JARID1B is a luminal lineage-driving oncogene in breast cancer

Cancer Cell

Volumn 25, Issue 6, 2014, Pages 762-777

  Yamamoto, Shoji ^a,b,c,p   Wu, Zhenhua ^a,d,q   Russnes, Hege G ^a,b,c,e   Takagi, Shinji ^a,b,c,r   Peluffo, Guillermo ^a,b,c   Vaske, Charles ^f   Zhao, Xi ^g   MoenVollan, Hans Kristian ^e   Maruyama, Reo ^a,b,c,h   Ekram, Muhammad B ^a,b,c   Sun, Hanfei ^a,i   Kim, Jee Hyun ^a,b,c,j   Carver, Kristopher ^a,b,c,s   Zucca, Mattia ^a,k   Feng, Jianxing ⁱ   Almendro, Vanessa ^a,b,c   Bessarabova, Marina ^l   Rueda, Oscar M ^m   Nikolsky, Yuri ^l   Caldas, Carlos ^m   Liu, X Shirley ^a,d,n   Polyak, Kornelia ^a,b,c,n,o   more..

^a DANA FARBER CANCER INSTITUTE   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^e OSLO UNIVERSITY HOSPITAL   (Norway)

^f Five3 Genomics   (United States)

^g STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

ⁱ TONGJI UNIVERSITY   (China)

^j Seoul National University College of Medicine   (South Korea)

^k VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^l Thomson Reuters   (United States)

^m UNIVERSITY OF CAMBRIDGE   (United Kingdom)

ⁿ BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^o HARVARD STEM CELL INSTITUTE   (United States)

^p DAIICHI SANKYO CO   (Japan)

^q EISAI INC   (United States)

^r TAKEDA PHARMACEUTICAL COMPANY LIMITED   (Japan)

^s Boston Scientific   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEMETHYLASE; HORMONE RECEPTOR; JARID 1B PROTEIN; PROTEIN INHIBITOR; TRANSFORMING GROWTH FACTOR BETA INHIBITOR; UNCLASSIFIED DRUG;

ARTICLE; BASAL LIKE BREAST CANCER; BREAST CANCER; BREAST CANCER CELL LINE; CANCER GROWTH; CHROMATIN; DOWN REGULATION; FLUORESCENCE IN SITU HYBRIDIZATION; GENE ACTIVITY; GENE AMPLIFICATION; GENE INTERACTION; GENE OVEREXPRESSION; GENE TARGETING; GENETIC TRANSFECTION; GROWTH DISORDER; HISTONE METHYLATION; HUMAN; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN BINDING; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SOMATIC MUTATION;

BREAST NEOPLASMS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; CELL LINEAGE; FEMALE; GENE AMPLIFICATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONES; HUMANS; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; MCF-7 CELLS; MUTATION; NUCLEAR PROTEINS; ONCOGENES; PROMOTER REGIONS, GENETIC; PYRAZOLES; PYRROLES; REPRESSOR PROTEINS; RNA, SMALL INTERFERING; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84902520020     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2014.04.024     Document Type: Article

References (55)

