Clonal evolution enhances leukemia-propagating cell frequency in T cell acute lymphoblastic leukemia through Akt/mTORC1 pathway activation

Cancer Cell

Volumn 25, Issue 3, 2014, Pages 366-378

  Blackburn, Jessica S ^a,b   Liu, Sali ^c   Wilder, Jayme L ^b   Dobrinski, Kimberly P ^d   Lobbardi, Riadh ^a,b   Moore, Finola E ^a,b   Martinez, Sarah A ^a   Chen, Eleanorc A ^a,b,e   Lee, Charles ^f,g   Langenau, David M ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD STEM CELL INSTITUTE   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d UNIVERSITY OF SOUTH FLORIDA   (United States)

^e UNIVERSITY OF WASHINGTON MEDICAL CENTER   (United States)

^f JACKSON LABORATORY   (United States)

^g Seoul National University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

DEXAMETHASONE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MYC PROTEIN; PROTEIN KINASE B;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CLONE; CLONAL EVOLUTION; CONTROLLED STUDY; DISEASE COURSE; ENZYME ACTIVATION; GROWTH RATE; HUMAN; HUMAN CELL; LEUKEMIA CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN STABILITY; SIGNAL TRANSDUCTION; T CELL LEUKEMIA; ZEBRA FISH; APOPTOSIS; CANCER GROWTH; CANCER PROGNOSIS; CELL GROWTH; CELL TRANSPLANTATION; CHRONIC LYMPHATIC LEUKEMIA; COMPARATIVE GENOMIC HYBRIDIZATION; EX VIVO STUDY; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC HETEROGENEITY; GENOTYPE; GRAFT RECIPIENT; IMMUNOHISTOCHEMISTRY; LATENT PERIOD; LEUKEMIA PROPAGATING CELL; PARACRINE SIGNALING; POINT MUTATION; PROTEIN EXPRESSION; TRANSGENIC ORGANISM; TRANSGENIC ZEBRAFISH; WESTERN BLOTTING;

DANIO RERIO;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTINEOPLASTIC AGENTS, HORMONAL; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CLONAL EVOLUTION; DEXAMETHASONE; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; GENETIC VARIATION; HETEROCYCLIC COMPOUNDS, 3-RING; HUMANS; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-MYC; T-LYMPHOCYTES; TOR SERINE-THREONINE KINASES; ZEBRAFISH;

EID: 84896070368     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2014.01.032     Document Type: Article

References (42)

