Summary
Post-translational modification of proteins with ADP-ribose alters their physical and functional characteristics. The relationship between ADP-ribosylation and several bacterial toxins (e.g. cholera toxin, pertussis toxin, diphtheria toxin) is well established. In contrast, the function of the endogenous ADP-ribosyl transferase enzyme is poorly understood. The latter statement also applies to poly(ADP-ribose) polymerase, although PARP has become familiar due to its association with apoptosis. This article summarizes the enzymology of ADP-ribosylation, reviews the various cellular processes in which it may participate and examines the possible functions of ADP-ribosylation in cardiovascular tissues. Poly (ADP-ribosyl) ation, which has been linked to ischemia-reperfusion injury, is known to participate in DNA repair. In contrast, mono (ADP-ribosyl) ation is best known for modulating G protein function. In the cardiovascular system, mono(ADP-ribosyl)ation may exert effects by modifying growth factors or by transducing the intracellular effects of nitric oxide. Alternatively, mono (ADP-ribosyl) ation could influence cell migration by modifying cytoskeletal proteins. By also examining the role of ADP-ribosylation in other systems, considerable insight into the possible contributions of ADP-ribosylation to cardiovascular function can be extrapolated to both normal and pathological conditions.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
D’Amours D, Desnoyers S, D’Silva I, Poirier GG. 1999. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J 342:249–268.
de Murcia G, Schreiber V, Molinete M, Saulier B, Poch O, Masson M, Niedergang C, Menissier de Murcia J. 1994. Structure and function of poly(ADP-ribose) polymerase. Mol Cell Biochem 138: 15–24.
Lagueux J, Shah GM, Menard L, Thomassin H, Duchaine C, Hengartner C, Poirier GG. 1994. Poly(ADP-ribose) catabolism in mammalian cells. Mol Cell Biochem 138:45–52.
Shall S. 1994. The function of poly (ADP-ribosylation) in DNA breakage and rejoining. Mol Cell Biochem 138:71–75.
Negri C, Donzelli M, Bernardi R, Rossi L, Burkle A, Scovassi AI. 1997. Multiparametric staining to identify apoptotic human cells. Exp Cell Res 234:174–177.
Pieper AA, Verma A, Zhang J, Snyder SH. 1999. Poly (ADP-ribose) polymerase, nitric oxide and cell death. Trends Pharmacol Sci 20:171–181.
Rosenthal DS, Ding R, Simbulan-Rosenthal CM, Vaillancourt JP, Nicholson DW, Smulson M. 1997. Intact cell evidence for the early synthesis, subsequent late apopain-mediated suppression, of poly(ADP-ribose) during apoptosis. Exp Cell Res 232:313–321.
Scovassi AI, Poirier GG. 1999. Poly(ADP-ribosylation) and apoptosis. Mol Cell Biochem 199: 125–137.
Burkle A, Muller M, Wolf I, Kupper JH. 1994. Poly(ADP-ribose) polymerase activity in intact or permeabilized leukocytes from mammalian species of different longevity. Mol Cell Biochem 138:85–90.
Grube K, Burkle A. 1992. Poly (ADP-ribose) polymerase activity in mononuclear leukocytes of 13 mammalian species correlates with species-specific life span. Proc Natl Acad Sci USA 89:11759–11763.
Hayaishi O, Ueda K. 1977. Poly(ADP-ribose) and ADP-ribosylation of proteins. Annu Rev Biochem 46:95–116.
Kleczkowska HE, Althaus FR. 1996. The role of poly(ADP-ribosyl)ation in the adaptive response. Mutat Res 358:215–221.
Purnell MR, Stone PR, Whish WJ. 1980. ADP-ribosylation of nuclear proteins. Biochem Soc Trans 8:215–227.
Zahradka P, Ebisuzaki K. 1982. A shuttle mechanism for DNA-protein interactions. The regulation of poly(ADP-ribose) polymerase. Eur J Biochem 127:579–585.
Lindahl T, Satoh MS, Poirier GG, Klungland A. 1995. Post-translational modification of poly(ADP-ribose) polymerase induced by DNA strand breaks. Trends Biochem Sci 20:405–411.
Schraufstatter IU, Hyslop PA, Hinshaw DB, Spragg RG, Sklar LA, Cochrane CG. 1986. Hydrogen peroxide-induced injury of cells and its prevention by inhibitors of poly(ADP-ribose) polymerase. Proc Natl Acad Sci USA 83:4908–4912.
Kirkland JB. 1991. Lipid peroxidation, protein thiol oxidation and DNA damage in hydrogen peroxide-induced injury to endothelial celkrole of activation of poly(ADP-ribose)polymerase. Biochim Biophys Acta 1092:319–325.
Thies RL, Alitor AR 1991. Reactive oxygen injury to cultured pulmonary artery endothelial cells:mediation by poly(ADP-ribose) polvmerase activation causing NAD depletion and altered energy balance. Arch Biochem Biophys 286:353–363.
Yamamoto K, Tsukidate K, Farber JL. 1993. Differing effects of the inhibition of poly(ADP-ribose) polymerase on the course of oxidative cell injury in hepatocytes and fibroblasts. Biochem Pharmacol 46:483–491.
Szabo C, Cuzzocrea S, Zingarelli B, O’Connor M, Salzman AL. 1997. Endothelial dysfunction in a rat model of endotoxic shock. Importance of the activation of poly (ADP-ribose) synthetase by peroxynitnte. J Clin Invest 100:723–735.
Bowes J, Ruetten H, Martorana PA, Stockhausen H, Thiemermann C. 1998. Reduction of myocardial reperfusion injury by an inhibitor of poly (ADP-ribose) synthetase in the pig. Eur J Pharmacol 359:143–150.
Stubberfield CR, Cohen CM. 1988. NAD+ depletion and cytotoxicity in isolated hepatocytes. Biochem Pharmacol 37:3967–3974.
Desnoyers S, Shah CM, Brochu G, Hoflack JC, Verreault A, Poirier GG. 1995. Biochemical properties and function of poly(ADP-ribose) glycohydrolase. Biochimie 77:433–438.
