Phosphorylation-dependent regulation of PSF by GSK3 controls CD45 alternative splicing

Molecular Cell

Volumn 40, Issue 1, 2010, Pages 126-137

  Heyd, Florian ^a   Lynch, Kristen W ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CD45 ANTIGEN; GLYCOGEN SYNTHASE KINASE 3; MESSENGER RNA PRECURSOR; PROTEIN PSF; PROTEIN TRAP150; UNCLASSIFIED DRUG; 2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; DNA BINDING PROTEIN; INDOLE DERIVATIVE; MALEIMIDE DERIVATIVE; MESSENGER RNA; MITOGENIC AGENT; OLIGONUCLEOTIDE; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN BINDING; PROTEIN KINASE INHIBITOR; PTB-ASSOCIATED SPLICING FACTOR; PTPRC PROTEIN, HUMAN; RNA BINDING PROTEIN; RNA PRECURSOR; THRAP3 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ARTICLE; CELL SURFACE; COMPLEX FORMATION; CONTROLLED STUDY; EXON; HUMAN; HUMAN CELL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RNA PROCESSING; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; ALTERNATIVE RNA SPLICING; BINDING SITE; CELL CULTURE; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MUTATION; PHOSPHORYLATION; T LYMPHOCYTE; TIME;

ALTERNATIVE SPLICING; ANTIGENS, CD45; BINDING SITES; CELLS, CULTURED; DNA-BINDING PROTEINS; EXONS; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHASE KINASE 3; HUMANS; INDOLES; LYMPHOCYTE ACTIVATION; MALEIMIDES; MITOGENS; MUTATION; OLIGONUCLEOTIDES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN KINASE INHIBITORS; RNA PRECURSORS; RNA, MESSENGER; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TETRADECANOYLPHORBOL ACETATE; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 77957377260     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2010.09.013     Document Type: Article

References (37)

