Complex roles of members of the ADP-ribosyl transferase super family in immune defences: Looking beyond PARP1

Biochemical Pharmacology

Volumn 84, Issue 1, 2012, Pages 11-20

  Welsby, Iain ^a   Hutin, David ^a   Leo, Oberdan ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

ADP ribosyl transferases (ARTs); Immunomodulation; Inflammation; Poly(ADP ribose) polymerases (PARPs)

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 12; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 13; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 14; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 5A; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 9; TANKYRASE 1; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; CELL DEATH; CELL SURVIVAL; CYTOPLASM; GENETIC TRANSCRIPTION; HUMAN; IMMUNITY; IMMUNOMODULATION; INNATE IMMUNITY; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

EID: 84860662327     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2012.02.016     Document Type: Note

References (115)

1. T. Honjo, Y. Nishizuka, and O. Hayaishi Diphtheria toxin-dependent adenosine diphosphate ribosylation of aminoacyl transferase II and inhibition of protein synthesis J Biol Chem 243 1968 3553 3555
2. Q. Deng, and J.T. Barbieri Molecular mechanisms of the cytotoxicity of ADP-ribosylating toxins Annu Rev Microbiol 62 2008 271 288
3. D. Eastman, and M. Dworkin Endogenous ADP-ribosylation during development of the prokaryote Myxococcus xanthus Microbiology (UK) 140 Pt 1994 3167 3176
4. H. Fu, R.H. Burris, and G.P. Roberts Reversible ADP-ribosylation is demonstrated to be a regulatory mechanism in prokaryotes by heterologous expression Proc Natl Acad Sci USA 87 1990 1720 1724
5. V. Rolli, M. O'Farrell, J. Ménissier-de Murcia, and G. de Murcia Random mutagenesis of the poly(ADP-ribose) polymerase catalytic domain reveals amino acids involved in polymer branching Biochemistry 36 1997 12147 12154
6. M.O. Hottiger, P.O. Hassa, B. Lüscher, H. Schüler, and F. Koch-Nolte Toward a unified nomenclature for mammalian ADP-ribosyltransferases Trends Biochem Sci 35 2010 208 219
7. H. Kleine, E. Poreba, K. Lesniewicz, P.O. Hassa, M.O. Hottiger, and D.W. Litchfield Substrate-assisted catalysis by PARP10 limits its activity to mono-ADP-ribosylation Mol Cell 32 2008 57 69
8. M. Prochazka, H.R. Gaskins, E.H. Leiter, F. Koch-Nolte, F. Haag, and H.G. Thiele Chromosomal localization, DNA polymorphism, and expression of Rt-6, the mouse homologue of rat T-lymphocyte differentiation marker RT6 Immunogenetics 33 1991 152 156
9. F. Haag, F. Koch-Nolte, M. Kühl, S. Lorenzen, and H.G. Thiele Premature stop codons inactivate the RT6 genes of the human and chimpanzee species J Mol Biol 243 1994 537 546
10. G. Glowacki, R. Braren, K. Firner, M. Nissen, M. Kühl, and P. Reche The family of toxin-related ecto-ADP-ribosyltransferases in humans and the mouse Protein Sci 11 2002 1657 1670
11. P. Kefalas, B. Saxty, M. Yadollahi-Farsani, and J. MacDermot Chemotaxin-dependent translocation of immunoreactive ADP-ribosyltransferase-1 to the surface of human neutrophil polymorphs Eur J Biochem 259 1999 866 871
12. H.G. Thiele, F. Koch, A. Hamann, and R. Arndt Biochemical characterization of the T-cell alloantigen RT-6.2 Immunology 59 1986 195 201
