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.

Subscribe

Logo for

Science 319 (5864): 819-821

Copyright © 2008 by the American Association for the Advancement of Science

Reciprocal Binding of PARP-1 and Histone H1 at Promoters Specifies Transcriptional Outcomes

Raga Krishnakumar,1,2* Matthew J. Gamble,1* Kristine M. Frizzell,1,2 Jhoanna G. Berrocal,1,2 Miltiadis Kininis,1,3 W. Lee Kraus1,2,3,4{dagger}

Abstract: Nucleosome-binding proteins act to modulate the promoter chromatin architecture and transcription of target genes. We used genomic and gene-specific approaches to show that two such factors, histone H1 and poly(ADP-ribose) polymerase-1 (PARP-1), exhibit a reciprocal pattern of chromatin binding at many RNA polymerase II–transcribed promoters. PARP-1 was enriched and H1 was depleted at these promoters. This pattern of binding was associated with actively transcribed genes. Furthermore, we showed that PARP-1 acts to exclude H1 from a subset of PARP-1–stimulated promoters, suggesting a functional interplay between PARP-1 and H1 at the level of nucleosome binding. Thus, although H1 and PARP-1 have similar nucleosome-binding properties and effects on chromatin structure in vitro, they have distinct roles in determining gene expression outcomes in vivo.

1 Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY 14853, USA.
2 Graduate Field of Biochemistry, Molecular and Cell Biology, Cornell University, Ithaca, NY 14853, USA.
3 Graduate Field of Genetics and Development, Cornell University, Ithaca, NY 14853, USA.
4 Department of Pharmacology, Weill Medical College of Cornell University, New York, NY 10021, USA.

* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed at Department of Molecular Biology and Genetics, Cornell University, 465 Biotechnology Building, Ithaca, NY 14853, USA. E-mail: wlk5{at}cornell.edu