1. An P., Grabowski P.J. Exon silencing by UAGG motifs in response to neuronal excitation. PLoS Biol. 2007, 5:e36. 10.1371/journal.pbio.0050036.
2. Bracken C.P., Wall S.J., Barre B., Panov K.I., Ajuh P.M., Perkins N.D. Regulation of cyclin D1 RNA stability by SNIP1. Cancer Res. 2008, 68:7621-7628.
3. Chalfant C.E., Mischak H., Watson J.E., Winkler B.C., Goodnight J., Farese R.V., Cooper D.R. Regulation of alternative splicing of protein kinase C beta by insulin. J. Biol. Chem. 1995, 270:13326-13332.
4. Cohen P., Frame S. The renaissance of GSK3. Natl. Rev. 2001, 2:769-776.
5. Conaway R.C., Sato S., Tomomori-Sato C., Yao T., Conaway J.W. The mammalian Mediator complex and its role in transcriptional regulation. Trends Biochem. Sci. 2005, 30:250-255.
6. Diehn M., Alizadeh A.A., Rando O.J., Liu C.L., Stankunas K., Botstein D., Crabtree G.R., Brown P.O. Genomic expression programs and the integration of the CD28 costimulatory signal in T cell activation. Proc. Natl. Acad. Sci. USA 2002, 99:11796-11801.
7. Fondell J.D., Ge H., Roeder R.G. Ligand induction of a transcriptionally active thyroid hormone receptor coactivator complex. Proc. Natl. Acad. Sci. USA 1996, 93:8329-8333.
8. Hermiston M.L., Xu Z., Majeti R., Weiss A. Reciprocal regulation of lymphocyte activation by tyrosine kinases and phosphatases. J. Clin. Invest. 2002, 109:9-14.
9. Hooper C., Killick R., Lovestone S. The GSK3 hypothesis of Alzheimer's disease. J. Neurochem. 2008, 104:1433-1439.
10. Hung L.H., Heiner M., Hui J., Schreiner S., Benes V., Bindereif A. Diverse roles of hnRNP L in mammalian mRNA processing: a combined microarray and RNAi analysis. RNA 2008, 14:284-296.
11. Ip J.Y., Tong A., Pan Q., Topp J.D., Blencowe B.J., Lynch K.W. Global analysis of alternative splicing during T-cell activation. RNA 2007, 13:563-572.
12. Izquierdo J.M., Valcárcel J. Fas-activated serine/threonine kinase (FAST K) synergizes with TIA-1/TIAR proteins to regulate Fas alternative splicing. J. Biol. Chem. 2007, 282:1539-1543.
13. Jacobsen M., Hoffmann S., Cepok S., Stei S., Ziegler A., Sommer N., Hemmer B. A novel mutation in PTPRC interferes with splicing and alters the structure of the human CD45 molecule. Immunogenetics 2002, 54:158-163.
14. Lee J.A., Xing Y., Nguyen D., Xie J., Lee C.J., Black D.L. Depolarization and CaM kinase IV modulate NMDA receptor splicing through two essential RNA elements. PLoS Biol. 2007, 5:e40. 10.1371/journal.pbio.0050040.
15. Li J., Hawkins I.C., Harvey C.D., Jennings J.L., Link A.J., Patton J.G. Regulation of alternative splicing by SRrp86 and its interacting proteins. Mol. Cell. Biol. 2003, 23:7437-7447.
16. Lynch K.W. Consequences of regulated pre-mRNA splicing in the immune system. Nat. Rev. Immunol. 2004, 4:931-940.
17. Lynch K.W. Regulation of alternative splicing by signal transduction pathways. Adv. Exp. Med. Biol. 2007, 623:161-174.
18. Lynch K.W., Weiss A. A model system for the activation-induced alternative-splicing of CD45 implicates protein kinase C and Ras. Mol. Cell. Biol. 2000, 20:70-80.
19. Martin M., Rehani K., Jope R.S., Michalek S.M. Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat. Immunol. 2005, 6:777-784.
20. Matter N., Herrlich P., Konig H. Signal-dependent regulation of splicing via phosphorylation of Sam68. Nature 2002, 420:691-695.
21. Melton A.A., Jackson J., Wang J., Lynch K.W. Combinatorial control of signal-induced exon repression by hnRNP L and PSF. Mol. Cell. Biol. 2007, 27:6972-6984.
22. Merz C., Urlaub H., Will C.L., Luhrmann R. Protein composition of human mRNPs spliced in vitro and differential requirements for mRNP protein recruitment. RNA 2007, 13:116-128.
23. Motta-Mena L.B., Heyd F., Lynch K.W. Context-dependent regulatory mechanism of the splicing factor hnRNP L. Mol. Cell 2010, 29:223-234.
24. Oberdoerffer S., Moita L.F., Neems D., Freitas R.P., Hacohen N., Rao A. Regulation of CD45 alternative splicing by heterogeneous ribonucleoprotein, hnRNPLL. Science 2008, 321:686-691.
25. Ohteki T., Parsons M., Zakarian A., Jones R.G., Nguyen L.T., Woodgett J.R., Ohashi P.S. Negative regulation of T cell proliferation and interleukin 2 production by the serine threonine kinase Gsk-3. J. Exp. Med. 2000, 192:99-104.
26. Plattner F., Angelo M., Giese K.P. The roles of cyclin-dependent kinase 5 and glycogen synthase kinase 3 in tau hyperphosphorylation. J. Biol. Chem. 2006, 281:25457-25465.
27. Rothrock C., Cannon B., Hahm B., Lynch K.W. A conserved signal-responsive sequence mediates activation-induced alternative splicing of CD45. Mol. Cell 2003, 12:1317-1324.
28. Rothrock C.R., House A.E., Lynch K.W. HnRNP L represses exon splicing via a regulated exonic splicing silencer. EMBO J. 2005, 24:2792-2802.
29. Sengupta S., Jayaraman P., Chilton P.M., Casella C.R., Mitchell T.C. Unrestrained glycogen synthase kinase-3 beta activity leads to activated T cell death and can be inhibited by natural adjuvant. J. Immunol. 2007, 178:6083-6091.
30. Shav-Tal Y., Zipori D. PSF and p54(nrb)/NonO-multi-functional nuclear proteins. FEBS Lett. 2002, 531:109-114.
31. Shav-Tal Y., Cohen M., Lapter S., Dye B., Patton J.G., Vandekerckhove J., Zipori D. Nuclear relocalization of the pre-mRNA splicing factor PSF during apoptosis involves hyperphosphorylation, masking of antigenic epitopes, and changes in protein interactions. Mol. Biol. Cell 2001, 12:2328-2340.
32. Shin C., Manley J.L. Cell signalling and the control of pre-mRNA splicing. Nat. Rev. Mol. Cell Biol. 2004, 5:727-738.
33. Topp J.D., Jackson J., Melton A.A., Lynch K.W. A cell-based screen for splicing regulators identifies hnRNP LL as a distinct signal-induced repressor of CD45 variable exon 4. RNA 2008, 14:2038-2049.
34. Welsh G.I., Miyamoto S., Price N.T., Safer B., Proud C.G. T-cell activation leads to rapid stimulation of translation initiation factor eIF2B and inactivation of glycogen synthase kinase-3. J. Biol. Chem. 1996, 271:11410-11413.
35. Wu Z., Jia X., de la Cruz L., Su X.C., Marzolf B., Troisch P., Zak D., Hamilton A., Whittle B., Yu D., et al. Memory T cell RNA rearrangement programmed by heterogeneous nuclear ribonucleoprotein hnRNPLL. Immunity 2008, 29:863-875.
36. Wu G., Huang H., Garcia-Abreu J., He X. Inhibition of GSK3 phosphorylation of beta-catenin via phosphorylated PPPSPXS motifs of Wnt coreceptor LRP6. PLoS ONE 2009, 4:e4926. 10.1371/journal.pone.0004926.
37. Xu Z., Weiss A. Negative regulation of CD45 by differential homodimerization of the alternatively spliced isoforms. Nat. Immunol. 2002, 3:764-771.