Telomerase inhibition effectively targets mouse and human AML stem cells and delays relapse following chemotherapy

Cell Stem Cell

Volumn 15, Issue 6, 2014, Pages 775-790

  Bruedigam, Claudia ^a   Bagger, Frederik O ^b   Heidel, Florian H ^c   Paine Kuhn, Catherine ^a   Guignes, Solene ^a   Song, Axia ^a   Austin, Rebecca ^a   Vu, Therese ^a   Lee, Erwin ^d   Riyat, Sarbjit ^e   Moore, Andrew S ^f,g   Lock, Richard B ^d   Bullinger, Lars ^h   Hill, Geoffrey R ^a,e,g   Armstrong, Scott A ⁱ   Williams, David A ^j   Lane, Steven W ^a,e,g  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY HOSPITAL MAGDEBURG   (Germany)

^d UNIVERSITY OF NEW SOUTH WALES   (Australia)

^e ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

^f Queensland Children s Medical Research Institute   (Australia)

^g UNIVERSITY OF QUEENSLAND   (Australia)

^h UNIVERSITY HOSPITAL ULM   (Germany)

ⁱ MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^j HARVARD MEDICAL SCHOOL   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; IMETELSTAT; PROTEIN P107; PROTEIN P16; PROTEIN P19; PROTEIN P53; SHORT HAIRPIN RNA; TELOMERASE; INDOLE DERIVATIVE; NICOTINAMIDE; SMALL INTERFERING RNA;

ACUTE MYELOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CHEMOTHERAPY; CANCER STEM CELL; CANCER SURVIVAL; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL FUNCTION; CELL HOMING; CELL PROLIFERATION; CELL RENEWAL; CELL STRUCTURE; CHROMOSOMAL INSTABILITY; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOGENETICS; DNA DAMAGE; DNA REPLICATION; ENZYME INHIBITION; FLOW CYTOMETRY; G1 PHASE CELL CYCLE CHECKPOINT; GENE DELETION; GENE EXPRESSION; GENE SILENCING; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; KARYOTYPE; LEUKEMIA RELAPSE; LEUKEMIA STEM CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; S PHASE CELL CYCLE CHECKPOINT; SPLEEN WEIGHT; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL CYCLE CHECKPOINT; DISEASE MODEL; DRUG EFFECTS; DRUG SCREENING; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; LEUKEMIA, MYELOID, ACUTE; METABOLISM; PATHOLOGY; PHYSIOLOGY; RECURRENT DISEASE; TRANSPLANTATION;

MURINAE;

ANIMALS; APOPTOSIS; CELL CYCLE CHECKPOINTS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKOUT TECHNIQUES; HUMANS; INDOLES; LEUKEMIA, MYELOID, ACUTE; MICE; MICE, INBRED C57BL; NEOPLASTIC STEM CELLS; NIACINAMIDE; RECURRENCE; RNA, SMALL INTERFERING; TELOMERASE; TUMOR SUPPRESSOR PROTEIN P53; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84919423400     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2014.11.010     Document Type: Article

References (47)