13. U.H. Kim, M.K. Kim, J.S. Kim, M.K. Han, B.H. Park, and H.R. Kim Purification and characterization of NAD glycohydrolase from rabbit erythrocytes Arch Biochem Biophys 305 1993 147 152
14. L.E. Donnelly, N.B. Rendell, S. Murray, J.R. Allport, G. Lo, and P. Kefalas Arginine-specific mono(ADP-ribosyl)transferase activity on the surface of human polymorphonuclear neutrophil leucocytes Biochem J 315 Pt 2 1996 635 641
15. S. Adriouch, S. Hubert, S. Pechberty, F. Koch-Nolte, F. Haag, and M. Seman NAD+ released during inflammation participates in T cell homeostasis by inducing ART2-mediated death of naive T cells in vivo J Immunol 179 2007 186 194
16. G. Paone, A. Wada, L.A. Stevens, A. Matin, T. Hirayama, and R.L. Levine ADP ribosylation of human neutrophil peptide-1 regulates its biological properties Proc Natl Acad Sci USA 99 2002 8231 8235
17. A. Lichtenstein, T. Ganz, M.E. Selsted, and R.I. Lehrer In vitro tumor cell cytolysis mediated by peptide defensins of human and rabbit granulocytes Blood 68 1986 1407 1410
18. J. Ashitani, H. Mukae, M. Nakazato, T. Ihi, H. Mashimoto, and J. Kadota Elevated concentrations of defensins in bronchoalveolar lavage fluid in diffuse panbronchiolitis Eur Respir J 11 1998 104 111
19. G. Paone, L. a Stevens, R.L. Levine, C. Bourgeois, W.K. Steagall, and B.R. Gochuico ADP-ribosyltransferase-specific modification of human neutrophil peptide-1 J Biol Chem 281 2006 17054 17060
20. M. Seman, S. Adriouch, F. Scheuplein, C. Krebs, D. Freese, and G. Glowacki NAD-induced T cell death: ADP-ribosylation of cell surface proteins by ART2 activates the cytolytic P2X7 purinoceptor Immunity 19 2003 571 582
21. L.V. Parijs, and Homeostasis Self-tolerance in the immune system: turning lymphocytes off Science 280 1998 243 248
22. S. Adriouch, P. Bannas, N. Schwarz, R. Fliegert, A.H. Guse, and M. Seman ADP-ribosylation at R125 gates the P2X7 ion channel by presenting a covalent ligand to its nucleotide binding site FASEB J 22 2008 861 869
23. S. Hubert, B. Rissiek, K. Klages, J. Huehn, T. Sparwasser, and F. Haag Extracellular NAD+ shapes the Foxp3+ regulatory T cell compartment through the ART2-P2X7 pathway J Exp Med 207 2010 2561 2568
24. C. Krebs, S. Adriouch, F. Braasch, W. Koestner, E.H. Leiter, and M. Seman CD38 controls ADP-ribosyltransferase-2-catalyzed ADP-ribosylation of T cell surface proteins J Immunol 174 2005 3298 3305
25. W.-X. Zong, D. Ditsworth, D.E. Bauer, Z.-Q. Wang, and C.B. Thompson Alkylating DNA damage stimulates a regulated form of necrotic cell death Genes Dev 18 2004 1272 1282
26. R.S. Moubarak, V.J. Yuste, C. Artus, A. Bouharrour, P.A. Greer, and J. Menissier-de Murcia Sequential activation of poly(ADP-ribose) polymerase 1, calpains, and Bax is essential in apoptosis-inducing factor-mediated programmed necrosis Mol Cell Biol 27 2007 4844 4862
27. I.U. Schraufstatter, D.B. Hinshaw, P.A. Hyslop, R.G. Spragg, and C.G. Cochrane Oxidant injury of cells. DNA strand-breaks activate polyadenosine diphosphate-ribose polymerase and lead to depletion of nicotinamide adenine dinucleotide J Clin Invest 77 1986 1312 1320
28. S.-W. Yu, H. Wang, M.F. Poitras, C. Coombs, W.J. Bowers, and H.J. Federoff Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor Science 297 2002 259 263
