The PARP superfamily

Poly(ADP‐ribosyl)ation is an immediate DNA‐damage‐dependent post‐translational modification of histones and other nuclear proteins that contributes to the survival of injured proliferating cells. Poly(ADP‐ribose) polymerases (PARPs) now constitute a large family of 18 proteins, encoded by different genes and displaying a conserved catalytic domain in which PARP‐1 (113 kDa), the founding member, and PARP‐2 (62 kDa) are so far the sole enzymes whose catalytic activity has been shown to be immediately stimulated by DNA strand breaks. A large repertoire of sequences encoding novel PARPs now extends considerably the field of poly(ADP‐ribosyl)ation reactions to various aspects of the cell biology including cell proliferation and cell death. Some of these new members interact with each other, share common partners and common subcellular localizations suggesting possible fine tuning in the regulation of this post‐translational modification of proteins. This review summarizes our present knowledge of this emerging superfamily, which might ultimately improve pharmacological strategies to enhance both antitumor efficacy and the treatment of a number of inflammatory and neurodegenerative disorders. A provisional nomenclature is proposed. BioEssays 26:882–893, 2004. © 2004 Wiley Periodicals, Inc.

[1]  R. Andriantsitohaina,et al.  Resistance to endotoxic shock as a consequence of defective NF‐κB activation in poly (ADP‐ribose) polymerase‐1 deficient mice , 1999, The EMBO journal.

[2]  F. Apiou,et al.  PARP-2, A Novel Mammalian DNA Damage-dependent Poly(ADP-ribose) Polymerase* , 1999, The Journal of Biological Chemistry.

[3]  G. Melillo.  HIF-1: A Target For Cancer, Ischemia and Inflammation—Too Good to be True? , 2004, Cell cycle.

[4]  L. Shaffer,et al.  Poly(ADP-ribose) polymerase at active centromeres and neocentromeres at metaphase. , 2000, Human molecular genetics.

[5]  M. Malanga,et al.  Poly(ADP-ribose) Reactivates Stalled DNA Topoisomerase I and Induces DNA Strand Break Resealing* , 2004, Journal of Biological Chemistry.

[6]  Alan E. Tomkinson,et al.  Physical and Functional Interaction between DNA Ligase IIIα and Poly(ADP-Ribose) Polymerase 1 in DNA Single-Strand Break Repair , 2003, Molecular and Cellular Biology.

[7]  G. Kroemer,et al.  Mitochondria, AIF and caspases — rivaling for cell death execution , 2003, Nature Cell Biology.

[8]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[9]  J. Vonesch,et al.  PARP-3 localizes preferentially to the daughter centriole and interferes with the G1/S cell cycle progression , 2003, Journal of Cell Science.

[10]  A. Bürkle.  Physiology and pathophysiology of poly(ADP‐ribosyl)ation * , 2001, BioEssays : news and reviews in molecular, cellular and developmental biology.

[11]  G. Falck,et al.  Segregation of sex chromosomes in human lymphocytes. , 2000, Mutagenesis.

[12]  A. Yasui,et al.  Spatial and Temporal Cellular Responses to Single-Strand Breaks in Human Cells , 2003, Molecular and Cellular Biology.

[13]  P. Chambon,et al.  Requirement of poly(ADP-ribose) polymerase in recovery from DNA damage in mice and in cells. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Susan Smith,et al.  TRF1 is degraded by ubiquitin-mediated proteolysis after release from telomeres. , 2003, Genes & development.

[15]  Q. Ma,et al.  TCDD-inducible poly(ADP-ribose) polymerase: a novel response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. , 2001, Biochemical and biophysical research communications.

[16]  Oscar Fernandez-Capetillo,et al.  Focusing on Foci: H2AX and the Recruitment of DNA-Damage Response Factors , 2003, Cell cycle.

[17]  H. Lodish,et al.  Tankyrase-2 oligomerizes with tankyrase-1 and binds to both TRF1 (telomere-repeat-binding factor 1) and IRAP (insulin-responsive aminopeptidase). , 2002, The Biochemical journal.

[18]  P. Stiegler,et al.  Poly(ADP-ribose) polymerase-1 dimerizes at a 5' recessed DNA end in vitro: a fluorescence study. , 2003, Biochemistry.

[19]  Jong-Wan Park,et al.  Role of apoptosis-inducing factor in myocardial cell death by ischemia-reperfusion. , 2003, Biochemical and biophysical research communications.

[20]  Laurence H Pearl,et al.  Crystal structure of the catalytic fragment of murine poly(ADP-ribose) polymerase-2. , 2002, Nucleic acids research.

[21]  G. Poirier,et al.  Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. , 1999, The Biochemical journal.

[22]  Zhao-Qi Wang,et al.  Involvement of Poly(ADP-Ribose) Polymerase 1 and Poly(ADP-Ribosyl)ation in Regulation of Centrosome Function , 2003, Molecular and Cellular Biology.

