Poly(ADP-ribose) polymerase-1 is a survival factor for radiation-exposed intestinal epithelial stem cells in vivo

Nucleic Acids Research

Volumn 31, Issue 21, 2003, Pages 6198-6205

  Ishizuka, Satoshi ^a,b,c   Martin, Kareen ^b   Booth, Catherine ^b   Potten, Christopher S ^b   de Murcia, Gilbert ^d   Bürkle, Alexander ^a   Kirkwood, Thomas B L ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b CHRISTIE HOSPITAL   (United Kingdom)

^c HOKKAIDO UNIVERSITY   (Japan)

^d Atomique Ecole Sup de Biotechnolgie   (France)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN MDM2; PROTEIN P21; PROTEIN P53;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTORADIOGRAPHY; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CRYPT CELL; DNA DAMAGE; DNA STRAND BREAKAGE; DNA SYNTHESIS INHIBITION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INTESTINE EPITHELIUM; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIATION DOSE; STEM CELL; WHOLE BODY RADIATION;

ANIMALS; APOPTOSIS; CELL SURVIVAL; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; DNA REPLICATION; EPITHELIAL CELLS; GAMMA RAYS; GENE DELETION; INTESTINES; MICE; MICE, KNOCKOUT; MITOSIS; NUCLEAR PROTEINS; POLY(ADP-RIBOSE) POLYMERASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MDM2; STEM CELLS; TIME FACTORS; TUMOR SUPPRESSOR PROTEIN P53;

ANIMALIA; MAMMALIA;

EID: 0344874229     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkg840     Document Type: Article

References (52)

