Construction and Quantitative Evaluation of a Tissue-Specific Sleeping Beauty by EDL2-Specific Transposase Expression in Esophageal Squamous Carcinoma Cell Line KYSE-30.
ED-L2 promoter
Hyperactive SB100X transposase
KYSE-30
Sleeping Beauty transposon
Journal
Molecular biotechnology
ISSN: 1559-0305
Titre abrégé: Mol Biotechnol
Pays: Switzerland
ID NLM: 9423533
Informations de publication
Date de publication:
Mar 2023
Mar 2023
Historique:
accepted:
29
03
2022
received:
03
07
2021
entrez:
27
4
2022
medline:
22
2
2023
pubmed:
28
4
2022
Statut:
ppublish
Résumé
Gene delivery to esophageal tissue could provide novel treatments for diseases, such as cancer. The Sleeping Beauty (SB) transposon system, as a natural and non-viral tool, is efficient at transferring transgene into the human genome for human cell genetic engineering. The plasmid-based SB transposon can insert into chromosomes through an accurate recombinase-mediated mechanism, providing long-term expression of transgene integrated into the target cells. In this study, we aimed to investigate the activity of ED-L2 tissue-specific promoter that was engineered from the Epstein-Barr Virus (EBV) and combined with the hyperactive SB100X transposase to achieve the stable expression of T2-Onc3 transposon in esophageal squamous epithelial cells. Here we constructed an SB transposon-based plasmid system to obtain the stable expression of transposon upon introduction of a hyperactive SB transposase under the control of tissue-specific ED-L2 promoter via the lipid-based delivery method in the cultured esophageal squamous cell carcinoma cells. Among established human and mouse cell lines, the (ED-L2)-SB100X transposase was active only in human esophageal stratified squamous epithelial and differentiated keratinocytes derived from skin (KYSE-30 and HaCaT cell lines), where it revealed high promoter activity. Data offered that the 782 bp sequence of ED-L2 promoter has a key role in its activity in vitro. The (ED-L2)-SB100X transposase mediated stable integration of T2-Onc3 in KYSE-30 cells, thereby providing further evidence of the tissue specificity of ED-L2 promoter. The KYSE-30 cells modified with the SB system integrate on average 187 copies of the T2-Onc3 transposon in its genome. In aggregate, the (ED-L2)-SB100X transposase can be efficiently applied for the tissue-specific stable expression of a transgene in human KYSE-30 cells using SB transposon.
Identifiants
pubmed: 35474410
doi: 10.1007/s12033-022-00490-4
pii: 10.1007/s12033-022-00490-4
doi:
Substances chimiques
DNA Transposable Elements
0
Transposases
EC 2.7.7.-
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
350-360Subventions
Organisme : mashhad university of medical sciences
ID : 921706
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Querques, I., et al. (2019). A highly soluble Sleeping Beauty transposase improves control of gene insertion. Nature biotechnology, 37(12), 1502–1512.
doi: 10.1038/s41587-019-0291-z
pmcid: 6894935
pubmed: 31685959
Vigdal, T. J., et al. (2002). Common physical properties of DNA affecting target site selection of sleeping beauty and other Tc1/mariner transposable elements. Journal of molecular biology, 323(3), 441–452.
doi: 10.1016/S0022-2836(02)00991-9
pubmed: 12381300
Amberger, M., & Ivics, Z. (2020). Latest advances for the sleeping beauty transposon system: 23 years of insomnia but prettier than ever: Refinement and recent innovations of the sleeping beauty transposon system enabling novel, nonviral genetic engineering applications. BioEssays, 42(11), 2000136.
doi: 10.1002/bies.202000136
Izsvák, Z., & Ivics, Z. (2004). Sleeping beauty transposition: Biology and applications for molecular therapy. Molecular Therapy, 9(2), 147–156.
doi: 10.1016/j.ymthe.2003.11.009
pubmed: 14759798
Katter, K., et al. (2013). Transposon-mediated transgenesis, transgenic rescue, and tissue-specific gene expression in rodents and rabbits. The FASEB Journal, 27(3), 930–941.
doi: 10.1096/fj.12-205526
pmcid: 3574282
pubmed: 23195032
Hudecek, M., et al. (2017). Going non-viral: The Sleeping Beauty transposon system breaks on through to the clinical side. Critical Reviews in Biochemistry and Molecular Biology, 52(4), 355–380.
