PIC-1/SUMO-1-modified PML-retinoic acid receptor α mediates arsenic trioxide-induced apoptosis in acute promyelocytic leukemia

Molecular and Cellular Biology

Volumn 19, Issue 7, 1999, Pages 5170-5178

  Sternsdorf, Thomas ^a   Puccetti, Elena ^b   Jensen, Kirsten ^a   Hoelzer, Dieter ^b   Will, Hans ^a   Ottmann, Oliver Gerhard ^b   Ruthardt, Martin ^b,c  

^a LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC TRIOXIDE; CASPASE 3; HYBRID PROTEIN; NUCLEAR PROTEIN; PROTEIN BCL 2; RETINOIC ACID; RETINOIC ACID RECEPTOR; ZINC;

ACUTE MYELOBLASTIC LEUKEMIA; APOPTOSIS; ARTICLE; CONTROLLED STUDY; GENETIC MARKER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; REMISSION;

EID: 0033037274     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.19.7.5170     Document Type: Article

References (57)

1. Alcalay, M., L. Tomassoni, E. Colombo, S. Stoldt, F. Grignani, M. Fagioli, L. Szekely, K. Helin, and P. G. Pelicci. 1998. The promyelocytic leukemia gene product (PML) forms stable complexes with the retinoblastoma protein. Mol. Cell. Biol. 18:1084-1093.
2. Ascoli, C. A., and G. G. Maui. 1991. Identification of a novel nuclear domain. J. Cell Biol. 112:785-795.
3. Bloch, D. B., S. M. de la Monte, P. Guigaouri, A. Filippov, and K. D. Bloch. 1996. Identification and characterization of a leukocyte-specific component of the nuclear body. J. Biol. Chem. 271:29198-29204.
4. Boddy, M. N., K. Howe, L. D. Etkin, E. Solomon, and P. S. Freemont. 1996. PIC 1, a novel ubiquitin-like protein which interacts with the PML component of a multiprotein complex that is disrupted in acute promyelocytic leukemia. Oncogene 13:971-982.
5. Chen, G. Q., X. G. Shi, W. Tang, S. M. Xiong, J. Zhu, X. Cai, Z. G. Han, J. H. Ni, G. Y. Shi, P. M. Jia, M. M. Liu, K. L. He, C. Niu, J. Ma, P. Zhang, T. D. Zhang, P. Paul, T. Naoe, K. Kitamura, W. Miller, S. Waxman, Z. Y. Wang, H. de The, S. J. Chen, and Z. Chen. 1997. Use of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia (APL). I. As2O3 exerts dose-dependent dual effects on APL cells. Blood 89:3345-3353.
6. Chen, G. Q., J. Zhu, X. G. Shi, J. H. Ni, H. J. Zhong, G. Y. Si, X. L. Jin, W. Tang, X. S. Li, S. M. Xong, Z. X. Shen, G. L. Sun, J. Ma, P. Zhang, T. D. Zhang, C. Gazin, T. Naoe, S. J. Chen, Z. Y. Wang, and Z. Chen. 1996. In vitro studies on cellular and molecular mechanisms of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia: As2O3 induces NB4 cell apoptosis with downregulation of Bcl-2 expression and modulation of PML-RAR alpha/PML proteins. Blood 88:1052-1061.
7. Chen, Z., N. J. Brand, A. Chen, S. J. Chen, J. H. Tong, Z. Y. Wang, S. Waxman, and A. Zelent. 1993. Fusion between a novel Kruppel-like zinc finger gene and the retinoic acid receptor-alpha locus due to a variant t(11;17) translocation associated with acute promyelocytic leukaemia. EMBO J. 12:1161-1167.
8. Collins, S. J. 1987. The HL-60 promyelocytic leukemia cell line: proliferation, differentiation, and cellular oncogene expression. Blood 70:1233-1244.