29. Y. Wang, N.S. Kim, J.-F. Haince, H.C. Kang, K.K. David, and S.A. Andrabi Poly(ADP-ribose) (PAR) binding to apoptosis-inducing factor is critical for PAR polymerase-1-dependent cell death (parthanatos) Sci Signal 4 2011 ra20
30. C. Artus, H. Boujrad, A. Bouharrour, M.-N. Brunelle, S. Hoos, and V.J. Yuste AIF promotes chromatinolysis and caspase-independent programmed necrosis by interacting with histone H2AX EMBO J 29 2010 1585 1599
31. S.A Andrabi, N.S. Kim, S.-W. Yu, H. Wang, D.W. Koh, and M. Sasaki Poly(ADP-ribose) (PAR) polymer is a death signal Proc Natl Acad Sci USA 103 2006 18308 18313
32. C.C. Alano, W. Ying, and R.A Swanson Poly(ADP-ribose) polymerase-1-mediated cell death in astrocytes requires NAD+ depletion and mitochondrial permeability transition J Biol Chem 279 2004 18895 18902
33. C.C. Alano, P. Garnier, W. Ying, Y. Higashi, T.M. Kauppinen, and R.A Swanson NAD+ depletion is necessary and sufficient for poly(ADP-ribose) polymerase-1-mediated neuronal death J Neurosci 30 2010 2967 2978
34. E. Fonfria, I.C.B. Marshall, C.D. Benham, I. Boyfield, J.D. Brown, and K. Hill TRPM2 channel opening in response to oxidative stress is dependent on activation of poly(ADP-ribose) polymerase Br J Pharmacol 143 2004 186 192
35. A.L. Perraud, A. Fleig, C.A. Dunn, L.A. Bagley, P. Launay, and C. Schmitz ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology Nature 411 2001 595 599
36. B. Buelow, Y. Song, and A.M. Scharenberg The Poly(ADP-ribose) polymerase PARP-1 is required for oxidative stress-induced TRPM2 activation in lymphocytes J Biol Chem 283 2008 24571 24583
37. 2+ fluxes in oxidative cell death Cell Mol Life Sci 68 2011 1455 1466
38. M. Miwa, and T. Sugimura Splitting of the ribose-ribose linkage of poly(adenosine diphosphate-robose) by a calf thymus extract J Biol Chem 246 1971 6362 6364
39. M. Miwa, K. Nakatsugawa, K. Hara, T. Matsushima, and T. Sugimura Degradation of poly(adenosine diphosphate ribose) by homogenates of various normal tissues and tumors of rats Arch Biochem Biophys 167 1975 54 60
40. 2-induced cell death Biochem J 396 2006 419 429
41. P.J. Magistretti, L. Pellerin, and J.-L. Martin Brain energy metabolism: an integrated cellular perspective F.E. Bloom, D.J. Kupfer, Psychopharmacology: the fourth generation of progress 1995 Raven Press New York 657 670
42. K.L. Rock, and H. Kono The inflammatory response to cell death Annu Rev Pathol-Mech 3 2008 99 126
43. R.B. Elliott, C.C. Pilcher, A. Stewart, D. Fergusson, and M.A. McGregor The use of nicotinamide in the prevention of type 1 diabetes Ann NY Acad Sci 696 1993 333 341
44. B. Heller, Z.Q. Wang, E.F. Wagner, J. Radons, A. Bürkle, and K. Fehsel Inactivation of the poly(ADP-ribose) polymerase gene affects oxygen radical and nitric oxide toxicity in islet cells J Biol Chem 270 1995 11176 11180
45. V. Giansanti, F. Donà, M. Tillhon, and A.I. Scovassi PARP inhibitors: new tools to protect from inflammation Biochem Pharmacol 80 2010 1869 1877
46. F.J. Oliver, J. Ménissier-de Murcia, C. Nacci, P. Decker, R. Andriantsitohaina, and S. Muller Resistance to endotoxic shock as a consequence of defective NF-kappaB activation in poly (ADP-ribose) polymerase-1 deficient mice EMBO J 18 1999 4446 4454
