Crossref journal-article
American Society for Microbiology
Microbiology and Molecular Biology Reviews (235)
Abstract

SUMMARYSince poly-ADP ribose was discovered over 40 years ago, there has been significant progress in research into the biology of mono- and poly-ADP-ribosylation reactions. During the last decade, it became clear that ADP-ribosylation reactions play important roles in a wide range of physiological and pathophysiological processes, including inter- and intracellular signaling, transcriptional regulation, DNA repair pathways and maintenance of genomic stability, telomere dynamics, cell differentiation and proliferation, and necrosis and apoptosis. ADP-ribosylation reactions are phylogenetically ancient and can be classified into four major groups: mono-ADP-ribosylation, poly-ADP-ribosylation, ADP-ribose cyclization, and formation ofO-acetyl-ADP-ribose. In the human genome, more than 30 different genes coding for enzymes associated with distinct ADP-ribosylation activities have been identified. This review highlights the recent advances in the rapidly growing field of nuclear mono-ADP-ribosylation and poly-ADP-ribosylation reactions and the distinct ADP-ribosylating enzyme families involved in these processes, including the proposed family of novel poly-ADP-ribose polymerase-like mono-ADP-ribose transferases and the potential mono-ADP-ribosylation activities of the sirtuin family of NAD+-dependent histone deacetylases. A special focus is placed on the known roles of distinct mono- and poly-ADP-ribosylation reactions in physiological processes, such as mitosis, cellular differentiation and proliferation, telomere dynamics, and aging, as well as “programmed necrosis” (i.e., high-mobility-group protein B1 release) and apoptosis (i.e., apoptosis-inducing factor shuttling). The proposed molecular mechanisms involved in these processes, such as signaling, chromatin modification (i.e., “histone code”), and remodeling of chromatin structure (i.e., DNA damage response, transcriptional regulation, and insulator function), are described. A potential cross talk between nuclear ADP-ribosylation processes and other NAD+-dependent pathways is discussed.

Bibliography

Hassa, P. O., Haenni, S. S., Elser, M., & Hottiger, M. O. (2006). Nuclear ADP-Ribosylation Reactions in Mammalian Cells: Where Are We Today and Where Are We Going? Microbiology and Molecular Biology Reviews, 70(3), 789–829.

Authors 4
  1. Paul O. Hassa (first)
  2. Sandra S. Haenni (additional)
  3. Michael Elser (additional)
  4. Michael O. Hottiger (additional)
References 468 Referenced 557
  1. 10.1016/S0021-9258(17)39804-6
  2. 10.1038/15640
  3. 10.1016/0006-291X(85)90261-X
  4. 10.4049/jimmunol.167.1.196
  5. 10.1074/jbc.M505408200
  6. 10.1182/blood.V96.13.4328
  7. 10.1105/tpc.021832
  8. 10.1074/jbc.M313329200
  9. 10.1073/pnas.84.5.1224
  10. 10.1096/fasebj.9.12.7672505
  11. 10.1016/0014-5793(94)80580-6
  12. 10.1242/jcs.102.4.663
  13. 10.1023/A:1006975002262
  14. Althaus, F. R., and C. Richter. 1987. ADP-ribosylation of proteins. Enzymology and biological significance. Mol. Biol. Biochem. Biophys.37:1-237. / Mol. Biol. Biochem. Biophys. (1987)
