The Emerging Role of Chromatin Remodeling Complexes in Ovarian Cancer
Abstract
:1. Introduction
1.1. Ovarian Cancer Types and Mutations
1.2. Chromatin Remodelers and Their Functions in Human Cancer
1.2.1. SWI/SNF Complex Members and Functions
1.2.2. ISWI Complex Members and Functions
1.2.3. CHD Family Remodelers
1.2.4. INO80 Family
2. Alterations of Chromatin Remodeler Complexes in Ovarian Cancer
2.1. ARID1A Alterations in Ovarian Cancer
2.2. Other SWI/SNF Alterations in Ovarian Cancer
2.3. ISWI Alterations in Ovarian Cancer
2.4. CHD Family Alterations in Ovarian Cancer
2.5. INO80 in Ovarian Cancer
3. Conclusions and Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
CRC | Chromatin remodeling complex |
DDR | DNA damage response |
DSB | Double-stranded break |
HGSOC | High-grade ovarian cancer |
HR | Homologous recombination |
NER | Nucleotide excision repair |
NHEJ | Non-homologous DNA end joining |
OC | Ovarian cancer |
OCCC | Ovarian clear cell carcinoma |
ROS | Reactive oxygen species |
SCCOHT | Small cell ovarian carcinoma, hypercalcemic type |
References
- Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J. Clin. 2021, 71, 209–249. [Google Scholar] [CrossRef]
- Siegel, R.L.; Miller, K.D.; Fuchs, H.E.; Jemal, A. Cancer statistics, 2022. CA Cancer J. Clin. 2022, 72, 7–33. [Google Scholar] [CrossRef]
- Testa, U.; Petrucci, E.; Pasquini, L.; Castelli, G.; Pelosi, E. Ovarian Cancers: Genetic Abnormalities, Tumor Heterogeneity and Progression, Clonal Evolution and Cancer Stem Cells. Medicines 2018, 5, 16. [Google Scholar] [CrossRef] [Green Version]
- Colombo, N.; Preti, E.; Landoni, F.; Carinelli, S.; Colombo, A.; Marini, C.; Sessa, C. Endometrial cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 2013, 24, vi33–vi38. [Google Scholar] [CrossRef]
- Matulonis, U.A.; Sood, A.K.; Fallowfield, L.; Howitt, B.E.; Sehouli, J.; Karlan, B.Y. Ovarian cancer. Nat. Rev. Dis. Prim. 2016, 2, 1–22. [Google Scholar] [CrossRef]
- Colombo, N.; Sessa, C.; Bois, A.D.; Ledermann, J.; McCluggage, W.G.; McNeish, I.; Morice, P.; Pignata, S.; Ray-Coquard, I.; Vergote, I.; et al. ESMO-ESGO consensus conference recommendations on ovarian cancer: Pathology and molecular biology, early and advanced stages, borderline tumours and recurrent disease. Ann. Oncol. 2019, 30, 672–705. [Google Scholar] [CrossRef] [Green Version]
- Hollis, R.L.; Gourley, C. Genetic and molecular changes in ovarian cancer. Cancer Biol. Med. 2016, 13, 236–247. [Google Scholar] [CrossRef] [Green Version]
- Kurman, R.J.; Shih, I.M. The dualistic model of ovarian carcinogenesis revisited, revised, and expanded. Am. J. Pathol. 2016, 186, 733–747. [Google Scholar] [CrossRef] [Green Version]
- Salazar, C.; Campbell, I.G.; Gorringe, K.L. When Is “type I” Ovarian Cancer Not “type I”? Indications of an Out-Dated Dichotomy. Front. Oncol. 2018, 8, 654. [Google Scholar] [CrossRef]
- Iijima, M.; Banno, K.; Okawa, R.; Yanokura, M.; Iida, M.; Takeda, T.; Kunitomi-Irie, H.; Adachi, M.; Nakamura, K.; Umene, K.; et al. Genome-wide analysis of gynecologic cancer: The Cancer Genome Atlas in ovarian and endometrial cancer. Oncol. Lett. 2017, 13, 1063–1070. [Google Scholar] [CrossRef]
- Liu, G.; Yang, D.; Sun, Y.; Shmulevich, I.; Xue, F.; Sood, A.K.; Zhang, W. Differing clinical impact of BRCA1 and BRCA2 mutations in serous ovarian cancer. Pharmacogenomics 2012, 13, 1523–1535. [Google Scholar] [CrossRef] [Green Version]
- Zhang, S.; Royer, R.; Li, S.; McLaughlin, J.R.; Rosen, B.; Risch, H.A.; Fan, I.; Bradley, L.; Shaw, P.A.; Narod, S.A. Frequencies of BRCA1 and BRCA2 mutations among 1,342 unselected patients with invasive ovarian cancer. Gynecol. Oncol. 2011, 121, 353–357. [Google Scholar] [CrossRef] [PubMed]
- Toss, A.; Tomasello, C.; Razzaboni, E.; Contu, G.; Grandi, G.; Cagnacci, A.; Schilder, R.J.; Cortesi, L. Hereditary ovarian cancer: Not only BRCA 1 and 2 Genes. BioMed Res. Int. 2015, 2015, 341723. [Google Scholar] [CrossRef] [Green Version]
- Wang, S.; Vogirala, V.K.; Soman, A.; Berezhnoy, N.V.; Liu, Z.B.; Wong, A.S.; Korolev, N.; Su, C.J.; Sandin, S.; Nordenskiöld, L. Linker histone defines structure and self-association behaviour of the 177 bp human chromatosome. Sci. Rep. 2021, 11, 380. [Google Scholar] [CrossRef]
- Cutter, A.R.; Hayes, J.J. A brief review of nucleosome structure. FEBS Lett. 2015, 589, 2914–2922. [Google Scholar] [CrossRef] [Green Version]
- Clapier, C.R.; Iwasa, J.; Cairns, B.R.; Peterson, C.L. Mechanisms of action and regulation of ATP-dependent chromatin-remodelling complexes. Nat. Rev. Mol. Cell Biol. 2017, 18, 407–422. [Google Scholar] [CrossRef]
- Magaña-Acosta, M.; Valadez-Graham, V. Chromatin Remodelers in the 3D Nuclear Compartment. Front. Genet. 2020, 11, 600615. [Google Scholar] [CrossRef]
- Längst, G.; Manelyte, L. Chromatin remodelers: From function to dysfunction. Genes 2015, 6, 299–324. [Google Scholar] [CrossRef] [Green Version]
- Sahu, R.K.; Singh, S.; Tomar, R.S. The mechanisms of action of chromatin remodelers and implications in development and disease. Biochem. Pharmacol. 2020, 180, 114200. [Google Scholar] [CrossRef]
- Giles, K.A.; Gould, C.M.; Du, Q.; Skvortsova, K.; Song, J.Z.; Maddugoda, M.P.; Achinger-Kawecka, J.; Stirzaker, C.; Clark, S.J.; Taberlay, P.C. Integrated epigenomic analysis stratifies chromatin remodellers into distinct functional groups. Epigenetics Chromatin 2019, 12, 12. [Google Scholar] [CrossRef]