Smulson ME. 1994. Poly(ADP-ribose) polymerase gene on chromosome 1q: early role in differentiation linked replication; gene on human chromosome 13q: marker of carcinogenesis. Mol Cell Biochem 138:77–84.
Smulson ME, Pang D, Jung M, Dimtchev A, Chasovskikh S, Spoonde A, Simbulan-Rosenthal C, Rosenthal D,Yakovlev A, Dritschilo A. 1998. Irreversible binding of poly(ADP)ribose polymerase cleavage product to DNA ends revealed by atomic force microscopy: possible role in apoptosis. Cancer Res 58:3495–3498.
Alvarez-Gonzalez R, Pacheco-Rodriguez G, Mendoza-Alvarez H. 1994. Enzymology of ADP-ribose polymer synthesis. Mol Cell Biochem 138:33–37.
Alvarez-Gonzalez R, Jacobson MK. 1987. Characterization of polymers of adenosine diphosphate ribose generated in vitro and in vivo. Biochemistry 26:3218–3224.
Kiehlbauch CC, Aboul-Ela N, Jacobson EL, Ringer DP, Jacobson MK. 1993. High resolution fractionation and characterization of ADP-ribose polymers. Anal Biochem 208:26–34.
Bauer PI, Buki KG, Hakam A, Kun E. 1990. Macromolecular association of ADP-ribosyltransferase and its correlation with enzymic activity. Biochem J 270:17–26.
Mendoza-Alvarez H, Alvarez-Gonzalez R. 1993. Poly(ADP-ribose) polymerase is a catalytic dimer and the automodification reaction is intermolecular. J Biol Chem 268:22575–22580.
Oei SL, Gnesenbeck J, Buchlow G, Jorcke D, Mayer-Kuckuk P, Wons T, Ziegler M. 1996. NAD+ analogs substituted in the purine base as substrates for poly(ADP-ribosyl) transferase. FEBS Lett 397:17–21.
Satoh MS, Lindahl T. 1992. Role of poly(ADP-ribose) formation in DNA repair. Nature 356: 356–358.
Boulikas T. 1988. At least 60 ADP-ribosylated variant histones are present in nuclei from dimethylsulfate-treated and untreated cells. EMBO J 7:57–67.
Boulikas T. 1990. Poly(ADP-ribosylated) histones in chromatin replication. J Biol Chem 265: 14638–14647.
Huletsky A, Niedergang C, Frechette A, Aubin R, Gaudreau A, Poirier GG. 1985. Sequential ADP-ribosylation pattern of nucleosomal histones. ADP-ribosylation of nucieosomal histones. Eur J Biochem 146:277–285.
Simbulan CM, Suzuki M, Izuta S, Sakurai T, Savoysky E, Kojima K, Miyahara K, Shizuta Y, Yoshida S. 1993. Poly(ADP-ribose) polymerase stimulates DNA polymerase alpha by physical association. J Biol Chem 268:93–99.
Yoshida S, Simbulan CM. 1994. Interaction of poly(ADP-ribose)polymerase with DNA polymerase alpha. Mol Cell Biochem 138:39–44.
Tanaka Y, Yoshihara K, Itaya A, Kamiya T, Koide SS. 1984. Mechanism of the inhibition of Ca2+, Mg2+-dependent endonuclease of bull seminal plasma induced by ADP-ribosylation. J Biol Chem 259:6579–6585.
Ferro AM, Olivera BM. 1984. Poly(ADP-ribosylation) of DNA topoisomerase I from calf thymus. J Biol Chem 259:547–554.
Kasid UN, Halligan B, Liu LF, Dritschilo A, Smulson M. 1989. Poly (ADP-ribose)-mediated post-translational modification of chromatin-associated human topoisomerase I. Inhibitory effects on catalytic activity. J Biol Chem 264:18687–18692.
Creissen D, Shall S. 1982. Regulation of DNA ligase activity by poly(ADP-ribose). Nature 296: 271–272.
Tanuma S, Johnson GS. 1983. ADP-ribosylation of nonhistone high mobility group proteins in intact cells. J Biol Chem 258:4067–4070.
Tanuma S, Yagi T, Johnson GS. 1985. Endogenous ADP ribosylation of high mobility group proteins 1 and 2 and histone H1 following DNA damage in intact cells. Arch Biochem Biophys 237:38–42.
Furneaux HM, Pearson CK. 1980. Intracellular NAD+ content and ADP-ribose polymerase activity of serum-stimulated baby hamster kidney fibroblasts. J Cell Physiol 105:401–407.
Taniguchi T, Suzuki S, Shizuta Y. 1985. Poly (ADP-ribosyl)ation of RNA polymerase II from wheat germ. Biochem Biophys Res Commun 127:526–532.
Amstad PA, Krupitza G, Cerutti PA. 1992. Mechanism of c-fos induction by active oxygen. Cancer Res 52:3952–3960.
Malanga M, Pleschke JM, Kleczkowska HE, Althaus FR. 1998. Poly(ADP-ribose) binds to specific domains of p53 and alters its DNA binding functions. J Biol Chem 273:11839–11843.
Pleschke JM, Kleczkowska HE, Strohm M, Althaus FR. 2000. Poly(ADP-ribose) binds to specific domains in DNA checkpoint proteins. J Biol Chem 275:40974–40980.
Simbulan-Rosenthal CM, Rosenthal DS, Luo R, Smulson ME. 1999. Poly(ADP-ribosyl)ation of p53 during apoptosis in human osteosarcoma cells. Cancer Res 59:2190–2194.
Adamietz P. 1987. Poly (ADP-ribose) synthase is the major endogenous nonhistone acceptor for poly(ADP-ribose) in alkylated rat hepatoma cells. Eur J Biochem 169:365–372.
Kawaichi M, Ueda K, Hayaishi O. 1981. Multiple autopoly(ADP-ribosyl)ation of rat liver poly(ADP-ribose) synthetase. Mode of modification and properties of automodified synthetase. J Biol Chem 256:9483–9489.
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 259:890–896.
