BAP1 deficiency causes loss of melanocytic cell identity in uveal melanoma

BMC Cancer

Volumn 13, Issue , 2013, Pages

  Matatall, Katie A ^a   Agapova, Olga A ^a   Onken, Michael D ^a   Worley, Lori A ^a   Bowcock, Anne M ^a   Harbour, J W ^a,b,c  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MIAMI   (United States)

Author keywords

BAP1; Differentiation; Metastasis; Stem cell; Tumor suppressor; Uveal melanoma

Indexed keywords

BRCA1 ASSOCIATED PROTEIN 1; BROXURIDINE; CELL MARKER; HYDROLASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAP1 GENE; CANCER CELL CULTURE; CANCER GROWTH; CARCINOGENICITY; CELL CYCLE CHECKPOINT; CELL DIFFERENTIATION; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; GENE LOSS; IN VITRO STUDY; MALE; MELANOCYTE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN DEPLETION; RNA INTERFERENCE; TUMOR INVASION; UVEA MELANOMA;

ANIMALS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CLUSTER ANALYSIS; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; HETEROGRAFTS; HOST CELL FACTOR C1; HUMANS; LIVER NEOPLASMS; MALE; MELANOCYTES; MELANOMA; MICE; NEOPLASTIC STEM CELLS; PHENOTYPE; PROTEIN BINDING; REPRODUCIBILITY OF RESULTS; RNA INTERFERENCE; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN THIOLESTERASE; UVEAL NEOPLASMS;

EID: 84881083031     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-13-371     Document Type: Article

References (35)