- Stern, M.; Jensen, R.; Herskowitz, I. Five SWI genes are required for expression of the HO gene in yeast. J. Mol. Biol. 1984, 178, 853–868. [Google Scholar] [CrossRef]
- Wu, J.N.; Roberts, C.W. ARID1A mutations in cancer: Another epigenetic tumor suppressor? Cancer Discov. 2013, 3, 35–43. [Google Scholar] [CrossRef] [Green Version]
- Alpsoy, A.; Dykhuizen, E.C. Glioma tumor suppressor candidate region gene 1 (GLTSCR1) and its paralog GLTSCR1-like form SWI/SNF chromatin remodeling subcomplexes. J. Biol. Chem. 2018, 293, 3892–3903. [Google Scholar] [CrossRef] [Green Version]
- Centore, R.C.; Sandoval, G.J.; Soares, L.M.M.; Kadoch, C.; Chan, H.M. Mammalian SWI/SNF Chromatin Remodeling Complexes: Emerging Mechanisms and Therapeutic Strategies. Trends Genet. 2020, 36, 936–950. [Google Scholar] [CrossRef]
- Michel, B.C.; D’Avino, A.R.; Cassel, S.H.; Mashtalir, N.; McKenzie, Z.M.; McBride, M.J.; Valencia, A.M.; Zhou, Q.; Bocker, M.; Soares, L.M.; et al. A non-canonical SWI/SNF complex is a synthetic lethal target in cancers driven by BAF complex perturbation. Nat. Cell Biol. 2018, 20, 1410–1420. [Google Scholar] [CrossRef]
- Erdel, F.; Schubert, T.; Marth, C.; Längst, G.; Rippe, K. Human ISWI chromatin-remodeling complexes sample nucleosomes via transient binding reactions and become immobilized at active sites. Proc. Natl. Acad. Sci. USA 2010, 107, 19873–19878. [Google Scholar] [CrossRef] [Green Version]
- Li, Y.; Gong, H.; Wang, P.; Zhu, Y.; Peng, H.; Cui, Y.; Li, H.; Liu, J.; Wang, Z. The emerging role of ISWI chromatin remodeling complexes in cancer. J. Exp. Clin. Cancer Res. 2021, 40, 346. [Google Scholar] [CrossRef]
- Erdel, F.; Rippe, K. Chromatin remodelling in mammalian cells by ISWI-type complexes - Where, when and why? FEBS J. 2011, 278, 3608–3618. [Google Scholar] [CrossRef]
- Li, W.; Mills, A.A. Architects of the genome: CHD dysfunction in cancer, developmental disorders and neurological syndromes. Epigenomics 2014, 6, 381–395. [Google Scholar] [CrossRef] [Green Version]
- Tyagi, M.; Imam, N.; Verma, K.; Patel, A.K. Chromatin remodelers: We are the drivers!! Nucleus 2016, 7, 388–404. [Google Scholar] [CrossRef]
- Lai, A.Y.; Wade, P.A. Cancer biology and NuRD: A multifaceted chromatin remodelling complex. Nat. Rev. Cancer 2011, 11, 588–596. [Google Scholar] [CrossRef]
- Stanley, C.E.; Kulathinal, R.J. Genomic signatures of domestication on neurogenetic genes in Drosophila melanogaster. BMC Evol. Biol. 2016, 16, 6. [Google Scholar] [CrossRef] [Green Version]
- Kolla, V.; Naraparaju, K.; Zhuang, T.; Higashi, M.; Kolla, S.; Blobel, G.A.; Brodeur, G.M. The tumour suppressor CHD5 forms a NuRD-type chromatin remodelling complex. Biochem. J. 2015, 468, 345–352. [Google Scholar] [CrossRef] [Green Version]
- Bagchi, A.; Papazoglu, C.; Wu, Y.; Capurso, D.; Brodt, M.; Francis, D.; Bredel, M.; Vogel, H.; Mills, A.A. CHD5 Is a Tumor Suppressor at Human 1p36. Cell 2007, 128, 459–475. [Google Scholar] [CrossRef] [Green Version]
- Mallette, F.A.; Richard, S. JMJD2A Promotes Cellular Transformation by Blocking Cellular Senescence through Transcriptional Repression of the Tumor Suppressor CHD5. Cell Rep. 2012, 2, 1233–1243. [Google Scholar] [CrossRef] [Green Version]
- Hall, W.A.; Petrova, A.V.; Colbert, L.E.; Hardy, C.W.; Fisher, S.B.; Saka, B.; Shelton, J.W.; Warren, M.D.; Pantazides, B.G.; Gandhi, K.; et al. Low CHD5 expression activates the DNA damage response and predicts poor outcome in patients undergoing adjuvant therapy for resected pancreatic cancer. Oncogene 2014, 33, 5450–5456. [Google Scholar] [CrossRef]
- Ebbert, R.; Birkmann, A.; Schüller, H.J. The product of the SNF2/SWI2 paralogue INO80 of Saccharomyces cerevisiae required for efficient expression of various yeast structural genes is part of a high-molecular-weight protein complex. Mol. Microbiol. 1999, 32, 741–751. [Google Scholar] [CrossRef]
- Morrison, A.J.; Shen, X. Chromatin remodelling beyond transcription: The INO80 and SWR1 complexes. Nat. Rev. Mol. Cell Biol. 2009, 10, 373–384. [Google Scholar] [CrossRef]
- Willhoft, O.; Wigley, D.B. INO80 and SWR1 complexes: The non-identical twins of chromatin remodelling. Curr. Opin. Struct. Biol. 2020, 61, 50–58. [Google Scholar] [CrossRef]
- Poli, J.; Gasser, S.M.; Papamichos-Chronakis, M. The INO80 remodeller in transcription, replication and repair. Philos. Trans. R. Soc. B Biol. Sci. 2017, 372. [Google Scholar] [CrossRef]
- Mittal, P.; Roberts, C.W. The SWI/SNF complex in cancer—Biology, Biomarkers and Therapy. Nat. Rev. Clin. Oncol. 2020, 17, 435–448. [Google Scholar] [CrossRef] [PubMed]
- Xu, S.; Tang, C. The Role of ARID1A in Tumors: Tumor Initiation or Tumor Suppression? Front. Oncol. 2021, 11, 745187. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Hoang, L.; Ji, J.X.; Huntsman, D.G. SWI/SNF Complex Mutations in Gynecologic Cancers: Molecular Mechanisms and Models. Annu. Rev. Pathol. Mech. Dis. 2020, 15, 467–492. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Suda, K.; Nakaoka, H.; Yoshihara, K.; Ishiguro, T.; Tamura, R.; Mori, Y.; Yamawaki, K.; Adachi, S.; Takahashi, T.; Kase, H.; et al. Clonal Expansion and Diversification of Cancer-Associated Mutations in Endometriosis and Normal Endometrium. Cell Rep. 2018, 24, 1777–1789. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zou, Y.; Zhou, J.Y.; Guo, J.B.; Wang, L.Q.; Luo, Y.; Zhang, Z.Y.; Liu, F.Y.; Tan, J.; Wang, F.; Huang, O.P. The presence of KRAS, PPP2R1A and ARID1A mutations in 101 Chinese samples with ovarian endometriosis. Mutat. Res. Fundam. Mol. Mech. Mutagen. 2018, 809, 1–5. [Google Scholar] [CrossRef]