Yoshihara K, Hashida T, Yoshihara H, Tanaka Y, Ohgushi H. 1977. Enzyme-bound early product of purified poly(ADP-ribose) polymerase. Biochem Biophys Res Commun 78:1281–1288.
de Murcia JM, Niedergang C, Trucco C, Ricoul M, Dutrillaux B, Mark M, Oliver FJ, Masson M, Dierich A, LeMeur M, Walztinger C, Chambon P, de Murcia G. 1997. Requirement of poly (ADP-ribose) polymerase in recovery from DNA damage in mice and in cells. Proc Natl Acad Sci USA 94:7303–7307.
Berger NA. 1985. Poly(ADP-ribose) in the cellular response to DNA damage. Radiat Res 101:4–15.
Carson DA, Seto S, Wasson DB, Carrera CJ. 1986. DNA strand breaks, NAD metabolism, and programmed cell death. Exp Cell Res 164:273–281.
Tanizawa A, Kubota M, Hashimoto H, Shimizu T, Takimoto T, Kitoh T, Akiyama Y, Mikawa H. 1989. VP-16-induced nucleotide pool changes and poly(ADP-ribose) synthesis: the role of VP-16 in interphase death. Exp Cell Res 185:237–246.
Wintersberger U, Wintersberger E. 1985. Poly ADP-ribosylation-a cellular emergency reaction? FEBS Lett 188:189–191.
Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier GG, Earnshaw WC. 1994. Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371:346–347.
Scovassi AI, Denegri M, Donzelli M, Rossi L, Bernardi R, Mandarino A, Frouin I, Negri C. 1998. Poly(ADP-ribose) synthesis in cells undergoing apoptosis: an attempt to face death before PARP degradation. Eur J Histochem 42:251–258.
Kuo ML, Chau YP, Wang JH, Shiah SG. 1996. Inhibitors of poly(ADP-ribose) polymerase block nitric oxide-induced apoptosis but not differentiation in human leukemia HL-60 cells. Biochem Biophys Res Commun 219:502–508.
Malorni W, Rivabene R, Straface E, Rainaldi G, Monti D, Salvioli S, Cossarizza A, Franceschi C. 1995. 3-Aminobenzamide protects cells from UV-B-induced apoptosis by acting on cytoskeleton and substrate adhesion. Biochem Biophys Res Commun 207:715–724.
Beneke R, Geisen C, Zevnik B, Bauch T, Muller WU, Kupper JH, Moroy T 2000. DNA excision repair and DNA damage-induced apoptosis are linked to Poly(ADP-ribosyl)ation but have different requirements for p53. Mol Cell Biol 20:6695–6703.
Kapasi AA, Singhal PC. 1999. Aging splenocyte and thymocyte apoptosis is associated with enhanced expression of p53. bax. and caspase-3. Mol Cell Biol Res Commun 1:78–81.
Simbulan-Rosenthal CM, Rosenthal DS, Boulares AH, Hickey RJ, Malkas LH, Coll JM, Smulson ME. 1998. Regulation of the expression or recruitment of components of the DNA synthesome by poly(ADP-ribose) polymerase. Biochemistry 37:9363–9370.
Wein KH, Netzker R, Brand K. 1993. Cell cycle-related expression of poly(ADP-ribosyl) transferase in proliferating rat thymocytes. Biochim Biophys Acta 1176:69–76.
Ghani QP, Hussain MZ, Zhang J, Hunt KH. 1992. Control of procollagen gene transcription and prolyl hydroxylase activity by poly(ADP-ribose) In: ADP-ribosylation reactions. Ed. GG Poirier and P Moreau, 211–217. New York: Springer-Verlag.
Leverence RR, Beale EG, Granner DK. 1988. 3-Aminobenzamide inhibits poly(ADP ribose) synthetase activity and induces phosphoenolpyruvate carboxykinase (GTP) in H4IIE hepatoma cells. Arch Biochem Biophys 260:667–673.
Yau L, Elliot T, Lalonde C, Zahradka P. 1998. Repression of phosphoenolpyruvate carboxykinase gene activity by insulin is blocked by 3-aminobenzamide but not by PD128763, a selective inhibitor of poly(ADP-ribose) polymerase. Eur J Biochem 253:91–100.
Zahradka P, Yau L. 1994. ADP-ribosylation and gene expression. Mol Cell Biochem 138:91–98.
Quesada P, d’Erme M, Parise G, Faraone-Mennella MR, Caiara P, Farina B. 1994. Nuclear matrix-associated poly(ADPribosyl)ation system in rat testis chromatin. Exp Cell Res 214:351–357.
Quesada P, Tramontano F, Faraone-Mennella MR, Farina B. 2000. The analysis of the poly(ADPR) polymerase mode of action in rat testis nuclear fractions defines a specific poly(ADP-ribosyl)ation system associated with the nuclear matrix. Mol Cell Biochem 205:91–99.
Hassa PO, Hottiger MO. 1999. A role of poly (ADP-ribose) polymerase in NF-kappaB transcriptional activation. Biol Chem 380:953–959.
Kameoka M, Ota K, Tetsuka T, Tanaka Y, Itaya A, Okamoto T, Yoshihara K. 2000. Evidence for regulation of NF-kappaB by poly(ADP-ribose) polymerase. Biochem J 346:641–649.
Oliver FJ, Menissier-de Murcia J, Nacci C, Decker P, Andnantsitohaina 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 18:4446–4454.
Pero RW, Axelsson B, Siemann D, Chaplin D, Dougherty G. 1999. Newly discovered antiinflammatory properties of the benzamides and nicotinamides. Mol Cell Biochem 193:119–125.
Ittel ME, Jongstra-Bilen J, Rochette-Egly C, Mandel P. 1983. Involvement of polyADP-ribose poly-merase in the initiation of phytohemagglutinin induced human lymphocyte proliferation. Biochem Biophys Res Commun 116:428–434.
Colon-Otero G, Sando JJ, Sims JL, McGrath E, Jensen DE, Quesenberry PJ. 1987. Inhibition of hemopoietic growth factor-induced proliferation by adenosine diphosphate-ribosylation inhibitors. Blood 70:686–693.
