Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Chromatin Loosening by Poly(ADP)-Ribose Polymerase (PARP) at Drosophila Puff Loci
Alexei Tulin,Allan Spradling
Steroid response and stress-activated genes such as
hsp70 undergo puffing in Drosophila larval
salivary glands, a local looseningof polytene chromatin structure
associated with gene induction.We find that puffs acquire elevated
levels of adenosine diphosphate(ADP)-ribose modified proteins and that
poly(ADP)-ribose polymerase(PARP) is required to produce
normal-sized puffs and normal amountsof Hsp70 after heat exposure. We
propose that chromosomal PARPmolecules become activated by
developmental or environmental cuesand strip nearby chromatin proteins
off DNA to generate a puff.Such local loosening may facilitate
transcription and may transientlymake protein complexes more
accessible to modification, promotingchromatin remodeling during
development.
Howard Hughes Medical Research Laboratories, Embryology
Department, Carnegie Institution of Washington, 115 West University
Parkway, Baltimore, MD 21210, USA.
The editors suggest the following Related Resources on Science sites:
In Science Magazine
PERSPECTIVES
Vincenzo Pirrotta (24 January 2003) Science299 (5606), 528.
[DOI: 10.1126/science.1081520] |Summary »|Full Text »|PDF »
Dual Roles of PARP-1 Promote Cancer Growth and Progression.
M. J. Schiewer, J. F. Goodwin, S. Han, J. C. Brenner, M. A. Augello, J. L. Dean, F. Liu, J. L. Planck, P. Ravindranathan, A. M. Chinnaiyan, et al. (2012)
Cancer Discovery
2, 1134-1149
|Abstract »|Full Text »|PDF »
Quantitative proteomics and dynamic imaging reveal that G3BP-mediated stress granule assembly is poly(ADP-ribose)-dependent following exposure to MNNG-induced DNA alkylation.
M. Isabelle, J.-P. Gagne, I.-E. Gallouzi, and G. G. Poirier (2012)
J. Cell Sci.
125, 4555-4566
|Abstract »|Full Text »|PDF »
Histone ADP-Ribosylation Facilitates Gene Transcription by Directly Remodeling Nucleosomes.
Recruitment of the ATP-dependent chromatin remodeler dMi-2 to the transcribed region of active heat shock genes.
E.-L. Mathieu, F. Finkernagel, M. Murawska, M. Scharfe, M. Jarek, and A. Brehm (2012)
Nucleic Acids Res.
40, 4879-4891
|Abstract »|Full Text »|PDF »
Regulation of Poly(ADP-ribose) Polymerase-1-dependent Gene Expression through Promoter-directed Recruitment of a Nuclear NAD+ Synthase.
T. Zhang, J. G. Berrocal, J. Yao, M. E. DuMond, R. Krishnakumar, D. D. Ruhl, K. W. Ryu, M. J. Gamble, and W. L. Kraus (2012)
J. Biol. Chem.
287, 12405-12416
|Abstract »|Full Text »|PDF »
On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1.
Role of ATRX in chromatin structure and function: implications for chromosome instability and human disease.
R. De La Fuente, C. Baumann, and M. M. Viveiros (2011)
Reproduction
142, 221-234
|Abstract »|Full Text »|PDF »
Loss of poly(ADP-ribose) polymerase 1 attenuates renal fibrosis and inflammation during unilateral ureteral obstruction.
J. Kim and B. J. Padanilam (2011)
Am J Physiol Renal Physiol
301, F450-F459
|Abstract »|Full Text »|PDF »
Poly(ADP-Ribose) Polymerases PARP1 and PARP2 Modulate Topoisomerase II Beta (TOP2B) Function During Chromatin Condensation in Mouse Spermiogenesis.
M. L. Meyer-Ficca, J. D. Lonchar, M. Ihara, M. L. Meistrich, C. A. Austin, and R. G. Meyer (2011)
Biol Reprod
84, 900-909
|Abstract »|Full Text »|PDF »
Poly(ADP-ribose) Metabolism Is Essential for Proper Nucleoprotein Exchange During Mouse Spermiogenesis.