- Mcconechy, M.K.; Ding, J.; Cheang, M.C.U.; Wiegand, K.; Tone, A.; Yang, W.; Prentice, L.; Tse, K.; Zeng, T.; Schmidt, A.P.; et al. Use of mutation profiles to refine the classification of endometrial carcinomas. J. Pathol. 2012, 228, 20–30. [Google Scholar] [CrossRef] [Green Version]
- Cherniack, A.D.; Shen, H.; Walter, V.; Stewart, C.; Murray, B.A.; Bowlby, R.; Hu, X.; Ling, S.; Soslow, R.A.; Broaddus, R.R.; et al. Integrated Molecular Characterization of Uterine Carcinosarcoma. Cancer Cell 2017, 31, 411–423. [Google Scholar] [CrossRef] [Green Version]
- Wiegand, K.C.; Shah, S.P.; Al-Agha, O.M.; Zhao, Y.; Al, E. ARID1A Mutations in Endometriosis-Associated Ovarian Carcinomas. N. Engl. J. Med. 2010, 363, 1532–1543. [Google Scholar] [CrossRef] [Green Version]
- Guan, B.; Wang, T.L.; Shih, I.M. ARID1A, a factor that promotes formation of SWI/SNF-mediated chromatin remodeling, is a tumor suppressor in gynecologic cancers. Cancer Res. 2011, 71, 6718–6727. [Google Scholar] [CrossRef] [Green Version]
- Cuevas, D.; Valls, J.; Gatius, S.; Roman-Canal, B.; Estaran, E.; Dorca, E.; Santacana, M.; Vaquero, M.; Eritja, N.; Velasco, A.; et al. Targeted sequencing with a customized panel to assess histological typing in endometrial carcinoma. Virchows Arch. 2019, 474, 585–598. [Google Scholar] [CrossRef]
- Hollis, R.L.; Thomson, J.P.; Stanley, B.; Churchman, M.; Meynert, A.M.; Rye, T.; Bartos, C.; Iida, Y.; Croy, I.; Mackean, M.; et al. Molecular stratification of endometrioid ovarian carcinoma predicts clinical outcome. Nat. Commun. 2020, 11, 4995. [Google Scholar] [CrossRef]
- Kuroda, Y.; Chiyoda, T.; Kawaida, M.; Nakamura, K.; Aimono, E.; Yoshimura, T.; Takahashi, M.; Saotome, K.; Yoshihama, T.; Iwasa, N.; et al. ARID1A mutation/ARID1A loss is associated with a high immunogenic profile in clear cell ovarian cancer. Gynecol. Oncol. 2021, 162, 679–685. [Google Scholar] [CrossRef]
- Teer, J.K.; Yoder, S.; Gjyshi, A.; Nicosia, S.V.; Zhang, C.; Alvaro, N.; Monteiro, A. Mutational heterogeneity in non- serous ovarian cancers. Sci. Rep. 2017, 7, 9728. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lapke, N.; Chen, C.H.; Chang, T.C.; Chao, A.; Lu, Y.J.; Lai, C.H.; Tan, K.T.; Chen, H.C.; Lu, H.Y.; Chen, S.J. Genetic alterations and their therapeutic implications in epithelial ovarian cancer. BMC Cancer 2021, 21, 499. [Google Scholar] [CrossRef] [PubMed]
- Eoh, K.J.; Kim, H.M.; Lee, J.Y.; Kim, S.; Kim, S.W.; Kim, Y.T.; Nam, E.J. Mutation landscape of germline and somatic BRCA1/2 in patients with high-grade serous ovarian cancer. BMC Cancer 2020, 20, 204. [Google Scholar] [CrossRef]
- Cheasley, D.; Nigam, A.; Zethoven, M.; Hunter, S.; Etemadmoghadam, D.; Semple, T.; Allan, P.; Carey, M.S.; Fernandez, M.L.; Dawson, A.; et al. Genomic analysis of low-grade serous ovarian carcinoma to identify key drivers and therapeutic vulnerabilities. J. Pathol. 2021, 253, 41–54. [Google Scholar] [CrossRef]
- Yachida, N.; Yoshihara, K.; Suda, K.; Nakaoka, H.; Ueda, H.; Sugino, K.; Yamaguchi, M.; Mori, Y.; Yamawaki, K.; Tamura, R.; et al. ARID1A protein expression is retained in ovarian endometriosis with ARID1A loss-of-function mutations: Implication for the two-hit hypothesis. Sci. Rep. 2020, 10, 14260. [Google Scholar] [CrossRef]
- Jones, S.; Wang, T.L.; Shih, I.M.; Mao, T.L.; Nakayama, K.; Roden, R.; Glas, R.; Slamon, D.; Diaz, L.A.; Vogelstein, B.; et al. Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma. Science 2010, 330, 228–231. [Google Scholar] [CrossRef] [Green Version]
- Wu, R.C.; Chen, S.J.; Chen, H.C.; Tan, K.T.; Jung, S.M.; Lin, C.Y.; Chao, A.S.; Huang, K.G.; Chou, H.H.; Chang, T.C.; et al. Comprehensive genomic profiling reveals ubiquitous KRAS mutations and frequent PIK3CA mutations in ovarian seromucinous borderline tumor. Mod. Pathol. 2020, 33, 2534–2543. [Google Scholar] [CrossRef]
- Heinze, K.; Nazeran, T.M.; Lee, S.; Krämer, P.; Cairns, E.S.; Chiu, D.S.; Leung, S.C.; Kang, E.Y.; Meagher, N.S.; Kennedy, C.J.; et al. Prognostic and Immunological Significance of ARID1A Status in Endometriosis-Associated Ovarian Carcinoma Short title: Significance of ARID1A Status in EAOC Authors. medRxiv 2021. [Google Scholar] [CrossRef]
- Shen, J.; Ju, Z.; Zhao, W.; Wang, L.; Peng, Y.; Ge, Z.; Nagel, Z.D.; Zou, J.; Wang, C.; Kapoor, P.; et al. ARID1A deficiency promotes mutability and potentiates therapeutic antitumor immunity unleashed by immune checkpoint blockade. Nat. Med. 2018, 24, 556–562. [Google Scholar] [CrossRef] [PubMed]
