The histone-H3K4-specific demethylase KDM5B Binds to its substrate and product through distinct PHD fingers

Cell Reports

Volumn 6, Issue 2, 2014, Pages 325-335

  Klein, Brianna J ^a   Piao, Lianhua ^b   Xi, Yuanxin ^c   Rincon Arano, Hector ^d   Rothbart, Scott B ^e   Peng, Danni ^b   Wen, Hong ^b   Larson, Connie ^f   Zhang, Xi ^b   Zheng, Xia ^c   Cortazar, Michael A ^a   Peña, Pedro V ^a   Mangan, Anthony ^a   Bentley, David L ^a   Strahl, Brian D ^e   Groudine, Mark ^d,g   Li, Wei ^c   Shi, Xiaobing ^b,f   Kutateladze, Tatiana G ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d Fred Hutchinson Cancer Research Center   (United States)

^e UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF TEXAS   (United States)

^g UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; BINDING SITES; BREAST NEOPLASMS; CELL LINE, TUMOR; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONE DEACETYLASE 1; HISTONES; HUMANS; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROTEIN BINDING; REPRESSOR PROTEINS;

CARRIER PROTEINS AND BINDING PROTEINS; HISTONE DEACETYLASE 1; HISTONE DEMETHYLASE; HISTONE H3; PHD1 FINGER PROTEIN; PHD3 FINGER PROTEIN; PROTEIN KDM5B; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BREAST CANCER CELL LINE; CELL INVASION; CELL MIGRATION; CHROMATIN; CONTROLLED STUDY; ENZYME SUBSTRATE; GENE REPRESSION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RNA SEQUENCE;

EID: 84895904908     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.12.021     Document Type: Article

References (37)

