The DOI matches its Crossref record; 52 of the 53 references it cites were found in a registry or an index.
The Drosophila heterochromatic gene encoding poly(ADP-ribose) polymerase (PARP) is required to modulate chromatin structure during development
Open accessAbstract
Poly(ADP-ribose) polymerase (PARP) is a major NAD-dependent modifying enzyme that mediates important steps in DNA repair, transcription, and apoptosis, but its role during development is poorly understood. We found that a single Drosophila Parp gene spans more than 150 kb of transposon-rich centromeric heterochromatin and produces several differentially spliced transcripts, including a novel isoform, PARP-e, predicted to encode a protein lacking enzymatic activity. An insertion mutation near the upstream promoter for Parp-e disrupts all Parp expression. Heterochromatic but not euchromatic sequences become hypersensitive to micrococcal nuclease, nucleoli fail to form, and transcript levels of the copia retrotransposon are elevated more than 50-fold; the variegated expression of certain transgenes is dominantly enhanced. Larval lethality can be rescued and PARP activity restored by expressing a cDNA encoding PARP-e. We propose that PARP-e autoregulates Parp transcription by influencing the chromatin structure of its heterochromatic environment. Our results indicate that Parp plays a fundamental role organizing the structure of Drosophila chromatin.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The cited source says what the claim attributes to it.
In the citing paper
“a protein which has been implicated in the silencing of retrotransposons in Drosophila30”
From SIRT6 represses LINE1 retrotransposons by ribosylating KAP1 but this repression fails with stress and age (2014) · cites this paper as [30]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Targeted gene expression as a means of altering cell fates and generating dominant phenotypes
Brand, A. H., & Perrimon, N. (1993) · Development · doi:10.1242/dev.118.2.401 · Cited by 9,510
The language of covalent histone modifications
Strahl, B. D., & Allis, C. D. (2000) · Nature · doi:10.1038/47412 · Cited by 8,679
The Genome Sequence of Drosophila melanogaster
Adams, M. D., Celniker, S., Holt, R. A., Evans, C. A., Gocayne, J. D., Amanatides, P. G., Scherer, S. E., Li, P. W., Hoskins, R. A., Galle, R. F., et al. (2000) · Science · doi:10.1126/science.287.5461.2185 · Cited by 5,902
Role of Histone H3 Lysine 9 Methylation in Epigenetic Control of Heterochromatin Assembly
Nakayama, J.-I., Rice, J. C., Strahl, B. D., Allis, C. D., & Grewal, S. I. S. (2001) · Science · doi:10.1126/science.1060118 · Cited by 1,739
Transposition of Cloned P Elements into Drosophila Germ Line Chromosomes
Spradling, A. C., & Rubin, G. M. (1982) · Science · doi:10.1126/science.6289435 · Cited by 1,563
Self-citationKennerdell, J. R., & Carthew, R. W. (1998) · Cell · doi:10.1016/s0092-8674(00)81725-0 · Cited by 1,154
Requirement of poly(ADP-ribose) polymerase in recovery from DNA damage in mice and in cells
Murcia, J. M., Niedergang, C., Trucco, C., Ricoul, M., Dutrillaux, B., Mark, M. P., Oliver, F. J., Masson, M., Dierich, A., LeMeur, M., et al. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.14.7303 · Cited by 1,058
Foe, V. E., & Alberts, B. (1983) · Journal of Cell Science · doi:10.1242/jcs.61.1.31 · Cited by 1,056
Tankyrase, a Poly(ADP-Ribose) Polymerase at Human Telomeres
Smith, S. H., Giriat, I., Schmitt, A., & de Lange, T. (1998) · Science · doi:10.1126/science.282.5393.1484 · Cited by 1,039
PARP-2, A Novel Mammalian DNA Damage-dependent Poly(ADP-ribose) Polymerase
Amé, J., Rolli, V., Schreiber, V., Niedergang, C., Apiou, F., Decker, P., Muller, S., Höger, T. H., Murcia, J. M., & de MURCIA, G. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.25.17860 · Cited by 744
Poly(ADP-ribose) Binds to Specific Domains in DNA Damage Checkpoint Proteins
Pleschke, J. M., Kleczkowska, H. E., Strohm, M., & Althaus, F. R. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m006520200 · Cited by 564
PARP is important for genomic stability but dispensable in apoptosisPreprint
Wang, Z., Stingl, L., Morrison, C. G., Jantsch, M. F., Łoś, M., Schulze‐Osthoff, K., & Wagner, E. F. (1997) · Genes & Development · doi:10.1101/gad.11.18.2347 · Cited by 557
Chromatin disruption and modification
Wolffe, A. P., & Hayes, J. J. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.3.711 · Cited by 551
HETEROCHROMATIN AND GENE EXPRESSION IN DROSOPHILA
Weiler, K. S., & Wakimoto, B. T. (1995) · Annual Review of Genetics · doi:10.1146/annurev.ge.29.120195.003045 · Cited by 533
Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure.