Cui Y, An S, Jabr S, Maturana JA, Wu JM, Gutstein WH. 1993. The anti-proliferative effects of nicotinamide and 3-aminobenzamide on human smooth muscle cells in vitro. Biochem Mol Biol Int 31:935–944.
Francis GE, Gray DA, Berney JJ, Wing MA, Guimaraes JE, Hoffbrand AV. 1983. Role of ADP-ribosyl transferase in differentiation of human granulocyte-macrophage progenitors to the macrophage lineage. Blood 62:1055–1062.
Ebisuzaki K, Casley WL, Griffiths A, Wheaton L. 1991. Temporal mapping of the differentiation pathway of the murine erythroleukemia cell. Cancer Res 51:1668–1673.
Bhatia M, Kirkland JB, Meckling-Gill KA. 1995. Modulation of poly(ADP-ribose) polymerase during neutrophilic and monocytic differentiation of promyelocytic (NB4) and myelocytic (HL-60) leukaemia cells. Biochem J 308:131–137.
Bhatia M, Kirkland JB, Meckling-Gill KA. 1996. Overexpression of poly(ADP-ribose) polymerase promotes cell cycle arrest and inhibits neutrophilic differentiation of NB4 acute promyelocytic leukemia cells. Cell Growth Differ 7:91–100.
Lea MA, Barra R, Randolph V, Kuhr WG. 1984. Effects of nicotinamide and structural analogs on DNA synthesis and cellular replication of rat hepatoma cells. Cancer Biochem Biophys 7:195–202.
Bowes J, McDonald MC, Piper J, Thiemermann C. 1999. Inhibitors of poly (ADP-ribose) synthetase protect rat cardiomyocytes against oxidant stress. Cardiovasc Res 41:126–134.
Thiemermann C, Bowes J, Myint FP, Vane JR. 1997. Inhibition of the activity of poly(ADP ribose) synthetase reduces ischemia-repertusion injury in the heart and skeletal muscle. Proc Natl Acad Sci USA 94:679–683.
Thyberg J, Hultgardh-Nilsson A, Kallin B. 1995. Inhibitors of ADP-ribosylation suppress pheno-typic modulation and proliferation of smooth muscle cells cultured from rat aorta. Differentiation 59:243–252.
Grainger DJ, Hesketh TR, Weissberg PL, Metcalfe JC. 1992. Hexamethylenebisacetamide selectively inhibits the proliferation of human and rat vascular smooth-muscle cells. Biochem J 283:403–408.
Weissberg PL, Grainger DJ, Shanahan CM, Metcalfe JC. 1993. Approaches to the development of selective inhibitors of vascular smooth muscle cell proliferation. Cardiovasc Res 27:1191–1198.
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 9:509–520.
Trucco C, Oliver FJ, de Murcia G, Menissier-de Murcia J. 1998. DNA repair defect in poly(ADP-ribose) polymerase-deficient cell lines. Nucleic Acids Res 26:2644–2649.
Masutani M, Suzuki H, Kamada N, Watanabe M, Ueda O, Nozaki T, Jishage K, Watanabe T, Sugimoto T, Nakagama H, Ochiya T, Sugimura T. 1999. Poly(ADP-ribose) polymerase gene disruption conferred mice resistant to streptozotocin-induced diabetes. Proc Natl Acad Sci USA 96:2301–2304.
Shieh WM, Ame JC, Wilson MV, Wang ZQ, Koh DW, Jacobson MK, Jacobson EL. 1998. Poly(ADP-ribose) polymerase null mouse cells synthesize ADP-ribose polymers. J Biol Chem 273: 30069–30072.
Ame JC, Rolli V, Schreiber V, Niedergang C, Apiou F, Decker P, Muller S, Hoger T, Menissier-de Murcia J, de Murcia G. 1999. PARP-2, A novel mammalian DNA damage-dependent poly(ADP-ribose) polymerase. J Biol Chem 274:17860–17868.
Johansson M. 1999. A human poly(ADP-ribose) polymerase gene family (ADPRTL):cDNA cloning of two novel poly(ADP-ribose) polymerase homologues. Genomics 57:442–445.
Shall S, de Murcia G. 2000. Poly(ADP-ribose) polymerase-1: what have we learned from the deficient mouse model? Mutat Res 460:1–15.
Smith S. 2001. The world according to PARP. Trends Biochem Sci 26:174–179.
Kickhoefer VA, Siva AC, Kedersha NL, Inman EM, Ruland C, Streuh M, Rome LH. 1999. The 193-kD vault protein, VPARP, is a novel poly(ADP-ribose) polymerase. J Cell Biol 146:917–928.
Chugani DC, Rome LH, Kedersha NL. 1993. Evidence that vault ribonucleoprotein particles localize to the nuclear pore complex. J Cell Sci 106:23–29.
Chypre C, Maniez C, Mandel P. 1988. Cytoplasmic poly (ADP-ribose) polymerase associated with free messenger ribonucleoprotein particles in rat brain. J Neurochem 51:561–565.
Jesser M, Chypre C, Hog F, Mandel P. 1993. Cytoplasmic poly(ADP-ribose)polymerase from mouse plasmacytoma free messenger ribonucleoprotein particles:purification and characterization. Biochem Biophys Res Commun 195:558–564.
Moss J, Zolkiewska A, Okazaki I. 1997. ADP-ribosylarginine hydrolases and ADP-ribosyl-transferases. Partners in ADP-ribosylation cycles. Adv Exp Med Biol 419:25–33.
Okazaki IJ, Moss J. 1996. Structure and function of eukaryotic mono-ADP-ribosyltransferases. Rev Physiol Biochem Pharmacol 129:51–104.
Zolkiewska A, Okazaki IJ, Moss J. 1994. Vertebrate mono-ADP-ribosyltransferases. Mol Cell Biochem 138:107–112.
Soman G, Graves DJ. 1988. Endogenous ADP-ribosylation in skeletal muscle membranes. Arch Biochem Biophys 260:56–66.
Kharadia SV, Huiatt TW, Huang HY, Peterson JE, Graves DJ. 1992. Effect of an arginine-specific ADP-ribosyltransferase inhibitor on differentiation of embryonic chick skeletal muscle cells in culture. Exp Cell Res 201:33–42.
