Signaling mechanism of poly(ADP-ribose) polymerase-1 (PARP-1) in inflammatory diseases

American Journal of Pathology

Volumn 178, Issue 3, 2011, Pages 946-955

  Ba, Xueqing ^a,b   Garg, Nisha Jain ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b NORTHEAST NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSE; CELL ADHESION MOLECULE; CYCLOOXYGENASE 2; CYTOKINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; PADGEM PROTEIN; RECEPTOR PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TUMOR NECROSIS FACTOR ALPHA;

CELL DEATH; DISEASE EXACERBATION; ENZYME ACTIVATION; ENZYME STRUCTURE; GENE EXPRESSION; HUMAN; INFLAMMATORY DISEASE; MITOCHONDRION; OXIDATION REDUCTION REACTION; PATHOGENESIS; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

EID: 79952768723     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2010.12.004     Document Type: Review

References (125)

1. Riquelme PT, Burzio LO, Koide SS: ADP ribosylation of rat liver lysine-rich histone in vitro. J Biol Chem 1979, 254:3018-3028
2. Burzio LO, Riquelme PT, Koide SS: ADP ribosylation of rat liver nucleosomal core histones. J Biol Chem 1979, 254:3029-3037
3. Suzuki H, Quesada P, Farina B, Leone E: In vitro poly(ADP-ribosyl)- ation of seminal ribonuclease. J Biol Chem 1986, 261:6048-6055
4. Pleschke JM, Kleczkowska HE, Strohm M, Althaus FR: Poly(ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J Biol Chem 2000, 275:40974-40980 (Pubitemid 32054922)
5. Otto H, Reche PA, Bazan F, Dittmar K, Haag F, Koch-Nolte F: In silico characterization of the family of PARP-like poly(ADP-ribosyl) transferases (pARTs). BMC Genomics 2005, 6:139
6. Lautier D, Lagueux J, Thibodeau J, Menard L, Poirier GG: Molecular and biochemical features of poly (ADP-ribose) metabolism. Mol Cell Biochem 1993, 122:171-193 (Pubitemid 23222327)
7. Lindahl T, Satoh MS, Poirier GG, Klungland A: Post-translational modification of poly(ADP-ribose) polymerase induced by DNA strand breaks. Trends Biochem Sci 1995, 20:405-411
8. Nguewa PA, Fuertes MA, Valladares B, Alonso C, Perez JM: Poly- (ADP-ribose) polymerases: homology, structural domains and functions: novel therapeutical applications. Prog Biophys Mol Biol 2005, 88:143-172 (Pubitemid 39547776)
9. Schreiber V, Dantzer F, Ame JC, de Murcia G: Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 2006, 7:517-528 (Pubitemid 44036457)
10. Shieh WM, Ame JC, Wilson MV, Wang ZQ, Koh DW, Jacobson MK, Jacobson EL: Poly(ADP-ribose) polymerase null mouse cells synthesize ADP-ribose polymers. J Biol Chem 1998, 273:30069-30072 (Pubitemid 28545464)
11. Chambon P, Weill JD, Mandel P: Nicotinamide mononucleotide activation of new DNA-dependent polyadenylic acid synthesizing nuclear enzyme. Biochem Biophys Res Commun 1963, 11:39-43
12. Slattery E, Dignam JD, Matsui T, Roeder RG: Purification and analysis of a factor which suppresses nick-induced transcription by RNA polymerase II and its identity with poly(ADP-ribose) polymerase. J Biol Chem 1983, 258:5955-5959
13. Woodhouse BC, Dianov GL: Poly ADP-ribose polymerase-1: an international molecule of mystery. DNA Repair (Amst) 2008, 7:1077-1086
14. Kameshita I, Matsuda Z, Taniguchi T, Shizuta Y: Poly (ADP-ribose) synthetase: separation and identification of three proteolytic fragments as the substrate-binding domain, the DNA-binding domain, and the automodification domain. J Biol Chem 1984, 259:4770-4776 (Pubitemid 14144197)
15. D'Amours D, Desnoyers S, D'Silva I, Poirier GG: Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J 1999, 342(pt 2):249-268 (Pubitemid 29425344)