1. Ali M., Rincón-Arano H., Zhao W., Rothbart S.B., Tong Q., Parkhurst S.M., Strahl B.D., Deng L.W., Groudine M., Kutateladze T.G. Molecular basis for chromatin binding and regulation of MLL5. Proc. Natl. Acad. Sci. USA 2013, 110:11296-11301.
2. Allen H.F., Wade P.A., Kutateladze T.G. The NuRD architecture. Cell. Mol. Life Sci. 2013, 70:3513-3524.
3. Barrett A., Santangelo S., Tan K., Catchpole S., Roberts K., Spencer-Dene B., Hall D., Scibetta A., Burchell J., Verdin E., et al. Breast cancer associated transcriptional repressor PLU-1/JARID1B interacts directly with histone deacetylases. Int. J. Cancer 2007, 121:265-275.
4. Bouazoune K., Mitterweger A., Längst G., Imhof A., Akhtar A., Becker P.B., Brehm A. The dMi-2 chromodomains are DNA binding modules important for ATP-dependent nucleosome mobilization. EMBO J. 2002, 21:2430-2440.
5. Catchpole S., Spencer-Dene B., Hall D., Santangelo S., Rosewell I., Guenatri M., Beatson R., Scibetta A.G., Burchell J.M., Taylor-Papadimitriou J. PLU-1/JARID1B/KDM5B is required for embryonic survival and contributes to cell proliferation in the mammary gland and in ER+ breast cancer cells. Int. J. Oncol. 2011, 38:1267-1277.
6. Chicas A., Kapoor A., Wang X., Aksoy O., Evertts A.G., Zhang M.Q., Garcia B.A., Bernstein E., Lowe S.W. H3K4 demethylation by Jarid1a and Jarid1b contributes to retinoblastoma-mediated gene silencing during cellular senescence. Proc. Natl. Acad. Sci. USA 2012, 109:8971-8976.
7. Christensen J., Agger K., Cloos P.A., Pasini D., Rose S., Sennels L., Rappsilber J., Hansen K.H., Salcini A.E., Helin K. RBP2 belongs to a family of demethylases, specific for tri-and dimethylated lysine 4 on histone 3. Cell 2007, 128:1063-1076.
8. Cloos P.A., Christensen J., Agger K., Helin K. Erasing the methyl mark: histone demethylases at the center of cellular differentiation and disease. Genes Dev. 2008, 22:1115-1140.
9. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J.Biomol. NMR 1995, 6:277-293.
10. Eissenberg J.C., Lee M.G., Schneider J., Ilvarsonn A., Shiekhattar R., Shilatifard A. The trithorax-group gene in Drosophila little imaginal discs encodes a trimethylated histone H3 Lys4 demethylase. Nat. Struct. Mol. Biol. 2007, 14:344-346.
11. Grzesiek S., Stahl S.J., Wingfield P.T., Bax A. The CD4 determinant for downregulation by HIV-1 Nef directly binds to Nef. Mapping of the Nef binding surface by NMR. Biochemistry 1996, 35:10256-10261.
12. Hayami S., Yoshimatsu M., Veerakumarasivam A., Unoki M., Iwai Y., Tsunoda T., Field H.I., Kelly J.D., Neal D.E., Yamaue H., et al. Overexpression of the JmjC histone demethylase KDM5B in human carcinogenesis: involvement in the proliferation of cancer cells through the E2F/RB pathway. Mol. Cancer 2010, 9:59.
13. Iwase S., Lan F., Bayliss P., de la Torre-Ubieta L., Huarte M., Qi H.H., Whetstine J.R., Bonni A., Roberts T.M., Shi Y. The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 2007, 128:1077-1088.
14. Klose R.J., Kallin E.M., Zhang Y. JmjC-domain-containing proteins and histone demethylation. Nat. Rev. Genet. 2006, 7:715-727.
15. Klose R.J., Yan Q., Tothova Z., Yamane K., Erdjument-Bromage H., Tempst P., Gilliland D.G., Zhang Y., Kaelin W.G. The retinoblastoma binding protein RBP2 is an H3K4 demethylase. Cell 2007, 128:889-900.
16. Krishnakumar R., Kraus W.L. PARP-1 regulates chromatin structure and transcription through a KDM5B-dependent pathway. Mol. Cell 2010, 39:736-749.
17. Lan F., Collins R.E., De Cegli R., Alpatov R., Horton J.R., Shi X., Gozani O., Cheng X., Shi Y. Recognition of unmethylated histone H3 lysine4links BHC80 to LSD1-mediated gene repression. Nature 2007, 448:718-722.
18. Lee N., Zhang J., Klose R.J., Erdjument-Bromage H., Tempst P., Jones R.S., Zhang Y. The trithorax-group protein Lid is a histone H3 trimethyl-Lys4 demethylase. Nat. Struct. Mol. Biol. 2007, 14:341-343.
