Generic placeholder image

Combinatorial Chemistry & High Throughput Screening

Editor-in-Chief

ISSN (Print): 1386-2073
ISSN (Online): 1875-5402

Research Article

MUM1L1 as a Tumor Suppressor and Potential Biomarker in Ovarian Cancer: Evidence from Bioinformatics Analysis and Basic Experiments

Author(s): Lu Zhang, Xue Wu, Xue Fan* and Hao Ai*

Volume 26, Issue 14, 2023

Published on: 02 May, 2023

Page: [2487 - 2501] Pages: 15

DOI: 10.2174/1386207326666230301141912

Price: $65

Abstract

Background: Ovarian cancer (OC) is the most prevalent gynecologic malignancy, with high mortality rates. However, its pathogenesis remains unclear. The current study aimed to explore potential biomarkers and suppressor genes for diagnosing and treating OC.

Methods: Biochemical and bioinformatics approaches were used to detect differentially expressed genes (DEGs) in ovarian tissues via integration analysis. Kaplan-Meier plot analysis was performed to assess progression-free survival and overall survival according to DEGs. Then, we constructed a protein-protein interaction (PPI) network based on data from the STRING database to identify the related target genes of DEGs. Finally, DEGs regulating the proliferation, migration, and invasion of SKOV3 cell lines were validated via in vitro experiments.

Results: Four DEGs (MUM1L1, KLHDC8A, CRYGD, and GREB1) with enriched expression in ovarian tissues were explicitly expressed in the ovary based on an analysis of all human proteins. MUM1L1 had high specificity, and its expression was higher in normal ovarian tissues than in OC tissues. Kaplan-Meier plot analysis showed that a high MUM1L1 expression was associated with longer progression-free survival and overall survival in OC. Based on the PPI analysis results, CBLN4, CBLN1, PTH2R, TMEM255B, and COL23A1 were associated with MUM1L1. In vitro studies revealed that MUM1L1 overexpression decreased the proliferation, migration, and invasion ability of SKOV3 cell lines. Meanwhile, MUM1L1 knockdown had contrasting results.

Conclusion: MUM1L1 is a tumor suppressor gene and is a potential biomarker for diagnosing and treating OC.

