Small-molecule inhibition of CBP/catenin interactions eliminates drug-resistant clones in acute lymphoblastic leukemia

Oncogene

Volumn 33, Issue 17, 2014, Pages 2169-2178

  Gang, E J ^a   Hsieh, Y T ^a   Pham, J ^a   Zhao, Y ^b   Nguyen, C ^b   Huantes, S ^a   Park, E ^a   Naing, K ^a   Klemm, L ^c   Swaminathan, S ^c   Conway, E M ^d   Pelus, L M ^e   Crispino, J ^f   Mullighan, C G ^g   McMillan, M ^b   Muschen M ^c   Kahn, M ^b   Kim, Y M ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e INDIANA UNIVERSITY   (United States)

^f NORTHWESTERN UNIVERSITY   (United States)

^g ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

acute lymphoblastic leukemia; CBP; drug resistance; ICG 001; p300; small molecule inhibitor

Indexed keywords

ANTILEUKEMIC AGENT; ASPARAGINASE; BETA CATENIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; DEXAMETHASONE; E1A ASSOCIATED P300 PROTEIN; ICG 001; INHIBITOR OF APOPTOSIS PROTEIN; NILOTINIB; PLAKOGLOBIN; SURVIVIN; UNCLASSIFIED DRUG; VINCRISTINE; WNT PROTEIN;

ACUTE LYMPHOBLASTIC LEUKEMIA; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PATIENT; CARBOXY TERMINAL SEQUENCE; CELL CLONE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL RENEWAL; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME ABERRATION; CONTROLLED STUDY; DOWN REGULATION; DRUG BINDING SITE; DRUG SELECTIVITY; GENE CASSETTE; GENE MUTATION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKEMIA RELAPSE; MOUSE; NOD SCID MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

MUS;

ANIMALS; ANTINEOPLASTIC AGENTS; ASPARAGINASE; BETA CATENIN; BICYCLO COMPOUNDS, HETEROCYCLIC; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DEXAMETHASONE; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MICE; MICE, INBRED NOD; MICE, SCID; MUTATION; PEPTIDE FRAGMENTS; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PYRIMIDINONES; SIALOGLYCOPROTEINS; VINCRISTINE; WNT SIGNALING PATHWAY; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84899625247     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.169     Document Type: Article

References (50)