[23]  J. M. Murcia,et al.  Poly(ADP-ribose) polymerase: a molecular nick-sensor. , 1994, Trends in biochemical sciences.

[24]  P. Mandel,et al.  Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[25]  L. Shaffer,et al.  Poly(ADP-ribose) polymerase 2 localizes to mammalian active centromeres and interacts with PARP-1, Cenpa, Cenpb and Bub3, but not Cenpc. , 2002, Human molecular genetics.

[26]  J. Bae,et al.  Tankyrase 1 Interacts with Mcl-1 Proteins and Inhibits Their Regulation of Apoptosis* , 2003, The Journal of Biological Chemistry.

[27]  W. Theurkauf,et al.  Drosophila Checkpoint Kinase 2 Couples Centrosome Function and Spindle Assembly to Genomic Integrity , 2003, Cell.

[28]  J. Ménissier-de murcia,et al.  DNA repair defect in poly(ADP-ribose) polymerase-deficient cell lines. , 1998, Nucleic acids research.

[29]  S. Shall,et al.  From DNA damage and stress signalling to cell death : poly-ADP-ribosylation reactions , 2000 .

[30]  T. Tsuruo,et al.  Functional Subdomain in the Ankyrin Domain of Tankyrase 1 Required for Poly(ADP-Ribosyl)ation of TRF1 and Telomere Elongation , 2004, Molecular and Cellular Biology.

[31]  E. Wagner,et al.  PARP is important for genomic stability but dispensable in apoptosis. , 1997, Genes & development.

[32]  T. Ochiya,et al.  Poly(ADP-ribose) polymerase gene disruption conferred mice resistant to streptozotocin-induced diabetes. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[33]  L. Aravind.  The WWE domain: a common interaction module in protein ubiquitination and ADP ribosylation. , 2001, Trends in biochemical sciences.

[34]  J. Ménissier-de murcia,et al.  Local DNA damage by proton microbeam irradiation induces poly(ADP-ribose) synthesis in mammalian cells. , 2003, Mutagenesis.

[35]  S. Hanai,et al.  Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in Drosophila melanogaster , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[36]  S. Petrucco.  Sensing DNA damage by PARP-like fingers. , 2003, Nucleic acids research.

[37]  V. Kickhoefer,et al.  The 193-Kd Vault Protein, Vparp, Is a Novel Poly(Adp-Ribose) Polymerase , 1999, The Journal of cell biology.

[38]  Samuel H. Wilson,et al.  DNA Polymerase (cid:1) -mediated Long Patch Base Excision Repair POLY(ADP-RIBOSE) POLYMERASE-1 STIMULATES STRAND DISPLACEMENT DNA SYNTHESIS* , 2022 .

[39]  R. Aguiar,et al.  BAL is a novel risk-related gene in diffuse large B-cell lymphomas that enhances cellular migration. , 2000, Blood.

[40]  V. Schreiber,et al.  Base excision repair is impaired in mammalian cells lacking Poly(ADP-ribose) polymerase-1. , 2000, Biochemistry.

[41]  K. Caldecott.  XRCC1 and DNA strand break repair. , 2003, DNA repair.

[42]  P. Chambon,et al.  Functional interaction between PARP‐1 and PARP‐2 in chromosome stability and embryonic development in mouse , 2003, The EMBO journal.

[43]  N. Davidson,et al.  Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. , 1993, Cancer research.

[44]  E. Gilson,et al.  Functional Interaction between Poly(ADP-Ribose) Polymerase 2 (PARP-2) and TRF2: PARP Activity Negatively Regulates TRF2 , 2004, Molecular and Cellular Biology.

[45]  E. Le Cam,et al.  Conformational analysis of a 139 base-pair DNA fragment containing a single-stranded break and its interaction with human poly(ADP-ribose) polymerase. , 1994, Journal of molecular biology.

[46]  E. Koonin,et al.  SAP - a putative DNA-binding motif involved in chromosomal organization. , 2000, Trends in biochemical sciences.

[47]  A. Spradling,et al.  Chromatin Loosening by Poly(ADP)-Ribose Polymerase (PARP) at Drosophila Puff Loci , 2003, Science.

[48]  V. Kickhoefer,et al.  Vault Poly(ADP-Ribose) Polymerase Is Associated with Mammalian Telomerase and Is Dispensable for Telomerase Function and Vault Structure In Vivo , 2004, Molecular and Cellular Biology.

[49]  T. Lange,et al.  Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. , 1998, Science.

[50]  A. Saxena,et al.  Centromere Proteins Cenpa, Cenpb, and Bub3 Interact with Poly(ADP-ribose) Polymerase-1 Protein and Are Poly(ADP-ribosyl)ated* , 2002, The Journal of Biological Chemistry.

