Increased acetylation of lysine 317/320 of p53 caused by BCR-ABL protects from cytoplasmic translocation of p53 and mitochondria-dependent apoptosis in response to DNA damage

Apoptosis

Volumn 17, Issue 9, 2012, Pages 950-963

  Kusio Kobialka, Monika ^a   Wolanin, Kamila ^a   Podszywalow Bartnicka, Paulina ^a   Sikora, Ewa ^a   Skowronek, Krzysztof ^a,b   McKenna, Sharon L ^c   Ghizzoni, Massimo ^d   Dekker, Frank J ^d   Piwocka, Katarzyna ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^b INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^c UNIVERSITY COLLEGE CORK   (Ireland)

^d UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Acetylation; Apoptosis; BCR ABL; DNA damage; p53; PCAF

Indexed keywords

ACYLTRANSFERASE; BCR ABL PROTEIN; LYSINE; PROTEIN BAX; PROTEIN P53;

ACETYLATION; ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN TRANSPORT;

ACETYLATION; ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE; CELL SURVIVAL; CYTOPLASM; DNA DAMAGE; ENZYME ACTIVATION; FUSION PROTEINS, BCR-ABL; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MICE; MITOCHONDRIA; P300-CBP TRANSCRIPTION FACTORS; PROTEIN TRANSPORT; RNA INTERFERENCE; RNA, SMALL INTERFERING; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84865125993     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-012-0739-9     Document Type: Article

References (47)