9. Daniel, M. T., M. Koken, O. Romagne, S. Barbey, A. Bazarbachi, M. Stadler, M. C. Guillemin, L. Degos, C. Chomienne, and H. de The. 1993. PML protein expression in hematopoietic and acute promyelocytic leukemia cells. Blood 82:1858-1867.
10. Degos, L. 1992. Retinoic acid in acute promyelocytic leukemia: a model for differentiation therapy. Curr. Opin. Oncol. 4:45-52.
11. Degos, L., H. Dombret, C. Chomienne, M. T. Daniel, J. M. Miclea, C. Chastang, S. Castaigne, and P. Fenaux. 1995. All-trans-retinoic acid as a differentiating agent in the treatment of acute promyelocytic leukemia. Blood 85:2643-2653.
12. Dent, A. L., J. Yewdell, F. Puvion-Dutilleul, M. H. Koken, H. de The, and L. M. Staudt. 1996. LYSP100-associated nuclear domain (LANDs): description of a new class of subnuclear structures and their relationship to PML nuclear bodies. Blood 88:1423-1426.
13. Desbois, C., R. Rousset, F. Bantignies, and P. Jalinot. 1996. Exclusion of Int-6 from PML nuclear bodies by binding to the HTLV-I Tax oncoprotein. Science 273:951-953.
14. Dyck, J. A., G. G. Maul, W. H. Miller, Jr., J. D. Chen, A. Kakizuka, and R. M. Evans. 1994. A novel macromolecular structure is a target of the promyelocyte-retinoic acid receptor oncoprotein. Cell 76:333-343.
15. Flenghi, L., M. Fagioli, L. Tomassoni, S. Pileri, M. Gambacorta, R. Pacini, F. Grignani, T. Casini, P. F. Ferrucci, M. F. Martelli, et al. 1995. Characterization of a new monoclonal antibody (PG-M3) directed against the aminoterminal portion of the PML gene product: immunocytochemical evidence for high expression of PML proteins on activated macrophages, endothelial cells, and epithelia. Blood 85:1871-1880.
16. Gianni, M., M. H. Koken, M. K. Chelbi-Alix, G. Benoit, M. Lanotte, Z. Chen, and H. de The. 1998. Combined arsenic and retinoic acid treatment enhances differentiation and apoptosis in arsenic-resistant NB4 cells. Blood 91:4300-4310.
17. Gongora, C., G. David, L. Pintard, C. Tissot, T. D. Hua, A. Dejean, and N. Mechti, 1997. Molecular cloning of a new interferon-induced PML nuclear body-associated protein. J. Biol. Chem. 272:19457-19463.
18. Grignani, F., M. Fagioli, M. Alcalay, L. Longo, P. P. Pandolfi, E. Donti, A. Biondi, F. Lo Coco, F. Grignani, and P. G. Pelicci. 1994. Acute promyelocytic leukemia: from genetics to treatment. Blood 83:10-25.
19. Grignani, F., P. F. Ferrucci, U. Testa, G. Talamo, M. Fagioli, M. Alcalay, A. Mencarelli, F. Grignani, C. Peschle, I. Nicholetti, et al. 1993. The acute promyelocytic leukemia-specific PML-RAR alpha fusion protein inhibits differentiation and promotes survival of myeloid precursor cells. Cell 74:423-431.
20. Grignani, F., U. Testa, D. Rogala, P. F. Ferrucci, P. Samoggia, A. Pinto, D. Aldinucci, V. Gelmetti, M. Fagioli, M. Alcalay, J. Seeler, F. Grignani, I. Nicholetti, C. Peschle, and P. G. Pelicci. 1996. Effects on differentiation by the promyelocytic leukemia PML/RARalpha protein depend on the fusion of the PML protein dimerization and RARalpha DNA biding domains. EMBO J. 15:4949-4958.
21. Grisolano, J. L., R. L. Wesselschmidt, P. G. Pelicci, and T. J. Ley. 1997. Altered myeloid development and acute leukemia in transgenic mice expressing PML-RAR alpha under control of cathepsin G regulatory sequences. Blood 89:376-387.
