Deletion of the RNA-binding proteins ZFP36L1 and ZFP36L2 leads to perturbed thymic development and T lymphoblastic leukemia

Nature Immunology

Volumn 11, Issue 8, 2010, Pages 717-724

  Hodson, Daniel J ^a   Janas, Michelle L ^a   Galloway, Alison ^a   Bell, Sarah E ^a   Andrews, Simon ^a   Li, Cheuk M ^a   Pannell, Richard ^b   Siebel, Christian W ^c   MacDonald, H Robson ^d   De Keersmaecker, Kim ^e   Ferrando, Adolfo A ^e   Grutz, Gerald ^f,g   Turner, Martin ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c GENENTECH INC   (United States)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

^e NewYork Presbyterian Hospital   (United States)

^f CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^g INSTITUTE OF MATERIALS RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH1 RECEPTOR; PROTEIN ZFP36L1; PROTEIN ZFP36L2; RNA BINDING PROTEIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CONTROLLED STUDY; GENE DELETION; GENE MUTATION; GENE TARGETING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; T LYMPHOCYTE; THYMUS;

AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; HUMANS; IMMUNOPHENOTYPING; KAPLAN-MEIERS ESTIMATE; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; RECEPTOR, NOTCH1; RECEPTORS, ANTIGEN, T-CELL; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT; T-LYMPHOCYTES; THYMUS GLAND; TRANSCRIPTION, GENETIC; TRISTETRAPROLIN;

EID: 77954939922     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.1901     Document Type: Article

References (49)

