Cyclin-Dependent Kinase 6 Is a Chromatin-Bound Cofactor for NF-κB-Dependent Gene Expression

Molecular Cell

Volumn 53, Issue 2, 2014, Pages 193-208

  Handschick, Katja ^a   Beuerlein, Knut ^a   Jurida, Liane ^a   Bartkuhn, Marek ^b   Müller, Helmut ^a   Soelch, Johanna ^a   Weber, Axel ^a   Dittrich Breiholz, Oliver ^c   Schneider, Heike ^c   Scharfe, Maren ^d   Jarek, Michael ^d   Stellzig, Julia ^b   Schmitz, M Lienhard ^b   Kracht, Michael ^a  

^a JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; SYNAPTOTAGMIN I; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1;

ARTICLE; BINDING SITE; CELL CYCLE REGULATION; CELL NUCLEUS; CHROMATIN; CHROMOSOME TRANSLOCATION; GENE EXPRESSION; GENE LOCUS; GENE TARGETING; HUMAN; TRANSCRIPTION INITIATION;

CELL CYCLE; CHROMATIN; CYCLIN-DEPENDENT KINASE 4; CYCLIN-DEPENDENT KINASE 6; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; INTERLEUKIN-1; INTERLEUKIN-8; MAP KINASE KINASE KINASES; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84892840172     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.12.002     Document Type: Article

References (47)

