CBP/catenin antagonist safely eliminates drug-resistant leukemia-initiating cells

Oncogene

Volumn 35, Issue 28, 2016, Pages 3705-3717

  Zhao, Y ^a,b   Masiello, D ^a   McMillian, M ^a,b   Nguyen, C ^a,b   Wu, Y ^a   Melendez, E ^a,b   Smbatyan, G ^a,b   Kida, A ^a   He, Y ^a   Teo, J L ^a,b   Kahn, M ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATENIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; N BENZYL 1,2,3,4,8,9 HEXAHYDRO 6 (4 HYDROXYBENZYL) 8 (1 NAPHTHYLMETHYL) 4,7 DIOXO 2H PYRAZINO[1,2 A]PYRIMIDINE 1(6H) CARBOXAMIDE; NILOTINIB; BCR ABL PROTEIN; CREBBP PROTEIN, HUMAN; E1A ASSOCIATED P300 PROTEIN; EP300 PROTEIN, HUMAN; FUSED HETEROCYCLIC RINGS; IL2RG PROTEIN, MOUSE; INTERLEUKIN 2 RECEPTOR GAMMA; PROTEIN BINDING; PYRIMIDINONE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CELL DIFFERENTIATION; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; DRUG ANTAGONISM; FEMALE; HUMAN; HUMAN CELL; LEUKEMIA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; TUMOR ENGRAFTMENT; ANIMAL; ANTAGONISTS AND INHIBITORS; CANCER STEM CELL; DEFICIENCY; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENETICS; IMMUNOBLOTTING; K-562 CELL LINE; KNOCKOUT MOUSE; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; METABOLISM; NONOBESE DIABETIC MOUSE; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCID MOUSE; TUMOR CELL LINE;

ANIMALS; BRIDGED BICYCLO COMPOUNDS, HETEROCYCLIC; CATENINS; CELL LINE, TUMOR; CREB-BINDING PROTEIN; DRUG RESISTANCE, NEOPLASM; E1A-ASSOCIATED P300 PROTEIN; FEMALE; FUSION PROTEINS, BCR-ABL; HUMANS; IMMUNOBLOTTING; INTERLEUKIN RECEPTOR COMMON GAMMA SUBUNIT; K562 CELLS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; NEOPLASTIC STEM CELLS; PROTEIN BINDING; PYRIMIDINONES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84949844600     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.438     Document Type: Article

References (50)

