Alteration of poly(ADP-ribose) glycohydrolase nucleocytoplasmic shuttling characteristics upon cleavage by apoptotic proteases

Biology of the Cell

Volumn 95, Issue 9, 2003, Pages 635-644

  Bonicalzi, Marie Eve ^a   Vodenicharov, Momchil ^a   Coulombe, Miryan ^a   Gagné, Jean Philippe ^a   Poirier, Guy G ^a  

^a LAVAL UNIVERSITY   (Canada)

Author keywords

Golgi; Leptomycin B; NES; PARG

Indexed keywords

DNA; EXPORTIN 1; GLYCOSIDASE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; LEPTOMYCIN B; NUCLEAR PROTEIN; POLY(ADENOSINE DIPHOSPHATE RIBOSE);

AMINO TERMINAL SEQUENCE; ANIMAL CELL; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CELL STRAIN COS7; CELLULAR DISTRIBUTION; CHEMICAL ANALYSIS; CONTROLLED STUDY; CYTOPLASM; DNA DAMAGE; ENZYME ACTIVITY; ENZYME SUBSTRATE; EXCISION REPAIR; FLUORESCENCE MICROSCOPY; GOLGI COMPLEX; INHIBITION KINETICS; INTRACELLULAR SPACE; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; REGULATORY MECHANISM; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CASPASES; CELL NUCLEUS; COS CELLS; FATTY ACIDS, UNSATURATED; GLYCOSIDE HYDROLASES; GOLGI APPARATUS; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; IMMUNOBLOTTING; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; PEPTIDE FRAGMENTS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT FUSION PROTEINS; TRANSFECTION;

NES;

EID: 0742323811     PISSN: 02484900     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biolcel.2003.10.003     Document Type: Article

References (56)