M. L. Meyer-Ficca, M. Ihara, J. D. Lonchar, M. L. Meistrich, C. A. Austin, W. Min, Z.-Q. Wang, and R. G. Meyer (2011)
Biol Reprod
84, 218-228
|Abstract »|Full Text »|PDF »
Epigenetic Reprogramming of Mouse Germ Cells toward Totipotency.
M. A. Surani and P. Hajkova (2010)
Cold Spring Harb Symp Quant Biol
|Abstract »|PDF »
Histone H1 Poly[ADP]-Ribosylation Regulates the Chromatin Alterations Required for Learning Consolidation.
A. Fontan-Lozano, I. Suarez-Pereira, A. Horrillo, Y. del-Pozo-Martin, A. Hmadcha, and A. M. Carrion (2010)
J. Neurosci.
30, 13305-13313
|Abstract »|Full Text »|PDF »
Epigenetic Regulation of Repetitive Elements Is Attenuated by Prolonged Heat Stress in Arabidopsis.
A. Pecinka, H. Q. Dinh, T. Baubec, M. Rosa, N. Lettner, and O. M. Scheid (2010)
PLANT CELL
22, 3118-3129
|Abstract »|Full Text »|PDF »
Genome-Wide Reprogramming in the Mouse Germ Line Entails the Base Excision Repair Pathway.
P. Hajkova, S. J. Jeffries, C. Lee, N. Miller, S. P. Jackson, and M. A. Surani (2010)
Science
329, 78-82
|Abstract »|Full Text »|PDF »
The Zn3 Domain of Human Poly(ADP-ribose) Polymerase-1 (PARP-1) Functions in Both DNA-dependent Poly(ADP-ribose) Synthesis Activity and Chromatin Compaction.
M.-F. Langelier, D. D. Ruhl, J. L. Planck, W. L. Kraus, and J. M. Pascal (2010)
J. Biol. Chem.
285, 18877-18887
|Abstract »|Full Text »|PDF »
PARP1 deficiency exacerbates diet-induced obesity in mice.
K. Devalaraja-Narashimha and B. J. Padanilam (2010)
J. Endocrinol.
205, 243-252
|Abstract »|Full Text »|PDF »
Global Analysis of Transcriptional Regulation by Poly(ADP-ribose) Polymerase-1 and Poly(ADP-ribose) Glycohydrolase in MCF-7 Human Breast Cancer Cells.
K. M. Frizzell, M. J. Gamble, J. G. Berrocal, T. Zhang, R. Krishnakumar, Y. Cen, A. A. Sauve, and W. L. Kraus (2009)
J. Biol. Chem.
284, 33926-33938
|Abstract »|Full Text »|PDF »
Poly(ADP-ribose) Polymerase-1 Down-regulates BRCA2 Expression through the BRCA2 Promoter.
J. Wang, C. Bian, J. Li, F. J. Couch, K. Wu, and R. C. Zhao (2008)
J. Biol. Chem.
283, 36249-36256
|Abstract »|Full Text »|PDF »
Potentiation of Temozolomide Cytotoxicity by Poly(ADP)Ribose Polymerase Inhibitor ABT-888 Requires a Conversion of Single-Stranded DNA Damages to Double-Stranded DNA Breaks.
X. Liu, Y. Shi, R. Guan, C. Donawho, Y. Luo, J. Palma, G.-d. Zhu, E. F. Johnson, L. E. Rodriguez, N. Ghoreishi-Haack, et al. (2008)
Mol. Cancer Res.
6, 1621-1629
|Abstract »|Full Text »|PDF »
CCCTC-binding Factor Activates PARP-1 Affecting DNA Methylation Machinery.
T. Guastafierro, B. Cecchinelli, M. Zampieri, A. Reale, G. Riggio, O. Sthandier, G. Zupi, L. Calabrese, and P. Caiafa (2008)
J. Biol. Chem.
283, 21873-21880
|Abstract »|Full Text »|PDF »
Poly(ADP-ribose) Binds to the Splicing Factor ASF/SF2 and Regulates Its Phosphorylation by DNA Topoisomerase I.
M. Malanga, A. Czubaty, A. Girstun, K. Staron, and F. R. Althaus (2008)
J. Biol. Chem.
283, 19991-19998
|Abstract »|Full Text »|PDF »
Ectopic histone H3S10 phosphorylation causes chromatin structure remodeling in Drosophila.