Norgauer J, Kownatzki E, Seifert R, Aktories K. 1988. Botulinum C2 toxin ADP-ribosylates actin and enhances O2- production and secretion but inhibits migration of activated human neutrophils. J Clin Invest 82:1376–1382.
Saxty BA, Yadollahi-Farsani M, Kefalas P, Paul S, MacDermot J. 1998. Inhibition of chemotaxis in A7r5 rat smooth muscle cells by a novel panel of inhibitors. Br J Pharmacol 125:152–158.
Saxty B, Yadollahi-Farsani M, Kefalas P, Paul S, MacDermot J. 1998. ADP-ribosyltransferase inhibitors and pseudo-substrates inhibit rat smooth muscle cell migration in vitro. Biochem Soc Trans 26:S130
Stasia MJ, Jouan A, Bourmeyster N, Boquet P, Vignais PV. 1991. ADP-ribosylation of a small size GTP-binding protein in bovine neutrophils by the C3 exoenzyme of Clostridium botulinum and effect on the cell motility. Biochem Biophys Res Commun 180:615–622.
Brune B, Dimmeler S, Molina y Vedia L, Lapetina EG. 1994. Nitric oxide:a signal for ADP-ribosylation of proteins. Life Sci 54:61–70
Hilz H. 1997. ADP-ribose. A historical overview. Adv Exp Med Biol 419:15–24.
Zolkiewska A, Moss J. 1993. Integrin alpha 7 as substrate for a glycosylphosphatidyhnositol-anchored ADP-ribosyltransferase on the surface of skeletal muscle cells. J Biol Chem 268:25273–25276.
Zolkiewska A, Nightingale MS, Moss J. 1992. Molecular characterization of NAD: arginine ADP-ribosyltransferase from rabbit skeletal muscle. Proc Natl Acad Sci USA 89:11352–11356.
Takada T, Okazaki IJ, Moss J. 1994. ADP-ribosylarginine hydrolases. Mol Cell Biochem 138: 119–122.
Williamson KC, Moss J. 1990. Mono-ADP-ribosyltransferases and ADP-ribosylarginine hydrolases: a Mono-ADP-ribosylation cycle in animal cells. In: ADP-ribosylating toxins and G proteins: Insights into signal. Ed. J Moss, M Vaughan, 493–510. Washington: American Society for Microbiology
Moss J, Tsai SC, Adamik R, Chen HC, Stanley SJ. 1988. Purification and characterization of ADP-ribosylarginine hydrolase from turkey erythrocytes. Biochemistry 27:5819–5823.
Smith KP, Benjamin RC, Moss J, Jacobson MK. 1985. Identification of enzymatic activities which process protein bound mono(ADP-ribose). Biochem Biophys Res Commun 126:136–142.
Chang YC, Soman G, Graves DJ. 1986. Identification of an enzymatic activity that hydrolyzes protein-bound ADP-ribose in skeletal muscle. Biochem Biophys Res Commun 139:932–939.
Moss J, Stanley SJ, Nightingale MS, Murtagh JJ, Jr., Monaco L, Mishima K, Chen HC, Williamson KC, Tsai SC. 1992. Molecular and immunological characterization of ADP-ribosylarginine hydrolases. J Biol Chem 267:10481–10488.
Graves JD, Krebs EG. 1999. Protein phosphorylation and signal transduction. Pharmacol Ther 82: 111–121.
Okazaki IJ, Moss J. 1999. Characterization of glycosylphosphatidylinositiol-anchored, secreted, and intracellular vertebrate mono-ADP-ribosyltransferases. Annu Rev Nutr 19:485–509.
Zolkiewska A, Moss J. 1997. The alpha 7 integrin as a target protein for cell surface mono-ADP-ribosylation in muscle cells. Adv Exp Med Biol 419:297–303.
Gill DM, Meren R. 1978. ADP-ribosylation of membrane proteins catalyzed by cholera toxin: basis of the activation of adenylate cyclase. Proc Natl Acad Sci USA 75:3050–3054.
Honjo T, Nishizuka Y, Hayaishi O. 1968. Diphtheria toxin-dependent adenosine diphosphate ribosylation of aminoacyl transferase II and inhibition of protein synthesis. J Biol Chem 243: 3553–3555.
Moss J, Vaughan M. 1977. Mechanism of action of choleragen. Evidence for ADP-ribosyl-transferase activity with arginine as an acceptor. J Biol Chem 252:2455–2457.
Aktories K. 1994. Clostridial ADP-ribosylating toxins: effects on ATP and GTP-binding proteins. Mol Cell Biochem 138:167–176.
Aktories K. 1997. Rho proteins: targets for bacterial toxins. Trends Microbiol 5:282–288.
Gierschik P. 1992. ADP-ribosylation of signal-transducing guanine nucleotide-binding proteins by pertussis toxin. Curr Top Microbiol Immunol 175:69–96.
Lerm M, Schmidt G, Aktories K. 2000. Bacterial protein toxins targeting rho GTPases. FEMS Microbiol Lett 188:1–6.
Moss J. 1987. Signal transduction by receptor-responsive guanyl nucleotide-binding proteins: modulation by bacterial toxin-catalyzed ADP-ribosylation. Clin Res 35:451–458.
Popoff MR. 1998. Interactions between bacterial toxins and intestinal cells. Toxicon 36:665–685.
Moss J, Stanley SJ. 1981. Histone-dependent and histone-independent forms of an ADP-ribosyltransferase from human and turkev erythrocytes. Proc Natl Acad Sci USA 78:4809–4812.
Moss J, Stanley SJ, Wukins PA. 1980. Isolation and properties of an NAD- and guanidine-depen-dent ADP- ribosyltransferase from turkey erythrocytes. J Biol Chem 255:5838–5840.
Moss J, Stanley SJ. 1981. Amino acid-specific ADP-ribosylation. Identification of an arginine-dependent ADP-ribosyltransferase in rat liver. J Biol Chem 256:7830–7833.