  15. 10.1016/0921-8777(89)90012-8
  16. 10.1021/bi00385a042
  17. 10.1016/0300-9084(96)88153-3
  18. 10.1023/A:1006912210439
  19. 10.1074/jbc.274.25.17860
  20. 10.1002/bies.20085
  21. 10.1006/bbrc.2001.4654
  22. 10.1042/bse0410049
  23. 10.1042/bj3250543
  24. 10.1016/S0968-0004(01)01787-X
  25. Aubin, R., A. Frechette, G. de Murcia, F. Malouin, A. Lord, P. Mandel, and G. G. Poirier. 1983. Nucleosomal poly(ADP-ribose) polymerase: properties and relaxation of the chromatin structure. Princess Takamatsu Symp.13:83-91. / Princess Takamatsu Symp. (1983)
  26. 10.1242/jcs.00341
  27. 10.1139/o01-147
  28. 10.1111/j.1460-9568.2004.03616.x
  29. Bauer, P. I., E. Kenesi, J. Mendeleyev, and E. Kun. 2005. The influence of ATP on poly(ADP-ribose) metabolism. Int. J. Mol. Med.16:321-324. / Int. J. Mol. Med. (2005)
  30. 10.1016/S0014-5793(00)02016-0
  31. 10.1074/jbc.M508660200
  32. 10.1016/j.tibs.2004.01.007
  33. 10.2307/3576299
  34. Berger, N. A., J. L. Sims, D. M. Catino, and S. J. Berger. 1983. Poly(ADP-ribose) polymerase mediates the suicide response to massive DNA damage: studies in normal and DNA-repair defective cells. Princess Takamatsu Symp.13:219-226. / Princess Takamatsu Symp. (1983)
  35. 10.1016/j.bbaexp.2003.10.017
  36. 10.1016/S0092-8674(04)00416-7
  37. 10.1146/annurev.biochem.73.011303.073651
  38. 10.1038/nrg1656
  39. 10.1016/S0304-4165(96)00085-2
  40. 10.1002/pmic.200300743
  41. Bonaldi, T., J. T. Regula, and A. Imhof. 2004. The use of mass spectrometry for the analysis of histone modifications. Methods Enzymol.377:111-130. / Methods Enzymol. (2004)
  42. 10.1093/emboj/cdg516
  43. 10.1074/jbc.272.25.15856
  44. 10.1007/s00018-004-4505-1
  45. 10.1111/j.1432-1033.1992.tb17387.x
  46. 10.1074/jbc.M111830200
  47. 10.1016/j.drup.2004.11.003
  48. 10.1016/S0301-472X(03)00083-3
  49. 10.1016/0003-2697(92)90310-4
  50. Boulikas, T. 1991. Relation between carcinogenesis, chromatin structure and poly(ADP-ribosylation). Anticancer Res.11:489-527. / Anticancer Res. (1991)
  51. 10.1111/j.1432-0436.1987.tb00060.x
  52. 10.1111/j.1432-1033.1994.tb18633.x
  53. 10.1016/0167-4781(94)90058-2
  54. 10.1006/abio.1994.1177
  55. 10.1016/S0021-9258(17)30178-3
  56. 10.1016/0014-4827(83)90166-0
  57. 10.1146/annurev.physiol.63.1.99
  58. 10.1016/S0300-9084(02)01374-3
  59. 10.1074/jbc.271.18.10461
  60. 10.1021/bi00057a017
  61. 10.1002/ijc.2910530522
  62. 10.1016/0167-4889(92)90257-C
  63. 10.1093/nar/29.13.2699
  64. 10.1093/hmg/10.10.1101
  65. 10.1016/0006-291X(63)90024-X
  66. 10.1038/ncb1322
  67. 10.1038/nature03061
  68. 10.1042/BJ20050885
  69. 10.1139/o94-052
  70. 10.1016/j.str.2005.05.016
  71. 10.1126/science.281.5382.1505
  72. 10.1016/j.cardiores.2004.04.018
  73. 10.1073/pnas.1934713100
  74. Chew, Y. C., G. Camporeale, N. Kothapalli, G. Sarath, and J. Zempleni. 2005. Lysine residues in N-terminal and C-terminal regions of human histone H2A are targets for biotinylation by biotinidase. J. Nutr. Biochem.17:225-233. / J. Nutr. Biochem. (2005)
