YAP-associated chromosomal instability and cholangiocarcinoma in mice

Oncotarget

Volumn 9, Issue 5, 2018, Pages 5892-5905

  Rizvi, Sumera ^a   Fischbach, Samantha R ^a   Bronk, Steven F ^a   Hirsova, Petra ^a,b,c   Krishnan, Anuradha ^a   Dhanasekaran, Renumathy ^d   Smadbeck, James B ^a   Smoot, Rory L ^a   Vasmatzis, George ^a   Gores, Gregory J ^a  

^a MAYO CLINIC   (United States)

^b UNIVERSITY HOSPITAL HRADEC KRALOVE   (Czech Republic)

^c CHARLES UNIVERSITY   (Czech Republic)

^d STANFORD UNIVERSITY   (United States)

Author keywords

Chromosomal instability; FOXM1; Mate pair sequencing; SB cell lines

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CYTOKERATIN 19; CYTOKERATIN 7; FORKHEAD BOX PROTEIN M1; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; SMALL INTERFERING RNA; THIOSTREPTON; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; YAP PROTEIN;

ANEUPLOIDY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT CARCINOMA; CANCER ASSOCIATED FIBROBLAST; CARCINOGENESIS; CELL DEATH; CHOLANGIOCARCINOMA CELL LINE; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; GENE EXPRESSION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; UPREGULATION;

EID: 85040645899     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.23638     Document Type: Article

References (35)