1. A.M. Aalbers, R.T. Calado, N.S. Young, C.M. Zwaan, C. Wu, S. Kajigaya, E.A. Coenen, A. Baruchel, K. Geleijns, and V. de Haas Telomere length and telomerase complex mutations in pediatric acute myeloid leukemia Leukemia 27 2013 1786 1789
2. R.C. Allsopp, G.B. Morin, R. DePinho, C.B. Harley, and I.L. Weissman Telomerase is required to slow telomere shortening and extend replicative lifespan of HSCs during serial transplantation Blood 102 2003 517 520
3. F.O. Bagger, N. Rapin, K. Theilgaard-Mönch, B. Kaczkowski, J. Jendholm, O. Winther, and B. Porse HemaExplorer: a Web server for easy and fast visualization of gene expression in normal and malignant hematopoiesis Blood 119 2012 6394 6395
4. N.L. Barbosa-Morais, M.J. Dunning, S.A. Samarajiwa, J.F. Darot, M.E. Ritchie, A.G. Lynch, and S. Tavaré A re-annotation pipeline for Illumina BeadArrays: improving the interpretation of gene expression data Nucleic Acids Res. 38 2010 e17
5. L. Bernard, C. Belisle, L. Mollica, S. Provost, D.C. Roy, D.G. Gilliland, R.L. Levine, and L. Busque Telomere length is severely and similarly reduced in JAK2V617F-positive and -negative myeloproliferative neoplasms Leukemia 23 2009 287 291
6. K.M. Bernt, N. Zhu, A.U. Sinha, S. Vempati, J. Faber, A.V. Krivtsov, Z. Feng, N. Punt, A. Daigle, and L. Bullinger MLL-rearranged leukemia is dependent on aberrant H3K79 methylation by DOT1L Cancer Cell 20 2011 66 78
7. M.A. Blasco, H.W. Lee, M.P. Hande, E. Samper, P.M. Lansdorp, R.A. DePinho, and C.W. Greider Telomere shortening and tumor formation by mouse cells lacking telomerase RNA Cell 91 1997 25 34
8. D. Bonnet, and J.E. Dick Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell Nat. Med. 3 1997 730 737
9. R.T. Calado, J.A. Regal, M. Hills, W.T. Yewdell, L.F. Dalmazzo, M.A. Zago, P.M. Lansdorp, D. Hogge, S.J. Chanock, and E.H. Estey Constitutional hypomorphic telomerase mutations in patients with acute myeloid leukemia Proc. Natl. Acad. Sci. USA 106 2009 1187 1192
10. Cancer Genome Atlas Research Network Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia N. Engl. J. Med. 368 2013 2059 2074
11. G.B. Celli, and T. de Lange DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion Nat. Cell Biol. 7 2005 712 718
12. F.S. Chou, M. Wunderlich, A. Griesinger, and J.C. Mulloy N-Ras(G12D) induces features of stepwise transformation in preleukemic human umbilical cord blood cultures expressing the AML1-ETO fusion gene Blood 117 2011 2237 2240
13. A.R. Choudhury, Z. Ju, M.W. Djojosubroto, A. Schienke, A. Lechel, S. Schaetzlein, H. Jiang, A. Stepczynska, C. Wang, and J. Buer Cdkn1a deletion improves stem cell function and lifespan of mice with dysfunctional telomeres without accelerating cancer formation Nat. Genet. 39 2007 99 105
14. A.B. Dash, I.R. Williams, J.L. Kutok, M.H. Tomasson, E. Anastasiadou, K. Lindahl, S. Li, R.A. Van Etten, J. Borrow, and D. Housman A murine model of CML blast crisis induced by cooperation between BCR/ABL and NUP98/HOXA9 Proc. Natl. Acad. Sci. USA 99 2002 7622 7627
15. M.A. Dawson, R.K. Prinjha, A. Dittmann, G. Giotopoulos, M. Bantscheff, W.I. Chan, S.C. Robson, C.W. Chung, C. Hopf, and M.M. Savitski Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia Nature 478 2011 529 533