16. Langelier MF, Ruhl DD, Planck JL, Kraus WL, Pascal JM: 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. J Biol Chem 2010, 285:18877-18887
17. Tao Z, Gao P, Hoffman DW, Liu HW: Domain C of human poly(ADP-ribose) polymerase-1 is important for enzyme activity and contains a novel zinc-ribbon motif. Biochemistry 2008, 47:5804-5813 (Pubitemid 351747059)
18. Langelier MF, Servent KM, Rogers EE, Pascal JM: A third zinc-binding domain of human poly(ADP-ribose) polymerase-1 coordinates DNA-dependent enzyme activation. J Biol Chem 2008, 283:4105-4114
19. Desmarais Y, Menard L, Lagueux J, Poirier GG: Enzymological properties of poly(ADP-ribose)polymerase: characterization of automodification sites and NADase activity. Biochim Biophys Acta 1991, 1078:179-186
20. Tao Z, Gao P, Liu HW: Identification of the ADP-ribosylation sites in the PARP-1 automodification domain: analysis and implications. J Am Chem Soc 2009, 131:14258-14260
21. Altmeyer M, Messner S, Hassa PO, Fey M, Hottiger MO: Molecular mechanism of poly(ADP-ribosyl)ation by PARP1 and identification of lysine residues as ADP-ribose acceptor sites. Nucleic Acids Res 2009, 37:3723-3738
22. Caldecott KW, Aoufouchi S, Johnson P, Shall S: XRCC1 polypeptide interacts with DNA polymerase beta and possibly poly (ADP-ribose) polymerase, and DNA ligase III is a novel molecular "nick-sensor" in vitro. Nucleic Acids Res 1996, 24:4387-4394
23. Schreiber V, Ame JC, Dolle P, Schultz I, Rinaldi B, Fraulob V, Menissier-de Murcia J, de Murcia G: Poly(ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J Biol Chem 2002, 277:23028-23036 (Pubitemid 34967289)
24. Masson M, Niedergang C, Schreiber V, Muller S, Menissier-de Murcia J, de Murcia G: XRCC1 is specifically associated with poly(ADP-ribose) polymerase and negatively regulates its activity following DNA damage. Mol Cell Biol 1998, 18:3563-3571 (Pubitemid 28240528)
25. Pion E, Ullmann GM, Ame JC, Gerard D, de Murcia G, Bombarda E: DNA-induced dimerization of poly(ADP-ribose) polymerase-1 triggers its activation. Biochemistry 2005, 44:14670-14681 (Pubitemid 41567474)
26. Simonin F, Hofferer L, Panzeter PL, Muller S, de Murcia G, Althaus FR: The carboxyl-terminal domain of human poly(ADP-ribose) polymerase: overproduction in Escherichia coli, large scale purification, and characterization. J Biol Chem 1993, 268:13454-13461 (Pubitemid 23307771)
27. Ruf A, Mennissier de Murcia J, de Murcia G, Schulz GE: Structure of the catalytic fragment of poly(AD-ribose) polymerase from chicken. Proc Natl Acad Sci U S A 1996, 93:7481-7485 (Pubitemid 26277060)
28. Lonskaya I, Potaman VN, Shlyakhtenko LS, Oussatcheva EA, Lyubchenko YL, Soldatenkov VA: Regulation of poly(ADP-ribose) polymerase-1 by DNA structure-specific binding. J Biol Chem 2005, 280:17076-17083 (Pubitemid 41389171)
29. Potaman VN, Shlyakhtenko LS, Oussatcheva EA, Lyubchenko YL, Soldatenkov VA: Specific binding of poly(ADP-ribose) polymerase-1 to cruciform hairpins. J Mol Biol 2005, 348:609-615 (Pubitemid 40515673)
30. Kim MY, Mauro S, Gevry N, Lis JT, Kraus WL: NAD+-dependent modulation of chromatin structure and transcription by nucleosome binding properties of PARP-1. Cell 2004, 119:803-814 (Pubitemid 40017687)
31. Wacker DA, Ruhl DD, Balagamwala EH, Hope KM, Zhang T, Kraus WL: The DNA binding and catalytic domains of poly(ADP-ribose) polymerase 1 cooperate in the regulation of chromatin structure and transcription. Mol Cell Biol 2007, 27:7475-7485 (Pubitemid 350033654)
