Epigenetic silencing ZSCAN23 promotes pancreatic cancer growth by activating Wnt signaling

References

• Kisling SG, Natarajan G, Pothuraju R, Shah A, Batra SK, Kaur S. Implications of prognosis-associated genes in pancreatic tumor metastasis: lessons from global studies in bioinformatics. Cancer Metastasis Rev. 2021;40(3):721–10. doi:10.1007/s10555-021-09991-1.
   PubMed Web of Science ®Google Scholar
• Halbrook CJ, Lyssiotis CA, Pasca di Magliano M, Maitra A. Pancreatic cancer: advances and challenges. Cell. 2023;186(8):1729–54. doi:10.1016/j.cell.2023.02.014.
   PubMed Web of Science ®Google Scholar
• Rahib L, Smith BD, Aizenberg R, Rosenzweig AB, Fleshman JM, Matrisian LM. Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res. 2014;74(11):2913–21. doi:10.1158/0008-5472.CAN-14-0155.
   PubMed Web of Science ®Google Scholar
• Goldstein JB, Zhao L, Wang X, Ghelman Y, Overman MJ, Javle MM, Shroff RT, Varadhachary GR, Wolff RA, McAllister F, et al. Germline DNA sequencing reveals novel mutations predictive of overall survival in a cohort of patients with pancreatic cancer. Clin Cancer Res. 2020;26(6):1385–94. doi:10.1158/1078-0432.CCR-19-0224.
   PubMed Web of Science ®Google Scholar
• Overbeek KA, Goggins MG, Dbouk M, Levink IJM, Koopmann BDM, Chuidian M, Konings ICAW, Paiella S, Earl J, Fockens P, et al. Timeline of development of pancreatic cancer and implications for successful early detection in high-risk individuals. Gastroenterology. 2022;162(3):772–85.e4. doi:10.1053/j.gastro.2021.10.014.
   PubMed Web of Science ®Google Scholar
• Goggins M, Overbeek KA, Brand R, Syngal S, Del Chiaro M, Bartsch DK, Bassi C, Carrato A, Farrell J, Fishman EK, et al. Management of patients with increased risk for familial pancreatic cancer: updated recommendations from the international cancer of the pancreas screening (CAPS) consortium. Gut. 2020;69(1):7–17. doi:10.1136/gutjnl-2019-319352.
   PubMed Web of Science ®Google Scholar
• Hosein AN, Dougan SK, Aguirre AJ, Maitra A. Translational advances in pancreatic ductal adenocarcinoma therapy. Nat Cancer. 2022;3(3):272–286. doi:10.1038/s43018-022-00349-2.
   PubMedGoogle Scholar
• Lowery MA, Jordan EJ, Basturk O, Ptashkin RN, Zehir A, Berger MF, Leach T, Herbst B, Askan G, Maynard H, et al. Real-time genomic profiling of pancreatic ductal adenocarcinoma: potential actionability and correlation with clinical phenotype. Clin Cancer Res. 2017;23(20):6094–100. doi:10.1158/1078-0432.CCR-17-0899.
   PubMed Web of Science ®Google Scholar
• Ma K, Cao B, Guo M. The detective, prognostic, and predictive value of DNA methylation in human esophageal squamous cell carcinoma. Clin Epigenetics. 2016;8(1):43. doi:10.1186/s13148-016-0210-9.
   PubMedGoogle Scholar
• Davalos V, Esteller M. Cancer epigenetics in clinical practice. CA Cancer J Clin. 2023;73(4):376–424. doi:10.3322/caac.21765.
   PubMed Web of Science ®Google Scholar
• Guo M, Peng Y, Gao A, Du C, Herman JG. Epigenetic heterogeneity in cancer. Biomarker Res. 2019;7:23. doi:10.1186/s40364-019-0174-y.
   PubMed Web of Science ®Google Scholar
• Zhu C, Zhang M, Wang Q, Jen J, Liu B, Guo M. Intratumor epigenetic heterogeneity-a panel gene methylation study in thyroid cancer. Front Genet. 2021;12:714071. doi:10.3389/fgene.2021.714071.
   PubMed Web of Science ®Google Scholar
• Yan W, Herman JG, Guo M. Epigenome-based personalized medicine in human cancer. Epigenomics. 2016;8(1):119–33. doi:10.2217/epi.15.84.
   PubMed Web of Science ®Google Scholar
• Miranda Furtado CL, Dos Santos Luciano MC, Silva Santos RD, Furtado GP, Moraes MO, Pessoa C. Epidrugs: targeting epigenetic marks in cancer treatment. Epigenetics. 2019;14(12):1164–1176. doi:10.1080/15592294.2019.1640546.
