Skip to main content
SpringerLink
Log in

Regulation of Chromatin Structure and Function by PARP-1 and ADP-Ribosylation

  • Chapter
  • First Online:
Fundamentals of Chromatin

  • 2685 Accesses

Abstract

Poly(ADP-ribose) polymerase-1 (PARP-1) is an abundant nuclear enzyme that catalyzes the transfer of ADP-ribose units from nicotinamide adenine dinucleotide (NAD+) to a variety of target proteins to regulate their activities and functions. Numerous studies over the past three decades have uncovered a close functional relationship between PARP-1 and chromatin during gene regulation and DNA repair. Recent studies have begun to reveal the underlying mechanisms of this functional interplay, including the role of DNA structures, histone modifications and variants, the chromatin-regulating machinery, cellular signaling pathways, and specific features of PARP-1 itself. The picture of PARP-1 that has emerged is of a multifunctional chromatin regulatory protein that can serve as an interface between external and internal cues, and the fundamental processes that control the biology of the genome. These studies have increased our understanding of the roles of PARP-1 in physiological and pathological processes from stress responses and inflammation to metabolism and apoptosis. In this chapter, we discuss how PARP-1 and ADP-ribosylation regulate chromatin structure and function to control a variety of nuclear processes, as well as downstream biological responses.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adamietz P, Rudolph A (1984) ADP-ribosylation of nuclear proteins in vivo. Identification of histone H2B as a major acceptor for mono- and poly(ADP-ribose) in dimethyl sulfate-treated hepatoma AH 7974 cells. J Biol Chem 259(11):6841–6846

    PubMed  CAS  Google Scholar 

  • Ahel I, Ahel D, Matsusaka T, Clark AJ, Pines J, Boulton SJ, West SC (2008) Poly(ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins. Nature 451(7174):81–85

    PubMed  CAS  Google Scholar 

  • Ahel D, Horejsi Z, Wiechens N, Polo SE, Garcia-Wilson E, Ahel I, Flynn H, Skehel M, West SC, Jackson SP, Owen-Hughes T, Boulton SJ (2009) Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science 325(5945):1240–1243

    PubMed  CAS  Google Scholar 

  • Althaus FR, Hofferer L, Kleczkowska HE, Malanga M, Naegeli H, Panzeter PL, Realini CA (1994) Histone shuttling by poly ADP-ribosylation. Mol Cell Biochem 138(1–2):53–59

    PubMed  CAS  Google Scholar 

  • Altmeyer M, Messner S, Hassa P, Fey M, Hottiger M (2009) Molecular mechanism of poly(ADP-ribosyl)ation by PARP1 and identification of lysine residues as ADP-ribose acceptor sites. Nucleic Acids Res 37(11):3723–3738

    PubMed  CAS  Google Scholar 

  • Andersen JS, Lyon CE, Fox AH, Leung AK, Lam YW, Steen H, Mann M, Lamond AI (2002) Directed proteomic analysis of the human nucleolus. Curr Biol 12(1):1–11

    PubMed  Google Scholar 

  • Aravind L (2001) The WWE domain: a common interaction module in protein ubiquitination and ADP ribosylation. Trends Biochem Sci 26(5):273–275

    PubMed  CAS  Google Scholar 

  • Asher G, Reinke H, Altmeyer M, Gutierrez-Arcelus M, Hottiger MO, Schibler U (2010) Poly(ADP-ribose) polymerase 1 participates in the phase entrainment of circadian clocks to feeding. Cell 142(6):943–953

    PubMed  CAS  Google Scholar 

  • Bai P, Canto C, Oudart H, Brunyanszki A, Cen Y, Thomas C, Yamamoto H, Huber A, Kiss B, Houtkooper RH, Schoonjans K, Schreiber V, Sauve AA, Menissier-de Murcia J, Auwerx J (2011) PARP-1 inhibition increases mitochondrial metabolism through SIRT1 activation. Cell Metab 13(4):461–468

    PubMed  CAS  Google Scholar 

  • Barkess G, West AG (2012) Chromatin insulator elements: establishing barriers to set heterochromatin boundaries. Epigenomics 4(1):67–80

    PubMed  CAS  Google Scholar 

  • Bauer PI, Farkas G, Buday L, Mikala G, Meszaros G, Kun E, Farago A (1992) Inhibition of DNA binding by the phosphorylation of poly ADP-ribose polymerase protein catalysed by protein kinase C. Biochem Biophys Res Commun 187(2):730–736