H. Deng, X. Bao, W. Cai, M. J. Blacketer, A. S. Belmont, J. Girton, J. Johansen, and K. M. Johansen (2008)
Development
135, 699-705
|Abstract »|Full Text »|PDF »
Reciprocal Binding of PARP-1 and Histone H1 at Promoters Specifies Transcriptional Outcomes.
R. Krishnakumar, M. J. Gamble, K. M. Frizzell, J. G. Berrocal, M. Kininis, and W. L. Kraus (2008)
Science
319, 819-821
|Abstract »|Full Text »|PDF »
Nucleosomal Core Histones Mediate Dynamic Regulation of Poly(ADP-ribose) Polymerase 1 Protein Binding to Chromatin and Induction of Its Enzymatic Activity.
A. Pinnola, N. Naumova, M. Shah, and A. V. Tulin (2007)
J. Biol. Chem.
282, 32511-32519
|Abstract »|Full Text »|PDF »
The histone variant mH2A1.1 interferes with transcription by down-regulating PARP-1 enzymatic activity.
K. Ouararhni, R. Hadj-Slimane, S. Ait-Si-Ali, P. Robin, F. Mietton, A. Harel-Bellan, S. Dimitrov, and A. Hamiche (2006)
Genes & Dev.
20, 3324-3336
|Abstract »|Full Text »|PDF »
ART2, a T Cell Surface Mono-ADP-ribosyltransferase, Generates Extracellular Poly(ADP-ribose).
A. R. Morrison, J. Moss, L. A. Stevens, J. E. Evans, C. Farrell, E. Merithew, D. G. Lambright, D. L. Greiner, J. P. Mordes, A. A. Rossini, et al. (2006)
J. Biol. Chem.
281, 33363-33372
|Abstract »|Full Text »|PDF »
Poly(ADP-ribose) polymerase-2 contributes to the fidelity of male meiosis I and spermiogenesis.
F. Dantzer, M. Mark, D. Quenet, H. Scherthan, A. Huber, B. Liebe, L. Monaco, A. Chicheportiche, P. Sassone-Corsi, G. de Murcia, et al. (2006)
PNAS
103, 14854-14859
|Abstract »|Full Text »|PDF »
Estrogen-receptor-{alpha} exchange and chromatin dynamics are ligand- and domain-dependent.
Z. D. Sharp, M. G. Mancini, C. A. Hinojos, F. Dai, V. Berno, A. T. Szafran, K. P. Smith, T. T. Lele, D. E. Ingber, and M. A. Mancini (2006)
J. Cell Sci.
119, 4101-4116
|Abstract »|Full Text »|PDF »
Nuclear ADP-Ribosylation Reactions in Mammalian Cells: Where Are We Today and Where Are We Going?.
P. O. Hassa, S. S. Haenni, M. Elser, and M. O. Hottiger (2006)
Microbiol. Mol. Biol. Rev.
70, 789-829
|Abstract »|Full Text »|PDF »
The Dynamic Alterations of H2AX Complex during DNA Repair Detected by a Proteomic Approach Reveal the Critical Roles of Ca2+/Calmodulin in the Ionizing Radiation-induced Cell Cycle Arrest.
Y.-C. Du, S. Gu, J. Zhou, T. Wang, H. Cai, M. A. MacInnes, E. M. Bradbury, and X. Chen (2006)
Mol. Cell. Proteomics
5, 1033-1044
|Abstract »|Full Text »|PDF »
Direct phosphorylation and regulation of poly(ADP-ribose) polymerase-1 by extracellular signal-regulated kinases 1/2.
T. M. Kauppinen, W. Y. Chan, S. W. Suh, A. K. Wiggins, E. J. Huang, and R. A. Swanson (2006)
PNAS
103, 7136-7141
|Abstract »|Full Text »|PDF »
Functional Characterization of the Putative Aspergillus nidulans Poly(ADP-Ribose) Polymerase Homolog PrpA.
C. P. Semighini, M. Savoldi, G. H. Goldman, and S. D. Harris (2006)
Genetics
173, 87-98
|Abstract »|Full Text »|PDF »
The Drosophila P68 RNA helicase regulates transcriptional deactivation by promoting RNA release from chromatin.