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Mapping of six somatic linker histone H1 variants in human breast cancer cells uncovers specific features of H1.2.
L. Millan-Arino, A. B. M. M. K. Islam, A. Izquierdo-Bouldstridge, R. Mayor, J.-M. Terme, N. Luque, M. Sancho, N. Lopez-Bigas, and A. Jordan (2014)
Nucleic Acids Res. 42, 4474-4493
   Abstract »    Full Text »    PDF »
Novel insights into the neuroendocrine control of inflammation: the role of GR and PARP1.
F. Aprile-Garcia, M. Antunica-Noguerol, M. L. Budzinski, A. C. Liberman, and E. Arzt (2014)
Endocrine Connections 3, R1-R12
   Abstract »    Full Text »    PDF »
2,3,7,8-Tetrachlorodibenzo-p-dioxin poly(ADP-ribose) polymerase (TiPARP, ARTD14) is a mono-ADP-ribosyltransferase and repressor of aryl hydrocarbon receptor transactivation.
L. MacPherson, L. Tamblyn, S. Rajendra, F. Bralha, J. P. McPherson, and J. Matthews (2013)
Nucleic Acids Res. 41, 1604-1621
   Abstract »    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 »
Alternative Modes of Binding of Poly(ADP-ribose) Polymerase 1 to Free DNA and Nucleosomes.
N. J. Clark, M. Kramer, U. M. Muthurajan, and K. Luger (2012)
J. Biol. Chem. 287, 32430-32439
   Abstract »    Full Text »    PDF »
CDK2-dependent activation of PARP-1 is required for hormonal gene regulation in breast cancer cells.
R. H. G. Wright, G. Castellano, J. Bonet, F. Le Dily, J. Font-Mateu, C. Ballare, A. S. Nacht, D. Soronellas, B. Oliva, and M. Beato (2012)
Genes & Dev. 26, 1972-1983
   Abstract »    Full Text »    PDF »
PARPs and the DNA damage response.
F. G. Sousa, R. Matuo, D. G. Soares, A. E. Escargueil, J. A. P. Henriques, A. K. Larsen, and J. Saffi (2012)
Carcinogenesis 33, 1433-1440
   Abstract »    Full Text »    PDF »
DNA Transcription and Repair: A Confluence.
R. E. Moses and B. W. O'Malley (2012)
J. Biol. Chem. 287, 23266-23270
   Abstract »    Full Text »    PDF »
Histone ADP-Ribosylation Facilitates Gene Transcription by Directly Remodeling Nucleosomes.
R. Martinez-Zamudio and H. C. Ha (2012)
Mol. Cell. Biol. 32, 2490-2502
   Abstract »    Full Text »    PDF »
CHD1L: a new candidate gene for congenital anomalies of the kidneys and urinary tract (CAKUT).
A. Brockschmidt, B. Chung, S. Weber, D.-C. Fischer, M. Kolatsi-Joannou, L. Christ, A. Heimbach, D. Shtiza, G. Klaus, G. D. Simonetti, et al. (2012)
Nephrol. Dial. Transplant. 27, 2355-2364
   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 »
PARP-1 Inhibition as a Targeted Strategy to Treat Ewing's Sarcoma.
J. C. Brenner, F. Y. Feng, S. Han, S. Patel, S. V. Goyal, L. M. Bou-Maroun, M. Liu, R. Lonigro, J. R. Prensner, S. A. Tomlins, et al. (2012)
Cancer Res. 72, 1608-1613
   Abstract »    Full Text »    PDF »
SRY (sex determining region Y)-box2 (Sox2)/poly ADP-ribose polymerase 1 (Parp1) complexes regulate pluripotency.
Y.-S. Lai, C.-W. Chang, K. M. Pawlik, D. Zhou, M. B. Renfrow, and T. M. Townes (2012)
PNAS 109, 3772-3777
   Abstract »    Full Text »    PDF »
Fluorescence strategies for high-throughput quantification of protein interactions.
A. R. Hieb, S. D'Arcy, M. A. Kramer, A. E. White, and K. Luger (2012)
Nucleic Acids Res. 40, e33
   Abstract »    Full Text »    PDF »
On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1.
X. Luo and W. L. Kraus (2012)
Genes & Dev. 26, 417-432
   Abstract »    Full Text »    PDF »
The p65 subunit of NF-{kappa}B and PARP1 assist Snail1 in activating fibronectin transcription.
J. Stanisavljevic, M. Porta-de-la-Riva, R. Batlle, A. G. de Herreros, and J. Baulida (2011)
J. Cell Sci. 124, 4161-4171
   Abstract »    Full Text »    PDF »
QKI-Mediated Alternative Splicing of the Histone Variant MacroH2A1 Regulates Cancer Cell Proliferation.
L. Novikov, J. W. Park, H. Chen, H. Klerman, A. S. Jalloh, and M. J. Gamble (2011)
Mol. Cell. Biol. 31, 4244-4255
   Abstract »    Full Text »    PDF »
Epigenetic reprogramming in the germline: towards the ground state of the epigenome.
P. Hajkova (2011)
Phil Trans R Soc B 366, 2266-2273
   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 »
Metformin Induces Both Caspase-Dependent and Poly(ADP-ribose) Polymerase-Dependent Cell Death in Breast Cancer Cells.
Y. Zhuang and W. K. Miskimins (2011)
Mol. Cancer Res. 9, 603-615
   Abstract »    Full Text »    PDF »
Four enzymes cooperate to displace histone H1 during the first minute of hormonal gene activation.
G. P. Vicent, A. S. Nacht, J. Font-Mateu, G. Castellano, L. Gaveglia, C. Ballare, and M. Beato (2011)
Genes & Dev. 25, 845-862
   Abstract »    Full Text »    PDF »
Drosophila histone H2A variant (H2Av) controls poly(ADP-ribose) polymerase 1 (PARP1) activation in chromatin.
E. Kotova, N. Lodhi, M. Jarnik, A. D. Pinnola, Y. Ji, and A. V. Tulin (2011)
PNAS 108, 6205-6210
   Abstract »    Full Text »    PDF »
Double-stranded DNA Binding Domain of Poly(ADP-ribose) Polymerase-1 and Molecular Insight into the Regulation of Its Activity.
O. Huambachano, F. Herrera, A. Rancourt, and M. S. Satoh (2011)
J. Biol. Chem. 286, 7149-7160
   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 »