  75. 10.1074/jbc.M007635200
  76. 10.1128/MCB.26.6.2037-2043.2006
  77. 10.1042/BJ20041971
  78. 10.1016/j.febslet.2005.06.041
  79. 10.1074/jbc.M414526200
  80. 10.1023/A:1025334006014
  81. 10.1016/0014-5793(93)80450-9
  82. 10.1126/science.1099196
  83. 10.1074/jbc.271.42.26200
  84. 10.1096/fasebj.11.4.9068610
  85. 10.1182/blood.V70.3.686.686
  86. 10.1146/annurev.biochem.69.1.95
  87. 10.1128/MCB.22.1.332-342.2002
  88. 10.1093/emboj/cdg209
  89. Corda, D., and M. Di Girolamo. 2002. Mono-ADP-ribosylation: a tool for modulating immune response and cell signaling. Sci. STKE2002:PE53. / Sci. STKE (2002)
  90. 10.1128/MCB.24.16.7163-7178.2004
  91. 10.1038/nsmb851
  92. 10.1038/sj.jcbfm.9600222
  93. 10.1042/bj3420249
  94. 10.1128/MCB.24.4.1595-1607.2004
  95. 10.1016/S0014-5793(00)01731-2
  96. 10.1006/excr.2001.5263
  97. 10.1023/B:JOBB.0000041755.22613.8d
  98. 10.1016/j.febslet.2004.12.028
  99. 10.2174/1389201023378265
  100. De Flora, A., E. Zocchi, L. Guida, L. Franco, and S. Bruzzone. 2004. Autocrine and paracrine calcium signaling by the CD38/NAD+/cyclic ADP-ribose system. Ann. N. Y. Acad. Sci.1028:176-191. (10.1196/annals.1322.021) / Ann. N. Y. Acad. Sci. (2004)
  101. 10.1002/bies.20176
  102. 10.1074/jbc.M509884200
  103. 10.1016/S0021-9258(19)62715-8
  104. 10.1073/pnas.94.14.7303
  105. 10.1126/science.1063957
  106. 10.1016/j.cbpa.2005.08.010
  107. 10.1016/0167-4838(91)99007-F
  108. 10.1016/0300-9084(96)88156-9
  109. 10.1111/j.1742-4658.2005.04876.x
  110. 10.1023/A:1024136927637
  111. Doly, J., and P. Mandel. 1967. Demonstration of the biosynthesis in vivo of a compound polymer, polyadenosine diphosphoribose in the nucleus of the liver of chickens. C. R. Acad. Sci. D264:2687-2690. / C. R. Acad. Sci. D (1967)
  112. 10.1126/science.1094754
  113. 10.1016/j.ceb.2004.09.011
  114. 10.1016/0014-5793(94)01280-6
  115. 10.1002/jcp.1040860509
  116. 10.1111/j.1574-6968.2000.tb09351.x
  117. 10.1042/bj2210223
  118. 10.1042/bj3350441
  119. 10.1038/nrm1428
  120. 10.1016/0304-4165(96)00019-0
  121. 10.1016/S0021-9258(18)32361-5
  122. 10.1016/0005-2787(78)90083-7
  123. 10.1016/S0021-9258(18)34453-3
  124. 10.1038/nature02017
  125. 10.1016/S0955-0674(03)00013-9
  126. 10.1182/blood.V62.5.1055.1055
  127. 10.1139/o85-096
  128. 10.1006/bbrc.1999.0897
  129. 10.1042/bj20021675
  130. 10.1126/science.1074276
  131. 10.1021/pr0498887
  132. 10.1093/emboj/cdg553
  133. 10.1139/o86-023
  134. 10.1016/S0959-437X(96)80049-9
  135. 10.1042/bj3170865
  136. 10.1084/jem.129.1.1
  137. 10.1101/gad.1214604
  138. Gloor, G. B. 2004. Gene targeting in Drosophila. Methods Mol. Biol.260:97-114. / Methods Mol. Biol. (2004)
  139. 10.1016/j.tibs.2004.09.010
  140. Glowacki, G., R. Braren, K. Firner, M. Nissen, M. Kuhl, P. Reche, F. Bazan, M. Cetkovic-Cvrlje, E. Leiter, F. Haag, and F. Koch-Nolte. 2002. The family of toxin-related ecto-ADP-ribosyltransferases in humans and the mouse. Protein Sci.11:1657-1670. (10.1110/ps.0200602) / Protein Sci. (2002)
  141. 10.1042/bj2770607
