Altered nuclear cofactor switching in retinoic-resistant variants of the PML-RARα oncoprotein of acute promyelocytic leukemia

Proteins: Structure, Function and Bioinformatics

Volumn 80, Issue 4, 2012, Pages 1095-1109

  Farris, Mindy ^a   Lague, Astrid ^b   Manuelyan, Zara ^b   Statnekov, Jacob ^a   Francklyn, Christopher ^a,b  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF VERMONT   (United States)

Author keywords

All trans retinoic acid; Coactivator; Corepressor; Fluorescence anisotropy; Nuclear receptor; Transcription regulation

Indexed keywords

NUCLEAR FACTOR; PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEINASE; RETINOIC ACID; RETINOIC ACID RECEPTOR ALPHA;

ANISOTROPY; ARTICLE; BONE MARROW CELL; CANCER RESISTANCE; CELL DIFFERENTIATION; CIRCULAR DICHROISM; CONTROLLED STUDY; DISSOCIATION CONSTANT; EMISSION ANISOTROPY; ENZYME ASSAY; GENE MUTATION; GENE TRANSLOCATION; LEUKEMIA CELL LINE; LIGAND BINDING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; QUANTITATIVE ANALYSIS; RNA INTERFERENCE; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE;

AMINO ACID SEQUENCE; ANTINEOPLASTIC AGENTS; CELL DIFFERENTIATION; CELL NUCLEUS; CHEMISTRY TECHNIQUES, SYNTHETIC; CIRCULAR DICHROISM; DRUG RESISTANCE, NEOPLASM; FLUORESCENCE POLARIZATION; HUMANS; LEUKEMIA, PROMYELOCYTIC, ACUTE; MOLECULAR SEQUENCE DATA; MUTATION; MYELOID CELLS; ONCOGENE PROTEINS, FUSION; PROTEOLYSIS; RECEPTORS, RETINOIC ACID; RETINOL-BINDING PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSLOCATION, GENETIC; TRETINOIN;

EID: 84857693180     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24010     Document Type: Article

References (68)

