DYRK1A binds to an evolutionarily conserved WD40-repeat protein WDR68 and induces its nuclear translocation

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1813, Issue 10, 2011, Pages 1728-1739

  Miyata, Yoshihiko ^a   Nishida, Eisuke ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Down's syndrome; DYRK1A; Nuclear translocation; WD40 repeat; WDR68

Indexed keywords

DUAL SPECIFICITY TYROSINE PHOSPHORYLATION REGULATED PROTEIN KINASE 1A; DUAL SPECIFICITY TYROSINE PHOSPHORYLATION REGULATED PROTEIN KINASE 1B; DUAL SPECIFICITY TYROSINE PHOSPHORYLATION REGULATED PROTEIN KINASE 2; DUAL SPECIFICITY TYROSINE PHOSPHORYLATION REGULATED PROTEIN KINASE 3; DUAL SPECIFICITY TYROSINE PHOSPHORYLATION REGULATED PROTEIN KINASE 4; MUTANT PROTEIN; PHOSPHOTRANSFERASE; PROTEIN; PROTEIN KINASE; UNCLASSIFIED DRUG; WDR68 PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; APOPTOSIS; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DOWN SYNDROME; ENZYME ACTIVE SITE; GENE OVEREXPRESSION; GENETIC CONSERVATION; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RNA INTERFERENCE; WILD TYPE;

ACTIVE TRANSPORT, CELL NUCLEUS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELL NUCLEUS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CONSERVED SEQUENCE; COS CELLS; EVOLUTION, MOLECULAR; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; TRANSFECTION;

MAMMALIA; PETUNIA;

EID: 80051788188     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2011.06.023     Document Type: Article

References (56)