1. Giles FJ, DeAngelo DJ, Baccarani M, Deininger M, Guilhot F, Hughes T et al. Optimizing outcomes for patients with advanced disease in chronic myelogenous leukemia. Semin Oncol 2008; 35: S1-S17.
2. Jabbour EJ, Cortes JE, Kantarjian HM. Resistance to tyrosine kinase inhibition therapy for chronic myelogenous leukemia: a clinical perspective and emerging treatment options. Clin Lymphoma Myeloma Leuk 2013; 13: 515-529.
3. Rice KN, Jamieson CH. Molecular pathways to CML stem cells. Int J Hematol 2010; 91: 748-752.
4. Jamieson CH, Ailles LE, Dylla SJ, Muijtjens M, Jones C, Zehnder JL et al. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blastcrisis CML. N Engl J Med 2004; 351: 657-667.
5. Fodde R, Brabletz T. Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol 2007; 19: 150-158.
6. Bolton-Gillespie E, Schemionek M, Klein HU, Flis S, Hoser G, Lange T et al. Genomic instability may originate from imatinib-refractory chronic myeloid leukemia stem cells. Blood 2013; 121: 4175-4183.
7. Heidel FH, Bullinger L, Feng Z, Wang Z, Neff TA, Stein L et al. Genetic and pharmacologic inhibition of β-catenin targets imatinib-resistant leukemia stem cells in CML. Cell Stem Cell 2012; 10: 412-424.
8. 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.
9. Radich JP, Dai H, Mao M, Oehler V, Schelter J, Druker B et al. Gene expression changes associated with progression and response in chronic myeloid leukemia. Proc Natl Acad Sci USA 2006; 103: 2794-2799.
10. 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.
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. Pehlivan M, Sercan Z, Sercan HO. sFRP1 promoter methylation is associated with persistent Philadelphia chromosome in chronic myeloid leukemia. Leuk Res 2009; 33: 1062-1067.
13. Yeung J, Esposito MT, Gandillet A, Zeisig BB, Griessinger E, Bonnet D et al. β-Catenin mediates the establishment and drug resistance of MLL leukemic stem cells. Cancer Cell 2010; 18: 606-618.
14. Reya T, Clevers H. Wnt signalling in stem cells and cancer. Nature 2005; 434: 843-850.
15. Takemaru KI, Moon RT. The transcriptional coactivator CBP interacts with betacatenin to activate gene expression. J Cell Biol 2000; 149: 249-254.
16. Hecht A, Vleminckx K, Stemmler MP, van Roy F, Kemler R. The p300/CBP acetyltransferases function as transcriptional coactivators of beta-catenin in vertebrates. EMBO J 2000; 19: 1839-1850.
17. 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.
18. Marson A, Foreman R, Chevalier B, Bilodeau S, Kahn M, Young RA et al. Wnt signaling promotes reprogramming of somatic cells to pluripotency. Cell Stem Cell 2008; 3: 132-135.
19. Wend P, Fang L, Zhu Q, Schipper JH, Loddenkemper C, Kosel F et al. Wnt/β-catenin signalling induces MLL to create epigenetic changes in salivary gland tumours. EMBO J 2013; 32: 1977-1989.
20. Gang EJ, Hsieh YT, Pham J, Zhao Y, Nguyen C, Huantes S et al. Small-molecule inhibition of CBP/catenin interactions eliminates drug-resistant clones in acute lymphoblastic leukemia. Oncogene 2014; 33: 2169-2178.
21. Ramos YF, Hestand MS, Verlaan M, Krabbendam E, Ariyurek Y, van Galen M et al. Genome-wide assessment of differential roles for p300 and CBP in transcription regulation. Nucleic Acids Res 2010; 38: 5396-5408.
22. 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.
23. Kawasaki H, Eckner R, Yao TP, Taira K, Chiu R, Livingston DM et al. Distinct roles of the co-activators p300 and CBP in retinoic-acid-induced F9-cell differentiation. Nature 1998; 393: 284-289.
24. 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.
25. Erratum in: Proc Natl Acad Sci USA 2004; 101: 16707.
26. 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.
27. Velculescu VE, Madden SL, Zhang L, Lash AE, Yu J, Rago C et al. Analysis of human transcriptomes. Nat Genet 1999; 23: 387-388.
28. 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: 12171-1276.
29. Kahn M. Symmetric division versus asymmetric division: a tale of two coactivators. Future Med Chem 2011; 3: 1745-1763.
30. Hao S, He W, Li Y, Ding H, Hou Y, Nie J et al. Targeted inhibition of β-catenin/CBP signaling ameliorates renal interstitial fibrosis. J Am Soc Nephrol 2011; 22: 1642-16453.
31. Zemans RL, Briones N, Campbell M, McClendon J, Young SK, Suzuki T et al. Neutrophil transmigration triggers repair of the lung epithelium via beta-catenin signaling. Proc Natl Acad Sci USA 2011; 108: 15990-15995.
32. Hasegawa K, Yasuda SY, Teo JL, Nguyen C, McMillan M, Hsieh CL et al. Wnt signaling orchestration with a small molecule DYRK inhibitor provides long-term xeno-free human pluripotent cell expansion. Stem Cells Transl Med 2012; 1: 18-28.
33. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105-111.
34. Notta F, Mullighan CG, Wang JC, Poeppl A, Doulatov S, Phillips LA et al. Evolution of human BCR-ABL1 lymphoblastic leukaemia-initiating cells. Nature 2011; 469: 362-367.
35. Hirschmann-Jax C, Foster AE, Wulf GG, Nuchtern JG, Jax TW, Gobel U et al. A distinct "side-population" of cells with high efflux capacity in human tumor cells. Proc Natl Acad Sci USA 2004; 101: 14228-14233.
36. Haraguchi N, Utsunomiya T, Inoue H, Tanaka F, Mimori K, Barnard GF et al. Characterization of a side population of cancer cells from human gastrointestinal system. Stem Cells 2006; 24: 506-513.
37. Yamada T, Mori Y, Hayashi R, Takada M, Ino Y, Naishiro Y et al. Suppression of intestinal polyposis in Mdr1-deficient ApcMin/+ mice. Cancer Res 2003; 63: 895-901.
38. He K, Xu T, Xu Y, Ring A, Kahn M, Goldkorn A. Cancer cells acquire a drug resistant, highly tumorigenic, cancer stem-like phenotype through modulation of the PI3K/Akt/β-catenin/CBP pathway. Int J Cancer 2014; 134: 43-54.
39. Konig H, Holtz M, Modi H, Manley P, Holyoake TL, Forman SJ et al. Enhanced BCRABL kinase inhibition does not result in increased inhibition of downstream signaling pathways or increased growth suppression in CML progenitors. Leukemia 2008; 22: 748-755.
40. Kim YM, Ma H, Oehler VG, Gang EJ, Nguyen C, Masiello D et al. The gamma catenin/CBP complex maintains survivin transcription in β-catenin deficient/depleted cancer cells. Curr Can Drug Targets 2011; 11: 213-225.
41. Nicholson E, Holyoake T. The chronic myeloid leukemia stem cell. Clin Lymphoma Myeloma 2009; 9: S376-S381.
42. Banerjee ER, Laflamme MA, Papayannopoulou T, Kahn M, Murry CE, Henderson WR Jr. Human embryonic stem cells differentiated to lung lineage-specific cells ameliorate pulmonary fibrosis in a xenograft transplant mouse model. PLoS One 2012; 7: e33165.
43. Mita AC, Mita MM, Nawrocki ST, Giles FJ. Survivin: key regulator of mitosis and apoptosis and novel target for cancer therapeutics. Clin Cancer Res 2008; 14: 5000-5005.
44. Sharma SV, Lee DY, Li B, Quinlan MP, Takahashi F, Maheswaran S et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 2010; 141: 69-80.
45. Xia B, Heimbach T, He H, Lin TH. Nilotinib preclinical pharmacokinetics and practical application toward clinical projections of oral absorption and systemic availability. Biopharm Drug Dispos 2012; 33: 536-549.
46. Miyabayashi T, Teo JL, Yamamoto M, McMillan M, Nguyen C, Kahn M. Wnt/betacatenin/CBP signaling maintains long-term murine embryonic stem cell pluripotency. Proc Natl Acad Sci USA 2007; 104: 5668-5673.
47. Kahn M. Can we safely target the WNT pathway? Nat Rev Drug Discov 2014; 13: 513-532.
48. Lenz HJ, Kahn M. Safely targeting cancer stem cells via selective catenin coactivator antagonism. Cancer Sci 2014; 105: 1087-1092.
49. el-Khoueiry A, Ning Y, Yang D, Cole S, Kahn M, Marwan Z et al. A phase I first inhuman study of PRI-724 in patients (pts) with advanced solid tumors. J Clin Oncol 2013; 31(Suppl): 2501 (abstract 2501).
50. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 1996; 183: 1797-1806.