doi: 10.1080/10409238.2017.1304354
pubmed: 28402189
Ivics, Z., et al. (2007). Targeted Sleeping Beauty transposition in human cells. Molecular therapy, 15(6), 1137–1144.
doi: 10.1038/sj.mt.6300169
pubmed: 17426709
Glover, D. J., Lipps, H. J., & Jans, D. A. (2005). Towards safe, non-viral therapeutic gene expression in humans. Nature Reviews Genetics, 6(4), 299–310.
doi: 10.1038/nrg1577
pubmed: 15761468
Zayed, H., et al. (2004). Development of hyperactive sleeping beauty transposon vectors by mutational analysis. Molecular Therapy, 9(2), 292–304.
doi: 10.1016/j.ymthe.2003.11.024
pubmed: 14759813
Wilber, A., et al. (2007). Messenger RNA as a source of transposase for sleeping beauty transposon–mediated correction of hereditary tyrosinemia type I. Molecular Therapy, 15(7), 1280–1287.
doi: 10.1038/sj.mt.6300160
pubmed: 17440442
Jin, Z., et al. (2011). The hyperactive Sleeping Beauty transposase SB100X improves the genetic modification of T cells to express a chimeric antigen receptor. Gene therapy, 18(9), 849–856.
doi: 10.1038/gt.2011.40
pmcid: 4083583
pubmed: 21451576
Furushima, K., et al. (2012). Insertional mutagenesis by a hybrid piggyBac and sleeping beauty transposon in the rat. Genetics, 192(4), 1235–1248.
doi: 10.1534/genetics.112.140855
pmcid: 3512136
pubmed: 23023007
Cocchiarella, F., et al. (2016). Transcriptionally regulated and nontoxic delivery of the hyperactive Sleeping Beauty transposase. Molecular Therapy-Methods & Clinical Development, 3, 16038.
doi: 10.1038/mtm.2016.38
Izsvák, Z., Ivics, Z., & Plasterk, R. H. (2000). Sleeping Beauty, a wide host-range transposon vector for genetic transformation in vertebrates. Journal of Molecular Biology, 302(1), 93–102.
doi: 10.1006/jmbi.2000.4047
pubmed: 10964563
Staunstrup, N. H., et al. (2009). Hybrid lentivirus-transposon vectors with a random integration profile in human cells. Molecular Therapy, 17(7), 1205–1214.
doi: 10.1038/mt.2009.10
pmcid: 2835219
pubmed: 19240688
Wang, K., Kievit, F. M., & Zhang, M. (2016). Nanoparticles for cancer gene therapy: Recent advances, challenges, and strategies. Pharmacological Research, 114, 56–66.
doi: 10.1016/j.phrs.2016.10.016
pubmed: 27771464
Chen, C., et al. (2018). Promoter-operating targeted expression of gene therapy in cancer: Current stage and prospect. Molecular Therapy-Nucleic Acids, 11, 508–514.
doi: 10.1016/j.omtn.2018.04.003
pmcid: 5992480
pubmed: 29858085
Okabe, S. (1999). Gene expression in transgenic mice using neural promoters. Current Protocols in Neuroscience. https://doi.org/10.1002/0471142301.ns0316s07
doi: 10.1002/0471142301.ns0316s07
Miskey, C., et al. (2005). DNA transposons in vertebrate functional genomics. Cellular and Molecular Life Sciences, 62(6), 629–641.
doi: 10.1007/s00018-004-4232-7
pubmed: 15770416
Nakagawa, H., Inomoto, T., & Rustgi, A. K. (1997). A CACCC box-like cis-regulatory element of the Epstein-Barr virus ED-L2 promoter interacts with a novel transcriptional factor in tissue-specific squamous epithelia. Journal of Biological Chemistry, 272(26), 16688–16699.
doi: 10.1074/jbc.272.26.16688
pubmed: 9195985
Mahmoudian, R. A., Farshchian, M., & Abbaszadegan, M. R. (2021). Genetically engineered mouse models of esophageal cancer. Experimental Cell Research, 406(2), 112757.
doi: 10.1016/j.yexcr.2021.112757
pubmed: 34331909
Nakagawa, H., et al. (1997). The targeting of the cyclin D1 oncogene by an Epstein-Barr virus promoter in transgenic mice causes dysplasia in the tongue, esophagus and forestomach. Oncogene, 14(10), 1185–1190.
