The WD40-repeat protein Han11 functions as a scaffold protein to control HIPK2 and MEKK1 kinase functions

EMBO Journal

Volumn 29, Issue 22, 2010, Pages 3750-3761

  Ritterhoff, Stefanie ^a   Farah, Carla M ^a   Grabitzki, Julia ^a   Lochnit, Günter ^a   Skurat, Alexander V ^b   Schmitz, Michael Lienhard ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Han11; HIPK2; MAP kinase; MEKK1; scaffold protein

Indexed keywords

HOMEODOMAIN INTERACTING PROTEIN KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 1; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; WD40 REPEAT PROTEIN HAN11;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; ENZYME REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; ORTHOLOGY; OSMOTIC STRESS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STOICHIOMETRY;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CARRIER PROTEINS; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; MAP KINASE KINASE KINASE 1; OSMOTIC PRESSURE; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES;

CAENORHABDITIS ELEGANS;

EID: 78449296172     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.251     Document Type: Article

References (66)

1. Aikawa Y, Nguyen LA, Isono K, Takakura N, Tagata Y, Schmitz ML, Koseki H, Kitabayashi I (2006) Roles of HIPK1 and HIPK2 in AML1- and p300-dependent transcription, hematopoiesis and blood vessel formation. EMBO J 25: 3955-3965
2. Albert R, Oltvai ZN (2007) Shaping specificity in signaling networks. Nat Genet 39: 286-287
3. Altafaj X, Dierssen M, Baamonde C, Marti E, Visa J, Guimera J, Oset M, Gonzalez JR, Florez J, Fillat C, Estivill X (2001) Neurodevelopmental delay, motor abnormalities and cognitive deficits in transgenic mice overexpressing Dyrk1A (minibrain), a murine model of Down's syndrome. Hum Mol Genet 10: 1915-1923
4. Alvarez M, Estivill X, de la Luna S (2003) DYRK1A accumulates in splicing speckles through a novel targeting signal and induces speckle disassembly. J Cell Sci 116: 3099-3107
5. Bashor CJ, Helman NC, Yan S, Lim WA (2008) Using engineered scaffold interactions to reshape MAP kinase pathway signaling dynamics. Science 319: 1539-1543
6. Becker W, Joost HG (1999) Structural and functional characteristics of Dyrk, a novel subfamily of protein kinases with dual specificity. Prog Nucleic Acid Res Mol Biol 62: 1-17
7. Becker W, Weber Y, Wetzel K, Eirmbter K, Tejedor FJ, Joost HG (1998) Sequence characteristics, subcellular localization, and substrate specificity of DYRK-related kinases, a novel family of dual specificity protein kinases. J Biol Chem 273: 25893-25902
8. Beyaert R, Cuenda A, Vanden Berghe W, Plaisance S, Lee JC, Haegeman G, Cohen P, Fiers W (1996) The p38/RK mitogen-activated protein kinase pathway regulates interleukin-6 synthesis response to tumor necrosis factor. EMBO J 15: 1914-1923
9. Bhattacharyya RP, Remenyi A, Good MC, Bashor CJ, Falick AM, Lim WA (2006) The Ste5 scaffold allosterically modulates signaling output of the yeast mating pathway. Science 311: 822-826
10. Bouwmeester T, Bauch A, Ruffner H, Angrand PO, Bergamini G, Croughton K, Cruciat C, Eberhard D, Gagneur J, Ghidelli S, Hopf C, Huhse B, Mangano R, Michon AM, Schirle M, Schlegl J, Schwab M, Stein MA, Bauer A, Casari G et al (2004) A physical and functional map of the human TNF-alpha/NF-kappa B signal transduction pathway. Nat Cell Biol 6: 97-105
11. Brummelkamp TR, Bernards R, Agami R (2002) A system for stable expression of short interfering RNAs in mammalian cells. Science 296: 550-553