47. P.O. Hassa, and M.O. Hottiger A role of poly (ADP-ribose) polymerase in NF-kappaB transcriptional activation Biol Chem 380 1999 953 959
48. Z. Chen, J. Hagler, V.J. Palombella, F. Melandri, D. Scherer, and D. Ballard Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway Genes Dev 9 1995 1586 1597
49. P.O. Hassa, M. Covic, S. Hasan, R. Imhof, and M.O. Hottiger The enzymatic and DNA binding activity of PARP-1 are not required for NF-kappa B coactivator function J Biol Chem 276 2001 45588 45597
50. P.O. Hassa, C. Buerki, C. Lombardi, R. Imhof, and M.O. Hottiger Transcriptional coactivation of nuclear factor-kappaB-dependent gene expression by p300 is regulated by poly(ADP)-ribose polymerase-1 J Biol Chem 278 2003 45145 45153
51. P.O. Hassa, S.S. Haenni, C. Buerki, N.I. Meier, W.S. Lane, and H. Owen Acetylation of poly(ADP-ribose) polymerase-1 by p300/CREB-binding protein regulates coactivation of NF-kappaB-dependent transcription J Biol Chem 280 2005 40450 40464
52. M. Kameoka, K. Ota, T. Tetsuka, Y. Tanaka, A. Itaya, and T. Okamoto Evidence for regulation of NF-kappaB by poly(ADP-ribose) polymerase Biochem J 346 Pt 3 2000 641 649
53. W.J. Chang, and R. Alvarez-Gonzalez The sequence-specific DNA binding of NF-kappa B is reversibly regulated by the automodification reaction of poly (ADP-ribose) polymerase 1 J Biol Chem 276 2001 47664 47670
54. H. Nakajima, H. Nagaso, N. Kakui, M. Ishikawa, T. Hiranuma, and S. Hoshiko Critical role of the automodification of poly(ADP-ribose) polymerase-1 in nuclear factor-kappaB-dependent gene expression in primary cultured mouse glial cells J Biol Chem 279 2004 42774 42786
55. K. Brzóska, and I. Szumiel Signalling loops and linear pathways: NF-kappaB activation in response to genotoxic stress Mutagenesis 24 2009 1 8
56. M. Stilmann, M. Hinz, S.C. Arslan, A. Zimmer, V. Schreiber, and C. Scheidereit A nuclear poly(ADP-ribose)-dependent signalosome confers DNA damage-induced IkappaB kinase activation Mol Cell 36 2009 365 378
57. Z.-H. Wu, Y. Shi, R.S. Tibbetts, and S. Miyamoto Molecular linkage between the kinase ATM and NF-kappaB signaling in response to genotoxic stimuli Science 311 2006 1141 1146
58. Y. Yang, F. Xia, N. Hermance, A. Mabb, S. Simonson, and S. Morrissey A cytosolic ATM/NEMO/RIP1 complex recruits TAK1 to mediate the NF-kappaB and p38 mitogen-activated protein kinase (MAPK)/MAPK-activated protein 2 responses to DNA damage Mol Cell Biol 31 2011 2774 2786
59. J. Niu, Y. Shi, K. Iwai, and Z.-H. Wu LUBAC regulates NF-κB activation upon genotoxic stress by promoting linear ubiquitination of NEMO EMBO J 30 2011 3741 3753
60. J.E. Hunter, E. Willmore, J.A.E. Irving, Z. Hostomsky, S.J. Veuger, and B.W. Durkacz NF-κB mediates radio-sensitization by the PARP-1 inhibitor, AG-014699 Oncogene 31 2011 251 264
61. R. Valdor, V. Schreiber, L. Saenz, T. Martínez, A. Muñoz-Suano, and M. Dominguez-Villar Regulation of NFAT by poly(ADP-ribose) polymerase activity in T cells Mol Immunol 45 2008 1863 1871
62. T.L. Andreone, M. O'Connor, A. Denenberg, P.W. Hake, and B. Zingarelli Poly(ADP-ribose) polymerase-1 regulates activation of activator protein-1 in murine fibroblasts J Immunol 170 2003 2113 2120