32. Davidovic L, Vodenicharov M, Affar EB, Poirier GG: Importance of poly(ADP-ribose) glycohydrolase in the control of poly(ADP-ribose) metabolism. Exp Cell Res 2001, 268:7-13 (Pubitemid 32678855)
33. Van Wijk SJ, Hageman GJ: Poly(ADP-ribose) polymerase-1 mediated caspase-independent cell death after ischemia/reperfusion. Free Radic Biol Med 2005, 39:81-90 (Pubitemid 40733118)
34. Kim MY, Zhang T, Kraus WL: Poly(ADP-ribosyl)ation by PARP-1: "PAR-laying" NAD+ into a nuclear signal. Genes Dev 2005, 19:1951-1967
35. Heeres JT, Hergenrother PJ: Poly(ADP-ribose) makes a date with death. Curr Opin Chem Biol 2007, 11:644-653 (Pubitemid 350180567)
36. Andrabi SA, Kim NS, Yu SW, Wang H, Koh DW, Sasaki M, Klaus JA, Otsuka T, Zhang Z, Koehler RC, Hurn PD, Poirier GG, Dawson VL, Dawson TM: Poly(ADP-ribose) (PAR) polymer is a death signal. Proc Natl Acad Sci U S A 2006, 103:18308-18313 (Pubitemid 44871654)
37. Cohausz O, Blenn C, Malanga M, Althaus FR: The roles of poly(ADP-ribose)- metabolizing enzymes in alkylation-induced cell death. Cell Mol Life Sci 2008, 65:644-655
38. Poitras MF, Koh DW, Yu SW, Andrabi SA, Mandir AS, Poirier GG, Dawson VL, Dawson TM: Spatial and functional relationship between poly(ADP-ribose) polymerase-1 and poly(ADP-ribose) glycohydrolase in the brain. Neuroscience 2007, 148:198-211 (Pubitemid 47224998)
39. Jagtap P, Szabo C: Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat Rev Drug Discov 2005, 4:421-440 (Pubitemid 40704125)
40. Beneke S: Poly(ADP-ribose) polymerase activity in different pathologies: the link to inflammation and infarction. Exp Gerontol 2008, 43:605-614
41. Chopra M, Sharma AC: Distinct cardiodynamic and molecular characteristics during early and late stages of sepsis-induced myocardial dysfunction. Life Sci 2007, 81:306-316 (Pubitemid 47030576)
42. Liaudet L, Pacher P, Mabley JG, Virag L, Soriano FG, Hasko G, Szabo C: Activation of poly(ADP-ribose) polymerase-1 is a central mechanism of lipopolysaccharide-induced acute lung inflammation. Am J Respir Crit Care Med 2002, 165:372-377 (Pubitemid 34118511)
43. Zerfaoui M, Naura AS, Errami Y, Hans CP, Rezk BM, Park J, Elsegeiny W, Kim H, Lord K, Kim JG, Boulares AH: Effects of PARP-1 deficiency on airway inflammatory cell recruitment in response to LPS or TNF: differential effects on CXCR2 ligands and Duffy antigen receptor for chemokines. J Leukoc Biol 2009, 86:1385-1392
44. Altmeyer M, Barthel M, Eberhard M, Rehrauer H, Hardt WD, Hottiger MO: Absence of poly(ADP-ribose) polymerase 1 delays the onset of Salmonella enterica serovar Typhimurium-induced gut inflammation. Infect Immun 2010, 78:3420-3431
45. Czapski GA, Cakala M, Gajkowska B, Strosznajder JB: Poly(ADP-ribose) polymerase-1 inhibition protects the brain against systemic inflammation. Neurochem Int 2006, 49:751-755 (Pubitemid 44648493)
46. Liaudet L, Oddo M: Role of poly(adenosine diphosphate-ribose) polymerase 1 in septic peritonitis. Curr Opin Crit Care 2003, 9:152-158 (Pubitemid 36408135)
47. Ba X, Gupta S, Davidson M, Garg NJ: Trypanosoma cruzi induces the reactive oxygen species-PARP-1-RelA pathway for up-regulation of cytokine expression in cardiomyocytes. J Biol Chem 2010, 285:11596-11606
48. Yang H, Rivera Z, Jube S, Nasu M, Bertino P, Goparaju C, Franzoso G, Lotze MT, Krausz T, Pass HI, Bianchi ME, Carbone M: Programmed necrosis induced by asbestos in human mesothelial cells causes high-mobility group box 1 protein release and resultant inflammation. Proc Natl Acad Sci U S A 2010, 107:12611-12616