16. R.A. Dickins, M.T. Hemann, J.T. Zilfou, D.R. Simpson, I. Ibarra, G.J. Hannon, and S.W. Lowe Probing tumor phenotypes using stable and regulated synthetic microRNA precursors Nat. Genet. 37 2005 1289 1295
17. M.W. Drummond, S.F. Hoare, A. Monaghan, S.M. Graham, M.J. Alcorn, W.N. Keith, and T.L. Holyoake Dysregulated expression of the major telomerase components in leukaemic stem cells Leukemia 19 2005 381 389
18. P. Du, W.A. Kibbe, and S.M. Lin lumi: a pipeline for processing Illumina microarray Bioinformatics 24 2008 1547 1548
19. A.J. Gentles, S.K. Plevritis, R. Majeti, and A.A. Alizadeh Association of a leukemic stem cell gene expression signature with clinical outcomes in acute myeloid leukemia JAMA 304 2010 2706 2715
20. A. Gessner, M. Thomas, P.G. Castro, L. Büchler, A. Scholz, T.H. Brümmendorf, N.M. Soria, J. Vormoor, J. Greil, and O. Heidenreich Leukemic fusion genes MLL/AF4 and AML1/MTG8 support leukemic self-renewal by controlling expression of the telomerase subunit TERT Leukemia 24 2010 1751 1759
21. J.A. Hartigan, and M.A. Wong Algorithm AS 136: A K-Means Clustering Algorithm J. R. Stat. Soc. Ser. C Appl. Stat. 28 1979 100 108
22. F.H. Heidel, L. Bullinger, Z. Feng, Z. Wang, T.A. Neff, L. Stein, D. Kalaitzidis, S.W. Lane, and S.A. Armstrong Genetic and pharmacologic inhibition of β-catenin targets imatinib-resistant leukemia stem cells in CML Cell Stem Cell 10 2012 412 424
23. B.S. Herbert, G.C. Gellert, A. Hochreiter, K. Pongracz, W.E. Wright, D. Zielinska, A.C. Chin, C.B. Harley, J.W. Shay, and S.M. Gryaznov Lipid modification of GRN163, an N3′ - >P5′ thio-phosphoramidate oligonucleotide, enhances the potency of telomerase inhibition Oncogene 24 2005 5262 5268
24. K.J. Hope, L. Jin, and J.E. Dick Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity Nat. Immunol. 5 2004 738 743
25. J. Hu, S.S. Hwang, M. Liesa, B. Gan, E. Sahin, M. Jaskelioff, Z. Ding, H. Ying, A.T. Boutin, and H. Zhang Antitelomerase therapy provokes ALT and mitochondrial adaptive mechanisms in cancer Cell 148 2012 651 663
26. F. Ishikawa, S. Yoshida, Y. Saito, A. Hijikata, H. Kitamura, S. Tanaka, R. Nakamura, T. Tanaka, H. Tomiyama, and N. Saito Chemotherapy-resistant human AML stem cells home to and engraft within the bone-marrow endosteal region Nat. Biotechnol. 25 2007 1315 1321
27. H. Ishwaran, and U.B. Kogalur Consistency of Random Survival Forests Stat. Probab. Lett. 80 2010 1056 1064
28. M. Kirwan, and I. Dokal Dyskeratosis congenita: a genetic disorder of many faces Clin. Genet. 73 2008 103 112
29. A.V. Krivtsov, D. Twomey, Z. Feng, M.C. Stubbs, Y. Wang, J. Faber, J.E. Levine, J. Wang, W.C. Hahn, and D.G. Gilliland Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9 Nature 442 2006 818 822
30. A.V. Krivtsov, Z. Feng, and S.A. Armstrong Transformation from committed progenitor to leukemia stem cells Ann. N Y Acad. Sci. 1176 2009 144 149
31. S.W. Lane, and D.G. Gilliland Leukemia stem cells Semin. Cancer Biol. 20 2010 71 76
32. S.W. Lane, Y.J. Wang, C. Lo Celso, C. Ragu, L. Bullinger, S.M. Sykes, F. Ferraro, S. Shterental, C.P. Lin, and D.G. Gilliland Differential niche and Wnt requirements during acute myeloid leukemia progression Blood 118 2011 2849 2856
