Novel role of sex-determining region Y-box 7 (SOX7) in tumor biology and cardiovascular developmental biology

Hou, 2017, Molecular basis for the genome engagement by Sox proteins, Semin. Cell Dev. Biol., 63, 2, 10.1016/j.semcdb.2016.08.005 Schepers, 2002, Twenty pairs of sox: extent, homology, and nomenclature of the mouse and human sox transcription factor gene families, Dev. Cell, 3, 167, 10.1016/S1534-5807(02)00223-X Harley, 1994, Definition of a consensus DNA binding site for SRY, Nucleic Acids Res., 22, 1500, 10.1093/nar/22.8.1500 Stovall, 2014, SOX7: from a developmental regulator to an emerging tumor suppressor, Histol. Histopathol., 29, 439 Hosking, 2009, Sox7 and Sox17 are strain-specific modifiers of the lymphangiogenic defects caused by Sox18 dysfunction in mice, Development, 136, 2385, 10.1242/dev.034827 Pennisi, 2000, Mice null for sox18 are viable and display a mild coat defect, Mol. Cell. Biol., 20, 9331, 10.1128/MCB.20.24.9331-9336.2000 Lilly, 2017, SOXF transcription factors in cardiovascular development, Semin. Cell Dev. Biol., 63, 50, 10.1016/j.semcdb.2016.07.021 Suba, 2015, DNA stabilization by the upregulation of estrogen signaling in BRCA gene mutation carriers, Drug Des. Devel. Ther., 9, 2663, 10.2147/DDDT.S84437 Suba, 2017, Activating mutations of ESR1, BRCA1 and CYP19 aromatase genes confer tumor response in breast cancers treated with antiestrogens, Recent Pat. Anticancer Drug Discov., 12, 136, 10.2174/1574892812666170227110842 Suba, 2018, Amplified crosstalk between estrogen binding and GFR signaling mediated pathways of ER activation drives responses in tumors treated with endocrine disruptors, Recent Pat. Anticancer Drug Discov., 13, 428, 10.2174/1574892813666180720123732 Yang, 2017, FOXC1 in cancer development and therapy: deciphering its emerging and divergent roles, Ther. Adv. Med. Oncol., 9, 797, 10.1177/1758834017742576 Man, 2015, Suppression of SOX7 by DNA methylation and its tumor suppressor function in acute myeloid leukemia, Blood, 125, 3928, 10.1182/blood-2014-06-580993 Stovall, 2013, The regulation of SOX7 and its tumor suppressive role in breast cancer, Am. J. Pathol., 183, 1645, 10.1016/j.ajpath.2013.07.025 Saegusa, 2012, Sox4 functions as a positive regulator of beta-catenin signaling through upregulation of TCF4 during morular differentiation of endometrial carcinomas, Lab. Invest., 92, 511, 10.1038/labinvest.2011.196 Wang, 2018, Classic SRY-box protein SOX7 functions as a tumor suppressor regulating WNT signaling and is methylated in renal cell carcinoma, FASEB J. Zhou, 2011, SOX7 is involved in aspirin-mediated growth inhibition of human colorectal cancer cells, World J. Gastroenterol., 17, 4922, 10.3748/wjg.v17.i44.4922 Afouda, 2018, Genome-wide transcriptomics analysis identifies sox7 and sox18 as specifically regulated by gata4 in cardiomyogenesis, Dev. Biol. (Basel), 434, 108, 10.1016/j.ydbio.2017.11.017 Wong, 2013, beta-catenin is essential for efficient in vitro premyogenic mesoderm formation but can be partially compensated by retinoic acid signalling, PLoS One, 8, e57501, 10.1371/journal.pone.0057501 Yang, 2016, The PDGF-BB-SOX7 axis-modulated IL-33 in pericytes and stromal cells promotes metastasis through tumour-associated macrophages, Nat. Commun., 7, 11385, 10.1038/ncomms11385 Yan, 2018, miR-24-3p promotes cell migration and proliferation in