    PubMed  CAS  Google Scholar 

  • Beckert S, Farrahi F, Perveen Ghani Q, Aslam R, Scheuenstuhl H, Coerper S, Konigsrainer A, Hunt TK, Hussain MZ (2006) IGF-I-induced VEGF expression in HUVEC involves phosphorylation and inhibition of poly(ADP-ribose)polymerase. Biochem Biophys Res Commun 341(1):67–72

    PubMed  CAS  Google Scholar 

  • Berger F, Lau C, Dahlmann M, Ziegler M (2005) Subcellular compartmentation and differential catalytic properties of the three human nicotinamide mononucleotide adenylyltransferase isoforms. J Biol Chem 280(43):36334–36341

    PubMed  CAS  Google Scholar 

  • Berger F, Lau C, Ziegler M (2007) Regulation of poly(ADP-ribose) polymerase 1 activity by the phosphorylation state of the nuclear NAD biosynthetic enzyme NMN adenylyl transferase 1. Proc Natl Acad Sci USA 104(10):3765–3770

    PubMed  CAS  Google Scholar 

  • Boamah EK, Kotova E, Garabedian M, Jarnik M, Tulin AV (2012) Poly(ADP-Ribose) polymerase 1 (PARP-1) regulates ribosomal biogenesis in Drosophila nucleoli. PLoS Genet 8(1):e1002442

    PubMed  CAS  Google Scholar 

  • Boisvert FM, van Koningsbruggen S, Navascues J, Lamond AI (2007) The multifunctional nucleolus. Nat Rev Mol Cell Biol 8(7):574–585

    PubMed  CAS  Google Scholar 

  • Bonicalzi ME, Vodenicharov M, Coulombe M, Gagne JP, Poirier GG (2003) Alteration of poly(ADP-ribose) glycohydrolase nucleocytoplasmic shuttling characteristics upon cleavage by apoptotic proteases. Biol Cell 95(9):635–644

    PubMed  CAS  Google Scholar 

  • Brockdorff N (2011) Chromosome silencing mechanisms in X-chromosome inactivation: unknown unknowns. Development 138(23):5057–5065

    PubMed  CAS  Google Scholar 

  • Buschbeck M, Di Croce L (2010) Approaching the molecular and physiological function of macroH2A variants. Epigenetics 5(2):118–123

    PubMed  CAS  Google Scholar 

  • Buschbeck M, Uribesalgo I, Wibowo I, Rue P, Martin D, Gutierrez A, Morey L, Guigo R, Lopez-Schier H, Di Croce L (2009) The histone variant macroH2A is an epigenetic regulator of key developmental genes. Nat Struct Mol Biol 16(10):1074–1079

    PubMed  CAS  Google Scholar 

  • Caiafa P, Zlatanova J (2009) CCCTC-binding factor meets poly(ADP-ribose) polymerase-1. J Cell Physiol 219(2):265–270

    PubMed  CAS  Google Scholar 

  • Caiafa P, Guastafierro T, Zampieri M (2009) Epigenetics: poly(ADP-ribosyl)ation of PARP-1 regulates genomic methylation patterns. FASEB J 23(3):672–678

    PubMed  CAS  Google Scholar 

  • Campos EI, Reinberg D (2009) Histones: annotating chromatin. Annu Rev Genet 43:559–599

    PubMed  CAS  Google Scholar 

  • Chan PK (1992) Characterization and cellular localization of nucleophosmin/B23 in HeLa cells treated with selected cytotoxic agents (studies of B23-translocation mechanism). Exp Cell Res 203(1):174–181

    PubMed  CAS  Google Scholar 

  • Changolkar LN, Pehrson JR (2006) macroH2A1 histone variants are depleted on active genes but concentrated on the inactive X chromosome. Mol Cell Biol 26(12):4410–4420

    PubMed  CAS  Google Scholar 

  • Ciccarone F, Klinger FG, Catizone A, Calabrese R, Zampieri M, Bacalini MG, De Felici M, Caiafa P (2012) Poly(ADP-ribosyl)ation acts in the DNA demethylation of mouse primordial germ cells also with DNA damage-independent roles. PLoS ONE 7(10):e46927

    PubMed  CAS  Google Scholar 

  • Cohen-Armon M, Visochek L, Rozensal D, Kalal A, Geistrikh I, Klein R, Bendetz-Nezer S, Yao Z, Seger R (2007) DNA-independent PARP-1 activation by phosphorylated ERK2 increases Elk1 activity: a link to histone acetylation. Mol Cell 25(2):297–308