   PubMed Web of Science ®Google Scholar
• Cossío FP, Esteller M, Berdasco M. Towards a more precise therapy in cancer: exploring epigenetic complexity. Curr Opin Chem Biol. 2020;57:41–9. doi:10.1016/j.cbpa.2020.04.008.
   PubMed Web of Science ®Google Scholar
• Morel D, Jeffery D, Aspeslagh S, Almouzni G, Postel-Vinay S. Combining epigenetic drugs with other therapies for solid tumours - past lessons and future promise. Nat Rev Clin Oncol. 2020;17(2):91–107. doi:10.1038/s41571-019-0267-4.
   PubMed Web of Science ®Google Scholar
• Berdasco M, Esteller M. Clinical epigenetics: seizing opportunities for translation. Nat Rev Genet. 2019;20(2):109–27. doi:10.1038/s41576-018-0074-2.
   PubMed Web of Science ®Google Scholar
• Gao A, Guo M. Epigenetic based synthetic lethal strategies in human cancers. Biomarker Res. 2020;8:44. doi:10.1186/s40364-020-00224-1.
   PubMed Web of Science ®Google Scholar
• Hu Y, Guo M. Synthetic lethality strategies: beyond BRCA1/2 mutations in pancreatic cancer. Cancer Sci. 2020;111(9):3111–21. doi:10.1111/cas.14565.
   PubMed Web of Science ®Google Scholar
• Kuchenbaecker KB, Ramus SJ, Tyrer J, Lee A, Shen HC, Beesley J, Lawrenson K, McGuffog L, Healey S, Lee JM, et al. Identification of six new susceptibility loci for invasive epithelial ovarian cancer. Nat Genet. 2015;47(2):164–71. doi:10.1038/ng.3185.
   PubMed Web of Science ®Google Scholar
• Edelstein LC, Collins T. The SCAN domain family of zinc finger transcription factors. Gene. 2005;359:1–17. doi:10.1016/j.gene.2005.06.022.
   PubMed Web of Science ®Google Scholar
• Sander TL, Stringer KF, Maki JL, Szauter P, Stone JR, Collins T. The SCAN domain defines a large family of zinc finger transcription factors. Gene. 2003;310:29–38. doi:10.1016/S0378-1119(03)00509-2.
   PubMed Web of Science ®Google Scholar
• Schumacher C, Wang H, Honer C, Ding W, Koehn J, Lawrence Q, Coulis CM, Wang LL, Ballinger D, Bowen BR, et al. The SCAN domain mediates selective oligomerization. J Biol Chem. 2000;275(22):17173–9. doi:10.1074/jbc.M000119200.
   PubMed Web of Science ®Google Scholar
• Williams AJ, Blacklow SC, Collins T. The zinc finger-associated SCAN box is a conserved oligomerization domain. Mol Cell Biol. 1999;19(12):8526–35. doi:10.1128/MCB.19.12.8526.
   PubMed Web of Science ®Google Scholar
• Stone JR, Maki JL, Blacklow SC, Collins T. The SCAN domain of ZNF174 is a dimer. J Biol Chem. 2002;277(7):5448–52. doi:10.1074/jbc.M109815200.
   PubMed Web of Science ®Google Scholar
• Li X, Han M, Zhang H, Liu F, Pan Y, Zhu J, Liao Z, Chen X, Zhang B. Structures and biological functions of zinc finger proteins and their roles in hepatocellular carcinoma. Biomarker Res. 2022;10(1):2. doi:10.1186/s40364-021-00345-1.
   PubMed Web of Science ®Google Scholar
• Lee K, Gollahon LS. ZSCAN4 and TRF1: a functionally indirect interaction in cancer cells independent of telomerase activity. Biochem Bioph Res Co. 2015;466(4):644–9. doi:10.1016/j.bbrc.2015.09.107.
   PubMed Web of Science ®Google Scholar
• Zhang X, Bai Y, Huang L, Liu S, Mo Y, Cheng W, Wang G, Cao Z, Chen X, Cui H, et al. CHD1L augments autophagy-mediated migration of hepatocellular carcinoma through targeting ZKSCAN3. Cell Death Disease. 2021;12(10):950. doi:10.1038/s41419-021-04254-x.
   PubMed Web of Science ®Google Scholar
• Kim CW, Roh SA, Tak KH, Koh BM, Ha YJ, Cho DH, Kim SY, Kim YS, Kim JC. ZKSCAN3 facilitates liver metastasis of colorectal cancer associated with CEA-expressing tumor. Anticancer Res. 2016;36(5):2397–2406.