1. Becker W., Joost H.-G. Structural and functional characteristics of DYRK, a novel subfamily of protein kinases with dual specificity. Prog. Nucleic Acid Res. Mol. Biol. 1999, 62:1-17.
2. Becker W., Weber Y., Wetzel K., Eirmbter K., Tejedor F.J., Joost H.-G. Sequence characteristics, subcellular localization, and substrate specificity of DYRK-related kinases, a novel family of dual specificity protein kinases. J. Biol. Chem. 1998, 273:25893-25902.
3. Miyata Y., Nishida E. Distantly related cousins of MAP kinase: biochemical properties and possible physiological functions. Biochem. Biophys. Res. Commun. 1999, 266:291-295.
4. Kentrup H., Becker W., Heukelbach J., Wilmes A., Schürmann A., Huppertz C., Kainulainen H., Joost H.-G. DYRK, a dual specificity protein kinase with unique structural features whose activity is dependent on tyrosine residues between subdomain VII and VIII. J. Biol. Chem. 1996, 271:3488-3495.
5. Lochhead P.A., Sibbet G., Morrice N., Cleghon V. Activation-loop autophosphorylation is mediated by a novel transitional intermediate form of DYRKs. Cell 2005, 121:925-936.
6. Galceran J., de Graaf K., Tejedor F.J., Becker W. The Mnb/Dyrk1A protein kinase: genetic and biochemical properties. J. Neural Transm. 2003, 67:139-148.
7. Hämmerle B., Elizalde C., Galceran J., Becker W., Tejedor F.J. The Mnb/Dyrk1A protein kinase: neurobiological functions and Down syndrome implications. J. Neural Transm. 2003, 67:129-137.
8. Altafaj X., Dierssen M., Baamonde C., Martí E., Visa J., Guimerà J., Oset M., González J.R., Flórez J., Fillat C., Estivill X. Neurodevelopmental delay, motor abnormalities and cognitive deficits in transgenic mice overexpressing Dyrk1A (minibrain), a murine model of Down's syndrome. Hum. Mol. Genet. 2001, 10:1915-1923.
9. Martínez de Lagrán M., Altafaj X., Gallego X., Martí E., Estivill X., Sahún I., Fillat C., Dierssen M. Motor phenotypic alterations in TgDyrk1a transgenic mice implicate DYRK1A in Down syndrome motor dysfunction. Neurobiol. Dis. 2004, 15:132-142.
10. Park J., Yang E.J., Yoon J.H., Chung K.C. Dyrk1A overexpression in immortalized hippocampal cells produces the neuropathological features of Down syndrome. Mol. Cell. Neurosci. 2007, 36:270-279.
11. Liu F., Liang Z., Wegiel J., Hwang Y.W., Iqbal K., Grundke-Iqbal I., Ramakrishna N., Gong C.X. Overexpression of Dyrk1A contributes to neurofibrillary degeneration in Down syndrome. FASEB J. 2008, 22:3224-3233.
12. Yabut O., Domogauer J., D'Arcangelo G. Dyrk1A overexpression inhibits proliferation and induces premature neuronal differentiation of neural progenitor cells. J. Neurosci. 2010, 30:4004-4014.
13. Arron J.R., Winslow M.M., Polleri A., Chang C.P., Wu H., Gao X., Neilson J.R., Chen L., Heit J.J., Kim S.K., Yamasaki N., Miyakawa T., Francke U., Graef I.A., Crabtree G.R. NFAT dysregulation by increased dosage of DSCR1 and DYRK1A on chromosome 21. Nature 2006, 441:595-600.
14. Gwack Y., Sharma S., Nardone J., Tanasa B., Iuga A., Srikanth S., Okamura H., Bolton D., Feske S., Hogan P.G., Rao A. A genome-wide Drosophila RNAi screen identifies DYRK-family kinases as regulators of NFAT. Nature 2006, 441:646-650.
15. Ryoo S.R., Jeong H.K., Radnaabazar C., Yoo J.J., Cho H.J., Lee H.W., Kim I.S., Cheon Y.H., Ahn Y.S., Chung S.H., Song W.J. DYRK1A-mediated hyperphosphorylation of Tau. A functional link between Down syndrome and Alzheimer disease. J. Biol. Chem. 2007, 282:34850-34857.
16. Skurat A.V., Dietrich A.D. Phosphorylation of Ser640 in muscle glycogen synthase by DYRK family protein kinases. J. Biol. Chem. 2004, 279:2490-2498.
17. Kurabayashi N., Hirota T., Sakai M., Sanada K., Fukada Y. DYRK1A and glycogen synthase kinase 3β, a dual-kinase mechanism directing proteasomal degradation of CRY2 for circadian timekeeping. Mol. Cell. Biol. 2010, 30:1757-1768.