1. Georgescu, C. et al. A gene regulatory network armature for T lymphocyte specifcation. Proc. Natl. Acad. Sci. USA 105, 20100-20105 (2008).
2. Rothenberg, E.V. Negotiation of the T lineage fate decision by transcription-factor interplay and microenvironmental signals. Immunity 26, 690-702 (2007).
3. Rothenberg, E.V., Moore, J.E. & Yui, M.A. Launching the T-cell-lineage developmental programme. Nat. Rev. Immunol. 8, 9-21 (2008).
4. Galante, P.A. et al. A comprehensive in silico expression analysis of RNA binding proteins in normal and tumor tissue: Identifcation of potential players in tumor formation. RNA Biol. 6, 426-433 (2009).
5. Taylor, G.A. et al. A pathogenetic role for TNFα in the syndrome of cachexia, arthritis, and autoimmunity resulting from tristetraprolin (TTP) defciency. Immunity 4, 445-454 (1996).
6. Carballo, E., Lai, W.S. & Blackshear, P.J. Feedback inhibition of macrophage tumor necrosis factor-α production by tristetraprolin. Science 281, 1001-1005 (1998).
7. Bell, S.E. et al. The RNA binding protein Zfp36l1 is required for normal vascularisation and post-transcriptionally regulates VEGF expression. Dev. Dyn. 235, 3144-3155 (2006).
8. Stumpo, D.J. et al. Chorioallantoic fusion defects and embryonic lethality resulting from disruption of Zfp36L1, a gene encoding a CCCH tandem zinc fnger protein of the Tristetraprolin family. Mol. Cell. Biol. 24, 6445-6455 (2004).
9. Stumpo, D.J. et al. Targeted disruption of Zfp36l2, encoding a CCCH tandem zinc fnger RNA-binding protein, results in defective hematopoiesis. Blood 114, 2401-2410 (2009).
10. Blackshear, P.J. et al. Characteristics of the interaction of a synthetic human tristetraprolin tandem zinc fnger peptide with AU-rich element-containing RNA substrates. J. Biol. Chem. 278, 19947-19955 (2003).
11. Hudson, B.P., Martinez-Yamout, M.A., Dyson, H.J. & Wright, P.E. Recognition of the mRNA AU-rich element by the zinc fnger domain of TIS11d. Nat. Struct. Mol. Biol. 11, 257-264 (2004).
12. Emmons, J. et al. Identifcation of TTP mRNA targets in human dendritic cells reveals TTP as a critical regulator of dendritic cell maturation. RNA 14, 888-902 (2008).
13. Klein, U. et al. The DLEU2/miR-15a/16-1 cluster controls B cell proliferation and its deletion leads to chronic lymphocytic leukemia. Cancer Cell 17, 28-40 2010).
14. Mayr, C. & Bartel, D.P. Widespread shortening of 3'UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138, 673-684 (2009).
15. Wiestner, A. et al. Point mutations and genomic deletions in CCND1 create stable truncated cyclin D1 mRNAs that are associated with increased proliferation rate and shorter survival. Blood 109, 4599-4606 (2007).
16. Sandberg, R., Neilson, J.R., Sarma, A., Sharp, P.A. & Burge, C.B. Proliferating cells express mRNAs with shortened 3' untranslated regions and fewer microRNA target sites. Science 320, 1643-1647 (2008).
17. Brennan, S.E. et al. The mRNA-destabilizing protein tristetraprolin is suppressed in many cancers, altering tumorigenic phenotypes and patient prognosis. Cancer Res. 69, 5168-5176 (2009).
18. Jackson, R.S. II, Cho, Y.J. & Liang, P. TIS11D is a candidate pro-apoptotic p53 target gene. Cell Cycle 5, 2889-2893 (2006).
19. Baou, M. et al. Involvement of Tis11b, an AU-rich binding protein, in induction of apoptosis by rituximab in B cell chronic lymphocytic leukemia cells. Leukemia 23, 986-989 (2009).
20. Benjamin, D. & Moroni, C. mRNA stability and cancer: an emerging link? Expert Opin. Biol. Ther. 7, 1515-1529 (2007).
21. de Boer, J. et al. Transgenic mice with hematopoietic and lymphoid specifc expression of Cre. Eur. J. Immunol. 33, 314-325 (2003).
22. Dumont, C. et al. Rac GTPases play critical roles in early T-cell development. Blood 113, 3990-3998 (2009).
23. Kelly, A.P. et al. Notch-induced T cell development requires phosphoinositide-dependent kinase 1. EMBO J. 26, 3441-3450 (2007).
24. Demarest, R.M., Ratti, F. & Capobianco, A.J. It's T-ALL about Notch. Oncogene 27, 5082-5091 (2008).
25. O'Neil, J. et al. Activating Notch1 mutations in mouse models of T-ALL. Blood 107, 781-785 (2006).
26. Wu, Y. et al. Therapeutic antibody targeting of individual Notch receptors. Nature 464, 1052-1057 (2010).
27. O'Connell, R.M., Rao, D.S., Chaudhuri, A.A. & Baltimore, D. Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 10, 111-122 (2010).
28. Papadaki, O. et al. Control of thymic T cell maturation, deletion and egress by the RNA-binding protein HuR. J. Immunol. 182, 6779-6788 (2009).
29. Winandy, S., Wu, L., Wang, J.H. & Georgopoulos, K. Pre-T cell receptor (TCR) and TCR-controlled checkpoints in T cell differentiation are set by Ikaros. J. Exp. Med. 190, 1039-1048 (1999).
30. Michie, A.M. & Zuniga-Pfucker, J.C. Regulation of thymocyte differentiation: pre-TCR signals and p-selection. Semin. Immunol. 14, 311-323 (2002).
31. Michie, A.M. et al. Constitutive Notch signalling promotes CD4 CD8 thymocyte differentiation in the absence of the pre-TCR complex, by mimicking pre-TCR signals. Int. Immunol. 19, 1421-1430 (2007).
32. Campese, A.F. et al. Notch1-dependent lymphomagenesis is assisted by but does not essentially require pre-TCR signaling. Blood 108, 305-310 (2006).
33. Ciofani, M. & Zuniga-Pfucker, J.C. Notch promotes survival of pre-T cells at the p-selection checkpoint by regulating cellular metabolism. Nat Immunol. 6, 881-888 (2005).
34. Pear, W.S. et al. Exclusive development of T cell neoplasms in mice transplanted with bone marrow expressing activated Notch alleles. J. Exp. Med. 183, 2283-2291 (1996).
35. Aster, J.C, Pear, W.S. & Blacklow, S.C. Notch signaling in leukemia. Annu. Rev. Pathol. 3, 587-613 (2008).
36. Li, X., Gounari, F., Protopopov, A., Khazaie, K. & von Boehmer, H. Oncogenesis of T-ALL and nonmalignant consequences of overexpressing intracellular NOTCH1. J. Exp. Med. 205, 2851-2861 (2008).
37. Gonsalves, F.C. & Weisblat, D.A. MAPK regulation of maternal and zygotic Notch transcript stability in early development. Proc. Natl. Acad. Sci. USA 104, 531-536 (2007).
38. Washburn, T. et al. Notch activity infuences the ap versus yd T cell lineage decision. Cell 88, 833-843 (1997).
39. Keene, J.D. RNA regulons: coordination of post-transcriptional events. Nat. Rev Genet. 8, 533-543 (2007).
40. Moellering, R.E. et al. Direct inhibition of the NOTCH transcription factor complex. Nature 462, 182-188 (2009).
41. Schmidlin, M. et al. The ARE-dependent mRNA-destabilizing activity of BRF1 is regulated by protein kinase B. EMBO J. 23, 4760-4769 (2004).
42. Benjamin, D., Schmidlin, M., Min, L., Gross, B. & Moroni, C. BRF1 protein turnover and mRNA decay activity are regulated by protein kinase B at the same phosphorylation sites. Mol. Cell. Biol. 26, 9497-9507 (2006).
43. Maitra, S. et al. The AU-rich element mRNA decay-promoting activity of BRF1 is regulated by mitogen-activated protein kinase-activated protein kinase 2. RNA 14, 950-959 (2008).
44. Palomero, T. et al. Mutational loss of PTEN induces resistance to NOTCH1 inhibition in T-cell leukemia. Nat. Med. 13, 1203-1210 (2007).
45. Palomero, T., Dominguez, M. & Ferrando, A.A. The role of the PTEN/AKT pathway in NOTCH1-induced leukemia. Cell Cycle 7, 965-970 (2008).
46. Weng, A.P. et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306, 269-271 (2004).
47. Rodriguez, C.I. et al. High-effciency deleter mice show that FLPe is an alternative to Cre-loxP. Nat. Genet. 25, 139-140 (2000).
48. Fiorini, E. et al. Dynamic regulation of notch 1 and notch 2 surface expression during T cell development and activation revealed by novel monoclonal antibodies. J. Immunol. 183, 7212-7222 (2009).
49. Dumortier, A. et al. Notch activation is an early and critical event during T-cell leukemogenesis in Ikaros-defcient mice. Mol. Cell. Biol. 26, 209-220 (2006).