[51]  J. Gagné,et al.  Analysis of ADP-ribose polymer sizes in intact cells , 2001, Molecular and Cellular Biochemistry.

[52]  M. Mark,et al.  Early Embryonic Lethality in PARP-1 AtmDouble-Mutant Mice Suggests a Functional Synergy in Cell Proliferation during Development , 2001, Molecular and Cellular Biology.

[53]  Samuel H. Wilson,et al.  Photoaffinity Labeling of Mouse Fibroblast Enzymes by a Base Excision Repair Intermediate , 2001, The Journal of Biological Chemistry.

[54]  G. Kroemer,et al.  Apoptosis-inducing factor (AIF): caspase-independent after all , 2004, Cell Death and Differentiation.

[55]  G. Sutherland,et al.  Identification of a Novel Human Tankyrase through Its Interaction with the Adaptor Protein Grb14* , 2001, The Journal of Biological Chemistry.

[56]  Brandoch D. Cook,et al.  Role for the Related Poly(ADP-Ribose) Polymerases Tankyrase 1 and 2 at Human Telomeres , 2002, Molecular and Cellular Biology.

[57]  H. Seimiya,et al.  The Telomeric Poly(ADP-ribose) Polymerase, Tankyrase 1, Contains Multiple Binding Sites for Telomeric Repeat Binding Factor 1 (TRF1) and a Novel Acceptor, 182-kDa Tankyrase-binding Protein (TAB182)* , 2002, The Journal of Biological Chemistry.

[58]  J. Pleschke,et al.  Poly(ADP-ribose) Binds to Specific Domains in DNA Damage Checkpoint Proteins* , 2000, The Journal of Biological Chemistry.

[59]  Juan I. Sbodio,et al.  Identification of a Tankyrase-binding Motif Shared by IRAP, TAB182, and Human TRF1 but Not Mouse TRF1 , 2002, The Journal of Biological Chemistry.

[60]  T. Dawson,et al.  Mediation of Poly(ADP-Ribose) Polymerase-1-Dependent Cell Death by Apoptosis-Inducing Factor , 2002, Science.

[61]  E. Rogakou,et al.  DNA Double-stranded Breaks Induce Histone H2AX Phosphorylation on Serine 139* , 1998, The Journal of Biological Chemistry.

[62]  Changlian Zhu,et al.  Involvement of apoptosis‐inducing factor in neuronal death after hypoxia‐ischemia in the neonatal rat brain , 2003, Journal of neurochemistry.

[63]  A. Huletsky,et al.  Modulation of Chromatin Structure by Poly(ADP-Ribosyl)ation , 1988 .

[64]  G. de Murcia,et al.  Poly(ADP-ribose) polymerase-1: what have we learned from the deficient mouse model? , 2000, Mutation research.

[65]  P. Dollé,et al.  Poly(ADP-ribose) Polymerase-2 (PARP-2) Is Required for Efficient Base Excision DNA Repair in Association with PARP-1 and XRCC1* , 2002, The Journal of Biological Chemistry.

[66]  Zhao-Qi Wang,et al.  Poly(ADP-ribose) Polymerase Null Mouse Cells Synthesize ADP-ribose Polymers* , 1998, The Journal of Biological Chemistry.

[67]  Susan Smith,et al.  Resolution of Sister Telomere Association Is Required for Progression Through Mitosis , 2004, Science.

[68]  G. Schulz,et al.  Structure of the catalytic fragment of poly(AD-ribose) polymerase from chicken. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[69]  M. Bycroft,et al.  The crystal structure of AF1521 a protein from Archaeoglobus fulgidus with homology to the non-histone domain of macroH2A. , 2003, Journal of molecular biology.

[70]  M. Hottiger,et al.  A Role of Poly (ADP-Ribose) Polymerase in NF- B Transcriptional Activation , 1999 .

[71]  G. Morin,et al.  TANK2, a New TRF1-associated Poly(ADP-ribose) Polymerase, Causes Rapid Induction of Cell Death upon Overexpression* , 2001, The Journal of Biological Chemistry.

[72]  H. Lodish,et al.  Tankyrase Is a Golgi-associated Mitogen-activated Protein Kinase Substrate That Interacts with IRAP in GLUT4 Vesicles* , 2000, The Journal of Biological Chemistry.

[73]  T. Lange,et al.  Tankyrase promotes telomere elongation in human cells , 2000, Current Biology.

[74]  C. Price,et al.  Vertebrate tankyrase domain structure and sterile alpha motif (SAM)-mediated multimerization. , 2003, The Biochemical journal.

[75]  Robert Almassy,et al.  Anticancer chemosensitization and radiosensitization by the novel poly(ADP-ribose) polymerase-1 inhibitor AG14361. , 2004, Journal of the National Cancer Institute.