1. Onken MD, Worley LA, Ehlers JP, Harbour JW. Gene expression profiling in uveal melanoma reveals two molecular classes and predicts metastatic death. Cancer Res 2004, 64:7205-7209. 10.1158/0008-5472.CAN-04-1750, 15492234.
2. Onken MD, Worley LA, Char DH, Augsburger JJ, Correa ZM, Nudleman E, Aaberg TM, Altaweel MM, Bardenstein DS, Finger PT, et al. Collaborative Ocular Oncology Group report number 1: prospective validation of a multi-gene prognostic assay in uveal melanoma. Ophthalmol 2012, 119(8):1596-1603.
3. Harbour JW, Onken MD, Roberson ED, Duan S, Cao L, Worley LA, Council ML, Matatall KA, Helms C, Bowcock AM. Frequent mutation of BAP1 in metastasizing uveal melanomas. Sci 2010, 330(6009):1410-1413.
4. Bott M, Brevet M, Taylor BS, Shimizu S, Ito T, Wang L, Creaney J, Lake RA, Zakowski MF, Reva B, et al. The nuclear deubiquitinase BAP1 is commonly inactivated by somatic mutations and 3p21.1 losses in malignant pleural mesothelioma. Nat Genet 2011, 43:668-672. 10.1038/ng.855, 21642991.
5. Testa JR, Cheung M, Pei J, Below JE, Tan Y, Sementino E, Cox NJ, Dogan AU, Pass HI, Trusa S, et al. Germline BAP1 mutations predispose to malignant mesothelioma. Nat Genet 2011, 43(10):1022-1025. 10.1038/ng.912, 3184199, 21874000.
6. Wiesner T, Obenauf AC, Murali R, Fried I, Griewank KG, Ulz P, Windpassinger C, Wackernagel W, Loy S, Wolf I, et al. Germline mutations in BAP1 predispose to melanocytic tumors. Nat Genet 2011, 43(10):1018-1021. 10.1038/ng.910, 3328403, 21874003.
7. Abdel-Rahman MH, Pilarski R, Cebulla CM, Massengill JB, Christopher BN, Boru G, Hovland P, Davidorf FH. Germline BAP1 mutation predisposes to uveal melanoma, lung adenocarcinoma, meningioma, and other cancers. J Med Genet 2011, 48(12):856-859. 10.1136/jmedgenet-2011-100156, 21941004.
8. Njauw CN, Kim I, Piris A, Gabree M, Taylor M, Lane AM, Deangelis MM, Gragoudas E, Duncan LM, Tsao H. Germline BAP1 Inactivation Is Preferentially Associated with Metastatic Ocular Melanoma and Cutaneous-Ocular Melanoma Families. PLoS ONE 2012, 7(4). e-pub ahead of print 24 April 2012.
9. Pena-Llopis S, Vega-Rubin-de-Celis S, Liao A, Leng N, Pavia-Jimenez A, Wang S, Yamasaki T, Zhrebker L, Sivanand S, Spence P, et al. BAP1 loss defines a new class of renal cell carcinoma. Nat Genet 2012, e-pub ahead of print 10 June 2012.
10. Jensen DE, Proctor M, Marquis ST, Gardner HP, Ha SI, Chodosh LA, Ishov AM, Tommerup N, Vissing H, Sekido Y, et al. BAP1: a novel ubiquitin hydrolase which binds to the BRCA1 RING finger and enhances BRCA1-mediated cell growth suppression. Oncogene 1998, 16(9):1097-1112. 10.1038/sj.onc.1201861, 9528852.
11. Nishikawa H, Wu W, Koike A, Kojima R, Gomi H, Fukuda M, Ohta T. BRCA1-associated protein 1 interferes with BRCA1/BARD1 RING heterodimer activity. Cancer Res 2009, 69(1):111-119. 10.1158/0008-5472.CAN-08-3355, 19117993.
12. Yu H, Mashtalir N, Daou S, Hammond-Martel I, Ross J, Sui G, Hart GW, Rauscher FJ, Drobetsky E, Milot E, et al. The ubiquitin carboxyl hydrolase BAP1 forms a ternary complex with YY1 and HCF-1 and is a critical regulator of gene expression. Mol Cell Biol 2010, 30(21):5071-5085. 10.1128/MCB.00396-10, 2953049, 20805357.
13. Misaghi S, Ottosen S, Izrael-Tomasevic A, Arnott D, Lamkanfi M, Lee J, Liu J, O'Rourke K, Dixit VM, Wilson AC. Association of C-terminal ubiquitin hydrolase BRCA1-associated protein 1 with cell cycle regulator host cell factor 1. Mol Cell Biol 2009, 29(8):2181-2192. 10.1128/MCB.01517-08, 2663315, 19188440.
14. Scheuermann JC, de Ayala Alonso AG, Oktaba K, Ly-Hartig N, McGinty RK, Fraterman S, Wilm M, Muir TW, Muller J. Histone H2A deubiquitinase activity of the Polycomb repressive complex PR-DUB. Nat 2010, 465(7295):243-247.
15. Raaphorst FM. Deregulated expression of Polycomb-group oncogenes in human malignant lymphomas and epithelial tumors. Hum Mol Genet 2005, 14(Spec No 1):R93-R100.
16. Landreville S, Agapova OA, Matatall KA, Kneass ZT, Onken MD, Lee RS, Bowcock AM, Harbour JW. Histone deacetylase inhibitors induce growth arrest and differentiation in uveal melanoma. Clin Cancer Res 2012, 18(2):408-416. 10.1158/1078-0432.CCR-11-0946, 3261307, 22038994.
