Clonal selection in xenografted human T cell acute lymphoblastic leukemia recapitulates gain of malignancy at relapse

Journal of Experimental Medicine

Volumn 208, Issue 4, 2011, Pages 653-661

  Clappier, Emmanuelle ^a,b,d,e   Gerby, Bastien ^a,e,f,g   Sigaux, François ^b,c,e,h   Delord, Marc ^e,h   Touzri, Farah ^a,b,h   Hernandez, Lucie ^e,h   Ballerini, Paola ^a,i   Baruchel, André ^d   Pflumio, Françoise ^a,e,f,g   Soulier, Jean ^b,c,e,h  

^a INSTITUT DE RADIOBIOLOGIE CELLULAIRE ET MOLÉCULAIRE   (France)

^b Institut Universitaire d'Hématologie   (France)

^c SAINT LOUIS HOSPITAL   (France)

^d HÔPITAL ROBERT DEBRÉ   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

^f Universite Paris Sud   (France)

^g UNIVERSITÉ PARIS SACLAY   (France)

^h UNIVERSITÉ PARIS DIDEROT   (France)

ⁱ ARMAND TROUSSEAU HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

SHORT HAIRPIN RNA;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER RELAPSE; CELL CLONE; CELL CYCLE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN TISSUE; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR SUPPRESSOR GENE; XENOGRAFT;

ANIMALS; CELL CYCLE; GENE EXPRESSION PROFILING; HUMANS; MICE; MITOSIS; NEOPLASM TRANSPLANTATION; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PTEN PHOSPHOHYDROLASE; RECURRENCE; TRANSPLANTATION, HETEROLOGOUS;

EID: 79955711142     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20110105     Document Type: Article

References (32)

