Notch1 gene mutations target KRAS G12D-expressing CD8+ cells and contribute to their leukemogenic transformation

Journal of Biological Chemistry

Volumn 288, Issue 25, 2013, Pages 18219-18227

  Kong, Guangyao ^a   Du, Juan ^a   Liu, Yangang ^a   Meline, Benjamin ^b   Chang, Yuan I ^a   Ranheim, Erik A ^c   Wang, Jinyong ^a   Zhang, Jing ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE MUTATIONS; LYMPHOBLASTIC LEUKEMIA; OVER-EXPRESSION; UP-REGULATION;

BIOCHEMISTRY; BIOLOGY;

T-CELLS;

BETA CATENIN; K RAS PROTEIN; NOTCH1 RECEPTOR; WNT PROTEIN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; GAIN OF FUNCTION MUTATION; GENE DELETION; GENE MUTATION; GENE OVEREXPRESSION; LEUKEMOGENESIS; MOUSE; NONHUMAN; NOTCH1 GENE; ONCOGENE K RAS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION;

KRAS; LEUKEMIA; LEUKEMIA-INITIATING CELLS; LYMPHOMA; NOTCH; ONCOGENE; WNT PATHWAY;

ADULT; ANIMALS; BETA CATENIN; BONE MARROW TRANSPLANTATION; CD8-POSITIVE T-LYMPHOCYTES; CELL TRANSFORMATION, NEOPLASTIC; FLOW CYTOMETRY; HUMANS; KAPLAN-MEIER ESTIMATE; MICE; MICE, INBRED BALB C; MUTATION; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PRELEUKEMIA; PROTO-ONCOGENE PROTEINS P21(RAS); RECEPTOR, NOTCH1; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 84880074423     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.475376     Document Type: Article

References (32)

