Loss of T cell progenitor checkpoint control underlies leukemia initiation in Rag1-deficient nonobese diabetic mice

Journal of Immunology

Volumn 190, Issue 7, 2013, Pages 3276-3288

  Yui, Mary A ^a   Feng, Ni ^a   Zhang, Jingli A ^a   Liaw, Chen Yee ^a   Rothenberg, Ellen V ^a   Longmate, Jeffrey A ^b  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b Division of Biostatistics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; PROTEIN TYROSINE KINASE; RAG1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD2 GENE; CD5 GENE; CELL CYCLE CHECKPOINT; CHROMOSOME 4; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENE REPRESSION; GENETIC ANALYSIS; HHEX GENE; IDD GENE; KIT GENE; LEUKEMIA; LEUKEMOGENESIS; LMO2 GENE; LYL1 GENE; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PRE T LYMPHOCYTE; PRIORITY JOURNAL; PROTO ONCOGENE; QUANTITATIVE TRAIT LOCUS MAPPING; RAG1 GENE; RNA SEQUENCE; SIGNAL TRANSDUCTION; STEM CELL; STRAIN DIFFERENCE; T LYMPHOCYTE; THYMOCYTE; THYMUS; TRANSCRIPTOMICS;

ACTINS; AGE FACTORS; ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; CHROMOSOME MAPPING; CHROMOSOMES, MAMMALIAN; CLUSTER ANALYSIS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; LYMPHOMA; MALE; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; PRECURSOR CELLS, T-LYMPHOID; QUANTITATIVE TRAIT LOCI; SIGNAL TRANSDUCTION; STEM CELLS; THYMOCYTES; TRANSCRIPTION, GENETIC;

EID: 84875413871     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202970     Document Type: Article

References (53)

1. Petrie, H. T., and J. C. Zúñiga-Pflücker. 2007. Zoned out: functional mapping of stromal signaling microenvironments in the thymus. Annu. Rev. Immunol. 25: 649-679.
2. Love, P. E., and A. Bhandoola. 2011. Signal integration and crosstalk during thymocyte migration and emigration. Nat. Rev. Immunol. 11: 469-477.
3. Godfrey, D. I., J. Kennedy, T. Suda, and A. Zlotnik. 1993. A developmental pathway involving four phenotypically and functionally distinct subsets of CD3- CD4-CD8- triple-negative adult mouse thymocytes defined by CD44 and CD25 expression. J. Immunol. 150: 4244-4252.
4. Porritt, H. E., L. L. Rumfelt, S. Tabrizifard, T. M. Schmitt, J. C. Zúñiga-Pflücker, and H. T. Petrie. 2004. Heterogeneity among DN1 prothymocytes reveals multiple progenitors with different capacities to generate T cell and non-T cell lineages. Immunity 20: 735-745.
5. Yui, M. A., N. Feng, and E. V. Rothenberg. 2010. Fine-scale staging of T cell lineage commitment in adult mouse thymus. J. Immunol. 185: 284-293.
6. Li, L., M. Leid, and E. V. Rothenberg. 2010. An early T cell lineage commitment checkpoint dependent on the transcription factor Bcl11b. Science 329: 89-93.
7. Ikawa, T., S. Hirose, K. Masuda, K. Kakugawa, R. Satoh, A. Shibano-Satoh, R. Kominami, Y. Katsura, and H. Kawamoto. 2010. An essential developmental checkpoint for production of the T cell lineage. Science 329: 93-96.
8. Rothenberg, E. V., J. E. Moore, and M. A. Yui. 2008. Launching the T-celllineage developmental programme. Nat. Rev. Immunol. 8: 9-21.
9. Rothenberg, E. V., J. Zhang, and L. Li. 2010. Multilayered specification of the T-cell lineage fate. Immunol. Rev. 238: 150-168.
10. Hoffman, E. S., L. Passoni, T. Crompton, T. M. Leu, D. G. Schatz, A. Koff, M. J. Owen, and A. C. Hayday. 1996. Productive T-cell receptor b-chain gene rearrangement: coincident regulation of cell cycle and clonality during development in vivo. Genes Dev. 10: 948-962.
11. Borowski, C., C. Martin, F. Gounari, L. Haughn, I. Aifantis, F. Grassi, and H. von Boehmer. 2002. On the brink of becoming a T cell. Curr. Opin. Immunol. 14: 200-206.
12. Anderson, M. S., and J. A. Bluestone. 2005. The NOD mouse: a model of immune dysregulation. Annu. Rev. Immunol. 23: 447-485.
13. Delovitch, T. L., and B. Singh. 1997. The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD. Immunity 7: 727-738.
14. Lyons, P. A., W. W. Hancock, P. Denny, C. J. Lord, N. J. Hill, N. Armitage, T. Siegmund, J. A. Todd, M. S. Phillips, J. F. Hess, et al. 2000. The NOD Idd9 genetic interval influences the pathogenicity of insulitis and contains molecular variants of Cd30, Tnfr2, and Cd137. Immunity 13: 107-115.
15. Serreze, D. V., and E. H. Leiter. 2001. Genes and cellular requirements for autoimmune diabetes susceptibility in nonobese diabetic mice. Curr. Dir. Autoimmun. 4: 31-67.
16. Todd, J. A., and L. S. Wicker. 2001. Genetic protection from the inflammatory disease type 1 diabetes in humans and animal models. Immunity 15: 387-395.
17. Feng, N., P. Vegh, E. V. Rothenberg, and M. A. Yui. 2011. Lineage divergence at the first TCR dependent checkpoint: preferential &gammaδ and impaired αβ T cell development in nonobese diabetic mice. J. Immunol. 186: 826-837.
18. Yui, M. A., and E. V. Rothenberg. 2004. Deranged early T cell development in immunodeficient strains of nonobese diabetic mice. J. Immunol. 173: 5381-5391.
19. Prochazka, M., H. R. Gaskins, L. D. Shultz, and E. H. Leiter. 1992. The nonobese diabetic scid mouse: model for spontaneous thymomagenesis associated with immunodeficiency. Proc. Natl. Acad. Sci. USA 89: 3290-3294.
20. Shultz, L. D., P. A. Lang, S. W. Christianson, B. Gott, B. Lyons, S. Umeda, E. Leiter, R. Hesselton, E. J. Wagar, J. H. Leif, et al. 2000. NOD/LtSz-Rag1null mice: an immunodeficient and radioresistant model for engraftment of human hematolymphoid cells, HIV infection, and adoptive transfer of NOD mouse diabetogenic T cells. J. Immunol. 164: 2496-2507.
21. Chiu, P. P., E. Ivakine, S. Mortin-Toth, and J. S. Danska. 2002. Susceptibility to lymphoid neoplasia in immunodeficient strains of nonobese diabetic mice. Cancer Res. 62: 5828-5834.
22. Broman, K. W., H. Wu, S. Sen, and G. A. Churchill. 2003. R/qtl: QTL mapping in experimental crosses. Bioinformatics 19: 889-890.
23. Kruglyak, L., and E. S. Lander. 1995. A nonparametric approach for mapping quantitative trait loci. Genetics 139: 1421-1428.
24. Zhang, J. A., A. Mortazavi, B. A. Williams, B. J. Wold, and E. V. Rothenberg. 2012. Dynamic transformations of genome-wide epigenetic marking and transcriptional control establish T cell identity. Cell 149: 467-482.
25. Edgar, R., M. Domrachev, and A. E. Lash. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30: 207-210.
26. Mortazavi, A., B. A. Williams, K. McCue, L. Schaeffer, and B. Wold. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5: 621-628.
27. Pepke, S., B. Wold, and A. Mortazavi. 2009. Computation for ChIP-seq and RNA-seq studies. Nat. Methods 6(Suppl.): S22-S32.
28. David-Fung, E. S., R. Butler, G. Buzi, M. A. Yui, R. A. Diamond, M. K. Anderson, L. Rowen, and E. V. Rothenberg. 2009. Transcription factor expression dynamics of early T-lymphocyte specification and commitment. Dev. Biol. 325: 444-467.
29. Ghosh, S., S. M. Palmer, N. R. Rodrigues, H. J. Cordell, C. M. Hearne, R. J. Cornall, J. B. Prins, P. McShane, G. M. Lathrop, L. B. Peterson, et al. 1993. Polygenic control of autoimmune diabetes in nonobese diabetic mice. Nat. Genet. 4: 404-409.
30. Brodnicki, T. C., P. McClive, S. Couper, and G. Morahan. 2000. Localization of Idd11 using NOD congenic mouse strains: elimination of Slc9a1 as a candidate gene. Immunogenetics 51: 37-41.
31. Inoue, K., H. Ikegami, T. Fujisawa, S. Noso, K. Nojima, N. Babaya, M. Itoi- Babaya, S. Makimo, and T. Ogihara. 2004. Allelic variation in class I K gene as candidate for a second component of MHC-linked susceptibility to type 1 diabetes in non-obese diabetic mice. Diabetologia 47: 739-747.
32. Boulard, O., D. Damotte, N. Deruytter, G. Fluteau, C. Carnaud, and H. J. Garchon. 2002. An interval tightly linked to but distinct from the H2 complex controls both overt diabetes (Idd16) and chronic experimental autoimmune thyroiditis (Ceat1) in nonobese diabetic mice. Diabetes 51: 2141-2147.
33. Hiromine, Y., T. Fujisawa, S. Noso, N. Babaya, Y. Kawabata, and H. Ikegami. 2008. Congenic mapping of the MHC-linked susceptibility to type 1 diabetes in the NOD mouse: at least two genes contribute to the Idd16 effect. Ann. N. Y. Acad. Sci. 1150: 90-92.
34. McAleer, M. A., P. Reifsnyder, S. M. Palmer, M. Prochazka, J. M. Love, J. B. Copeman, E. E. Powell, N. R. Rodrigues, J. B. Prins, D. V. Serreze, et al. 1995. Crosses of NOD mice with the related NON strain: a polygenic model for IDDM. Diabetes 44: 1186-1195.
35. Huang, W., B. T. Sherman, and R. A. Lempicki. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4: 44-57.
36. Burkhardt, J. K., E. Carrizosa, and M. H. Shaffer. 2008. The actin cytoskeleton in T cell activation. Annu. Rev. Immunol. 26: 233-259.
37. Wadleigh, M., D. J. DeAngelo, J. D. Griffin, and R. M. Stone. 2005. After chronic myelogenous leukemia: tyrosine kinase inhibitors in other hematologic malignancies. Blood 105: 22-30.
38. Mingueneau, M., W. Jiang, M. Feuerer, D. Mathis, and C. Benoist. 2012. Thymic negative selection is functional in NOD mice. J. Exp. Med. 209: 623-637.
39. Schmitt, T. M., and J. C. Zúñiga-Pflücker. 2002. Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity 17: 749-756.
40. Moore, K. A., B. Pytowski, L. Witte, D. Hicklin, and I. R. Lemischka. 1997. Hematopoietic activity of a stromal cell transmembrane protein containing epidermal growth factor-like repeat motifs. Proc. Natl. Acad. Sci. USA 94: 4011-4016.
41. De Keersmaecker, K., P. J. Real, G. D. Gatta, T. Palomero, M. L. Sulis, V. Tosello, P. Van Vlierberghe, K. Barnes, M. Castillo, X. Sole, et al. 2010. The TLX1 oncogene drives aneuploidy in T cell transformation. Nat. Med. 16: 1321-1327.
42. Gutierrez, A., A. Kentsis, T. Sanda, L. Holmfeldt, S. C. Chen, J. Zhang, A. Protopopov, L. Chin, S. E. Dahlberg, D. S. Neuberg, et al. 2011. The BCL11B tumor suppressor is mutated across the major molecular subtypes of T-cell acute lymphoblastic leukemia. Blood 118: 4169-4173.
43. Zhang, J., L. Ding, L. Holmfeldt, G. Wu, S. L. Heatley, D. Payne-Turner, J. Easton, X. Chen, J. Wang, M. Rusch, et al. 2012. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 481: 157-163.
44. Wolfer, A., T. Bakker, A. Wilson, M. Nicolas, V. Ioannidis, D. R. Littman, P. P. Lee, C. B. Wilson, W. Held, H. R. MacDonald, and F. Radtke. 2001. Inactivation of Notch 1 in immature thymocytes does not perturb CD4 or CD8T cell development. Nat. Immunol. 2: 235-241.
45. 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.
46. Iwai, L. K., C. Benoist, D. Mathis, and F. M. White. 2010. Quantitative phosphoproteomic analysis of T cell receptor signaling in diabetes prone and resistant mice. J. Proteome Res. 9: 3135-3145.
47. 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.
48. Coustan-Smith, E., C. G. Mullighan, M. Onciu, F. G. Behm, S. C. Raimondi, D. Pei, C. Cheng, X. Su, J. E. Rubnitz, G. Basso, et al. 2009. Early T-cell precursor leukaemia: a subtype of very high-risk acute lymphoblastic leukaemia. Lancet Oncol. 10: 147-156.
49. McCormack, M. P., L. F. Young, S. Vasudevan, C. A. de Graaf, R. Codrington, T. H. Rabbitts, S. M. Jane, and D. J. Curtis. 2010. The Lmo2 oncogene initiates leukemia in mice by inducing thymocyte self-renewal. Science 327: 879-883.
50. Aifantis, I., E. Raetz, and S. Buonamici. 2008. Molecular pathogenesis of T-cell leukaemia and lymphoma. Nat. Rev. Immunol. 8: 380-390.
51. Shu, X., J. Ji, X. Li, J. Sundquist, K. Sundquist, and K. Hemminki. 2010. Cancer risk among patients hospitalized for type 1 diabetes mellitus: a population-based cohort study in Sweden. Diabet. Med. 27: 791-797.
52. Manda, S. O., R. G. Feltbower, and M. S. Gilthorpe. 2009. Investigating spatiotemporal similarities in the epidemiology of childhood leukaemia and diabetes. Eur. J. Epidemiol. 24: 743-752.
53. Goodnow, C. C. 2007. Multistep pathogenesis of autoimmune disease. Cell 130: 25-35.