1. Rizvi S, Gores GJ. Pathogenesis, diagnosis, and management of cholangiocarcinoma. Gastroenterology. 2013; 145:1215-29. https://doi.org/10.1053/j.gastro.2013.10.013
2. Everhart JE, Ruhl CE. Burden of digestive diseases in the United States Part III: Liver, biliary tract, and pancreas. Gastroenterology. 2009; 136:1134-44. https://doi.org/10. 1053/j.gastro.2009.02.038
3. Farshidfar F, Zheng S, Gingras MC, Newton Y, Shih J, Robertson AG, Hinoue T, Hoadley KA, Gibb EA, Roszik J, Covington KR, Wu CC, Shinbrot E, et al, and Cancer Genome Atlas Network. Integrative Genomic Analysis of Cholangiocarcinoma Identifies Distinct IDH-Mutant Molecular Profiles. Cell Reports. 2017; 19:2878-80
4. Johnson R, Halder G. The two faces of Hippo: targeting the Hippo pathway for regenerative medicine and cancer treatment. Nat Rev Drug Discov. 2014; 13:63-79. https:// doi.org/10.1038/nrd4161
5. Li H, Wolfe A, Septer S, Edwards G, Zhong X, Abdulkarim AB, Ranganathan S, Apte U. Deregulation of Hippo kinase signalling in human hepatic malignancies. Liver Int. 2012; 32:38-47. https://doi. org/10.1111/j.1478-3231.2011.02646.x
6. Perra A, Kowalik MA, Ghiso E, Ledda-Columbano GM, Di Tommaso L, Angioni MM, Raschioni C, Testore E, Roncalli M, Giordano S, Columbano A. YAP activation is an early event and a potential therapeutic target in liver cancer development. J Hepatol. 2014; 61:1088-96. https:// doi.org/10.1016/j.jhep.2014.06.033
7. Rizvi S, Yamada D, Hirsova P, Bronk SF, Werneburg NW, Krishnan A, Salim W, Zhang L, Trushina E, Truty MJ, Gores GJ. A Hippo and Fibroblast Growth Factor Receptor Autocrine Pathway in Cholangiocarcinoma. J Biol Chem. 2016; 291:8031-47. https://doi.org/10.1074/ jbc.M115.698472
8. Zender L, Spector MS, Xue W, Flemming P, Cordon-Cardo C, Silke J, Fan ST, Luk JM, Wigler M, Hannon GJ, Mu D, Lucito R, Powers S, et al. Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach. Cell. 2006; 125:1253-67. https:// doi.org/10.1016/j.cell.2006.05.030
9. Li X, Tao J, Cigliano A, Sini M, Calderaro J, Azoulay D, Wang C, Liu Y, Jiang L, Evert K, Demartis MI, Ribback S, Utpatel K, et al. Co-activation of PIK3CA and Yap promotes development of hepatocellular and cholangiocellular tumors in mouse and human liver. Oncotarget. 2015; 6:10102-15. https://doi.org/10.18632/oncotarget.3546
10. Marti P, Stein C, Blumer T, Abraham Y, Dill MT, Pikiolek M, Orsini V, Jurisic G, Megel P, Makowska Z, Agarinis C, Tornillo L, Bouwmeester T, et al. YAP promotes proliferation, chemoresistance, and angiogenesis in human cholangiocarcinoma through TEAD transcription factors. Hepatology. 2015; 62:1497-510. https://doi.org/10.1002/ hep.27992
11. Pei T, Li Y, Wang J, Wang H, Liang Y, Shi H, Sun B, Yin D, Sun J, Song R, Pan S, Sun Y, Jiang H, et al. YAP is a critical oncogene in human cholangiocarcinoma. Oncotarget. 2015; 6:17206-20. https://doi.org/10.18632/oncotarget.4043
12. Yamada D, Rizvi S, Razumilava N, Bronk SF, Davila JI, Champion MD, Borad MJ, Bezerra JA, Chen X, Gores GJ. IL-33 facilitates oncogene-induced cholangiocarcinoma in mice by an interleukin-6-sensitive mechanism. Hepatology. 2015; 61:1627-42. https://doi.org/10.1002/hep.27687
13. Carter SL, Eklund AC, Kohane IS, Harris LN, Szallasi Z. A signature of chromosomal instability inferred from gene expression profiles predicts clinical outcome in multiple human cancers. Nat Genet. 2006; 38:1043-8. https://doi. org/10.1038/ng1861
14. Thompson SL, Bakhoum SF, Compton DA. Mechanisms of chromosomal instability. Curr Biol. 2010; 20:R285-95. https://doi.org/10.1016/j.cub.2010.01.034
15. Weiler SME, Pinna F, Wolf T, Lutz T, Geldiyev A, Sticht C, Knaub M, Thomann S, Bissinger M, Wan S, Rossler S, Becker D, Gretz N, et al. Induction of Chromosome Instability by Activation of Yes-Associated Protein and Forkhead Box M1 in Liver Cancer. Gastroenterology. 2017; 152:2037-51.e22. https://doi.org/10.1053/j. gastro.2017.02.018