1. Ferrando, A. A., Neuberg, D. S., Staunton, J., Loh, M. L., Huard, C., Raimondi, S. C., Behm, F. G., Pui, C. H., Downing, J. R., Gilliland, D. G., Lander, E. S., Golub, T. R., and Look, A. T. (2002) Gene expression signatures define novel oncogenic pathways in T cell acute lymphoblastic leukemia. Cancer Cell 1, 75-87 (Pubitemid 41039178)
2. Teitell, M. A., and Pandolfi, P. P. (2009) Molecular genetics of acute lymphoblastic leukemia. Annu. Rev. Pathol. 4, 175-198
3. Uckun, F. M., Gaynon, P. S., Sensel, M. G., Nachman, J., Trigg, M. E., Steinherz, P. G., Hutchinson, R., Bostrom, B. C., Sather, H. N., and Reaman, G. H. (1997) Clinical features and treatment outcome of childhood T-lineage acute lymphoblastic leukemia according to the apparent maturational stage of T-lineage leukemic blasts: A Children's Cancer Group study. J. Clin. Oncol. 15, 2214-2221 (Pubitemid 27251121)
4. Brunning, R. D., Flandrin, G., Barowitz, M., Swerdlow, S. H., Matutes, E., and al., e. (2001) WHO histological classification of precursor B-cell and T-cell neoplasms. in Pathology & Genetics: Tumours of Haematopoietic and Lymphoid Tissues (Jaffe, E. S., Harris, N. L., Stein, H., and Vardiman, J. W., eds.) pp. 110-117, IARC Press, Lyon, France
5. Aifantis, I., Raetz, E., and Buonamici, S. (2008) Molecular pathogenesis of T-cell leukaemia and lymphoma. Nat. Rev. Immunol. 8, 380-390 (Pubitemid 351595220)
6. Weng, A. P., Ferrando, A. A., Lee, W., Morris, J. P., 4th, Silverman, L. B., Sanchez-Irizarry, C., Blacklow, S. C., Look, A. T., and Aster, J. C. (2004) Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306, 269-271 (Pubitemid 39336870)
7. van Grotel, M., Meijerink, J. P., van Wering, E. R., Langerak, A. W., Beverloo, H. B., Buijs-Gladdines, J. G., Burger, N. B., Passier, M., van Lieshout, E. M., Kamps, W. A., Veerman, A. J., van Noesel, M. M., and Pieters, R. (2008) Prognostic significance of molecular-cytogenetic abnormalities in pediatric T-ALL is not explained by immunophenotypic differences. Leukemia 22, 124-131
8. Genot, E., and Cantrell, D. A. (2000) Ras regulation and function in lymphocytes. Curr. Opin. Immunol. 12, 289-294 (Pubitemid 30240538)
9. von Lintig, F. C., Huvar, I., Law, P., Diccianni, M. B., Yu, A. L., and Boss, G. R. (2000) Ras activation in normal white blood cells and childhood acute lymphoblastic leukemia. Clin. Cancer Res. 6, 1804-1810 (Pubitemid 30305075)
10. Zhang, J., Ding, L., Holmfeldt, L., Wu, G., Heatley, S. L., Payne-Turner, D., Easton, J., Chen, X., Wang, J., Rusch, M., Lu, C., Chen, S. C., Wei, L., Collins-Underwood, J. R., Ma, J., Roberts, K. G., Pounds, S. B., Ulyanov, A., Becksfort, J., Gupta, P., Huether, R., Kriwacki, R. W., Parker, M., McGoldrick, D. J., Zhao, D., Alford, D., Espy, S., Bobba, K. C., Song, G., Pei, D., Cheng, C., Roberts, S., Barbato, M. I., Campana, D., Coustan-Smith, E., Shurtleff, S. A., Raimondi, S. C., Kleppe, M., Cools, J., Shimano, K. A., Hermiston, M. L., Doulatov, S., Eppert, K., Laurenti, E., Notta, F., Dick, J. E., Basso, G., Hunger, S. P., Loh, M. L., Devidas, M., Wood, B., Winter, S., Dunsmore, K. P., Fulton, R. S., Fulton, L. L., Hong, X., Harris, C. C., Dooling, D. J., Ochoa, K., Johnson, K. J., Obenauer, J. C., Evans, W. E., Pui, C. H., Naeve, C. W., Ley, T. J., Mardis, E. R., Wilson, R. K., Downing, J. R., and Mullighan, C. G. (2012) The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 481, 157-163
11. Guo, W., Lasky, J. L., Chang, C. J., Mosessian, S., Lewis, X., Xiao, Y., Yeh, J. E., Chen, J. Y., Iruela-Arispe, M. L., Varella-Garcia, M., and Wu, H. (2008) Multi-genetic events collaboratively contribute to Pten-null leukaemia stem-cell formation. Nature 453, 529-533 (Pubitemid 351733319)
12. Kelly, P. N., Dakic, A., Adams, J. M., Nutt, S. L., and Strasser, A. (2007) Tumor growth need not be driven by rare cancer stem cells. Science 317, 337 (Pubitemid 47106366)
13. Du, J., Liu, Y., Meline, B., Kong, G., Tan, L. X., Lo, J. C., Wang, J., Ranheim, E., Zhang, L., Chang, Y. I., Ryu, M. J., Zhang, J. F., and Zhang, J. (2013) Loss of CD44 attenuates aberrant GM-CSF signaling in Kras G12D hematopoietic progenitor/precursor cells and prolongs the survival of diseased animals. Leukemia 27, 754-757
14. Zhang, J., Wang, J., Liu, Y., Sidik, H., Young, K. H., Lodish, H. F., and Fleming, M. D. (2009) Oncogenic Kras-induced leukemogeneis: Hematopoietic stem cells as the initial target and lineage-specific progenitors as the potential targets for final leukemic transformation. Blood 113, 1304-1314