1. Adey A., Burton J.N., Kitzman J.O., Hiatt J.B., Lewis A.P., Martin B.K., Qiu R., Lee C., Shendure J. The haplotype-resolved genome and epigenome of the aneuploid HeLa cancer cell line. Nature 2013, 500:207-211.
2. Anders L., Ke N., Hydbring P., Choi Y.J., Widlund H.R., Chick J.M., Zhai H., Vidal M., Gygi S.P., Braun P., Sicinski P. A systematic screen for CDK4/6 substrates links FOXM1 phosphorylation to senescence suppression in cancer cells. Cancer Cell 2011, 20:620-634.
3. Beyaert R., Cuenda A., Vanden Berghe W., Plaisance S., Lee J.C., Haegeman G., Cohen P., Fiers W. The p38/RK mitogen-activated protein kinase pathway regulates interleukin-6 synthesis response to tumor necrosis factor. EMBO J. 1996, 15:1914-1923.
4. Bockstaele L., Bisteau X., Paternot S., Roger P.P. Differential regulation of cyclin-dependent kinase 4 (CDK4) and CDK6, evidence that CDK4 might not be activated by CDK7, and design of a CDK6 activating mutation. Mol. Cell. Biol. 2009, 29:4188-4200.
5. Buss H., Handschick K., Jurrmann N., Pekkonen P., Beuerlein K., Müller H., Wait R., Saklatvala J., Ojala P.M., Schmitz M.L., et al. Cyclin-dependent kinase 6 phosphorylates NF-κB P65 at serine 536 and contributes to the regulation of inflammatory gene expression. PLoS ONE 2012, 7:e51847.
6. Choi Y.J., Anders L. Signaling through cyclin D-dependent kinases. Oncogene 2013, 10.1038/onc.2013.137.
7. Collombat P., Xu X., Ravassard P., Sosa-Pineda B., Dussaud S., Billestrup N., Madsen O.D., Serup P., Heimberg H., Mansouri A. The ectopic expression of Pax4 in the mouse pancreas converts progenitor cells into alpha and subsequently beta cells. Cell 2009, 138:449-462.
8. DiDonato J.A., Mercurio F., Karin M. NF-κB and the link between inflammation and cancer. Immunol. Rev. 2012, 246:379-400.
9. Diefenbacher M., Sekula S., Heilbock C., Maier J.V., Litfin M., van Dam H., Castellazzi M., Herrlich P., Kassel O. Restriction to Fos family members of Trip6-dependent coactivation and glucocorticoid receptor-dependent trans-repression of activator protein-1. Mol. Endocrinol. 2008, 22:1767-1780.
10. Fry D.W., Harvey P.J., Keller P.R., Elliott W.L., Meade M., Trachet E., Albassam M., Zheng X., Leopold W.R., Pryer N.K., Toogood P.L. Specific inhibition of cyclin-dependent kinase 4/6 by PD 0332991 and associated antitumor activity in human tumor xenografts. Mol. Cancer Ther. 2004, 3:1427-1438.
11. Grossel M.J., Hinds P.W. Beyond the cell cycle: a new role for Cdk6 in differentiation. J. Cell. Biochem. 2006, 97:485-493.
12. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
13. Hargreaves D.C., Horng T., Medzhitov R. Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 2009, 138:129-145.
14. Hennessy E.J., Sheedy F.J., Santamaria D., Barbacid M., O'Neill L.A. Toll-like receptor-4 (TLR4) down-regulates microRNA-107, increasing macrophage adhesion via cyclin-dependent kinase 6. J. Biol. Chem. 2011, 286:25531-25539.
15. Hu J., Haseebuddin M., Young M., Colburn N.H. Suppression of p65 phosphorylation coincides with inhibition of IkappaBalpha polyubiquitination and degradation. Mol. Carcinog. 2005, 44:274-284.
16. Huang B., Yang X.D., Lamb A., Chen L.F. Posttranslational modifications of NF-kappaB: another layer of regulation for NF-kappaB signaling pathway. Cell. Signal. 2010, 22:1282-1290.
17. Huberts D.H., van der Klei I.J. Moonlighting proteins: an intriguing mode of multitasking. Biochim. Biophys. Acta 2010, 1803:520-525.
18. Kassel O., Schneider S., Heilbock C., Litfin M., Göttlicher M., Herrlich P. A nuclear isoform of the focal adhesion LIM-domain protein Trip6 integrates activating and repressing signals at AP-1- and NF-kappaB-regulated promoters. Genes Dev. 2004, 18:2518-2528.
19. Kollmann K., Heller G., Schneckenleithner C., Warsch W., Scheicher R., Ott R.G., Schäfer M., Fajmann S., Schlederer M., Schiefer A.I., et al. A kinase-independent function of CDK6 links the cell cycle to tumor angiogenesis. Cancer Cell 2013, 24:167-181.
20. Lapenna S., Giordano A. Cell cycle kinases as therapeutic targets for cancer. Nat. Rev. Drug Discov. 2009, 8:547-566.
21. Larochelle S., Amat R., Glover-Cutter K., Sansó M., Zhang C., Allen J.J., Shokat K.M., Bentley D.L., Fisher R.P. Cyclin-dependent kinase control of the initiation-to-elongation switch of RNA polymerase II. Nat. Struct. Mol. Biol. 2012, 19:1108-1115.
22. Leonard J.P., LaCasce A.S., Smith M.R., Noy A., Chirieac L.R., Rodig S.J., Yu J.Q., Vallabhajosula S., Schoder H., English P., et al. Selective CDK4/6 inhibition with tumor responses by PD0332991 in patients with mantle cell lymphoma. Blood 2012, 119:4597-4607.
23. Li H., Wittwer T., Weber A., Schneider H., Moreno R., Maine G.N., Kracht M., Schmitz M.L., Burstein E. Regulation of NF-κB activity by competition between RelA acetylation and ubiquitination. Oncogene 2012, 31:611-623.