Poirier, G. G., de MURCIA, G., Jongstra‐Bilen, J., Niedergang, C., & Mandel, P. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.11.3423 · Cited by 516
The 193-Kd Vault Protein, Vparp, Is a Novel Poly(Adp-Ribose) Polymerase
Kickhoefer, V. A., Siva, A. C., Kedersha, N., Inman, E. M., Ruland, C. T., Streuli, M., & Rome, L. H. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.146.5.917 · Cited by 404
Karpen, G. H., & Spradling, A. C. (1992) · Genetics · doi:10.1093/genetics/132.3.737 · Cited by 392
Self-citationUncoupling cadherin-based adhesion from wingless signalling in Drosophila
Sanson, B., White, P., & Vincent, J. (1996) · Nature · doi:10.1038/383627a0 · Cited by 360
A Drosophila Complementary DNA Resource
Rubin, G. M., Hong, L., Brokstein, P. B., Evans-Holm, M. E., Frise, E., Stapleton, M., & Harvey, D. A. (2000) · Science · doi:10.1126/science.287.5461.2222 · Cited by 330
The FlyBase Database of the Drosophila Genome Projects and community literature
(1999) · Nucleic Acids Research · doi:10.1093/nar/27.1.85 · Cited by 325
The fusome organizes the microtubule network during oocyte differentiation in Drosophila
Grieder, N. C., de Cuevas, M., & Spradling, A. C. (2000) · Development · doi:10.1242/dev.127.19.4253 · Cited by 271
Self-citationGenes controlling essential cell-cycle functions in Drosophila melanogaster.Preprint
Gatti, M., & Baker, B. (1989) · Genes & Development · doi:10.1101/gad.3.4.438 · Cited by 256
Monoclonal antibodies to poly(adenosine diphosphate ribose) recognize different structures
Kawamitsu, H., Hoshino, H., Okada, H., Miwa, M., Momoi, H., & Sügimura, T. (1984) · Biochemistry · doi:10.1021/bi00311a032 · Cited by 232
Lu, B. Y., Emtage, P. C. R., Duyf, B., Hilliker, A. J., & Eissenberg, J. C. (2000) · Genetics · doi:10.1093/genetics/155.2.699 · Cited by 187
Chromatin remodeling machines: similar motors, ulterior motives
Cairns, B. R. (1998) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(97)01160-2 · Cited by 174
GFP-tagged balancer chromosomes for Drosophila melanogaster
Casso, D. J., Ramı́rez-Weber, F.-A., & Kornberg, T. B. (1999) · Mechanisms of Development · doi:10.1016/s0925-4773(99)00174-4 · Cited by 174
The endocycle controls nurse cell polytene chromosome structure during Drosophila oogenesis
Dej, K. J., & Spradling, A. C. (1999) · Development · doi:10.1242/dev.126.2.293 · Cited by 161
Self-citationChromatin Insulators and Boundaries: Effects on Transcription and Nuclear Organization
Gerasimova, T. I., & Corces, V. G. (2001) · Annual Review of Genetics · doi:10.1146/annurev.genet.35.102401.090349 · Cited by 157
Dantzer, F. (1998) · Nucleic Acids Research · doi:10.1093/nar/26.8.1891 · Cited by 155
Poly ADP-ribosylation: a histone shuttle mechanism in DNA excision repair
Us, F. R. A. (1992) · Journal of Cell Science · doi:10.1242/jcs.102.4.663 · Cited by 139
From DNA damage and stress signalling to cell death : poly-ADP-ribosylation reactions
de MURCIA, G., & Shall, S. (2000) · Medical Entomology and Zoology · Cited by 134
Genetic controls of meiotic recombination and somatic DNA metabolism in Drosophila melanogaster.