- Guan, B.; Rahmanto, Y.S.; Wu, R.C.; Wang, Y.; Wang, Z.; Wang, T.L.; Shih, I.M. Roles of deletion of Arid1a, a tumor suppressor, in mouse ovarian tumorigenesis. J. Natl. Cancer Inst. 2014, 106, dju146. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alver, B.H.; Kim, K.H.; Lu, P.; Wang, X.; Manchester, H.E.; Wang, W.; Haswell, J.R.; Park, P.J.; Roberts, C.W. The SWI/SNF chromatin remodelling complex is required for maintenance of lineage specific enhancers. Nat. Commun. 2017, 8, 14648. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Trizzino, M.; Barbieri, E.; Petracovici, A.; Wu, S.; Welsh, S.A.; Owens, T.A.; Licciulli, S.; Zhang, R.; Gardini, A. The Tumor Suppressor ARID1A Controls Global Transcription via Pausing of RNA Polymerase II. Cell Rep. 2018, 23, 3933–3945. [Google Scholar] [CrossRef]
- Bitler, B.G.; Wu, S.; Park, P.H.; Hai, Y.; Aird, K.M.; Wang, Y.; Zhai, Y.; Kossenkov, A.V.; Vara-Ailor, A.; Rauscher, F.J.; et al. ARID1A-mutated ovarian cancers depend on HDAC6 activity. Nat. Cell Biol. 2017, 19, 962–973. [Google Scholar] [CrossRef] [Green Version]
- Caumanns, J.J.; Wisman, G.B.A.; Berns, K.; van der Zee, A.G.; de Jong, S. ARID1A mutant ovarian clear cell carcinoma: A clear target for synthetic lethal strategies. Biochim. Biophys. Acta Rev. Cancer 2018, 1870, 176–184. [Google Scholar] [CrossRef]
- Miller, R.E.; Brough, R.; Bajrami, I.; Williamson, C.T.; McDade, S.; Campbell, J.; Kigozi, A.; Rafiq, R.; Pemberton, H.; Natrajan, R.; et al. Synthetic lethal targeting of ARID1A-Mutant ovarian clear cell tumors with dasatinib. Mol. Cancer Ther. 2016, 15, 1472–1484. [Google Scholar] [CrossRef] [Green Version]
- Zhao, B.; Lin, J.; Rong, L.; Wu, S.; Deng, Z.; Fatkhutdinov, N.; Zundell, J.; Fukumoto, T.; Liu, Q.; Kossenkov, A.; et al. ARID1A promotes genomic stability through protecting telomere cohesion. Nat. Commun. 2019, 10, 4067. [Google Scholar] [CrossRef] [Green Version]
- Dykhuizen, E.C.; Hargreaves, D.C.; Miller, E.L.; Cui, K.; Korshunov, A.; Kool, M.; Pfister, S.; Cho, Y.J.; Zhao, K.; Crabtree, G.R. BAF complexes facilitate decatenation of DNA by topoisomerase IIα. Nature 2013, 497, 624–627. [Google Scholar] [CrossRef] [Green Version]
- Tsai, S.; Fournier, L.A.; Chang, E.Y.C.; Wells, J.P.; Minaker, S.W.; Zhu, Y.D.; Wang, A.Y.H.; Wang, Y.; Huntsman, D.G.; Stirling, P.C. ARID1A regulates R-loop associated DNA replication stress. PLoS Genet. 2021, 17, e1009238. [Google Scholar] [CrossRef]
- Rahmanto, Y.S.; Jung, J.G.; Wu, R.C.; Kobayashi, Y.; Heaphy, C.M.; Meeker, A.K.; Wang, T.L.; Shih, I.M. Inactivating ARID1A tumor suppressor enhances TERT transcription and maintains telomere length in cancer cells. J. Biol. Chem. 2016, 291, 9690–9699. [Google Scholar] [CrossRef] [Green Version]
- Shen, J.; Peng, Y.; Wei, L.; Zhang, W.; Yang, L.; Lan, L.; Kapoor, P.; Ju, Z.; Mo, Q.; Shih, I.M.; et al. ARID1A Deficiency Impairs the DNA Damage Checkpoint and Sensitizes Cells to PARP Inhibitors. Cancer Discov. 2015, 5, 752–767. [Google Scholar] [CrossRef] [Green Version]
- Watanabe, R.; Ui, A.; Kanno, S.I.; Ogiwara, H.; Nagase, T.; Kohno, T.; Yasui, A. SWI/SNF factors required for cellular resistance to dna damage include arid1a and arid1b and show interdependent protein stability. Cancer Res. 2014, 74, 2465–2475. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Watanabe, R.; Kanno, S.I.; Roushandeh, A.M.; Ui, A.; Yasui, A. Nucleosome remodelling, DNA repair and transcriptional regulation build negative feedback loops in cancer and cellular ageing. Philos. Trans. R. Soc. B Biol. Sci. 2017, 372, 20160473. [Google Scholar] [CrossRef] [PubMed]
- Ogiwara, H.; Takahashi, K.; Sasaki, M.; Kuroda, T.; Yoshida, H.; Watanabe, R.; Maruyama, A.; Makinoshima, H.; Chiwaki, F.; Sasaki, H.; et al. Targeting the Vulnerability of Glutathione Metabolism in ARID1A-Deficient Cancers. Cancer Cell 2019, 35, 177–190. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kwan, S.Y.; Cheng, X.; Tsang, Y.T.; Choi, J.S.; Kwan, S.Y.; Izaguirre, D.I.; Kwan, H.S.; Gershenson, D.M.; Wong, K.K. Loss of ARID1A expression leads to sensitivity to ROS-inducing agent elesclomol in gynecologic cancer cells. Oncotarget 2016, 7, 56933–56943. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- De, P.; Dey, N. Mutation-driven signals of ARID1A and PI3K pathways in ovarian carcinomas: Alteration is an opportunity. Int. J. Mol. Sci. 2019, 20, 5732. [Google Scholar] [CrossRef] [Green Version]
- Berns, K.; Caumanns, J.J.; Hijmans, E.M.; Gennissen, A.M.; Severson, T.M.; Evers, B.; Wisman, G.B.A.; Meersma, G.J.; Lieftink, C.; Beijersbergen, R.L.; et al. ARID1A mutation sensitizes most ovarian clear cell carcinomas to BET inhibitors. Oncogene 2018, 37, 4611–4625. [Google Scholar] [CrossRef]
- Fukumoto, T.; Magno, E.; Zhang, R. SWI/SNF complexes in ovarian cancer: Mechanistic insights and therapeutic implications. Mol. Cancer Res. 2018, 16, 1819–1825. [Google Scholar] [CrossRef] [Green Version]
- Li, X.S.; Trojer, P.; Matsumura, T.; Treisman, J.E.; Tanese, N. Mammalian SWI/SNF-A Subunit BAF250/ARID1 Is an E3 Ubiquitin Ligase That Targets Histone H2B. Mol. Cell. Biol. 2010, 30, 1673–1688. [Google Scholar] [CrossRef]
- Srikanth, S.; Ramachandran, S.; Mohan, S. Construction of the gene regulatory network identifies MYC as a transcriptional regulator of SWI/SNF complex. Sci. Rep. 2020, 10, 158. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lakshminarasimhan, R.; Andreu-Vieyra, C.; Lawrenson, K.; Duymich, C.E.; Gayther, S.A.; Liang, G.; Jones, P.A. Down-regulation of ARID1A is sufficient to initiate neoplastic transformation along with epigenetic reprogramming in non-tumorigenic endometriotic cells. Cancer Lett. 2017, 401, 11–19. [Google Scholar] [CrossRef] [PubMed]