18. Laguna A., Aranda S., Barallobre M.J., Barhoum R., Fernandez E., Fotaki V., Delabar J.M., de la Luna S., de la Villa P., Arbones M.L. The protein kinase DYRK1A regulates caspase-9-mediated apoptosis during retina development. Dev. Cell 2008, 15:841-853.
19. Seifert A., Allan L.A., Clarke P.R. DYRK1A phosphorylates caspase 9 at an inhibitory site and is potently inhibited in human cells by harmine. FEBS J. 2008, 275:6268-6280.
20. Leder S., Weber Y., Altafaj X., Estivill X., Joost H.G., Becker W. Cloning and characterization of DYRK1B, a novel member of the DYRK family of protein kinases. Biochem. Biophys. Res. Commun. 1999, 254:474-479.
21. Mercer S.E., Friedman E. Mirk/Dyrk1B: a multifunctional dual-specificity kinase involved in growth arrest, differentiation, and cell survival. Cell Biochem. Biophys. 2006, 45:303-315.
22. Mercer S.E., Ewton D.Z., Deng X., Lim S., Mazur T.R., Friedman E. Mirk/Dyrk1B mediates survival during the differentiation of C2C12 myoblasts. J. Biol. Chem. 2005, 280:25788-25801.
23. Gao J., Zheng Z., Rawal B., Schell M.J., Bepler G., Haura E.B. Mirk/Dyrk1B, a novel therapeutic target, mediates cell survival in non-small cell lung cancer cells. Cancer Biol. Ther. 2009, 8:1671-1679.
24. Jin K., Park S., Ewton D.Z., Friedman E. The survival kinase Mirk/Dyrk1B is a downstream effector of oncogenic K-ras in pancreatic cancer. Cancer Res. 2007, 67:7247-7255.
25. Lauth M., Bergstrom A., Shimokawa T., Tostar U., Jin Q., Fendrich V., Guerra C., Barbacid M., Toftgard R. DYRK1B-dependent autocrine-to-paracrine shift of Hedgehog signaling by mutant RAS. Nat. Struct. Mol. Biol. 2010, 17:718-725.
26. de Vetten N., Nissen R.M., Mol J., Koes R. The an11 locus controlling flower pigmentation in petunia encodes a novel WD-repeat protein conserved in yeast, plants, and animals. Genes Dev. 1997, 11:1422-1434.
27. Jin J., Arias E.E., Chen J., Harper J.W., Walter J.C. A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol. Cell 2006, 23:709-721.
28. Smith T.F., Gaitatzes C., Saxena K., Neer E.J. The WD repeat: a common architecture for diverse functions. Trends Biochem. Sci. 1999, 24:181-185.
29. Li D., Roberts R. WD-repeat proteins: structure characteristics, biological function, and their involvement in human diseases. Cell. Mol. Life Sci. 2001, 58:2058-2097.
30. Mao J., Maye P., Kogerman P., Tejedor F.J., Toftgard R., Xie W., Wu G., Wu D. Regulation of Gli1 transcriptional activity in the nucleus by Dyrk1. J. Biol. Chem. 2002, 277:35156-35161.
31. Morita K., Lo Celso C., Spencer-Dene B., Zouboulis C.C., Watt F.M. HAN11 binds mDia1 and controls GLI1 transcriptional activity. J. Dermatol. Sci. 2006, 44:11-20.
32. Koyasu S., Nishida E., Kadowaki T., Matsuzaki F., Iida K., Harada F., Kasuga M., Sakai H., Yahara I. Two mammalian heat shock proteins, HSP90 and HSP100, are actin-binding proteins. Proc. Natl. Acad. Sci. U.S.A. 1986, 83:8054-8058.
33. Miyata Y., Yahara I. p53-independent association between SV40 large T antigen and the major cytosolic heat shock protein, HSP90. Oncogene 2000, 19:1477-1484.
34. Miyata Y., Chambraud B., Radanyi C., Leclerc J., Lebeau M.-C., Renoir J.-M., Shirai R., Catelli M.-G., Yahara I., Baulieu E.-E. Phosphorylation of the immunosuppressant FK506-binding protein FKBP52 by casein kinase II (CK2): Regulation of HSP90-binding activity of FKBP52. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:14500-14505.
35. Miyata Y., Akashi M., Nishida E. Molecular cloning and characterization of a novel member of the MAP kinase superfamily. Genes Cells 1999, 4:299-309.
36. Miyata Y., Ikawa Y., Shibuya M., Nishida E. Specific association of a set of molecular chaperones including HSP90 and Cdc37 with MOK, a member of the MAP kinase superfamily. J. Biol. Chem. 2001, 276:21841-21848.
