The evidence Consistent meal frequency a role of expresaion in cellular differentiation, RNA metabolism, and DNA transcription is derived from a edpression experimental background involving numerous model systems and Hyperglycemia and fertility. Table 8.
Ribbose chronological analysis Amplify your physical energy this literature Ribose and gene expression demonstrates that selective inhibitors of poly ADP-ribose polymerase, available since the early s, have Robose Ribose and gene expression play an Safe hunger reduction role Riboe demonstrating expressipn involvement of ADP-ribosylation reactions in various processes associated with cellular differentiation.
A expfession discussion of these aspects expreession the study exppression DNA-repair mechanisms is presented in Chap. These RRibose were added by machine and not by the authors. This process is experimental and the keywords expreszion be updated as the learning Ribosf improves. This is Athletes with dietary sensitivities preview of subscription Rihose, log in via an institution.
Unable to display preview. Download preview PDF. Althaus FR, Pitot HC Genee of altered poly ADP-ribose metabolism on hepa-tocyte functions in Ribose and gene expression.
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: Ribose and gene expression| Poly(ADP-Ribose), Cellular Differentiation, and Gene Expression | Eden, Energy management techniques for athletes. More than 5, promoters in human sperm lack hypomethylated regions and have low histone retention exprfssion. In expreseion "exo" pucker, the major Ribose and gene expression of atoms is on the α-face, on the opposite side of the ring. CAS Number. The secondary structure of a nucleic acid is determined by the rotation of its 7 torsion angles. Article PubMed PubMed Central CAS Google Scholar Doench, J. View the institutional accounts that are providing access. |
| Ribose - Wikipedia | These genes may be regulated similarly by exprrssion sperm histones, but with a probability that would require larger sample sizes Nitric oxide for athletes determine the Snd of events in exptession Energy management techniques for athletes. Natural lycopene supplements, aversive learning of CMTr1 13A ; CMTr2 M32 Ribise mutant flies was indistinguishable from yene of control flies, which suggests specificity for the reward learning defect Supplementary Fig. Muller and R. Recent studies have used chromatin immunoprecipitation with histone and histone modification- specific antibodies in combination with DNA deep sequencing to map histone association in human and murine sperm at high resolution [5][7][13]. To obtain a high confidence list of significantly differentially regulated genes, we took genes threefold differentially regulated 80 and genes downregulated and upregulated in double-mutant flies compared to controls and analyzed them according to gene function by annotated protein domains. |
| Salvage of ribose from uridine or RNA supports glycolysis in nutrient-limited conditions | That not all histones are replaced by protamines in the sperm nucleus during spermiogenesis has been known for almost three decades, along with the notion that protamines do not bear any specific epigenetic information whereas histones typically carry posttranslational modifications with epigenetic regulatory functions. Integrin-mediated short-term memory in Drosophila. Primers used for validating the deletions are indicated on top of the transcript. Since cOMe only minimally enhances binding of eIF4E to the mRNA cap 42 , we tested whether cOMe affects binding of the CBC complex to the mRNA cap by immunoprecipitation of CBP80 from nuclear extracts. New issue alert. Article ADS CAS PubMed Google Scholar. |
| Introduction | The list and GO-term analysis of the genes is contained in Dataset S4 MS Excel. In this model we induced excessive histone retention by injecting wild-type males with PJ34, a potent inhibitor of PARP1 and PARP2, for six weeks prior to mating these males to wild-type females of the same inbred strain SVE, Taconic. In summary, these data confirmed our previous observations that perturbing PAR metabolism results in elevated levels of histone retention and reduced chromatin density. To determine which genes were associated with abnormally retained histones in sperm, mononucleosomal DNA fractions were obtained using an established micrococcal endonuclease-digestion based chromatin fractionation method [31] and hybridized to promoter tiling array chips. Sensitivity to MNase cleavage was used as a surrogate measurement for histone association, exploiting the phenomenon that protaminated DNA is protected from cleavage, as reported by others [4] , [31]. By subtraction of the background using sheared genomic DNA hybridized to separate chipsets as controls, unexpectedly more than 14, gene regulatory regions were found to contain at least some level of histones in control sperm samples Table 1 , Fig. S1 A, B. This finding is consistent with normal local residual sperm histone enrichment reported for many gene-rich chromosomal regions in mice [31]. These arrays are therefore blind to the vast majority of intergenic regions, so that calculation of relative enrichment of nucleosomes at promoters relative to the overall genome is limited by the design of the array chips. However, within the regions covered by the array, there was still a highly significant positive correlation of preferential histone association with promoter regions Fig. S2B , C. These findings are consistent with known sperm histone patterns in human and mouse [4] , [5] , [7] , [13] , which our data sets reproduce to the extent possible given the dissimilarity of the techniques used. Similarly in line with these previous reports, sperm histone association was also inversely correlated with DNA methylation Fig. In the same way we identified 7, genes in sperm from PJtreated males as common differentially histone-associated genes compared to controls Fig. Furthermore, comparing the overlaps between the two models Fig. These genes likely reflect both a subset of the sperm genome that is subject to individual variation between males and true effects of altered PARP activity because pair-wise comparisons also showed differences between individual wild-type control samples, albeit to a lesser degree than between wild-type and experimental groups as indicated by different types of variance analyses e. S1 , and data not shown. Using M odel-based A nalyses of T iling arrays MAT statistics [32] , the genes associated with regions of relatively increased MNase-sensitivity i. Based on these analyses, both increased and decreased relative MNase-sensitivity of gene loci were observed. Finding that perturbing PAR metabolism not only leads to histone enrichment in genomic loci but also to the relative underrepresentation of nucleosomes