  142. Golderer, G., P. Loidl, and P. Grobner. 1991. Cell cycle-dependent ADP-ribosylation of the nuclear matrix. Eur. J. Cell Biol.55:183-185. / Eur. J. Cell Biol. (1991)
  143. 10.1016/0304-4165(78)90312-4
  144. 10.1161/01.STR.0000014203.65693.1E
  145. 10.1073/pnas.87.8.2990
  146. 10.1042/bj3620717
  147. 10.1111/j.1742-4658.2005.04862.x
  148. 10.1016/0022-4731(89)90007-1
  149. 10.1073/pnas.96.24.13978
  150. 10.1080/10446670310001593514
  151. Haag, F., and F. Koch-Nolte. 1998. Endogenous relatives of ADP-ribosylating bacterial toxins in mice and men: potential regulators of immune cell function. J. Biol. Regul. Homeost. Agents12:53-62. / J. Biol. Regul. Homeost. Agents (1998)
  152. 10.1016/j.bbamcr.2005.11.015
  153. 10.1074/jbc.M001189200
  154. 10.1073/pnas.2237114100
  155. 10.1074/jbc.273.19.11881
  156. Hansen, T. M., and P. Nagley. 2003. AIF: a multifunctional cog in the life and death machine. Sci. STKE2003:PE31. / Sci. STKE (2003)
  157. 10.1074/jbc.M307957200
  158. 10.1074/jbc.M106528200
  159. 10.1074/jbc.M507553200
  160. 10.1139/o05-034
  161. 10.1007/s00018-002-8527-2
  162. 10.1073/pnas.2035256100
  163. 10.1093/emboj/20.10.2404
  164. Hilz, H., K. Wielckens, P. Adamietz, R. Bredehorst, and A. Kreymeier. 1983. Functional aspects of mono- and poly(ADP-ribosyl)ation: subcellular distribution and ADP-ribosyl turnover under conditions of repair and ‘starvation.’ Princess Takamatsu Symp.13:155-163. / Princess Takamatsu Symp. (1983)
  165. 10.1038/nsmb0705-560
  166. 10.1111/j.1432-1033.1983.tb07153.x
  167. 10.1083/jcb.150.2.293
  168. 10.1016/j.tips.2004.03.005
  169. 10.1016/S0021-9258(18)93347-8
  170. 10.1128/MCB.26.6.2044-2054.2006
  171. 10.1016/S0021-9258(18)45824-3
  172. 10.1016/0006-291X(91)90383-I
  173. 10.1016/S0021-9258(18)33226-5
  174. 10.1007/978-1-4419-8632-0_49
  175. Jacobson, M. K., J. Y. Smith, M. Mingmuang, D. M. Payne, and E. L. Jacobson. 1983. Mono- and poly(ADP-ribose) metabolism following DNA damage. Princess Takamatsu Symp.13:165-174. / Princess Takamatsu Symp. (1983)
  176. 10.1038/nrd1718
  177. 10.1126/science.1063127
  178. 10.1006/geno.1999.5799
  179. 10.1038/nature03871
  180. 10.1016/j.cell.2004.11.017
  181. 10.1016/S0021-9258(19)68235-9
  182. 10.1016/0003-2697(83)90192-6
  183. 10.1021/bi00001a040
  184. 10.1111/j.1432-1033.1994.tb18823.x
  185. 10.1074/jbc.M105968200
  186. 10.1016/S0021-9258(20)65127-4
  187. 10.1006/bbrc.2000.3801
  188. Kanai, Y., M. Miwa, T. Matsushima, and T. Sugimura. 1978. Comparative studies on antibody and antibody production to poly(ADP-ribose) in mice. Immunology34:501-508. / Immunology (1978)
  189. 10.1038/sj.emboj.7600664
  190. 10.1016/S0021-9258(18)51522-2
  191. 10.1006/bbrc.1998.9403
  192. 10.1016/j.cbpa.2005.08.018
  193. 10.1021/ac990684x
  194. 10.1016/0014-4827(92)90345-9
  195. 10.1074/jbc.M908231199
  196. 10.1083/jcb.146.5.917
  197. 10.1038/sj.embor.7400625
  198. 10.1016/j.cell.2004.11.002
  199. 10.1038/nature01034
  200. 10.4161/cc.4.1.1398
  201. 10.1111/j.1742-4658.2005.04839.x
  202. 10.1007/978-1-4419-8632-0_1
  203. 10.1074/jbc.271.13.7686
  204. 10.1042/bj2930275
