Targeting Serous Epithelial Ovarian Cancer with Designer Zinc Finger Transcription Factors
Open accessAbstract
Background: There is a need for novel targeted therapies for metastatic ovarian cancers.Results: We reactivated the tumor suppressor Maspin in ovarian carcinoma cells by delivering tumor-specific nanoparticles encapsulating a chemically modified ATF-mRNA.Conclusion: LPR nanoparticles encapsulating the ATF mRNA inhibited ovarian cancer tumor growth in a mouse model.Significance: We report the first non-viral delivery of an ATF in vivo and the discovery of novel anti-metastatic targets for ovarian cancer.Ovarian cancer is the leading cause of death among gynecological malignancies.It is detected at late stages when the disease is spread through the abdominal cavity in a condition known as peritoneal carcinomatosis.Thus, there is an urgent need to develop novel therapeutic interventions to target advanced stages of ovarian cancer.Mammary serine protease inhibitor (Maspin) represents an important metastasis suppressor initially identified in breast cancer.Herein we have generated a sequence-specific zinc finger artificial transcription factor (ATF) to up-regulate the Maspin promoter in aggressive ovarian cancer cell lines and to interrogate the therapeutic potential of Maspin in ovarian cancer.We found that although Maspin was expressed in some primary ovarian tumors, the promoter was epigenetically silenced in cell lines derived from ascites.Transduction of the ATF in MOVCAR 5009 cells derived from ascitic cultures of a TgMISIIR-TAg mouse model of ovarian cancer resulted in tumor cell growth inhibition, impaired cell invasion, and severe disruption of actin cytoskeleton.Systemic delivery of lipid-protamine-RNA nanoparticles encapsulating a chemically modified ATF mRNA resulted in inhibition of ovarian cancer cell growth in nude mice accompanied with Maspin re-expression in the treated tumors.Gene expression microarrays of ATF-transduced cells revealed an exceptional specificity for the Maspin promoter.These analyses identified novel targets coregulated with Maspin in human short-term cultures derived from ascites, such as TSPAN12, that could mediate the antimetastatic phenotype of the ATF.Our work outlined the first targeted, non-viral delivery of ATFs into tumors with potential clinical applications for metastatic ovarian cancers.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Regulation of other tumour-associated genes, such as PLK1, Bax, Maspin, PUMA and PTEN, can delay tumour growth in vivo.
“Similarly, the regulation of other tumour-associated genes, such as PLK1 (ref.133), Bax219, Maspin37, PUMA70 and PTEN220, can delay tumour growth in vivo.”
From Lipid nanoparticles for mRNA delivery (2021) · cites this paper as [37]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Jemal, A., Bray, F., Ferlay, J., Ward, E., & Forman, D. (2011) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.20107 · Cited by 54,708 · see citing works
Rubin, M., & Stephen, C. D. (1993) · Cited by 3,161 · see citing works
Warren, L., Manos, P. D., Ahfeldt, T., Loh, Y.-H., Li, H., Lau, F., Ebina, W., Mandal, P. K., Smith, Z. D., Meissner, A., et al. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.08.012 · Cited by 2,662 · see citing works
Zinc Finger-DNA Recognition: Crystal Structure of a Zif268-DNA Complex at 2.1 Å
Pavletich, N. P., & Pabo, C. O. (1991) · Science · doi:10.1126/science.2028256 · Cited by 2,081 · see citing works
Identifying biological themes within lists of genes with EASE
Hosack, D. A., Dennis, G., Sherman, B. T., Lane, H. C., & Lempicki, R. A. (2003) · Genome biology · doi:10.1186/gb-2003-4-10-r70 · Cited by 1,950 · see citing works
Tetraspanin functions and associated microdomains
Hemler, M. E. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1736 · Cited by 1,355 · cited 1× · see citing works
“Tetraspanins are transmembrane proteins that physically associate with integrins to transduce signals inside the cell (60).”