63. F. Macian NFAT proteins: key regulators of T-cell development and function Nat Rev Immunol 5 2005 472 484
64. E.F. Wagner, and R. Eferl Fos/AP-1 proteins in bone and the immune system Immunol Rev 208 2005 126 140
65. F. Nasta, F. Laudisi, M. Sambucci, M.M. Rosado, and C. Pioli Increased Foxp3+ regulatory T cells in poly(ADP-ribose) polymerase-1 deficiency J Immunol 184 2010 3470 3477
66. A.K.L. Leung, S. Vyas, J.E. Rood, A. Bhutkar, P.A. Sharp, and P. Chang Poly(ADP-ribose) regulates stress responses and microRNA activity in the cytoplasm Mol Cell 42 2011 489 499
67. S. Smith, I. Giriat, A. Schmitt, and T. de Lange Tankyrase, a poly(ADP-ribose) polymerase at human telomeres Science 282 1998 1484 1487
68. W. Chang, J.N. Dynek, and S. Smith TRF1 is degraded by ubiquitin-mediated proteolysis after release from telomeres Genes Dev 17 2003 1328 1333
69. T.-Y.J. Yeh, K.K. Beiswenger, P. Li, K.E. Bolin, R.M. Lee, and T.-S. Tsao Hypermetabolism, hyperphagia, and reduced adiposity in tankyrase-deficient mice Diabetes 58 2009 2476 2485
70. Y.J. Chiang, S.J. Hsiao, D. Yver, S.W. Cushman, L. Tessarollo, and S. Smith Tankyrase 1 and tankyrase 2 are essential but redundant for mouse embryonic development PLoS One 3 2008 e2639
71. Y.J. Chiang, M.-L. Nguyen, S. Gurunathan, P. Kaminker, L. Tessarollo, and J. Campisi Generation and characterization of telomere length maintenance in tankyrase 2-deficient mice Mol. Cell. Biol 26 2006 2037 2043
72. S.-M. a Huang, Y.M. Mishina, S. Liu, A. Cheung, F. Stegmeier, and G.A. Michaud Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling Nature 461 2009 614 620
73. N. Levaot, O. Voytyuk, I. Dimitriou, F. Sircoulomb, A. Chandrakumar, and M. Deckert Loss of tankyrase-mediated destruction of 3BP2 is the underlying pathogenic mechanism of cherubism Cell 147 2011 1324 1339
74. S. Guettler, J. LaRose, E. Petsalaki, G. Gish, A. Scotter, and T. Pawson Structural basis and sequence rules for substrate recognition by tankyrase explain the basis for cherubism disease Cell 147 2011 1340 1354
75. V. Schreiber, F. Dantzer, J.-C. Ame, and G. de Murcia Poly(ADP-ribose): novel functions for an old molecule Nat Rev Mol Cell Biol 7 2006 517 528
76. M. Neuvonen, and T. Ahola Differential activities of cellular and viral macro domain proteins in binding of ADP-ribose metabolites J Mol Biol 385 2009 212 225
77. M.-P. Egloff, H. Malet, A. Putics, M. Heinonen, H. Dutartre, and A. Frangeul Structural and functional basis for ADP-ribose and poly(ADP-ribose) binding by viral macro domains J Virol 80 2006 8493 8502
78. R.C. Aguiar, Y. Yakushijin, S. Kharbanda, R. Salgia, J.A. Fletcher, and M.A. Shipp BAL is a novel risk-related gene in diffuse large B-cell lymphomas that enhances cellular migration Blood 96 2000 4328 4334
79. R.C.T. Aguiar, K. Takeyama, C. He, K. Kreinbrink, and M.A. Shipp B-aggressive lymphoma family proteins have unique domains that modulate transcription and exhibit poly(ADP-ribose) polymerase activity J Biol Chem 280 2005 33756 33765
80. P. Juszczynski, J.L. Kutok, C. Li, J. Mitra, R.C.T. Aguiar, and M.A. Shipp BAL1 and BBAP are regulated by a gamma interferon-responsive bidirectional promoter and are overexpressed in diffuse large B-cell lymphomas with a prominent inflammatory infiltrate Mol Cell Biol 26 2006 5348 5359