22. Grotzinger, T., K. Jensen, H. H. Guldner, T. Sternsdorf, C. Szostecki, M. Schwab, L. Savelyeva, B. Reich, and H. Will. 1996. A highly amplified mouse gene is homologous to the human interferon-responsive Sp100 gene encoding an autoantigen associated with nuclear dots. Mol. Cell. Biol. 16:1150-1156.
23. Guidez, F., W. Huang, J. H. Tong, C. Dubais, N. Balitrand, S. Waxman, J. L. Michaux, P. Martiat, L. Degos, Z. Chen, et al. 1994. Poor response to all-trans retinoic acid therapy in a t(11;17) PLZF/RAR alpha patient. Leukemia 8:312-317.
24. Huang, M. E., Y. C. Ye, S. R. Chen, J. R. Chai, J. X. Lu, L. Zhoa, L. J. Gu, and Z. Y. Wang. 1988. Use of all-trans retinoic acid in the treatment of acute promyelocytic leukemia. Blood 72:567-572.
25. Kakizuka, A., W. H. Miller, Jr., K. Umesono, R. P. Warrell, Jr., S. R. Frankel, V. V. Murty, E. Dmitrovsky, and R. M. Evans. 1991. Chromosomal translocation t(15;17) in human acute promyelocytic leukemia fuses RAR alpha with a novel putative transcription factor, PML. Cell 64:663-674.
26. Kamilani, T., H. P. Nguyen, K. Kito, T. Fukuda-Kamitani, and E. T. Yeh. 1998. Covalent modification of PML by the sentrin family of ubiquitin-like proteins. J. Biol. Chem. 273:3117-3120.
27. Kastner, P., A. Perez, Y. Lutz, C. Rochette-Egly, M. P. Gaub, B. Durand, M. Lanotte, R. Berger, and P. Chambon. 1992. Structure, localization and transcriptional properties of two classes of retinoic acid receptor alpha fusion proteins in acute promyelocytic leukemia (APL): structural similarities with a new family of oncoproteins. EMBO J. 11:629-642.
28. Koken, M. H., F. Puvion-Dutilleul, M. C. Guillemin, A. Viron, G. Linares-Cruz, N. Stuurman, L. de Jong, C. Szostecki, F. Calvo, C. Chomienne, et al. 1994. The t(15;17) translocation alters a nuclear body in a retinoic acid-reversible fashion. EMBO J. 13:1073-1083.
29. Koken, M. H., A. Reid, F. Quignon, M. K. Chelbi-Alix, J. M. Davies, J. H. Kabarowski, j. Zhu, S. Dong, S. Chen, Z. Chen, C. C. Tan, J. Licht, S. Waxman, H. de The, and A. Zelent 1997. Leukemia-associated retinoic acid receptor alpha fusion partners, PML and PLZF, heterodimerize and colocalize to nuclear bodies. Proc. Natl. Acad. Sci. USA 94:10255-10260.
30. Lanotte, M., V. Martin-Thouvenin, S. Najman, P. Balerin, F. Valensi, and R. Berger. 1991. NB4, a maturation inducible cell line with t(15;17) marker isolated from a human acute promyelocytic leukemia (M3). Blood 77:1080-1086.
31. Licht, J. D., C. Chomienne, A. Goy, A. Chen, A. A. Scott, D. R. Head, J. L. Michaux, Y. Wu, A. DeBlasio, W. H. Miller, Jr., et al. 1995. Clinical and molecular characterization of a rare syndrome of acute promyelocytic leukemia associated with translocation (11;17). Blood 85:1083-1094.
32. Lo Coco, F., G. Awisati, D. Diverio, M. C. Petti, M. Alcalay, P. P. Pandolfi, D. Zangrilli, A. Biondi, A. Rambaldi, M. L. Moleti, et al. 1991. Molecular evaluation of response to all-trans-retinoic acid therapy in patients with acute promyelocytic leukemia. Blood 77:1657-1659.