1. Pui CH, Robison LL, Look AT. Acute lymphoblastic leukaemia. Lancet 2008; 371: 1030-1043.
2. Reya T, Duncan AW, Ailles L, Domen J, Scherer DC, Willert K et al. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 2003; 423: 409-414.
3. Luis TC, Naber BA, Roozen PP, Brugman MH, de Haas EF, Ghazvini M et al. Canonical wnt signaling regulates hematopoiesis in a dosage-dependent fashion. Cell Stem Cell 2011; 9: 345-356.
4. Chan WI, Hannah RL, Dawson MA, Pridans C, Foster D, Joshi A et al. The transcriptional coactivator Cbp regulates self-renewal and differentiation in adult hematopoietic stem cells. Mol Cell Biol 2011; 31: 5046-5060.
5. Wang Y, Krivtsov AV, Sinha AU, North TE, Goessling W, Feng Z et al. The Wnt/ beta-catenin pathway is required for the development of leukemia stem cells in AML. Science 2010; 327: 1650-1653.
6. Zhao C, Blum J, Chen A, Kwon HY, Jung SH, Cook JM et al. Loss of beta-catenin impairs the renewal of normal and CML stem cells in vivo. Cancer Cell 2007; 12: 528-541.
7. Hu Y, Chen Y, Douglas L, Li S. beta-Catenin is essential for survival of leukemic stem cells insensitive to kinase inhibition in mice with BCR-ABL-induced chronic myeloid leukemia. Leukemia 2009; 23: 109-116.
8. Jamieson CH, Ailles LE, Dylla SJ, Muijtjens M, Jones C, Zehnder JL et al. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med 2004; 351: 657-667.
9. Khan NI, Bradstock KF, Bendall LJ. Activation of Wnt/beta-catenin pathway mediates growth and survival in B-cell progenitor acute lymphoblastic leukaemia. Br J Haematol 2007; 138: 338-348.
10. Mazieres J, You L, He B, Xu Z, Lee AY, Mikami I et al. Inhibition of Wnt16 in human acute lymphoblastoid leukemia cells containing the t(1;19) translocation induces apoptosis. Oncogene 2005; 24: 5396-5400.
11. Park E, Gang EJ, Hsieh YT, Schaefer P, Chae S, Klemm L et al. Targeting survivin overcomes drug resistance in acute lymphoblastic leukemia. Blood 2011; 118: 2191-2199.
12. Altieri DC. Survivin, cancer networks and pathway-directed drug discovery. Nat Rev Cancer 2008; 8: 61-70.
13. Tyner JW, Jemal AM, Thayer M, Druker BJ, Chang BH. Targeting survivin and p53 in pediatric acute lymphoblastic leukemia. Leukemia 2012; 26: 623-632.
14. Morrison DJ, Hogan LE, Condos G, Bhatla T, Germino N, Moskowitz NP et al. Endogenous knockdown of survivin improves chemotherapeutic response in ALL models. Leukemia 2012; 26: 271-279.
15. Reya T, Clevers H. Wnt signalling in stem cells and cancer. Nature 2005; 434: 843-850.
16. Takemaru KI, Moon RT. The transcriptional coactivator CBP interacts with beta-catenin to activate gene expression. J Cell Biol 2000; 149: 249-254.
17. Hecht A, Vleminckx K, Stemmler MP, van RF, Kemler R. The p300/CBP acetyltransferases function as transcriptional coactivators of beta-catenin in vertebrates. EMBO J 2000; 19: 1839-1850.
18. Rebel VI, Kung AL, Tanner EA, Yang H, Bronson RT, Livingston DM. Distinct roles for CREB-binding protein and p300 in hematopoietic stem cell self-renewal. Proc Natl Acad Sci USA 2002; 99: 14789-14794.
19. Teo JL, Ma H, Nguyen C, Lam C, Kahn M. Specific inhibition of CBP/beta-catenin interaction rescues defects in neuronal differentiation caused by a presenilin-1 mutation. Proc Natl Acad Sci USA 2005; 102: 12171-12176.
20. Kahn M. Symmetric division versus asymmetric division: a tale of two coactivators. Future Med Chem 2011; 3: 1745-1763.
21. Ma H, Nguyen C, Lee KS, Kahn M. Differential roles for the coactivators CBP and p300 on TCF/beta-catenin-mediated survivin gene expression. Oncogene 2005; 24: 3619-3631.
22. Emami KH, Nguyen C, Ma H, Kim DH, Jeong KW, Eguchi M et al. A small molecule inhibitor of beta-catenin/CREB-binding protein transcription [corrected]. Proc Natl Acad Sci USA 2004; 101: 12682-12687.
23. Kim YM, Ma H, Oehler VG, Gang EJ, Nguyen C, Masiello D et al. The gamma catenin/CBP complex maintains survivin transcription in beta-catenin deficient/ depleted cancer cells. Curr Cancer Drug Targets 2011; 11: 213-225.
24. Muljo SA, Schlissel MS. A small molecule Abl kinase inhibitor induces differentiation of Abelson virus-transformed pre-B cell lines. Nat Immunol 2003; 4: 31-37.
25. Klein F, Feldhahn N, Mooster JL, Sprangers M, Hofmann WK, Wernet P et al. Tracing the pre-B to immature B cell transition in human leukemia cells reveals a coordinated sequence of primary and secondary IGK gene rearrangement, IGK deletion, and IGL gene rearrangement. J Immunol 2005; 174: 367-375.