doi: 10.1038/sj.onc.1200937
pubmed: 9121767
Mueller, A., et al. (1997). A transgenic mouse model with cyclin D1 overexpression results in cell cycle, epidermal growth factor receptor, and p53 abnormalities. Cancer Research, 57(24), 5542–5549.
pubmed: 9407965
Opitz, O. G., et al. (2002). A mouse model of human oral-esophageal cancer. The Journal of Clinical Investigation, 110(6), 761–769.
doi: 10.1172/JCI0215324
pmcid: 151126
pubmed: 12235107
Stairs, D. B., et al. (2011). Deletion of p120-catenin results in a tumor microenvironment with inflammation and cancer that establishes it as a tumor suppressor gene. Cancer Cell, 19(4), 470–483.
doi: 10.1016/j.ccr.2011.02.007
pmcid: 3077713
pubmed: 21481789
Kikuchi, K., et al. (2017). Epstein-Barr virus (EBV)-associated epithelial and non-epithelial lesions of the oral cavity. Japanese Dental Science Review, 53(3), 95–109.
doi: 10.1016/j.jdsr.2017.01.002
pmcid: 5501733
pubmed: 28725300
Dupuy, A. J., et al. (2009). A modified sleeping beauty transposon system that can be used to model a wide variety of human cancers in mice. Cancer Research, 69(20), 8150–8156.
doi: 10.1158/0008-5472.CAN-09-1135
pmcid: 3700628
pubmed: 19808965
Kim, J. H., et al. (2011). High cleavage efficiency of a 2A peptide derived from porcine teschovirus-1 in human cell lines, zebrafish and mice. PLoS ONE, 6(4), e18556.
doi: 10.1371/journal.pone.0018556
pmcid: 3084703
pubmed: 21602908
Khaleghizadeh, M., et al. (2018). Ectopic expression of human DPPA2 gene in ESCC cell line using retroviral system. Avicenna Journal of Medical Biotechnology, 10(2), 75.
pmcid: 5960063
pubmed: 29849983
Ayyoob, K., et al. (2016). Authentication of newly established human esophageal squamous cell carcinoma cell line (YM-1) using short tandem repeat (STR) profiling method. Tumor Biology, 37(3), 3197–3204.
doi: 10.1007/s13277-015-4133-4
pubmed: 26432330
Mahmoudian, R. A., Farshchian, M., & Abbaszadegan, M. R. (2020). Evaluation and optimization of lipofectamine 3000 reagents for transient gene expression in KYSE-30 esophagus cancer cell line. Archives of Medical Laboratory Sciences, 6, 1–9.
Mahmoudian, R. A., et al. (2021). Interaction between LINC-ROR and stemness state in gastric cancer cells with helicobacter pylori Infection. Iranian Biomedical Journal, 25(3), 157–168.
doi: 10.52547/ibj.25.3.157
Han, X., et al. (2012). Selection of reliable reference genes for gene expression studies using real-time PCR in tung tree during seed development. PLoS ONE, 7(8), e43084.
doi: 10.1371/journal.pone.0043084
pmcid: 3422230
pubmed: 22912794
Schmittgen, T. D., & Livak, K. J. (2008). Analyzing real-time PCR data by the comparative C T method. Nature Protocols, 3(6), 1101.
doi: 10.1038/nprot.2008.73
pubmed: 18546601
Bustin, S. A., et al. (2009). The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Oxford University Press.
Raeisossadati, R., et al. (2011). Quantitative analysis of TEM-8 and CEA tumor markers indicating free tumor cells in the peripheral blood of colorectal cancer patients. International Journal of Colorectal Disease, 26(10), 1265–1270.
doi: 10.1007/s00384-011-1230-8
pubmed: 21573768
Kawakami, K., Largaespada, D. A., & Ivics, Z. (2017). Transposons as tools for functional genomics in vertebrate models. Trends in Genetics, 33(11), 784–801.
doi: 10.1016/j.tig.2017.07.006
pubmed: 28888423
Narayanavari, S. A., et al. (2017). Sleeping Beauty transposition: From biology to applications. Critical Reviews in Biochemistry and Molecular Biology, 52(1), 18–44.
doi: 10.1080/10409238.2016.1237935
pubmed: 27696897
Kuzmin, D., et al. (2010). Novel strong tissue specific promoter for gene expression in human germ cells. BMC Biotechnology, 10(1), 1–10.
doi: 10.1186/1472-6750-10-58
Liew, C. G., et al. (2007). Transient and stable transgene expression in human embryonic stem cells. Stem Cells, 25(6), 1521–1528.
doi: 10.1634/stemcells.2006-0634
pubmed: 17379764
Tabar, M. S., et al. (2015). Evaluating electroporation and lipofectamine approaches for transient and stable transgene expressions in human fibroblasts and embryonic stem cells. Cell Journal (Yakhteh), 17(3), 438.