lung cancer by targeting SOX7, J. Cell. Biochem., 119, 3989, 10.1002/jcb.26553 Wang, 2017, MicroRNA-616 promotes the growth and metastasis of non-small cell lung cancer by targeting SOX7, Oncol. Rep., 38, 2078, 10.3892/or.2017.5854 Han, 2017, MiR-9 is involved in TGF-beta1-induced lung cancer cell invasion and adhesion by targeting SOX7, J. Cell. Mol. Med., 21, 2000, 10.1111/jcmm.13120 Peng, 2018, Knockdown of miR935 increases paclitaxel sensitivity via regulation of SOX7 in nonsmallcell lung cancer, Mol. Med. Rep., 18, 3397 Wang, 2017, LncRNA MEG3 enhances cisplatin sensitivity in non-small cell lung cancer by regulating miR-21-5p/SOX7 axis, Onco. Ther., 10, 5137, 10.2147/OTT.S146423 Liu, 2017, miR-935 promotes liver Cancer cell proliferation and migration by targeting SOX7, Oncol. Res., 25, 427, 10.3727/096504016X14747300207374 Ma, 2014, miR-24 promotes the proliferation and invasion of HCC cells by targeting SOX7, Tumour Biol., 35, 10731, 10.1007/s13277-014-2018-6 Wu, 2014, Mir-184 post-transcriptionally regulates SOX7 expression and promotes cell proliferation in human hepatocellular carcinoma, PLoS One, 9, e88796, 10.1371/journal.pone.0088796 Zheng, 2016, MicroRNA-452 promotes stem-like cells of hepatocellular carcinoma by inhibiting Sox7 involving Wnt/beta-catenin signaling pathway, Oncotarget, 7, 28000, 10.18632/oncotarget.8584 Yang, 2016, miR-935 promotes gastric cancer cell proliferation by targeting SOX7, Biomed. Pharmacother., 79, 153, 10.1016/j.biopha.2016.01.011 Hao, 2016, MiR-595 targeting regulation of SOX7 expression promoted cell proliferation of human glioblastoma, Biomed. Pharmacother., 80, 121, 10.1016/j.biopha.2016.03.008 Xiuju, 2016, SOX7 inhibits tumor progression of glioblastoma and is regulated by miRNA-24, Open Med. Wars. (Wars), 11, 133, 10.1515/med-2016-0026 Bai, 2017, MiR-616 promotes proliferation and inhibits apoptosis in glioma cells by suppressing expression of SOX7 via the Wnt signaling pathway, Eur. Rev. Med. Pharmacol. Sci., 21, 5630 Bao, 2017, Overexpression of miR-664 is associated with enhanced osteosarcoma cell migration and invasion ability via targeting SOX7, Clin. Exp. Med., 17, 51, 10.1007/s10238-015-0398-6 Shen, 2015, MiR-492 contributes to cell proliferation and cell cycle of human breast cancer cells by suppressing SOX7 expression, Tumour Biol., 36, 1913, 10.1007/s13277-014-2794-z Yang, 2018, Overexpression of microRNA-34a attenuates proliferation and induces apoptosis in pituitary adenoma cells via SOX7, Mol. Ther. Oncolytics, 10, 40, 10.1016/j.omto.2018.07.001 Li, 2017, Long noncoding RNA AB073614 promotes the malignance of glioma by activating Wnt/beta-catenin signaling through downregulating SOX7, Oncotarget, 8, 65577, 10.18632/oncotarget.19305 Liz, 2016, lncRNAs and microRNAs with a role in cancer development, Biochim. Biophys. Acta, 1859, 169, 10.1016/j.bbagrm.2015.06.015 Liu, 2016, SOX7 co-regulates Wnt/beta-catenin signaling with Axin-2: both expressed at low levels in breast cancer, Sci. Rep., 6, 26136, 10.1038/srep26136 Cui, 2014, Decreased expression of Sox7 correlates with the upregulation of the Wnt/beta-catenin signaling pathway and the poor survival of gastric cancer patients, Int. J. Mol. Med., 34, 197, 10.3892/ijmm.2014.1759 Kramps, 2002, Wnt/wingless signaling requires BCL9/legless-mediated recruitment of pygopus to the nuclear