1. Larson RA, Kondo K, Vardiman JW, Butler AE, Golomb HM, Rowley JD. Evidence for a 15;17 translocation in every patient with acute promyelocytic leukemia. Am J Med 1984; 76: 827-841.
2. Warrell RP, Jr., de The H, Wang ZY, Degos L. Acute promyelocytic leukemia. N Engl J Med 1993; 329: 177-189.
3. Slack JL, Gallagher RE. The molecular biology of acute promyelocytic leukemia. Cancer Treat Res 1999; 99: 75-124.
4. Borrow J, Goddard AD, Sheer D, Solomon E. Molecular analysis of acute promyelocytic leukemia breakpoint cluster region on chromosome 17. Science 1990; 249: 1576-1580.
5. de The H, Lavau C, Marchio A, Chomienne C, Degos L, Dejean A. The PML-RAR alpha fusion mRNA generated by the t(15;17) translocation in acute promyelocytic leukemia encodes a functionally altered RAR. Cell 1991; 66: 675-684.
6. Kakizuka A, Miller WH, Jr, Umesono K, Warrell RP, Jr, Frankel SR, Murty VV, Dmitrovsky E, Evans RM. Chromosomal translocation t(15;17) in human acute promyelocytic leukemia fuses RAR alpha with a novel putative transcription factor, PML. Cell 1991; 66: 663-674.
7. Grisolano JL, Wesselschmidt RL, Pelicci PG, Ley TJ. Altered myeloid development and acute leukemia in transgenic mice expressing PML-RAR alpha under control of cathepsin G regulatory sequences. Blood 1997; 89: 376-387.
8. He LZ, Tribioli C, Rivi R, Peruzzi D, Pelicci PG, Soares V, Cattoretti G, Pandolfi PP. Acute leukemia with promyelocytic features in PML/RARalpha transgenic mice. Proc Natl Acad Sci USA 1997; 94: 5302-5307.
9. Westervelt P, Lane AA, Pollock JL, Oldfather K, Holt MS, Zimonjic DB, Popescu NC, DiPersio JF, Ley TJ. A high penetrance mouse model of acute promyelocytic leukemia with very low levels of PML-RAR alpha expression. Blood 2003; 102: 1857-1865.
10. Sanz MA, Lo-Coco F. Modern approaches to treating acute promyelocytic leukemia. J Clin Oncol 2011; 29: 495-503.
11. Bernardi R, Pandolfi PP. Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat Rev Mol Cell Biol 2007; 8: 1006-1016.
12. Salomoni P, Bellodi C. New insights into the cytoplasmic function of PML. Histol Histopathol 2007; 22: 937-946.
13. Lallemand-Breitenbach V, de The H. PML nuclear bodies. Cold Spring Harb Perspect Biol 2010; 2: a000661.
14. Bernardi R, Papa A, Pandolfi PP. Regulation of apoptosis by PML and the PML-NBs. Oncogene 2008; 27: 6299-6312.
15. Ito K, Bernardi R, Morotti A, Matsuoka S, Saglio G, Ikeda Y, Rosenblatt J, Avigan DE, Teruya-Feldstein J, Pandolfi PP. PML targeting eradicates quiescent leukaemia-initiating cells. Nature 2008; 453: 1072-1078.
16. Regad T, Bellodi C, Nicotera P, Salomoni P. The tumor suppressor Pml regulates cell fate in the developing neocortex. Nat Neurosci 2009; 12: 132-140.
17. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J 1996; 10: 940-954.
18. Bourguet W, Germain P, Gronemeyer H. Nuclear receptor ligand-binding domains: three-dimensional structures, molecular interactions and pharmacological implications. Trends Pharmacol Sci 2000; 21: 381-388.
19. McKenna NJ, O'Malley BW. Nuclear receptors, coregulators, ligands, and selective receptor modulators: making sense of the patchwork quilt. Ann N Y Acad Sci 2001; 949: 3-5.
20. Kastner P, Mark M, Chambon P. Nonsteroid nuclear receptors: what are genetic studies telling us about their role in real life? Cell 1995; 83: 859-869.
21. He LZ, Guidez F, Tribioli C, Peruzzi D, Ruthardt M, Zelent A, Pandolfi PP. Distinct interactions of PML-RARalpha and PLZF-RARalpha with co-repressors determine differential responses to RA in APL. Nat Genet 1998; 18: 126-135.
22. Ordentlich P, Downes M, Evans RM. Corepressors and nuclear hormone receptor function. Curr Top Microbiol Immunol 2001; 254: 101-116.
23. McKenna NJ, O'Malley BW. Minireview: nuclear receptor coactivators-an update. Endocrinology 2002; 143: 2461-2465.
24. Nagy L, Kao HY, Chakravarti D, Lin RJ, Hassig CA, Ayer DE, Schreiber SL, Evans RM. Nuclear receptor repression mediated by a complex containing SMRT, mSin3A, and histone deacetylase. Cell 1997; 89: 373-380.
25. Collingwood TN, Urnov FD, Wolffe AP. Nuclear receptors: coactivators, corepressors and chromatin remodeling in the control of transcription. J Mol Endocrinol 1999; 23: 255-275.
26. Warrell RP, Jr, Frankel SR, Miller WH, Jr, Scheinberg DA, Itri LM, Hittelman WN, Vyas R, Andreeff M, Tafuri A, Jakubowski A, Gabrilove J, Gordon MS, Dmitrovsky E. Differentiation therapy of acute promyelocytic leukemia with tretinoin (all-trans-retinoic acid). N Engl J Med 1991; 324: 1385-1393.