17. Dey A, Seshasayee D, Noubade R, French DM, Liu J, Chaurushiya MS, Kirkpatrick DS, Pham VC, Lill JR, Bakalarski CE, et al. Loss of the tumor suppressor BAP1 causes myeloid transformation. Sci 2012, 337(6101):1541-1546.
18. Sowa ME, Bennett EJ, Gygi SP, Harper JW. Defining the human deubiquitinating enzyme interaction landscape. Cell 2009, 138(2):389-403. 10.1016/j.cell.2009.04.042, 2716422, 19615732.
19. Griewank KG, Yu X, Khalili J, Sozen MM, Stempke-Hale K, Bernatchez C, Wardell S, Bastian BC, Woodman SE. Genetic and molecular characterization of uveal melanoma cell lines. Pigment Cell Melanoma Res 2012, 25(2):182-187. 10.1111/j.1755-148X.2012.00971.x, 3288394, 22236444.
20. Onken MD, Worley LA, Person E, Char DH, Bowcock AM, Harbour JW. Loss of heterozygosity of chromosome 3 detected with single nucleotide polymorphisms is superior to monosomy 3 for predicting metastasis in uveal melanoma. Clin Cancer Res 2007, 13(10):2923-2927. 10.1158/1078-0432.CCR-06-2383, 17504992.
21. Stewart SA, Dykxhoorn DM, Palliser D, Mizuno H, Yu EY, An DS, Sabatini DM, Chen IS, Hahn WC, Sharp PA, et al. Lentivirus-delivered stable gene silencing by RNAi in primary cells. RNA 2003, 9(4):493-501. 10.1261/rna.2192803, 1370415, 12649500.
22. Delston RB, Matatall KA, Sun Y, Onken MD, Harbour JW. p38 phosphorylates Rb on Ser567 by a novel, cell cycle-independent mechanism that triggers Rb-Hdm2 interaction and apoptosis. Oncogene 2011, 30(5):588-599. 10.1038/onc.2010.442, 3012146, 20871633.
23. Landreville S, Agapova OA, Kneass ZT, Salesse C, Harbour JW. ABCB1 identifies a subpopulation of uveal melanoma cells with high metastatic propensity. Pigment Cell Melanoma Res 2011, 24(3):430-437. 10.1111/j.1755-148X.2011.00841.x, 3096470, 21575142.
24. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001, 98(9):5116-5121. 10.1073/pnas.091062498, 33173, 11309499.
25. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstråle M, Laurila E, et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 2003, 34(3):267-273. 10.1038/ng1180, 12808457.
26. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 2005, 102(43):15545-15550. 10.1073/pnas.0506580102, 1239896, 16199517.
27. Machida YJ, Machida Y, Vashisht AA, Wohlschlegel JA, Dutta A. The deubiquitinating enzyme BAP1 regulates cell growth via interaction with HCF-1. J Biol Chem 2009, 284(49):34179-34188. 10.1074/jbc.M109.046755, 2797188, 19815555.
28. O'Hagan RC, Chang S, Maser RS, Mohan R, Artandi SE, Chin L, DePinho RA. Telomere dysfunction provokes regional amplification and deletion in cancer genomes. Cancer Cell 2002, 2(2):149-155. 10.1016/S1535-6108(02)00094-6, 12204535.
29. Xu X, Weaver Z, Linke SP, Li C, Gotay J, Wang XW, Harris CC, Ried T, Deng CX. Centrosome amplification and a defective G2-M cell cycle checkpoint induce genetic instability in BRCA1 exon 11 isoform-deficient cells. Mol Cell 1999, 3(3):389-395. 10.1016/S1097-2765(00)80466-9, 10198641.
30. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, Chen X, Bourque G, George J, Leong B, Liu J, et al. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 2006, 38(4):431-440. 10.1038/ng1760, 16518401.
31. Dejosez M, Levine SS, Frampton GM, Whyte WA, Stratton SA, Barton MC, Gunaratne PH, Young RA, Zwaka TP. Ronin/Hcf-1 binds to a hyperconserved enhancer element and regulates genes involved in the growth of embryonic stem cells. Genes Dev 2010, 24(14):1479-1484. 10.1101/gad.1935210, 2904937, 20581084.
32. Chang SH, Worley LA, Onken MD, Harbour JW. Prognostic biomarkers in uveal melanoma: evidence for a stem cell-like phenotype associated with metastasis. Melanoma Res 2008, 18(3):191-200. 10.1097/CMR.0b013e3283005270, 18477893.
33. Dantuma NP, Groothuis TA, Salomons FA, Neefjes J. A dynamic ubiquitin equilibrium couples proteasomal activity to chromatin remodeling. J Cell Biol 2006, 173(1):19-26. 10.1083/jcb.200510071, 2063781, 16606690.
34. Bergink S, Salomons FA, Hoogstraten D, Groothuis TA, de Waard H, Wu J, Yuan L, Citterio E, Houtsmuller AB, Neefjes J, et al. DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes Dev 2006, 20(10):1343-1352. 10.1101/gad.373706, 1472908, 16702407.
35. Ismail IH, Andrin C, McDonald D, Hendzel MJ. BMI1-mediated histone ubiquitylation promotes DNA double-strand break repair. J Cell Biol 2010, 191(1):45-60. 10.1083/jcb.201003034, 2953429, 20921134.