BackgroundHerschkowitz, J. I., Simin, K. J., Weigman, V., Mikaelian, I., Usary, J., Hu, Z., Rasmussen, K., Jones, L. P., Assefnia, S., Chandrasekharan, S., et al. (2007) · Genome biology · doi:10.1186/gb-2007-8-5-r76 · Cited by 1,287 · see citing works
Vascular Endothelial Growth Factor
Ferrara, N. (2009) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.108.179663 · Cited by 1,283 · see citing works
Risch, H. A., McLaughlin, J. R., Cole, D. E. C., Rosen, B. P., Bradley, L., Kwan, E., Jack, E., Vesprini, D., Kuperstein, G., Abrahamson, J., et al. (2001) · The American Journal of Human Genetics · doi:10.1086/318787 · Cited by 985 · see citing works
Maspin, a Serpin with Tumor-Suppressing Activity in Human Mammary Epithelial Cells
Zou, Z., Anisowicz, A., Hendrix, M. J. C., Thor, A. D., Neveu, M. J., Sheng, S., Rafidi, K., Seftor, E. A., & Sager, R. (1994) · Science · doi:10.1126/science.8290962 · Cited by 912 · see citing works
Wright, M. H., Calcagno, A. M., Salcido, C. D., Carlson, M. D., Ambudkar, S. V., & Varticovski, L. (2008) · Breast Cancer Research · doi:10.1186/bcr1855 · Cited by 643 · see citing works
Beerli, R. R., Segal, D. J., Dreier, B., & Barbas, C. F. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.25.14628 · Cited by 539 · see citing works
Durai, S. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki912 · Cited by 522 · see citing works
Engineering polydactyl zinc-finger transcription factors
Beerli, R. R., & Barbas, C. F. (2002) · Nature Biotechnology · doi:10.1038/nbt0202-135 · Cited by 495 · see citing works
Brenner, R., Jegla, T. J., Wickenden, A., Liu, Y., & Aldrich, R. W. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.9.6453 · Cited by 480 · see citing works
Role for DNA methylation in the control of cell type–specific maspin expression
Futscher, B. W., Oshiro, M. M., Wozniak, R. J., Holtan, N., Hanigan, C. L., Duan, H., & Domann, F. E. (2002) · Nature Genetics · doi:10.1038/ng886 · Cited by 442 · see citing works
Sheng, S., Carey, J., Seftor, E. A., Dias, L., Hendrix, M. J. C., & Sager, R. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.21.11669 · Cited by 376 · see citing works
Positive and negative regulation of endogenous genes by designed transcription factors
Beerli, R. R., Dreier, B., & Barbas, C. F. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.040552697 · Cited by 349 · see citing works
Dreier, B., Beerli, R. R., Segal, D. J., Flippin, J. D., & Barbas, C. F. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m102604200 · Cited by 329 · see citing works
Design of polydactyl zinc-finger proteins for unique addressing within complex genomes
Liu, Q., Segal, D. J., Ghiara, J. B., & Barbas, C. F. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.11.5525 · Cited by 327 · see citing works
Ikeyama, S., Koyama, M., Yamaoko, M., Sasada, R., & Miyake, M. (1993) · The Journal of Experimental Medicine · doi:10.1084/jem.177.5.1231 · Cited by 280 · see citing works
Banerjee, R., Tyagi, P., Li, S., & Huang, L. (2004) · International Journal of Cancer · doi:10.1002/ijc.20452 · Cited by 274 · see citing works
Self-citationLiu, P., Rebar, E. J., Zhang, L., Liu, Q., Jamieson, A. C., Liang, Y., Qi, H., Li, P.-X., Chen, B., Mendel, M. C., et al. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m011172200 · Cited by 239 · see citing works
Herrera, F. J., & Triezenberg, S. J. (2004) · Journal of Virology · doi:10.1128/jvi.78.18.9689-9696.2004 · Cited by 210 · see citing works
Comparative oncogenomics identifies breast tumors enriched in functional tumor-initiating cells
Herschkowitz, J. I., Zhao, W., Zhang, M., Usary, J., Murrow, G., Edwards, D., Knezevic, J., Greene, S. B., Darr, D. B., Troester, M. A., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1018862108 · Cited by 209 · see citing works
TALE nucleases: tailored genome engineering made easy
Mussolino, C., & Cathomen, T. (2012) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2012.01.013 · Cited by 205 · see citing works
The paradoxical expression of maspin in ovarian carcinoma.
Sood, A. K., Fletcher, M. S., Gruman, L. M., Coffin, J. E., Jabbari, S., Khalkhali‐Ellis, Z., Arbour, N. C., Seftor, E. A., & Hendrix, M. J. C. (2002) · PubMed · Cited by 205 · see citing works
Huang, C., Kohno, N., Ogawa, E., Adachi, M., Taki, T., & Miyake, M. (1998) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65639-8 · Cited by 203 · see citing works
Building zinc fingers by selection: toward a therapeutic application.