Godeau F, Belin D, Koide SS. 1984. Mono(adenosine diphosphate ribosyl) transferase in Xenopus tissues. Direct demonstration by a zymographic localization in sodium dodecyl sulfate—polyacrylamide gels. Anal Biochem 137:287–296.
Tsuchiya M, Shimoyama M. 1994. Target protein for eucaryotic arginine-specific ADP-ribosyltransferase. Mol Cell Biochem 138:113–118.
Fujita H, Okamoto H, Tsuyama S. 1995. ADP-ribosylation in adrenal glands: purification and characterization of mono-ADP-ribosyltransferases and ADP-ribosylhydrolase affecting cytoskeletal actin. Int J Biochem Cell Biol 27:1065–1078.
Matsuyama S, Tsuyama S. 1991. Mono-ADP-ribosylation in brain: purification and characterization of ADP-ribosyltransferases affecting actin from rat brain. J Neurochem 57:1380–1387.
Duman RS, Terwilliger RZ, Nestler EJ. 1991. Endogenous ADP-ribosylation in brain: initial characterization of substrate proteins. J Neurochem 57:2124–2132.
Hara N, Mishima K, Tsuchiya M, Tanigawa Y, Shimoyama M. 1987. Mono(ADP-ribosyl)ation of Ca2+-dependent ATPase in rabbit skeletal muscle sarcoplasmic reticulum and the effect of poly L-lysine. Biochem Biophys Res Commun 144:856–862.
Obara S, Mishima K, Yamada K, Taniguchi M, Shimoyama M. 1989. DNA-regulated arginine-specific mono(ADP-ribosyl)ation and de-ADP-ribosylation of endogenous acceptor proteins in human neutrophils. Biochem Biophys Res Commun 163:452–457.
Obara S, Yamada K, Yoshimura Y, Shimoyama M. 1991. Evidence for the endogenous GTP-dependent ADP-ribosylation of the alpha-subunit of the stimulatory guanyl-nucleotide-binding protein concomitant with an increase in basal adenylyl cyclase activity in chicken spleen cell mem-brane. Eur J Biochem 200:75–80.
Peterson JE, Larew JS, Graves DJ. 1990. Purification and partial characterization of arginine-specific ADP-ribosyltransferase from skeletal muscle microsomal membranes. J Biol Chem 265: 17062–17069.
Piron KJ, McMahon KK. 1990. Localization and partial characterization of ADP-ribosylation products in hearts from adult and neonatal rats. Biochem J 270:591–597.
Soman G, Haregewoin A, Horn RC, Finberg RW. 1991. Guanidine group specific ADP-ribosyltransferase in murine cells. Biochem Biophys Res Commun 176:301–308.
Soman G, Mickelson JR, Louis CF, Graves DJ. 1984. NAD: guanidino group specific mono ADP-ribosyltransferase activity in skeletal muscle. Biochem Biophys Res Commun 120:973–980.
Soman G, Tomer KB, Graves DJ. 1983. Assay of mono ADP-ribosyltransferase activity by using guanylhydrazones. Anal Biochem 134:101–110.
Yamashita A, Sato E, Yasuda H, Kurokawa T, Ishibashi S. 1991. Reduction of mono(ADP-ribosyl)ation of 20kDa protein with maturation in rat testis: involvement of guanine nucleotides. Biochim Biophys Acta 1091:46–50.
Ledford BE, Leno GH. 1994. ADP-ribosylation of the molecular chaperone GRP78/BiP. Mol Cell Biochem 138:141–148.
Leno GH, Ledford BE. 1989. ADP-ribosylation of the 78-kDa glucose-regulated protein during nutritional stress. Eur J Biochem 186:205–211.
Li PL, Chen CL, Bortell R, Campbell WB. 1999. 11,12-Epoxyeicosatrienoic acid stimulates endogenous mono-ADP-ribosylation in bovine coronary arterial smooth muscle. Circ Res 85:349–356.
Halldorsson H, Bodvarsdottir T, Kjeld M, Thorgeirsson G. 1992. Role of ADP-ribosylation in endothelial signal transduction and prostacyclin production. FEBS Lett 314:322–326.
Domenighini M, Rappuoli R. 1996. Three conserved consensus sequences identify the NAD-binding site of ADP-ribosylating enzymes, expressed by eukaryotes, bacteria and T-even bacterio-phages. Mol Microbiol 21:667–674.
Takada T, Iida K, Moss J. 1995. Conservation of a common motif in enzymes catalyzing ADP-ribose transfer. Identification of domains in mammalian transferases. J Biol Chem 270:541–544.
Ferguson MA, Williams AF. 1988. Cell-surface anchoring of proteins via glycosyl-phosphatidylinositol structures. Annu Rev Biochem 57:285–320.
Low MG. 1989. Glycosyl-phosphatidylinositol: a versatile anchor for cell surface proteins. FASEB J 3:1600–1608.
Okazaki IJ, Moss J. 1998. Glycosylphosphatidylinositol-anchored and secretory isoforms of mono-ADP-ribosyltransferases. J Biol Chem 273:23617–23620.
Weng B, Thompson WC, Kim HJ, Levine RL, Moss J. 1999. Modification of the ADP-ribosyltransferase and NAD glycohydrolase activities of a mammalian transferase (ADP-ribosyltransferase 5) by auto-ADP-ribosylation. J Biol Chem 274:31797–31803.
Taniguchi M, Tsuchiya M, Shimoyama M. 1993. Comparison of acceptor protein specificities on the formation of ADP-ribose.acceptor adducts by arginine-specific ADP-ribosyltransferase from rabbit skeletal muscle sarcoplasmic reticulum with those of the enzyme from chicken peripheral polymorphonuclear cells. Biochim Biophys Acta 1161:265–271.
Huang HY, Graves DJ, Robson RM, Huiatt TW. 1993. ADP-ribosylation of the intermediate filament protein desmin and inhibition of desmin assembly in vitro by muscle ADP-ribosyltransferase. Biochem Biophys Res Commun 197:570–577.
Wang J, Nemoto E, Dennert G. 1996. Regulation of CTL by ecto-nictinamide adenine dinucleotide (NAD) involves ADP-ribosvlation of a p56kk-associated protein. J Immunol 156:2819–2827.