1. Almendro V., Cheng Y.K., Randles A., Itzkovitz S., Marusyk A., Ametller E., Gonzalez-Farre X., Munoz M., Russnes H.G., Helland A., et al. Inference of tumor evolution during chemotherapy by computational modeling and insitu analysis of genetic and phenotypic cellular diversity. Cell Rep. 2014, 6:514-527.
2. Bernardo G.M., Lozada K.L., Miedler J.D., Harburg G., Hewitt S.C., Mosley J.D., Godwin A.K., Korach K.S., Visvader J.E., Kaestner K.H., et al. FOXA1 is an essential determinant of ERalpha expression and mammary ductal morphogenesis. Development 2010, 137:2045-2054.
3. Bessarabova M., Pustovalova O., Shi W., Serebriyskaya T., Ishkin A., Polyak K., Velculescu V.E., Nikolskaya T., Nikolsky Y. Functional synergies yet distinct modulators affected by genetic alterations in common human cancers. Cancer Res. 2011, 71:3471-3481.
4. 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.
5. 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.
6. Ciriello G., Miller M.L., Aksoy B.A., Senbabaoglu Y., Schultz N., Sander C. Emerging landscape of oncogenic signatures across human cancers. Nat. Genet. 2013, 45:1127-1133.
7. Curtis C., Shah S.P., Chin S.F., Turashvili G., Rueda O.M., Dunning M.J., Speed D., Lynch A.G., Samarajiwa S., Yuan Y., et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 2012, 486:346-352. METABRIC Group.
8. Das P.P., Shao Z., Beyaz S., Apostolou E., Pinello L., Angeles A.D., O'Brien K., Atsma J.M., Fujiwara Y., Nguyen M., et al. Distinct and combinatorial functions of Jmjd2b/Kdm4b and Jmjd2c/Kdm4c in mouse embryonic stem cell identity. Mol. Cell 2014, 53:32-48.
9. Dawson M.A., Kouzarides T. Cancer epigenetics: from mechanism to therapy. Cell 2012, 150:12-27.
10. Delmore J.E., Issa G.C., Lemieux M.E., Rahl P.B., Shi J., Jacobs H.M., Kastritis E., Gilpatrick T., Paranal R.M., Qi J., et al. BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell 2011, 146:904-917.
11. Dey B.K., Stalker L., Schnerch A., Bhatia M., Taylor-Papidimitriou J., Wynder C. The histone demethylase KDM5b/JARID1b plays a role incell fate decisions by blocking terminal differentiation. Mol. Cell. Biol. 2008, 28:5312-5327.
12. Ellis M.J., Ding L., Shen D., Luo J., Suman V.J., Wallis J.W., Van Tine B.A., Hoog J., Goiffon R.J., Goldstein T.C., et al. Whole-genome analysis informs breast cancer response to aromatase inhibition. Nature 2012, 486:353-360.
13. Feng J., Meyer C.A., Wang Q., Liu J.S., Shirley Liu X., Zhang Y. GFOLD: a generalized fold change for ranking differentially expressed genes from RNA-seq data. Bioinformatics 2012, 28:2782-2788.
14. Filippakopoulos P., Qi J., Picaud S., Shen Y., Smith W.B., Fedorov O., Morse E.M., Keates T., Hickman T.T., Felletar I., et al. Selective inhibition of BET bromodomains. Nature 2010, 468:1067-1073.
15. Filippova G.N. Genetics and epigenetics of the multifunctional protein CTCF. Curr. Top. Dev. Biol. 2008, 80:337-360.
16. Fiorentino F.P., Giordano A. The tumor suppressor role of CTCF. J.Cell. Physiol. 2012, 227:479-492.
17. Frankenberg S., Smith L., Greenfield A., Zernicka-Goetz M. Novel gene expression patterns along the proximo-distal axis of the mouse embryo before gastrulation. BMC Dev. Biol. 2007, 7:8.
18. 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.
19. 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.
20. Kidder B.L., Hu G., Yu Z.X., Liu C., Zhao K. Extended self-renewal and accelerated reprogramming in the absence of Kdm5b. Mol. Cell. Biol. 2013, 33:4793-4810.
21. Kouros-Mehr H., Slorach E.M., Sternlicht M.D., Werb Z. GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland. Cell 2006, 127:1041-1055.
22. Kouros-Mehr H., Kim J.W., Bechis S.K., Werb Z. GATA-3 and the regulation of the mammary luminal cell fate. Curr. Opin. Cell Biol. 2008, 20:164-170.
23. Kristensen L.H., Nielsen A.L., Helgstrand C., Lees M., Cloos P., Kastrup J.S., Helin K., Olsen L., Gajhede M. Studies of H3K4me3 demethylation by KDM5B/Jarid1B/PLU1 reveals strong substrate recognition invitro and identifies 2,4-pyridine-dicarboxylic acid as an invitro and in cell inhibitor. FEBS J. 2012, 279:1905-1914.
24. Lee B.K., Bhinge A.A., Battenhouse A., McDaniell R.M., Liu Z., Song L., Ni Y., Birney E., Lieb J.D., Furey T.S., et al. Cell-type specific and combinatorial usage of diverse transcription factors revealed by genome-wide binding studies in multiple human cells. Genome Res. 2012, 22:9-24.
25. Li B., Carey M., Workman J.L. The role of chromatin during transcription. Cell 2007, 128:707-719.
26. Lopez-Bigas N., Kisiel T.A., Dewaal D.C., Holmes K.B., Volkert T.L., Gupta S., Love J., Murray H.L., Young R.A., Benevolenskaya E.V. Genome-wide analysis of the H3K4 histone demethylase RBP2 reveals a transcriptional program controlling differentiation. Mol. Cell 2008, 31:520-530.
27. Lu P.J., Sundquist K., Baeckstrom D., Poulsom R., Hanby A., Meier-Ewert S., Jones T., Mitchell M., Pitha-Rowe P., Freemont P., Taylor-Papadimitriou J. A novel gene (PLU-1) containing highly conserved putative DNA/chromatin binding motifs is specifically up-regulated in breast cancer. J.Biol. Chem. 1999, 274:15633-15645.