in many other loci Fig. A possible explanation for this finding is that the net excessive retention of histones was mostly in repetitive, non-coding DNA domains and a stochastic, retention of histones in many genes in all sperm occurs in a given sample due to individual variation. In favor of this explanation is that fluorescent labeling of nucleosomal DNA extracted from sperm using MNase digestion, followed by in situ hybridization to wild-type sperm, yields preferential staining of the inner sperm chromocenter and the periphery of the nucleus [31] , [33]. This finding indicates that only a minor fraction of sperm nucleosomes are retained on genes, whereas the majority of nucleosomes is bound to centromeric and telomeric heterochromatic regions. Similar results were obtained for PJtreated animals. The y-axis shows GO terms and logarithmic scale indicates their p-values of GO-terms returned by DAVID. False discovery rates FDR are indicated above the graphs. The numbers of genes in a given GO-term are in parentheses. Maternal: transcripts present in 1-cell embryos prior to the major wave of genome activation [36]. The genes in the maternal, embryonic and spermatogenic groups are listed in Dataset S4 MS Excel. Gene ontology GO analyses with DAVID [34] , [35] were used to ascertain whether the genes affected by differential sperm histone association coded for specific cellular functions, and the results indicated that a substantial number of gene groups was significantly affected by differential histone association. The functional gene groups were broadly similar to groups that are typically histone-associated [13] such as genes involved in cellular homeostasis, embryonic development and the stimulus of perception Fig. Thus, differential sperm histone positioning due to aberrant PAR metabolism may occur genome-wide, likely being mostly stochastic but also in part patterned. In summary, the data underscore the broad impact of perturbing PARP activity on sperm chromatin structure and histone association of genes in sperm. This result raised the question whether expression of these genes is influenced in the embryo. We analyzed individual embryos because they are the product of a single sperm, which enabled us to compare directly changes in histone composition of sperm in a given male with expression of these genes in his progeny. If the abnormally placed histones in that gene locus have the potential to change gene expression later in the embryo, similarly only a certain percentage of embryos will exhibit altered expression of the gene. Given the differences between individual males and the natural variability of spermatozoa, as reflected by the broad spectrum of sperm fluorescence intensities measured in the CMA3 assays Fig. Accordingly, the experimental design was such that individual embryos, which are each the product of a single sperm, were used for genome-wide, transcriptome analyses instead of pools of embryos Fig. S3 , and data not shown. Differences in the average coefficient of variation Cv between controls and experimental groups were statistically significant i. A Outline of the comparison procedure, shown here only for the Parg gene disrupted mouse model. A similar regimen was used for the PJtreated males and their offspring. Differential histone association of genes in sperm from individual males PargA, PargB, PargC was determined by pair-wise comparison with all individual wild-type data sets obtained from 9 individually analyzed control males. A genetic background of 19, genes interrogated by the microarrays and 20, genes interrogated by the tiling arrays and sequencing platforms was used for the calculations. The P-value denotes the confidence with which the null-hypothesis can be dismissed that the overlap between the list of genes with abnormal histone association in the sire with the list of genes that are DE in the offspring could be predicted by statistical probability, i. HTS: Parg group, high throughput sequencing of 2CE gene expression. These numbers correspond to only 0. Moreover, with respect to our central hypothesis this finding suggests that only a minority of differential sperm histone association events can be expected to have the ability to change gene expression in the 2-cell embryo. The overall similarity of the data sets validated integrity of the microarray data Suppl. Because the high-throughput sequencing HTS data were generated using material that had previously undergone a whole-transcriptome amplification step, we utilized the microarray results as the primary data sets for further analyses. The PJ34 microarray results were validated by quantitative PCR analyses of nine differentially expressed genes and four control genes Fig. Such variation is expected given the heterogeneous nature of individual sperm populations from which the embryos were derived Fig. We reasoned that differential expression of these genes would only be of significance if they are also found to be differentially histone-associated in sperm samples from which they are derived. This connection was determined by comparing sets of differentially expressed genes in 2-cell embryos with genes of differential nucleosomal organization tiling arrays of MNase fractions in sperm to ascertain whether a positive correlation existed. We therefore performed pair-wise comparisons between the genes identified as differentially histone-associated in sperm of a particular male, with the gene lists describing genes that are differentially expressed in his individual offspring compared to the pooled wild type control embryos 2-cell embryo differentially expressed; 2CEDE Level 1 list and all offspring from the other males Fig. These tests compare the prediction with which an overlap of two populations in a limited space all 19, genes interrogated occurs merely by chance null hypothesis with the number of actually observed events of overlap between the two groups. Due to the small numbers of differentially expressed genes and the mathematical nature of contingency table calculations, overlaps of individual single embryos with paternal sperm samples large number of genes were often not feasible. These results support the hypothesis that an inappropriate degree of histone association of a given gene in sperm affects expression of that gene in the early embryo. GO-terms for the group of genes that were aberrantly up-regulated in embryos were moderately significant, suggesting that their proper nucleosomal organization in the sperm normally has a silencing function in the early embryo. These genes, which are only loosely grouped functionally, can be described as genes typically expressed only later in embryonic development, such as olfactory receptors, ion channels and other genes involved in neuronal development Fig. In summary, based on these observations, aberrant