16. Zhang S, Chen Q, Liu Q, Li Y, Sun X, Hong L, Ji S, Liu C, Geng J, Zhang W, Lu Z, Yin ZY, Zeng Y, et al. Hippo Signaling Suppresses Cell Ploidy and Tumorigenesis through Skp2. Cancer Cell. 2017; 31:669-84.e7. https:// doi.org/10.1016/j.ccell.2017.04.004
17. Drucker TM, Johnson SH, Murphy SJ, Cradic KW, Therneau TM, Vasmatzis G. BIMA V3: an aligner customized for mate pair library sequencing. Bioinformatics. 2014; 30:1627-9. https://doi.org/10.1093/ bioinformatics/btu078
18. Baca SC, Prandi D, Lawrence MS, Mosquera JM, Romanel A, Drier Y, Park K, Kitabayashi N, MacDonald TY, Ghandi M, Van Allen E, Kryukov GV, Sboner A, et al. Punctuated evolution of prostate cancer genomes. Cell. 2013; 153:666-77. https://doi.org/10.1016/j.cell.2013.03.021
19. Shen MM. Chromoplexy: a new category of complex rearrangements in the cancer genome. Cancer Cell. 2013; 23:567-9. https://doi.org/10.1016/j.ccr.2013.04.025
20. Yang C, Chen H, Yu L, Shan L, Xie L, Hu J, Chen T, Tan Y. Inhibition of FOXM1 transcription factor suppresses cell proliferation and tumor growth of breast cancer. Cancer Gene Ther. 2013; 20:117-24. https://doi.org/10.1038/ cgt.2012.94
21. Kwok JM, Myatt SS, Marson CM, Coombes RC, Constantinidou D, Lam EW. Thiostrepton selectively targets breast cancer cells through inhibition of forkhead box M1 expression. Mol Cancer Ther. 2008; 7:2022-32. https://doi. org/10.1158/1535-7163.MCT-08-0188
22. Wang IC, Chen YJ, Hughes D, Petrovic V, Major ML, Park HJ, Tan Y, Ackerson T, Costa RH. Forkhead box M1 regulates the transcriptional network of genes essential for mitotic progression and genes encoding the SCF (Skp2-Cks1) ubiquitin ligase. Mol Cell Biol. 2005; 25:10875-94. https://doi.org/10.1128/MCB.25.24.10875-10894.2005
23. Laoukili J, Kooistra MR, Bras A, Kauw J, Kerkhoven RM, Morrison A, Clevers H, Medema RH. FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat Cell Biol. 2005; 7:126-36. https://doi. org/10.1038/ncb1217
24. Korver W, Roose J, Clevers H. The winged-helix transcription factor Trident is expressed in cycling cells. Nucleic Acids Res. 1997; 25:1715-9. https://doi.org/10
25. Laoukili J, Stahl M, Medema RH. FoxM1: at the crossroads of ageing and cancer. Biochim Biophys Acta. 2007; 1775:92-102. https://doi.org/10.1016/j.bbcan.2006.08.006
26. Kalin TV, Ustiyan V, Kalinichenko VV. Multiple faces of FoxM1 transcription factor: lessons from transgenic mouse models. Cell Cycle. 2011; 10:396-405. https://doi. org/10.4161/cc.10.3.14709
27. Halasi M, Gartel AL. FOX(M1) news-it is cancer. Mol Cancer Ther. 2013; 12:245-54. https://doi. org/10.1158/1535-7163.MCT-12-0712
28. Gartel AL. FOXM1 in Cancer: Interactions and Vulnerabilities. Cancer Res. 2017; 77:3135-9. https://doi. org/10.1158/0008-5472.CAN-16-3566
29. Yahagi K, Ishii M, Kobayashi K, Ueno Y, Mano Y, Niitsuma H, Igarashi T, Toyota T. Primary culture of cholangiocytes from normal mouse liver. In Vitro Cell Dev Biol Anim. 1998; 34:512-4. https://doi.org/10.1007/ s11626-998-0106-x
30. Mott JL, Bronk SF, Mesa RA, Kaufmann SH, Gores GJ. BH3-only protein mimetic obatoclax sensitizes cholangiocarcinoma cells to Apo2L/TRAIL-induced apoptosis. Mol Cancer Ther. 2008; 7:2339-47. https://doi. org/10.1158/1535-7163.MCT-08-0285
31. Kalari KR, Nair AA, Bhavsar JD, O'Brien DR, Davila JI, Bockol MA, Nie J, Tang X, Baheti S, Doughty JB, Middha S, Sicotte H, Thompson AE, et al. MAP-RSeq: Mayo Analysis Pipeline for RNA sequencing. BMC Bioinformatics. 2014; 15:224. https://doi.org/10.1186/1471-2105-15-224
32. Wang L, Wang S, Li W. RSeQC: quality control of RNAseq experiments. Bioinformatics. 2012; 28:2184-5. https:// doi.org/10.1093/bioinformatics/bts356
33. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009; 25:1105-11. https://doi.org/10.1093/bioinformatics/btp120
34. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009; 10:R25. https://doi. org/10.1186/gb-2009-10-3-r25
35. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010; 26:139-40. https://doi.org/10.1093/bioinformatics/btp616