Wu, H., Yang, W. P., & Barbas, C. F. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.2.344 · Cited by 195 · see citing works
Synthetic Zinc Finger Transcription Factor Action at an Endogenous Chromosomal Site
Zhang, L., Spratt, S. K., Liu, Q., Johnstone, B. H., Qi, H., Raschke, E. E., Jamieson, A. C., Rebar, E. J., Wolffe, A. P., & Case, C. C. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m005341200 · Cited by 180 · see citing works
maspin suppresses the invasive phenotype of human breast carcinoma.
Seftor, R. E. B., Seftor, E. A., Sheng, S., Pemberton, P. A., Sager, R., & Hendrix, M. J. C. (1998) · PubMed · Cited by 163 · see citing works
Havrilesky, L. J., Darcy, K. M., Hamdan, H. B., Priore, R. L., Leon, J., Bell, J., & Berchuck, A. (2003) · Journal of Clinical Oncology · doi:10.1200/jco.2003.11.052 · Cited by 156 · see citing works
Zinc-finger nucleases: a powerful tool for genetic engineering of animals
Remy, S., Tesson, L., Ménoret, S., Usal, C., Scharenberg, A. M., & Anegón, I. (2009) · Transgenic Research · doi:10.1007/s11248-009-9323-7 · Cited by 139 · see citing works
Maspin expression in invasive breast cancer: association with other prognostic factors
Mohsin, S. K., Zhang, M., Clark, G. M., & Allred, D. C. (2003) · The Journal of Pathology · doi:10.1002/path.1319 · Cited by 137 · see citing works
Ovarian cancer: pathology, biology, and disease models
Daniel, G. R. (2009) · Frontiers in bioscience · doi:10.2741/3364 · Cited by 131 · see citing works
Scanning the human genome with combinatorial transcription factor libraries
Blancafort, P., Magnenat, L., & Barbas, C. F. (2003) · Nature Biotechnology · doi:10.1038/nbt794 · Cited by 124 · see citing works
Self-citationThe expression and functional characterization of sigma (σ) 1 receptors in breast cancer cell lines
Aydar, E., Onganer, P. U., Perrett, R. M., Djamgoz, M. B. A., & Palmer, C. P. (2006) · Cancer Letters · doi:10.1016/j.canlet.2005.11.011 · Cited by 117 · see citing works
Advances in the management of epithelial ovarian cancer.
Berkenblit, A., & Cannistra, S. A. (2005) · PubMed · Cited by 107 · see citing works
Re-activation of a dormant tumor suppressor gene maspin by designed transcription factors
Beltrán, A. S., Parikh, S., Liu, Y., Cuevas, B. D., Johnson, G. L., Futscher, B. W., & Blancafort, P. (2006) · Oncogene · doi:10.1038/sj.onc.1210072 · Cited by 103 · see citing works
Self-citationGeneration of tumor-initiating cells by exogenous delivery of OCT4transcription factor
Beltrán, A. S., Rivenbark, A. G., Richardson, B. T., Yuan, X., Quian, H., Hunt, J. P., Zimmerman, E. I., Graves, L. M., & Blancafort, P. (2011) · Breast Cancer Research · doi:10.1186/bcr3019 · Cited by 98 · see citing works
Self-citationRice, J. C. (2000) · Nucleic Acids Research · doi:10.1093/nar/28.17.3233 · Cited by 96 · see citing works
Tetraspanin protein contributions to cancer
Wang, H.-X., Li, Q., Sharma, C., Knoblich, K., & Hemler, M. E. (2011) · Biochemical Society Transactions · doi:10.1042/bst0390547 · Cited by 95 · see citing works
Li, Y., Ye, F., Hu, Y., Lü, W., & Xie, X. (2009) · Analytical Biochemistry · doi:10.1016/j.ab.2009.07.022 · Cited by 95 · see citing works
Pfetin as a Prognostic Biomarker of Gastrointestinal Stromal Tumors Revealed by Proteomics
Suehara, Y., Kondo, T., Seki, K., Shibata, T., Fujii, K., Gotoh, M., Hasegawa, T., Shimada, Y., Sasako, M., Shimoda, T., et al. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-1478 · Cited by 95 · see citing works