1. Aifantis, I., E. Raetz, and S. Buonamici. 2008. Molecular pathogenesis of T-cell leukaemia and lymphoma. Nat. Rev. Immunol. 8:380-390.
2. Anderson, K., C. Lutz, F.W. van Delft, C.M. Bateman, Y. Guo, S.M. Colman, H. Kempski, A.V. Moorman, I. Titley, J. Swansbury, et al. 2011. Genetic variegation of clonal architecture and propagating cells in leukaemia. Nature. 469:356-361.
3. Armstrong, F., P. Brunet de la Grange, B. Gerby, M.C. Rouyez, J. Calvo, M. Fontenay, N. Boissel, H. Dombret, A. Baruchel, J. Landman-Parker, et al. 2009. NOTCH is a key regulator of human T-cell acute leukemia initiating cell activity. Blood. 113:1730-1740.
4. Bailey, L.C., B.J. Lange, S.R. Rheingold, and N.J. Bunin. 2008. Bonemarrow relapse in paediatric acute lymphoblastic leukaemia. Lancet Oncol. 9:873-883.
5. Bhojwani, D., H. Kang, N.P. Moskowitz, D.J. Min, H. Lee, J.W. Potter, G. Davidson, C.L. Willman, M.J. Borowitz, I. Belitskaya-Levy, et al. 2006. Biologic pathways associated with relapse in childhood acute lymphoblastic leukemia: a Children's Oncology Group study. Blood. 108:711-717.
6. Boiko, A.D., O.V. Razorenova, M. van de Rijn, S.M. Swetter, D.L. Johnson, D.P. Ly, P.D. Butler, G.P. Yang, B. Joshua, M.J. Kaplan, et al. 2010. Human melanoma-initiating cells express neural crest nerve growth factor receptor CD271. Nature. 466:133-137.
7. Choi, S., M.J. Henderson, E. Kwan, A.H. Beesley, R. Sutton, A.Y. Bahar, J. Giles, N.C. Venn, L.D. Pozza, D.L. Baker, et al. 2007. Relapse in children with acute lymphoblastic leukemia involving selection of a preexisting drug-resistant subclone. Blood. 110:632-639.
8. Clappier, E., W. Cuccuini, A. Kalota, A. Crinquette, J.M. Cayuela, W.A. Dik, A.W. Langerak, B. Montpellier, B. Nadel, P. Walrafen, et al. 2007. The C-MYB locus is involved in chromosomal translocation and genomic duplications in human T-cell acute leukemia (T-ALL), the translocation defining a new T-ALL subtype in very young children. Blood. 110:1251-1261.
9. De Keersmaecker, K., P. Marynen, and J. Cools. 2005. Genetic insights in the pathogenesis of T-cell acute lymphoblastic leukemia. Haematologica. 90:1116-1127.
10. Dick, J.E. 2008. Stem cell concepts renew cancer research. Blood. 112:4793-4807.
11. Ferrando, A.A., D.S. Neuberg, J. Staunton, M.L. Loh, C. Huard, S.C. Raimondi, F.G. Behm, C.H. Pui, J.R. Downing, D.G. Gilliland, et al. 2002. Gene expression signatures define novel oncogenic pathways in T cell acute lymphoblastic leukemia. Cancer Cell. 1:75-87.
12. Freyer, D.R., M. Devidas, M. La, W.L. Carroll, P.S. Gaynon, S.P. Hunger, and N.L. Seibel. 2011. Postrelapse survival in childhood acute lymphoblastic leukemia is independent of initial treatment intensity: a report from the Children's Oncology Group. Blood. 117:3010-3015.
13. Gerby, B., F. Armstrong, P.B. de la Grange, H. Medyouf, J. Calvo, E. Verhoeyen, F.L. Cosset, I. Bernstein, S. Amselem, N. Boissel, et al. 2010. Optimized gene transfer into human primary leukemic T cell with NOD-SCID/leukemia-initiating cell activity. Leukemia. 24:646-649.
14. Gutierrez, A., T. Sanda, R. Grebliunaite, A. Carracedo, L. Salmena, Y. Ahn, S. Dahlberg, D. Neuberg, L.A. Moreau, S.S. Winter, et al. 2009. High frequency of PTEN, PI3K, and AKT abnormalities in T-cell acute lymphoblastic leukemia. Blood. 114:647-650.
15. Kirschner-Schwabe, R., C. Lottaz, J. Tödling, P. Rhein, L. Karawajew, C. Eckert, A. von Stackelberg, U. Ungethüm, D. Kostka, A.E. Kulozik, et al. 2006. Expression of late cell cycle genes and an increased proliferative capacity characterize very early relapse of childhood acute lymphoblastic leukemia. Clin. Cancer Res. 12:4553-4561.
16. Kleppe, M., I. Lahortiga, T. El Chaar, K. De Keersmaecker, N. Mentens, C. Graux, K. Van Roosbroeck, A.A. Ferrando, A.W. Langerak, J.P. Meijerink, et al. 2010. Deletion of the protein tyrosine phosphatase gene PTPN2 in T-cell acute lymphoblastic leukemia. Nat. Genet. 42:530-535.
