Serine phosphorylation by SYK is critical for nuclear localization and transcription factor function of Ikaros

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 44, 2012, Pages 18072-18077

  Uckun, Fatih M ^a,b   Ma, Hong ^a,c   Zhang, Jian ^d   Ozer, Zahide ^a,c   Dovat, Sinisa ^e   Mao, Cheney ^f   Ishkhanian, Rita ^a   Goodman, Patricia ^c,g   Qazi, Sanjive ^a,h  

^a CHILDREN S HOSPITAL LOS ANGELES   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c PARKER HUGHES INSTITUTE   (United States)

^d SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^e PENNSYLVANIA STATE UNIVERSITY   (United States)

^f Viva Biotech ^*  (United States)

^g UNIVERSITY OF MINNESOTA   (United States)

^h GUSTAVUS ADOLPHUS COLLEGE   (United States)

Author keywords

Bioinformatics; Molecular modeling; Signaling; Site directed mutagenesis; Systems immunobiology

Indexed keywords

CD19 ANTIGEN; CD20 ANTIGEN; IKAROS TRANSCRIPTION FACTOR; PROTEIN KINASE SYK; SERINE;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; DNA BINDING; ENZYME ACTIVATION; ENZYME ACTIVITY; GENETICS; HUMAN; HUMAN CELL; IN VITRO STUDY; MUTAGENESIS; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY;

CELL NUCLEUS; HUMANS; IKAROS TRANSCRIPTION FACTOR; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTEIN-TYROSINE KINASES; SERINE;

EID: 84868129066     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1209828109     Document Type: Article

References (40)