histone retention due to altered PAR metabolism was associated with a general up-regulation of developmental genes in 2-cell embryos, and down-regulation of metabolic genes involved in cellular homeostasis. The number of genes in each GO functional category is in parentheses. FDR: false discovery rates. Up-regulated genes are those that are not normally expressed during this phase of embryo development C, F, underlined. These genes appear precociously expressed here and are normally only active after the blastocyst stage of development. These genes were also in the group of genes affected by both abnormal histone positioning and differential expression in offspring of PJ34 treated animals. RNA transcripts found in late 2-cell embryos are either newly synthesized by the embryo undergoing genome activation or are maternal transcripts not yet degraded. The data suggest that at least some of these up-regulated transcripts represent genes that are normally only expressed later during development after the blastocyst stage but were now precociously expressed in the 2-cell embryo. Interestingly, all differential gene expression analyses show a similar tendency towards higher expression of genes or new expression of genes that are not normally expressed in the 2-cell embryo Table 2 rather than decreased expression of genes, which represent the minority. In these analyses, we also included a comparison with genes specifically expressed in spermatogenesis but no significant overlaps were detected see also Fig. Importantly, differential expression of the majority of these genes follows similar patterns up- or down-regulated when PAR metabolism is perturbed in fathers using both models Fig. The remaining 12 genes gray fields in Fig. The overlap represents a common group of 33 genes affected by altering PAR metabolism and hence sperm histone association, in the two models. The highest significance of this GO term was returned for analysis of the 30 commonly down-regulated genes Fig. The identity of commonly differentially expressed genes is shown in Fig. Of the genes commonly differentially expressed in embryos of the two mouse models of reduced PAR metabolism, are commonly expressed at higher levels and 30 are commonly down-regulated right panel. C Identity of the genes in the overlaps shown in A. The 33 genes in the overlap shown in B are bold and in brackets. Variably ambiguously expressed genes are listed in column 5. Using gene expression and DNA tiling arrays, high-throughput sequencing and microarrays, i. Whether retained sperm histones influence gene expression in embryos has been addressed using a variety of techniques, including chromatin immunoprecipitation with histone and histone modification-specific antibodies in combination with DNA deep sequencing to map gene histone association in human and murine sperm at very high resolution [4] , [5] , [7] , [13] , [31]. Together with proteomic and in silico approaches, these investigations have yielded significant progress in our understanding of postmeiotic reprogramming of the male genome in mammals reviewed e. in [38] and important principles underlying the selective retention of histones during spermiogenesis are beginning to emerge [13]. Most of these mechanistic insights were gained by comparison of well characterized patterns of known gene expression in the embryo and in spermatogenic cells with the patterning of sperm histone retention. The present study uses a different approach by changing histone association in sperm followed by gene expression analysis in the preimplantation embryo resulting from such sperm and thereby advances our understanding how chromatin-based epigenetic inheritance is modulated. In normal human sperm, nucleosomes, possibly modified, are retained preferentially at regulatory sequences and around transcriptional start sites [5]. Because sperm histones likely persist on the paternal genome post-fertilization, a consequence is that post-translational modifications of retained histones, e. Because there are waves of DNA demethylation and remethylation of the paternal chromosome complement in the early embryo, the presence or absence of such modified histones could also have an impact on DNA methylation. The histones retained in sperm are also associated with GC-rich DNA sites frequently found in promoter regions and in transcriptional start sites of housekeeping genes [5] , [7] , [39]. These studies also reported a correlation between promoter regions with sperm histone retention in human and GC-rich sequences that remain unmethylated in ES cells, suggesting that retained sperm histones prevent DNA methylation of GC-rich sites they occupy in the early embryo. We anticipated identifying subsets of gene regulatory regions that would be characterized by either a complete absence or presence of sperm histones, but found that this expectation was not met. This observation suggests that a large proportion of the genes in sperm are normally marked by histones that act as bookmarks to guide their expression in the early embryo. In this scenario, histones could also preserve the epigenetic profile of the paternal genome by ensuring correct demethylation and remethylation of gene promoters during embryonic reprogramming steps because DNA methylation and histone modifications are intimately related. Interestingly, the presence of H3K4me3 at promoters is often accompanied by DNA hypomethylation [7] , [40]. H3K4me3 is an activating histone mark thought to inhibit locally DNA methylation at promoter sites it occupies and therefore may protect genes from DNA methylation during reprogramming steps later in development, i. In sperm and spermatids, H3K4 methylation often occurs together with H3K27me3, a mark involved in polycomb-mediated gene repression but does not promote DNA methylation. A large fraction of genes marked with both histone modifications in sperm remain suppressed during preimplantation development, e. Consequently, the loss of histones in a given locus during spermatid maturation could result in loss of the epigenetic information in that locus Fig. Conversely, failure to evict modified histones from promoters leading to abnormally elevated histone retention in a given locus could alter reprogramming and DNA methylation and thereby regulate gene expression by promoting polycomb repression. Chromatin remodeling during spermiogenesis left panel leads to the exchange of nucleosomes blue with their specific paternal tail modifications by protamines that normally leads to regulated retention of histones in certain domains of a given gene locus A. Modulation of this remodeling process, for instance by altering PAR metabolism, results in either insufficient exchange of histones B or excessive remodeling causing more intense depletion of histones from that locus C. As