  205. Kofler, J., T. Otsuka, Z. Zhang, R. Noppens, M. R. Grafe, D. W. Koh, V. L. Dawson, J. M. de Murcia, P. D. Hurn, and R. J. Traystman. 2005. Differential effect of PARP-2 deletion on brain injury after focal and global cerebral ischemia. J. Cereb. Blood Flow Metab.26:135-141. / J. Cereb. Blood Flow Metab. (2005)
  206. 10.1073/pnas.0406182101
  207. 10.1016/S0092-8674(03)00719-0
  208. 10.1016/j.jnutbio.2005.03.025
  209. 10.1093/jn/135.10.2337
  210. 10.4049/jimmunol.174.6.3298
  211. 10.1515/bchm3.1985.366.1.537
  212. 10.1016/S0021-9258(17)43540-X
  213. 10.1021/bi00435a063
  214. 10.1073/pnas.73.9.3131
  215. 10.1021/bi0301791
  216. 10.1006/bbrc.1996.0263
  217. 10.1016/S0021-9258(18)47687-9
  218. 10.1038/nsmb956
  219. 10.1016/S1097-2765(03)00284-3
  220. 10.1016/S0065-2423(05)40005-0
  221. 10.1007/BF00928456
  222. 10.1016/0167-4889(86)90239-9
  223. 10.1016/S0021-9258(18)94230-4
  224. 10.1016/0003-2697(89)90655-6
  225. 10.1016/j.ab.2003.08.031
  226. 10.1002/jcb.240520207
  227. 10.1016/0014-5793(90)80499-9
  228. 10.1016/j.cub.2004.03.026
  229. 10.1002/neu.20229
  230. 10.1074/jbc.272.18.11895
  231. 10.1016/j.cell.2005.03.035
  232. 10.1152/physrev.1999.79.4.1431
  233. 10.1016/S0092-8674(02)01046-2
  234. 10.1074/jbc.M413296200
  235. 10.1128/MCB.24.12.5314-5323.2004
  236. 10.1006/abbi.2000.2215
  237. 10.1016/j.bbagen.2004.03.017
  238. 10.1038/sj.cdd.4400527
  239. 10.1002/jcp.1041210210
  240. 10.1074/jbc.275.13.9418
  241. 10.1006/bbrc.2001.5987
  242. 10.1016/j.molcel.2005.08.032
  243. 10.1007/s00018-003-3161-1
  244. 10.2174/0929867043455666
  245. Magni, G., A. Amici, M. Emanuelli, N. Raffaelli, and S. Ruggieri. 1999. Enzymology of NAD+ synthesis. Adv. Enzymol. Relat. Areas Mol. Biol.73:135-182, xi. / Adv. Enzymol. Relat. Areas Mol. Biol. (1999)
  246. 10.1139/o05-038
  247. 10.1016/S0167-4781(98)00110-9
  248. 10.1002/(SICI)1097-4644(19980915)70:4<596::AID-JCB15>3.0.CO;2-F
  249. 10.1074/jbc.273.19.11839
  250. 10.1016/S0021-9258(17)43521-6
  251. 10.1016/0014-5793(89)80948-2
  252. 10.1111/j.1742-4658.2005.04653.x
  253. 10.1038/35073047
  254. 10.1074/jbc.M414018200
  255. 10.1074/jbc.270.7.3247
  256. 10.1093/oxfordjournals.jbchem.a022307
  257. 10.1016/S0742-8413(97)00173-4
  258. 10.1023/A:1006941016799
  259. 10.1073/pnas.96.5.2301
  260. 10.1093/emboj/cdf682
  261. 10.1042/bst0270832
  262. 10.1021/cr0103017
  263. 10.1073/pnas.94.6.2261
  264. 10.1016/S0021-9258(18)41568-2
  265. 10.1002/mas.20009
  266. 10.1093/emboj/cdg206
  267. 10.1016/S0378-1119(03)00738-8
  268. 10.1016/j.yexcr.2004.03.050
  269. 10.1016/j.biocel.2004.09.011
  270. 10.1007/s00412-005-0344-6
  271. 10.1091/mbc.e05-01-0033
  272. 10.1016/S0021-9258(20)81953-X
  273. 10.1016/S0021-9258(18)33108-9
  274. 10.1093/oxfordjournals.jbchem.a123999
  275. 10.1023/A:1006920429095
  276. 10.1016/S0021-9258(19)69701-2
  277. 10.1073/pnas.76.2.595
  278. 10.1016/S0021-9258(18)61798-3
  279. 10.1110/ps.03554604
  280. 10.1111/j.1365-2958.1991.tb01971.x
  281. 10.1023/A:1006993000870
  282. 10.1016/S0021-9258(17)42962-0
  283. 10.1007/978-1-4419-8632-0_3