24. Li M., Lockwood W., Zielenska M., Northcott P., Ra Y.S., Bouffet E., Yoshimoto M., Rutka J.T., Yan H., Taylor M.D., et al. Multiple CDK/CYCLIND genes are amplified in medulloblastoma and supratentorial primitive neuroectodermal brain tumor. Cancer Genet 2012, 205:220-231.
25. Lin V.T., Lin F.T. TRIP6: an adaptor protein that regulates cell motility, antiapoptotic signaling and transcriptional activity. Cell. Signal. 2011, 23:1691-1697.
26. Malumbres M., Barbacid M. Cell cycle, CDKs and cancer: a changing paradigm. Nat. Rev. Cancer 2009, 9:153-166.
27. Malumbres M., Sotillo R., Santamaría D., Galán J., Cerezo A., Ortega S., Dubus P., Barbacid M. Mammalian cells cycle without the D-type cyclin-dependent kinases Cdk4 and Cdk6. Cell 2004, 118:493-504.
28. Mattioli I., Geng H., Sebald A., Hodel M., Bucher C., Kracht M., Schmitz M.L. Inducible phosphorylation of NF-kappa B p65 at serine 468 by T cell costimulation is mediated by IKK epsilon. J. Biol. Chem. 2006, 281:6175-6183.
29. Meyerson M., Harlow E. Identification of G1 kinase activity for cdk6, a novel cyclin D partner. Mol. Cell. Biol. 1994, 14:2077-2086.
30. Nagel S., Leich E., Quentmeier H., Meyer C., Kaufmann M., Drexler H.G., Zettl A., Rosenwald A., MacLeod R.A. Amplification at 7q22 targets cyclin-dependent kinase 6 in T-cell lymphoma. Leukemia 2008, 22:387-392.
31. Natoli G., Saccani S., Bosisio D., Marazzi I. Interactions of NF-kappaB with chromatin: the art of being at the right place at the right time. Nat. Immunol. 2005, 6:439-445.
32. Nonomura Y., Nagasaka K., Hagiyama H., Sekine C., Nanki T., Tamamori-Adachi M., Miyasaka N., Kohsaka H. Direct modulation of rheumatoid inflammatory mediator expression in retinoblastoma protein-dependent and -independent pathways by cyclin-dependent kinase 4/6. Arthritis Rheum. 2006, 54:2074-2083.
33. Ortega S., Malumbres M., Barbacid M. Cyclin D-dependent kinases, INK4 inhibitors and cancer. Biochim. Biophys. Acta 2002, 1602:73-87.
34. Perkins N.D. The diverse and complex roles of NF-κB subunits in cancer. Nat. Rev. Cancer 2012, 12:121-132.
35. Raychaudhuri S., Remmers E.F., Lee A.T., Hackett R., Guiducci C., Burtt N.P., Gianniny L., Korman B.D., Padyukov L., Kurreeman F.A., et al. Common variants at CD40 and other loci confer risk of rheumatoid arthritis. Nat. Genet. 2008, 40:1216-1223.
36. Sakaue-Sawano A., Kurokawa H., Morimura T., Hanyu A., Hama H., Osawa H., Kashiwagi S., Fukami K., Miyata T., Miyoshi H., et al. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 2008, 132:487-498.
37. Sakurai H. Targeting of TAK1 in inflammatory disorders and cancer. Trends Pharmacol. Sci. 2012, 33:522-530.
38. Schmitz M.L., Mattioli I., Buss H., Kracht M. NF-kappaB: a multifaceted transcription factor regulated at several levels. ChemBioChem 2004, 5:1348-1358.
39. Schmitz M.L., Weber A., Roxlau T., Gaestel M., Kracht M. Signal integration, crosstalk mechanisms and networks in the function of inflammatory cytokines. Biochim. Biophys. Acta 2011, 1813:2165-2175.
40. Tanaka T., Grusby M.J., Kaisho T. PDLIM2-mediated termination of transcription factor NF-kappaB activation by intranuclear sequestration and degradation of the p65 subunit. Nat. Immunol. 2007, 8:584-591.
41. Wang Y., Gilmore T.D. LIM domain protein Trip6 has a conserved nuclear export signal, nuclear targeting sequences, and multiple transactivation domains. Biochim. Biophys. Acta 2001, 1538:260-272.
42. Weber A., Wasiliew P., Kracht M. Interleukin-1 (IL-1) pathway. Sci. Signal. 2010, 3:cm1.
43. Westphal M., Hänsel M., Hamel W., Kunzmann R., Hölzel F. Karyotype analyses of 20 human glioma cell lines. Acta Neurochir. (Wien) 1994, 126:17-26.
44. Wiedemeyer W.R., Dunn I.F., Quayle S.N., Zhang J., Chheda M.G., Dunn G.P., Zhuang L., Rosenbluh J., Chen S., Xiao Y., et al. Pattern of retinoblastoma pathway inactivation dictates response to CDK4/6 inhibition in GBM. Proc. Natl. Acad. Sci. USA 2010, 107:11501-11506.
45. Wietek C., O'Neill L.A. Diversity and regulation in the NF-kappaB system. Trends Biochem. Sci. 2007, 32:311-319.
46. Yang P., Guo L., Duan Z.J., Tepper C.G., Xue L., Chen X., Kung H.J., Gao A.C., Zou J.X., Chen H.W. Histone methyltransferase NSD2/MMSET mediates constitutive NF-κB signaling for cancer cell proliferation, survival, and tumor growth via a feed-forward loop. Mol. Cell. Biol. 2012, 32:3121-3131.
47. Ziesché E., Kettner-Buhrow D., Weber A., Wittwer T., Jurida L., Soelch J., Müller H., Newel D., Kronich P., Schneider H., et al. The coactivator role of histone deacetylase 3 in IL-1-signaling involves deacetylation of p65 NF-κB. Nucleic Acids Res. 2013, 41:90-109.