33. K.H. Metzeler, K. Maharry, M.D. Radmacher, K. Mrózek, D. Margeson, H. Becker, J. Curfman, K.B. Holland, S. Schwind, and S.P. Whitman TET2 mutations improve the new European LeukemiaNet risk classification of acute myeloid leukemia: a Cancer and Leukemia Group B study J. Clin. Oncol. 29 2011 1373 1381
34. K. Okamoto, C. Bartocci, I. Ouzounov, J.K. Diedrich, J.R. Yates 3rd, and E.L. Denchi A two-step mechanism for TRF2-mediated chromosome-end protection Nature 494 2013 502 505
35. M.E. Ritchie, M.J. Dunning, M.L. Smith, W. Shi, and A.G. Lynch BeadArray expression analysis using bioconductor PLoS Comput. Biol. 7 2011 e1002276
36. F.G. Rücker, R.F. Schlenk, L. Bullinger, S. Kayser, V. Teleanu, H. Kett, M. Habdank, C.M. Kugler, K. Holzmann, and V.I. Gaidzik TP53 alterations in acute myeloid leukemia with complex karyotype correlate with specific copy number alterations, monosomal karyotype, and dismal outcome Blood 119 2012 2114 2121
37. C. Scholl, D. Bansal, K. Döhner, K. Eiwen, B.J. Huntly, B.H. Lee, F.G. Rücker, R.F. Schlenk, L. Bullinger, and H. Döhner The homeobox gene CDX2 is aberrantly expressed in most cases of acute myeloid leukemia and promotes leukemogenesis J. Clin. Invest. 117 2007 1037 1048
38. S.M. Sykes, S.W. Lane, L. Bullinger, D. Kalaitzidis, R. Yusuf, B. Saez, F. Ferraro, F. Mercier, H. Singh, and K.M. Brumme AKT/FOXO signaling enforces reversible differentiation blockade in myeloid leukemias Cell 146 2011 697 708
39. J. Szer The prevalent predicament of relapsed acute myeloid leukemia Hematology (Am Soc Hematol Educ Program) 2012 2012 43 48
40. A. Viale, F. De Franco, A. Orleth, V. Cambiaghi, V. Giuliani, D. Bossi, C. Ronchini, S. Ronzoni, I. Muradore, and S. Monestiroli Cell-cycle restriction limits DNA damage and maintains self-renewal of leukaemia stem cells Nature 457 2009 51 56
41. C. Vicente-Dueñas, M. Barajas-Diego, I. Romero-Camarero, I. González-Herrero, T. Flores, and I. Sánchez-García Essential role for telomerase in chronic myeloid leukemia induced by BCR-ABL in mice Oncotarget 3 2012 261 266
42. Y. Wang, A.V. Krivtsov, A.U. Sinha, T.E. North, W. Goessling, Z. Feng, L.I. Zon, and S.A. Armstrong The Wnt/beta-catenin pathway is required for the development of leukemia stem cells in AML Science 327 2010 1650 1653
43. J. Wang, Q. Sun, Y. Morita, H. Jiang, A. Gross, A. Lechel, K. Hildner, L.M. Guachalla, A. Gompf, and D. Hartmann A differentiation checkpoint limits hematopoietic stem cell self-renewal in response to DNA damage Cell 148 2012 1001 1014
44. M. Wunderlich, F.S. Chou, K.A. Link, B. Mizukawa, R.L. Perry, M. Carroll, and J.C. Mulloy AML xenograft efficiency is significantly improved in NOD/SCID-IL2RG mice constitutively expressing human SCF, GM-CSF and IL-3 Leukemia 24 2010 1785 1788
45. S. Zhao, Y. Zhang, K. Sha, Q. Tang, X. Yang, C. Yu, Z. Liu, W. Sun, L. Cai, C. Xu, and S. Cui KRAS (G12D) Cooperates with AML1/ETO to Initiate a Mouse Model Mimicking Human Acute Myeloid Leukemia Cell. Physiol. Biochem. 33 2014 78 87
46. J. Zuber, I. Radtke, T.S. Pardee, Z. Zhao, A.R. Rappaport, W. Luo, M.E. McCurrach, M.M. Yang, M.E. Dolan, and S.C. Kogan Mouse models of human AML accurately predict chemotherapy response Genes Dev. 23 2009 877 889
47. J. Zuber, J. Shi, E. Wang, A.R. Rappaport, H. Herrmann, E.A. Sison, D. Magoon, J. Qi, K. Blatt, and M. Wunderlich RNAi screen identifies Brd4 as a therapeutic target in acute myeloid leukaemia Nature 478 2011 524 528