Chromatin Decondensation and Nuclear Reprogramming by Nucleoplasmin.
H. Tamada, N. V. Thuan, P. Reed, D. Nelson, N. Katoku-Kikyo, J. Wudel, T. Wakayama, and N. Kikyo (2006)
Mol. Cell. Biol.
26, 1259-1271
|Abstract »|Full Text »|PDF »
Modulation of nucleosome-binding activity of FACT by poly(ADP-ribosyl)ation..
J.-Y. Huang, W.-H. Chen, Y.-L. Chang, H.-T. Wang, W.-t. Chuang, and S.-C. Lee (2006)
Nucleic Acids Res.
34, 2398-2407
|Abstract »|Full Text »|PDF »
Drosophila Poly(ADP-Ribose) Glycohydrolase Mediates Chromatin Structure and SIR2-Dependent Silencing.
A. Tulin, N. M. Naumova, A. K. Menon, and A. C. Spradling (2006)
Genetics
172, 363-371
|Abstract »|Full Text »|PDF »
Acetylation of Poly(ADP-ribose) Polymerase-1 by p300/CREB-binding Protein Regulates Coactivation of NF-{kappa}B-dependent Transcription.
P. O. Hassa, S. S. Haenni, C. Buerki, N. I. Meier, W. S. Lane, H. Owen, M. Gersbach, R. Imhof, and M. O. Hottiger (2005)
J. Biol. Chem.
280, 40450-40464
|Abstract »|Full Text »|PDF »
B-aggressive Lymphoma Family Proteins Have Unique Domains That Modulate Transcription and Exhibit Poly(ADP-ribose) Polymerase Activity.
R. C. T. Aguiar, K. Takeyama, C. He, K. Kreinbrink, and M. A. Shipp (2005)
J. Biol. Chem.
280, 33756-33765
|Abstract »|Full Text »|PDF »
Inhibition of Aurora-B kinase activity by poly(ADP-ribosyl)ation in response to DNA damage.
L. Monaco, U. Kolthur-Seetharam, R. Loury, J. M.-d. Murcia, G. de Murcia, and P. Sassone-Corsi (2005)
PNAS
102, 14244-14248
|Abstract »|Full Text »|PDF »
Cooperation of the Cockayne Syndrome Group B Protein and Poly(ADP-Ribose) Polymerase 1 in the Response to Oxidative Stress.
T. Thorslund, C. von Kobbe, J. A. Harrigan, F. E. Indig, M. Christiansen, T. Stevnsner, and V. A. Bohr (2005)
Mol. Cell. Biol.
25, 7625-7636
|Abstract »|Full Text »|PDF »
Poly(ADP-ribosyl)ation by PARP-1: `PAR-laying' NAD+ into a nuclear signal.
PolyADP-Ribosylation Is Involved in Neurotrophic Activity.
L. Visochek, R. A. Steingart, I. Vulih-Shultzman, R. Klein, E. Priel, I. Gozes, and M. Cohen-Armon (2005)
J. Neurosci.
25, 7420-7428
|Abstract »|Full Text »|PDF »
Regulation of Poly(ADP-ribose) Polymerase-1 by DNA Structure-specific Binding.
I. Lonskaya, V. N. Potaman, L. S. Shlyakhtenko, E. A. Oussatcheva, Y. L. Lyubchenko, and V. A. Soldatenkov (2005)
J. Biol. Chem.
280, 17076-17083
|Abstract »|Full Text »|PDF »
Inhibition of Epstein-Barr Virus OriP Function by Tankyrase, a Telomere-Associated Poly-ADP Ribose Polymerase That Binds and Modifies EBNA1.
Z. Deng, C. Atanasiu, K. Zhao, R. Marmorstein, J. I. Sbodio, N.-W. Chi, and P. M. Lieberman (2005)
J. Virol.
79, 4640-4650
|Abstract »|Full Text »|PDF »
Mechanism of early biphasic activation of poly(ADP-ribose) polymerase-1 in response to ultraviolet B radiation.
M. D. Vodenicharov, M. M. Ghodgaonkar, S. S. Halappanavar, R. G. Shah, and G. M. Shah (2005)
J. Cell Sci.
118, 589-599
|Abstract »|Full Text »|PDF »
Increased expression of poly(ADP-ribose) polymerase-1 contributes to caspase-independent myocyte cell death during heart failure.