beta-catenin-TCF complex, Cell, 109, 47, 10.1016/S0092-8674(02)00679-7 Zhao, 2016, SOX7 is associated with the suppression of human glioma by HMG-box dependent regulation of Wnt/beta-catenin signaling, Cancer Lett., 375, 100, 10.1016/j.canlet.2016.02.044 Chan, 2012, Down-regulation of Sox7 is associated with aberrant activation of Wnt/b-catenin signaling in endometrial cancer, Oncotarget, 3, 1546, 10.18632/oncotarget.667 Guo, 2008, Sox7 is an independent checkpoint for beta-catenin function in prostate and colon epithelial cells, Mol. Cancer Res., 6, 1421, 10.1158/1541-7786.MCR-07-2175 Fan, 2018, SOX7 Suppresses Wnt Signaling by Disrupting beta-Catenin/BCL9 Interaction, DNA Cell Biol., 37, 126, 10.1089/dna.2017.3866 Liu, 2014, Reduced expression of SOX7 in ovarian cancer: a novel tumor suppressor through the Wnt/beta-catenin signaling pathway, J. Ovarian Res., 7, 87, 10.1186/s13048-014-0087-1 Wang, 2014, The suppressive role of SOX7 in hepatocarcinogenesis, PLoS One, 9, e97433, 10.1371/journal.pone.0097433 Inoue, 2016, Cooperation of Sox4 with beta-catenin/p300 complex in transcriptional regulation of the Slug gene during divergent sarcomatous differentiation in uterine carcinosarcoma, BMC Cancer, 16, 53, 10.1186/s12885-016-2090-y Murakami, 2004, SOX7 and GATA-4 are competitive activators of Fgf-3 transcription, J. Biol. Chem., 279, 28564, 10.1074/jbc.M313814200 Zhang, 2018, SOX7 target genes and their contribution to its tumor suppressive function, Int. J. Mol. Sci., 19 Schaaf, 2010, Silencing of SPRY1 triggers complete regression of rhabdomyosarcoma tumors carrying a mutated RAS gene, Cancer Res., 70, 762, 10.1158/0008-5472.CAN-09-2532 Dallol, 2002, SLIT2, a human homologue of the Drosophila Slit2 gene, has tumor suppressor activity and is frequently inactivated in lung and breast cancers, Cancer Res., 62, 5874 Salazar, 2015, TRIB3 suppresses tumorigenesis by controlling mTORC2/AKT/FOXO signaling, Mol. Cell. Oncol., 2, e980134 Su, 2017, Emodin induces apoptosis of lung cancer cells through ER stress and the TRIB3/NF-kappaB pathway, Oncol. Rep., 37, 1565, 10.3892/or.2017.5428 Dong, 2016, Overexpression of TRIB3 promotes angiogenesis in human gastric cancer, Oncol. Rep., 36, 2339, 10.3892/or.2016.5017 Liu, 2014, Increased MTHFD2 expression is associated with poor prognosis in breast cancer, Tumour Biol., 35, 8685, 10.1007/s13277-014-2111-x Carmeliet, 2011, Molecular mechanisms and clinical applications of angiogenesis, Nature, 473, 298, 10.1038/nature10144 de Aguiar, 2019, Exploring the immunological mechanisms underlying the anti-vascular endothelial growth factor activity in tumors, Front. Immunol., 10, 1023, 10.3389/fimmu.2019.01023 Sawamiphak, 2010, Ephrin-B2 regulates VEGFR2 function in developmental and tumour angiogenesis, Nature, 465, 487, 10.1038/nature08995 Prewett, 1999, Antivascular endothelial growth factor receptor (fetal liver kinase 1) monoclonal antibody inhibits tumor angiogenesis and growth of several mouse and human tumors, Cancer Res., 59, 5209 Spratlin, 2010, Phase I pharmacologic and biologic study of ramucirumab (IMC-1121B), a fully human immunoglobulin G1 monoclonal antibody targeting the vascular endothelial growth factor receptor-2, J. Clin. Oncol., 28, 780, 10.1200/JCO.2009.23.7537 Kim, 2018, Sox7 promotes high-grade glioma by increasing VEGFR2-mediated vascular abnormality, J. Exp. Med., 