Zou, Z., Zhang, Y., Young, D., Gleave, M. G., Rennie, P. S., Connell, T., Connelly, R. R., Moul, J. W., Srivastava, S. K., & Sesterhenn, I. A. (2002) · PubMed · Cited by 94 · see citing works
Tetraspanins and tumor progression
Richardson, M. M., Jennings, L. K., & Zhang, X. A. (2010) · Clinical & Experimental Metastasis · doi:10.1007/s10585-010-9365-5 · Cited by 87 · see citing works
Essential role of CIB1 in regulating PAK1 activation and cell migration
Leisner, T. M., Liu, M., Jaffer, Z. M., Chernoff, J., & Parise, L. V. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200502090 · Cited by 86 · see citing works
Lonardo, F., Li, X., Siddiq, F., Singh, R., Al-Abbadi, M., Pass, H. I., & Sheng, S. (2005) · Lung Cancer · doi:10.1016/j.lungcan.2005.07.011 · Cited by 84 · see citing works
Odero-Marah, V., Khalkhali‐Ellis, Z., Chunthapong, J., Amir, S., Seftor, R. E. B., Seftor, E. A., & Hendrix, M. J. C. (2003) · Cancer Biology & Therapy · doi:10.4161/cbt.2.4.471 · Cited by 82 · see citing works
Min, Y., Ghose, S., Boelte, K. C., Li, J., Yang, L., & Lin, P. (2011) · Oncogene · doi:10.1038/onc.2011.187 · Cited by 80 · see citing works
Maspin expression and localization impact on angiogenesis and prognosis in ovarian cancer
Solomon, L. A., Munkarah, A. R., Schimp, V. L., Arabi, H., Morris, R. T., Nassar, H., & Ali‐Fehmi, R. (2006) · Gynecologic Oncology · doi:10.1016/j.ygyno.2005.11.049 · Cited by 72 · see citing works
Nuclear localization of maspin is essential for its inhibition of tumor growth and metastasis
Goulet, B., Kennette, W., Ablack, A. L., Postenka, C. O., Hague, M. N., Mymryk, J. S., Tuck, A. B., Giguère, V., Chambers, A. F., & Lewis, J. D. (2011) · Laboratory Investigation · doi:10.1038/labinvest.2011.66 · Cited by 71 · see citing works
Milde‐Langosch, K., Löning, T., & Bamberger, A. (2003) · Breast Cancer Research and Treatment · doi:10.1023/a:1023929504884 · Cited by 71 · see citing works
Yasuniwa, Y., Izumi, H., Wang, K., Shimajiri, S., Sasaguri, Y., Kawai, K., Kasai, H., Shimada, T., Miyake, K., Kashiwagi, E., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015330 · Cited by 65 · see citing works
Identification of genes for normalization of quantitative real-time PCR data in ovarian tissues
Fu, J., Bian, L., Li, Z., Dong, Z., Gao, X., Luan, H., Sun, Y., & Song, H. (2010) · Acta Biochimica et Biophysica Sinica · doi:10.1093/abbs/gmq062 · Cited by 65 · see citing works
MRP-1/CD9 gene transduction downregulates Wnt signal pathways
Huang, C., Liu, D., Masuya, D., Kameyama, K., Nakashima, T., Yokomise, H., Ueno, M., & Miyake, M. (2004) · Oncogene · doi:10.1038/sj.onc.1208063 · Cited by 65 · see citing works
Beltrán, A. S., Sun, X., Lizardi, P. M., & Blancafort, P. (2008) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-07-0526 · Cited by 63 · see citing works
Self-citationFuruya, M., Kato, H., Nishimura, N., Ishiwata, I., Ikeda, H., Ito, R., Yoshiki, T., & Ishikura, H. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-3123 · Cited by 60 · see citing works
Beltrán, A. S., & Blancafort, P. (2011) · Epigenetics · doi:10.4161/epi.6.2.13700 · Cited by 58 · see citing works
Self-citationDevelopment of a syngeneic mouse model of epithelial ovarian cancer
Quinn, B. A., Fang, X., Bickel, L. E., Martin, L. P., Xiang, H., Klein–Szanto, A. J., & Connolly, D. C. (2010) · Journal of Ovarian Research · doi:10.1186/1757-2215-3-24 · Cited by 55 · see citing works
Self-citationSuppression of Breast Tumor Growth and Metastasis by an Engineered Transcription Factor