[1]
Armstrong, D.K.; Alvarez, R.D.; Bakkum-Gamez, J.N.; Barroilhet, L.; Behbakht, K.; Berchuck, A.; Chen, L.; Cristea, M.; DeRosa, M.; Eisenhauer, E.L.; Gershenson, D.M.; Gray, H.J.; Grisham, R.; Hakam, A.; Jain, A.; Karam, A.; Konecny, G.E.; Leath, C.A.; Liu, J.; Mahdi, H.; Martin, L.; Matei, D.; McHale, M.; McLean, K.; Miller, D.S.; O’Malley, D.M.; Percac-Lima, S.; Ratner, E.; Remmenga, S.W.; Vargas, R.; Werner, T.L.; Zsiros, E.; Burns, J.L.; Engh, A.M. Ovarian cancer, version 2.2020, NCCN clinical practice guidelines in oncology. J. Natl. Compr. Canc. Netw., 2021, 19(2), 191-226.
[http://dx.doi.org/10.6004/jnccn.2021.0007] [PMID: 33545690]
[2]
Sung, Hyuna; Ferlay, Jacques; Siegel Rebecca, L.; Laversanne, Mathieu; Soerjomataram, Isabelle; Jemal, Ahmedin Bray, Freddie 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.
[3]
Ekmann-Gade, A.W.; Høgdall, C.K.; Seibæk, L.; Noer, M.C.; Fagö-Olsen, C.L.; Schnack, T.H. Incidence, treatment, and survival trends in older versus younger women with epithelial ovarian cancer from 2005 to 2018: A nationwide Danish study. Gynecol. Oncol., 2022, 164(1), 120-128.
[http://dx.doi.org/10.1016/j.ygyno.2021.10.081] [PMID: 34716025]
[4]
Menon, U.; Gentry-Maharaj, A.; Burnell, M.; Singh, N.; Ryan, A.; Karpinskyj, C.; Carlino, G.; Taylor, J.; Massingham, S.K.; Raikou, M.; Kalsi, J.K.; Woolas, R.; Manchanda, R.; Arora, R.; Casey, L.; Dawnay, A.; Dobbs, S.; Leeson, S.; Mould, T.; Seif, M.W.; Sharma, A.; Williamson, K.; Liu, Y.; Fallowfield, L.; McGuire, A.J.; Campbell, S.; Skates, S.J.; Jacobs, I.J.; Parmar, M. Ovarian cancer population screening and mortality after long-term follow-up in the UK Collaborative Trial of Ovarian Cancer Screening (UKCTOCS): a randomised controlled trial. Lancet, 2021, 397(10290), 2182-2193.
[http://dx.doi.org/10.1016/S0140-6736(21)00731-5] [PMID: 33991479]
[5]
Akinwunmi, B.O.; Babic, A.; Vitonis, A.F.; Cramer, D.W.; Titus, L.; Tworoger, S.S.; Terry, K.L. Chronic medical conditions and CA125 levels among women without ovarian cancer. Cancer Epidemiol. Biomarkers Prev., 2018, 27(12), 1483-1490.
[http://dx.doi.org/10.1158/1055-9965.EPI-18-0203] [PMID: 30237250]
[6]
Galucio, N.C.R.; Moysés, D.A.; Pina, J.R.S.; Marinho, P.S.B.; Gomes Júnior, P.C.; Cruz, J.N.; Vale, V.V.; Khayat, A.S.; Marinho, A.M.R. Antiproliferative, genotoxic activities and quantification of extracts and cucurbitacin B obtained from Luffa operculata (L.). Cogn. Arab. J. Chem., 2022, 15(2), 103589.
[http://dx.doi.org/10.1016/j.arabjc.2021.103589]
[7]
Neto, R.A.M.; Santos, C.B.R.; Henriques, S.V.C.; Machado, L.O.; Cruz, J.N.; da Silva, C.H.T.P.; Federico, L.B.; Oliveira, E.H.C.; de Souza, M.P.C.; da Silva, P.N.B.; Taft, C.A.; Ferreira, I.M.; Gomes, M.R.F. Novel chalcones derivatives with potential antineoplastic activity investigated by docking and molecular dynamics simulations. J. Biomol. Struct. Dyn., 2022, 40(5), 2204-2216.
[http://dx.doi.org/10.1080/07391102.2020.1839562] [PMID: 33146078]
[8]
Mohaghegh Neyshabouri, M.; Jun, S.H.; Lagergren, J. Inferring tumor progression in large datasets. PLOS Comput. Biol., 2020, 16(10), e1008183.