215, 963, 10.1084/jem.20170123 Kim, 2016, Tumor-associated macrophages and neutrophils in tumor microenvironment, Mediators Inflamm., 2016, 6058147, 10.1155/2016/6058147 Jinushi, 2015, Tumor-associated macrophages as an emerging target against tumors: creating a new path from bench to bedside, Biochim. Biophys. Acta, 1855, 123 MA, 2019, Crossroad between obesity and cancer: a defective signaling function of heavily lipid laden adipocytes (online first) Wang, 2017, Clinical signi fi cance and prognostic value of SOX7 expression in liver and pancreatic carcinoma, Mol. Med. Rep., 16, 499, 10.3892/mmr.2017.6660 Wolfgang, 2013, Recent progress in pancreatic cancer, CA, Cancer J Clin, 63, 318, 10.3322/caac.21190 Hu, 2016, Clinical and pathological significance of N-Myc downstream-regulated gene 2 (NDRG2) in diverse human cancers, Apoptosis, 21, 675, 10.1007/s10495-016-1244-3 Torre, 2015, Global cancer statistics, 2012, CA Cancer J. Clin., 65, 87, 10.3322/caac.21262 Hu, 2016, Emerging role of N-myc downstream-regulated gene 2 (NDRG2) in cancer, Oncotarget, 7, 209, 10.18632/oncotarget.6228 Zhang, 2009, SOX7, down-regulated in colorectal cancer, induces apoptosis and inhibits proliferation of colorectal cancer cells, Cancer Lett., 277, 29, 10.1016/j.canlet.2008.11.014 Li, 2012, Decreased expression of SOX7 is correlated with poor prognosis in lung adenocarcinoma patients, Pathol. Oncol. Res., 18, 1039, 10.1007/s12253-012-9542-8 Hayano, 2013, SOX7 is down-regulated in lung cancer, J. Exp. Clin. Cancer Res., 32, 17, 10.1186/1756-9966-32-17 Rani, 2017, Genome-wide DNA methylation profiling integrated with gene expression profiling identifies PAX9 as a novel prognostic marker in chronic lymphocytic leukemia, Clin. Epigenetics, 9, 57, 10.1186/s13148-017-0356-0 Fan, 2012, Methylation of the CpG island near SOX7 gene promoter is correlated with the poor prognosis of patients with myelodysplastic syndrome, Tohoku J. Exp. Med., 227, 119, 10.1620/tjem.227.119 Zhong, 2012, SOXs in human prostate cancer: implication as progression and prognosis factors, BMC Cancer, 12, 248, 10.1186/1471-2407-12-248 Pula, 2013, Impact of SOX18 expression in cancer cells and vessels on the outcome of invasive ductal breast carcinoma, Cell. Oncol. Dordr. (Dordr), 36, 469 Yamamoto, 2008, Identification of genes that exhibit changes in expression on the 8p chromosomal arm by the Systematic Multiplex RT-PCR (SM RT-PCR) and DNA microarray hybridization methods, Gene Expr., 14, 217, 10.3727/105221608786883816 Oh, 2017, Decreased expression of SOX7 induces cell proliferation and invasion and correlates with poor prognosis in oral squamous cell carcinoma, J. Oral Pathol. Med., 46, 752, 10.1111/jop.12566 Katoh, 2002, Expression of human SOX7 in normal tissues and tumors, Int. J. Mol. Med., 9, 363 Futaki, 2003, Molecular basis of constitutive production of basement membrane components. Gene expression profiles of Engelbreth-Holm-Swarm tumor and F9 embryonal carcinoma cells, J. Biol. Chem., 278, 50691, 10.1074/jbc.M304985200 Wiech, 2009, Genome-wide analysis of genetic alterations in Barrett’s adenocarcinoma using single nucleotide polymorphism arrays, Lab. Invest., 89, 385, 10.1038/labinvest.2008.67 Seguin, 2008, Establishment of endoderm progenitors by SOX transcription factor expression in human embryonic stem cells, Cell Stem Cell, 