Beltrán, A. S., Russo, A., Lara, H., Fan, C., Lizardi, P. M., & Blancafort, P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024595 · Cited by 55 · see citing works
Self-citationEpigenetic regulation of maspin expression in human ovarian carcinoma cells
Rose, S. L., Fitzgerald, M. P., White, N. O., Hitchler, M. J., Futscher, B. W., Geest, K. D., & Domann, F. E. (2006) · Gynecologic Oncology · doi:10.1016/j.ygyno.2005.12.025 · Cited by 53 · see citing works
Genetic reprogramming of tumor cells by zinc finger transcription factors
Blancafort, P., Chen, E. I., Gonzalez, B., Bergquist, S. H., Zijlstra, A., Guthy, D. A., Brachat, A., Brakenhoff, R. H., Quigley, J. P., Erdmann, D., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0501162102 · Cited by 48 · see citing works
Self-citationNidogen-1 and Nidogen-2 are Found in Basement Membranes During Human Embryonic Development
Miosge, N., Holzhausen, S., Zelent, C., Sprysch, P., & Herken, R. (2001) · The Histochemical Journal · doi:10.1023/a:1014995523521 · Cited by 46 · see citing works
Holzer, R. G., MacDougall, C. A., Cortright, G., Atwood, K., Green, J. E., & Jorcyk, C. L. (2003) · Breast Cancer Research and Treatment · doi:10.1023/a:1021175931177 · Cited by 46 · see citing works
Molecular analysis reveals heterogeneity of mouse mammary tumors conditionally mutant for Brca1
Wright, M. H., Robles, A., Herschkowitz, J. I., Hollingshead, M., Anver, M., Perou, C., & Varticovski, L. (2008) · Molecular Cancer · doi:10.1186/1476-4598-7-29 · Cited by 39 · see citing works
The Natural Tumor Suppressor Protein Maspin and Potential Application in Non Small Cell Lung Cancer
Lonardo, F., Li, X., Kaplun, A., Soubani, A. O., Sethi, S. N., Gadgeel, S. M., & Sheng, S. (2010) · Current Pharmaceutical Design · doi:10.2174/138161210791208974 · Cited by 34 · see citing works
New advances in ovarian cancer.
Liu, J. F., & Matulonis, U. A. (2010) · PubMed · Cited by 31 · see citing works
Animal Models of Ovarian Cancer
Connolly, D. C. (2009) · Cancer treatment and research · doi:10.1007/978-0-387-98094-2_17 · Cited by 30 · see citing works
Self-citationMaehara, Y., Tomisaki, S., Oda, S., Kakeji, Y., Tsujitani, S., Ichiyoshi, Y., Akazawa, K., & Sugimachi, K. (1997) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(19970422)74:2 · Cited by 29 · see citing works
Rapamycin delays growth of Wnt-1 tumors in spite of suppression of host immunity
Svirshchevskaya, E. V., Mariotti, J., Wright, M. H., Viskova, N. Y., Telford, W. G., Fowler, D. H., & Varticovski, L. (2008) · BMC Cancer · doi:10.1186/1471-2407-8-176 · Cited by 25 · see citing works
Blancafort, P., & Beltrán, A. S. (2008) · Combinatorial Chemistry & High Throughput Screening · doi:10.2174/138620708783744453 · Cited by 19 · see citing works
Self-citationCyclophilin A Protects Peg3 from Hypermethylation and Inactive Histone Modification
Lu, Y., Song, J., Cho, H., Fan, G., Yokoyama, K. K., & Chiu, R. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m606687200 · Cited by 19 · see citing works
Current and Future Directions of Clinical Trials for Ovarian Cancer
Gardner, G. J., & Jewell, E. L. (2011) · Cancer Control · doi:10.1177/107327481101800106 · Cited by 18 · see citing works
Beltrán, A. S., Liu, Y., Parikh, S., Temple, B. R. S., & Blancafort, P. (2006) · Assay and Drug Development Technologies · doi:10.1089/adt.2006.4.317 · Cited by 18 · see citing works
Self-citationNuclear maspin expression as a good prognostic factor in human epithelial ovarian carcinoma.