33. Mahajan, R., C. Delphin, T. Guan, L. Gerace, and F. Melchior. 1997. A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 88:97-107.
34. Mahajan, R., L. Gerace, and F. Melchior. 1998. Molecular characterization of the SUMO-1 modification of RanGAP1 and its role in nuclear envelope association. J. Cell Biol. 140:259-270.
35. Matunis, M. J., E. Coutavas, and G. Blobel. 1996. A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J. Cell Biol. 135:1457-1470.
36. Matunis, M. J., J. Wu, and G. Blobel. 1998. SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear probe complex. J. Cell Biol. 140:499-509.
37. Muller, S., M. J. Matunis, and A. Dejean. 1998. Conjugation with the ubiquitin-related modifier SUMO-1 regulates the partitioning of PML within the nucleus. EMBO J. 17:61-70.
38. Nervi, C., F. F. Ferrara, M. Fanelli, M. R. Rippo, B. Tomassini, P. F. Ferrucci, M. Ruthardt, V. Gelmetti, C. Gambacorti-Passerini, D. Diverio, F. Grignani, P. G. Pelicci, and R. Testi. 1998. Caspases mediate retinoic acid-induced degradation of the acute promyelocytic leukemia PML/RARalpha fusion protein. Blood 92:2244-2251.
39. Okura, T., L. Gong, T. Kamitani, T. Wada, I. Okura, C. F. Wei, H. M. Chang, and E. T. Yeh. 1996. Protection against Fas/APO-1- and tumor necrosis factor-mediated cell death by a novel protein, sentrin. J. Immunol. 157:4277-4281.
40. Pandolfi, P. P., F. Grignani, M. Alcalay, A. Mencarelli, A. Biondi, F. LoCoco, F. Grignani, and P. G. Pelicci. 1991. Structure and origin of the acute promyelocytic leukemia myl/RARalpha cDNA and characterization of its retinoid-binding and transactivation properties. Oncogene 6:1285-1292.
41. Perez, A., P. Kastner, S. Sethi, Y. Lutz, C. Reibel, and P. Chambon. 1993. PMLRAR homodimers: distinct DNA binding properties and heteromeric interactions with RXR. EMBO J. 12:3171-3182.
42. Reid, A., A. Gould, N. Brand, M. Cook, P. Strutt, J. Li, J. Licht, S. Waxman, R. Krumlauf, and A. Zelent. 1996. Leukemia translocation gene, PLZF, is expressed with a speckled nuclear pattern in early hematopoietic progenitors. Am. J. Kidney Dis. 27:134-137.
43. Ruthardt, M., A. Orleth, L. Tomassoni, E. Puccetti, D. Riganelli, M. Alcalay, R. Mannucci, I. Nicoletti, F. Grignani, M. Fagioli, and P. G. Pelicci. 1998 The acute promyelocytic leukaemia specific PML and PLZF proteins localize to adjacent and functionally distinct nuclear bodies. Oncogene 16:1945-1953.
44. Ruthardt, M., U. Testa, C. Nervi, F. Ferrucci, F. Grignani, E. Puccetti, F. Grignani, C. Peschle, and P. G. Pelicci. 1997. Opposite effects of the acute promyelocytic leukemia PML-retinoic acid receptor a (RARα) and PLZF-RARα fusion proteins on retinoic acid signalling. Mol. Cell. Biol. 17:4859-4869.
45. Schmid, I., C. H. Uittenbogaart, B. Keld, and J. V. Giorgi. 1994. A rapid method for measuring apoptosis and dual-color immunofluorescence by single laser flow cytometry. J. Immunol. Methods 170:145-157.