[http://dx.doi.org/10.1371/journal.pcbi.1008183] [PMID: 33035204]
[9]
Fu, Y.; Ling, Z.; Arabnia, H.; Deng, Y. Current trend and development in bioinformatics research. BMC Bioinformatics, 2020, 21(S9)(Suppl. 9), 538.
[http://dx.doi.org/10.1186/s12859-020-03874-y] [PMID: 33272214]
[10]
Sayers, E.W.; Beck, J.; Bolton, E.E.; Bourexis, D.; Brister, J.R.; Canese, K.; Comeau, D.C.; Funk, K.; Kim, S.; Klimke, W.; Marchler-Bauer, A.; Landrum, M.; Lathrop, S.; Lu, Z.; Madden, T.L.; O’Leary, N.; Phan, L.; Rangwala, S.H.; Schneider, V.A.; Skripchenko, Y.; Wang, J.; Ye, J.; Trawick, B.W.; Pruitt, K.D.; Sherry, S.T. Database resources of the National Center for Information. Nucleic Acids Res., 2021, 49(D1), D10-D17.
[http://dx.doi.org/10.1093/nar/gkaa892] [PMID: 33095870]
[11]
Qi, Y.; Wang, N.; Pang, L.J.; Zou, H.; Hu, J.M.; Zhao, J.; Zhang, J.; Liu, C.X.; Zhang, W.J.; Yuan, X.L.; Li, F. Identification of potential mutations and genomic alterations in the epithelial and spindle cell components of biphasic synovial sarcomas using a human exome SNP chip. BMC Med. Genomics, 2015, 8(1), 69.
[http://dx.doi.org/10.1186/s12920-015-0144-7] [PMID: 26503545]
[12]
Shi, Z.; Li, X.; Zhang, L.; Luo, Y.; Shrestha, B.; Hu, X. Potential novel modules and hub genes as prognostic candidates of thyroid cancer by weighted gene co-expression network analysis. Int. J. Gen. Med., 2021, 14, 9433-9444.
[http://dx.doi.org/10.2147/IJGM.S329128] [PMID: 34908870]
[13]
Thul, P.J.; Lindskog, C. The human protein atlas: A spatial map of the human proteome. Protein Sci., 2018, 27(1), 233-244.
[http://dx.doi.org/10.1002/pro.3307] [PMID: 28940711]
[14]
Rhodes Daniel, R.; Yu, Jianjun; Shanker, K.; Deshpande, Nandan; Varambally, Radhika; Ghosh, Debashis; Barrette, Terrence; Pandey, Akhilesh Chinnaiyan, Arul M ONCOMINE: A cancer microarray database and integrated data-mining platform. Neoplasia, 2004, 6(1), 1-6.
[15]
Li, C.; Tang, Z.; Zhang, W.; Ye, Z.; Liu, F. GEPIA2021: Integrating multiple deconvolution-based analysis into GEPIA. Nucleic Acids Res., 2021, 49(W1), W242-W246.
[http://dx.doi.org/10.1093/nar/gkab418] [PMID: 34050758]
[16]
Lánczky, A. Győrffy, B. (KMplot): Development and implementation. J. Med. Internet Res., 2021, 23(7), e27633.
[PMID: 34309564]
[17]
Szklarczyk, D.; Gable, A.L.; Lyon, D.; Junge, A.; Wyder, S.; Huerta-Cepas, J.; Simonovic, M.; Doncheva, N.T.; Morris, J.H.; Bork, P.; Jensen, L.J.; Mering, C. STRING v11: Protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res., 2019, 47(D1), D607-D613.
[http://dx.doi.org/10.1093/nar/gky1131] [PMID: 30476243]
[18]
Otasek, D.; Morris, J.H.; Bouças, J.; Pico, A.R.; Demchak, B. Cytoscape Automation: Empowering workflow-based network analysis. Genome Biol., 2019, 20(1), 185.
[http://dx.doi.org/10.1186/s13059-019-1758-4] [PMID: 31477170]
[19]