    PubMed  CAS  Google Scholar 

  • Corona DF, Tamkun JW (2004) Multiple roles for ISWI in transcription, chromosome organization and DNA replication. Biochim Biophys Acta 1677(1–3):113–119

    PubMed  CAS  Google Scholar 

  • Corona DF, Siriaco G, Armstrong JA, Snarskaya N, McClymont SA, Scott MP, Tamkun JW (2007) ISWI regulates higher-order chromatin structure and histone H1 assembly in vivo. PLoS Biol 5(9):e232

    PubMed  Google Scholar 

  • Costanzi C, Stein P, Worrad DM, Schultz RM, Pehrson JR (2000) Histone macroH2A1 is concentrated in the inactive X chromosome of female preimplantation mouse embryos. Development 127(11):2283–2289

    PubMed  CAS  Google Scholar 

  • D’Amours D, Desnoyers S, D’Silva I, Poirier GG (1999) Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J 342(Pt 2):249–268

    PubMed  Google Scholar 

  • Davidovic L, Vodenicharov M, Affar EB, Poirier GG (2001) Importance of poly(ADP-ribose) glycohydrolase in the control of poly(ADP-ribose) metabolism. Exp Cell Res 268(1):7–13

    PubMed  CAS  Google Scholar 

  • de Capoa A, Febbo FR, Giovannelli F, Niveleau A, Zardo G, Marenzi S, Caiafa P (1999) Reduced levels of poly(ADP-ribosyl)ation result in chromatin compaction and hypermethylation as shown by cell-by-cell computer-assisted quantitative analysis. FASEB J 13(1):89–93

    PubMed  Google Scholar 

  • Desnoyers S, Kaufmann SH, Poirier GG (1996) Alteration of the nucleolar localization of poly(ADP-ribose) polymerase upon treatment with transcription inhibitors. Exp Cell Res 227(1):146–153

    PubMed  CAS  Google Scholar 

  • Devalaraja-Narashimha K, Padanilam BJ (2010) PARP1 deficiency exacerbates diet-induced obesity in mice. J Endocrinol 205(3):243–252

    PubMed  CAS  Google Scholar 

  • Doege CA, Inoue K, Yamashita T, Rhee DB, Travis S, Fujita R, Guarnieri P, Bhagat G, Vanti WB, Shih A, Levine RL, Nik S, Chen EI, Abeliovich A (2012) Early-stage epigenetic modification during somatic cell reprogramming by Parp1 and Tet2. Nature 488(7413):652–655

    PubMed  CAS  Google Scholar 

  • Dunn KL, Davie JR (2003) The many roles of the transcriptional regulator CTCF. Biochem Cell Biol 81(3):161–167

    PubMed  CAS  Google Scholar 

  • Frizzell KM, Gamble MJ, Berrocal JG, Zhang T, Krishnakumar R, Cen Y, Sauve AA, Kraus WL (2009) Global analysis of transcriptional regulation by poly(ADP-ribose) polymerase-1 and poly(ADP-ribose) glycohydrolase in MCF-7 human breast cancer cells. J Biol Chem 284(49):33926–33938

    PubMed  CAS  Google Scholar 

  • Gagne JP, Isabelle M, Lo KS, Bourassa S, Hendzel MJ, Dawson VL, Dawson TM, Poirier GG (2008) Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADP-ribose)-associated protein complexes. Nucleic Acids Res 36(22):6959–6976

    PubMed  CAS  Google Scholar 

  • Gamble MJ, Kraus WL (2010) Multiple facets of the unique histone variant macroH2A: from genomics to cell biology. Cell Cycle 9(13):2568–2574

    PubMed  CAS  Google Scholar 

  • Gamble MJ, Frizzell KM, Yang C, Krishnakumar R, Kraus WL (2010) The histone variant macroH2A1 marks repressed autosomal chromatin, but protects a subset of its target genes from silencing. Genes Dev 24(1):21–32

    PubMed  CAS  Google Scholar 

  • Gibson BA, Kraus WL (2012) New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat Rev Mol Cell Biol 13(7):411–424

    PubMed  CAS  Google Scholar 

  • Gottschalk AJ, Timinszky G, Kong SE, Jin J, Cai Y, Swanson SK, Washburn MP, Florens L, Ladurner AG, Conaway JW, Conaway RC (2009) Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler. Proc Natl Acad Sci USA 106(33):13770–13774