3, 182, 10.1016/j.stem.2008.06.018 Shirai, 2005, Identification of an enhancer that controls up-regulation of fibronectin during differentiation of embryonic stem cells into extraembryonic endoderm, J. Biol. Chem., 280, 7244, 10.1074/jbc.M410731200 Lim, 2008, Sall4 regulates distinct transcription circuitries in different blastocyst-derived stem cell lineages, Cell Stem Cell, 3, 543, 10.1016/j.stem.2008.08.004 Artus, 2011, The primitive endoderm lineage of the mouse blastocyst: sequential transcription factor activation and regulation of differentiation by Sox17, Dev. Biol. (Basel), 350, 393, 10.1016/j.ydbio.2010.12.007 Futaki, 2004, Sox7 plays crucial roles in parietal endoderm differentiation in F9 embryonal carcinoma cells through regulating Gata-4 and Gata-6 expression, Mol. Cell. Biol., 24, 10492, 10.1128/MCB.24.23.10492-10503.2004 Wat, 2014, Sox7 in vascular development: review, insights and potential mechanisms, Int. J. Dev. Biol., 58, 1, 10.1387/ijdb.130323mw Costa, 2012, SOX7 regulates the expression of VE-cadherin in the haemogenic endothelium at the onset of haematopoietic development, Development, 139, 1587, 10.1242/dev.071282 Lilly, 2016, Interplay between SOX7 and RUNX1 regulates hemogenic endothelial fate in the yolk sac, Development, 143, 4341, 10.1242/dev.140970 Lilly, 2017, SOX7 expression is critically required in FLK1-expressing cells for vasculogenesis and angiogenesis during mouse embryonic development, Mech. Dev., 146, 31, 10.1016/j.mod.2017.05.004 Serrano, 2010, Contrasting effects of Sox17- and Sox18-sustained expression at the onset of blood specification, Blood, 115, 3895, 10.1182/blood-2009-10-247395 Nelson, 2009, Lineage specification of Flk-1+ progenitors is associated with divergent Sox7 expression in cardiopoiesis, Differentiation, 77, 248, 10.1016/j.diff.2008.10.012 Duong, 2014, VEGFD regulates blood vascular development by modulating SOX18 activity, Blood, 123, 1102, 10.1182/blood-2013-04-495432 Sakamoto, 2007, Redundant roles of Sox17 and Sox18 in early cardiovascular development of mouse embryos, Biochem. Biophys. Res. Commun., 360, 539, 10.1016/j.bbrc.2007.06.093 Molck, 2017, Genomic imbalances in syndromic congenital heart disease, J. Pediatr., 93, 497, 10.1016/j.jped.2016.11.007 Mei, 2014, [Analysis of genomic copy number variations in two unrelated neonates with 8p deletion and duplication associated with congenital heart disease], Zhonghua Er Ke Za Zhi, 52, 460 Long, 2013, A potential relationship among beta-defensins haplotype, SOX7 duplication and cardiac defects, PLoS One, 8, e72515, 10.1371/journal.pone.0072515 Savage, 2009, SOX15 and SOX7 differentially regulate the myogenic program in P19 cells, Stem Cells, 27, 1231, 10.1002/stem.57 Herpers, 2008, Redundant roles for sox7 and sox18 in arteriovenous specification in zebrafish, Circ. Res., 102, 12, 10.1161/CIRCRESAHA.107.166066 Chiang, 2017, SoxF factors induce Notch1 expression via direct transcriptional regulation during early arterial development, Development, 144, 2629, 10.1242/dev.146241 Hermkens, 2015, Sox7 controls arterial specification in conjunction with hey2 and efnb2 function, Development, 142, 1695, 10.1242/dev.117275 Sacilotto, 2013, Analysis of Dll4 regulation reveals a combinatorial role for Sox and Notch in arterial development, Proc Natl Acad Sci U S A, 110, 11893, 10.1073/pnas.1300805110