Aurelien, M.; Le, Dung T.; Ascierto, Paolo A.; Di Giacomo, Anna Maria; Jesus-Acosta, Ana De; Delord, Jean-Pierre; Geva, Ravit; Gottfried, Maya; Penel, Nicolas; Hansen, Aaron R.; Piha-Paul, Sarina A.; Doi, Toshihiko; Gao, Bo; Chung, Hyun Cheol; Lopez-Martin, Jose; Bang, Yung-Jue; Frommer, Ronnie Shapira; Shah, Manisha; Ghori, Razi; Joe, Andrew K.; Pruitt, Scott K.; Diaz, Luis A., Jr. Efficacy of pembrolizumab in patients with noncolorectal high microsatellite instability/mismatch repair-deficient cancer: Results from the phase II KEYNOTE-158 study. J. Clin. Oncol., 2020, 38(1), 1-10.
[http://dx.doi.org/10.1200/JCO.19.02105] [PMID: 31682550]
[20]
Yoshihara, K.; Tsunoda, T.; Shigemizu, D.; Fujiwara, H.; Hatae, M.; Fujiwara, H.; Masuzaki, H.; Katabuchi, H.; Kawakami, Y.; Okamoto, A.; Nogawa, T.; Matsumura, N.; Udagawa, Y.; Saito, T.; Itamochi, H.; Takano, M.; Miyagi, E.; Sudo, T.; Ushijima, K.; Iwase, H.; Seki, H.; Terao, Y.; Enomoto, T.; Mikami, M.; Akazawa, K.; Tsuda, H.; Moriya, T.; Tajima, A.; Inoue, I.; Tanaka, K. High-risk ovarian cancer based on 126-gene expression signature is uniquely characterized by downregulation of antigen presentation pathway. Clin. Cancer Res., 2012, 18(5), 1374-1385.
[http://dx.doi.org/10.1158/1078-0432.CCR-11-2725] [PMID: 22241791]
[21]
Anglesio, M.S.; Arnold, J.M.; George, J.; Tinker, A.V.; Tothill, R.; Waddell, N.; Simms, L.; Locandro, B.; Fereday, S.; Traficante, N.; Russell, P.; Sharma, R.; Birrer, M.J.; deFazio, A.; Chenevix-Trench, G.; Bowtell, D.D.L.; Bowtell, D.D. Mutation of ERBB2 provides a novel alternative mechanism for the ubiquitous activation of RAS-MAPK in ovarian serous low malignant potential tumors. Mol. Cancer Res., 2008, 6(11), 1678-1690.
[http://dx.doi.org/10.1158/1541-7786.MCR-08-0193] [PMID: 19010816]
[22]
Tothill, R.W.; Tinker, A.V.; George, J.; Brown, R.; Fox, S.B.; Lade, S.; Johnson, D.S.; Trivett, M.K.; Etemadmoghadam, D.; Locandro, B.; Traficante, N.; Fereday, S.; Hung, J.A.; Chiew, Y.E.; Haviv, I.; Gertig, D.; deFazio, A.; Bowtell, D.D.L. Novel molecular subtypes of serous and endometrioid ovarian cancer linked to clinical outcome. Clin. Cancer Res., 2008, 14(16), 5198-5208.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-0196] [PMID: 18698038]
[23]
Zhu, X.; Chen, T.; Yang, H.; Lv, K. Lactate induced up‐regulation of KLHDC8A (Kelch domain‐containing 8A) contributes to the proliferation, migration and apoptosis of human glioma cells. J. Cell. Mol. Med., 2020, 24(20), 11691-11702.
[http://dx.doi.org/10.1111/jcmm.15780] [PMID: 32851798]
[24]
Cai, S.P.; Wang, X-Z.; Wang, Y.; He, F.; Fan, N.; Weng, J-N.; Zhang, J-H.; Liu, X-Y.; Liu, X.Y. A mutated CRYGD associated with congenital coralliform cataracts in two Chinese pedigrees. Int. J. Ophthalmol., 2021, 14(6), 800-804.
[http://dx.doi.org/10.18240/ijo.2021.06.03] [PMID: 34150533]
[25]
Haines, C.N.; Klingensmith, H.D.; Komara, M.; Burd, C.J. GREB1 regulates PI3K/Akt signaling to control hormone-sensitive breast cancer proliferation. Carcinogenesis, 2020, 41(12), 1660-1670.
[http://dx.doi.org/10.1093/carcin/bgaa096] [PMID: 32894276]
[26]
Yang, X.; Zhu, S.; Li, L.; Zhang, L.; Xian, S.; Wang, Y.; Cheng, Y. Identification of differentially expressed genes and signaling pathways in ovarian cancer by integrated bioinformatics analysis. OncoTargets Ther., 2018, 11, 1457-1474.
