Phosphorylation of PML by mitogen-activated protein kinases plays a key role in arsenic trioxide-mediated apoptosis

Cancer Cell

Volumn 5, Issue 4, 2004, Pages 389-401

  Hayakawa, Fumihiko ^a   Privalsky, Martin L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; ARSENIC TRIOXIDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PROMYELOCYTIC LEUKEMIA PROTEIN; RETINOIC ACID RECEPTOR ALPHA;

ANIMAL CELL; APOPTOSIS; ARTICLE; CHEMICAL REACTION; CHO CELL; CONTROLLED STUDY; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; PROTEIN PHOSPHORYLATION; SUMOYLATION; TUMOR SUPPRESSOR GENE;

ANIMALIA;

EID: 1842785771     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1535-6108(04)00082-0     Document Type: Article

References (64)

1. Bode A.M., Dong Z. The paradox of arsenic. molecular mechanisms of cell transformation and chemotherapeutic effects Crit. Rev. Oncol. Hematol. 42:2002;5-24.
2. Brown D., Kogan S., Lagasse E., Weissman I., Alcalay M., Pelicci P.G., Atwater S., Bishop J.M. A PMLRARalpha transgene initiates murine acute promyelocytic leukemia. Proc. Natl. Acad. Sci. USA. 94:1997;2551-2556.
3. 3 exerts dose-dependent dual effects on APL cells Blood. 89:1997;3345-3353.
4. Cobb M.H. MAP kinase pathways. Prog. Biophys. Mol. Biol. 71:1999;479-500.
5. Cuvillier O., Pirianov G., Kleuser B., Vanek P.G., Coso O.A., Gutkind S., Spiegel S. Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature. 381:1996;800-803.
6. D'Orazi G., Cecchinelli B., Bruno T., Manni I., Higashimoto Y., Saito S., Gostissa M., Coen S., Marchetti A., Del Sal G.et al. Homeodomain-interacting protein kinase-2 phosphorylates p53 at Ser 46 and mediates apoptosis. Nat. Cell Biol. 4:2002;11-19.
7. David M., Petricoin E. 3rd, Benjamin C., Pine R., Weber M.J., Larner A.C. Requirement for MAP kinase (ERK2) activity in interferon α- and interferon β-stimulated gene expression through STAT proteins. Science. 269:1995;1721-1723.
8. de The H. Altered retinoic acid receptors. FASEB J. 10:1996;955-960.
9. Deshaies R.J. Phosphorylation and proteolysis. partners in the regulation of cell division in budding yeast Curr. Opin. Genet. Dev. 7:1997;7-16.
10. Desterro J.M., Rodriguez M.S., Hay R.T. SUMO-1 modification of IkappaBalpha inhibits NF-κB activation. Mol. Cell. 2:1998;233-239.
11. Dyck J.A., Maul G.G., Miller W.H. Jr., Chen J.D., Kakizuka A., Evans R.M. A novel macromolecular structure is a target of the promyelocyte-retinoic acid receptor oncoprotein. Cell. 76:1994;333-343.
12. Everett R.D., Lomonte P., Sternsdorf T., van Driel R., Orr A. Cell cycle regulation of PML modification and ND10 composition. J. Cell Sci. 112:1999;4581-4588.
13. Fogal V., Gostissa M., Sandy P., Zacchi P., Sternsdorf T., Jensen K., Pandolfi P.P., Will H., Schneider C., Del Sal G. Regulation of p53 activity in nuclear bodies by a specific PML isoform. EMBO J. 19:2000;6185-6195.
14. Frey R.S., Mulder K.M. Involvement of extracellular signal-regulated kinase 2 and stress-activated protein kinase/Jun N-terminal kinase activation by transforming growth factor beta in the negative growth control of breast cancer cells. Cancer Res. 57:1997;628-633.