    PubMed  CAS  Google Scholar 

  • Griesenbeck J, Ziegler M, Tomilin N, Schweiger M, Oei SL (1999) Stimulation of the catalytic activity of poly(ADP-ribosyl) transferase by transcription factor Yin Yang 1. FEBS Lett 443(1):20–24

    PubMed  CAS  Google Scholar 

  • Guetg C, Santoro R (2012) Noncoding RNAs link PARP1 to heterochromatin. Cell Cycle 11(12):2217–2218

    PubMed  CAS  Google Scholar 

  • Guetg C, Scheifele F, Rosenthal F, Hottiger MO, Santoro R (2012) Inheritance of silent rDNA chromatin is mediated by PARP1 via noncoding RNA. Mol Cell 45(6):790–800

    PubMed  CAS  Google Scholar 

  • Hassa PO, Haenni SS, Buerki C, Meier NI, Lane WS, Owen H, Gersbach M, Imhof R, Hottiger MO (2005) Acetylation of poly(ADP-ribose) polymerase-1 by p300/CREB-binding protein regulates coactivation of NF-kappaB-dependent transcription. J Biol Chem 280(49):40450–40464

    PubMed  CAS  Google Scholar 

  • Hottiger MO, Hassa PO, Luscher B, Schuler H, Koch-Nolte F (2010) Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem Sci 35(4):208–219

    PubMed  CAS  Google Scholar 

  • Huletsky A, Niedergang C, Frechette A, Aubin R, Gaudreau A, Poirier GG (1985) Sequential ADP-ribosylation pattern of nucleosomal histones. ADP-ribosylation of nucleosomal histones. Eur J Biochem 146(2):277–285

    PubMed  CAS  Google Scholar 

  • Huletsky A, de Murcia G, Muller S, Hengartner M, Menard L, Lamarre D, Poirier GG (1989) The effect of poly(ADP-ribosyl)ation on native and H1-depleted chromatin. A role of poly(ADP-ribosyl)ation on core nucleosome structure. J Biol Chem 264(15):8878–8886

    PubMed  CAS  Google Scholar 

  • Ji Y, Tulin AV (2010) The roles of PARP1 in gene control and cell differentiation. Curr Opin Genet Dev 20(5):512–518

    PubMed  CAS  Google Scholar 

  • Ju BG, Solum D, Song EJ, Lee KJ, Rose DW, Glass CK, Rosenfeld MG (2004) Activating the PARP-1 sensor component of the groucho/TLE1 corepressor complex mediates a CaMKinase IIdelta-dependent neurogenic gene activation pathway. Cell 119(6):815–829

    PubMed  CAS  Google Scholar 

  • Ju BG, Lunyak VV, Perissi V, Garcia-Bassets I, Rose DW, Glass CK, Rosenfeld MG (2006) A topoisomerase IIbeta-mediated dsDNA break required for regulated transcription. Science 312(5781):1798–1802

    PubMed  CAS  Google Scholar 

  • Karras GI, Kustatscher G, Buhecha HR, Allen MD, Pugieux C, Sait F, Bycroft M, Ladurner AG (2005) The macro domain is an ADP-ribose binding module. EMBO J 24(11):1911–1920

    PubMed  CAS  Google Scholar 

  • Kauppinen TM, Chan WY, Suh SW, Wiggins AK, Huang EJ, Swanson RA (2006) Direct phosphorylation and regulation of poly(ADP-ribose) polymerase-1 by extracellular signal-regulated kinases 1/2. Proc Natl Acad Sci USA 103(18):7136–7141

    PubMed  CAS  Google Scholar 

  • Kim MY, Mauro S, Gevry N, Lis JT, Kraus WL (2004) NAD+-dependent modulation of chromatin structure and transcription by nucleosome binding properties of PARP-1. Cell 119(6):803–814

    PubMed  CAS  Google Scholar 

  • Kim MY, Zhang T, Kraus WL (2005) Poly(ADP-ribosyl)ation by PARP-1: ‘PAR-laying’ NAD+ into a nuclear signal. Genes Dev 19(17):1951–1967

    PubMed  CAS  Google Scholar 

  • Kolthur-Seetharam U, Dantzer F, McBurney MW, de Murcia G, Sassone-Corsi P (2006) Control of AIF-mediated cell death by the functional interplay of SIRT1 and PARP-1 in response to DNA damage. Cell Cycle 5(8):873–877