[http://dx.doi.org/10.2147/OTT.S152238] [PMID: 29588600]
[27]
Larsen, K. The porcine cerebellin gene family. Gene, 2021, 799, 145852.
[http://dx.doi.org/10.1016/j.gene.2021.145852] [PMID: 34274480]
[28]
Zhong, C.; Shen, J.; Zhang, H.; Li, G.; Shen, S.; Wang, F.; Hu, K.; Cao, L.; He, Y.; Ding, J. Cbln1 and Cbln4 are structurally similar but differ in GluD2 binding interactions. Cell Rep., 2017, 20(10), 2328-2340.
[http://dx.doi.org/10.1016/j.celrep.2017.08.031] [PMID: 28877468]
[29]
Yang, D.; Li, N.; Ma, A.; Dai, F.; Zheng, Y.; Hu, X.; Wang, Y.; Xian, S.; Zhang, L.; Yuan, M.; Liu, S.; Deng, Z.; Yang, Y.; Cheng, Y. Identification of potential biomarkers of polycystic ovary syndrome via integrated bioinformatics analysis. Reprod. Sci., 2021, 28(5), 1353-1361.
[http://dx.doi.org/10.1007/s43032-020-00352-x] [PMID: 33067753]
[30]
Bradford, S.T.; Hiramatsu, R.; Maddugoda, M.P.; Bernard, P.; Chaboissier, M.C.; Sinclair, A.; Schedl, A.; Harley, V.; Kanai, Y.; Koopman, P.; Wilhelm, D. The cerebellin 4 precursor gene is a direct target of SRY and SOX9 in mice. Biol. Reprod., 2009, 80(6), 1178-1188.
[http://dx.doi.org/10.1095/biolreprod.108.071480] [PMID: 19211811]
[31]
Sato, E.; Zhang, L.; Dorschner, R.A.; Adase, C.A.; Choudhury, B.P.; Gallo, R.L. Activation of parathyroid hormone 2 receptor induces decorin expression and promotes wound repair. J. Invest. Dermatol., 2017, 137(8), 1774-1783.
[http://dx.doi.org/10.1016/j.jid.2017.03.034] [PMID: 28454729]
[32]
Xiaowei, W.; Tong, L.; Yanjun, Q.; Lili, F. PTH2R is related to cell proliferation and migration in ovarian cancer: A multi-omics analysis of bioinformatics and experiments. Cancer Cell Int., 2022, 22(1), 148.
[http://dx.doi.org/10.1186/s12935-022-02566-2] [PMID: 35410353]
[33]
Panda, D.; Goltzman, D.; Jüppner, H.; Karaplis, A.C. TIP39/parathyroid hormone type 2 receptor signaling is a potent inhibitor of chondrocyte proliferation and differentiation. Am. J. Physiol. Endocrinol. Metab., 2009, 297(5), E1125-E1136.
[http://dx.doi.org/10.1152/ajpendo.00254.2009] [PMID: 19706789]
[34]
Watase, C.; Fuse, M.; Ino, Y.; Naito, C.; Hiraoka, N. Novel insights into immunohistochemical analysis for diagnosing serous neoplasm of the pancreas: aquaporin 1, stereocilin, and transmembrane protein 255B. Histopathology, 2021, 79(5), 872-879.
[http://dx.doi.org/10.1111/his.14456] [PMID: 34288030]
[35]
Zhang, L.; Zhao, X.; Wang, W. lncRNA and mRNA sequencing of the left testis in experimental varicocele rats treated with Morinda officinalis polysaccharide. Exp. Ther. Med., 2021, 22(4), 1136.
[http://dx.doi.org/10.3892/etm.2021.10570] [PMID: 34466146]
[36]
Pan, M.; Wang, Y.; Li, L.; Li, Z.; Wu, S.; Liu, Q. Postmortem detection of COL gene family variants in two aortic dissection cases. Int. J. Legal Med., 2022, 136(1), 85-91.
[http://dx.doi.org/10.1007/s00414-021-02605-z] [PMID: 34125279]
[37]