15. Goillot E., Raingeaud J., Ranger A., Tepper R.I., Davis R.J., Harlow E., Sanchez I. Mitogen-activated protein kinase-mediated Fas apoptotic signaling pathway. Proc. Natl. Acad. Sci. USA. 94:1997;3302-3307.
16. Goodson M.L., Hong Y., Rogers R., Matunis M.J., Park-Sarge O.K., Sarge K.D. Sumo-1 modification regulates the DNA binding activity of heat shock transcription factor 2, a promyelocytic leukemia nuclear body associated transcription factor. J. Biol. Chem. 276:2001;18513-18518.
17. Gostissa M., Hengstermann A., Fogal V., Sandy P., Schwarz S.E., Scheffner M., Del Sal G. Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1. EMBO J. 18:1999;6462-6471.
18. Grignani F., Fagioli M., Ferrucci P.F., Alcalay M., Pelicci P.G. The molecular genetics of acute promyelocytic leukemia. Blood Rev. 7:1993;87-93. a.
19. Grignani F., Ferrucci P.F., Testa U., Talamo G., Fagioli M., Alcalay M., Mencarelli A., Peschle C., Nicoletti I.et al. The acute promyelocytic leukemia-specific PML-RARα fusion protein inhibits differentiation and promotes survival of myeloid precursor cells. Cell. 74:1993;423-431. b.
20. Guo A., Salomoni P., Luo J., Shih A., Zhong S., Gu W., Paolo Pandolfi P. The function of PML in p53-dependent apoptosis. Nat. Cell Biol. 2:2000;730-736.
21. Hofmann T.G., Moller A., Sirma H., Zentgraf H., Taya Y., Droge W., Will H., Schmitz M.L. Regulation of p53 activity by its interaction with homeodomain-interacting protein kinase-2. Nat. Cell Biol. 4:2002;1-10.
22. Hong S.H., Privalsky M.L. The SMRT corepressor is regulated by a MEK-1 kinase pathway. inhibition of corepressor function is associated with SMRT phosphorylation and nuclear export Mol. Cell. Biol. 20:2000;6612-6625.
23. Hong S.H., Yang Z., Privalsky M.L. Arsenic trioxide is a potent inhibitor of the interaction of SMRT corepressor with Its transcription factor partners, including the PML-retinoic acid receptor alpha oncoprotein found in human acute promyelocytic leukemia. Mol. Cell. Biol. 21:2001;7172-7182.
24. Ishov A.M., Sotnikov A.G., Negorev D., Vladimirova O.V., Neff N., Kamitani T., Yeh E.T., Strauss J.F. 3rd, Maul G.G. PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J. Cell Biol. 147:1999;221-234.
25. Jansen J.H., Mahfoudi A., Rambaud S., Lavau C., Wahli W., Dejean A. Multimeric complexes of the PML-retinoic acid receptor alpha fusion protein in acute promyelocytic leukemia cells and interference with retinoid and peroxisome-proliferator signaling pathways. Proc. Natl. Acad. Sci. USA. 92:1995;7401-7405.
26. Joazeiro C.A., Weissman A.M. RING finger proteins. mediators of ubiquitin ligase activity Cell. 102:2000;549-552.
27. Kahyo T., Nishida T., Yasuda H. Involvement of PIAS1 in the sumoylation of tumor suppressor p53. Mol. Cell. 8:2001;713-718.
28. Kamitani T., Kito K., Nguyen H.P., Wada H., Fukuda-Kamitani T., Yeh E.T. Identification of three major sentrinization sites in PML. J. Biol. Chem. 273:1998;26675-26682. a.
29. Kamitani T., Nguyen H.P., Kito K., Fukuda-Kamitani T., Yeh E.T. Covalent modification of PML by the sentrin family of ubiquitin-like proteins. J. Biol. Chem. 273:1998;3117-3120. b.
30. Kawasaki A., Matsumura I., Kataoka Y., Takigawa E., Nakajima K., Kanakura Y. Opposing effects of PML and PML/RAR alpha on STAT3 activity. Blood. 101:2003;3668-3673.