Sopel, M., Surowiak, P., & Berdowska, I. (2010) · PubMed · Cited by 13 · see citing works
Remodeling Genomes with Artificial Transcription Factors (ATFs)
Beltrán, A. S., & Blancafort, P. (2010) · Methods in molecular biology · doi:10.1007/978-1-60761-753-2_10 · Cited by 11 · see citing works
Self-citationInvestigating Maspin in Breast Cancer Progression Using Mouse Models
Endsley, M. P., & Zhang, M. (2011) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/b978-0-12-386471-0.00008-0 · Cited by 9 · see citing works
Identification of DNA-Binding of Tumor Suppressor Genes by Chromatin Immunoprecipitation
MacLachlan, T. K., & El‐Deiry, W. S. (2003) · Humana Press eBooks · doi:10.1385/1-59259-329-1:129 · Cited by 7 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Lipid nanoparticles for mRNA delivery
Hou, X., Zaks, T., Langer, R., & Dong, Y. (2021) · Nature Reviews Materials · doi:10.1038/s41578-021-00358-0 · Cited by 4,076 · see citing works
de Groote, M. L., Verschure, P. J., & Rots, M. G. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks863 · Cited by 180 · see citing works
Activating PTEN Tumor Suppressor Expression with the CRISPR/dCas9 System
Moses, C., Nugent, F., Waryah, C. B., García‐Bloj, B., Harvey, A. R., & Blancafort, P. (2018) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2018.12.003 · Cited by 133 · see citing works
Self-citationNanoplatforms for mRNA Therapeutics
Meng, C., Chen, Z., Li, G., Welte, T., & Shen, H. (2021) · Advanced Therapeutics · doi:10.1002/adtp.202000099 · Cited by 130 · see citing works
Zinc Fingers, TALEs, and CRISPR Systems: A Comparison of Tools for Epigenome Editing
Waryah, C. B., Moses, C., Arooj, M., & Blancafort, P. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-7774-1_2 · Cited by 114 · see citing works
Self-citationEnabling functional genomics with genome engineeringPreprint
Hilton, I. B., & Gersbach, C. A. (2015) · Genome Research · doi:10.1101/gr.190124.115 · Cited by 104 · see citing works
The Role of Zinc and Copper in Gynecological Malignancies
Michalczyk, K., & Cymbaluk‐Płoska, A. (2020) · Nutrients · doi:10.3390/nu12123732 · Cited by 104 · see citing works
Stolzenburg, S., Beltrán, A. S., Swift‐Scanlan, T., Rivenbark, A. G., Rashwan, R., & Blancafort, P. (2015) · Oncogene · doi:10.1038/onc.2014.470 · Cited by 94 · see citing works
Self-citationEpigenome engineering: new technologies for precision medicine
Sgro, A., & Blancafort, P. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa1000 · Cited by 96 · see citing works
Self-citationWaking up dormant tumor suppressor genes with zinc fingers, TALEs and the CRISPR/dCas9 system
García‐Bloj, B., Moses, C., Sgro, A., Plani-Lam, J. H. C., Arooj, M., Duffy, C., Thiruvengadam, S., Sorolla, A., Rashwan, R., Mancera, R. L., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.11142 · Cited by 91 · see citing works
Self-citationHallmarks of cancer: The CRISPR generation
Moses, C., García‐Bloj, B., Harvey, A. R., & Blancafort, P. (2018) · European Journal of Cancer · doi:10.1016/j.ejca.2018.01.002 · Cited by 87 · see citing works
Self-citationTowards Sustained Silencing of HER2/neu in Cancer By Epigenetic Editing
Falahi, F., Huisman, C., Kazemier, H. G., van der Vlies, P., Kok, K., Hospers, G. A. P., & Rots, M. G. (2013) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-12-0567 · Cited by 76 · see citing works
Vallazza, B., Petri, S., Poleganov, M. A., Eberle, F., Kuhn, A. N., & Şahin, U. (2015) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1288 · Cited by 73 · see citing works
Epigenome Engineering in Cancer: Fairytale or a Realistic Path to the Clinic?