49. Brunyanszki A, Hegedus C, Szanto M, Erdelyi K, Kovacs K, Schreiber V, Gergely S, Kiss B, Szabo E, Virag L, Bai P: Genetic ablation of PARP-1 protects against oxazolone-induced contact hypersensitivity by modulating oxidative stress. J Invest Dermatol 2010, 130:2629-2637
50. Genovese T, Mazzon E, Muia C, Patel NS, Threadgill MD, Bramanti P, De Sarro A, Thiemermann C, Cuzzocrea S: Inhibitors of poly(ADP-ribose) polymerase modulate signal transduction pathways and secondary damage in experimental spinal cord trauma. J Pharmacol Exp Ther 2005, 312:449-457 (Pubitemid 40189541)
51. Mota RA, Hernandez-Espinosa D, Galbis-Martinez L, Ordonez A, Minano A, Parrilla P, Vicente V, Corral J, Yelamos J: Poly(ADP-ribose) polymerase-1 inhibition increases expression of heat shock proteins and attenuates heat stroke-induced liver injury. Crit Care Med 2008, 36:526-534 (Pubitemid 351158629)
52. Chiang J, Shen YC, Wang YH, Hou YC, Chen CC, Liao JF, Yu MC, Juan CW, Liou KT: Honokiol protects rats against eccentric exercise-induced skeletal muscle damage by inhibiting NF-kappaB induced oxidative stress and inflammation. Eur J Pharmacol 2009, 610:119-127
53. Thiemermann C, Bowes J, Myint FP, Vane JR: Inhibition of the activity of poly(ADP ribose) synthetase reduces ischemia-reperfusion injury in the heart and skeletal muscle. Proc Natl Acad Sci U S A 1997, 94:679-683 (Pubitemid 27053693)
54. Zingarelli B, Szabo C, Salzman AL: Blockade of poly(ADP-ribose) synthetase inhibits neutrophil recruitment, oxidant generation, and mucosal injury in murine colitis. Gastroenterology 1999, 116:335-345 (Pubitemid 29055356)
55. Pacher P, Liaudet L, Mabley J, Komjati K, Szabo C: Pharmacologic inhibition of poly(adenosine diphosphate-ribose) polymerase may represent a novel therapeutic approach in chronic heart failure. J Am Coll Cardiol 2002, 40:1006-1016 (Pubitemid 34994999)
56. Molnar A, Toth A, Bagi Z, Papp Z, Edes I, Vaszily M, Galajda Z, Papp JG, Varro A, Szuts V, Lacza Z, Gero D, Szabo C: Activation of the poly(ADP-ribose) polymerase pathway in human heart failure. Mol Med 2006, 12:143-152 (Pubitemid 44646343)
57. Von Lukowicz T, Hassa PO, Lohmann C, Boren J, Braunersreuther V, Mach F, Odermatt B, Gersbach M, Camici GG, Stahli BE, Tanner FC, Hottiger MO, Luscher TF, Matter CM: PARP1 is required for adhesion molecule expression in atherogenesis. Cardiovasc Res 2008, 78:158-166 (Pubitemid 351430953)
58. Hans CP, Feng Y, Naura AS, Troxclair D, Zerfaoui M, Siddiqui D, Jihang J, Kim H, Kaye AD, Matrougui K, Lazartigues E, Boulares AH: Opposing roles of PARP-1 in MMP-9 and TIMP-2 expression and mast cell degranulation in dyslipidemic dilated cardiomyopathy. Cardiovasc Pathol 2010, [Epub ahead of press]
59. Oumouna-Benachour K, Hans CP, Suzuki Y, Naura A, Datta R, Belmadani S, Fallon K, Woods C, Boulares AH: Poly(ADP-ribose) polymerase inhibition reduces atherosclerotic plaque size and promotes factors of plaque stability in apolipoprotein E-deficient mice: effects on macrophage recruitment, nuclear factor-kappaB nuclear translocation, and foam cell death. Circulation 2007, 115:2442-2450 (Pubitemid 46717967)
60. Garcia S, Bodano A, Gonzalez A, Forteza J, Gomez-Reino JJ, Conde C: Partial protection against collagen antibody-induced arthritis in PARP-1 deficient mice. Arthritis Res Ther 2006, 8:R14