46. Shao, W., M. Fanelli, F. F. Ferrara, R. Riccioni, A. Rosenauer, K. Davison, W. W. Lamph, S. Waxman, P. G. Pelicci, F. Lo Coco, G. Awisati, U. Testa, C. Peschle, C. Gambacorti-Passerni, C. Nervi, W. H. Miller, Jr., A. T. Look, X. Song, J. E. Bishop, W. H. Okamura, A. W. Norman, C. J. Hogan, J. S. Wiley, and T. Billington. 1998. Arsenic trioxide as an inducer of apoptosis and loss of PML/RAR alpha protein in acute promyelocytic leukemia cells. J. Natl. Cancer Inst. 90:124-133.
47. Shen, Z., P. E. Pardington-Purtymun, J. C. Comeaux, R. K. Moyzis, and D. J. Chen. 1996. UBL1, a human ubiquitin-like protein associating with human RAD51/RAD52 proteins. Genomics 36:271-279.
48. Shenk, Z. X., G. Q. Chen, J. H. Ni, X. S. Li, S. M. Xiong, Q. Y. Qiu, J. Zhu, W. Tang, G. L. Sun, K. Q. Yang, Y. Chen, L. Zhou, Z. W. Fang, Y. T. Wang, J. Ma, P. Zhang, T. D. Zhang, S. J. Chen, Z. Chen, and Z. Y. Wang. 1997. Use of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia (APL). II. Clinical efficacy and pharmacokinetics in relapsed patients. Blood 89:3354-3360.
49. Sternsdorf, T., H. H. Guldner, C. Szostecki, T. Grolzinger, and H. Will. 1995. Two nuclear dot-associated proteins, PML and Sp100, are often coautoimmunogenic in patients with primary biliary cirrhosis. Scand. J. Immunol. 42:257-268.
50. Sternsdorf, T., K. Jensen, and H. Will. 1997. Evidence for covalent modification of the nuclear dot-associated proteins PML and Sp100 by PIC-1/SUMO-1. J. Cell Biol. 139:1621-1634.
51. Szostecki, C., H. H. Guldner, H. J. Netler, and H. Will. 1990. Isolation and characterization of cDNA encoding a human nuclear antigen predominantly recognized by autoantibodies from patients with primary biliary cirrhosis. J. Immunol. 145:4338-4347.
52. Warrell, R. P., Jr. 1993. Retinoid resistance in acute promyelocytic leukemia: new mechanisms, strategies, and implications. Blood 82:1949-1953. (Editorial.)
53. Warrell, R. P., Jr., S. R. Frankel, W. H. Miller, Jr., D. A. Scheinberg, L. M. Itri, W. N. Hittelman, R. Vyas, M. Andreeff, A. Tafuri, A. Jakubowski, et al. 1991. Differentiation therapy of acute promyelocytic leukemia with tretinoin (all-trans-retinoic acid). N. Engl. J. Med. 324:1385-1393.
54. Weis, K., S. Rambaud, C. Lavau, J. Jansen, T. Carvalho, M. Carmo-Fonseca, A. Lamond, and A. Dejean. 1994. Retinoic acid regulates aberrant nuclear localization of PML-RAR alpha in acute promyelocytic leukemia cells. Cell 76:345-356.
55. Yang, E., and S. J. Korsmeyer. 1996. Molecular thanatopsis; a discourse on the BCL2 family and cell death. Blood 88:386-401.
56. Yoshida, H., K. Kitamura, K. Tanaka, S. Omura, T. Miyazaki, T. Hachiya, R. Ohno, and T. Naoe. 1996. Accelerated degradation of PML-retinoic acid receptor alpha (PML-RARA) oncoprotein by all-trans-retinoic acid in acute promyelocytic leukemia: possible role of the proteasome pathway. Cancer Res. 56:2945-2948.
57. Zhu, J., M. H. Koken, F. Quignon, M. K. Chelbi-Alix, L. Degos, Z. Y. Wang, Z. Chen, and H. de The. 1997. Arsenic-induced PML targeting onto nuclear bodies: implications for the treatment of acute promyelocytic leukemia. Proc. Natl. Acad. Sci. USA 94:3978-3983.