Okazaki IJ, Moss J. 1996. Mono-ADP-ribosylation: a reversible posttranslational modification of proteins. Adv Pharmacol 35:247–280.
Donnelly LE, Boyd RS, MacDermot J. 1992. Gs alpha is a substrate for mono(ADP-ribosyl) transferase of NG108-15 cells. ADP-ribosylation regulates Gs alpha activity and abundance. Biochem J 288:331–336.
Jacquemin C, Thibout H, Lambert B, Correze C. 1986. Endogenous ADP-ribosylation of Gs subunit and autonomous regulation of adenylate cyclase. Nature 323:182–184.
Molina y Vedia L, Nolan RD, Lapetina EG. 1989. The effect of lloprost on the ADP-ribosylation of Gs alpha (the alpha-subunit of Gs). Biochem J 261:841–845.
Saxty BA, van Heyningen S. 1995. The purification of a cysteine-dependent NAD+ glycohydro-lase activity from bovine erythrocytes and evidence that it exhibits a novel ADP- ribosyltransferase activity. Biochem J 310:931–937.
Tanuma S, Kawashima K, Endo H. 1988. Eukaryotic mono(ADP-ribosyl)transferase that ADP-ribosylates GTP-binding regulatory Gi protein. J Biol Chem 263:5485–5489.
McDonald LJ, Wamschel LA, Oppenheimer NJ, Moss J. 1992. Amino acid-specific ADP-ribosylation: structural characterization and chemical differentiation of ADP-ribose-cysteine adducts formed nonenzvmaticallv and in a pertussis toxin-catalvzed reaction. Biochemistry 31:11881–11887.
Cassel D, Pfeurfer T. 1978. Mechanism of cholera toxin action: covalent modification of the guanyl nucleotide-binding protein of the adenylate cyclase system. Proc Natl Acad Sci USA 75:2669–2673.
Ui M, Katada T. 1990. Bacterial toxins as probe for receptor-Gi coupling. Adv Second Messenger Phosphoprotein Res 24:63–69.
Field M. 1976. Regulation of active ion transport in the small intestine. Ciba Found Symp 42: 109–127.
Moss J, Vaughan M. 1988. ADP–ribosylation of guanyl nucleotide-binding regulatory proteins by bacterial toxins. Adv Enzymol Relat Areas Mol Biol 61:303–379.
Sharp GW. 1973. Action of cholera toxin on fluid and electrolyte movement in the small intestine. Annu Rev Med 24:19–23.
Collier RJ. 1967. Effect of diphtheria toxin on protein synthesis: inactivation of one of the transfer factors. J Mol Biol 25:83–98.
Collier RJ. 1975. Diphtheria toxin: mode of action and structure. Bacteriol Rev 39:54–85.
Iglewski WJ. 1994. Cellular ADP-ribosvlation of elongation factor 2. Mol Cell Biochem 138: 131–133.
Wick MJ, Frank DW, Storey DC, Iglewski BH. 1990. Structure, function, and regulation of Pseudomonas aeruginosa exotoxin A. Annu Rev Microbiol 44:335–363.
vanderSpek J, Cosenza L, Woodworth T, Nichols JC, Murphy JR. 1994. Diphtheria toxin-related cytokine fusion proteins: elongation factor 2 as a target for the treatment of neoplastic disease. Mol Cell Biochem 138:151–156.
Kumagai N, Morii N, Fujisawa K, Nemoto Y, Narumiya S. 1993. ADP-ribosylation of rho p21 inhibits lysophosphatidic acid-induced protein tyrosine phosphorylation phosphatidylinositol 3-kinase activation in cultured Swiss 3T3 cells. J Biol Chem 268:24535–24538.
Kishi K, Sasaki T, Kuroda S, Itoh T, Takai Y. 1993. Regulation of cytoplasmic division of Xenopus embryo by rho p21 and its inhibitory GDP/GTP exchange protein (rho GDI). J Cell Biol 120: 1187–1195.
Maehama T, Sekine N, Nishina H, Takahashi K, Katada T. 1994. Characterization of botulinum C3-catalyzed ADP-ribosylation of rho proteins and identification of mammalian C3-like ADP-ribosyltransferase. Mol Cell Biochem 138:135–140.
Nishiki T, Narumiya S, Morii N, Yamamoto M, Fujiwara M, Kamata Y, Sakaguchi G, Kozaki S. 1990. ADP-ribosylation of the rho/rac proteins induces growth inhibition, neurite outgrowth and acetylcholine esterase in cultured PC-12 cells. Biochem Biophys Res Commun 167:265–272.
Paterson HF, Self AJ, Garrett MD, Just I, Aktories K, and Hall A. 1990. Microinjection of recombinant p21rho induces rapid changes in cell morphology. J Cell Biol 111:1001–1007.
Ridley AJ, Hall A. 1992. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70:389–399.
Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A. 1992. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70:401–410.
Graves DJ, Huiatt TW, Zhou H, Huang HY, Sernett SW, Robson RM, McMahon KK. 1997. Regulatory role of arginine-specific mono (ADP-ribosyl) transferase in muscle cells. Adv Exp Med Biol 419:305–313.
Huang HY, Zhou H, Huiatt TW, Graves DJ. 1996. Target proteins for arginine-specific mono (ADP-ribosyl) transferase in membrane fractions from chick skeletal muscle cells. Exp Cell Res 226:147–153.
Yuan J, Huiatt TW, Liao CX, Robson RM, Graves DJ. 1999. The effects of mono-ADP-ribosylation on desmin assembly-disassembly. Arch Biochem Biophys 363:314–322.
Terashima M, Mishima K, Yamada K, Tsuchiya M, Wakutani T, Shimoyama M. 1992. ADP-ribosylation of actins by arginine-specific ADP-ribosyltransferase purified from chicken heterophils. Eur J Biochem 204:305–311.
Zolkiewska A, Thompson WC, Moss J. 1998. Interaction of integrin alpha 7 beta 1 in C2C12 myotubes and in solution with laminin. Exp Cell Res 240:86–94.