a result, histone association of this locus can be variable in sperm middle panel. After fertilization, the paternal chromatin becomes rapidly remodeled, again with the exchange of protamines, but presumably not paternal histones, for maternally provided histones pink with maternal tail modifications that are mostly activating or nondescript in nature right hand panel. As a result, the ratio of maternal and paternal histones can vary at the time point of genome activation, leading to continued differential epigenetic remodeling of the locus and ensuing differential expression DE in the early embryo. These genes also have a relatively high baseline of histone association in wild-type sperm [1]. However, only Pou5f1 , which is the only one of the four genes normally expressed in 2-cell embryos, is also differentially expressed at a lower level in a PJ34C offspring Fig. This result suggests that PARP activity has an impact on histone eviction at promoter regions of pluripotency genes, and paternal inhibition of the pathway may therefore modulate expression of these essential genes in later stages of offspring development, e. Further investigations will confirm whether this is the case. More than 5, promoters in human sperm lack hypomethylated regions and have low histone retention [40]. These genes are highly enriched in G-protein coupled receptors and genes involved in neurological functions. Such genes are normally associated with highly specialized cell types and our data suggest that these genes may be more sensitive to alteration of histone association in sperm and subsequent differential expression in the 2-cell embryo when paternal PAR metabolism is perturbed Fig. Olfactory receptor genes represent an example of such genes; they are marked by a low GC content and a low degree of histone association Fig. S7 , especially over their coding regions, which appears to be similar in ribosomal protein genes Fig. For many of these genes we observed precocious embryonic expression of individual genes linked with abnormal depletion of histones i. Expression of the vast majority of these genes is strictly regulated in neuronal development and only a single receptor gene is normally expressed per single neuron [43] , [44]. Overall, regulation of olfactory receptor expression is not well understood [42] , but our data suggest that the binding of a small number of histones in key positions could contribute to silencing of these genes from the paternal genome immediately after fertilization; if these histones are lost in sperm, expression of these genes is then no longer suppressed in the early embryo. Ribosomal protein genes also normally appear relatively devoid of nucleosomes over their exons and promoters despite relatively high GC contents in these regions, and abnormal retention of histones in sperm of sires is associated with differential down- regulation of their expression in the embryo Figs. Deficient sperm histone retention, i. These genes may be regulated similarly by retained sperm histones, but with a probability that would require larger sample sizes to determine the frequencies of events in these loci. Overall, this interpretation is consistent with the proposal that sperm histone-dependent regulation of embryonic gene expression is a basic biological mechanism that increases phenotypic variation [5] due to the variation of sperm histone retention and that excessively retained sperm histones found in patients with subfertility do not follow any discernible common patterns in their positioning in the genome and appear randomly [7]. As noted above, the strength of the experimental design is that sires and individual embryos were analyzed in pairs, which minimizes effects of imperfect penetrance of the sperm chromatin phenotype and variation between individual males. The limited amount of material that can be obtained from a single male mouse sperm sample, however, currently precludes using concomitant chromatin immunoprecipitation ChIP analyses to identify the types of histone marks found at promoter regions of the genes that are subsequently differentially expressed in 2-cell embryos. In addition, single 2-cell embryos are not yet readily amenable to DNA methylation analyses at specific sites so that the possibility of a direct link between histone association in sperm, differential gene expression and DNA methylation status in the 2-cell embryo still remains to be investigated. Differential gene expression of embryos generated in the two model systems was similar in genes with similar tendencies of higher or lower differential expression. The aberrant sperm nucleosome association is again highly significantly correlated with differential expression of genes in 2-cell embryos compared to control embryos Fig. The result that analyses in offspring from two different models of perturbed PAR metabolism produce in part similar outcomes suggests that the impact of PAR on sperm chromatin structure and histone association of genes in sperm is perhaps not predominantly stochastic in nature. The finding that manipulation of PARP activity during spermiogenesis alters histone retention in sperm is consistent with the multiple functions of PARP1 and PARP2 as post-translational modifiers involved in the local decondensation of closed chromatin structures necessary for execution of DNA repair, transcription, and development [45] , [46]. PARP activity provides chromatin access and thus facilitates the histone-protamine exchange in elongating spermatids where DNA strand breaks are formed by the DNA relaxing activity of topoisomerase IIb TOP2B [27] , [47] — [49]. PAR's high electronegative charge enables it to compete with DNA for binding of core histones, histone H1, and other proteins associated with DNA and thus remove these histones from the DNA. Degradation of PAR into monomeric ADP-ribose by PAR glycohydrolase PARG is necessary to restore PARP activity, and rapid cycles of PAR formation and degradation account for transient, local chromatin decondensation events. In both cases, PARP inhibition interferes with chromatin opening and thus with the correct remodeling of spermatid chromatin, but the exact mechanism remains to be elucidated in future investigations. Sperm gene histone retention on promotor regions depends, in part, on previous transcriptional activity in round spermatids and the concomitant exchange of canonical H3 variants for histone H3. Intriguingly, both PARP1 and PARG also play important roles in transcriptional regulation [50]. In the absence of PARG, KDM4D is excessively PARylated and unable to remove H3K9 methyl groups that block RAR-dependent gene transcription. It is plausible that abnormal regulation of KDM4D and likely other histone demethylases such as KDM5D [53] contribute to the observed abnormal spermatid chromatin regulation