12. Calzado MA, Renner F, Roscic A, Schmitz ML (2007) HIPK2: a versatile switchboard regulating the transcription machinery and cell death. Cell Cycle 6: 139-143
13. Cuevas BD, Abell AN, Johnson GL (2007) Role of mitogen-activated protein kinase kinase kinases in signal integration. Oncogene 26: 3159-3171
14. D'Orazi G, Cecchinelli B, Bruno T, Manni I, Higashimoto Y, Saito S, Gostissa M, Coen S, Marchetti A, Del Sal G, Piaggio G, Fanciulli M, Appella E, Soddu S (2002) Homeodomain-interacting protein kinase-2 phosphorylates p53 at Ser 46 and mediates apoptosis. Nat Cell Biol 4: 11-19
15. De Vetten N, Quattrocchio F, Mol J, Koes R (1997) The an11 locus controlling flower pigmentation in petunia encodes a novel WD-repeat protein conserved in yeast, plants, and animals. Genes Dev 11 : 1422-1434
16. Dhanasekaran DN, Kashef K, Lee CM, Xu H, Reddy EP (2007) Scaffold proteins of MAP-kinase modules. Oncogene 26: 3185-3202
17. Dowjat WK, Adayev T, Kuchna I, Nowicki K, Palminiello S, Hwang YW, Wegiel J (2007) Trisomy-driven overexpression of DYRK1A kinase in the brain of subjects with Down syndrome. Neurosci Lett 413: 77-81
18. Fraser AG, Kamath RS, Zipperlen P, Martinez-Campos M, Sohrmann M, Ahringer J (2000) Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408: 325-330
19. Gallagher E, Enzler T, Matsuzawa A, Anzelon-Mills A, Otero D, Holzer R, Janssen E, Gao M, Karin M (2007) Kinase MEKK1 is required for CD40-dependent activation of the kinases Jnk and p38, germinal center formation, B cell proliferation and antibody production. Nat Immunol 8: 57-63
20. Garcia-Higuera I, Gaitatzes C, Smith TF, Neer EJ (1998) Folding a WD repeat propeller. Role of highly conserved aspartic acid residues in the G protein beta subunit and Sec13. J Biol Chem 273: 9041-9049
21. Gresko E, Ritterhoff S, Sevilla-Perez J, Roscic A, Frobius K, Kotevic I, Vichalkovski A, Hess D, Hemmings BA, Schmitz ML (2009) PML tumor suppressor is regulated by HIPK2-mediated phos-phorylation in response to DNA damage. Oncogene 28: 698-708
22. Gwack Y, Sharma S, Nardone J, Tanasa B, Iuga A, Srikanth S, Okamura H, Bolton D, Feske S, Hogan PG, Rao A (2006) A genome-wide Drosophila RNAi screen identifies DYRK-family kinases as regulators of NFAT. Nature 441: 646-650
23. Hattangadi SM, Burke KA, Lodish HF (2010) Homeodomain-inter-acting protein kinase 2 plays an important role in normal terminal erythroid differentiation. Blood 115: 4853-4861
24. Hofmann TG, Mincheva A, Lichter P, Droge W, Schmitz ML (2000) Human homeodomain-interacting protein kinase-2 (HIPK2) is a member of the DYRK family of protein kinases and maps to chromosome 7q32-q34. Biochimie 82: 1123-1127
25. Hofmann TG, Moller A, Sirma H, Zentgraf H, Taya Y, Droge W, Will H, Schmitz ML (2002) Regulation of p53 activity by its interaction with homeodomain-interacting protein kinase-2. Nat Cell Biol 4: 1-10
26. Hofmann TG, Stollberg N, Schmitz ML, Will H (2003) HIPK2 regulates transforming growth factor-beta-induced c-Jun NH(2)-terminal kinase activation and apoptosis in human hepatoma cells. Cancer Res 63: 8271-8277
27. Hudson AM, Cooley L (2008) Phylogenetic, structural and functional relationships between WD- and Kelch-repeat proteins. Subcell Biochem 48: 6-19
28. Ito M, Yoshioka K, Akechi M, Yamashita S, Takamatsu N, Sugiyama K, Hibi M, Nakabeppu Y, Shiba T, Yamamoto KI (1999) JSAP1, a novel jun N-terminal protein kinase (JNK)-binding protein that functions as a Scaffold factor in the JNK signaling pathway. Mol Cell Biol 19: 7539-7548