15. Kindler, T., Cornejo, M. G., Scholl, C., Liu, J., Leeman, D. S., Haydu, J. E., Fröhling, S., Lee, B. H., and Gilliland, D. G. (2008) K-RasG12D-induced T-cell lymphoblastic lymphoma/leukemias harbor Notch1 mutations and are sensitive to γ-secretase inhibitors. Blood 112, 3373-3382
16. Sabnis, A. J., Cheung, L. S., Dail, M., Kang, H. C., Santaguida, M., Hermiston, M. L., Passegué, E., Shannon, K., and Braun, B. S. (2009) Oncogenic Kras initiates leukemia in hematopoietic stem cells. PLoS Biol. 7, e59
17. Wang, J., Liu, Y., Li, Z., Wang, Z., Tan, L. X., Ryu, M. J., Meline, B., Du, J., Young, K. H., Ranheim, E., Chang, Q., and Zhang, J. (2011) Endogenous oncogenic Nras mutation initiates hematopoietic malignancies in a doseand cell type-dependent manner. Blood 118, 368-379
18. Chiang, M. Y., Xu, L., Shestova, O., Histen, G., L'Heureux, S., Romany, C., Childs, M. E., Gimotty, P. A., Aster, J. C., and Pear, W. S. (2008) Leukemiaassociated NOTCH1 alleles are weak tumor initiators but accelerate Kras-initiated leukemia. J. Clin. Invest. 118, 3181-3194
19. Ashworth, T. D., Pear, W. S., Chiang, M. Y., Blacklow, S. C., Mastio, J., Xu, L., Kelliher, M., Kastner, P., Chan, S., and Aster, J. C. (2010) Deletionbased mechanisms of Notch1 activation in T-ALL: Key roles for RAG recombinase and a conserved internal translational start site in Notch1. Blood 116, 5455-5464
20. Van Meter, M. E., Díaz-Flores, E., Archard, J. A., Passegué, E., Irish, J. M., Kotecha, N., Nolan, G. P., Shannon, K., and Braun, B. S. (2007) K-RasG12D expression induces hyperproliferation and aberrant signaling in primary hematopoietic stem/progenitor cells. Blood 109, 3945-3952 (Pubitemid 46641747)
21. Guo, Z., Dose, M., Kovalovsky, D., Chang, R., O'Neil, J., Look, A. T., von Boehmer, H., Khazaie, K., and Gounari, F. (2007) β-Catenin stabilization stalls the transition from double-positive to single-positive stage and predisposes thymocytes to malignant transformation. Blood 109, 5463-5472 (Pubitemid 46890570)
22. Dietrich, W. F., Lander, E. S., Smith, J. S., Moser, A. R., Gould, K. A., Luongo, C., Borenstein, N., and Dove, W. (1993) Genetic identification of Mom-1, a major modifier locus affecting Min-induced intestinal neoplasia in the mouse. Cell 75, 631-639 (Pubitemid 23346362)
23. Zhang, X., and Ren, R. (1998) Bcr-Abl efficiently induces a myeloproliferative disease and production of excess interleukin-3 and granulocytemacrophage colony-stimulating factor in mice: A novel model for chronic myelogenous leukemia. Blood 92, 3829-3840 (Pubitemid 28525209)
24. Parikh, C., Subrahmanyam, R., and Ren, R. (2007) Oncogenic NRAS, KRAS, and HRAS exhibit different leukemogenic potentials in mice. Cancer Res. 67, 7139-7146 (Pubitemid 47206541)
25. Perentesis, J. P., Bhatia, S., Boyle, E., Shao, Y., Shu, X. O., Steinbuch, M., Sather, H. N., Gaynon, P., Kiffmeyer, W., Envall-Fox, J., and Robison, L. L. (2004) RAS oncogene mutations and outcome of therapy for childhood acute lymphoblastic leukemia. Leukemia 18, 685-692 (Pubitemid 38500186)
26. Beier, D., Hau, P., Proescholdt, M., Lohmeier, A., Wischhusen, J., Oefner, P. J., Aigner, L., Brawanski, A., Bogdahn, U., and Beier, C. P. (2007) CD133+ and CD133-glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res. 67, 4010-4015 (Pubitemid 46815044)
27. Bagley, B. N., Keane, T. M., Maklakova, V. I., Marshall, J. G., Lester, R. A., Cancel, M. M., Paulsen, A. R., Bendzick, L. E., Been, R. A., Kogan, S. C., Cormier, R. T., Kendziorski, C., Adams, D. J., and Collier, L. S. (2012) A dominantly acting murine allele of Mcm4 causes chromosomal abnormalities and promotes tumorigenesis. PLoS Genet. 8, e1003034
28. Grabher, C., von Boehmer, H., and Look, A. T. (2006) Notch 1 activation in the molecular pathogenesis of T-cell acute lymphoblastic leukaemia. Nat. Rev. Cancer 6, 347-359
29. Mansour, M. R., Duke, V., Foroni, L., Patel, B., Allen, C. G., Ancliff, P. J., Gale, R. E., and Linch, D. C. (2007) Notch-1 mutations are secondary events in some patients with T-cell acute lymphoblastic leukemia. Clin. Cancer Res. 13, 6964-6969 (Pubitemid 350276876)
30. Li, X., Gounari, F., Protopopov, A., Khazaie, K., and von Boehmer, H. (2008) Oncogenesis of T-ALL and nonmalignant consequences of overexpressing intracellular NOTCH1. J. Exp. Med. 205, 2851-2861
31. Wang, J., Liu, Y., Li, Z., Du, J., Ryu, M. J., Taylor, P. R., Fleming, M. D., Young, K. H., Pitot, H., and Zhang, J. (2010) Endogenous oncogenic Nras mutation promotes aberrant GM-CSF signaling in granulocytic/monocytic precursors in a murine model of chronic myelomonocytic leukemia. Blood 116, 5991-6002
32. Gutierrez, A., and Look, A. T. (2007) NOTCH and PI3K-AKT pathways intertwined. Cancer Cell 12, 411-413 (Pubitemid 350046412)