Zhu, H.; Shang, D.; Sun, M.; Choi, S.; Liu, Q.; Hao, J.; Figuera, L.E.; Zhang, F.; Choy, K.W.; Ao, Y.; Liu, Y.; Zhang, X.L.; Yue, F.; Wang, M.R.; Jin, L.; Patel, P.I.; Jing, T.; Zhang, X. X-linked congenital hypertrichosis syndrome is associated with interchromosomal insertions mediated by a human-specific palindrome near SOX3. Am. J. Hum. Genet., 2011, 88(6), 819-826.
[http://dx.doi.org/10.1016/j.ajhg.2011.05.004] [PMID: 21636067]
[38]
Koop, A.; Sellami, N.; Adam-Klages, S.; Lettau, M.; Kabelitz, D.; Janssen, O.; Heidebrecht, H-J. Down-regulation of the cancer/testis antigen 45 (CT45) is associated with altered tumor cell morphology, adhesion and migration. Cell Commun. Signal., 2013, 11(1), 41.
[http://dx.doi.org/10.1186/1478-811X-11-41]
[39]
Emmanuel, C.; Gava, N.; Kennedy, C.; Balleine, R.L.; Sharma, R.; Wain, G.; Brand, A.; Hogg, R.; Etemadmoghadam, D.; George, J.; Birrer, M.J.; Clarke, C.L.; Chenevix-Trench, G.; Bowtell, D.D.L.; Harnett, P.R.; deFazio, A. Comparison of expression profiles in ovarian epithelium in vivo and ovarian cancer identifies novel candidate genes involved in disease pathogenesis. PLoS One, 2011, 6(3), e17617.
[http://dx.doi.org/10.1371/journal.pone.0017617] [PMID: 21423607]
[40]
Song, C.; Kim, K.B.; Lee, J.H.; Kim, S. Bioinformatic analysis for influential core gene identification and prognostic significance in advanced serous ovarian carcinoma. Medicina (Kaunas), 2021, 57(9), 933.
[http://dx.doi.org/10.3390/medicina57090933] [PMID: 34577856]
[41]
Wu, M.; Sun, Y.; Wu, J.; Liu, G. Identification of hub genes in high-grade serous ovarian cancer using weighted gene co-expression network analysis. Med. Sci. Monit., 2020, 26, e922107.
[http://dx.doi.org/10.12659/MSM.922107] [PMID: 32180586]
[42]
Zhu, Y.; Zheng, M.; Song, D.; Ye, L.; Wang, X. Global comparison of chromosome X genes of pulmonary telocytes with mesenchymal stem cells, fibroblasts, alveolar type II cells, airway epithelial cells, and lymphocytes. J. Transl. Med., 2015, 13(1), 318.
[http://dx.doi.org/10.1186/s12967-015-0669-8] [PMID: 26416664]
[43]
Etter, J.L.; Moysich, K.; Kohli, S.; Lele, S.; Odunsi, K.; Eng, K.H. Transmission of X-linked ovarian cancer: Characterization and implications. Diagnostics (Basel), 2020, 10(2), 90.
[http://dx.doi.org/10.3390/diagnostics10020090] [PMID: 32046210]
[44]
Fagerberg, L.; Hallström, B.M.; Oksvold, P.; Kampf, C.; Djureinovic, D.; Odeberg, J.; Habuka, M.; Tahmasebpoor, S.; Danielsson, A.; Edlund, K.; Asplund, A.; Sjöstedt, E.; Lundberg, E.; Szigyarto, C.A.K.; Skogs, M.; Takanen, J.O.; Berling, H.; Tegel, H.; Mulder, J.; Nilsson, P.; Schwenk, J.M.; Lindskog, C.; Danielsson, F.; Mardinoglu, A.; Sivertsson, Å.; von Feilitzen, K.; Forsberg, M.; Zwahlen, M.; Olsson, I.; Navani, S.; Huss, M.; Nielsen, J.; Ponten, F.; Uhlén, M. Analysis of the human tissue-specific expression by genome-wide integration of transcriptomics and antibody-based proteomics. Mol. Cell. Proteomics, 2014, 13(2), 397-406.
[http://dx.doi.org/10.1074/mcp.M113.035600] [PMID: 24309898]
[45]
Zhan, J.; Cui, P.; Yu, Z.; Qu, W.; Luo, M. SDX on the X chromosome is required for male sex determination. Cell Res., 2022, 32(1), 99-102.