29. Kanei-Ishii C, Ninomiya-Tsuji J, Tanikawa J, Nomura T, Ishitani T, Kishida S, Kokura K, Kurahashi T, Ichikawa-Iwata E, Kim Y, Matsumoto K, Ishii S (2004) Wnt-1 signal induces phosphoryla-tion and degradation of c-Myb protein via TAK1, HIPK2, and NLK. Genes Dev 18: 816-829
30. Karandikar M, Xu S, Cobb MH (2000) MEKK1 binds raf-1 and the ERK2 cascade components. J Biol Chem 275: 40120-40127
31. Kim JW, Joe CO, Choi EJ (2001) Role of receptor-interacting protein in tumor necrosis factor-alpha-dependent MEKK1 activation. J Biol Chem 276: 27064-27070
32. Kim YH, Choi CY, Lee SJ, Conti MA, Kim Y (1998) Homeodomain-interacting protein kinases, a novel family of co-repressors for homeo-domain transcription factors. J Biol Chem 273: 25875-25879
33. Kimura R, Kamino K, Yamamoto M, Nuripa A, Kida T, Kazui H, Hashimoto R, Tanaka T, Kudo T, Yamagata H, Tabara Y, Miki T, Akatsu H, Kosaka K, Funakoshi E, Nishitomi K, Sakaguchi G, Kato A, Hattori H, Uema T et al (2007) The DYRK1A gene, encoded in chromosome 21 Down syndrome critical region, bridges between beta-amyloid production and tau phosphoryla-tion in Alzheimer disease. Hum Mol Genet 16: 15-23
34. Kolch W (2005) Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat Rev Mol Cell Biol 6: 827-837
35. Levchenko A, Bruck J, Sternberg PW (2000) Scaffold proteins may biphasically affect the levels of mitogen-activated protein kinase signaling and reduce its threshold properties. Proc Natl Acad Sci USA 97: 5818-5823
36. Li XL, Arai Y, Harada H, Shima Y, Yoshida H, Rokudai S, Aikawa Y, Kimura A, Kitabayashi I (2007) Mutations of the HIPK2 gene in acute myeloid leukemia and myelodysplastic syndrome impair AML1- and p53-mediated transcription. Oncogene 26: 7231-7239
37. Lu Z, Xu S, Joazeiro C, Cobb MH, Hunter T (2002) The PHD domain of MEKK1 acts as an E3 ubiquitin ligase and mediates ubiquitina-tion and degradation of ERK1/2. Mol Cell 9: 945-956
38. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S (2002) The protein kinase complement of the human genome. Science 298: 1912-1934
39. Matsuo R, Ochiai W, Nakashima K, Taga T (2001) A new expression cloning strategy for isolation of substrate-specific kinases by using phos-phorylation site-specific antibody. J Immunol Methods 247: 141-151
40. Matsuzawa A, Tseng PH, Vallabhapurapu S, Luo JL, Zhang W, Wang H, Vignali DA, Gallagher E, Karin M (2008) Essential cytoplasmic translocation of a cytokine receptor-assembled signaling complex. Science 321: 663-668
41. Mercer SE, Ewton DZ, Deng X, Lim S, Mazur TR, Friedman E (2005) Mirk/Dyrk1B mediates survival during the differentiation of C2C12 myoblasts. J Biol Chem 280: 25788-25801
42. Morrison DK, Davis RJ (2003) Regulation of MAP kinase signaling modules by scaffold proteins in mammals. Annu Rev Cell Dev Biol 19: 91-118
43. Pimienta G, Pascual J (2007) Canonical and alternative MAPK signaling. Cell Cycle 6: 2628-2632
44. Puca R, Nardinocchi L, Gal H, Rechavi G, Amariglio N, Domany E, Notterman DA, Scarsella M, Leonetti C, Sacchi A, Blandino G, Givol D, D'Orazi G (2008) Reversible dysfunction of wild-type p53 following homeodomain-interacting protein kinase-2 knockdown. Cancer Res 68: 3707-3714
45. Puca R, Nardinocchi L, Givol D, D'Orazi G (2010) Regulation of p53 activity by HIPK2: molecular mechanisms and therapeutical implications in human cancer cells. Oncogene 29: 4378-4387
46. Renner F, Moreno R, Schmitz ML (2010) SUMOylation-dependent localization of IKKepsilon in PML nuclear bodies is essential for protection against DNA-damage-triggered cell death. Mol Cell 37: 503-515
47. Rinaldo C, Prodosmo A, Siepi F, Soddu S (2007) HIPK2: a multi-talented partner for transcription factors in DNA damage response and development. Biochem Cell Biol 85: 411-418