    PubMed  CAS  Google Scholar 

  • Kotova E, Jarnik M, Tulin AV (2009) Poly (ADP-ribose) polymerase 1 is required for protein localization to Cajal body. PLoS Genet 5(2):e1000387

    PubMed  Google Scholar 

  • Kotova E, Lodhi N, Jarnik M, Pinnola AD, Ji Y, Tulin AV (2011) Drosophila histone H2A variant (H2Av) controls poly(ADP-ribose) polymerase 1 (PARP1) activation in chromatin. Proc Natl Acad Sci USA 108(15):6205–6210

    PubMed  CAS  Google Scholar 

  • Kowalski A, Palyga J (2012) Linker histone subtypes and their allelic variants. Cell Biol Int 36(11):981–996

    PubMed  CAS  Google Scholar 

  • Kraus WL (2008) Transcriptional control by PARP-1: chromatin modulation, enhancer-binding, coregulation, and insulation. Curr Opin Cell Biol 20(3):294–302

    PubMed  CAS  Google Scholar 

  • Kraus WL, Lis JT (2003) PARP goes transcription. Cell 113(6):677–683

    PubMed  CAS  Google Scholar 

  • Kreimeyer A, Wielckens K, Adamietz P, Hilz H (1984) DNA repair-associated ADP-ribosylation in vivo. Modification of histone H1 differs from that of the principal acceptor proteins. J Biol Chem 259(2):890–896

    PubMed  CAS  Google Scholar 

  • Krishnakumar R, Kraus WL (2010a) The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol Cell 39(1):8–24

    PubMed  CAS  Google Scholar 

  • Krishnakumar R, Kraus WL (2010b) PARP-1 regulates chromatin structure and transcription through a KDM5B-dependent pathway. Mol Cell 39(5):736–749

    PubMed  CAS  Google Scholar 

  • Krishnakumar R, Gamble MJ, Frizzell KM, Berrocal JG, Kininis M, Kraus WL (2008) Reciprocal binding of PARP-1 and histone H1 at promoters specifies transcriptional outcomes. Science 319(5864):819–821

    PubMed  CAS  Google Scholar 

  • Langelier MF, Servent KM, Rogers EE, Pascal JM (2008) A third zinc-binding domain of human poly(ADP-ribose) polymerase-1 coordinates DNA-dependent enzyme activation. J Biol Chem 283(7):4105–4114

    PubMed  CAS  Google Scholar 

  • Langelier MF, Planck JL, Roy S, Pascal JM (2012) Structural basis for DNA damage-dependent poly(ADP-ribosyl)ation by human PARP-1. Science 336(6082):728–732

    PubMed  CAS  Google Scholar 

  • Langst G, Becker PB (2001) Nucleosome mobilization and positioning by ISWI-containing chromatin-remodeling factors. J Cell Sci 114(Pt 14):2561–2568

    PubMed  CAS  Google Scholar 

  • Li B, Carey M, Workman JL (2007) The role of chromatin during transcription. Cell 128(4):707–719

    PubMed  CAS  Google Scholar 

  • Loeffler PA, Cuneo MJ, Mueller GA, DeRose EF, Gabel SA, London RE (2011) Structural studies of the PARP-1 BRCT domain. BMC Struct Biol 11:37

    PubMed  CAS  Google Scholar 

  • Luo X, Kraus WL (2011) A one and a two … expanding roles for poly(ADP-ribose) polymerases in metabolism. Cell Metab 13(4):353–355

    PubMed  CAS  Google Scholar 

  • Luo X, Kraus WL (2012) On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev 26(5):417–432

    PubMed  Google Scholar 

  • Martinez-Zamudio R, Ha HC (2012) Histone ADP-ribosylation facilitates gene transcription by directly remodeling nucleosomes. Mol Cell Biol 32(13):2490–2502

    PubMed  CAS  Google Scholar 

  • Mathis G, Althaus FR (1987) Release of core DNA from nucleosomal core particles following (ADP-ribose)n-modification in vitro. Biochem Biophys Res Commun 143(3):1049–1054

    PubMed  CAS  Google Scholar 

  • Mayer C, Schmitz KM, Li J, Grummt I, Santoro R (2006) Intergenic transcripts regulate the epigenetic state of rRNA genes. Mol Cell 22(3):351–361

    PubMed  CAS  Google Scholar 

  • Meder VS, Boeglin M, de Murcia G, Schreiber V (2005) PARP-1 and PARP-2 interact with nucleophosmin/B23 and accumulate in transcriptionally active nucleoli. J Cell Sci 118(Pt 1):211–222

    PubMed  CAS  Google Scholar 

  • Menissier de Murcia J, Ricoul M, Tartier L, Niedergang C, Huber A, Dantzer F, Schreiber V, Ame JC, Dierich A, LeMeur M, Sabatier L, Chambon P, de Murcia G (2003) Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. EMBO J 22(9):2255–2263

    PubMed  CAS  Google Scholar 

  • Murawska M, Hassler M, Renkawitz-Pohl R, Ladurner A, Brehm A (2011) Stress-induced PARP activation mediates recruitment of Drosophila Mi-2 to promote heat shock gene expression. PLoS Genet 7(7):e1002206

    PubMed  CAS  Google Scholar 

  • Nusinow DA, Hernandez-Munoz I, Fazzio TG, Shah GM, Kraus WL, Panning B (2007) Poly(ADP-ribose) polymerase 1 is inhibited by a histone H2A variant, MacroH2A, and contributes to silencing of the inactive X chromosome. J Biol Chem 282(17):12851–12859

    PubMed  CAS  Google Scholar 

  • Ogata N, Ueda K, Kawaichi M, Hayaishi O (1981) Poly(ADP-ribose) synthetase, a main acceptor of poly(ADP-ribose) in isolated nuclei. J Biol Chem 256(9):4135–4137

    PubMed  CAS  Google Scholar 

  • Ohashi S, Kanai M, Hanai S, Uchiumi F, Maruta H, Tanuma S, Miwa M (2003) Subcellular localization of poly(ADP-ribose) glycohydrolase in mammalian cells. Biochem Biophys Res Commun 307(4):915–921

    PubMed  CAS  Google Scholar 

  • Oliver FJ, Menissier-de Murcia J, Nacci C, Decker P, Andriantsitohaina R, Muller S, de la Rubia G, Stoclet JC, de Murcia G (1999) Resistance to endotoxic shock as a consequence of defective NF-kappaB activation in poly (ADP-ribose) polymerase-1 deficient mice. EMBO J 18(16):4446–4454

    PubMed  CAS  Google Scholar 

  • Pavri R, Lewis B, Kim TK, Dilworth FJ, Erdjument-Bromage H, Tempst P, de Murcia G, Evans R, Chambon P, Reinberg D (2005) PARP-1 determines specificity in a retinoid signaling pathway via direct modulation of mediator. Mol Cell 18(1):83–96

    PubMed  CAS  Google Scholar 

  • Petesch SJ, Lis JT (2008) Rapid, transcription-independent loss of nucleosomes over a large chromatin domain at Hsp70 loci. Cell 134(1):74–84

    PubMed  CAS  Google Scholar 

  • Petesch SJ, Lis JT (2012a) Activator-induced spread of poly(ADP-ribose) polymerase promotes nucleosome loss at Hsp70. Mol Cell 45(1):64–74

    PubMed  CAS  Google Scholar 

  • Petesch SJ, Lis JT (2012b) Overcoming the nucleosome barrier during transcript elongation. Trends Genet 28(6):285–294

    PubMed  CAS  Google Scholar 

  • Poirier GG, de Murcia G, Jongstra-Bilen J, Niedergang C, Mandel P (1982) Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure. Proc Natl Acad Sci USA 79(11):3423–3427

    PubMed  CAS  Google Scholar 

  • Rapizzi E, Fossati S, Moroni F, Chiarugi A (2004) Inhibition of poly(ADP-ribose) glycohydrolase by gallotannin selectively up-regulates expression of proinflammatory genes. Mol Pharmacol 66(4):890–898

    PubMed  CAS  Google Scholar 

  • Reale A, Matteis GD, Galleazzi G, Zampieri M, Caiafa P (2005) Modulation of DNMT1 activity by ADP-ribose polymers. Oncogene 24(1):13–19

    PubMed  CAS  Google Scholar 

  • Realini CA, Althaus FR (1992) Histone shuttling by poly(ADP-ribosylation). J Biol Chem 267(26):18858–18865