31. Kim K.I., Baek S.H., Chung C.H. Versatile protein tag, SUMO. its enzymology and biological function J. Cell. Physiol. 191:2002;257-268.
32. Kirsh O., Seeler J.S., Pichler A., Gast A., Muller S., Miska E., Mathieu M., Harel-Bellan A., Kouzarides T., Melchior F., Dejean A. The SUMO E3 ligase RanBP2 promotes modification of the HDAC4 deacetylase. EMBO J. 21:2002;2682-2691.
33. Koken M.H., Puvion-Dutilleul F., Guillemin M.C., Viron A., Linares-Cruz G., Stuurman N., de Jong L., Szostecki C., Calvo F., Chomienne C.et al. The t(15;17) translocation alters a nuclear body in a retinoic acid-reversible fashion. EMBO J. 13:1994;1073-1083.
34. Lavau C., Dejean A. The t(15;17) translocation in acute promyelocytic leukemia. Leukemia. 8:1994;1615-1621.
35. Le X.F., Vallian S., Mu Z.M., Hung M.C., Chang K.S. Recombinant PML adenovirus suppresses growth and tumorigenicity of human breast cancer cells by inducing G1 cell cycle arrest and apoptosis. Oncogene. 16:1998;1839-1849.
36. Li T., Dai W., Lu L. Ultraviolet-induced junD activation and apoptosis in myeloblastic leukemia ML-1 cells. J. Biol. Chem. 277:2002;32668-32676.
37. Liu J.H., Mu Z.M., Chang K.S. PML suppresses oncogenic transformation of NIH/3T3 cells by activated neu. J. Exp. Med. 181:1995;1965-1973.
38. Liu Y., Guyton K.Z., Gorospe M., Xu Q., Lee J.C., Holbrook N.J. Differential activation of ERK, JNK/SAPK and P38/CSBP/RK map kinase family members during the cellular response to arsenite. Free Radic. Biol. Med. 21:1996;771-781.
39. Mahajan R., Gerace L., Melchior F. Molecular characterization of the SUMO-1 modification of RanGAP1 and its role in nuclear envelope association. J. Cell Biol. 140:1998;259-270.
40. Matunis M.J., Wu J., Blobel G. SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex. J. Cell Biol. 140:1998;499-509.
41. Mu Z.M., Chin K.V., Liu J.H., Lozano G., Chang K.S. PML, a growth suppressor disrupted in acute promyelocytic leukemia. Mol. Cell. Biol. 14:1994;6858-6867.
42. Muller S., Matunis M.J., Dejean A. Conjugation with the ubiquitin-related modifier SUMO-1 regulates the partitioning of PML within the nucleus. EMBO J. 17:1998;61-70.
43. Muller S., Berger M., Lehembre F., Seeler J.S., Haupt Y., Dejean A. c-Jun and p53 activity is modulated by SUMO-1 modification. J. Biol. Chem. 275:2000;13321-13329.
44. Niu C., Yan H., Yu T., Sun H.P., Liu J.X., Li X.S., Wu W., Zhang F.Q., Chen Y., Zhou L.et al. Studies on treatment of acute promyelocytic leukemia with arsenic trioxide. remission induction, follow-up, and molecular monitoring in 11 newly diagnosed and 47 relapsed acute promyelocytic leukemia patients Blood. 94:1999;3315-3324.
45. Perez A., Kastner P., Sethi S., Lutz Y., Reibel C., Chambon P. PMLRAR homodimers. distinct DNA binding properties and heteromeric interactions with RXR EMBO J. 12:1993;3171-3182.
46. Pichler A., Gast A., Seeler J.S., Dejean A., Melchior F. The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell. 108:2002;109-120.
47. Rego E.M., Wang Z.G., Peruzzi D., He L.Z., Cordon-Cardo C., Pandolfi P.P. Role of promyelocytic leukemia (PML) protein in tumor suppression. J. Exp. Med. 193:2001;521-529.