19. Li Q., Shi L., Gui B., Yu W., Wang J., Zhang D., Han X., Yao Z., Shang Y. Binding of the JmjC demethylase JARID1B to LSD1/NuRD suppresses angiogenesis and metastasis in breast cancer cells by repressing chemokine CCL14. Cancer Res. 2011, 71:6899-6908.
20. Liang G., Klose R.J., Gardner K.E., Zhang Y. Yeast Jhd2p is a histone H3 Lys4 trimethyl demethylase. Nat. Struct. Mol. Biol. 2007, 14:243-245.
21. Morris S.R., Carey L.A. Molecular profiling in breast cancer. Rev. Endocr. Metab. Disord. 2007, 8:185-198.
22. Murzina N.V., Pei X.Y., Zhang W., Sparkes M., Vicente-Garcia J., Pratap J.V., McLaughlin S.H., Ben-Shahar T.R., Verreault A., Luisi B.F., Laue E.D. Structural basis for the recognition of histone H4 by the histone-chaperone RbAp46. Structure 2008, 16:1077-1085.
23. Musselman C.A., Kutateladze T.G. Handpicking epigenetic marks with PHD fingers. Nucleic Acids Res. 2011, 39:9061-9071.
24. Musselman C.A., Mansfield R.E., Garske A.L., Davrazou F., Kwan A.H., Oliver S.S., O'Leary H., Denu J.M., Mackay J.P., Kutateladze T.G. Binding of the CHD4 PHD2 finger to histone H3 is modulated by covalent modifications. Biochem. J. 2009, 423:179-187.
25. Nijwening J.H., Geutjes E.J., Bernards R., Beijersbergen R.L. The histone demethylase Jarid1b (Kdm5b) is a novel component of the Rb pathway and associates with E2f-target genes in MEFs during senescence. PLoS ONE 2011, 6:e25235.
26. Roesch A., Becker B., Meyer S., Wild P., Hafner C., Landthaler M., Vogt T. Retinoblastoma-binding protein 2-homolog 1: a retinoblastoma-binding protein downregulated in malignant melanomas. Mod. Pathol. 2005, 18:1249-1257.
27. Roesch A., Fukunaga-Kalabis M., Schmidt E.C., Zabierowski S.E., Brafford P.A., Vultur A., Basu D., Gimotty P., Vogt T., Herlyn M. A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 2010, 141:583-594.
28. Scibetta A.G., Santangelo S., Coleman J., Hall D., Chaplin T., Copier J., Catchpole S., Burchell J., Taylor-Papadimitriou J. Functional analysis of the transcription repressor PLU-1/JARID1B. Mol. Cell. Biol. 2007, 27:7220-7235.
29. Secombe J., Li L., Carlos L., Eisenman R.N. The Trithorax group protein Lid is a trimethyl histone H3K4 demethylase required for dMyc-induced cell growth. Genes Dev. 2007, 21:537-551.
30. Seward D.J., Cubberley G., Kim S., Schonewald M., Zhang L., Tripet B., Bentley D.L. Demethylation of trimethylated histone H3 Lys4 invivo by JARID1 JmjC proteins. Nat. Struct. Mol. Biol. 2007, 14:240-242.
31. Shen Y., Lange O., Delaglio F., Rossi P., Aramini J.M., Liu G., Eletsky A., Wu Y., Singarapu K.K., Lemak A., et al. Consistent blind protein structure generation from NMR chemical shift data. Proc. Natl. Acad. Sci. USA 2008, 105:4685-4690.
32. Vicent G.P., Nacht A.S., Zaurin R., Font-Mateu J., Soronellas D., Le Dily F., Reyes D., Beato M. Unliganded progesterone receptor-mediated targeting of an RNA-containing repressive complex silences a subset of hormone-inducible genes. Genes Dev. 2013, 27:1179-1197.
33. Vranken W.F., Boucher W., Stevens T.J., Fogh R.H., Pajon A., Llinas M., Ulrich E.L., Markley J.L., Ionides J., Laue E.D. The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 2005, 59:687-696.
34. Wang G.G., Song J., Wang Z., Dormann H.L., Casadio F., Li H., Luo J.L., Patel D.J., Allis C.D. Haematopoietic malignancies caused by dysregulation of a chromatin-binding PHD finger. Nature 2009, 459:847-851.
35. Xiang Y., Zhu Z., Han G., Ye X., Xu B., Peng Z., Ma Y., Yu Y., Lin H., Chen A.P., Chen C.D. JARID1B is a histone H3 lysine 4 demethylase up-regulated in prostate cancer. Proc. Natl. Acad. Sci. USA 2007, 104:19226-19231.
36. Yamane K., Tateishi K., Klose R.J., Fang J., Fabrizio L.A., Erdjument-Bromage H., Taylor-Papadimitriou J., Tempst P., Zhang Y. PLU-1 is an H3K4 demethylase involved in transcriptional repression and breast cancer cell proliferation. Mol. Cell 2007, 25:801-812.
37. Yoshida M., Ishimura A., Terashima M., Enkhbaatar Z., Nozaki N., Satou K., Suzuki T. PLU1 histone demethylase decreases the expression of KAT5 and enhances the invasive activity of the cells. Biochem. J. 2011, 437:555-564.