- Bitler, B.G.; Aird, K.M.; Garipov, A.; Li, H.; Amatangelo, M.; Kossenkov, A.V.; Schultz, D.C.; Liu, Q.; Shih, I.M.; Conejo-Garcia, J.R.; et al. Synthetic lethality by targeting EZH2 methyltransferase activity in ARID1A-mutated cancers. Nat. Med. 2015, 21, 231–238. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shigetomi, H.; Oonogi, A.; Tsunemi, T.; Tanase, Y.; Yamada, Y.; Kajihara, H.; Yoshizawa, Y.; Furukawa, N.; Haruta, S.; Yoshida, S.; et al. The role of components of the chromatin modification machinery in carcinogenesis of clear cell carcinoma of the ovary. Oncol. Lett. 2011, 2, 591–597. [Google Scholar] [CrossRef] [Green Version]
- Helming, K.C.; Wang, X.; Wilson, B.G.; Vazquez, F.; Haswell, J.R.; Manchester, H.E.; Kim, Y.; Kryukov, G.V.; Ghandi, M.; Aguirre, A.J.; et al. ARID1B is a specific vulnerability in ARID1A-mutant cancers. Nat. Med. 2014, 20, 251–254. [Google Scholar] [CrossRef] [Green Version]
- Williamson, C.T.; Miller, R.; Pemberton, H.N.; Jones, S.E.; Campbell, J.; Konde, A.; Badham, N.; Rafiq, R.; Brough, R.; Gulati, A.; et al. ATR inhibitors as a synthetic lethal therapy for tumours deficient in ARID1A. Nat. Commun. 2016, 7, 13837. [Google Scholar] [CrossRef] [Green Version]
- Banerjee, S.; Stewart, J.; Porta, N.; Toms, C.; Leary, A.; Lheureux, S.; Khalique, S.; Tai, J.; Attygalle, A.; Vroobel, K.; et al. ATARI trial: ATR inhibitor in combination with olaparib in gynecological cancers with ARID1A loss or no loss (ENGOT/GYN1/NCRI). Int. J. Gynecol. Cancer Off. J. Int. Gynecol. Cancer Soc. 2021, 31, 1471–1475. [Google Scholar] [CrossRef]
- Lyu, C.; Zhang, Y.; Zhou, X.; Lang, J. ARID1A gene silencing reduces the sensitivity of ovarian clear cell carcinoma to cisplatin. Exp. Ther. Med. 2016, 12, 4067–4071. [Google Scholar] [CrossRef] [Green Version]
- Okamura, R.; Kato, S.; Lee, S.; Jimenez, R.E.; Sicklick, J.K.; Kurzrock, R. ARID1A alterations function as a biomarker for longer progression-free survival after anti-PD-1/PD-L1 immunotherapy. J. Immunother. Cancer 2020, 8, 1–6. [Google Scholar] [CrossRef] [Green Version]
- Lu, B.; Shi, H. An In-Depth Look at Small Cell Carcinoma of the Ovary, Hypercalcemic Type (SCCOHT): Clinical Implications from Recent Molecular Findings. J. Cancer 2019, 10, 223–237. [Google Scholar] [CrossRef]
- Chen, Y.; Zhang, H.; Xu, Z.; Tang, H.; Geng, A.; Cai, B.; Su, T.; Shi, J.; Jiang, C.; Tian, X.; et al. A PARP1-BRG1-SIRT1 axis promotes HR repair by reducing nucleosome density at DNA damage sites. Nucleic Acids Res. 2019, 47, 8563–8580. [Google Scholar] [CrossRef] [PubMed]
- Park, J.H.; Park, E.J.; Lee, H.S.; Kim, S.J.; Hur, S.K.; Imbalzano, A.N.; Kwon, J. Mammalian SWI/SNF complexes facilitate DNA double-strand break repair by promoting γ-H2AX induction. EMBO J. 2006, 25, 3986–3997. [Google Scholar] [CrossRef]
- Coatham, M.; Li, X.; Karnezis, A.N.; Hoang, L.N.; Tessier-Cloutier, B.; Meng, B.; Soslow, R.A.; Gilks, C.B.; Huntsman, D.G.; Stewart, C.J.; et al. Concurrent ARID1A and ARID1B inactivation in endometrial and ovarian dedifferentiated carcinomas. Mod. Pathol. 2016, 29, 1586–1593. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Itamochi, H.; Oishi, T.; Oumi, N.; Takeuchi, S.; Yoshihara, K.; Mikami, M.; Yaegashi, N.; Terao, Y.; Takehara, K.; Ushijima, K.; et al. Whole-genome sequencing revealed novel prognostic biomarkers and promising targets for therapy of ovarian clear cell carcinoma. Br. J. Cancer 2017, 117, 717–724. [Google Scholar] [CrossRef] [Green Version]
- Karnezis, A.N.; Wang, Y.; Ramos, P.; Hendricks, W.P.; Oliva, E.; D’Angelo, E.; Prat, J.; Nucci, M.R.; Nielsen, T.O.; Chow, C.; et al. Dual loss of the SWI/SNF complex ATPases SMARCA4/BRG1 and SMARCA2/BRM is highly sensitive and specific for small cell carcinoma of the ovary, hypercalcaemic type. J. Pathol. 2016, 238, 389–400. [Google Scholar] [CrossRef] [Green Version]
- Wang, L.; Zhao, Z.; Meyer, M.B.; Saha, S.; Yu, M.; Guo, A.; Wisinski, K.B.; Huang, W.; Cai, W.; Pike, J.W.; et al. CARM1 methylates chromatin remodeling factor BAF155 to enhance tumor progression and metastasis. Cancer Cell 2014, 25, 21–36. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sima, X.; He, J.; Peng, J.; Xu, Y.; Zhang, F.; Deng, L. The genetic alteration spectrum of the SWI/SNF complex: The oncogenic roles of BRD9 and ACTL6A. PLoS ONE 2019, 14, e0222305. [Google Scholar] [CrossRef] [Green Version]
- Zhang, J.; Zhang, J.; Wei, Y.; Li, Q.; Wang, Q. ACTL6A regulates follicle-stimulating hormone-driven glycolysis in ovarian cancer cells via PGK1. Cell Death Dis. 2019, 10, 811. [Google Scholar] [CrossRef] [Green Version]
- Xiao, Y.; Lin, F.T.; Lin, W.C. ACTL6A promotes repair of cisplatin-induced DNA damage, a new mechanism of platinum resistance in cancer. Proc. Natl. Acad. Sci. USA 2021, 118, e2015808118. [Google Scholar] [CrossRef]
- Pépin, D.; Vanderhyden, B.C.; Picketts, D.J.; Murphy, B.D. ISWI chromatin remodeling in ovarian somatic and germ cells: Revenge of the NURFs. Trends Endocrinol. Metab. 2007, 18, 215–224. [Google Scholar] [CrossRef]