  284. 10.1016/j.cell.2005.11.044
  285. 10.1002/(SICI)1097-0185(20000215)261:1<14::AID-AR5>3.0.CO;2-E
  286. 10.1074/jbc.M209313200
  287. 10.1038/ncb1352
  288. 10.1016/S0021-9258(18)95947-8
  289. 10.1016/S1097-2765(03)00038-8
  290. 10.1002/jssc.200500258
  291. 10.1139/o05-039
  292. 10.1016/S0021-9258(19)43872-6
  293. 10.1016/S0021-9258(19)43873-8
  294. 10.1016/S0021-9258(19)69404-4
  295. 10.1128/MCB.22.21.7535-7542.2002
  296. 10.1016/S0021-9258(17)43555-1
  297. 10.1074/jbc.M510290200
  298. 10.1016/S0021-9258(19)66926-7
  299. 10.1016/0006-291X(78)90769-6
  300. 10.1073/pnas.75.5.2254
  301. 10.1073/pnas.75.3.1111
  302. 10.1074/jbc.271.36.22052
  303. 10.1007/978-1-4419-8632-0_15
  304. 10.1146/annurev.nutr.19.1.485
  305. 10.1016/S1054-3589(08)60277-X
  306. 10.1016/0300-9084(96)88141-7
  307. 10.1126/science.1113398
  308. 10.1042/bj1610583
  309. 10.1186/1471-2164-6-139
  310. 10.1124/jpet.105.088336
  311. 10.1016/S1534-5807(02)00200-9
  312. 10.1021/bi00120a014
  313. 10.1007/s10495-005-6074-7
  314. 10.1182/blood-2004-07-2938
  315. 10.1042/BJ20040942
  316. 10.1016/j.molcel.2005.02.034
  317. 10.1196/annals.1329.069
  318. 10.1016/S0166-2236(00)01787-2
  319. 10.1172/JCI200421854
  320. Philibert, K., and H. Zwiers. 1995. Evidence for multisite ADP-ribosylation of neuronal phosphoprotein B-50/GAP-43. Mol. Cell. Biochem.149-150:183-190. / Mol. Cell. Biochem. (1995)
  321. 10.1074/jbc.M006520200
  322. 10.1093/carcin/6.2.283
  323. 10.1073/pnas.79.11.3423
  324. Poirier, G. G., C. Niedergang, M. Champagne, A. Mazen, and P. Mandel. 1982. Adenosine diphosphate ribosylation of chicken-erythrocyte histones H1, H5 and high-mobility-group proteins by purified calf-thymus poly(adenosinediphosphate-ribose) polymerase. Eur. J. Biochem.127:437-442. (10.1111/j.1432-1033.1982.tb06891.x) / Eur. J. Biochem. (1982)
  325. 10.1016/0167-4781(89)90035-3
  326. 10.1006/jmcc.1994.1028
  327. 10.1074/jbc.M208997200
  328. 10.1016/S0021-9258(19)37040-1
  329. 10.1002/jcp.1040880210
  330. 10.1016/S0021-9258(18)95948-X
  331. 10.1016/j.jasms.2005.06.001
  332. 10.1006/bbrc.1995.2237
  333. 10.1016/S0304-4165(01)00113-1
  334. 10.1016/S0022-2836(02)00946-4
  335. 10.1016/S0021-9258(17)30177-1
  336. 10.1016/0014-5793(80)81033-7
  337. 10.1016/0006-291X(85)91206-9
  338. 10.1021/bi971055p
  339. 10.1002/bies.10297
  340. 10.1242/jcs.01080
  341. 10.1074/jbc.M513728200
  342. 10.1006/jmbi.1998.1673
  343. 10.1074/jbc.275.20.15504
  344. 10.1074/jbc.M508957200
  345. 10.1021/bi981248s
  346. 10.1021/bi0258795
  347. 10.2174/0929867043455675
  348. 10.1002/cbic.200400189
  349. 10.1074/jbc.M200620200
  350. 10.1093/hmg/11.19.2319
  351. 10.1021/bi00116a042
  352. 10.1021/bi973063b
  353. 10.1074/jbc.M202390200
  354. 10.2174/1566524043360708
  355. 10.1006/excr.1993.1135
  356. 10.2174/0929867043455611
  357. 10.1074/jbc.M503305200
  358. 10.1016/S0921-8777(00)00016-1
  359. 10.1002/bies.20350
  360. 10.1074/jbc.273.46.30069
  361. 10.1002/jcb.10761