61. Oumouna M, Datta R, Oumouna-Benachour K, Suzuki Y, Hans C, Matthews K, Fallon K, Boulares H: Poly(ADP-ribose) polymerase-1 inhibition prevents eosinophil recruitment by modulating Th2 cytokines in a murine model of allergic airway inflammation: a potential specific effect on IL-5. J Immunol 2006, 177:6489-6496 (Pubitemid 44628868)
62. Havranek T, Aujla PK, Nickola TJ, Rose MC, Scavo LM: Increased poly(ADP-ribose) polymerase (PARP)-1 expression and activity are associated with inflammation but not goblet cell metaplasia in murine models of allergen-induced airway inflammation. Exp Lung Res 2010, 36:381-389
63. Garcia Soriano F, Virag L, Jagtap P, Szabo E, Mabley JG, Liaudet L, Marton A, Hoyt DG, Murthy KG, Salzman AL, Southan GJ, Szabo C: Diabetic endothelial dysfunction: the role of poly(ADP-ribose) polymerase activation. Nat Med 2001, 7:108-113 (Pubitemid 32095649)
64. Szabo C, Zanchi A, Komjati K, Pacher P, Krolewski AS, Quist WC, LoGerfo FW, Horton ES, Veves A: Poly(ADP-ribose) polymerase is activated in subjects at risk of developing type 2 diabetes and is associated with impaired vascular reactivity. Circulation 2002, 106:2680-2686 (Pubitemid 35364922)
65. Jog NR, Dinnall JA, Gallucci S, Madaio MP, Caricchio R: Poly(ADP-ribose) polymerase-1 regulates the progression of autoimmune nephritis in males by inducing necrotic cell death and modulating inflammation. J Immunol 2009, 182:7297-7306
66. Genovese T, Cuzzocrea S: Role of free radicals and poly(ADP-ribose) polymerase-1 in the development of spinal cord injury: new potential therapeutic targets. Curr Med Chem 2008, 15:477-487 (Pubitemid 351472414)
67. Veres B, Gallyas F Jr, Varbiro G, Berente Z, Osz E, Szekeres G, Szabo C, Sumegi B: Decrease of the inflammatory response and induction of the Akt/protein kinase B pathway by poly-(ADP-ribose) polymerase 1 inhibitor in endotoxin-induced septic shock. Biochem Pharmacol 2003, 65:1373-1382 (Pubitemid 36407788)
68. Galbis-Martinez M, Saenz L, Ramirez P, Parrilla P, Yelamos J: Poly- (ADP-ribose) polymerase-1 modulates interferon-gamma-inducible protein (IP)-10 expression in murine embryonic fibroblasts by stabilizing IP-10 mRNA. Mol Immunol 2010, 47:1492-1499
69. Kaplin AI, Deshpande DM, Scott E, Krishnan C, Carmen JS, Shats I, Martinez T, Drummond J, Dike S, Pletnikov M, Keswani SC, Moran TH, Pardo CA, Calabresi PA, Kerr DA: IL-6 induces regionally selective spinal cord injury in patients with the neuroinflammatory disorder transverse myelitis. J Clin Invest 2005, 115:2731-2741 (Pubitemid 41434400)
70. Park EM, Cho S, Frys K, Racchumi G, Zhou P, Anrather J, Iadecola C: Interaction between inducible nitric oxide synthase and poly- (ADP-ribose) polymerase in focal ischemic brain injury. Stroke 2004, 35:2896-2901 (Pubitemid 39565191)
71. Mazzon E, Genovese T, Di Paola R, Muia C, Crisafulli C, Malleo G, Esposito E, Meli R, Sessa E, Cuzzocrea S: Effects of 3-aminobenzamide, an inhibitor of poly (ADP-ribose) polymerase, in a mouse model of acute pancreatitis induced by cerulein. Eur J Pharmacol 2006, 549:149-156 (Pubitemid 44441255)
72. Kraus WL, Lis JT: PARP goes transcription. Cell 2003, 113:677-683 (Pubitemid 36724932)
73. Ogata N, Ueda K, Hayaishi O: ADP-ribosylation of histone H2B: identification of glutamic acid residue 2 as the modification site. J Biol Chem 1980, 255:7610-7615
74. Aubin RJ, Dam VT, Miclette J, Brousseau Y, Huletsky A, Poirier GG: Hyper(ADP-ribosyl)ation of histone H1. Can J Biochem 1982, 60:1085-1094
75. Andreone TL, O'Connor M, Denenberg A, Hake PW, Zingarelli B: Poly(ADP-ribose) polymerase-1 regulates activation of activator protein-1 in murine fibroblasts. J Immunol 2003, 170:2113-2120 (Pubitemid 36197434)