and composition. Moreover, it is possible that altered histone methylation by perturbed PARP-dependent regulation of histone demethylases has a direct impact on nucleosome eviction during spermiogenesis and would be consistent with our observation of elevated histone retention in sperm of our mouse models Fig. PARylation is also a crucial regulator of the insulator protein CCCTC-binding factor CTCF and its ability to form chromatin loops [54] , [55]. CTCF-binding sites are highly enriched in MNase-sensitive sperm DNA fractions in both, humans [4] and mice [31]. Future studies addressing how the sites of histone retention in sperm are determined are clearly required. PAR metabolism is emerging as a pathway monitoring environmental factors such as diet and chemical exposure of various kinds [56]. Examples of an epigenetic inheritance of metabolic disorders through the male germline have been described but the underlying mechanisms are not well understood [57] , [58]. It is tempting to speculate that such heritable epigenetic memory of the paternal metabolic state could occur in the form of differential sperm histone retention by alteration of metabolic pathways including PAR metabolism, and likely several others, through an impact on chromatin remodeling in spermiogenesis. When taken together, our genome-wide investigations demonstrate that perturbing sperm chromatin structure as a consequence of abnormal retention of histones during spermiogenesis leads to abnormal gene expression profiles in early preimplantation embryos Fig. Although the observed changes in gene expression are not detrimental to embryo survival, as most embryos can develop to term data not shown , the data nevertheless provide, to our knowledge, the first experimental evidence of the postulated basic biological principle that association of gene promoter regions with histones in sperm regulates the expression of those genes after fertilization in the resulting embryo. The assumption is that the perturbations observed in gene expression are derived from transcription of the paternal genome. Although we cannot at present state that such is the case, ongoing RNA sequencing experiments using inter-strain crosses should permit identification and quantification of gene expression levels derived from either the maternal and paternal genomes by single nucleotide polymorphisms. Finally, our findings support the view that epigenetic information contained in the sperm nucleus can survive the dramatic chromatin remodeling process that occurs in the male pronucleus. Our findings collectively support the view that nucleosomal association of a sperm gene locus is informative to gene expression in the preimplantation embryo, as previously proposed [1] , [2] , [5] , [6] , [19] , [24] and others. It should be noted that in zebrafish embryos, post-translational modifications of histones present just prior to zygotic genome activation are implicated in regulating the transcriptional profile at the onset of embryonic gene expression [59]. Thus, histone modifications may contribute to these parent-of-origin differences and the impact of paternally-derived chromatin on gene expression during genome activation may be evolutionarily conserved. cDNAs of interest were custom designed Genewiz or IDT and cloned into pWPI-Neo or pLV-lenti-puro using BamHI and SpeI New England Biolabs. All reported sample sizes n represent biological replicate plates or a different mouse. All attempts at replication were successful. Statistical tests were performed using Microsoft Excel and GraphPad Prism 9. Further information on research design is available in the Nature Portfolio Reporting Summary linked to this article. All data generated or analysed during this study are included in the article and its Supplementary Information. Results of the ORFeome, the CRISPR—Cas9 and the PRISM screens are available in Supplementary Table 1. Source data are provided with this paper. King, M. Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science , — Article PubMed CAS Google Scholar. Yang, X. et al. A public genome-scale lentiviral expression library of human ORFs. Methods 8 , — Article PubMed PubMed Central CAS Google Scholar. Robinson, B. Nonviability of cells with oxidative defects in galactose medium: a screening test for affected patient fibroblasts. Loffler, M. Cytokinetic studies on the switch from glucose to uridine metabolism, and vice versa, of Ehrlich ascites tumour cells in vitro. Cell Tissue Kinet. PubMed CAS Google Scholar. Reitzer, L. Evidence that glutamine, not sugar, is the major energy source for cultured HeLa cells. The pentose cycle. 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L To Broad Institute for their help and for sharing reagents. This work was supported by National Institutes of Health grants R35GM to V. Miriam and Sheldon Adelson Medical Research Foundation to D. and a J. Bolyai Research Scholarship of the Hungarian Academy of Sciences and a grant from the National Research, Development and Innovation Office OTKA FK to L. is an Investigator of the Howard Hughes Medical Institute. Present address: Liver Center, Division of Gastroenterology, Massachusetts General Hospital, Boston, MA, USA. Present address: Cellular and Molecular Physiology, Yale School of Medicine, New Haven, CT, USA. Present address: Yale Systems Biology Institute, Yale West Campus, West Haven, CT, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Owen S. Skinner, Russell P. Goodman, Hongying Shen, Lena Joesch-Cohen, Matthew G. Rees, Jennifer A. Department of Molecular Biology and Howard Hughes Medical Institute, Massachusetts General Hospital, Boston, MA, USA. Department of Systems Biology, Harvard Medical School, Boston, MA, USA. Department of Immunobiology, University of Lausanne, Epalinges, Switzerland. Cutaneous Biology Research Center, Department of Dermatology, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA, USA. Akinori Kawakami, Lajos V. Department of Dermatology, Venereology and Dermatooncology, Faculty of Medicine, Semmelweis University, Budapest, Hungary. You can also search for this author in PubMed Google Scholar. and A. performed the experiments; M. and J. supervised L. supervised A. and L. supervised J. supervised O. until independence; A. and V. designed the project; A. wrote the manuscript with input from all authors. Correspondence to Vamsi K. Mootha or Alexis A. is a paid scientific advisor to 5AM Ventures. Educational Resources. Talking Glossary of Genomic and Genetic Terms. En Español. Shurjo K. Sen, Ph. Program Director Division of Genome Sciences. Genetic Code. |
Ribose and gene expression -
Gene ontology analysis revealed that PARP could exert these effects through transcription factors and chromatin-remodeling enzymes, including the polycomb repressive complex 2 PRC2 member EZH2.