Falahi, F., Sgro, A., & Blancafort, P. (2015) · Frontiers in Oncology · doi:10.3389/fonc.2015.00022 · Cited by 70 · see citing works
Self-citationGrimmer, M., Stolzenburg, S., Ford, E., Lister, R., Blancafort, P., & Farnham, P. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku708 · Cited by 66 · see citing works
Self-citationTetraspanin TSPAN12 regulates tumor growth and metastasis and inhibits β-catenin degradation
Knoblich, K., Wang, H., Sharma, C., Fletcher, A. L., Turley, S. J., & Hemler, M. E. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1444-8 · Cited by 65 · see citing works
Huisman, C., Wisman, G. B. A., Kazemier, H. G., van Vugt, M. A. T. M., van der Zee, A. G. J., Schuuring, E. M. D., & Rots, M. G. (2013) · Molecular Oncology · doi:10.1016/j.molonc.2013.02.017 · Cited by 43 · see citing works
Regulation of Gene Expression and Pain States by Epigenetic Mechanisms
Géranton, S. M., & Tochiki, K. K. (2015) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2014.11.012 · Cited by 43 · see citing works
Lin, S., & Yang, H. (2020) · Clinical Nutrition · doi:10.1016/j.clnu.2020.10.011 · Cited by 41 · see citing works
Promising RNA-based cancer gene therapy using extracellular vesicles for drug delivery
Xue, V. W., Wong, S. C. C., Song, G., & Cho, W. C. S. (2020) · Expert Opinion on Biological Therapy · doi:10.1080/14712598.2020.1738377 · Cited by 37 · see citing works
Consensus reference gene(s) for gene expression studies in human cancers: end of the tunnel visible?
Sharan, R. N., Vaiphei, S. T., Nongrum, S., Keppen, J., & Ksoo, M. (2015) · Cellular Oncology · doi:10.1007/s13402-015-0244-6 · Cited by 35 · see citing works
Blancafort, P., Jin, J. J., & Frye, S. V. (2012) · Molecular Pharmacology · doi:10.1124/mol.112.080697 · Cited by 33 · see citing works
Self-citationHuisman, C., van der Wijst, M. G. P., Falahi, F., Overkamp, J., Karsten, G., Terpstra, M. M., Kok, K., van der Zee, A. G., Schuuring, E. M. D., Wisman, G. B. A., et al. (2015) · Epigenetics · doi:10.1080/15592294.2015.1034415 · Cited by 33 · see citing works
Lewis, C. R., Tafur, J., Spencer, S., Green, J. M., Harrison, C., Kelmendi, B., Rabin, D. M., Yehuda, R., Yazar‐Klosinski, B., & Cahn, B. R. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.959590 · Cited by 31 · see citing works
Wang, P., Qu, X., Wang, X., Zhu, X., Zeng, H., Chen, H., & Zhu, H. (2014) · Gene Therapy · doi:10.1038/gt.2014.21 · Cited by 23 · see citing works
Breaking through an epigenetic wall
Juárez‐Moreno, K., Erices, R., Beltrán, A. S., Stolzenburg, S., Cuello, M. A., Owen, G. I., Qian, H., & Blancafort, P. (2013) · Epigenetics · doi:10.4161/epi.23503 · Cited by 21 · see citing works
Self-citationEpigenomic engineering for Down syndrome
Mentis, A. A. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.09.012 · Cited by 20 · see citing works
Rewriting DNA Methylation Signatures at Will: The Curable Genome Within Reach?
Stolzenburg, S., Goubert, D., & Rots, M. G. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-43624-1_17 · Cited by 16 · see citing works
Olney, K. C., Nyer, D. B., Vargas, D. A., Sayres, M. A. W., & Haynes, K. A. (2018) · BMC Systems Biology · doi:10.1186/s12918-018-0608-4 · Cited by 15 · see citing works
Epigenetic Editing in Prostate Cancer: Challenges and Opportunities
Pacheco, M. B., Camilo, V., Henrique, R., & Jerónimo, C. (2021) · Epigenetics · doi:10.1080/15592294.2021.1939477 · Cited by 12 · see citing works
Lee, Y., Yoo, S., Cho, S., Kim, I., & Kim, I.-S. (2025) · Journal of Controlled Release · doi:10.1016/j.jconrel.2025.113885 · Cited by 9 · see citing works
Chromatin engineering offers an opportunity to advance epigenetic cancer therapy
Baskin, N. L., & Haynes, K. A. (2019) · Nature Structural & Molecular Biology · doi:10.1038/s41594-019-0299-6 · Cited by 9 · see citing works
Zhao, X., Dong, Y., Zhao, Z., Guo, J., Liu, J., Huang, P., Dong, D., Fan, H., Guo, Q., Yang, X., et al. (2013) · Protein Expression and Purification · doi:10.1016/j.pep.2013.04.007 · Cited by 8 · see citing works
Can Genome Engineering be used to Target Cancer-Associated Enhancers?