1. Halazonetis TD, Gorgoulis VG, Bartek J (2008) An oncogene-induced DNA damage model for cancer development. Science 319:1352-1355 (Pubitemid 351354863)
2. Hoeijmakers JH (2007) Genome maintenance mechanisms are critical for preventing cancer as well as other aging-associated diseases. Mech Ageing Dev 128:460-462 (Pubitemid 47223370)
3. Jeggo PA (2005) Genomic instability in cancer development. Adv Exp Med Biol 570:175-197 (Pubitemid 47413189)
4. Meek DW (2009) Tumour suppression by p53: a role for the DNA damage response? Nat Rev Cancer 9:714-723
5. Melo JV, Barnes DJ (2007) Chronic myeloid leukaemia as a model of disease evolution in human cancer. Nat Rev Cancer 7:441-453 (Pubitemid 46823444)
6. Di Bacco A, Keeshan K, McKenna SL, Cotter TG (2000) Molecular abnormalities in chronic myeloid leukemia: deregulation of cell growth and apoptosis. Oncologist 5:405-415
7. Fridman JS, Lowe SW (2003) Control of apoptosis by p53. Oncogene 22:9030-9040 (Pubitemid 38121703)
8. Galluzzi L, Morselli E, Kepp O, Tajeddine N, Kroemer G (2008) Targeting p53 to mitochondria for cancer therapy. Cell Cycle 7:1949-1955 (Pubitemid 352030339)
9. Pietrzak M, Puzianowska-Kuznicka M (2008) p53-Dependent repression of the human MCL-1 gene encoding an anti-apoptotic member of the BCL-2 family: the role of Sp1 and of basic transcription factor binding sites in the MCL-1 promoter. Biol Chem 389:383-393 (Pubitemid 351773909)
10. Speidel D (2010) Transcription-independent p53 apoptosis: an alternative route to death. Trends Cell Biol 20:14-24
11. Chipuk JE, Maurer U, Green DR, Schuler M (2003) Pharmacologic activation of p53 elicits Bax-dependent apoptosis in the absence of transcription. Cancer Cell 4:371-381 (Pubitemid 37491098)
12. Toledo F, Wahl GM (2006) Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat Rev Cancer 6:909-923 (Pubitemid 44862676)
13. Ferecatu I, Rincheval V, Mignotte B, Vayssiere JL (2009) Tickets for p53 journey among organelles. Front Biosci 14:4214-4228
14. Yamaguchi H, Woods NT, Piluso LG, Lee HH, Chen J, Bhalla KN, Monteiro A, Liu X, Hung MC, Wang HG (2009) p53 Acetylation is crucial for its transcription-independent proapoptotic functions. J Biol Chem 284:11171-11183
15. Ogryzko VV, Schiltz RL, Russanova V, Howard BH, Nakatani Y (1996) The transcription coactivators p300 and CBP are histone acetyltransferases. Cell 87(5):953-959 (Pubitemid 26404293)
16. Liu L, Scolnick DM, Trievel RC, Zhang HB, Marmorstein R, Halazonetis TD, Berger SL (1999) p53 Sites acetylated in vitro by PCAF and p300 are acetylated in vivo in response to DNA damage. Mol Cell Biol 19(2):1202-1209 (Pubitemid 29046862)
17. Sakaguchi K, Herrera JE, Saito S, Miki T, Bustin M, Vassilev A, Anderson CW, Appella E (1998) DNA damage activates p53 through a phosphorylation- acetylation cascade. Genes Dev 12:2831-2841 (Pubitemid 28440142)
18. Lee SM, Bae JH, Kim MJ, Lee HS, Lee MK, Chung BS, Kim DW, Kang CD, Kim SH (2007) Bcr-Abl-independent imatinib-resistant K562 cells show aberrant protein acetylation and increased sensitivity to histone deacetylase inhibitors. J Pharmacol Exp Ther 322:1084-1092 (Pubitemid 47295793)
19. Skorski T (2008) BCR/ABL, DNA damage and DNA repair: implications for new treatment concepts. Leuk Lymphoma 49:610-614 (Pubitemid 351517197)
20. Stoklosa T, Poplawski T, Koptyra M, Nieborowska-Skorska M, Basak G, Slupianek A, Rayevskaya M, Seferynska I, Herrera L, Blasiak J, Skorska T (2008) BCR/ABL inhibits mismatch repair to protect from apoptosis and induce point mutations. Cancer Res 68:2576-2580 (Pubitemid 351556254)
21. Keeshan K, Mills KI, Cotter TG, McKenna SL (2001) Elevated Bcr-Abl expression levels are sufficient for a haematopoietic cell line to acquire a drug-resistant phenotype. Leukemia 15:1823-1833 (Pubitemid 33114987)
22. Keeshan K, Cotter TG, McKenna SL (2002) High Bcr-Abl expression prevents the translocation of Bax and Bad to the mitochondrion. Leukemia 16:1725-1734
23. Ghizzoni M, Boltjes A, Graaf C, Haisma HJ, Dekker FJ (2010) Improved inhibition of the histone acetyltransferase PCAF by an anacardic acid derivative. Bioorg Med Chem 18(16):5826-5834
24. Moll UM, Wolff S, Speidel D, Deppert W (2005) Transcription-independent pro-apoptotic functions of p53. Curr Opin Cell Biol 17:631-636 (Pubitemid 41540413)
25. Chipiuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, Green DR (2004) Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303(5660):1010-1014 (Pubitemid 38209704)
26. Strom E, Sahte S, Komaroy PG, Chernova OB, Pavlovska I, Shynhynova I, Bosykh DA, Burdelya LG, Macklis RM, Skaliter R, Komarova EA, Gudkov AV (2006) Small-molecule inhibitor of p53 binding to mitochondria protects mice from gamma radiation. Nat Chem Biol 2(9):474-479 (Pubitemid 44266309)
27. Hagn F, Klein C, Demmer O, Marchenko N, Vaseya A, Moll UM, Kessler H (2010) BclxL changes conformation upon binding to wild-type but not mutant p53 DNA binding domain. J Biol Chem 285(5):3439-3450
28. Liang SH, Clarke MF (2001) Regulation of p53 localization. Eur J Biochem 268:2779-2783 (Pubitemid 32862959)
29. Dekker FJ, Ghizzoni M, van der Meer N, Wisastra R, Haisma HJ (2009) Inhibition of the PCAF histone acetyl transferase and cell proliferation by isothiazolones. Bioorg Med Chem 17(2):460-466
30. Green DR, Kroemer G (2009) Cytoplasmic functions of the tumour suppressor p53. Nature 458(7242):1127-1130
31. Schuler M, Green DR (2005) Transcription, apoptosis and p53: catch-22. Trends Genet 21:182-187 (Pubitemid 40269857)
32. Speidel D, Helmbold H, Deppert W (2006) Dissection of transcriptional and non-transcriptional p53 activities in the response to genotoxic stress. Oncogene 25:940-953 (Pubitemid 43237712)
33. Chipuk JE, Green DR (2004) Cytoplasmic p53: Bax and forward. Cell Cycle 3:429-431 (Pubitemid 40278229)
34. Gavathiotis E, Reyna DE, Davis ML, Bird GH, Walensky LD (2010) BH3-triggered structural reorganization drives the activation of proapoptotic BAX. Moll Cell 40(3):481-492
35. Knudson AG (2001) Two genetic hits (more or less) to cancer. Nat Rev Cancer 1(2):157-162 (Pubitemid 33741891)
36. Callus BA, Moujallad DM, Silke J, Gerl R, Jabbour AM, Ekert PG, Vaux DL (2008) Triggering apoptosis by Puma is determined by the he threshold set by prosurvival Bcl-2 family proteins. J Mol Biol 384(2):313-323
37. Degenhart K, Chen G, Lindsten T, White E (2002) BAX and BAK mediate p53-independent suppression of tumorigenesis. Cancer Cell 2(3):193-203 (Pubitemid 41043975)
38. Chao C, Wu Z, Mazur SJ, Borges H, Rossi M, Lin T, Wang J, Anderson CW, Appella E, Xu Y (2006) Acetylation of mouse p53 at lysine 317 negatively regulates p53 apoptotic activities after DNA damage. Mol Cell Biol 26:6859-6869 (Pubitemid 44387635)
39. Knights CD, Catania J, Di Giovanni S, Muratoglu S, Perez R, Swartzbeck A, Quong AA, Zhang X, Beerman T, Pestell RG, Avantaggiati ML (2006) Distinct p53 acetylation cassettes differentially influence gene-expression patterns and cell fate. J Cell Biol 173:533-544 (Pubitemid 43765200)
40. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P, Moll UM (2003) p53 Has a direct apoptogenic role at the mitochondria. Mol Cell 11(3):577-590 (Pubitemid 36385115)
41. Horita M, Andreu EJ, Benito A, Arbona C, Sanz C, Benet I, Prosper F, Fernandez-Luna JL (2000) Blockade of the Bcr-Abl kinase activity induces apoptosis of chronic myelogenous leukemia cells by suppressing signal transducer and activator of transcription 5-dependent expression of Bcl-xL. J Exp Med 191(6):977-984
42. Bai L, Zhu W-G (2006) p53: structure, function and therapeutic applications. J Cancer Mol 2(4):141-153
43. Li M, Luo J, Brooks CL, Gu W (2002) Acetylation of p53 inhibits its ubiquitination by Mdm2. J Biol Chem 277(52):50607-50611 (Pubitemid 36042220)
44. Le Cam L, Linares LK, Paul C, Julien E, Lacroix M, Hatchi E, Triboulet R, Bossis G, Shmueli A, Rodriguez MS, Coux O, Sardet C (2006) E4F1 is an atypical ubiquitin ligase that modulates p53 effector functions independently of degradation. Cell 127(4):775-788 (Pubitemid 44716249)
45. Marchenko ND, Wolff S, Erster S, Becker K, Moll UM (2007) Monoubiquitylation promotes mitochondrial p53 translocation. EMBO J 26(4):923-934
46. Palacios G, Moll UM (2006) Mitochondrially targeted wild-type p53 suppresses growth of mutant p53 lymphomas in vivo. Oncogene 25(45):6133-6139 (Pubitemid 44562412)
47. Chipuk JE, Bouchier-Hayes L, Kuwana T, Newmeyer DD, Green DR (2005) PUMA couples the nuclear and cytoplasmic proapoptotic function of p53. Science 309(5741):1732-1735 (Pubitemid 41285944)