76. Zingarelli B, Hake PW, Burroughs TJ, Piraino G, O'Connor M, Denenberg A: Activator protein-1 signalling pathway and apoptosis are modulated by poly(ADP-ribose) polymerase-1 in experimental colitis. Immunology 2004, 113:509-517 (Pubitemid 39593370)
77. Hassa PO, Haenni SS, Buerki C, Meier NI, Lane WS, Owen H, Gersbach M, Imhof R, Hottiger MO: Acetylation of poly(ADP-ribose) polymerase-1 by p300/CREB-binding protein regulates coactivation of NF-kappaB-dependent transcription. J Biol Chem 2005, 280:40450-40464 (Pubitemid 41780532)
78. Kameoka M, Ota K, Tetsuka T, Tanaka Y, Itaya A, Okamoto T, Yoshihara K: Evidence for regulation of NF-kappaB by poly(ADP-ribose) polymerase. Biochem J 2000, 346(pt 3):641-649 (Pubitemid 30171024)
79. Zerfaoui M, Errami Y, Naura AS, Suzuki Y, Kim H, Ju J, Liu T, Hans CP, Kim JG, Abd Elmageed ZY, Koochekpour S, Catling A, Boulares AH: Poly(ADP-ribose) polymerase-1 is a determining factor in Crm1-mediated nuclear export and retention of p65 NF-kappa B upon TLR4 stimulation. J Immunol 2010, 185:1894-1902
80. Boulares AH, Zoltoski AJ, Sherif ZA, Jolly P, Massaro D, Smulson ME: Gene knockout or pharmacological inhibition of poly(ADP-ribose) polymerase-1 prevents lung inflammation in a murine model of asthma. Am J Respir Cell Mol Biol 2003, 28:322-329 (Pubitemid 36238009)
81. Mabley JG, Jagtap P, Perretti M, Getting SJ, Salzman AL, Virag L, Szabo E, Soriano FG, Liaudet L, Abdelkarim GE, Hasko G, Marton A, Southan GJ, Szabo C: Anti-inflammatory effects of a novel, potent inhibitor of poly (ADP-ribose) polymerase. Inflamm Res 2001, 50:561-569 (Pubitemid 33121903)
82. Adaikalakoteswari A, Rema M, Mohan V, Balasubramanyam M: Oxidative DNA damage and augmentation of poly(ADP-ribose) polymerase/nuclear factor-kappa B signaling in patients with type 2 diabetes and microangiopathy. Int J Biochem Cell Biol 2007, 39:1673-1684 (Pubitemid 47088311)
83. Chang WJ, Alvarez-Gonzalez R: 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 2001, 276:47664-47670
84. Hossain MB, Ji P, Anish R, Jacobson RH, Takada S: Poly(ADP-ribose) polymerase 1 interacts with nuclear respiratory factor 1 (NRF-1) and plays a role in NRF-1 transcriptional regulation. J Biol Chem 2009, 284:8621-8632
85. Zaniolo K, Desnoyers S, Leclerc S, Guerin SL: Regulation of poly- (ADP-ribose) polymerase-1 (PARP-1) gene expression through the post-translational modification of Sp1: a nuclear target protein of PARP-1. BMC Mol Biol 2007, 8:96
86. Li M, Naidu P, Yu Y, Berger NA, Kannan P: Dual regulation of AP-2alpha transcriptional activation by poly(ADP-ribose) polymerase-1. Biochem J 2004, 382:323-329 (Pubitemid 39141596)
87. Amiri KI, Ha HC, Smulson ME, Richmond A: Differential regulation of CXC ligand 1 transcription in melanoma cell lines by poly(ADP-ribose) polymerase-1. Oncogene 2006, 25:7714-7722 (Pubitemid 44967966)
88. Yu Z, Kuncewicz T, Dubinsky WP, Kone BC: Nitric oxide-dependent negative feedback of PARP-1 trans-activation of the inducible nitricoxide synthase gene. J Biol Chem 2006, 281:9101-9109 (Pubitemid 43864623)
89. Buja LM, Vela D: Cardiomyocyte death and renewal in the normal and diseased heart. Cardiovasc Pathol 2008, 17:349-374
90. Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL: Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 2002, 297:259-263 (Pubitemid 34761289)
91. Yu SW, Andrabi SA, Wang H, Kim NS, Poirier GG, Dawson TM, Dawson VL: Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death. Proc Natl Acad Sci U S A 2006, 103:18314-18319 (Pubitemid 44871655)