Baker, B. S., Boyd, J. B., Carpenter, A. T. C., Green, M. M., Nguyen, T. D., Ripoll, P. L., & Smith, P. D. (1976) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.73.11.4140 · Cited by 132
A cellular survival switch: poly(ADP‐ribosyl)ation stimulates DNA repair and silences transcription
Ziegler, M., & Oei, S. L. (2001) · BioEssays · doi:10.1002/bies.1074 · Cited by 125
GFP-tagged balancer chromosomes for Drosophila melanogaster
Casso, D. J., Ramı́rez-Weber, F.-A., & Kornberg, T. B. (2000) · Mechanisms of Development · doi:10.1016/s0925-4773(00)00248-3 · Cited by 120
Rosenberg, M. I., & Parkhurst, S. M. (2002) · Cell · doi:10.1016/s0092-8674(02)00732-8 · Cited by 118
Tanuma, S.-I., Johnson, L. D., & Johnson, G. S. (1983) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)43816-6 · Cited by 89
Chromatin organization and transcriptional control of gene expression in Drosophila
Farkas, G., Leibovitch, B. A., & Elgin, S. C. R. (2000) · Gene · doi:10.1016/s0378-1119(00)00240-7 · Cited by 88
Cellular memory of transcriptional states by Polycomb-group proteins
Jacobs, J. J. L., & van Lohuizen, M. (1999) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.1999.0304 · Cited by 76
Uchida, K., Hanai, S., Ishikawa, K., Ozawa, Y., Uchida, M., Sügimura, T., & Miwa, M. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.8.3481 · Cited by 71
[14] Analysis of hypersensitive sites in chromatin
Wu, C. (1989) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(89)70052-5 · Cited by 71
dSIR2 and dHDAC6: Two Novel, Inhibitor-Resistant Deacetylases in Drosophila melanogaster
Barlow, A. L., van Drunen, C. M., Johnson, C. A., Tweedie, S., Bird, A. P., & Turner, B. M. (2001) · Experimental Cell Research · doi:10.1006/excr.2001.5162 · Cited by 65
A P1-based physical map of the Drosophila euchromatic genome.Preprint
Kimmerly, W. J., Stultz, K., Lewis, S., Lewis, K., Lustre, V. M., Romero, R., Benke, J., Sun, D., Shirley, G., Martin, C., et al. (1996) · Genome Research · doi:10.1101/gr.6.5.414 · Cited by 63
Insertional mutagenesis of Drosophila heterochromatin with single P elements.
Zhang, P., & Spradling, A. C. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.9.3539 · Cited by 60
Self-citationPoly(ADP-ribosylation) of histones in intact human keratinocytes
Krupitza, G., & Cerutti, P. (1989) · Biochemistry · doi:10.1021/bi00435a063 · Cited by 55
Interactions of poly(ADP-ribose) with nuclear proteins
Althaus, F. R., Bachmann, S., Höfferer, L., Kleczkowska, H. E., Malanga, M., Panzeter, P. L., Realini, C. A., & Zweifel, B. (1995) · Biochimie · doi:10.1016/0300-9084(96)88155-7 · Cited by 31
Remembrance of things past: maintaining gene expression patterns with altered chromatin
Hagstrom, K., & Schedl, P. D. (1997) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(97)80045-7 · Cited by 30
A rosy future for heterochromatin.