- Lazzaro, M.A.; Pépin, D.; Pescador, N.; Murphy, B.D.; Vanderhyden, B.C.; Picketts, D.J. The imitation switch protein SNF2L regulates steroidogenic acute regulatory protein expression during terminal differentiation of ovarian granulosa cells. Mol. Endocrinol. 2006, 20, 2406–2417. [Google Scholar] [CrossRef] [PubMed]
- Ye, Y.; Xiao, Y.; Wang, W.; Wang, Q.; Yearsley, K.; Wani, A.A.; Yan, Q.; Gao, J.X.; Shetuni, B.S.; Barsky, S.H. Inhibition of expression of the chromatin remodeling inhibition of expression of the chromatin remodeling gene, SNF2L, selectively leads to DNA damage, growth inhibition, and cancer cell death. Mol. Cancer Res. 2009, 7, 1984–1999. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Manelyte, L. Chromatin remodelers, their implication in cancer and therapeutic potential. J. Rare Dis. Res. Treat. 2017, 2, 34–40. [Google Scholar] [CrossRef] [Green Version]
- Sheu, J.J.C.; Jung, H.C.; Yildiz, I.; Tsai, F.J.; Shaul, Y.; Wang, T.L.; Shih, I.M. The roles of human sucrose nonfermenting protein 2 homologue in the tumor-promoting functions of Rsf-1. Cancer Res. 2008, 68, 4050–4057. [Google Scholar] [CrossRef] [Green Version]
- Cai, G.; Yang, Q.; Sun, W. RSF1 in cancer: Interactions and functions. Cancer Cell Int. 2021, 21, 315. [Google Scholar] [CrossRef] [PubMed]
- Maeda, D.; Chen, X.; Guan, B.; Nakagawa, S.; Yano, T.; Taketani, Y.; Fukayama, M.; Wang, T.L.; Shih, I.M. Rsf-1 (HBXAP) expression is associated with advanced stage and lymph node metastasis in ovarian clear cell carcinoma. Int. J. Gynecol. Pathol. Off. J. Int. Soc. Gynecol. Pathol. 2011, 30, 30–35. [Google Scholar] [CrossRef]
- Sheu, J.J.C.; Guan, B.; Choi, J.H.; Lin, A.; Lee, C.H.; Hsiao, Y.T.; Wang, T.L.; Tsai, F.J.; Shih, I.M. Rsf-1, a chromatin remodeling protein, induces DNA damage and promotes genomic instability. J. Biol. Chem. 2010, 285, 38260–38269. [Google Scholar] [CrossRef] [Green Version]
- Kshirsagar, M.; Jiang, W.; Shih, I.M. DNA damage response is prominent in ovarian high-grade serous carcinomas, especially those with Rsf-1 (HBXAP) overexpression. J. Oncol. 2012, 2012, 621685. [Google Scholar] [CrossRef] [Green Version]
- Sheu, J.J.C.; Choi, J.H.; Guan, B.; Tsai, F.J.; Hua, C.H.; Lai, M.T.; Wang, T.L.; Shih, I.M. Rsf-1, a chromatin remodelling protein, interacts with cyclin E1 and promotes tumour development. J. Pathol. 2013, 229, 559–568. [Google Scholar] [CrossRef] [Green Version]
- Yang, Y.I.; Ahn, J.H.; Lee, K.T.; Shih, I.M.; Choi, J.H. RSF1 is a positive regulator of NF-κB-induced gene expression required for ovarian cancer chemoresistance. Cancer Res. 2014, 74, 2258–2269. [Google Scholar] [CrossRef]
- Yang, H.; Zhang, X.; Zhu, L.; Yang, Y.; Yin, X. YY1-Induced lncRNA PART1 Enhanced Resistance of Ovarian Cancer Cells to Cisplatin by Regulating miR-512-3p/CHRAC1 Axis. DNA Cell Biol. 2021, 40, 821–832. [Google Scholar] [CrossRef] [PubMed]
- Iness, A.N.; Litovchick, L. MuvB: A key to cell cycle control in ovarian cancer. Front. Oncol. 2018, 8, 223. [Google Scholar] [CrossRef] [PubMed]
- Gorringe, K.L.; Choong, D.Y.; Williams, L.H.; Ramakrishna, M.; Sridhar, A.; Qiu, W.; Bearfoot, J.L.; Campbell, I.G. Mutation and methylation analysis of the chromodomain-helicase-DNA binding 5 gene in ovarian cancer. Neoplasia 2008, 10, 1253–1258. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mulero-Navarro, S.; Esteller, M. Chromatin remodeling factor CHD5 is silenced by promoter CpG island hypermethylation in human cancer. Epigenetics 2008, 3, 210–215. [Google Scholar] [CrossRef] [Green Version]
- Falconer, H.; Sundqvist, J.; Xu, H.; Vodolazkaia, A.; Fassbender, A.; Kyama, C.; Bokor, A.; D’Hooghe, T.M. Analysis of common variations in tumor-suppressor genes on chr1p36 among Caucasian women with endometriosis. Gynecol. Oncol. 2012, 127, 398–402. [Google Scholar] [CrossRef]
- Wong, R.R.; Chan, L.K.; Tsang, T.P.; Lee, C.W.; Cheung, T.H.; Yim, S.F.; Siu, N.S.; Lee, S.N.; Yu, M.Y.; Chim, S.S.; et al. CHD5 downregulation associated with poor prognosis in epithelial ovarian cancer. Gynecol. Obstet. Investig. 2011, 72, 203–207. [Google Scholar] [CrossRef]
- Jones, D.; Lin, D. Amplification of the NSD3-BRD4-CHD8 pathway in pelvic high-grade serous carcinomas of tubo-ovarian and endometrial origin. Mol. Clin. Oncol. 2017, 7, 301–307. [Google Scholar] [CrossRef] [Green Version]
- Thompson, B.A.; Tremblay, V.; Lin, G.; Bochar, D.A. CHD8 Is an ATP-Dependent Chromatin Remodeling Factor That Regulates β-Catenin Target Genes. Mol. Cell. Biol. 2008, 28, 3894–3904. [Google Scholar] [CrossRef] [Green Version]
- Oyama, Y.; Shigeta, S.; Tokunaga, H.; Tsuji, K.; Ishibashi, M.; Shibuya, Y.; Shimada, M.; Yasuda, J.; Yaegashi, N. CHD4 regulates platinum sensitivity through MDR1 expression in ovarian cancer: A potential role of CHD4 inhibition as a combination therapy with platinum agents. PLoS ONE 2021, 16, e0251079. [Google Scholar] [CrossRef]
- Bauer, T.L.; Collmar, K.; Kaltofen, T.; Loeffler, A.K.; Decker, L.; Mueller, J.; Pinter, S.; Eisler, S.A.; Mahner, S.; Fraungruber, P.; et al. Functional analysis of non-genetic resistance to platinum in epithelial ovarian cancer reveals a role for the mbd3-nurd complex in resistance development. Cancers 2021, 13, 3801. [Google Scholar] [CrossRef]