92. Modjtahedi N, Giordanetto F, Madeo F, Kroemer G: Apoptosis-inducing factor: vital and lethal. Trends Cell Biol 2006, 16:264-272 (Pubitemid 44250822)
93. Tanaka S, Takehashi M, Iida S, Kitajima T, Kamanaka Y, Stedeford T, Banasik M, Ueda K: Mitochondrial impairment induced by poly- (ADP-ribose) polymerase-1 activation in cortical neurons after oxygen and glucose deprivation. J Neurochem 2005, 95:179-190 (Pubitemid 41384436)
94. Ethier C, Labelle Y, Poirier GG: PARP-1-induced cell death through inhibition of the MEK/ERK pathway in MNNG-treated HeLa cells. Apoptosis 2007, 12:2037-2049 (Pubitemid 47498234)
95. Cipriani G, Rapizzi E, Vannacci A, Rizzuto R, Moroni F, Chiarugi A: Nuclear poly(ADP-ribose) polymerase-1 rapidly triggers mitochondrial dysfunction. J Biol Chem 2005, 280:17227-17234 (Pubitemid 41389190)
96. Blenn C, Althaus FR, Malanga M: Poly(ADP-ribose) glycohydrolase silencing protects against H2O2-induced cell death. Biochem J 2006, 396:419-429 (Pubitemid 44228157)
97. Belenky P, Bogan KL, Brenner C: NAD+ metabolism in health and disease. Trends Biochem Sci 2007, 32:12-19
98. Alano CC, Garnier P, Ying W, Higashi Y, Kauppinen TM, Swanson RA: NAD+ depletion is necessary and sufficient for poly(ADP-ribose) polymerase-1-mediated neuronal death. J Neurosci 2010, 30:2967-2978
99. Alano CC, Ying W, Swanson RA: Poly(ADP-ribose) polymerase-1- mediated cell death in astrocytes requires NAD+ depletion and mitochondrial permeability transition. J Biol Chem 2004, 279:18895-18902 (Pubitemid 38623317)
100. Ying W, Alano CC, Garnier P, Swanson RA: NAD+ as a metabolic link between DNA damage and cell death. J Neurosci Res 2005, 79:216-223 (Pubitemid 40116438)
101. Peralta-Leal A, Rodriguez MI, Oliver FJ: Poly(ADP-ribose)polymerase-1 (PARP-1) in carcinogenesis: potential role of PARP inhibitors in cancer treatment. Clin Transl Oncol 2008, 10:318-323
102. Moncada S, Bolanos JP: Nitric oxide, cell bioenergetics and neurodegeneration. J Neurochem 2006, 97:1676-1689 (Pubitemid 43873660)
103. Pacher P, Szabo C: Role of the peroxynitrite-poly(ADP-ribose) polymerase pathway in human disease. Am J Pathol 2008, 173:2-13 (Pubitemid 351947950)
104. Peralta-Leal A, Rodriguez-Vargas JM, Aguilar-Quesada R, Rodriguez MI, Linares JL, de Almodovar MR, Oliver FJ: PARP inhibitors: new partners in the therapy of cancer and inflammatory diseases. Free Radic Biol Med 2009, 47:13-26
105. Krishnakumar R, Kraus WL: The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol Cell 2010, 39:8-24
106. Tapodi A, Debreceni B, Hanto K, Bognar Z, Wittmann I, Gallyas F Jr, Varbiro G, Sumegi B: Pivotal role of Akt activation in mitochondrial protection and cell survival by poly(ADP-ribose)polymerase-1 inhibition in oxidative stress. J Biol Chem 2005, 280:35767-35775 (Pubitemid 41532770)
107. Kauppinen TM, Chan WY, Suh SW, Wiggins AK, Huang EJ, Swanson RA: Direct phosphorylation and regulation of poly(ADP-ribose) polymerase-1 by extracellular signal-regulated kinases 1/2. Proc Natl Acad Sci U S A 2006, 103:7136-7141
108. Xu Y, Huang S, Liu ZG, Han J: Poly(ADP-ribose) polymerase-1 signaling to mitochondria in necrotic cell death requires RIP1/ TRAF2-mediated JNK1 activation. J Biol Chem 2006, 281:8788-8795 (Pubitemid 43847985)
109. Duan Y, Gross RA, Sheu SS: Ca2+-dependent generation of mitochondrial reactive oxygen species serves as a signal for poly(ADP-ribose) polymerase-1 activation during glutamate excitotoxicity. J Physiol 2007, 585:741-758 (Pubitemid 350278713)