81. S. Goenka, and M. Boothby Selective potentiation of Stat-dependent gene expression by collaborator of Stat6 (CoaSt6), a transcriptional cofactor Proc Natl Acad Sci USA 103 2006 4210 4215
82. S. Goenka, S.H. Cho, and M. Boothby Collaborator of Stat6 (CoaSt6)-associated poly(ADP-ribose) polymerase activity modulates Stat6-dependent gene transcription J Biol Chem 282 2007 18732 18739
83. J. Yang, S. Aittomäki, M. Pesu, K. Carter, J. Saarinen, and N. Kalkkinen Identification of p100 as a coactivator for STAT6 that bridges STAT6 with RNA polymerase II EMBO J 21 2002 4950 4958
84. S.H. Cho, A.K. Ahn, P. Bhargava, C.-H. Lee, C.M. Eischen, and O. McGuinness Glycolytic rate and lymphomagenesis depend on PARP14, an ADP ribosyltransferase of the B aggressive lymphoma (BAL) family Proc Natl Acad Sci USA 108 2011 15972 15977
85. G. Gao, X. Guo, and S.P. Goff Inhibition of retroviral RNA production by ZAP, a CCCH-type zinc finger protein Science 297 2002 1703 1706
86. M. Katoh, and M. Katoh Identification and characterization of human TIPARP gene within the CCNL amplicon at human chromosome 3q25.31 Int J Oncol 23 2003 541 547
87. J.-C. Amé, C. Spenlehauer, and G. de Murcia The PARP superfamily Bioessays 26 2004 882 893
88. M.J. Bick, J. William, N. Carroll, G. Gao, S.P. Goff, and C.M. Rice Expression of the zinc-finger antiviral protein inhibits alphavirus replication J Virol 77 2003 11555 11562
89. S. Müller, P. Möller, M.J. Bick, S. Wurr, S. Becker, and S. Günther Inhibition of filovirus replication by the zinc finger antiviral protein J Virol 81 2007 2391 2400
90. R.N. DuBois, M.W. McLane, K. Ryder, L.F. Lau, and D. Nathans A growth factor-inducible nuclear protein with a novel cysteine/histidine repetitive sequence J Biol Chem 265 1990 19185 19191
91. E. Carballo, W.S. Lai, and P.J. Blackshear Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin Science 281 1998 1001 1005
92. J. Liang, W. Song, G. Tromp, P.E. Kolattukudy, and M. Fu Genome-wide survey and expression profiling of CCCH-zinc finger family reveals a functional module in macrophage activation PLoS One 3 2008 e2880
93. E.S. Hwang, A. Choi, and I.-C. Ho Transcriptional regulation of GATA-3 by an intronic regulatory region and fetal liver zinc finger protein 1 J Immunol 169 2002 248 253
94. X. Guo, J. William, N. Carroll, M.R. Macdonald, S.P. Goff, and G. Gao The zinc finger antiviral protein directly binds to specific viral mRNAs through the CCCH zinc finger motifs J Virol 78 2004 12781 12787
95. X. Guo, J. Ma, J. Sun, and G. Gao The zinc-finger antiviral protein recruits the RNA processing exosome to degrade the target mRNA Proc Natl Acad Sci USA 104 2007 151 156
96. E. Lorentzen, P. Walter, S. Fribourg, E. Evguenieva-Hackenberg, G. Klug, and E. Conti The archaeal exosome core is a hexameric ring structure with three catalytic subunits Nat Struct Mol Biol 12 2005 575 581
97. P. Ye, S. Liu, Y. Zhu, G. Chen, and G. Gao DEXH-Box protein DHX30 is required for optimal function of the zinc-finger antiviral protein Protein Cell 1 2010 956 964
98. G. Chen, X. Guo, F. Lv, Y. Xu, and G. Gao p72 DEAD box RNA helicase is required for optimal function of the zinc-finger antiviral protein Proc Natl Acad Sci USA 105 2008 4352 4357