J. B. Pillai, H. M. Russell, J. Raman, V. Jeevanandam, and M. P. Gupta (2005)
Am J Physiol Heart Circ Physiol
288, H486-H496
|Abstract »|Full Text »|PDF »
Inhibition of Poly(ADP-Ribose) Glycohydrolase by Gallotannin Selectively Up-Regulates Expression of Proinflammatory Genes.
E. Rapizzi, S. Fossati, F. Moroni, and A. Chiarugi (2004)
Mol. Pharmacol.
66, 890-898
|Abstract »|Full Text »|PDF »
Long-Term Memory Requires PolyADP-ribosylation.
M. Cohen-Armon, L. Visochek, A. Katzoff, D. Levitan, A. J. Susswein, R. Klein, M. Valbrun, and J. H. Schwartz (2004)
Science
304, 1820-1822
|Abstract »|Full Text »|PDF »
Defective transcription factor activation for proinflammatory gene expression in poly(ADP-ribose) polymerase 1-deficient glia.
Differential regulation of activator protein-1 and heat shock factor-1 in myocardial ischemia and reperfusion injury: role of poly(ADP-ribose) polymerase-1.
B. Zingarelli, P. W. Hake, M. O'Connor, A. Denenberg, H. R. Wong, S. Kong, and B. J. Aronow (2004)
Am J Physiol Heart Circ Physiol
286, H1408-H1415
|Abstract »|Full Text »|PDF »
M. Rouleau, R. A. Aubin, and G. G. Poirier (2004)
J. Cell Sci.
117, 815-825
|Abstract »|Full Text »|PDF »
Studies of the Role of the Drosophila scs and scs' Insulators in Defining Boundaries of a Chromosome Puff.
E. J. Kuhn, C. M. Hart, and P. K. Geyer (2004)
Mol. Cell. Biol.
24, 1470-1480
|Abstract »|Full Text »|PDF »
Transcription regulation of TNF-{alpha}-early response genes by poly(ADP-ribose) polymerase-1 in murine heart endothelial cells.
A. Carrillo, Y. Monreal, P. Ramirez, L. Marin, P. Parrilla, F. J. Oliver, and J. Yelamos (2004)
Nucleic Acids Res.
32, 757-766
|Abstract »|Full Text »|PDF »
Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in Drosophila melanogaster.
S. Hanai, M. Kanai, S. Ohashi, K. Okamoto, M. Yamada, H. Takahashi, and M. Miwa (2004)
PNAS
101, 82-86
|Abstract »|Full Text »|PDF »
Poly(ADP-Ribose) Polymerase 1 and Ste20-Like Kinase hKFC Act as Transcriptional Repressors for Gamma-2 Herpesvirus Lytic Replication.
Y. Gwack, H. Nakamura, S. H. Lee, J. Souvlis, J. T. Yustein, S. Gygi, H.-J. Kung, and J. U. Jung (2003)
Mol. Cell. Biol.
23, 8282-8294
|Abstract »|Full Text »|PDF »
Transcriptional Coactivation of Nuclear Factor-{kappa}B-dependent Gene Expression by p300 Is Regulated by Poly(ADP)-ribose Polymerase-1.
P. O. Hassa, C. Buerki, C. Lombardi, R. Imhof, and M. O. Hottiger (2003)
J. Biol. Chem.
278, 45145-45153
|Abstract »|Full Text »|PDF »
A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage.
S. F. El-Khamisy, M. Masutani, H. Suzuki, and K. W. Caldecott (2003)
Nucleic Acids Res.
31, 5526-5533
|Abstract »|Full Text »|PDF »
Intra-mitochondrial Poly(ADP-ribosylation) Contributes to NAD+ Depletion and Cell Death Induced by Oxidative Stress.
L. Du, X. Zhang, Y. Y. Han, N. A. Burke, P. M. Kochanek, S. C. Watkins, S. H. Graham, J. A. Carcillo, C. Szabo, and R. S. B. Clark (2003)
J. Biol. Chem.
278, 18426-18433
|Abstract »|Full Text »|PDF »