37. Miyata Y., Nishida E. CK2 controls multiple protein kinases by phosphorylating a kinase-targeting molecular chaperone Cdc37. Mol. Cell. Biol. 2004, 24:4065-4074.
38. Miyata Y., Nishida E. CK2 binds, phosphorylates, and regulates its pivotal substrate Cdc37, an Hsp90-cochaperone. Mol. Cell. Biochem. 2005, 274:171-179.
39. Nicholson D.W., Ali A., Thornberry N.A., Vaillancourt J.P., Ding C.K., Gallant M., Gareau Y., Griffin P.R., Labelle M., Lazebnik Y.A., Munday N.A., Raju S.M., Smulson M.E., Yamin T.-T., Yu V.L., Miller D.K. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995, 376:37-43.
40. Tewari M., Quan L.T., O'Rourke K., Desnoyers S., Zeng Z., Beidler D.R., Poirier G.G., Salvesen G.S., Dixit V.M. Yama/CPP32β, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 1995, 81:801-809.
41. Alvarez M., Estivill X., de la Luna S. DYRK1A accumulates in splicing speckles through a novel targeting signal and induces speckle disassembly. J. Cell Sci. 2003, 116:3099-3107.
42. Mazmanian G., Kovshilovsky M., Yen D., Mohanty A., Mohanty S., Nee A., Nissen R.M. The zebrafish dyrk1b gene is important for endoderm formation. Genesis 2010, 48:20-30.
43. Ritterhoff S., Farah C.M., Grabitzki J., Lochnit G., Skurat A.V., Schmitz M.L. The WD40-repeat protein Han11 functions as a scaffold protein to control HIPK2 and MEKK1 kinase functions. EMBO J. 2010, 29:3750-3761.
44. Walker A.R., Davison P.A., Bolognesi-Winfield A.C., James C.M., Srinivasan N., Blundell T.L., Esch J.J., Marks M.D., Gray J.C. The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 1999, 11:1337-1350.
45. Nissen R.M., Amsterdam A., Hopkins N. A zebrafish screen for craniofacial mutants identifies wdr68 as a highly conserved gene required for endothelin-1 expression. BMC Dev. Biol. 2006, 6:28-44.
46. van der Voorn L., Ploegh H.L. The WD-40 repeat. FEBS J. 1992, 307:131-134.
47. Wall M.A., Coleman D.E., Lee E., Iñiguez-Lluhi J.A., Posner B.A., Gilman A.G., Sprang S.R. The structure of the G protein heterotrimer Giα1β1γ2. Cell 1995, 83:1047-1058.
48. Sondek J., Bohm A., Lambright D.G., Hamm H.E., Sigler P.B. Crystal structure of a GA protein βγ betagamma dimer at 2.1Å resolution. Nature 1996, 379:369-374.
49. Hao B., Oehlmann S., Sowa M.E., Harper J.W., Pavletich N.P. Structure of a Fbw7-Skp1-cyclin E complex: multisite-phosphorylated substrate recognition by SCF ubiquitin ligases. Mol. Cell 2007, 26:131-143.
50. Coyle S.M., Gilbert W.V., Doudna J.A. Direct link between RACK1 function and localization at the ribosome in vivo. Mol. Cell. Biol. 2009, 29:1626-1634.
51. Ullah H., Scappini E.L., Moon A.F., Williams L.V., Armstrong D.L., Pedersen L.C. Structure of a signal transduction regulator, RACK1, from Arabidopsis thaliana. Protein Sci. 2008, 17:1771-1780.
52. Appleton B.A., Wu P., Wiesmann C. The crystal structure of murine coronin-1: a regulator of actin cytoskeletal dynamics in lymphocytes. Structure 2006, 14:87-96.
53. Ahn K.J., Jeong H.K., Choi H.S., Ryoo S.R., Kim Y.J., Goo J.S., Choi S.Y., Han J.S., Ha I., Song W.J. DYRK1A BAC transgenic mice show altered synaptic plasticity with learning and memory defects. Neurobiol. Dis. 2006, 22:463-472.
54. Ortiz-Abalia J., Sahún I., Altafaj X., Andreu N., Estivill X., Dierssen M., Fillat C. Targeting Dyrk1A with AAVshRNA attenuates motor alterations in TgDyrk1A, a mouse model of Down syndrome. Am. J. Hum. Genet. 2008, 83:479-488.
55. Göckler N., Jofre G., Papadopoulos C., Soppa U., Tejedor F.J., Becker W. Harmine specifically inhibits protein kinase DYRK1A and interferes with neurite formation. FEBS J. 2009, 276:6324-6337.
56. Orlicky S., Tang X., Neduva V., Elowe N., Brown E.D., Sicheri F., Tyers M. An allosteric inhibitor of substrate recognition by the SCFCdc4 ubiquitin ligase. Nat. Biotechnol. 2010, 28:733-737.