Poly(ADP-ribose) Polymerase-1 (PARP-1) Contributes to the Barrier Function of a Vertebrate Chromatin Insulator.
M. Aker, K. Bomsztyk, and D. W. Emery (2010)
J. Biol. Chem. 285, 37589-37597
   Abstract »    Full Text »    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 »
The KRAS Promoter Responds to Myc-associated Zinc Finger and Poly(ADP-ribose) Polymerase 1 Proteins, Which Recognize a Critical Quadruplex-forming GA-element.
S. Cogoi, M. Paramasivam, A. Membrino, K. K. Yokoyama, and L. E. Xodo (2010)
J. Biol. Chem. 285, 22003-22016
   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 »
Regulation of Epstein-Barr Virus OriP Replication by Poly(ADP-Ribose) Polymerase 1.
I. Tempera, Z. Deng, C. Atanasiu, C. J. Chen, M. D'Erme, and P. M. Lieberman (2010)
J. Virol. 84, 4988-4997
   Abstract »    Full Text »    PDF »
Poly ADP-ribose polymerase-1 and health.
J. B. Kirkland (2010)
Experimental Biology and Medicine 235, 561-568
   Abstract »    Full Text »    PDF »
Human sodium-iodide symporter (hNIS) gene expression is inhibited by a trans-active transcriptional repressor, NIS-repressor, containing PARP-1 in thyroid cancer cells.
W. Li and K. B. Ain (2010)
Endocr. Relat. Cancer 17, 383-398
   Abstract »    Full Text »    PDF »
Uncoupling of the transactivation and transrepression functions of PARP1 protein.
E. Kotova, M. Jarnik, and A. V. Tulin (2010)
PNAS 107, 6406-6411
   Abstract »    Full Text »    PDF »
Characterization of somatic cell nuclear reprogramming by oocytes in which a linker histone is required for pluripotency gene reactivation.
J. Jullien, C. Astrand, R. P. Halley-Stott, N. Garrett, and J. B. Gurdon (2010)
PNAS 107, 5483-5488
   Abstract »    Full Text »    PDF »
Mutational Analysis of the Poly(ADP-Ribosyl)ation Sites of the Transcription Factor CTCF Provides an Insight into the Mechanism of Its Regulation by Poly(ADP-Ribosyl)ation.
D. Farrar, S. Rai, I. Chernukhin, M. Jagodic, Y. Ito, S. Yammine, R. Ohlsson, A. Murrell, and E. Klenova (2010)
Mol. Cell. Biol. 30, 1199-1216
   Abstract »    Full Text »    PDF »
The histone variant macroH2A1 marks repressed autosomal chromatin, but protects a subset of its target genes from silencing.
M. J. Gamble, K. M. Frizzell, C. Yang, R. Krishnakumar, and W. L. Kraus (2010)
Genes & Dev. 24, 21-32
   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 »
Histone H1 binding is inhibited by histone variant H3.3.
U. Braunschweig, G. J. Hogan, L. Pagie, and B. van Steensel (2009)
EMBO J. 28, 3635-3645
   Abstract »    Full Text »    PDF »
PARP-1 transcriptional activity is regulated by sumoylation upon heat shock.
N. Martin, K. Schwamborn, V. Schreiber, A. Werner, C. Guillier, X.-D. Zhang, O. Bischof, J.-S. Seeler, and A. Dejean (2009)
EMBO J. 28, 3534-3548
   Abstract »    Full Text »    PDF »
PARP-1 Deficiency Increases the Severity of Disease in a Mouse Model of Multiple Sclerosis.
V. Selvaraj, M. M. Soundarapandian, O. Chechneva, A. J. Williams, M. K. Sidorov, A. M. Soulika, D. E. Pleasure, and W. Deng (2009)
J. Biol. Chem. 284, 26070-26084
   Abstract »    Full Text »    PDF »
The Paralogous Genes RADICAL-INDUCED CELL DEATH1 and SIMILAR TO RCD ONE1 Have Partially Redundant Functions during Arabidopsis Development.
S. Teotia and R. S. Lamb (2009)
Plant Physiology 151, 180-198
   Abstract »    Full Text »    PDF »
Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler.
A. J. Gottschalk, G. Timinszky, S. E. Kong, J. Jin, Y. Cai, S. K. Swanson, M. P. Washburn, L. Florens, A. G. Ladurner, J. W. Conaway, et al. (2009)
PNAS 106, 13770-13774
   Abstract »    Full Text »    PDF »
Poly-(ADP-Ribose) Polymerase-1 Is Necessary for Long-Term Facilitation in Aplysia.
A. I. Hernandez, J. Wolk, J.-Y. Hu, J. Liu, T. Kurosu, J. H. Schwartz, and S. Schacher (2009)
J. Neurosci. 29, 9553-9562
   Abstract »    Full Text »    PDF »
Enzymes in the NAD+ Salvage Pathway Regulate SIRT1 Activity at Target Gene Promoters.
T. Zhang, J. G. Berrocal, K. M. Frizzell, M. J. Gamble, M. E. DuMond, R. Krishnakumar, T. Yang, A. A. Sauve, and W. L. Kraus (2009)
J. Biol. Chem. 284, 20408-20417
   Abstract »    Full Text »    PDF »
Poly(ADP-ribose) Polymerase 1 Interacts with Nuclear Respiratory Factor 1 (NRF-1) and Plays a Role in NRF-1 Transcriptional Regulation.
M. B. Hossain, P. Ji, R. Anish, R. H. Jacobson, and S. Takada (2009)
J. Biol. Chem. 284, 8621-8632
   Abstract »    Full Text »    PDF »
Dynamic Histone H1 Isotype 4 Methylation and Demethylation by Histone Lysine Methyltransferase G9a/KMT1C and the Jumonji Domain-containing JMJD2/KDM4 Proteins.
P. Trojer, J. Zhang, M. Yonezawa, A. Schmidt, H. Zheng, T. Jenuwein, and D. Reinberg (2009)
J. Biol. Chem. 284, 8395-8405
   Abstract »    Full Text »    PDF »
Epigenetics: poly(ADP-ribosyl)ation of PARP-1 regulates genomic methylation patterns.
P. Caiafa, T. Guastafierro, and M. Zampieri (2009)
FASEB J 23, 672-678
   Abstract »    Full Text »    PDF »
Nucleosome repeat length and linker histone stoichiometry determine chromatin fiber structure.
A. Routh, S. Sandin, and D. Rhodes (2008)
PNAS 105, 8872-8877
   Abstract »    Full Text »    PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882