- Dannenmann, C.; Shabani, N.; Friese, K.; Jeschke, U.; Mylonas, I.; Brüning, A. The metastasis-associated gene MTA1 is upregulated in advanced ovarian cancer, represses ERβ, and enhances expression of oncogenic cytokine GRO. Cancer Biol. Ther. 2008, 7, 1460–1467. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, B.; Wang, L.; Zhang, S.; Bennett, B.D.; He, F.; Zhang, Y.; Xiong, C.; Han, L.; Diao, L.; Li, P.; et al. INO80 governs superenhancer-mediated oncogenic transcription and tumor growth in melanoma. Genes Dev. 2016, 30, 1440–1453. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hu, J.; Liu, J.; Chen, A.; Lyu, J.; Ai, G.; Zeng, Q.; Sun, Y.; Chen, C.; Wang, J.; Qiu, J.; et al. Ino80 promotes cervical cancer tumorigenesis by activating Nanog expression. Oncotarget 2016, 7, 72250–72262. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, S.; Zhou, B.; Wang, L.; Li, P.; Bennett, B.D.; Snyder, R.; Garantziotis, S.; Fargo, D.C.; Cox, A.D.; Chen, L.; et al. INO80 is required for oncogenic transcription and tumor growth in non-small cell lung cancer. Oncogene 2017, 36, 1430–1439. [Google Scholar] [CrossRef]
- Cerami, E.; Gao, J.; Dogrusoz, U.; Gross, B.E.; Sumer, S.O.; Aksoy, B.A.; Jacobsen, A.; Byrne, C.J.; Heuer, M.L.; Larsson, E.; et al. The cBio cancer genomics portal: An open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012, 2, 401–404. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gao, J.; Aksoy, B.A.; Dogrusoz, U.; Dresdner, G.; Gross, B.; Sumer, S.O.; Sun, Y.; Jacobsen, A.; Sinha, R.; Larsson, E.; et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci. Signal. 2013, 6, pl1. [Google Scholar] [CrossRef] [Green Version]
- Kang, K.T.; Kwon, Y.W.; Kim, D.K.; Lee, S.I.; Kim, K.H.; Suh, D.S.; Kim, J.H. TRRAP stimulates the tumorigenic potential of ovarian cancer stem cells. BMB Rep. 2018, 51, 514–519. [Google Scholar] [CrossRef]
- Xia, B.; Li, H.; Yang, S.; Liu, T.; Lou, G. MiR-381 inhibits epithelial ovarian cancer malignancy via YY1 suppression. Tumor Biol. 2016, 37, 9157–9167. [Google Scholar] [CrossRef]
- Qian, S.; Wang, W.; Li, M. Transcriptional factor Yin Yang 1 facilitates the stemness of ovarian cancer via suppressing miR-99a activity through enhancing its deacetylation level. Biomed. Pharmacother. 2020, 126, 110085. [Google Scholar] [CrossRef]
- Li, H.; Tong, X.; Xu, Y.; Wang, M.; Dai, H.; Shi, T.; Sun, M.; Chen, K.; Cheng, X.; Wei, Q. Functional genetic variants of RUVBL1 predict overall survival of Chinese patients with epithelial ovarian cancer. Carcinogenesis 2019, 40, 1209–1219. [Google Scholar] [CrossRef]
- Shin, S.H.; Lee, J.S.; Zhang, J.M.; Choi, S.; Boskovic, Z.V.; Zhao, R.; Song, M.; Wang, R.; Tian, J.; Lee, M.H.; et al. Synthetic lethality by targeting the RUVBL1/2-TTT complex in mTORC1-hyperactive cancer cells. Sci. Adv. 2020, 6, eaay9131. [Google Scholar] [CrossRef]
- Becker, P.B.; Workman, J.L. Nucleosome Remodeling and Epigenetics. Cold Spring Harb. Perspect. Biol. 2013, 5, a017905. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lin, D.I.; Chudnovsky, Y.; Duggan, B.; Zajchowski, D.; Greenbowe, J.; Ross, J.S.; Gay, L.M.; Ali, S.M.; Elvin, J.A. Comprehensive genomic profiling reveals inactivating SMARCA4 mutations and low tumor mutational burden in small cell carcinoma of the ovary, hypercalcemic-type. Gynecol. Oncol. 2017, 147, 626–633. [Google Scholar] [CrossRef] [PubMed]
- Auguste, A.; Blanc-Durand, F.; Deloger, M.; Formal, A.L.; Bareja, R.; Wilkes, D.C.; Richon, C.; Brunn, B.; Caron, O.; Devouassoux-Shisheboran, M.; et al. Small Cell Carcinoma of the Ovary, Hypercalcemic Type (SCCOHT) beyond SMARCA4 Mutations: A Comprehensive Genomic Analysis. Cells 2020, 9, 1496. [Google Scholar] [CrossRef]
- Coughlan, A.Y.; Testa, G. Exploiting epigenetic dependencies in ovarian cancer therapy. Int. J. Cancer 2021, 149, 1732–1743. [Google Scholar] [CrossRef] [PubMed]
SWI/SNF Subunits | Coding Gene | Protein Names |
---|---|---|
SMARCA4 | BRG1 | |
Helicases/ATPases | SMARCA2 | BRM |
ACTB | -actin | |
ATPase cap subunit | ACTL6A/B | BRAF53A/B |
BCL7A/B/C | ||
BAF specific | SS18/SS18L1 | |
BCL11A/B | ||
SMARCB1 | BAF47/INI1 | |
SMARCE1 | BAF57 | |
Common core subunit | SMARCC1 | BAF155 |
SMARCD1/2/3 | BAF60A/B/C | |
SMARCC2 | BAF170 | |
ARID1A/B | BAF250A/B, OSHA1/2 | |
cBAF specific | DPF1/2/3 | BAF45B/D/C |
ARID2 | BAF200 | |
PBRM1 | BAF180 | |
PBAF specific | PHF10 | BAF45A |
BRD7 | ||
GLTSCR1/L | BIRCA/L | |
ncBAF specific | BRD9 |
Gynecologic Disease | ARID1A Mutation Frequency | References |
---|---|---|
Endometriosis | 10% (9/107) | [44] |
2% (2/101) | [45] | |
Low-grade endometrioid endometrial cancer | 46.7% (129/276) | [46] |
High-grade endometrioid endometrial cancer | 60% (18/30) | [46] |
Serous endometrial cancer | 10.8% (4/37) | [46] |
23.8 % (10/42) | [46] | |
Endometrial carcinosarcoma | 12% (7/57) | [47] |
30% (10/33) | [48] | |
Endometrioid endometrial cancer | 40% (10/25) | [49] |
68% (11/16) | [50] | |
36% (40/122) | [51] | |
45% (9/20) | [52] | |
Endometrioid ovarian cancer | 43% (6/14) | [53] |
36% (8/22) | [54] | |
Granulosa cell ovarian cancer | 0% (0/5) | [53] |
0% (0/76) | [48] | |
0% (0/36) | [52] | |
High-grade serous ovarian cancer | 1% (1/98) | [55] |
48% (11/23) | [54] | |
Low-grade serous ovarian cancer | 8.5% (6/71) | [56] |
33% (2/6) | [52] | |
Mucinous ovarian cancer | 50% (2/4) | [53] |
46% (55/119) | [48] | |
42% (17/41) | [52] | |
69.7% (69/99) | [57] | |