    PubMed  CAS  Google Scholar 

  • Redon C, Pilch D, Rogakou E, Sedelnikova O, Newrock K, Bonner W (2002) Histone H2A variants H2AX and H2AZ. Curr Opin Genet Dev 12(2):162–169

    PubMed  CAS  Google Scholar 

  • Robertson KD (2002) DNA methylation and chromatin—unraveling the tangled web. Oncogene 21(35):5361–5379

    PubMed  CAS  Google Scholar 

  • Sala A, La Rocca G, Burgio G, Kotova E, Di Gesu D, Collesano M, Ingrassia AM, Tulin AV, Corona DF (2008) The nucleosome-remodeling ATPase ISWI is regulated by poly-ADP-ribosylation. PLoS Biol 6(10):e252

    PubMed  Google Scholar 

  • Santos-Rosa H, Caldas C (2005) Chromatin modifier enzymes, the histone code and cancer. Eur J Cancer 41(16):2381–2402

    PubMed  CAS  Google Scholar 

  • Scherl A, Coute Y, Deon C, Calle A, Kindbeiter K, Sanchez JC, Greco A, Hochstrasser D, Diaz JJ (2002) Functional proteomic analysis of human nucleolus. Mol Biol Cell 13(11):4100–4109

    PubMed  CAS  Google Scholar 

  • Schreiber V, Dantzer F, Ame JC, de Murcia G (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 7(7):517–528

    PubMed  CAS  Google Scholar 

  • Sif S (2004) ATP-dependent nucleosome remodeling complexes: enzymes tailored to deal with chromatin. J Cell Biochem 91(6):1087–1098

    PubMed  CAS  Google Scholar 

  • Svedruzic ZM (2008) Mammalian cytosine DNA methyltransferase Dnmt1: enzymatic mechanism, novel mechanism-based inhibitors, and RNA-directed DNA methylation. Curr Med Chem 15(1):92–106

    PubMed  CAS  Google Scholar 

  • Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, Rao A (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324(5929):930–935

    PubMed  CAS  Google Scholar 

  • Timinszky G, Till S, Hassa PO, Hothorn M, Kustatscher G, Nijmeijer B, Colombelli J, Altmeyer M, Stelzer EH, Scheffzek K, Hottiger MO, Ladurner AG (2009) A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat Struct Mol Biol 16(9):923–929

    PubMed  CAS  Google Scholar 

  • Tulin A, Spradling A (2003) Chromatin loosening by poly(ADP)-ribose polymerase (PARP) at Drosophila puff loci. Science 299(5606):560–562

    PubMed  CAS  Google Scholar 

  • Tulin A, Stewart D, Spradling AC (2002) The Drosophila heterochromatic gene encoding poly(ADP-ribose) polymerase (PARP) is required to modulate chromatin structure during development. Genes Dev 16(16):2108–2119

    PubMed  CAS  Google Scholar 

  • Wacker DA, Ruhl DD, Balagamwala EH, Hope KM, Zhang T, Kraus WL (2007) The DNA binding and catalytic domains of poly(ADP-ribose) polymerase 1 cooperate in the regulation of chromatin structure and transcription. Mol Cell Biol 27(21):7475–7485

    PubMed  CAS  Google Scholar 

  • Wang ZQ, Auer B, Stingl L, Berghammer H, Haidacher D, Schweiger M, Wagner EF (1995) Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease. Genes Dev 9(5):509–520

    PubMed  CAS  Google Scholar 

  • Wang Z, Michaud GA, Cheng Z, Zhang Y, Hinds TR, Fan E, Cong F, Xu W (2012) Recognition of the iso-ADP-ribose moiety in poly(ADP-ribose) by WWE domains suggests a general mechanism for poly(ADP-ribosyl)ation-dependent ubiquitination. Genes Dev 26(3):235–240

    PubMed  Google Scholar 

  • Wesierska-Gadek J, Sauermann G (1988) The effect of poly(ADP-ribose) on interactions of DNA with histones H1, H3 and H4. Eur J Biochem 173(3):675–679

    PubMed  CAS  Google Scholar 

  • Williams K, Christensen J, Helin K (2012) DNA methylation: TET proteins-guardians of CpG islands? EMBO Rep 13(1):28–35

    CAS  Google Scholar 

  • Wolffe AP, Guschin D (2000) Review: chromatin structural features and targets that regulate transcription. J Struct Biol 129(2–3):102–122