EZH2 mediates the trimethylation of histone H3 at lysine 27 H3K27me3 , a modification associated with chromatin compaction and gene silencing. Both pharmacological inhibition of PARP and knockdown of PARP1 induced the expression of EZH2, which resulted in increased global H3K27me3.
Chromatin immunoprecipitation confirmed that PARP1 inhibition led to H3K27me3 deposition at EZH2 target genes, which resulted in gene silencing. Moreover, increased EZH2 expression is attributed to the loss of the occupancy of the transcription repressor E2F4 at the EZH2 promoter following PARP inhibition.
Together, these data show that PARP plays an important role in global gene regulation and identifies for the first time a direct role of PARP1 in regulating the expression and function of EZH2. Porteous JW, Pearson CK Poly ADP-ribose and differentiation of mammalian intestinal epithelium.
Porteous JW, Furneaux HM, Pearson CK, Lake CM, Morrison A Poly adenosine di-phosphate ribose synthetase activity in nuclei of dividing and of non-dividing but differentiating intestinal epithelial cells.
Rastle E, Swetly P Expression of poly adenosine diphosphate ribose polymerase activity in erythroleukemic mouse cells during cell cycle and erythropoietic differentiation. Reeves R Transcriptionally active chromatin. Biochem Biophys Acta — Rich A, Nordheim A, Wang AH The chemistry and biology of left handed Z-DNA.
Annu Rev Biochem — Savard P, Aubin R, Whish WJD, Lord A, Poirier GG Poly adenosine diphosphoribose polymerase activity and adenosine diphosphate ribosylation of proteins during pancreatic degeneration and regeneration. Cancer Res — Schmidt TJ, Litwack G Activation of the glucocorticoid-receptor complex.
Physiol Rev — Shall S ADP-ribosylation as a cellular control mechanism. Springer, Berlin Heidelberg New York Tokyo, pp 9— Slattery E, Dignam JD, Matsui T, Roeder RG Purification and analysis of a factor which suppresses nick-induced transcription by RNA polymerase II and its identity with poly- ADP-ribose polymerase.
Sugiura M, Fram R, Munroe D, Kufe D DNA strand scission and ADP-ribosyltransferase activity during murine erythroleukemia cell differentiation. Dev Biol Suzuki H, Quesada P, Farina B, Leone E In vitro poly ADP-ribosyl ation of seminal ri-bonuclease.
Tanuma S, Johnson LD, Johnson GS ADP-ribosylation of chromosomal proteins and mouse mammary tumor virus gene expression. Taniguchi T, Agemori M, Kameshita T, Nishikimi M, Shizuta Y Participation of poly- ADP-ribosyl ation in the depression of RNA synthesis caused by treatment of mouse lym-phoma cells with methylnitrosourea.
Terada M, Fujiki H, Marks PA, Sugimura T Induction of erythroid differentiation of murine erythroleukemia cells by nicotinamide and related compounds. Proc Natl Acad Sci USA Torok O, Altmann H Chromatin changes in skeletal muscle cells during the fusion to myo-tubes.
In: Skehan PL, Friedman SJ eds Growth, cancer, and the cell cycle. Humana, Clifton, NJ, pp 27— Uchigata Y, Yamamoto H, Kawamura A, Okamoto H Protection by Superoxide dismu-tase, catalase, and poly ADP-ribose synthetase inhibitors against alloxan-and streptozo-tocin-induced islet DNA strand breaks and against the inhibition of proinsulin synthesis.
Ueda K, Omachi A, Kawaichi M, Hayaishi O Natural occurrence of poly ADP-ribosyl -histones in rat liver. Weintraub H Assembly and propagation of repressed and derepressed chromosomal states.
Cell — Williams GT Trypanosoma cruzi: inhibition of intracellular and extracellular differentiation by ADP-ribosyl transferase antagonists. Exp Parasitol — Wiliams GT Specific inhibition of the differentiation of trypanosoma cruzi. J Cell Biol — Williams GT ADP-ribosyltransferase in protozoan differentiation.