1. Affar E.B. Germain M. Winstall E. Vodenicharov M. Shah R.G. Salvesen G. Poirier G.G. Caspase-3 mediated processing of poly(ADP-ribose) glycohydrolase during apoptosis J. Biol. Chem. 276 2001 2935-2942
2. Althaus F.R. Richter C. ADP-ribosylation of Proteins: Enzymology and Biological Significance 1987 Springer Verlag Berlin
3. Alvarez-Gonzalez R. Jacobson M.K. Characterization of polymer of ADP-ribose generated in vitro and in vivo Biochemistry 26 1987 3218-3224
4. Alvarez-Gonzalez R. Althaus F.R. Poly(ADP-ribose) catabolism in mammalian cells exposed to DNA-damaging agents Mutation Res 218 1989 67-74
5. Amé J.C. Rolli V. Schreiber V. Niedergang C. Apiou P. Decker P. Muller S. Hoger T. Menissier-de Murcia J. de Murcia G. PARP-2, a novel mammalian DNA damage dependent poly(ADP-ribose) polymerase J. Biol. Chem. 274 1999 17860-17868
6. Benjamin R.C. Gill D.M. Poly(ADP-ribose) synthesis in vitro programmed by damaged DNA: A comparison of DNA molecules containing different types of strand breaks J. Biol. Chem. 255 1980 10502-10508
7. Berghammer H. Ebner M. Marksteiner R. Auer B. pADPRT-2: a novel mammalian polymerizing(ADP-ribosyl)transferase gene related to truncated pADPRT homologues in plants and Caenorhabditis elegans FEBS Lett. 449 1999 259-263
8. Birbach A. Gold P. Binder B.R. Hofer E. de Martin R. Schmid J.A. Signaling molecules of the NF-kappa B pathway shuttle constitutively between cytoplasm and nucleus J. Biol. Chem. 277 2002 10842-10851
9. Brochu G. Shah G.M. Poirier G.G. Purification of poly(ADP-ribose) glycohydrolase and detection of its isoforms by a zymogram following one- or twodimensional electrophoresis Anal Biochem. 218 1994 265-272
10. Casiano C.A. Martin S.J. Green D.R. Tan E.M. Selective cleavage of nuclear autoantigens during CD95 (Fas/APO-1)-mediated T cell apoptosis J. Exp. Med. 184 1996 765-770
11. Chi N.W. Lodish H.F. Tankyrase is a golgi-associated mitogen-activated protein kinase substrate that interacts with IRAP in GLUT4 vesicles J. Biol. Chem. 275 2000 38437-38444
12. D'Amours D. Desnoyers S. D'Silva I. Poirier G.G. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions Biochem. J. 342 1999 249-268
13. Davidovic L. Vodenicharov M. Affar E.B. Poirier G.G. Importance of poly(ADPribose) glycohydrolase in the control of poly(ADP-ribose) metabolism Exp Cell Res. 268 2001 7-13
14. Di Meglio S. Denegri M. Vallefuoco S. Tramontano F. Scovassi A.I. Quesada P. Poly(ADPR) polymerase-1 and poly(ADPR) glycohydrolase level and distribution in differentiating rat germinal cells Mol. Cell Biochem. 248 2003 85-91
15. Du L. Zhang X. Han Y.Y. Burke N.A. Kochanek P.M. Watkins S.C. Graham S.H. Carcillo J.A. Szabo C. Clark R.S. Intra-mitochondrial poly(ADP-ribosylation) contributes to NAD+ depletion and cell death induced by oxidative stress J. Biol. Chem. 278 2003 18426-18433
16. Fan X.C. Steitz J.A. HNS, a nuclear-cytoplasmic shuttling sequence in HuR Proc Natl Acad Sci U S A 95 1998 15293-15298
17. Graham J.M. Rickwood D. Subcellular fractionation-A practical approach 1997 70-81 Oxford University Press Oxford
18. Graves P.R. Lovly C.M. Uy G.L. Piwnica-Worms H. Localization of human Cdc25C is regulated both by nuclear export and 14-3-3 protein binding Oncogene 20 2001 1839-1851
19. Groulx I. Bonicalzi M.E. Lee S. Ran-mediated nuclear export of the von Hippel-Lindau tumor suppressor protein occurs independently of its assembly with cullin-2 J. Biol.Chem. 275 2000 8991-9000
20. Huletsky A. de Murcia G. Muller S. Hengartner M. Lamarre D. Poirier G.G. The effect of poly(ADP-ribosyl)ation on native and H1-depleted chromatin. A role of poly(ADP-ribosyl)ation on core nucleosome structure J. Biol. Chem. 264 1989 8878-8886
21. Johansson M. A human poly(ADP-ribose) polymerase gene family (ADPRTL): cDNA cloning of two novel poly(ADP-ribose) polymerase homologues Genomics 57 1999 442-445
22. Jonsson G.G. Ménard L. Jacobson E.L. Poirier G.G. Jacobson M.K. Effect of hyperthermia on poly(adenosine diphosphate-ribose) glycohydrolase Cancer Res. 48 1988 4240-4243
23. Kaminker P.G. Kim S.H. Taylor R.D. Zebarjadian Y. Funk W.D. Morin G.B. Yaswen P. Campisi J. TANK2, a new TRF1-associated poly(ADP-ribose) polymerase, causes rapid induction of cell death upon overexpression J. Biol. Chem. 276 2001 35891-35899
24. Kaufmann S.H. Desnoyers S. Ottaviano Y. Davidson N.E. Poirier G.G. Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapyinduced apoptosis Cancer Res. 53 1993 3976-3985
25. Kickhoefer V.A. Siva A.C. Kedersha N.L. Inman E.M. Ruland C. Streuli M. Rome L.H. The 193-kD Vault Protein, VPARP, is a novel poly(ADP-ribose) polymerase J. Cell Biol. 146 1999 917-928
26. Krupitza G. Cerutti P. ADP-ribosylation of ADPR-transferase and topoisomerase I in intact mouse epidermal cells JB6 Biochemistry 28 1989 2034-2040
27. Lautier D. Lagueux J. Thibodeau J. Ménard L. Poirier G.G. Molecular and biochemical features of poly(ADP-ribose) metabolism Mol. Cell. Biochem. 122 1993 171-193
28. Lazebnik Y.A. Kaufmann S.H. Desnoyers S. Poirier G.G. Earnshaw W.C. Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE Nature 371 1994 346-347
29. Lin W. Ame J.C. Aboul-Ela N. Jacobson E.L. Jacobson M.K. Isolation and characterization of the cDNA encoding bovine poly(ADP-ribose) glycohydrolase J. Biol. Chem. 272 1997 11895-11901