    PubMed  CAS  Google Scholar 

  • Woodcock CL, Skoultchi AI, Fan Y (2006) Role of linker histone in chromatin structure and function: H1 stoichiometry and nucleosome repeat length. Chromosome Res 14(1):17–25

    PubMed  CAS  Google Scholar 

  • Wright RH, Castellano G, Bonet J, Le Dily F, Font-Mateu J, Ballare C, Nacht AS, Soronellas D, Oliva B, Beato M (2012) CDK2-dependent activation of PARP-1 is required for hormonal gene regulation in breast cancer cells. Genes Dev 26(17):1972–1983

    PubMed  CAS  Google Scholar 

  • Wu H, Zhang Y (2011) Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation. Genes Dev 25(23):2436–2452

    PubMed  CAS  Google Scholar 

  • Yu W, Ginjala V, Pant V, Chernukhin I, Whitehead J, Docquier F, Farrar D, Tavoosidana G, Mukhopadhyay R, Kanduri C, Oshimura M, Feinberg AP, Lobanenkov V, Klenova E, Ohlsson R (2004) Poly(ADP-ribosyl)ation regulates CTCF-dependent chromatin insulation. Nat Genet 36(10):1105–1110

    PubMed  CAS  Google Scholar 

  • Yusufzai TM, Tagami H, Nakatani Y, Felsenfeld G (2004) CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Mol Cell 13(2):291–298

    PubMed  CAS  Google Scholar 

  • Zampieri M, Passananti C, Calabrese R, Perilli M, Corbi N, De Cave F, Guastafierro T, Bacalini MG, Reale A, Amicosante G, Calabrese L, Zlatanova J, Caiafa P (2009) Parp1 localizes within the Dnmt1 promoter and protects its unmethylated state by its enzymatic activity. PLoS ONE 4(3)

    Google Scholar 

  • Zampieri M, Guastafierro T, Calabrese R, Ciccarone F, Bacalini MG, Reale A, Perilli M, Passananti C, Caiafa P (2012) ADP-ribose polymers localized on Ctcf-Parp1-Dnmt1 complex prevent methylation of Ctcf target sites. Biochem J 441(2):645–652

    PubMed  CAS  Google Scholar 

  • Zardo G, Caiafa P (1998) The unmethylated state of CpG islands in mouse fibroblasts depends on the poly(ADP-ribosyl)ation process. J Biol Chem 273(26):16517–16520

    PubMed  CAS  Google Scholar 

  • Zhang T, Kraus WL (2010) SIRT1-dependent regulation of chromatin and transcription: linking NAD(+) metabolism and signaling to the control of cellular functions. Biochim Biophys Acta 1804(8):1666–1675

    PubMed  CAS  Google Scholar 

  • Zhang S, Lin Y, Kim YS, Hande MP, Liu ZG, Shen HM (2007) c-Jun N-terminal kinase mediates hydrogen peroxide-induced cell death via sustained poly(ADP-ribose) polymerase-1 activation. Cell Death Differ 14(5):1001–1010

    PubMed  CAS  Google Scholar 

  • Zhang T, Berrocal JG, Yao J, DuMond ME, Krishnakumar R, Ruhl DD, Ryu KW, Gamble MJ, Kraus WL (2012) Regulation of poly(ADP-ribose) polymerase-1-dependent gene expression through promoter-directed recruitment of a nuclear NAD+ synthase. J Biol Chem 287(15):12405–12416

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. The Laboratory of Signaling and Gene Regulation, Cecil H. and Ida Green Center for Reproductive Biology Sciences, The University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX, 75390-8511, USA

    Ziying Liu & W. Lee Kraus Ph.D.

  2. Division of Basic Research, Department of Obstetrics and Gynecology, University of Texas Southwestern Medical Center, Dallas, TX, 75390, USA

    Ziying Liu & W. Lee Kraus Ph.D.

Authors
  1. Ziying Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. W. Lee Kraus Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to W. Lee Kraus Ph.D. .

Editor information

Editors and Affiliations

  1. Stowers Institute for Medical Research, Kansas City, Missouri, USA

    Jerry L. Workman

  2. Stowers Institute for Medical Research, Kansas City, Missouri, USA

    Susan M. Abmayr

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Liu, Z., Kraus, W.L. (2014). Regulation of Chromatin Structure and Function by PARP-1 and ADP-Ribosylation. In: Workman, J., Abmayr, S. (eds) Fundamentals of Chromatin. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8624-4_7

Download citation

Publish with us

Policies and ethics

Search

Navigation