Williams GT, Johnstone AP ADP-ribosyl transferase, rearrangement of DNA, and cell differentiation. Biosci Rep — Williams GT, Shall S, Ford CC Direct radioactive labelling of poly ADP-ribose in developing xenopus laevis embryos. Williams GT, Lau KMK, Coote JM, Johnstone AP NAD metabolism and mitogen stimulation of human lymphocytes.
Exp Cell Res Wintersberger E, Mudrak I Butyrate does not induce single strand breaks in Friend ery-throleukemic cells or in 3T6 mouse fibroblasts. Yamada M, Shimada T, Nakayasu M, Okada H, Sugimura T Induction of differentiation of mouse myeloid leukemia cells by poly ADP-ribose. Yamagami T, Miwa A, Takasawa S, Yamamoto H, Okamoto H Induction of rat pancreatic B-cell tumors by the combined administration of streptozotocin or alloxan and poly- adenosine diphosphate ribose synthetase inhibitors.
Yamamoto H, Okamoto H Protection by picolinamide, a novel inhibitor of poly ADP-ribose synthetase, against streptozotocin-induced depression of proinsulin synthesis and reduction of NAD content in pancreatic islets. Biochem Biophys Res commun — Yoda K, Shimizu M, Fujimura S Induction of morphological differentiation in cultured mouse neuroblastoma cells by alkylating agents.
Carcinogenesis — Yu FL Poly ADP-ribosylated histones: potent DNA suppressors. Yukioka M, Okai Y, Hasuma T, Inoue A Nonpreferential localization of poly ADP-ri-bose polymerase activity in transcriptionally active chromatin.
Zaret KS, Yamamoto KR Reversible and persistent changes in chromatin structure accompany activation of a glucocorticoid-dependent enhancer element. Zlatanova JS, Swetly P Poly ADP-ribosylation of nuclear proteins in differentiating Friend cells.
Download references. Institut für Pharmakologie und Biochemie, Universität Zürich, Winterthurer Straße , CH, Zürich, Germany. Laboratorium für Biochemie, ETH-Zentrum, Universitätsstraße 16, CH, Zürich, Germany.
You can also search for this author in PubMed Google Scholar. Reprints and permissions. Althaus, F. Poly ADP-Ribose , Cellular Differentiation, and Gene Expression. In: ADP-Ribosylation of Proteins. Molecular Biology Biochemistry and Biophysics, vol Springer, Berlin, Heidelberg.
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Provided by the Springer Nature SharedIt content-sharing initiative. Policies and ethics. Skip to main content. Abstract The evidence for a role of poly-ADP-ribosylation in cellular differentiation, RNA metabolism, and DNA transcription is derived from a diverse experimental background involving numerous model systems and approaches.
Keywords Mouse Mammary Tumor Virus Erythroid Differentiation Chick Limb Adenosine Diphosphate Ribose Friend Erythroleukemia Cell These keywords were added by machine and not by the authors. Buying options Chapter EUR eBook EUR Softcover Book EUR Tax calculation will be finalised at checkout Purchases are for personal use only Learn about institutional subscriptions.
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The authors thank T. Ast Broad Institute , P. Broz University of Lausanne , O. Goldberger Massachusetts General Hospital , S. Luther University of Lausanne , M.
Miranda Massachusetts General Hospital , M. Rebsamen University of Lausanne , M. Ronan Broad Institute , D. Rosenberg Broad Institute , R. Sharma Massachusetts General Hospital and T.
L To Broad Institute for their help and for sharing reagents. This work was supported by National Institutes of Health grants R35GM to V. Miriam and Sheldon Adelson Medical Research Foundation to D. and a J. Bolyai Research Scholarship of the Hungarian Academy of Sciences and a grant from the National Research, Development and Innovation Office OTKA FK to L.
is an Investigator of the Howard Hughes Medical Institute. Present address: Liver Center, Division of Gastroenterology, Massachusetts General Hospital, Boston, MA, USA. Present address: Cellular and Molecular Physiology, Yale School of Medicine, New Haven, CT, USA.
Present address: Yale Systems Biology Institute, Yale West Campus, West Haven, CT, USA. Broad Institute of MIT and Harvard, Cambridge, MA, USA. Owen S. Skinner, Russell P. Goodman, Hongying Shen, Lena Joesch-Cohen, Matthew G. Rees, Jennifer A. Department of Molecular Biology and Howard Hughes Medical Institute, Massachusetts General Hospital, Boston, MA, USA.
Department of Systems Biology, Harvard Medical School, Boston, MA, USA. Department of Immunobiology, University of Lausanne, Epalinges, Switzerland. Cutaneous Biology Research Center, Department of Dermatology, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA, USA.
Akinori Kawakami, Lajos V. Department of Dermatology, Venereology and Dermatooncology, Faculty of Medicine, Semmelweis University, Budapest, Hungary. You can also search for this author in PubMed Google Scholar. and A. performed the experiments; M. and J. supervised L. supervised A.
and L. supervised J. supervised O. until independence; A. and V. designed the project; A. wrote the manuscript with input from all authors. Correspondence to Vamsi K. Mootha or Alexis A. is a paid scientific advisor to 5AM Ventures. was a paid consultant for Proteinaceous Inc.
has a financial interest in Soltego, a company developing salt-inducible kinase inhibitors for topical skin-darkening treatments that might be used for a broad set of human applications.