1. Almendro V., Marusyk A., Polyak K. Cellular heterogeneity and molecular evolution in cancer. Annu. Rev. Pathol. 2013, 8:277-302.
2. Anderson K., Lutz C., van Delft F.W., Bateman C.M., Guo Y., Colman S.M., Kempski H., Moorman A.V., Titley I., Swansbury J., et al. Genetic variegation of clonal architecture and propagating cells in leukaemia. Nature 2011, 469:356-361.
3. Aparicio S., Caldas C. The implications of clonal genome evolution for cancer medicine. N.Engl. J. Med. 2013, 368:842-851.
4. Beesley A.H., Firth M.J., Ford J., Weller R.E., Freitas J.R., Perera K.U., Kees U.R. Glucocorticoid resistance in T-lineage acute lymphoblastic leukaemia is associated with a proliferative metabolism. Br. J. Cancer 2009, 100:1926-1936.
5. Blackburn J.S., Liu S., Langenau D.M. Quantifying the frequency of tumor-propagating cells using limiting dilution cell transplantation in syngeneic zebrafish. J.Vis. Exp. 2011, July 14:e2790.
6. Blackburn J.S., Liu S., Raiser D.M., Martinez S.A., Feng H., Meeker N.D., Gentry J., Neuberg D., Look A.T., Ramaswamy S., et al. Notch signaling expands a pre-malignant pool of T-cell acute lymphoblastic leukemia clones without affecting leukemia-propagating cell frequency. Leukemia 2012, 26:2069-2078.
7. Bonnet M., Loosveld M., Montpellier B., Navarro J.-M., Quilichini B., Picard C., Di Cristofaro J., Bagnis C., Fossat C., Hernandez L., et al. Posttranscriptional deregulation of MYC via PTEN constitutes a major alternative pathway of MYC activation in T-cell acute lymphoblastic leukemia. Blood 2011, 117:6650-6659.
8. Chan S.M., Weng A.P., Tibshirani R., Aster J.C., Utz P.J. Notch signals positively regulate activity of the mTOR pathway in T-cell acute lymphoblastic leukemia. Blood 2007, 110:278-286.
9. Chiarini F., Grimaldi C., Ricci F., Tazzari P.L., Evangelisti C., Ognibene A., Battistelli M., Falcieri E., Melchionda F., Pession A., et al. Activity of the novel dual phosphatidylinositol 3-kinase/mammalian target of rapamycin inhibitor NVP-BEZ235 against T-cell acute lymphoblastic leukemia. Cancer Res. 2010, 70:8097-8107.
10. Clappier E., Gerby B., Sigaux F., Delord M., Touzri F., Hernandez L., Ballerini P., Baruchel A., Pflumio F., Soulier J. Clonal selection in xenografted human Tcell acute lymphoblastic leukemia recapitulates gain of malignancy at relapse. J.Exp. Med. 2011, 208:653-661.
11. Clarke M.F., Dick J.E., Dirks P.B., Eaves C.J., Jamieson C.H.M., Jones D.L., Visvader J., Weissman I.L., Wahl G.M. Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 2006, 66:9339-9344.
12. Ding L., Ley T.J., Larson D.E., Miller C.A., Koboldt D.C., Welch J.S., Ritchey J.K., Young M.A., Lamprecht T., McLellan M.D., et al. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 2012, 481:506-510.
13. Einsiedel H.G., von Stackelberg A., Hartmann R., Fengler R., Schrappe M., Janka-Schaub G., Mann G., Hählen K., Göbel U., Klingebiel T., et al. Long-term outcome in children with relapsed ALL by risk-stratified salvage therapy: results of trial acute lymphoblastic leukemia-relapse study of the Berlin-Frankfurt-Münster Group 87. J.Clin. Oncol. 2005, 23:7942-7950.
14. Gerlinger M., Swanton C. How Darwinian models inform therapeutic failure initiated by clonal heterogeneity in cancer medicine. Br. J. Cancer 2010, 103:1139-1143.
15. Gerlinger M., Rowan A.J., Horswell S., Larkin J., Endesfelder D., Gronroos E., Martinez P., Matthews N., Stewart A., Tarpey P., et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N.Engl. J. Med. 2012, 366:883-892.
16. Gutierrez A., Sanda T., Grebliunaite R., Carracedo A., Salmena L., Ahn Y., Dahlberg S., Neuberg D., Moreau L.A., Winter S.S., et al. High frequency of PTEN, PI3K, and AKT abnormalities in T-cell acute lymphoblastic leukemia. Blood 2009, 114:647-650.
17. Gutierrez A., Grebliunaite R., Feng H., Kozakewich E., Zhu S., Guo F., Payne E., Mansour M., Dahlberg S.E., Neuberg D.S., et al. Pten mediates Myc oncogene dependence in a conditional zebrafish model of Tcell acute lymphoblastic leukemia. J.Exp. Med. 2011, 208:1595-1603.
18. Hu Y., Smyth G.K. ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J.Immunol. Methods 2009, 347:70-78.
19. Jiang H., Vogt P.K. Constitutively active Rheb induces oncogenic transformation. Oncogene 2008, 27:5729-5740.
20. Kalaitzidis D., Sykes S.M., Wang Z., Punt N., Tang Y., Ragu C., Sinha A.U., Lane S.W., Souza A.L., Clish C.B., et al. mTOR complex 1 plays critical roles in hematopoiesis and Pten-loss-evoked leukemogenesis. Cell Stem Cell 2012, 11:429-439.
21. Kawamura M., Ohnishi H., Guo S.X., Sheng X.M., Minegishi M., Hanada R., Horibe K., Hongo T., Kaneko Y., Bessho F., et al. Alterations of the p53, p21, p16, p15 and RAS genes in childhood T-cell acute lymphoblastic leukemia. Leuk. Res. 1999, 23:115-126.
22. King B., Trimarchi T., Reavie L., Xu L., Mullenders J., Ntziachristos P., Aranda-Orgilles B., Perez-Garcia A., Shi J., Vakoc C., et al. The ubiquitin ligase FBXW7 modulates leukemia-initiating cell activity by regulating MYC stability. Cell 2013, 153:1552-1566.