99. Z. Huang, X. Wang, and G. Gao Analyses of SELEX-derived ZAP-binding RNA aptamers suggest that the binding specificity is determined by both structure and sequence of the RNA Protein Cell 1 2010 752 759
100. J.A. Kerns, M. Emerman, and H.S. Malik Positive selection and increased antiviral activity associated with the PARP-containing isoform of human zinc-finger antiviral protein PLoS Genet 4 2008 e21
101. Y. Zhu, G. Chen, F. Lv, X. Wang, X. Ji, and Y. Xu Zinc-finger antiviral protein inhibits HIV-1 infection by selectively targeting multiply spliced viral mRNAs for degradation Proc Natl Acad Sci USA 108 2011 15834 15839
102. M. Stremlau, M. Perron, M. Lee, Y. Li, B. Song, and H. Javanbakht Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor Proc Natl Acad Sci USA 103 2006 5514 5519
103. T. Pertel, S. Hausmann, D. Morger, S. Züger, J. Guerra, and J. Lascano TRIM5 is an innate immune sensor for the retrovirus capsid lattice Nature 472 2011 361 365
104. S. Hayakawa, S. Shiratori, H. Yamato, T. Kameyama, C. Kitatsuji, and F. Kashigi ZAPS is a potent stimulator of signaling mediated by the RNA helicase RIG-I during antiviral responses Nat Immunol 2010 1 9
105. V. Hornung, J. Ellegast, S. Kim, K. Brzózka, A. Jung, and H. Kato 5′-Triphosphate RNA is the ligand for RIG-I Science 314 2006 994 997
106. J.W. Schoggins, S.J. Wilson, M. Panis, M.Y. Murphy, C.T. Jones, and P. Bieniasz A diverse range of gene products are effectors of the type I interferon antiviral response Nature 1 2011
107. C. Erbel, J. Achenbach, M. Akhavanpoor, T.J. Dengler, F. Lasitschka, and C.A. Gleissner PARP inhibition in atherosclerosis and its effects on dendritic cells, T cells and auto-antibody levels Eur J Med Res 16 2011 367 374
108. A. Chiarugi, and M.A. Moskowitz Poly(ADP-ribose) polymerase-1 activity promotes NF-κB-driven transcription and microglial activation: implication for neurodegenerative disorders J Neurochem 85 2003 306 317
109. C. Le Page, J. Sanceau, J.C. Drapier, and J. Wietzerbin Inhibitors of ADP-ribosylation impair inducible nitric oxide synthase gene transcription through inhibition of NF kappa B activation Biochem Biophys Res Commun 243 1998 451 457
110. G. Haskó, J.G. Mabley, Z.H. Németh, P. Pacher, E.A. Deitch, and C. Szabó Poly(ADP-ribose) polymerase is a regulator of chemokine production: relevance for the pathogenesis of shock and inflammation Mol Med 8 2002 283 289
111. A. Aldinucci, G. Gerlini, S. Fossati, G. Cipriani, C. Ballerini, and T. Biagioli A key role for poly(ADP-ribose) polymerase-1 activity during human dendritic cell maturation J Immunol 179 2007 305 312
112. D.V. Ferraris Evolution of poly(ADP-ribose) polymerase-1 (PARP-1) inhibitors. From concept to clinic J Med Chem 53 2010 4561 4584
113. M. Rouleau, A. Patel, M.J. Hendzel, S.H. Kaufmann, and G.G. Poirier PARP inhibition: PARP1 and beyond Nat Rev Cancer 10 2010 293 301
114. J.M. Olefsky, and C.K. Glass Macrophages, inflammation, and insulin resistance Annu Rev Physiol 72 2010 219 246
115. M. Narwal, H. Venkannagari, and L. Lehtiö Structural basis of selective inhibition of human tankyrases J Med Chem 55 2012 1360 1367