1. Yoshida T, Ng SY, Georgopoulos K (2010) Awakening lineage potential by Ikarosmediated transcriptional priming. Curr Opin Immunol 22(2):154-160.
2. Cobb BS, et al. (2000) Targeting of Ikaros to pericentromeric heterochromatin by direct DNA binding. Genes Dev 14(17):2146-2160.
3. Thompson EC, et al. (2007) Ikaros DNA-binding proteins as integral components of B cell developmental-stage-specific regulatory circuits. Immunity 26(3):335-344.
4. Merkenschlager M (2010) Ikaros in immune receptor signaling, lymphocyte differentiation, and function. FEBS Lett 584(24):4910-4914.
5. Bottardi S, et al. (2011) Ikaros interacts with P-TEFb and cooperates with GATA-1 to enhance transcription elongation. Nucleic Acids Res 39(9):3505-3519.
6. Ma S, et al. (2010) Ikaros and Aiolos inhibit pre-B-cell proliferation by directly suppressing c-Myc expression. Mol Cell Biol 30(17):4149-4158.
7. Zhang J, et al. (2012) Harnessing of the nucleosome-remodeling- deacetylase complex controls lymphocyte development and prevents leukemogenesis. Nat Immunol 13(1): 86-94.
8. Dovat S, Song C, Payne KJ, Li Z (2011) Ikaros, CK2 kinase, and the road to leukemia. Mol Cell Biochem 356(1-2):201-207.
9. Sun L, et al. (1999) Expression of dominant-negative and mutant isoforms of the antileukemic transcription factor Ikaros in infant acute lymphoblastic leukemia. Proc Natl Acad Sci USA 96(2):680-685.
10. Mullighan CG, et al.; Children's Oncology Group (2009) Deletion of IKZF1 and prognosis in acute lymphoblastic leukemia. N Engl J Med 360(5):470-480.
11. Sun L, Liu A, Georgopoulos K (1996) Zinc finger-mediated protein interactions modulate Ikaros activity, a molecular control of lymphocyte development. EMBO J 15 (19):5358-5369.
12. Gurel Z, et al. (2008) Recruitment of Ikaros to pericentromeric heterochromatin is regulated by phosphorylation. J Biol Chem 283(13):8291-8300.
13. Gómez-del Arco P, Maki K, Georgopoulos K (2004) Phosphorylation controls Ikaros's ability to negatively regulate the G(1)-S transition. Mol Cell Biol 24(7):2797-2807.
14. Popescu M, et al. (2009) Ikaros stability and pericentromeric localization are regulated by protein phosphatase 1. J Biol Chem 284(20):13869-13880.
15. Cheng AM, et al. (1995) Syk tyrosine kinase required for mouse viability and B-cell development. Nature 378(6554):303-306.
16. Mócsai A, Ruland J, Tybulewicz VL (2010) The SYK tyrosine kinase: A crucial player in diverse biological functions. Nat Rev Immunol 10(6):387-402.
17. Turner M, et al. (1997) Syk tyrosine kinase is required for the positive selection of immature B cells into the recirculating B cell pool. J Exp Med 186(12):2013-2021.
18. Uckun FM, Qazi S (2010) Spleen tyrosine kinase as a molecular target for treatment of leukemias and lymphomas. Expert Rev Anticancer Ther 10(9):1407-1418.
19. Zhou F, Hu J, Ma H, Harrison ML, Geahlen RL (2006) Nucleocytoplasmic trafficking of the Syk protein tyrosine kinase. Mol Cell Biol 26(9):3478-3491.
20. Koretzky GA, Abtahian F, Silverman MA (2006) SLP76 and SLP65: Complex regulation of signalling in lymphocytes and beyond. Nat Rev Immunol 6(1):67-78.
21. Heizmann B, Reth M, Infantino S (2010) Syk is a dual-specificity kinase that self-regulates the signal output from the B-cell antigen receptor. Proc Natl Acad Sci USA 107 (43):18563-18568.
22. Uckun FM, Qazi S, Ma H, Tuel-Ahlgren L, Ozer Z (2010) STAT3 is a substrate of SYK tyrosine kinase in B-lineage leukemia/lymphoma cells exposed to oxidative stress. Proc Natl Acad Sci USA 107(7):2902-2907.
23. Wang L, Devarajan E, He J, Reddy SP, Dai JL (2005) Transcription repressor activity of spleen tyrosine kinase mediates breast tumor suppression. Cancer Res 65(22): 10289-10297.
24. Xue L, et al. (2012) Sensitive kinase assay linked with phosphoproteomics for identifying direct kinase substrates. Proc Natl Acad Sci USA 109(15):5615-5620.
25. Goodman PA, Wood CM, Vassilev A, Mao C, Uckun FM (2001) Spleen tyrosine kinase (Syk) deficiency in childhood pro-B cell acute lymphoblastic leukemia. Oncogene 20 (30):3969-3978.
26. Molnár A, Georgopoulos K (1994) The Ikaros gene encodes a family of functionally diverse zinc finger DNA-binding proteins. Mol Cell Biol 14(12):8292-8303.
27. Georgopoulos K, Moore DD, Derfler B (1992) Ikaros, an early lymphoid-specific transcription factor and a putative mediator for T cell commitment. Science 258 (5083):808-812.
28. Payne MA, et al. (2011) Zinc finger structure-function in Ikaros. World J Biol Chem 2 (6):161-166.
29. Tsutsui H, et al. (1999) The DNA-binding and transcriptional activities of MAZ, a mycassociated zinc finger protein, are regulated by casein kinase II. Biochem Biophys Res Commun 262(1):198-205.
30. Deindl S, et al. (2007) Structural basis for the inhibition of tyrosine kinase activity of ZAP-70. Cell 129(4):735-746.
31. deCastro RO (2011) Regulation and function of Syk tyrosine kinase in mast cell signaling and beyond. J Signal Transduct, 10.1155/2011/507291.
32. Sada K, Takano T, Yanagi S, Yamamura H (2001) Structure and function of Syk protein- tyrosine kinase. J Biochem 130(2):177-186.
33. Uckun FM, Ozer Z, Qazi S, Tuel-Ahlgren L, Mao C (2010) Polo-like-kinase 1 (PLK1) as a molecular target to overcome SYK-mediated resistance of B-lineage acute lymphoblastic leukaemia cells to oxidative stress. Br J Haematol 148(5):714-725.
34. Atwell S, et al. (2004) A novel mode of Gleevec binding is revealed by the structure of spleen tyrosine kinase. J Biol Chem 279(53):55827-55832.
35. Arias-Palomo E, Recuero-Checa MA, Bustelo XR, Llorca O (2009) Conformational rearrangements upon Syk auto-phosphorylation. Biochim Biophys Acta 1794(8): 1211-1217.
36. Tsang E, et al. (2008) Molecular mechanism of the Syk activation switch. J Biol Chem 283(47):32650-32659.
37. DeFranco AL (1996) The two-headed antigen. B-cell co-receptors. Curr Biol 6(5): 548-550.
38. Uckun FM, et al. (2010) Targeting human B precursor acute lymphoblastic leukemia cells with recombinant human CD19 ligand. Available at https://ash.confex.com/ash/2010/webprogram/Paper32270.html. Accessed December 4, 2010.
39. Depoil D, et al. (2008) CD19 is essential for B cell activation by promoting B cell receptor- antigen microcluster formation in response to membrane-bound ligand. Nat Immunol 9(1):63-72.
40. Zhong H, Tran LM, Stang JL (2009) Induced-fit docking studies of the active and inactive states of protein tyrosine kinases. J Mol Graph Model 28(4):336-346.