Grimmer, M., & Farnham, P. (2014) · Epigenomics · doi:10.2217/epi.14.30 · Cited by 7 · see citing works
Genome Engineering for Therapeutic Applications
Thakore, P. I., & Gersbach, C. A. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-800563-7.00003-8 · Cited by 7 · see citing works
Pawar, S., Pingale, P., Garkal, A., Osmani, R. A. M., Gajbhiye, K. R., Kulkarni, M., Pardeshi, K., Mehta, T. A., & Rajput, A. (2024) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2024.131139 · Cited by 6 · see citing works
Al-Mamun, M., Ravenhill, L., Srisukkham, W., Hossain, A., Fall, C., Ellis, V., & Bass, R. (2016) · Microscopy and Microanalysis · doi:10.1017/s1431927616000520 · Cited by 6 · see citing works
A quantitative image analysis for the cellular cytoskeleton during in vitro tumor growth
Al-Mamun, M. A., Srisukkham, W., Farid, D. M., Ravenhill, L., Zhang, L., Hossain, A., & Bass, R. (2017) · Expert Systems with Applications · doi:10.1016/j.eswa.2017.08.048 · Cited by 2 · see citing works
de Groote, M. L., Verschure, P. J., & Rots, M. G. (2012)
Epigenetic editing as a novel approach to modulate expression of key genes in cancer
Falahi, F. (2014) · University of Groningen research database (University of Groningen / Centre for Information Technology)
Liver Cancer and the Curative Potential of Nanomedicine
Kuzmanović, A., Lin, C., & Bartneck, M. (2023) · Interdisciplinary cancer research · doi:10.1007/16833_2023_129
Eisenhut, P., Marx, N., Borsi, G., Papež, M., Ruggeri, C., Baumann, M., & Borth, N. (2024) · New Biotechnology · doi:10.1016/j.nbt.2024.09.001
- Authors
- Lara, H., Wang, Y., Beltran, A. S., Juárez-Moreno, K., Yuan, X., Kato, S., Leisewitz, A. V., Cuello Fredes, M., Licea, A. F., Connolly, D. C., Huang, L., & Blancafort, P.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- Pontificia Universidad Católica de Chile (CL)
- Fox Chase Cancer Center (US)
- Corresponding author
- Blancafort, Pilar
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2012-08
- Volume
- 287
- Issue
- 35
- Pages
- 29873-29886
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC3436144
- OpenAlex
- W2034110171
- Cited by
- 42
- References
- 79
- Citations by year
- 2025: 1 · 2024: 2 · 2023: 2 · 2021: 2 · 2020: 5 · 2019: 1 · 2018: 4 · 2017: 1 · 2016: 4 · 2015: 8 · 2014: 4 · 2013: 5 · 2012: 3
- FWCI
- 2.57
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- UWA Profiles and Research Repository (UWA) (submittedVersion)
- Americanae (AECID Library) (submittedVersion, other-oa)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, other-oa)
- UNC Libraries
- Funders
- National Institutes of Health (7r01ca136596-05, W81XWH, 3r01ca125273-03s1, CA006927, CA083638)
- National Cancer Institute (3R01CA125273-03S1, R01CA129835, CA136596, R01CA170370, CA 006927, R01-CA136596, P50CA083638, 1R01CA125273, R01 CA125273, CA083638, CA129835, P30CA006927)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
- Health Sciences › Medicine › Reproductive Medicine › Ovarian cancer diagnosis and treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
- Keywords
- serous epithelial ovarian cancer, maspin, non-viral gene delivery, tumor suppressor gene reactivation, metastasis suppression, peritoneal carcinomatosis, TSPAN12, actin cytoskeleton, cell invasion, targeted cancer therapy
- MeSH terms
- Animals, Female, Mice, Transgenic, Actin Cytoskeleton, Neoplasm Invasiveness, Neoplasms, Experimental, Ovarian Neoplasms, RNA, Messenger, Transcription Factors, Serpins, Gene Expression Regulation, Neoplastic, Zinc Fingers, Oligonucleotide Array Sequence Analysis, Cell Line, Tumor, Mice, Transcriptome, Tetraspanins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