17. Klumper, E., R. Pieters, A.J. Veerman, D.R. Huismans, A.H. Loonen, K. Hählen, G.J. Kaspers, E.R. van Wering, R. Hartmann, and G. Henze. 1995. In vitro cellular drug resistance in children with relapsed/refractory acute lymphoblastic leukemia. Blood. 86:3861-3868.
18. Mullighan, C.G., L.A. Phillips, X. Su, J. Ma, C.B. Miller, S.A. Shurtleff, and J.R. Downing. 2008. Genomic analysis of the clonal origins of relapsed acute lymphoblastic leukemia. Science. 322:1377-1380.
19. Palomero, T., W.K. Lim, D.T. Odom, M.L. Sulis, P.J. Real, A. Margolin, K.C. Barnes, J. O'Neil, D. Neuberg, A.P. Weng, et al. 2006. NOTCH1 directly regulates c-MYC and activates a feed-forward-loop transcriptional network promoting leukemic cell growth. Proc. Natl. Acad. Sci. USA. 103:18261-18266.
20. Palomero, T., M.L. Sulis, M. Cortina, P.J. Real, K. Barnes, M. Ciofani, E. Caparros, J. Buteau, K. Brown, S.L. Perkins, et al. 2007. Mutational loss of PTEN induces resistance to NOTCH1 inhibition in T-cell leukemia. Nat. Med. 13:1203-1210.
21. Pui, C.H., L.L. Robison, and A.T. Look. 2008. Acute lymphoblastic leukaemia. Lancet. 371:1030-1043.
22. Real, P.J., V. Tosello, T. Palomero, M. Castillo, E. Hernando, E. de Stanchina, M.L. Sulis, K. Barnes, C. Sawai, I. Homminga, et al. 2009. Gamma-secretase inhibitors reverse glucocorticoid resistance in T cell acute lymphoblastic leukemia. Nat. Med. 15:50-58.
23. Shackleton, M., E. Quintana, E.R. Fearon, and S.J. Morrison. 2009. Heterogeneity in cancer: cancer stem cells versus clonal evolution. Cell. 138:822-829.
24. Singh, S.K., C. Hawkins, I.D. Clarke, J.A. Squire, J. Bayani, T. Hide, R.M. Henkelman, M.D. Cusimano, and P.B. Dirks. 2004. Identification of human brain tumour initiating cells. Nature. 432:396-401.
25. Soulier, J., E. Clappier, J.M. Cayuela, A. Regnault, M. García-Peydró, H. Dombret, A. Baruchel, M.L. Toribio, and F. Sigaux. 2005. HOXA genes are included in genetic and biologic networks defining human acute T-cell leukemia (T-ALL). Blood. 106:274-286.
26. Staal, F.J., D. de Ridder, T. Szczepanski, T. Schonewille, E.C. van der Linden, E.R. van Wering, V.H. van der Velden, and J.J. van Dongen. 2010. Genome-wide expression analysis of paired diagnosis-relapse samples in ALL indicates involvement of pathways related to DNA replication, cell cycle and DNA repair, independent of immune phenotype. Leukemia. 24:491-499.
27. Tosello, V., M.R. Mansour, K. Barnes, M. Paganin, M.L. Sulis, S. Jenkinson, C.G. Allen, R.E. Gale, D.C. Linch, T. Palomero, et al. 2009. WT1 mutations in T-ALL. Blood. 114:1038-1045.
28. Van Vlierberghe, P., R. Pieters, H.B. Beverloo, and J.P. Meijerink. 2008. Molecular-genetic insights in paediatric T-cell acute lymphoblastic leukaemia. Br. J. Haematol. 143:153-168.
29. Weng, A.P., A.A. Ferrando, W. Lee, J.P. Morris IV, L.B. Silverman, C. Sanchez-Irizarry, S.C. Blacklow, A.T. Look, and J.C. Aster. 2004. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science. 306:269-271.
30. Yang, J.J., D. Bhojwani, W. Yang, X. Cai, G. Stocco, K. Crews, J. Wang, D. Morrison, M. Devidas, S.P. Hunger, et al. 2008. Genome-wide copy number profiling reveals molecular evolution from diagnosis to relapse in childhood acute lymphoblastic leukemia. Blood. 112:4178-4183.
31. Yilmaz, O.H., R. Valdez, B.K. Theisen, W. Guo, D.O. Ferguson, H. Wu, and S.J. Morrison. 2006. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature. 441:475-482.
32. Zuna, J., A.M. Ford, M. Peham, N. Patel, V. Saha, C. Eckert, J. Köchling, R. Panzer-Grümayer, J. Trka, and M. Greaves. 2004. TEL deletion analysis supports a novel view of relapse in childhood acute lymphoblastic leukemia. Clin. Cancer Res. 10:5355-5360.