26. Hardy RR, Hayakawa K. B cell development pathways. Annu Rev Immunol 2001; 19: 595-621.
27. Herzog S, Reth M, Jumaa H. Regulation of B-cell proliferation and differentiation by pre-B-cell receptor signalling. Nat Rev Immunol 2009; 9: 195-205.
28. Pear WS, Miller JP, Xu L, Pui JC, Soffer B, Quackenbush RC et al. Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood 1998; 92: 3780-3792.
29. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984; 22: 27-55.
30. Mullighan CG, Zhang J, Kasper LH, Lerach S, Payne-Turner D, Phillips LA et al. CREBBP mutations in relapsed acute lymphoblastic leukaemia. Nature 2011; 471: 235-239.
31. Zhang J, Mullighan CG, Harvey RC, Wu G, Chen X, Edmonson M et al. Key pathways are frequently mutated in high-risk childhood acute lymphoblastic leukemia: a report from the Children's Oncology Group. Blood 2011; 118: 3080-3087.
32. Logan CY, Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 2004; 20: 781-810.
33. Zheng X, Beissert T, Kukoc-Zivojnov N, Puccetti E, Altschmied J, Strolz C et al. Gamma-catenin contributes to leukemogenesis induced by AML-associated translocation products by increasing the self-renewal of very primitive progenitor cells. Blood 2004; 103: 3535-3543.
34. Gastaldi T, Bonvini P, Sartori F, Marrone A, Iolascon A, Rosolen A. Plakoglobin is differentially expressed in alveolar and embryonal rhabdomyosarcoma and is regulated by DNA methylation and histone acetylation. Carcinogenesis 2006; 27: 1758-1767.
35. Koch U, Wilson A, Cobas M, Kemler R, Macdonald HR, Radtke F. Simultaneous loss of beta- and gamma-catenin does not perturb hematopoiesis or lymphopoiesis. Blood 2008; 111: 160-164.
36. Marmorstein R. Structure and function of histone acetyltransferases. Cell Mol Life Sci 2001; 58: 693-703.
37. Yao TP, Oh SP, Fuchs M, Zhou ND, Ch'ng LE, Newsome D et al. Gene dosagedependent embryonic development and proliferation defects in mice lacking the transcriptional integrator p300. Cell 1998; 93: 361-372.
38. Tanaka Y, Naruse I, Hongo T, Xu M, Nakahata T, Maekawa T et al. Extensive brain hemorrhage and embryonic lethality in a mouse null mutant of CREB-binding protein. Mech Dev 2000; 95: 133-145.
39. Kumar SR, Scehnet JS, Ley EJ, Singh J, Krasnoperov V, Liu R et al. Preferential induction of EphB4 over EphB2 and its implication in colorectal cancer progression. Cancer Res 2009; 69: 3736-3745.
40. Kawasaki H, Taira K, Yokoyama KK. Functional analysis of the transcriptional coactivators p300 and CBP using ribozyme. Nucleic Acids Symp Ser 1999; 42: 263-264.
41. Xu W, Fukuyama T, Ney PA, Wang D, Rehg J, Boyd K et al. Global transcriptional coactivators CREB-binding protein and p300 are highly essential collectively but not individually in peripheral B cells. Blood 2006; 107: 4407-4416.
42. Ramos YF, Hestand MS, Verlaan M, Krabbendam E, Ariyurek Y, van GM et al. Genome-wide assessment of differential roles for p300 and CBP in transcription regulation. Nucleic Acids Res 2010; 38: 5396-5408.
43. Leung CG, Xu Y, Mularski B, Liu H, Gurbuxani S, Crispino JD. Requirements for survivin in terminal differentiation of erythroid cells and maintenance of hematopoietic stem and progenitor cells. J Exp Med 2007; 204: 1603-1611.
44. Takahashi-Yanaga F, Kahn M. Targeting Wnt signaling: can we safely eradicate cancer stem cells? Clin Cancer Res 2010; 16: 3153-3162.
45. Takebe N, Harris PJ, Warren RQ, Ivy SP. Targeting cancer stem cells by inhibiting Wnt, Notch, and Hedgehog pathways. Nat Rev Clin Oncol 2011; 8: 97-106.
46. Verkaar F, van der SM, Blankesteijn WM, van der Doelen AA, Zaman GJ. Discovery of novel small molecule activators of beta-catenin signaling. PLoS One 2011; 6: e19185.
47. Blough RI, Petrij F, Dauwerse JG, Milatovich-Cherry A, Weiss L, Saal HM et al. Variation in microdeletions of the cyclic AMP-responsive element-binding protein gene at chromosome band 16p13.3 in the Rubinstein-Taybi syndrome. Am J Med Genet 2000; 90: 29-34.
48. Petrij F, Giles RH, Dauwerse HG, Saris JJ, Hennekam RC, Masuno M et al. Rubinstein-Taybi syndrome caused by mutations in the transcriptional co-activator CBP. Nature 1995; 376: 348-351.
49. Pasqualucci L, Trifonov V, Fabbri G, Ma J, Rossi D, Chiarenza A et al. Analysis of the coding genome of diffuse large B-cell lymphoma. Nat Genet 2011; 43: 830-837.
50. Spencer VA, Sun JM, Li L, Davie JR. Chromatin immunoprecipitation: a tool for studying histone acetylation and transcription factor binding. Methods 2003; 31: 67-75.