Thus, different mechanisms could be used in Tetrahymena. Also, during conjugation, the parental MAC is destroyed by a process that has been suggested to be related to apoptosis in higher eukaryotes (20,26), and phosphorylation of H2A.X accompanies formation of the DSBs associated with DNA fragmentation during apoptosis in mammals (46,54,68).…”

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confidence: 99%

Phosphorylation of the SQ H2A.X Motif Is Required for Proper Meiosis and Mitosis in Tetrahymena thermophila

Song

Gjoneska

Ren

et al. 2007

Molecular and Cellular Biology

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Phosphorylation of the C terminus SQ motif that defines H2A.X variants is required for efficient DNA double-strand break (DSB) repair in diverse organisms but has not been studied in ciliated protozoa. Tetrahymena H2A.X is one of two similarly expressed major H2As, thereby differing both from mammals, where H2A.X is a quantitatively minor component, and from Saccharomyces cerevisiae where it is the only type of major H2A. Tetrahymena H2A.X is phosphorylated in the SQ motif in both the mitotic micronucleus and the amitotic macronucleus in response to DSBs induced by chemical agents and in the micronucleus during prophase of meiosis, which occurs in the absence of a synaptonemal complex. H2A.X is phosphorylated when programmed DNA rearrangements occur in developing macronuclei, as for immunoglobulin gene rearrangements in mammals, but not during the DNA fragmentation that accompanies breakdown of the parental macronucleus during conjugation, correcting the previous interpretation that this process is apoptosis-like. Using strains containing a mutated (S134A) SQ motif, we demonstrate that phosphorylation of this motif is important for Tetrahymena cells to recover from exogenous DNA damage and is required for normal micronuclear meiosis and mitosis and, to a lesser extent, for normal amitotic macronuclear division; its absence, while not lethal, leads to the accumulation of DSBs in both micro-and macronuclei. These results demonstrate multiple roles of H2A.X phosphorylation in maintaining genomic integrity in different phases of the Tetrahymena life cycle.

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Programmed nuclear death: Apoptotic-like degradation of specific nuclei in conjugating Tetrahymena

Cited by 111 publications

References 24 publications

Characterization of Tetrahymena Histone H2B Variants and Posttranslational Populations by Electron Capture Dissociation (ECD) Fourier Transform Ion Cyclotron Mass Spectrometry (FT-ICR MS)

Characterization of Tetrahymena Histone H2B Variants and Posttranslational Populations by Electron Capture Dissociation (ECD) Fourier Transform Ion Cyclotron Mass Spectrometry (FT-ICR MS)

On the origin, evolution, and nature of programmed cell death: a timeline of four billion years

Phosphorylation of the SQ H2A.X Motif Is Required for Proper Meiosis and Mitosis in Tetrahymena thermophila

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