27. Degos L, Dombret H, Chomienne C, Daniel MT, Miclea JM, Chastang C, Castaigne S, Fenaux P. All-trans-retinoic acid as a differentiating agent in the treatment of acute promyelocytic leukemia. Blood 1995; 85: 2643-2653.
28. Gallagher RE. Retinoic acid resistance in acute promyelocytic leukemia. Leukemia 2002; 16: 1940-1958.
29. Tsimberidou AM, Tirado-Gomez M, Andreeff M, O'Brien S, Kantarjian H, Keating M, Lopez-Berestein G, Estey E. Single-agent liposomal all-trans retinoic acid can cure some patients with untreated acute promyelocytic leukemia: an update of The University of Texas M. D. Anderson Cancer Center Series. Leuk Lymphoma 2006; 47: 1062-1068.
30. Lo-Coco F, Ammatuna E, Montesinos P, Sanz MA. Acute promyelocytic leukemia: recent advances in diagnosis and management. Semin Oncol 2008; 35: 401-409.
31. Estey E, Garcia-Manero G, Ferrajoli A, Faderl S, Verstovsek S, Jones D, Kantarjian H. Use of all-trans retinoic acid plus arsenic trioxide as an alternative to chemotherapy in untreated acute promyelocytic leukemia. Blood 2006; 107: 3469-3473.
32. Ablain J, de The H. Revisiting the differentiation paradigm in acute promyelocytic leukemia. Blood 2011; 117: 5795-5802.
33. Melnick A, Licht JD. Deconstructing a disease: RARalpha, its fusion partners, and their roles in the pathogenesis of acute promyelocytic leukemia. Blood 1999; 93: 3167-3215.
34. Lin RJ, Nagy L, Inoue S, Shao W, Miller WH, Jr, Evans RM. Role of the histone deacetylase complex in acute promyelocytic leukaemia. Nature 1998; 391: 811-814.
35. Cote S, Zhou D, Bianchini A, Nervi C, Gallagher RE, Miller WH, Jr. Altered ligand binding and transcriptional regulation by mutations in the PML/RARalpha ligand-binding domain arising in retinoic acid-resistant patients with acute promyelocytic leukemia. Blood 2000; 96: 3200-3208.
36. Weber G. Polarization of the fluorescence of macromolecules. I. Theory and experimental method. Biochem J 1952; 51: 145-155.
37. Lakowicz JR. Principles of fluorescence spectroscopy. New York: Kluwer Academic; 1999.
38. Wilson GM. In: Geddes CD, Lakowicz JR, editors. Reviews in fluorescence, Vol. 2. New York: Springer Science Business Media; 2005. Chapter 10, pp 223-243.
39. Moras D, Gronemeyer H. The nuclear receptor ligand-binding domain: structure and function. Curr Opin Cell Biol 1998; 10: 384-391.
40. Egea PF, Mitschler A, Moras D. Molecular recognition of agonist ligands by RXRs. Mol Endocrinol 2002; 16: 987-997.
41. Chen H, Lin RJ, Schiltz RL, Chakravarti D, Nash A, Nagy L, Privalsky ML, Nakatani Y, Evans RM. Nuclear receptor coactivator ACTR is a novel histone acetyltransferase and forms a multimeric activation complex with P/CAF and CBP/p300. Cell 1997; 90: 569-580.
42. Westin S, Kurokawa R, Nolte RT, Wisely GB, McInerney EM, Rose DW, Milburn MV, Rosenfeld MG, Glass CK. Interactions controlling the assembly of nuclear-receptor heterodimers and co-activators. Nature 1998; 395: 199-202.
43. Westin S, Rosenfeld MG, Glass CK. Nuclear receptor coactivators. Adv Pharmacol 2000; 47: 89-112.
44. Shao W, Benedetti L, Lamph WW, Nervi C, Miller WH, Jr. A retinoid-resistant acute promyelocytic leukemia subclone expresses a dominant negative PML-RAR alpha mutation. Blood 1997; 89: 4282-4289.
45. Imaizumi M, Suzuki H, Yoshinari M, Sato A, Saito T, Sugawara A, Tsuchiya S, Hatae Y, Fujimoto T, Kakizuka A, Konno T, Iinuma K. Mutations in the E-domain of RAR portion of the PML/RAR chimeric gene may confer clinical resistance to all-trans retinoic acid in acute promyelocytic leukemia. Blood 1998; 92: 374-382.
46. Ding W, Li YP, Nobile LM, Grills G, Carrera I, Paietta E, Tallman MS, Wiernik PH, Gallagher RE. Leukemic cellular retinoic acid resistance and missense mutations in the PML-RARalpha fusion gene after relapse of acute promyelocytic leukemia from treatment with all-trans retinoic acid and intensive chemotherapy. Blood 1998; 92: 1172-1183.
47. DeLano WL. PyMOL, Version 0.95. San Carlos, CA: Delano Scientific LLS; 2004.
48. Cote S, Rosenauer A, Bianchini A, Seiter K, Vandewiele J, Nervi C, Miller WH, Jr. Response to histone deacetylase inhibition of novel PML/RARalpha mutants detected in retinoic acid-resistant APL cells. Blood 2002; 100: 2586-2596.
49. Lupisella JA, Driscoll JE, Metzler WJ, Reczek PR. The ligand binding domain of the human retinoic acid receptor gamma is predominantly alpha-helical with a Trp residue in the ligand binding site. J Biol Chem 1995; 270: 24884-24890.