The interests of D. were reviewed and are managed by Massachusetts General Hospital and Partners HealthCare in accordance with their conflict-of-interest policies. The remaining authors declare no competing interests.
Nature Metabolism thanks the anonymous reviewers for their contribution to the peer review of this work. Primary Handling Editor: Alfredo Giménez-Cassina, in collaboration with the Nature Metabolism team. c Top 10 ontologies associated with the ORFs enriched and depleted in galactose relative to glucose.
The complete gene ontology analysis is reported in the Supplementary Data Table 1. Total S6 loading control was performed on the same gel. Top: Data shown at the individual sgRNA level. Bottom: Data shown at the gene level.
b Top 10 ontologies associated with the genes enriched and depleted in uridine relative to glucose. Only 8 terms scored for the analysis of essential genes in uridine. Data are shown as ±SEM with two-sided t-test relative DMSO. b Immunoblot analysis of proteins from upper glycolysis, the PPP and pyrimidine salvage in UPP1 -expressing K cells treated with their corresponding sgRNAs.
UCK1 is expressed at low levels in K cells and its protein could not be detected. c Simplified representation of the uridine salvage pathway and thymidine synthesis. TUBB and Actin loading controls were performed on the same gels. Hmgc2 transcripts are expected to increase with fasting. MDA: MDA-MBS.
c Top: Immunoblot of UACC melanoma cells with wild-type UPP1 WT and knock-out UPP1 KO. Bottom: Immunoblot of MDA-MBS melanoma cells in wild-type UPP1 WT , knock-out UPP1 KO and hypomorphic UPP1 hypo clones see methods. Negative doublings indicate cell death.
LOX-IMVI is a melanoma cell line with low endogenous MITF expression and over-expressing MITF or a control gene. P values were calculated using a two-sided student T test. Statistics were not adjusted for multiple comparison. c MITF occupancy in UPP1 transcription start site TSS and promoter a region 3.
d ChIP-qPCR validation of MITF binding in UPP1 promoter and TSS in MDA-MBS melanoma cells. TYR is a known transcriptional target of MITF, ACTB is not.
TUBB loading controls were performed on the same gels. Western blot quantification is shown as fold of untreated cells monocytes. Western blot quantification is shown as fold of untreated cells and relative to each donor. c Expression of UCK1 and UCK2 in THP1 cells as determined by qPCR after treatment as in a.
O: oligomycin. C: CCCP. A: antimycin A. d Schematic representation of de novo pyrimidine synthesis and uridine auxotrophy during OXPHOS inhibition. CoQ: co-enzyme Q. Ox: oxidized. Red: reduced. Open Access This article is licensed under a Creative Commons Attribution 4. Reprints and permissions.
Skinner, O. Salvage of ribose from uridine or RNA supports glycolysis in nutrient-limited conditions. Nat Metab 5 , — Download citation.
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Skip to main content Thank you for visiting nature. nature nature metabolism letters article. Download PDF. Subjects Carbohydrates Metabolism Metabolomics. Abstract Glucose is vital for life, serving as both a source of energy and carbon building block for growth.
Main We sought to identify new genes and pathways that might serve as alternative sources of energy when glucose is limiting. Full size image. Methods Cell lines K CCL , T CRL , HeLa CCL-2 , A CRL , A CRL , SH4 CRL , MDA-MBS HTB , SK-MEL-5 HTB , SK-MEL HTB and THP1 TIB cell lines were obtained from the American Type Culture Collection ATCC.
Open reading frame screen For ORF screening, K cells were infected with a lentiviral-carried ORFeome v8. Data availability All data generated or analysed during this study are included in the article and its Supplementary Information. References King, M. Article PubMed CAS Google Scholar Yang, X.
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Reprints and permissions. Althaus, F. Poly ADP-Ribose , Cellular Differentiation, and Gene Expression. In: ADP-Ribosylation of Proteins. Molecular Biology Biochemistry and Biophysics, vol Springer, Berlin, Heidelberg. Publisher Name : Springer, Berlin, Heidelberg. Print ISBN : Online ISBN : eBook Packages : Springer Book Archive.
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Policies and ethics. Skip to main content. Abstract The evidence for a role of poly-ADP-ribosylation in cellular differentiation, RNA metabolism, and DNA transcription is derived from a diverse experimental background involving numerous model systems and approaches. Keywords Mouse Mammary Tumor Virus Erythroid Differentiation Chick Limb Adenosine Diphosphate Ribose Friend Erythroleukemia Cell These keywords were added by machine and not by the authors.
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The Energy management techniques for athletes for a role of poly-ADP-ribosylation MRI for cardiology cellular Expdession, RNA metabolism, and DNA transcription is derived from a Energy management techniques for athletes experimental background involving numerous model systems anf approaches. Table 8. A chronological analysis of this literature background Ribos that selective inhibitors of poly ADP-ribose polymerase, available since the early s, have come to play an important role in demonstrating the involvement of ADP-ribosylation reactions in various processes associated with cellular differentiation. A brief discussion of these aspects in the study of DNA-repair mechanisms is presented in Chap. These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
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