48. Rodriguez M.S., Desterro J.M., Lain S., Midgley C.A., Lane D.P., Hay R.T. SUMO-1 modification activates the transcriptional response of p53. EMBO J. 18:1999;6455-6461.
49. Sachdev S., Bruhn L., Sieber H., Pichler A., Melchior F., Grosschedl R. PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev. 15:2001;3088-3103.
50. Salomoni P., Pandolfi P.P. The role of PML in tumor suppression. Cell. 108:2002;165-170.
51. Seeler J.S., Dejean A. Sumo. of branched proteins and nuclear bodies Oncogene. 20:2001;7243-7249.
52. Shen Z.X., Chen G.Q., Ni J.H., Li X.S., Xiong S.M., Qiu Q.Y., Zhu J., Tang W., Sun G.L., Yang K.Q.et al. Use of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia (APL). II. Clinical efficacy and pharmacokinetics in relapsed patients Blood. 89:1997;3354-3360.
53. Sternsdorf T., Jensen K., Will H. Evidence for covalent modification of the nuclear dot-associated proteins PML and Sp100 by PIC1/SUMO-1. J. Cell Biol. 139:1997;1621-1634.
54. Vietor I., Schwenger P., Li W., Schlessinger J., Vilcek J. Tumor necrosis factor-induced activation and increased tyrosine phosphorylation of mitogen-activated protein (MAP) kinase in human fibroblasts. J. Biol. Chem. 268:1993;18994-18999.
55. Wang Z.G., Delva L., Gaboli M., Rivi R., Giorgio M., Cordon-Cardo C., Grosveld F., Pandolfi P.P. Role of PML in cell growth and the retinoic acid pathway. Science. 279:1998;1547-1551. a.
56. Wang Z.G., Ruggero D., Ronchetti S., Zhong S., Gaboli M., Rivi R., Pandolfi P.P. PML is essential for multiple apoptotic pathways. Nat. Genet. 20:1998;266-272. b.
57. Weis K., Rambaud S., Lavau C., Jansen J., Carvalho T., Carmo-Fonseca M., Lamond A., Dejean A. Retinoic acid regulates aberrant nuclear localization of PML-RARα in acute promyelocytic leukemia cells. Cell. 76:1994;345-356.
58. Wu W.S., Xu Z.X., Hittelman W.N., Salomoni P., Pandolfi P.P., Chang K.S. Promyelocytic leukemia protein sensitizes tumor necrosis factor alpha-induced apoptosis by inhibiting the NF-κB survival pathway. J. Biol. Chem. 278:2003;12294-12304.
59. Yang S., Kuo C., Bisi J.E., Kim M.K. PML-dependent apoptosis after DNA damage is regulated by the checkpoint kinase hCds1/Chk2. Nat. Cell Biol. 4:2002;865-870.
60. Zhang T.D., Chen G.Q., Wang Z.G., Wang Z.Y., Chen S.J., Chen Z. Arsenic trioxide, a therapeutic agent for APL. Oncogene. 20:2001;7146-7153.
61. Zhong S., Muller S., Ronchetti S., Freemont P.S., Dejean A., Pandolfi P.P. Role of SUMO-1-modified PML in nuclear body formation. Blood. 95:2000;2748-2752.
62. Zhu J., Koken M.H., Quignon F., Chelbi-Alix M.K., Degos L., Wang Z.Y., Chen Z., de The H. Arsenic-induced PML targeting onto nuclear bodies. implications for the treatment of acute promyelocytic leukemia Proc. Natl. Acad. Sci. USA. 94:1997;3978-3983.
63. Zhu J., Lallemand-Breitenbach V., de The H. Pathways of retinoic acid- or arsenic trioxide-induced PML/RARalpha catabolism, role of oncogene degradation in disease remission. Oncogene. 20:2001;7257-7265.
64. Zhu L., Yu X., Akatsuka Y., Cooper J.A., Anasetti C. Role of mitogen-activated protein kinases in activation-induced apoptosis of T cells. Immunology. 97:1999;26-35.