  362. Sibley, J. T., R. P. Braun, and J. S. Lee. 1986. The production of antibodies to DNA in normal mice following immunization with poly(ADP-ribose). Clin. Exp. Immunol.64:563-569. / Clin. Exp. Immunol. (1986)
  363. Sibley, J. T., L. J. Latimer, and J. S. Lee. 1988. Shared idiotypes on anti-DNA and anti-poly (ADP-ribose) antibodies. J. Immunol.140:3502-3507. (10.4049/jimmunol.140.10.3502) / J. Immunol. (1988)
  364. 10.1021/bi9731089
  365. 10.1038/sj.onc.1206897
  366. 10.1016/S0021-9258(18)52907-0
  367. 10.1016/0006-291X(85)91204-5
  368. 10.1093/carcin/6.10.1489
  369. 10.1111/j.1432-1033.1979.tb04225.x
  370. 10.1016/S0021-9258(20)81989-9
  371. 10.1021/bi052014t
  372. 10.1093/carcin/20.8.1439
  373. 10.1042/bj1470523
  374. 10.1016/0006-291X(85)90582-0
  375. 10.1242/jcs.112.21.3649
  376. 10.1126/science.282.5393.1484
  377. 10.1016/S0006-291X(83)80025-4
  378. 10.1038/ng1410
  379. 10.1016/S0091-679X(08)60022-9
  380. 10.1038/47412
  381. 10.1073/pnas.0408351102
  382. 10.1007/BF03348885
  383. 10.1016/0005-2787(67)90507-2
  384. 10.1038/17135
  385. 10.1016/S0021-9258(17)46780-9
  386. 10.1016/j.bbrc.2004.08.132
  387. 10.1073/pnas.221444598
  388. 10.4049/jimmunol.170.2.686
  389. 10.1016/S0021-9258(17)43510-1
  390. 10.1073/pnas.250422697
  391. 10.1016/S0092-8674(00)81671-2
  392. 10.1016/0014-5793(90)80597-C
  393. 10.1016/0167-4889(89)90168-7
  394. 10.1016/S0021-9258(18)32583-3
  395. 10.1093/oxfordjournals.jbchem.a135553
  396. 10.1016/S0006-291X(85)80028-0
  397. 10.1016/S0021-9258(18)60743-4
  398. 10.1016/0003-9861(85)90251-6
  399. 10.1074/jbc.M507075200
  400. 10.1073/pnas.76.12.6411
  401. 10.1111/j.1432-1033.1992.tb16638.x
  402. 10.1111/j.1432-1033.1995.tb20693.x
  403. 10.3177/jnsv.45.393
  404. Terui, T., K. Murakami, R. Takimoto, M. Takahashi, K. Takada, T. Murakami, S. Minami, T. Matsunaga, T. Takayama, J. Kato, and Y. Niitsu. 2003. Induction of PIG3 and NOXA through acetylation of p53 at 320 and 373 lysine residues as a mechanism for apoptotic cell death by histone deacetylase inhibitors. Cancer Res.63:8948-8954. / Cancer Res. (2003)
  405. 10.1016/0047-6374(90)90037-G
  406. 10.1046/j.1432-0436.1995.5940243.x
  407. Tong, W. M., U. Cortes, and Z. Q. Wang. 2001. Poly(ADP-ribose) polymerase: a guardian angel protecting the genome and suppressing tumorigenesis. Biochim. Biophys. Acta1552:27-37. / Biochim. Biophys. Acta (2001)
  408. 10.1126/science.1078764
  409. 10.1101/gad.1003902
  410. 10.1016/S0092-8674(02)01080-2
  411. 10.1002/1521-1878(200009)22:9<836::AID-BIES9>3.0.CO;2-X
  412. 10.1007/s000180050122
  413. 10.1038/nsmb0205-110
  414. 10.1016/0006-291X(87)90921-1
  415. 10.1038/sj.emboj.7600746
  416. 10.1111/j.1432-1033.1985.tb09082.x
  417. 10.1038/sj.emboj.7600461
  418. van Empel, V. P., A. T. Bertrand, R. van der Nagel, S. Kostin, P. A. Doevendans, H. J. Crijns, E. de Wit, W. Sluiter, S. L. Ackerman, and L. J. De Windt. 2005. Downregulation of apoptosis-inducing factor in harlequin mutant mice sensitizes the myocardium to oxidative stress-related cell death and pressure overload-induced decompensation. Circ. Res.96:e92-e101. / Circ. Res. (2005)