110. Maffi SK, Rathinam ML, Cherian PP, Pate W, Hamby-Mason R, Schenker S, Henderson GI: Glutathione content as a potential mediator of the vulnerability of cultured fetal cortical neurons to ethanol-induced apoptosis. J Neurosci Res 2008, 86:1064-1076 (Pubitemid 351441304)
111. Yakovlev AG, Wang G, Stoica BA, Boulares HA, Spoonde AY, Yoshihara K, Smulson ME: A role of the Ca2+/Mg2+-dependent endonuclease in apoptosis and its inhibition by poly(ADP-ribose) polymerase. J Biol Chem 2000, 275:21302-21308 (Pubitemid 30481828)
112. Szabo C, Pacher P, Zsengeller Z, Vaslin A, Komjati K, Benko R, Chen M, Mabley JG, Kollai M: Angiotensin II-mediated endothelial dysfunction: role of poly(ADP-ribose) polymerase activation. Mol Med 2004, 10:28-35 (Pubitemid 39440318)
113. Du X, Matsumura T, Edelstein D, Rossetti L, Zsengeller Z, Szabo C, Brownlee M: Inhibition of GAPDH activity by poly(ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells. J Clin Invest 2003, 112:1049-1057 (Pubitemid 38056320)
114. Chiu HJ, Fischman DA, Hammerling U: Vitamin A depletion causes oxidative stress, mitochondrial dysfunction, and PARP-1-dependent energy deprivation. FASEB J 2008, 22:3878-3887
115. Gupta S, Bhatia V, Wen JJ, Wu Y, Huang MH, Garg NJ: Trypanosoma cruzi infection disturbs mitochondrial membrane potential and ROS production rate in cardiomyocytes. Free Radic Biol Med 2009, 47:1414-1421
116. Caler EV, Morty RE, Burleigh BA, Andrews NW: Dual role of signaling pathways leading to Ca(2+) and cyclic AMP elevation in host cell invasion by Trypanosoma cruzi. Infect Immun 2000, 68:6602-6610 (Pubitemid 32463360)
117. Burleigh BA, Caler EV, Webster P, Andrews NW: A cytosolic serine endopeptidase from Trypanosoma cruzi is required for the generation of Ca2+ signaling in mammalian cells. J Cell Biol 1997, 136:609-620 (Pubitemid 27083762)
118. Maruyama T, Nara K, Yoshikawa H, Suzuki N: Txk, a member of the non-receptor tyrosine kinase of the Tec family, forms a complex with poly(ADP-ribose) polymerase 1 and elongation factor 1alpha and regulates interferon-gamma gene transcription in Th1 cells. Clin Exp Immunol 2007, 147:164-175 (Pubitemid 44915568)
119. Esposito E, Cuzzocrea S: Superoxide: NO, peroxynitrite and PARP in circulatory shock and inflammation. Front Biosci 2009, 14:263-296
120. Giansanti V, Donà F, Tillhon M, Scovassi AI: PARP inhibitors: new tools to protect from inflammation. Biochem Pharmacol 2010, 80:1869-1877
121. Horvath EM, Benko R, Gero D, Kiss L, Szabo C: Treatment with insulin inhibits poly(ADP-ribose)polymerase activation in a rat model of endotoxemia. Life Sci 2008, 82:205-209
122. Geraets L, Haegens A, Brauers K, Haydock JA, Vernooy JH, Wouters EF, Bast A, Hageman GJ: Inhibition of LPS-induced pulmonary inflammation by specific flavonoids. Biochem Biophys Res Commun 2009, 382:598-603
123. Geraets L, Moonen HJ, Brauers K, Wouters EF, Bast A, Hageman GJ: Dietary flavones and flavonoles are inhibitors of poly(ADP-ribose) polymerase-1 in pulmonary epithelial cells. J Nutr 2007, 137:2190-2195 (Pubitemid 47529575)
124. Mabley JG, Wallace R, Pacher P, Murphy K, Szabo C: Inhibition of poly(adenosine diphosphate-ribose) polymerase by the active form of vitamin D. Int J Mol Med 2007, 19:947-952
125. Vagnerova K, Liu K, Ardeshiri A, Cheng J, Murphy SJ, Hurn PD, Herson PS: Poly (ADP-ribose) polymerase-1 initiated neuronal cell death pathway: do androgens matter? Neuroscience 2010, 166:476-481