   PubMed Web of Science ®Google Scholar
• Li Q, Luo H, Dai FQ, Wang RT, Fan XQ, Luo YY, Deng M-S, Wang Y, Long T, Guo W, et al. SAMD9 promotes postoperative recurrence of esophageal squamous cell carcinoma by stimulating MYH9-mediated GSK3β/β-catenin signaling. Adv Sci (Weinheim, Baden-Wurttemberg, Germany). 2023;10(11):e2203573. doi:10.1002/advs.202203573.
   PubMedGoogle Scholar
• Hu S, Ren S, Cai Y, Liu J, Han Y, Zhao Y, Yang J, Zhou X, Wang X. Glycoprotein PTGDS promotes tumorigenesis of diffuse large B-cell lymphoma by MYH9-mediated regulation of wnt–β-catenin–STAT3 signaling. Cell Death Differ. 2022;29(3):642–656. doi:10.1038/s41418-021-00880-2.
   PubMed Web of Science ®Google Scholar
• Zhou P, Li Y, Li B, Zhang M, Liu Y, Yao Y, Li D. NMIIA promotes tumor growth and metastasis by activating the Wnt/β-catenin signaling pathway and EMT in pancreatic cancer. Oncogene. 2019;38(27):5500–5515. doi:10.1038/s41388-019-0806-6.
   PubMed Web of Science ®Google Scholar
• Thool M, Sundaravadivelu PK, Sudhagar S, Thummer RP. A comprehensive review on the role of ZSCAN4 in embryonic development, stem cells, and cancer. Stem Cell Rev Rep. 2022;18(8):2740–56. doi:10.1007/s12015-022-10412-1.
   PubMed Web of Science ®Google Scholar
• Wang Y, Luo Y, Fu S, He L, Pan G, Fan D, Wen Q, Fan Y. Zinc finger and SCAN domain-containing protein 18 is a potential DNA methylation-modified tumor suppressor and biomarker in breast cancer. Front Endocrinol (Lausanne). 2023;14:1095604. doi:10.3389/fendo.2023.1095604.
   PubMed Web of Science ®Google Scholar
• Srinivasan R, Nady N, Arora N, Hsieh LJ, Swigut T, Narlikar GJ, Wossidlo M, Wysocka J. Zscan4 binds nucleosomal microsatellite DNA and protects mouse two-cell embryos from DNA damage. Sci Adv. 2020;6(12):eaaz9115. doi:10.1126/sciadv.aaz9115.
   PubMed Web of Science ®Google Scholar
• Cho YE, Kim JH, Che YH, Kim YJ, Sung JY, Kim YW, Choe B-G, Lee S, Park J-H. Role of the WNT/β-catenin/ZKSCAN3 pathway in regulating chromosomal instability in colon cancer Cell lines and tissues. Int J Mol Sci. 2022;23(16):9302. doi:10.3390/ijms23169302.
   PubMed Web of Science ®Google Scholar
• Li Y, Wang Z, Su P, Liang Y, Li Z, Zhang H, Song X, Han D, Wang X, Liu Y, et al. Circ-EIF6 encodes EIF6-224aa to promote TNBC progression via stabilizing MYH9 and activating the Wnt/beta-catenin pathway. Mol Ther. 2022;30(1):415–30. doi:10.1016/j.ymthe.2021.08.026.
   PubMed Web of Science ®Google Scholar
• Kai JD, Cheng LH, Li BF, Kang K, Xiong F, Fu JC, Wang S. MYH9 is a novel cancer stem cell marker and prognostic indicator in esophageal cancer that promotes oncogenesis through the PI3K/AKT/mTOR axis. Cell Biol Int. 2022;46(12):2085–2094. doi:10.1002/cbin.11894.
   PubMed Web of Science ®Google Scholar
• Zhao R, Ge Y, Gong Y, Li B, Xiao B, Zuo S. NAP1L5 targeting combined with MYH9 inhibit HCC progression through PI3K/AKT/mTOR signaling pathway. Aging. 2022;14(22):9000–19. doi:10.18632/aging.204377.
   PubMedGoogle Scholar
• Yang SB, Zhou ZH, Lei J, Li XW, Chen Q, Li B, Zhang Y-W, Ge Y-Z, Zuo S. TM4SF1 upregulates MYH9 to activate the NOTCH pathway to promote cancer stemness and lenvatinib resistance in HCC. Biol Direct. 2023;18(1):18. doi:10.1186/s13062-023-00376-8.
   PubMed Web of Science ®Google Scholar
• Eubelen M, Bostaille N, Cabochette P, Gauquier A, Tebabi P, Dumitru AC, Koehler M, Gut P, Alsteens D, Stainier DYR, et al. A molecular mechanism for Wnt ligand-specific signaling. Sci (New York, NY). 2018;361(6403). doi:10.1126/science.aat1178.