Jenkins, T. D., et al. (1998). Transactivation of the human keratin 4 and Epstein-Barr virus ED-L2 promoters by gut-enriched Krüppel-like factor. Journal of Biological Chemistry, 273(17), 10747–10754.
doi: 10.1074/jbc.273.17.10747
pubmed: 9553140
Jenkins, T. D., Nakagawa, H., & Rustgi, A. K. (1997). The keratinocyte-specific Epstein-Barr virus ED-L2 promoter is regulated by phorbol 12-myristate 13-acetate through twocis-regulatory elements containing E-box and Krüppel-like factor motifs. Journal of Biological Chemistry, 272(39), 24433–24442.
doi: 10.1074/jbc.272.39.24433
pubmed: 9305903
Tétreault, M.-P., et al. (2016). Esophageal expression of active IκB Kinase-β in mice up-regulates tumor necrosis factor and granulocyte-macrophage colony-stimulating factor, promoting inflammation and angiogenesis. Gastroenterology, 150(7), 1609-1619.e11.
doi: 10.1053/j.gastro.2016.02.025
pubmed: 26896735
Tetreault, M. P., et al. (2010). Klf4 overexpression activates epithelial cytokines and inflammation-mediated esophageal squamous cell cancer in mice. Gastroenterology, 139(6), 2124-2134.e9.
doi: 10.1053/j.gastro.2010.08.048
pubmed: 20816834
Andl, C. D., et al. (2003). Epidermal growth factor receptor mediates increased cell proliferation, migration, and aggregation in esophageal keratinocytes in vitro and in vivo. Journal of Biological Chemistry, 278(3), 1824–1830.
doi: 10.1074/jbc.M209148200
pubmed: 12435727
Belur, L. R., et al. (2003). Gene insertion and long-term expression in lung mediated by the Sleeping Beauty transposon system. Molecular Therapy, 8(3), 501–507.
doi: 10.1016/S1525-0016(03)00211-9
pubmed: 12946324
Fong, L. Y., et al. (2003). Combined cyclin D1 overexpression and zinc deficiency disrupts cell cycle and accelerates mouse forestomach carcinogenesis. Cancer Research, 63(14), 4244–4252.
pubmed: 12874033
Galla, M., et al. (2011). Avoiding cytotoxicity of transposases by dose-controlled mRNA delivery. Nucleic Acids Research, 39(16), 7147–7160.
doi: 10.1093/nar/gkr384
pmcid: 3167617
pubmed: 21609958
Izsvák, Z., et al. (2009). Efficient stable gene transfer into human cells by the Sleeping Beauty transposon vectors. Methods, 49(3), 287–297.
doi: 10.1016/j.ymeth.2009.07.001
pubmed: 19615447
Dalsgaard, T., et al. (2009). Shielding of sleeping beauty DNA transposon-delivered transgene cassettes by heterologous insulators in early embryonal cells. Molecular Therapy, 17(1), 121–130.
doi: 10.1038/mt.2008.224
pubmed: 18985029
Mátés, L., et al. (2009). Molecular evolution of a novel hyperactive Sleeping Beauty transposase enables robust stable gene transfer in vertebrates. Nature Genetics, 41(6), 753–761.
doi: 10.1038/ng.343
pubmed: 19412179
Grabundzija, I., et al. (2010). Comparative analysis of transposable element vector systems in human cells. Molecular Therapy, 18(6), 1200–1209.
doi: 10.1038/mt.2010.47
pmcid: 2889740
pubmed: 20372108
Lajos, M., et al. (2009). Sleeping Beauty transposase enables robust stable gene transfer in vertebrates. Nature Genetics, 41, 753–761.
doi: 10.1038/ng.343