23. Kong G., Du J., Liu Y., Meline B., Chang Y.-I., Ranheim E.A., Wang J., Zhang J. Notch1 gene mutations target KRAS G12D-expressing CD8+ cells and contribute to their leukemogenic transformation. J.Biol. Chem. 2013, 288:37368.
24. Landau D.A., Carter S.L., Stojanov P., McKenna A., Stevenson K., Lawrence M.S., Sougnez C., Stewart C., Sivachenko A., Wang L., et al. Evolution and impact of subclonal mutations in chronic lymphocytic leukemia. Cell 2013, 152:714-726.
25. Langenau D.M., Traver D., Ferrando A.A., Kutok J.L., Aster J.C., Kanki J.P., Lin S., Prochownik E., Trede N.S., Zon L.I., Look A.T. Myc-induced Tcell leukemia in transgenic zebrafish. Science 2003, 299:887-890.
26. Langenau D.M., Feng H., Berghmans S., Kanki J.P., Kutok J.L., Look A.T. Cre/lox-regulated transgenic zebrafish model with conditional myc-induced Tcell acute lymphoblastic leukemia. Proc. Natl. Acad. Sci. USA 2005, 102:6068-6073.
27. McCormack M.P., Young L.F., Vasudevan S., de Graaf C.A., Codrington R., Rabbitts T.H., Jane S.M., Curtis D.J. The Lmo2 oncogene initiates leukemia in mice by inducing thymocyte self-renewal. Science 2010, 327:879-883.
28. Mullighan C.G., Phillips L.A., Su X., Ma J., Miller C.B., Shurtleff S.A., Downing J.R. Genomic analysis of the clonal origins of relapsed acute lymphoblastic leukemia. Science 2008, 322:1377-1380.
29. Notta F., Mullighan C.G., Wang J.C.Y., Poeppl A., Doulatov S., Phillips L.A., Ma J., Minden M.D., Downing J.R., Dick J.E. Evolution of human BCR-ABL1 lymphoblastic leukaemia-initiating cells. Nature 2011, 469:362-367.
30. Palomero T., Lim W.K., Odom D.T., Sulis M.L., Real P.J., Margolin A., Barnes K.C., O'Neil J., Neuberg D., Weng A.P., et al. NOTCH1 directly regulates c-MYC and activates a feed-forward-loop transcriptional network promoting leukemic cell growth. Proc. Natl. Acad. Sci. USA 2006, 103:18261-18266.
31. Palomero T., Sulis M.L., Cortina M., Real P.J., Barnes K., Ciofani M., Caparros E., Buteau J., Brown K., Perkins S.L., et al. Mutational loss of PTEN induces resistance to NOTCH1 inhibition in T-cell leukemia. Nat. Med. 2007, 13:1203-1210.
32. Piovan E., Yu J., Tosello V., Herranz D., Ambesi-Impiombato A., Da Silva A.C., Sanchez-Martin M., Perez-Garcia A., Rigo I., Castillo M., et al. Direct reversal of glucocorticoid resistance by AKT inhibition in acute lymphoblastic leukemia. Cancer Cell 2013, 24:766-776.
33. Pui C.-H., Robison L.L., Look A.T. Acute lymphoblastic leukaemia. Lancet 2008, 371:1030-1043.
34. Schult C., Dahlhaus M., Glass A., Fischer K., Lange S., Freund M., Junghanss C. The dual kinase inhibitor NVP-BEZ235 in combination with cytotoxic drugs exerts anti-proliferative activity towards acute lymphoblastic leukemia cells. Anticancer Res. 2012, 32:463-474.
35. Shieh A., Ward A.F., Donlan K.L., Harding-Theobald E.R., Xu J., Mullighan C.G., Zhang C., Chen S.-C., Su X., Downing J.R., et al. Defective K-Ras oncoproteins overcome impaired effector activation to initiate leukemia invivo. Blood 2013, 121:4884-4893.
36. Silva A., Yunes J.A., Cardoso B.A., Martins L.R., Jotta P.Y., Abecasis M., Nowill A.E., Leslie N.R., Cardoso A.A., Barata J.T. PTEN posttranslational inactivation and hyperactivation of the PI3K/Akt pathway sustain primary Tcell leukemia viability. J.Clin. Invest. 2008, 118:3762-3774.
37. Smith A.C.H., Raimondi A.R., Salthouse C.D., Ignatius M.S., Blackburn J.S., Mizgirev I.V., Storer N.Y., de Jong J.L.O., Chen A.T., Zhou Y., et al. High-throughput cell transplantation establishes that tumor-initiating cells are abundant in zebrafish T-cell acute lymphoblastic leukemia. Blood 2010, 115:3296-3303.
38. Trinquand A., Tanguy-Schmidt A., Ben Abdelali R., Lambert J., Beldjord K., Lengliné E., De Gunzburg N., Payet-Bornet D., Lhermitte L., Mossafa H., et al. Toward a NOTCH1/FBXW7/RAS/PTEN-based oncogenetic risk classification of adult T-cell acute lymphoblastic leukemia: a Group for Research in Adult Acute Lymphoblastic Leukemia study. J.Clin. Oncol. 2013, 31:4333-4342.
39. Van Vlierberghe P., Ferrando A. The molecular basis of Tcell acute lymphoblastic leukemia. J.Clin. Invest. 2012, 122:3398-3406.
40. Yachida S., Jones S., Bozic I., Antal T., Leary R., Fu B., Kamiyama M., Hruban R.H., Eshleman J.R., Nowak M.A., et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 2010, 467:1114-1117.
41. Yap T.A., Yan L., Patnaik A., Fearen I., Olmos D., Papadopoulos K., Baird R.D., Delgado L., Taylor A., Lupinacci L., et al. First-in-man clinical trial of the oral pan-AKT inhibitor MK-2206 in patients with advanced solid tumors. J.Clin. Oncol. 2011, 29:4688-4695.
42. Zhang J., Ding L., Holmfeldt L., Wu G., Heatley S.L., Payne-Turner D., Easton J., Chen X., Wang J., Rusch M., et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 2012, 481:157-163.