30. Lyons R.J. Deane R. Lynch D.K. Ye Z.S. Sanderson G.M. Eyre H.J. Sutherland G.R. Daly R.J. Identification of a novel human tankyrase through its interaction with the adaptor protein Grb14 J. Biol. Chem. 276 2001 17172-17180
31. Ma Q. Baldwin K.T. Renzelli A.J. McDaniel A. Dong L. TCDD-Inducible Poly(ADP-ribose) Polymerase: A Novel Response to 2,3,7,8-Tetracholorodibenzo-p-dioxin Biochem. Biophys. Res. Commun. 289 2001 499-506
32. Malanga M. Althaus F.R. Poly(ADP-ribose) molecules formed during DNA repair in vivo J. Biol. Chem. 269 1994 17691-17696
33. Ménissier de Murcia J. Ricoul M. Tartier L. Niedergang C. Huber A. Dantzer F. Schreiber V. Ame J.C. Dierich A. LeMeur M. Sabatier L. Chambon P. de Murcia G. Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse EMBO J. 22 2003 2255-2263
34. Meyer R.G. Meyer-Ficca M.L. Jacobson E.L. Jacobson M.K. Human poly(ADP-ribose) glycohydrolase (PARG) gene and the common promoter sequence it shares with inner mitochondrial membrane translocase 23 (TIM23) Gene 314 2003 181-190
35. Michael W.M. Choi M. Dreyfuss G. A nuclear export signal in hnRNP A1: a signalmediated, temperature-dependent nuclear protein export pathway Cell 83 1995 415-422
36. Michael W.M. Eder P.S. Dreyfuss G. The K nuclear shuttling domain: a novel signal for nuclear import and nuclear export in the hnRNP K protein EMBO J 16 1997 3587-3598
37. Moll U.M. LaQuaglia M. Benard J. Riou G. Wild-type p53 protein undergoes cytoplasmic sequestration in undifferentiated neuroblastomas but not in differentiated tumors Proc Natl Acad Sci U S A 92 1995 4407-4411
38. Nishi K. Yoshida M. Fujiwara D. Nishikawa M. Horinouchi S. Beppu T. Leptomycin B targets a regulatory cascade of crm1, a fission yeast nuclear protein, involved in control of higher order chromosome structure and gene expression J. Biol. Chem. 269 1994 6320-6324
39. Ogata N. Ueda K. Kawaichi M. Hayaishi O. Poly(ADP-ribose) synthetase, a main acceptor of poly(ADP-ribose) in isolated nuclei J. Biol. Chem. 256 1981 4135-4137
40. Ohashi S. Kanai M. Hanai S. Uchiumi F. Maruta H. Tanuma S. Miwa M. Subcellular localization of poly(ADP-ribose) glycohydrolase in mammalian cells Biochem. Biophys. Res. Commun. 307 2003 915-921
41. Panda S. Poirier G.G. Kay S.A. tej defines a role for poly(ADP-ribosyl)ation in establishing period length of the arabidopsis circadian oscillator Developmental Cell 3 2002 1-20
42. Perkins E. Sun D. Nguyen A. Tulac S. Francesco M. Tavana H. Nguyen H. Tugendreich S. Barthmaier P. Couto J. Yeh E. Thode S. Jarnagin K. Jain A. Morgans D. Melese T. Novel inhibitors of poly(ADP-ribose) polymerase/PARP1 and PARP2 identified using a cell-based screen in yeast Cancer Res. 61 2001 4175-4183
43. Roth J. Dobbelstein M. Freedman D.A. Shenk T. Levine A.J. Nucleocytoplasmic shuttling of the hdm2 oncoprotein regulates the levels of the p53 protein via a pathway used by the human immunodeficiency virus rev protein EMBO J. 17 1998 554-564
44. Sallmann F.R. Vodenicharov M.D. Wang Z.Q. Poirier G.G. Characterization of sPARP-1. An alternative product of PARP-1 gene with poly(ADP-ribose) polymerase independent activity of DNA strand breaks J. Biol. Chem. 275 2000 15504-15511
45. Satoh M. Lindahl T. Role of poly(ADP-ribose) formation in DNA repair Nature 356 1992 356-358
46. Satoh M.S. Poirier G.G. Lindahl T. NAD+ dependent repair of damaged DNA by human cell extracts J. Biol. Chem. 268 1993 5480-5487
47. Schreiber V. Ame J.C. Dolle P. Schultz I. Rinaldi B. Fraulob V. Ménissier-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. 277 2002 23028-23036
48. Shaulsky G. Ben-Ze'ev A. Rotter V. Subcellular distribution of the p53 protein during the cell cycle of Balb/c 3T3 cells Oncogene 5 1990 1707-1711
49. Shieh W.M. Ame J.C. Wilson M.V. Wang Z.Q. Koh D.W. Jacobson M.K. Jacobson E.L. Poly(ADP-ribose) polymerase null mouse cells synthesize ADP-ribose polymers J. Biol. Chem. 273 1998 30069-30072
50. Shimokawa T. Masutani M. Nagasawa S. Nozaki T. Ikota N. Aoki Y. Nakagama H. Sugimura T. Isolation and cloning of rat poly(ADP-ribose) glycohydrolase: presence of a potential nuclear export signal conserved in mammalian orthologs J. Biochem. 126 1999 748-755
51. Smith S. Giriat I. Schmitt A. de Lange T. Tankyrase, a poly(ADP-ribose) polymerase at human telomeres Science 282 1998 1484-1487
52. Toyoshima F. Moriguchi T. Wada A. Fukuda M. Nishida E. Nuclear export of cyclin B1 and its possible role in the DNA damage-induced G2 checkpoint EMBO J. 17 1998 2728-2735
53. Winstall E. Affar E.B. Shah R. Bourassa S. Scovassi I. Poirier G.G. Poly(ADP-ribose) glycohydrolase is present and active in mammalian cells as a 110-kDa protein Exp. Cell Res. 246 1999a 395-398
54. Winstall E. Affar E.B. Shah R. Bourassa S. Scovassi I.A. Poirier G.G. Preferential perinuclear localization of poly(ADP-ribose) glycohydrolase Exp. Cell Res. 251 1999b 372-378
55. Wolff B. Sanglier J.J. Wang Y. Leptomycin B is an inhibitor of nuclear export: inhibition of nucleo-cytoplasmic translocation of the human immunodeficiency virus type 1 (HIV-1) Rev protein and Rev-dependent mRNA Chem. Biol. 4 1997 139-147
56. Yu S.W. Wang H. Poitras M.F. Coombs C. Bowers W.J. Federoff H.J. Poirier G.G. Dawson T.M. Dawson V.L. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor Science 297 2002 259-263