Lupi R, Corda D, Di Girolamo M. 2000. Endogenous ADP-ribosylation of the G protein beta subunit prevents the inhibition of type 1 adenylyl cyclase. J Biol Chem 275:9418–9424.
Aktories K, Wegner A. 1992. Mechanisms of the cytopathic action of actin-ADP-ribosylating toxins. Mol Microbiol 6:2905–2908.
Chao D, Severson DL, Zwiers H, Hollenberg MD. 1994. Radiolabelling of bovine myristoylated alanine-rich protein kinase C substrate (MARCKS) in an ADP-ribosylation reaction. Biochem Cell Biol 72:391–396.
Scaife RM, Wilson L, Purich DL. 1992. Microtubule protein ADP-ribosylation in vitro leads to assembly inhibition and rapid depolymerization. Biochemistry 31:310–316.
Donadoni ML, Gavezzotti R, Borella F, Di Giulio AM, Gorio A. 1995. Experimental diabetic neuropathy. Inhibition of protein mono-ADP-ribosylation prevents reduction of substance P axonal transport. J Pharmacol Exp Ther 274:570–576.
Jones EM, Baird A. 1997. Cell-surface ADP-ribosylation of fibroblast growth factor-2 by an argi-nine-specific ADP-ribosyltransferase. Biochem J 323:173–177.
Boulle N, Jones EM, Auguste P, Baird A. 1995. Adenosine diphosphate ribosylation of fibroblast growth factor-2. Mol Endocrinol 9:767–775.
Feige JJ, Baird A. 1989. Basic fibroblast growth factor is a substrate for protein phosphorylation and is phosphorylated by capillary endothelial cells in culture. Proc Natl Acad Sci USA 86: 3174–3178.
Vilgrain I, Baird A. 1991. Phosphorylation of basic fibroblast growth factor by a protein kinase associated with the outer surface of a target cell. Mol Endocrinol 5:1003–1012.
Vilgrain I, Gonzalez AM, Baird A. 1993. Phosphorylation of basic fibroblast growth factor (FGF-2) in the nuclei of SK-Hep-1 cells. FEBS Lett 331:228–232.
Saxty BA, Yadollahi-Farsani M, Upton PD, Johnstone SR, MacDermot J. 2001. Inactivation of platelet-derived growth factor-BB following modification by ADP-ribosyltransferase. Br J Pharmacol 133:1219–1226.
Brune B, Lapetina EG. 1989. Activation of a cytosolic ADP-ribosyltransferase by nitric oxide-generating agents. J Biol Chem 264:8455–8458.
Schuman EM, Meffert MK, Schulman H, Madison DV. 1994. An ADP-ribosyltransferase as a potential target for nitric oxide action in hippocampal long-term potentiation. Proc Natl Acad Sci USA 91:11958–11962.
Zhang J, Snyder SH. 1992. Nitric oxide stimulates auto-ADP-ribosylation of glyceraldehyde-3-phosphate dehydrogenase. Proc Natl Acad Sci USA 89:9382–9385.
Parrado J, Bougria M, Ayala A, Machado A. 1999. Induced mono-(ADP)-ribosylation of rat liver cytosolic proteins by lipid peroxidant agents. Free Radic Biol Med 26:1079–1084.
Kanagy NL, Charpie JR, Webb RC. 1995. Nitric oxide regulation of ADP-ribosylation of G proteins in hypertension. Med Hypotheses 44:159–164.
Zhang DX, Zou AP, Li PL. 2001. Adenosine diphosphate ribose dilates bovine coronary small arteries through apyrase- and 5’-nucleotidase-mediated metabolism. J Vase Res 38:64–72.
Taguchi J, Abe J, Okazaki H, Takuwa Y, Kurokawa K. 1993. L-arginine inhibits neointimal formation following balloon injury. Life Sci 53:387–392.
Suzuki T, Hayase M, Hibi K, Hosokawa H, Yokoya K, Fitzgerald PJ, Yock PG, Cooke JP, Suzuki T, Yeung AC. 2002. Effect of local delivery of L-arginine on m-stent restenosis in humans. Am J Cardiol 89:363–367.
Loesberg C, van Rooij H, Smets LA. 1990. Meta-iodobenzylguanidine (MIBG), a novel high-affinity substrate for cholera toxin that interferes with cellular mono(ADP-ribosylation). Biochim Biophys Acta 1037:92–99.
Uemura S, Fathman CG, Rothbard JB, Cooke J P. 2000. Rapid and efficient vascular transport of argimne polymers inhibits myointimal hyperplasia. Circulation 102:2629–2635.
Cornelissen J, Wanders RJ, Van den Bogert C, Van Kuilenburg AB, Elzinga L, Voute PA, Van Gennip AH. 1995. Meta-iodobenzylguanidine (MIBG) inhibits malate and succinate driven mitochondrial ATP synthesis in the human neuroblastoma cell line SK-N-BE(2c). Eur J Cancer 4:582–586.
Loesberg C, van Rooij H, Nooijen WJ, Meijer AJ, Smets LA. 1990. Impaired mitochondrial respiration and stimulated glycolysis by m-iodobenzylguanidine (MIBG). Int J Cancer 46:276–281.
Duriez PJ, Shah GM. 1997. Cleavage of poly(ADP-ribose) polymerase: a sensitive parameter to study cell death. Biochem Cell Biof 75:337–349.
Gilad E, Zingarelli B, Salzman AL, Szabo C. 1997. Protection by inhibition of poly (ADP-ribose) synthetase against oxidant injury in cardiac myoblasts In vitro. J Mol Cell Cardiol 29:2585–2597
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2004 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Yau, L., Zahradka, P. (2004). ADP-Ribosylation and the Cardiovascular System. In: Dhalla, N.S., Rupp, H., Angel, A., Pierce, G.N. (eds) Pathophysiology of Cardiovascular Disease. Progress in Experimental Cardiology, vol 10. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0453-5_27
Download citation
DOI: https://doi.org/10.1007/978-1-4615-0453-5_27
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4613-5084-2
Online ISBN: 978-1-4615-0453-5
eBook Packages: Springer Book Archive