1. Bürkle,A. (2001) Physiology and pathophysiology of poly(ADP-ribosyl)ation. Bioessays, 23, 795-806.
2. Shall,S. and de Murcia,G. (2000) Poly(ADP-ribose) polymerase-1: what have we learned from the deficient mouse model? Mutat. Res., 460, 1-15.
3. Grube,K., and Bürkle,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, 759-763.
4. Muiras,M.-L., Müller,M., Schächter,F. and Bürkle,A. (1998) Increased poly(ADP-ribose) polymerase activity in lymphoblastoid cell lines from centenarians. J. Mol. Med, 76, 346-354.
5. Malanga,M., Pleschke,J.M., Kleczkowska,H.E. and Althaus,F.R. (1998) Poly(ADP-ribose) binds to specific domains of p53 and alters its DNA binding functions. J. Biol. Chem., 273, 11839-11843.
6. Pleschke,J.M., Keczkowska,H.E., Strohm,M. and Althaus,F.R. (2000) Poly(ADP-ribose) binds to specific domains in DNA damage checkpoint proteins. J. Biol. Chem., 275, 40974-40980.
7. Lu,Y., Hall,T., Gay,L.S. and Donelson,J.E. (1993) Point mutations are associated with a gene duplication leading to the bloodstream reexpression of a trypanosome metacyclic VSG. Cell, 72, 397-406.
8. Kumari,S.R., Mendoza-Alvarez,H. and Alvarez-Gonzalez,R. (1998) Functional interactions of p53 with poly(ADP-ribose) polymerase (PARP) during apoptosis following DNA damage: covalent poly(ADP-ribosyl)ation of p53 by exogenous PARP and noncovalent binding of p53 to the M(r) 85,000 proteolytic fragment. Cancer Res., 58, 5075-5078.
9. Wesierska-Gadek,J., Bugajska-Schretter,A. and Cerni,C. (1996) ADP-ribosylation of p53 tumor suppressor protein: mutant but not wild-type p53 is modified. J. Cell. Biochem., 62, 90-101.
10. Smith,H.M. and Grosovsky,A.J. (1999) PolyADP-ribose-mediated regulation of p53 complexed with topoisomerase I following ionizing radiation. Carcinogenesis, 20, 1439-1443.
11. Harper,J.W., Adami,G.R., Wei,N., Keyomarsi,K. and Elledge,S.J. (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell, 75, 805-816.
12. Xiong,Y., Hannon,G.J., Zhang,H., Casso,D., Kobayashi,R. and Beach,D. (1993) p21 is a universal inhibitor of cyclin kinases. Nature, 366, 701-704.
13. Gartel,A.L. and Tyner,A.L. (1999) Transcriptional regulation of the p21((WAF1/CIP1)) gene. Exp. Cell Res., 246, 280-289.
14. Macleod,K.F., Sherry,N., Hannon,G., Beach,D., Tokino,T., Kinzler,K., Vogelstein,B. and Jacks,T. (1995) p53-dependent and independent expression of p21 during cell growth, differentiation and DNA damage. Genes Dev., 9, 935-944.
15. Ménissier-deMurcia,J.M., Niedergang,C., Trucco,C., Ricoul,M., Dutrillaux,B., Mark,M., Oliver,F.J., Masson,M., Dierich,A., LeMeur,M., Walztinger,C., Chambon,P. and 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.
16. Potten,C.S. (1998) Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Philos. Trans. R. Soc. Lond. B Biol. Sci., 353, 821-830.
17. Martin,K., Kirkwood,T.B.L. and Potten,C.S. (1998) Age changes in stem cells of murine small intestinal crypts. Exp. Cell Res., 241, 316-323.
18. Martin,K., Potten,C.S. and Kirkwood,T.B.L. (2000) Age-related changes in irradiation-induced apoptosis and expression of p21 and p53 in crypt stem cells of murine intestine. Ann. N. Y. Acad. Sci., 908, 315-318.
19. Wilson,J.W. and Potten,C.S. (1996) Immunohistochemical localization of BAX and BAD in the normal and BCL-2 null gastrointestinal tract. Apoptosis, 1, 183-190.
20. Ijiri,K. and Potten,C.S. (1983) Response of intestinal cells of differing topographical and hierarchical status to ten cytotoxic drugs and five sources of radiation. Br. J. Cancer, 47, 175-185.
21. Keff,J.F., Wyllie,A.H. and Currie,A.R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer, 26, 239-257.
22. Potten,C.S. (1990) A comprehensive study of the radiobiological response of the murine (BDF1) small intestine. Int. J. Radiat. Biol., 58, 925-973.
23. Potten,C.S. and Hendry,J.H. (1985) The microcolony assay in mouse small intestine. In Potten,C.S. and Hendry,J.H. (eds), Cell Clones: Manual Mammalian Cell Techniques. Churchill Livingstone, Edinburgh, UK, pp. 50-60.
24. Potten,C.S., Rezvani,M., Hendry,J.H., Moore,J.V. and Major,D. (1981) The correction of intestinal microcolony counts for variation in size. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med., 40, 321-326.
25. Roberts,S.A. (1990) DRFIT: a program for fitting radiation survival models. Int. J. Radiat. Biol., 57, 1243-1246.
26. Wilson,J.W., Pritchard,D.M., Hickman,J.A. and Potten,C.S. (1998) Radiation-induced p53 and p21WAF-1/CIP1 expression in the murine intestinal epithelium: apoptosis and cell cycle arrest. Am. J. Pathol., 153, 899-909.
27. Vaziri,H., West,M.D., Allsopp,R.C., Davison,T.S., Wu,Y.S., Arrowsmith,C.H., Poirier,G.G. and Benchimol,S. (1997) ATM-dependent telomere loss in aging human diploid fibroblasts and DNA damage lead to the post-translational activation of p53 protein involving poly(ADP-ribose) polymerase. EMBO J., 16, 6018-6033.