Cook, K. R., & Karpen, G. H. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.12.5219 · Cited by 29
Hanai, S., Uchida, M., Kobayashi, S., Miwa, M., & Uchida, K. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.19.11881 · Cited by 28
Double Hydrocœle in the Development and Metamorphosis of the Larva of Asterias rubens, L.
Gemmill, J. F. (1915) · Journal of Cell Science · doi:10.1242/jcs.s2-61.241.51 · Cited by 14
Kawamura, T., Hanai, S., Yokota, T., Hayashi, T., Poltronieri, P., Miwa, M., & Uchida, K. (1998) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1998.9403 · Cited by 13
Prokhorova, A. V., Voloshina, M. A., Shostak, N. G., Barskiĭ, V. E., & Golubovskii, M. D. (1994) · PubMed · Cited by 7
Genomic Footprinting ofDrosophilaEmbryo Nuclei by Linker Tag Selection LM-PCR
Quivy, J., & Becker, P. B. (1997) · Methods · doi:10.1006/meth.1996.0403 · Cited by 5
Cited by
Sorted by citations
Poly(ADP-ribose): novel functions for an old molecule
Schreiber, V., Dantzer, F., Amé, J., & de MURCIA, G. (2006) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1963 · Cited by 1,975
Advances in autism genetics: on the threshold of a new neurobiology
Abrahams, B. S., & Geschwind, D. H. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2346 · Cited by 1,866
Single-strand break repair and genetic disease
Caldecott, K. W. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2380 · Cited by 1,097
Rosenfeld, M. G., Lunyak, V. V., & Glass, C. K. (2006) · Genes & Development · doi:10.1101/gad.1424806 · Cited by 952
The BDGP Gene Disruption Project
Bellen, H. J., Levis, R. W., Liao, G., He, Y., Carlson, J. W., Tsang, G., Evans-Holm, M. E., Hiesinger, P. R., Schulze, K. L., Rubin, G. M., et al. (2004) · Genetics · doi:10.1534/genetics.104.026427 · Cited by 864
Self-citation
Metadata
- Authors
- Tulin, A., Stewart, D., & Spradling, A. C.
- Affiliations
- Carnegie Institution for Science (US)
- Venue
- Genes & Development
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2002-08-15
- Volume
- 16
- Issue
- 16
- Pages
- 2108-2119
- ISSN
- 0890-9369 (ISSN-L)
- 1549-5477
- PMC
- PMC186441
- OpenAlex
- W2128974910
- Cited by
- 204
- References
- 53
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 8 · 2023: 8 · 2022: 6 · 2021: 4 · 2020: 3 · 2019: 5 · 2017: 1 · 2016: 10 · 2015: 3 · 2014: 10 · 2013: 10 · 2012: 9
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genes & Development (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute of General Medical Sciences (GM-27875)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Keywords
- poly(ADP-ribose) polymerase, Drosophila, centromeric heterochromatin, chromatin structure, alternative splicing, nucleolus formation, copia retrotransposon, developmental lethality
- MeSH terms
- Animals, Cell Nucleolus, Chromatin, Chromosome Mapping, Chromosomes, DNA, DNA Transposable Elements, Drosophila, Genes, Dominant, Genotype, Heterochromatin, Immunohistochemistry, Micrococcal Nuclease, Microscopy, Fluorescence, Models, Genetic, Mutation, Poly(ADP-ribose) Polymerases, RNA, Messenger, Time Factors, Blotting, Northern, In Situ Hybridization, Fluorescence, DNA, Complementary, Gene Expression Regulation, Developmental, Protein Isoforms, Reverse Transcriptase Polymerase Chain Reaction
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review