Clear cell ovarian cancer | 57% (24/42) | [58] |
20% (1/5) | [53] | |
14% (5/37) | [54] | |
Seromucinous borderline ovarian cancer | 14% (4/27) | [59] |
Affected Cell Processes | Result | Actionable Therapy Approach | References |
---|---|---|---|
Gene expression changes: | |||
p300/CRB histone acetyltransferase interaction | Due to lost p300/CRB interactions with ARID1A, changes in H3K27ac marks lead to many gene expression changes | [63] | |
RNAPII pausing | Loss of normal RNAPII pausing may be due to reduced promoter acetylation and results in decreased gene expression | [64] | |
HDAC6 deacetylase activation, p53 deacetylation | HDAC6 is activated by ARID1A reduction. In turn, p53 K120 is deacetylated (which inhibits apoptosis) | HDAC6 inhibitor | [65] |
ARID1B | As an ARID1A homolog, ARID1B is left to restore most of the functions | BRD2 (BET, required for ARID1B transcription) inhibitors | [66] |
YES1 deregulation | In ARID1A deficient cell line model treated with dasatinib, YES1 was identified as the main target gene | YES1 inhibitor (dasatinib) | [67] |
Telomere/cell division: | |||
STAG1 (cohesin protein) reduction | Reduced STAG1 leads to decreased mitotic telomere cohesion | [68] | |
TOP2A (topoisomerase) interaction loss | TOP2A interactions with SWI/SNF complex ATPase BRG1 are lost/reduced. This causes replication stress through reduced sister chromatid decatenation and anaphase bridge formation during mitosis | [69,70] | |
TERT (telomerase reverse transriptase) upregulation | TERT promoter is upregulated in ARID1A deficient cells (increased survival) | ATR inhibitor | [71] |
DNA damage reparation: | |||
HR (homologous DSB repair) | ARID1A interacts and activates ATR and is required for DNA end processing (RPA and RAD51 loading), as well as G2-M cell-cycle arrest maintenance | PARP inhibitor | [72] |
NHEJ (non-homologous end joining) | ARID1A/B are required for KU70/KU80 protein recruitment to DSB | cisplatin | [73] |
MMR (miss match repair) | ARID1A may interact and direct MSH2 to MMR sites | PD-L1 inhibitor | [61] |
NER (nucleotide excision repair) | ARID1A/B required for XPA (NER protein) requirement | [74] | |
ROS (reactive oxygen species) formation | Reduces SLC7A11 levels to impair antioxidant GSH production | ROS inducers (e.g., HSP90 inhibitor, elesclomol) | [75,76] |
PI3K/AKT/mTOR pathway: | |||
PI3K/AKT/mTOR regulation | Mutually inclusive KRAS, PIK3CA, and PTEN mutations | [77] | |
ANXA1 (AKT activator) upregulation | Upregulation by ARID1A loss | AKT inhibitor | [78] |
PIK3IP1(PI3K inhibitor) downregulation | Downregulation by ARID1A loss (through EZH2 methyltransferase activation) | PI3K, EZH2, HDAC2 inhibitors | [79] |
Protein interactions: | |||
E3 ubiquitin ligase interaction | ARID1 forms E3 ubiquitin ligase, and mutations result in decreased ubiquitination of H2B histones | [80] | |
MYC interaction | Interaction with and regulation of MYC | [81] |
Chromatin Remodeler Complex | Gene | Change | Type of OC | References |
---|---|---|---|---|
SCCOHT | [133] | |||
SWI/SNF | SMARCA4 | Inactivating mutation | OCCC | [94] |
Dedefenrentiated OC | [93] | |||
SWI/SNF | SMARCB1 | Inactivating mutation | SCCOHT | [95] |
Epigenetic silencing, downregulation | SCCOHT | [134] | ||
SWI/SNF | SMARCA2 | Inactivating mutation | OCCC | [94] |
SWI/SNF, ISWI | SMARCA1 | Inactivating mutation | OCCC | [94] |
SWI/SNF | BCL11A | Inactivating mutation | OCCC | [94] |
SWI/SNF | DPF1 | Inactivating mutation | OCCC | [94] |
Inactivating mutation | OCCC | [94] | ||
SWI/SNF | SMARCC1 | Protein methylation by upregulated CARM1 | HGSOC | [96] |
SWI/SNF, INO80 | ACTL6A | Amplification | Non-specified OC | [97] |
SWI/SNF | BRD9 | Amplification | Non-specified OC | [97] |
ISWI | RSF1 | Amplification, gene fusion | HGSOC | [27,104] |
ISWI | CHARC1 | Amplification | HSGOC | [27] |
ISWI | RBBP4 | Amplification, gene fusion | HSGOC | [27] |
CHD | CHD5 | Inactivating mutation, promoter methylation | Non-specified OC | [113,116] |
CHD | CHD8 | Amplification | HSGOC | [117] |
CHD | CHD4 | mRNA overexpression | Non-specified OC | [119] |
INO80 | RUVBL1 | Polymorphisms | Epithelial OC | [130] |
INO80 | YY1 | Protein overexpression | Epithelial OC | [129] |
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Vaicekauskaitė, I.; Sabaliauskaitė, R.; Lazutka, J.R.; Jarmalaitė, S. The Emerging Role of Chromatin Remodeling Complexes in Ovarian Cancer. Int. J. Mol. Sci. 2022, 23, 13670. https://doi.org/10.3390/ijms232213670
Vaicekauskaitė I, Sabaliauskaitė R, Lazutka JR, Jarmalaitė S. The Emerging Role of Chromatin Remodeling Complexes in Ovarian Cancer. International Journal of Molecular Sciences. 2022; 23(22):13670. https://doi.org/10.3390/ijms232213670
Chicago/Turabian StyleVaicekauskaitė, Ieva, Rasa Sabaliauskaitė, Juozas Rimantas Lazutka, and Sonata Jarmalaitė. 2022. "The Emerging Role of Chromatin Remodeling Complexes in Ovarian Cancer" International Journal of Molecular Sciences 23, no. 22: 13670. https://doi.org/10.3390/ijms232213670
APA StyleVaicekauskaitė, I., Sabaliauskaitė, R., Lazutka, J. R., & Jarmalaitė, S. (2022). The Emerging Role of Chromatin Remodeling Complexes in Ovarian Cancer. International Journal of Molecular Sciences, 23(22), 13670. https://doi.org/10.3390/ijms232213670