28. Wesierska-Gadek,J., Schmid,G. and Cerni,C. (1996) ADP-ribosylation of wild-type p53 in vitro: binding of p53 protein to specific p53 consensus sequence prevents its modification. Biochem. Biophys. Res. Commun., 224, 96-102.
29. Berger,N.A. and Petzold,A.J. (1985) Identification of minimal size requirements of DNA for activation of poly(ADP-ribose) polymerase. Biochemistry, 24, 4352-4355.
30. Bürkle,A., Chen,G., Küpper,J.H., Grube,K. and Zeller,W.J. (1993) Increased poly(ADP-ribosyl)ation in intact cells by cisplatin treatment. Carcinogenesis, 14, 559-561.
31. Juarez-Salinas,H., Sims,J.L. and Jacobson,M.K. (1979) Poly(ADP-ribose) levels in carcinogen-treated cells. Nature, 282, 740-741.
32. Janz,C. and Wiesmüller,L. (2002) Wild-type p53 inhibits replication-associated homologous recombination. Oncogene, 21, 5929-5933.
33. Meyer,R., Müller,M., Beneke,S., Küpper,J.H. and Bürkle,A. (2000) Negative regulation of alkylation-induced sister-chromatid exchanges by poly(ADP-ribose) polymerase-1 activity. Int. J. Cancer, 88, 351-355.
34. Simbulan-Rosenthal,C.M., Haddad,B.R., Rosenthal,D.S., Weaver,Z., Coleman,A., Luo,R., Young,H.M., Wang,Z.Q., Ried,T. and Smulson,M.E. (1999) Chromosomal aberrations in PARP(-/-) mice: genome stabilization in immortalized cells by reintroduction of poly(ADP-ribose) polymerase cDNA. Proc. Natl Acad Sci. USA, 96, 13191-13196.
35. Wesierska-Gadek,J., Wang,Z.Q. and Schmid,G. (1999) Reduced stability of regularly spliced but not alternatively spliced p53 protein in PARP-deficient mouse fibroblasts. Cancer Res., 59, 28-34.
36. Agarwal,M.L., Agarwal,A., Taylor,W.R., Wang,Z.Q., Wagner,E.F. and Stark,G.R. (1997) Defective induction but normal activation and function of p53 in mouse cells lacking poly-ADP-ribose polymerase. Oncogene, 15, 1035-1041.
37. Valenzuela,M.T., Guerrero,R., Nunez,M.I., Ruiz De Almodovar,J.M., Sarker,M., de Murcia,G. and Oliver,F.J. (2002) PARP-1 modifies the effectiveness of p53-mediated DNA damage response. Oncogene, 21, 1108-1116.
38. Beneke,R., Geisen,C., Zevnik,B., Bauch,T., Müller,,W.U., Küpper,J.H. and 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.
39. Waga,S., Hannon,G.J., Beach,D. and Stillman,B. (1994) The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature, 369, 574-578.
40. Brugarolas,J., Chandrasekaran,C., Gordon,J.I., Beach,D., Jacks,T. and Hannon,G.J. (1995) Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature, 377, 552-557.
41. DelSal,G., Murphy,M., Ruaro,E., Lazarevic,D., Levine,A.J. and Schneider,C. (1996) Cyclin D1 and p21/waf1 are both involved in p53 growth suppression. Oncogene, 12, 177-185.
42. Dulic,V., Kaufmann,W.K., Wilson,S.J., Tlsty,T.D., Lees,E., Harper,J.W., Elledge,S.J. and Reed,S.I. (1994) p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell, 76, 1013-1023.
43. Waldman,T., Kinzler,K.W. and Vogelstein,B. (1995) p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res., 55, 5187-5190.
44. Pritchard,D.M., Jackman,A., Potten,C.S. and Hickman,J.A. (1998) Chemically-induced apoptosis: p21 and p53 as determinants of enterotoxin activity. Toxicol. Lett., 102-103, 19-27.
45. Wang,X., Ohnishi,K., Takahashi,A. and Ohnishi,J. (1998) Poly(ADP-ribosyl)ation is required for p53-dependent signal transduction induced by radiation. Oncogene, 17, 2819-2825.
46. Masutani,M., Nozaki,T., Nakamoto,K., Nakagama,H., Suzuki,H., Kusuoka,O., Tsutsumi,M. and Sugimura,T. (2000) The response of Parp knockout mice against DNA damaging agents. Mutat. Res., 462, 159-166.
47. Hendry,J.H., Cai,W.B., Roberts,S.A. and Potten,C.S. (1997) p53 deficiency sensitizes clonogenic cells to irradiation in the large but not the small intestine. Radiat. Res., 148, 254-259.
48. Hendry,J.H., Broadbent,D.A., Roberts,S.A. and Potten,C.S. (2000) Effects of deficiency in p53 or bcl-2 on the sensitivity of clonogenic cells in the small intestine to low dose-rate irradiation. Int. J. Radiat. Biol., 76, 559-565.
49. Hoyes,K.P., Cai,W.B., Potten,C.S. and Hendry,J.H. (2000) Effect of bcl-2 deficiency on the radiation response of clonogenic cells in small and large intestine, bone marrow and testis. Int. J. Radiat. Biol., 76, 1435-1442.
50. Merritt,A.J., Potten,C.S., Kemp,C.J., Hickman,J.A., Balmain,A., Lane,D.P. and Hall,P.A. (1994) The role of p53 in spontaneous and radiation-induced apoptosis in the gastrointestinal tract of normal and p53-deficient mice. Cancer Res., 54, 614-617.
51. Merritt,A.J., Allen,T.D., Potten,C.S. and Hickman,J.A. (1997) Apoptosis in small intestinal epithelial from p53-null mice: evidence for a delayed, p53-independent G2/M-associated cell death after gamma-irradiation. Oncogene, 14, 2759-2766.
52. Ménissier-deMurcia,J., Mark,M., Wendling,O., Wynshaw-Boris,A. and de Murcia,G. (2001) Early embryonic lethality in PARP-1 Atm double-mutant mice suggests a functional synergy in cell proliferation during development. Mol. Cell Biol., 21, 1828-1832.