  419. van Wijk, S. J., and G. J. Hageman. 2005. Poly(ADP-ribose) polymerase-1 mediated caspase-independent cell death after ischemia/reperfusion. Free Radic. Biol. Med.39:81-90. / Free Radic. Biol. Med. (2005)
  420. Vaquero, A., A. Loyola, and D. Reinberg. 2003. The constantly changing face of chromatin. Sci. Aging Knowledge Environ.2003:RE4. / Sci. Aging Knowledge Environ. (2003)
  421. 10.1007/978-1-4419-8632-0_41
  422. 10.1016/S0092-8674(01)00527-X
  423. 10.1016/S0006-2952(03)00077-7
  424. 10.1124/jpet.104.065151
  425. 10.1124/pr.54.3.375
  426. 10.1042/bj1990813
  427. 10.1126/science.285.5425.248
  428. 10.1016/S0039-6060(99)70182-0
  429. 10.1523/JNEUROSCI.3461-04.2004
  430. 10.1046/j.0014-2956.2001.02675.x
  431. 10.1101/gad.9.5.509
  432. 10.1101/gad.11.18.2347
  433. 10.1016/0006-291X(63)90036-6
  434. 10.1111/j.1432-1033.1984.tb07979.x
  435. 10.1016/0065-2571(82)90006-1
  436. 10.1016/0076-6879(84)06051-1
  437. 10.1016/S0021-9258(18)32589-4
  438. 10.1016/0014-4827(85)90189-2
  439. 10.1074/jbc.M202285200
  440. 10.1038/sj.onc.1207909
  441. 10.1016/j.jchromb.2005.01.030
  442. 10.1124/jpet.104.077164
  443. 10.1074/jbc.M508135200
  444. 10.1159/000474990
  445. Yang, J. S., and H. S. Moon. 2006. Role of HIV Vpr as a regulator of apoptosis and an effector on bystander cells. Mol. Cells21:7-20. (10.1016/s1016-8478(23)12897-4) / Mol. Cells (2006)
  446. 10.1038/sj.onc.1208173
  447. 10.1042/BJ20041480
  448. 10.1038/nsb836
  449. 10.1002/jnr.20289
  450. 10.1074/jbc.271.15.9129
  451. 10.1016/0006-291X(77)91431-0
  452. 10.1038/sj.onc.1208410
  453. 10.1126/science.1072221
  454. 10.1038/ng1426
  455. Zahradka, P., and K. Ebisuzaki. 1982. A shuttle mechanism for DNA-protein interactions. The regulation of poly(ADP-ribose) polymerase. Eur. J. Biochem.127:579-585. (10.1111/j.1432-1033.1982.tb06912.x) / Eur. J. Biochem. (1982)
  456. 10.1007/BF00928448
  457. 10.1016/S0021-9258(18)38452-7
  458. 10.1007/s004390100601
  459. 10.1002/bies.10317
  460. 10.1074/jbc.M300073200
  461. 10.1111/j.1460-9568.2004.03651.x
  462. 10.1016/j.str.2003.09.016
  463. 10.1073/pnas.0401057101
  464. 10.1006/abbi.1996.0449
  465. 10.1007/s10541-005-0098-z
  466. 10.1046/j.1432-1327.2000.01187.x
  467. 10.1073/pnas.89.23.11352
  468. 10.1101/gad.1199904
Dates
Type When
Created 18 years, 11 months ago (Sept. 7, 2006, 3:08 p.m.)
Deposited 1 year, 6 months ago (Feb. 6, 2024, 5:16 a.m.)
Indexed 5 days, 16 hours ago (Aug. 20, 2025, 8:32 a.m.)
Issued 18 years, 11 months ago (Sept. 1, 2006)
Published 18 years, 11 months ago (Sept. 1, 2006)
Published Print 18 years, 11 months ago (Sept. 1, 2006)
Funders 0

None

@article{Hassa_2006, title={Nuclear ADP-Ribosylation Reactions in Mammalian Cells: Where Are We Today and Where Are We Going?}, volume={70}, ISSN={1098-5557}, url={http://dx.doi.org/10.1128/mmbr.00040-05}, DOI={10.1128/mmbr.00040-05}, number={3}, journal={Microbiology and Molecular Biology Reviews}, publisher={American Society for Microbiology}, author={Hassa, Paul O. and Haenni, Sandra S. and Elser, Michael and Hottiger, Michael O.}, year={2006}, month=sep, pages={789–829} }