28. Nikolsky Y., Sviridov E., Yao J., Dosymbekov D., Ustyansky V., Kaznacheev V., Dezso Z., Mulvey L., Macconaill L.E., Winckler W., et al. Genome-wide functional synergy between amplified and mutated genes in human breast cancer. Cancer Res. 2008, 68:9532-9540.
29. Ooi S.K., Qiu C., Bernstein E., Li K., Jia D., Yang Z., Erdjument-Bromage H., Tempst P., Lin S.P., Allis C.D., et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 2007, 448:714-717.
30. Paredes S.H., Melgar M.F., Sethupathy P. Promoter proximal CTCF binding is associated with an increase in the transcriptional pausing index. Bioinformatics 2013, 29:1485-1487.
31. Parker J.S., Mullins M., Cheang M.C.U., Leung S., Voduc D., Vickery T., Davies S., Fauron C., He X., Hu Z., et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J.Clin. Oncol. 2009, 27:1160-1167.
32. Perou C.M., Sørlie T., Eisen M.B., van de Rijn M., Jeffrey S.S., Rees C.A., Pollack J.R., Ross D.T., Johnsen H., Akslen L.A., et al. Molecular portraits of human breast tumours. Nature 2000, 406:747-752.
33. Polyak K., Metzger Filho O. SnapShot: breast cancer. Cancer Cell 2012, 22:562-562.e561.
34. Ram O., Goren A., Amit I., Shoresh N., Yosef N., Ernst J., Kellis M., Gymrek M., Issner R., Coyne M., et al. Combinatorial patterning of chromatin regulators uncovered by genome-wide location analysis in human cells. Cell 2011, 147:1628-1639.
35. Roesch A., Becker B., Schneider-Brachert W., Hagen I., Landthaler M., Vogt T. Re-expression of the retinoblastoma-binding protein 2-homolog 1 reveals tumor-suppressive functions in highly metastatic melanoma cells. J.Invest. Dermatol. 2006, 126:1850-1859.
36. Roesch A., Mueller A.M., Stempfl T., Moehle C., Landthaler M., Vogt T. RBP2-H1/JARID1B is a transcriptional regulator with a tumor suppressive potential in melanoma cells. Int. J. Cancer 2008, 122:1047-1057.
37. 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.
38. Roesch A., Vultur A., Bogeski I., Wang H., Zimmermann K.M., Speicher D., Körbel C., Laschke M.W., Gimotty P.A., Philipp S.E., et al. Overcoming intrinsic multidrug resistance in melanoma by blocking the mitochondrial respiratory chain of slow-cycling JARID1B(high) cells. Cancer Cell 2013, 23:811-825.
39. Schmitz S.U., Albert M., Malatesta M., Morey L., Johansen J.V., Bak M., Tommerup N., Abarrategui I., Helin K. Jarid1b targets genes regulating development and is involved in neural differentiation. EMBO J. 2011, 30:4586-4600.
40. 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.
41. Shapiro I.M., Cheng A.W., Flytzanis N.C., Balsamo M., Condeelis J.S., Oktay M.H., Burge C.B., Gertler F.B. An EMT-driven alternative splicing program occurs in human breast cancer and modulates cellular phenotype. PLoS Genet. 2011, 7:e1002218.
42. Shipitsin M., Campbell L.L., Argani P., Weremowicz S., Bloushtain-Qimron N., Yao J., Nikolskaya T., Serebryiskaya T., Beroukhim R., Hu M., et al. Molecular definition of breast tumor heterogeneity. Cancer Cell 2007, 11:259-273.
43. Shukla S., Kavak E., Gregory M., Imashimizu M., Shutinoski B., Kashlev M., Oberdoerffer P., Sandberg R., Oberdoerffer S. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 2011, 479:74-79.
44. Siegel P.M., Muller W.J. Transcription factor regulatory networks in mammary epithelial development and tumorigenesis. Oncogene 2010, 29:2753-2759.
45. Sørlie T., Perou C.M., Tibshirani R., Aas T., Geisler S., Johnsen H., Hastie T., Eisen M.B., van de Rijn M., Jeffrey S.S., et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. USA 2001, 98:10869-10874.
46. Comprehensive molecular portraits of human breast tumours. Nature 2012, 490:61-70. TCGA.
47. Vaske C.J., Benz S.C., Sanborn J.Z., Earl D., Szeto C., Zhu J., Haussler D., Stuart J.M. Inference of patient-specific pathway activities from multi-dimensional cancer genomics data using PARADIGM. Bioinformatics 2010, 26:i237-i245.
48. 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.
49. Warzecha C.C., Carstens R.P. Complex changes in alternative pre-mRNA splicing play a central role in the epithelial-to-mesenchymal transition (EMT). Semin. Cancer Biol. 2012, 22:417-427.
50. Whyte W.A., Orlando D.A., Hnisz D., Abraham B.J., Lin C.Y., Kagey M.H., Rahl P.B., Lee T.I., Young R.A. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 2013, 153:307-319.
51. 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.
52. Xie L., Pelz C., Wang W., Bashar A., Varlamova O., Shadle S., Impey S. KDM5B regulates embryonic stem cell self-renewal and represses cryptic intragenic transcription. EMBO J. 2011, 30:1473-1484.
53. 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.
54. You J.S., Jones P.A. Cancer genetics and epigenetics: two sides of the same coin?. Cancer Cell 2012, 22:9-20.
55. Zhang Z., Pugh B.F. High-resolution genome-wide mapping of the primary structure of chromatin. Cell 2011, 144:175-186.