   Google Scholar
• Zhao H, Ming T, Tang S, Ren S, Yang H, Liu M, Tao Q, Xu H. Wnt signaling in colorectal cancer: pathogenic role and therapeutic target. Mol Cancer. 2022;21(1):144. doi:10.1186/s12943-022-01616-7.
   PubMed Web of Science ®Google Scholar
• Kaur A, Lim JYS, Sepramaniam S, Patnaik S, Harmston N, Lee MA, Petretto E, Virshup DM, Madan B. WNT inhibition creates a BRCA-like state in Wnt-addicted cancer. EMBO Mol Med. 2021;13(4):e13349. doi:10.15252/emmm.202013349.
   PubMed Web of Science ®Google Scholar
• Angers S. Wnt signaling inhibition confers induced synthetic lethality to PARP inhibitors. EMBO Mol Med. 2021;13(4):e14002. doi:10.15252/emmm.202114002.
   PubMed Web of Science ®Google Scholar
• Seshagiri S, Stawiski EW, Durinck S, Modrusan Z, Storm EE, Conboy CB, Chaudhuri S, Guan Y, Janakiraman V, Jaiswal BS, et al. Recurrent R-spondin fusions in colon cancer. Nature. 2012;488(7413):660–4. doi:10.1038/nature11282.
   PubMed Web of Science ®Google Scholar
• Giannakis M, Hodis E, Jasmine Mu X, Yamauchi M, Rosenbluh J, Cibulskis K, Saksena G, Lawrence MS, Qian ZR, Nishihara R, et al. RNF43 is frequently mutated in colorectal and endometrial cancers. Nat Genet. 2014;46(12):1264–6. doi:10.1038/ng.3127.
   PubMed Web of Science ®Google Scholar
• Gao A, Bai P, Zhang M, Yao Y, Herman JG, Guo M. RASSF1A promotes ATM signaling and RASSF1A methylation is a synthetic lethal marker for ATR inhibitors. Epigenomics. 2023;15(22):1205–20. doi:10.2217/epi-2023-0306.
   PubMedGoogle Scholar
• Li H, Yang W, Zhang M, He T, Zhou F, GH J, Hu L, Guo M. Methylation of TMEM176A, a key ERK signaling regulator, is a novel synthetic lethality marker of ATM inhibitors in human lung cancer. Epigenomics. 2021;13(17):1403–1419. doi:10.2217/epi-2021-0217.
   PubMed Web of Science ®Google Scholar
• Du W, Gao A, Herman JG, Wang L, Zhang L, Jiao S, Guo M. Methylation of NRN1 is a novel synthetic lethal marker of PI3K-Akt-mTOR and ATR inhibitors in esophageal cancer. Cancer Sci. 2021;112(7):2870–2883. doi:10.1111/cas.14917.
   PubMed Web of Science ®Google Scholar
• Li H, Zhang M, Linghu E, Zhou F, Herman JG, Hu L, Guo M. Epigenetic silencing of TMEM176A activates ERK signaling in human hepatocellular carcinoma. Clin Epigenetics. 2018;10(1):137. doi:10.1186/s13148-018-0570-4.
   PubMedGoogle Scholar
• Herman JG, Graff JR, Myöhänen S, Nelkin BD, Baylin SB. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA. 1996;93(18):9821–9826. doi:10.1073/pnas.93.18.9821.
   PubMed Web of Science ®Google Scholar
• Yang W, Guo C, Herman JG, Zhu C, Lv H, Su X, Zhang L, Zhang M, Guo M. Epigenetic silencing of JAM3 promotes esophageal cancer development by activating Wnt signaling. Clin Epigenetics. 2022;14(1):164. doi:10.1186/s13148-022-01388-3.
   PubMed Web of Science ®Google Scholar
• Liu Y, Zhang M, He T, Yang W, Wang L, Zhang L, Guo M. Epigenetic silencing of IGFBPL1 promotes esophageal cancer growth by activating PI3K-AKT signaling. Clin Epigenetics. 2020;12(1):22. doi:10.1186/s13148-020-0815-x.
   PubMed Web of Science ®Google Scholar
• Yan W, Wu K, Herman JG, Brock MV, Fuks F, Yang L, Zhu H, Li Y, Yang Y, Guo M, et al. Epigenetic regulation of DACH1, a novel Wnt signaling component in colorectal cancer. Epigenetics. 2013;8(12):1373–83. doi:10.4161/epi.26781.
   PubMed Web of Science ®Google Scholar
• Wang Y, He T, Herman JG, Linghu E, Yang Y, Fuks F, Zhou F, Song L, Guo M. Correction to: methylation of ZNF331 is an independent prognostic marker of colorectal cancer and promotes colorectal cancer growth. Clin Epigenetics. 2018;10:36. doi:10.1186/s13148-018-0467-2.
   PubMed Web of Science ®Google Scholar