48. Rinaldo C, Siepi F, Prodosmo A, Soddu S (2008) HIPKs: Jack of all trades in basic nuclear activities. Biochim Biophys Acta 1783: 2124-2129
49. Roscic A, Moller A, Calzado MA, Renner F, Wimmer VC, Gresko E, Ludi KS, Schmitz ML (2006) Phosphorylation-dependent control of Pc2 SUMO E3 ligase activity by its substrate protein HIPK2. Mol Cell 24: 77-89
50. Rui Y, Xu Z, Lin S, Li Q, Rui H, Luo W, Zhou HM, Cheung PY, Wu Z, Ye Z, Li P, Han J, Lin SC (2004) Axin stimulates p53 functions by activation of HIPK2 kinase through multimeric complex formation. EMBO J 23: 4583-4594
51. Russell M, Lange-Carter CA, Johnson GL (1995) Direct interaction between Ras and the kinase domain of mitogen-activated protein kinase kinase kinase (MEKK1). J Biol Chem 270: 11757-11760
52. Schlesinger TK, Bonvin C, Jarpe MB, Fanger GR, Cardinaux JR, Johnson GL, Widmann C (2002) Apoptosis stimulated by the 91-kDa caspase cleavage MEKK1 fragment requires translocation to soluble cellular compartments. J Biol Chem 277: 10283-10291
53. See RH, Calvo D, Shi Y, Kawa H, Luke MP, Yuan Z (2001) Stimulation of p300-mediated transcription by the kinase MEKK1. J Biol Chem 276: 16310-16317
54. Shaw AS, Filbert EL (2009) Scaffold proteins and immune-cell signalling. Nat Rev Immunol 9: 47-56
55. Skurat AV, Dietrich AD (2004) Phosphorylation of Ser640 in muscle glycogen synthase by DYRK family protein kinases. J Biol Chem 279: 2490-2498
56. Smith FD, Langeberg LK, Scott JD (2006) The where's and when's of kinase anchoring. Trends Biochem Sci 31 : 316-323
57. Takahashi-Yanaga F, Mori J, Matsuzaki E, Watanabe Y, Hirata M, Miwa Y, Morimoto S, Sasaguri T (2006) Involvement of GSK-3beta and DYRK1B in differentiation-inducing factor-3-induced phosphory-lation of cyclin D1 in HeLa cells. J Biol Chem 281: 38489-38497
58. Uhlik MT, Abell AN, Cuevas BD, Nakamura K, Johnson GL (2004) Wiring diagrams of MAPK regulation by MEKK1, 2, and 3. Biochem Cell Biol 82: 658-663
59. Van Der Voorn L, Ploegh HL (1992) The WD-40 repeat. FEBS Lett 307: 131-134
60. Vermeulen L, De Wilde G, Van Damme P, Vanden Berghe W, Haegeman G (2003) Transcriptional activation of the NF-kappaB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J 22: 1313-1324
61. Vomastek T, Schaeffer HJ, Tarcsafalvi A, Smolkin ME, Bissonette EA, Weber MJ (2004) Modular construction of a signaling scaffold: MORG1 interacts with components of the ERK cascade and links ERK signaling to specific agonists. Proc Natl Acad Sci USA 101 : 6981-6986
62. Wei G, Ku S, Ma GK, Saito S, Tang AA, Zhang J, Mao JH, Appella E, Balmain A, Huang EJ (2007) HIPK2 represses beta-catenin-mediated transcription, epidermal stem cell expansion, and skin tumorigenesis. Proc Natl Acad Sci USA 104: 13040-13045
63. Winter-Vann AM, Johnson GL (2007) Integrated activation of MAP3Ks balances cell fate in response to stress. J Cell Biochem 102: 848-858
64. Yu J, Deshmukh H, Gutmann RJ, Emnett RJ, Rodriguez FJ, Watson MA, Nagarajan R, Gutmann DH (2009) Alterations of BRAF and HIPK2 loci predominate in sporadic pilocytic astrocytoma. Neurology 73: 1526-1531
65. Yujiri T, Sather S, Fanger GR, Johnson GL (1998) Role of MEKK1 in cell survival and activation of JNK and ERK pathways defined by targeted gene disruption. Science 282: 1911-1914
66. Zhang Y, Neo SY, Wang X, Han J, Lin SC (1999) Axin forms a complex with MEKK1 and activates c-Jun NH(2)-terminal kinase/ stress-activated protein kinase through domains distinct from Wnt signaling. J Biol Chem 274: 35247-35254