[http://dx.doi.org/10.1038/s41422-021-00539-0] [PMID: 34341487]
[46]
Winham, S.J.; Larson, N.B.; Armasu, S.M.; Fogarty, Z.C.; Larson, M.C.; McCauley, B.M.; Wang, C.; Lawrenson, K.; Gayther, S.; Cunningham, J.M.; Fridley, B.L.; Goode, E.L. Molecular signatures of X chromosome inactivation and associations with clinical outcomes in epithelial ovarian cancer. Hum. Mol. Genet., 2019, 28(8), 1331-1342.
[http://dx.doi.org/10.1093/hmg/ddy444] [PMID: 30576442]
[47]
Larson, N.B.; Fogarty, Z.C.; Larson, M.C.; Kalli, K.R.; Lawrenson, K.; Gayther, S.; Fridley, B.L.; Goode, E.L.; Winham, S.J. An integrative approach to assess X-chromosome inactivation using allele-specific expression with applications to epithelial ovarian cancer. Genet. Epidemiol., 2017, 41(8), 898-914.
[http://dx.doi.org/10.1002/gepi.22091] [PMID: 29119601]
[48]
Kumar, S.; Stecher, G.; Suleski, M.; Hedges, S.B. TimeTree: A resource for timelines, timetrees, and divergence times. Mol. Biol. Evol., 2017, 34(7), 1812-1819.
[http://dx.doi.org/10.1093/molbev/msx116] [PMID: 28387841]
[49]
Frauenfeld, L.; Castrejon-de-Anta, N.; Ramis-Zaldivar, J.E.; Streich, S.; Salmerón-Villalobos, J.; Otto, F.; Mayer, A.K.; Steinhilber, J.; Pinyol, M.; Mankel, B.; Ramsower, C.; Bonzheim, I.; Fend, F.; Rimsza, L.M.; Salaverria, I.; Campo, E.; Balagué, O.; Quintanilla-Martinez, L. Diffuse large B-cell lymphomas in adults with aberrant coexpression of CD10, BCL6, and MUM1 are enriched in IRF4 rearrangements. Blood Adv., 2022, 6(7), 2361-2372.
[http://dx.doi.org/10.1182/bloodadvances.2021006034] [PMID: 34654055]
[50]
Bar, I.; Theate, I.; Haussy, S.; Beniuga, G.; Carrasco, J.; Canon, J.L.; Delrée, P.; Merhi, A. MiR-210 Is overexpressed in tumor-infiltrating plasma cells in triple-negative breast cancer. J. Histochem. Cytochem., 2020, 68(1), 25-32.
[http://dx.doi.org/10.1369/0022155419892965] [PMID: 31787032]
[51]
Zhu, X.; Lan, B.; Yi, X.; He, C.; Dang, L.; Zhou, X.; Lu, Y.; Sun, Y.; Liu, Z.; Bai, X.; Zhang, K.; Li, B.; Li, M.J.; Chen, Y.; Zhang, L. HRP2-DPF3a-BAF complex coordinates histone modification and chromatin remodeling to regulate myogenic gene transcription. Nucleic Acids Res., 2020, 48(12), 6563-6582.
[http://dx.doi.org/10.1093/nar/gkaa441] [PMID: 32459350]
[52]
Mellid, S.; Coloma, J.; Calsina, B.; Monteagudo, M.; Roldán-Romero, J.M.; Santos, M.; Leandro-García, L.J.; Lanillos, J.; Martínez-Montes, Á.M.; Rodríguez-Antona, C.; Montero-Conde, C.; Martínez-López, J.; Ayala, R.; Matias-Guiu, X.; Robledo, M.; Cascón, A. Novel DNMT3A germline variant in a patient with multiple paragangliomas and papillary thyroid carcinoma. Cancers (Basel), 2020, 12(11), 3304.
[http://dx.doi.org/10.3390/cancers12113304] [PMID: 33182397]
[53]
Xie, K.; Fu, C.; Wang, S.; Xu, H.; Liu, S.; Shao, Y.; Gong, Z.; Wu, X.; Xu, B.; Han, J.; Xu, J.; Xu, P.; Jia, X.; Wu, J. Cancer-testis antigens in ovarian cancer: implication for biomarkers and therapeutic targets. J. Ovarian Res., 2019, 12(1), 1.
[http://dx.doi.org/10.1186/s13048-018-0475-z] [PMID: 30609934]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy