A Myc-dependent division timer complements a cell-death timer to regulate T cell and B cell responses

Nature Immunology

Volumn 18, Issue 1, 2017, Pages 96-103

  Heinzel, Susanne ^a,b   Binh Giang, Tran ^a,b   Kan, Andrey ^a,b   Marchingo, Julia M ^a,b,c   Lye, Bryan K ^a,b   Corcoran, Lynn M ^a,b   Hodgkin, Philip D ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MYC PROTEIN; MYC PROTEIN, MOUSE; PROTEIN BCL 2;

ANIMAL CELL; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL CYCLE REGULATION; CELL DIVISION; CELL GROWTH; CELL LOSS; CONTROLLED STUDY; GENE OVEREXPRESSION; IMMUNE RESPONSE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; ANIMAL; C57BL MOUSE; CD8+ T LYMPHOCYTE; CELL CULTURE; CELL DEATH; CELL PROLIFERATION; CELLULAR IMMUNITY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; B-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL DEATH; CELL DIVISION; CELL PROLIFERATION; CELLS, CULTURED; GENE EXPRESSION REGULATION; IMMUNITY, CELLULAR; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTO-ONCOGENE PROTEINS C-MYC; SIGNAL TRANSDUCTION; TRANSGENES;

EID: 84994462722     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3598     Document Type: Article

References (36)

1. Marchingo, J. M. et al. T cell signaling. Antigen affinity, costimulation, and cytokine inputs sum linearly to amplify T cell expansion. Science 346, 1123-1127 (2014).
2. Mescher, M. F. et al. Signals required for programming effector and memory development by CD8+ T cells. Immunol. Rev. 211, 81-92 (2006).
3. Zehn, D., Lee, S. Y. & Bevan, M. J. Complete but curtailed T-cell response to very low-affinity antigen. Nature 458, 211-214 (2009).
4. Hawkins, E. D., Markham, J. F., McGuinness, L. P. & Hodgkin, P. D. A single-cell pedigree analysis of alternative stochastic lymphocyte fates. Proc. Natl. Acad. Sci. USA 106, 13457-13462 (2009).
5. Turner, M. L., Hawkins, E. D. & Hodgkin, P. D. Quantitative regulation of B cell division destiny by signal strength. J. Immunol. 181, 374-382 (2008).
6. Vervoorts, J., Lüscher-Firzlaff, J. & Lüscher, B. The ins and outs of MYC regulation by posttranslational mechanisms. J. Biol. Chem. 281, 34725-34729 (2006).
7. Laurenti, E. et al. Hematopoietic stem cell function and survival depend on c-Myc and N-Myc activity. Cell Stem Cell 3, 611-624 (2008).
8. Donnelly, R. P. & Finlay, D. K. Glucose, glycolysis and lymphocyte responses. Mol. Immunol. 68, 2 Pt C, 513-519 (2015).
9. Preston, G. C. et al. Single cell tuning of Myc expression by antigen receptor signal strength and interleukin-2 in T lymphocytes. EMBO J. 34, 2008-2024 (2015).
10. Wang, R. et al. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity 35, 871-882 (2011).
11. Liu, J. & Levens, D. Making myc. Curr. Top. Microbiol. Immunol. 302, 1-32 (2006).
12. Conacci-Sorrell, M., McFerrin, L. & Eisenman, R. N. An overview of MYC and its interactome. Cold Spring Harb. Perspect. Med. 4, a014357 (2014).
13. Dang, C. V. MYC on the path to cancer. Cell 149, 22-35 (2012).
14. Vita, M. & Henriksson, M. The Myc oncoprotein as a therapeutic target for human cancer. Semin. Cancer Biol. 16, 318-330 (2006).
15. Adams, J. M. et al. The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 318, 533-538 (1985).
16. Ogilvy, S. et al. Constitutive Bcl-2 expression throughout the hematopoietic compartment affects multiple lineages and enhances progenitor cell survival. Proc. Natl. Acad. Sci. USA 96, 14943-14948 (1999).
17. Hawkins, E. D., Turner, M. L., Dowling, M. R., van Gend, C. & Hodgkin, P. D. A model of immune regulation as a consequence of randomized lymphocyte division and death times. Proc. Natl. Acad. Sci. USA 104, 5032-5037 (2007).
18. Gregory, M. A. & Hann, S. R. c-Myc proteolysis by the ubiquitin-proteasome pathway: stabilization of c-Myc in Burkitt's lymphoma cells. Mol. Cell. Biol. 20, 2423-2435 (2000).
19. Nie, Z. et al. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 151, 68-79 (2012).
20. Duffy, K. R. & Hodgkin, P. D. Intracellular competition for fates in the immune system. Trends Cell Biol. 22, 457-464 (2012).
21. Duffy K.R. et al. Activation-induced B cell fates are selected by intracellular stochastic competition. Science 335, 338-341 (2012).
22. Hawkins, E. D. et al. Measuring lymphocyte proliferation, survival and differentiation using CFSE time-series data. Nat. Protoc. 2, 2057-2067 (2007).
23. Kinjyo, I. et al. Real-time tracking of cell cycle progression during CD8+ effector and memory T-cell differentiation. Nat. Commun. 6, 6301 (2015).
24. Marchingo, J. M. et al. T cell stimuli independently sum to regulate an inherited clonal division fate. Nat. Commun. (in the press).
25. Raff, M. The mystery of intracellular developmental programmes and timers. Biochem. Soc. Trans. 34, 663-670 (2006).
26. Burton, P. B. J., Raff, M. C., Kerr, P., Yacoub, M. H. & Barton, P. J. R. An intrinsic timer that controls cell-cycle withdrawal in cultured cardiac myocytes. Dev. Biol. 216, 659-670 (1999).
27. Link, J. M. & Hurlin, P. J. The activities of MYC, MNT and the MAX-interactome in lymphocyte proliferation and oncogenesis. Biochimica et Biophysica Acta. 1849, 554-562 (2015).
28. Prendergast, G. C. Mechanisms of apoptosis by c-Myc. Oncogene 18, 2967-2987 (1999).
29. Cory, S., Huang, D. C. S. & Adams, J. M. The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene 22, 8590-8607 (2003).
30. Strasser, A., Harris, A. W., Bath, M. L. & Cory, S. Novel primitive lymphoid tumours induced in transgenic mice by cooperation between myc and bcl-2. Nature 348, 331-333 (1990).
31. Aukema, S. M. et al. Double-hit B-cell lymphomas. Blood 117, 2319-2331 (2011).
32. Hommel, M. & Hodgkin, P. D. TCR affinity promotes CD8+ T cell expansion by regulating survival. J. Immunol. 179, 2250-2260 (2007).
33. Bouillet, P. et al. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286, 1735-1738 (1999).
34. Smith, D. P., Bath, M. L., Metcalf, D., Harris, A. W. & Cory, S. MYC levels govern hematopoietic tumor type and latency in transgenic mice. Blood 108, 653-661 (2006).
35. Deenick, E. K., Gett, A. V. & Hodgkin, P. D. Stochastic model of T cell proliferation: a calculus revealing IL-2 regulation of precursor frequencies, cell cycle time, and survival. J. Immunol. 170, 4963-4972 (2003).
36. Liu, X. et al. Generation of mammalian cells stably expressing multiple genes at predetermined levels. Anal. Biochem. 280, 20-28 (2000).