50. 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 2001; 20: 7257-7265.
51. Cote S, McNamara S, Brambilla D, Bianchini A, Rizzo G, del Rincon SV, Grignani F, Nervi C, Miller WH, Jr. Expression of SMRTbeta promotes ligand-induced activation of mutated and wild-type retinoid receptors. Blood 2004; 104: 4226-4235.
52. Cohen RN, Brzostek S, Kim B, Chorev M, Wondisford FE, Hollenberg AN. The specificity of interactions between nuclear hormone receptors and corepressors is mediated by distinct amino acid sequences within the interacting domains. Mol Endocrinol 2001; 15: 1049-1061.
53. Cohen RN, Putney A, Wondisford FE, Hollenberg AN. The nuclear corepressors recognize distinct nuclear receptor complexes. Mol Endocrinol 2000; 14: 900-914.
54. Heun P. SUMOrganization of the nucleus. Curr Opin Cell Biol 2007; 19: 350-355.
55. Zhou J, Peres L, Honore N, Nasr R, Zhu J, de The H. Dimerization-induced corepressor binding and relaxed DNA-binding specificity are critical for PML/RARA-induced immortalization. Proc Natl Acad Sci USA 2006; 103: 9238-9243.
56. Bourguet W, Vivat V, Wurtz JM, Chambon P, Gronemeyer H, Moras D. Crystal structure of a heterodimeric complex of RAR and RXR ligand-binding domains. Mol Cell 2000; 5: 289-298.
57. Pogenberg V, Guichou JF, Vivat-Hannah V, Kammerer S, Perez E, Germain P, de Lera AR, Gronemeyer H, Royer CA, Bourguet W. Characterization of the interaction between retinoic acid receptor/retinoid X receptor (RAR/RXR) heterodimers and transcriptional coactivators through structural and fluorescence anisotropy studies. J Biol Chem 2005; 280: 1625-1633.
58. Renaud JP, Rochel N, Ruff M, Vivat V, Chambon P, Gronemeyer H, Moras D. Crystal structure of the RAR-gamma ligand-binding domain bound to all-trans retinoic acid. Nature 1995; 378: 681-689.
59. Grignani F, De Matteis S, Nervi C, Tomassoni L, Gelmetti V, Cioce M, Fanelli M, Ruthardt M, Ferrara FF, Zamir I, Seiser C, Lazar MA, Minucci S, Pelicci PG. Fusion proteins of the retinoic acid receptor-alpha recruit histone deacetylase in promyelocytic leukaemia. Nature 1998; 391: 815-818.
60. Di Croce L, Raker VA, Corsaro M, Fazi F, Fanelli M, Faretta M, Fuks F, Lo Coco F, Kouzarides T, Nervi C, Minucci S, Pelicci PG. Methyltransferase recruitment and DNA hypermethylation of target promoters by an oncogenic transcription factor. Science 2002; 295: 1079-1082.
61. Chen SJ, Zhou GB, Zhang XW, Mao JH, de The H, Chen Z. From an old remedy to a magic bullet: molecular mechanisms underlying the therapeutic effects of arsenic in fighting leukemia. Blood 2011; 117: 6425-6437.
62. Zhu J, Nasr R, Peres L, Riaucoux-Lormiere F, Honore N, Berthier C, Kamashev D, Zhou J, Vitoux D, Lavau C, de The H. RXR is an essential component of the oncogenic PML/RARA complex in vivo. Cancer Cell 2007; 12: 23-35.
63. Figueroa ME, Lugthart S, Li Y, Erpelinck-Verschueren C, Deng X, Christos PJ, Schifano E, Booth J, van Putten W, Skrabanek L, Campagne F, Mazumdar M, Greally JM, Valk PJ, Lowenberg B, Delwel R, Melnick A. DNA methylation signatures identify biologically distinct subtypes in acute myeloid leukemia. Cancer Cell 2010; 17: 13-27.
64. Nervi C, Ferrara FF, Fanelli M, Rippo MR, Tomassini B, Ferrucci PF, Ruthardt M, Gelmetti V, Gambacorti-Passerini C, Diverio D, Grignani F, Pelicci PG, Testi R. Caspases mediate retinoic acid-induced degradation of the acute promyelocytic leukemia PML/RARalpha fusion protein. Blood 1998; 92: 2244-2251.
65. Zhu J, Gianni M, Kopf E, Honore N, Chelbi-Alix M, Koken M, Quignon F, Rochette-Egly C, de The H. Retinoic acid induces proteasome-dependent degradation of retinoic acid receptor alpha (RARalpha) and oncogenic RARalpha fusion proteins. Proc Natl Acad Sci USA 1999; 96: 14807-14812.
66. vom Baur E, Harbers M, Um SJ, Benecke A, Chambon P, Losson R. The yeast Ada complex mediates the ligand-dependent activation function AF-2 of retinoid X and estrogen receptors. Genes Dev 1998; 12: 1278-1289.
67. Lallemand-Breitenbach V, Jeanne M, Benhenda S, Nasr R, Lei M, Peres L, Zhou J, Zhu J, Raught B, de The H. Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat Cell Biol 2008; 10: 547-555.
68. Nasr R, Guillemin MC, Ferhi O, Soilihi H, Peres L, Berthier C, Rousselot P, Robledo-Sarmiento M, Lallemand-Breitenbach V, Gourmel B, Vitoux D, Pandolfi PP, Rochette-Egly C, Zhu J, de The H. Eradication of acute promyelocytic leukemia-initiating cells through PML-RARA degradation. Nat Med 2008; 14: 1333-1342.