De La Vieja A, Dohan O, Levy O, Carrasco N. Molecular analysis of the sodium/iodide symporter: impact on thyroid and extrathyroid pathophysiology. Physiol Rev. 2000;80(3):1083–105.
Article
Google Scholar
Hingorani M, Spitzweg C, Vassaux G, Newbold K, Melcher A, Pandha H, et al. The biology of the sodium iodide symporter and its potential for targeted gene delivery. Curr Cancer Drug Targets. 2010;10(2):242–67.
Article
CAS
PubMed
PubMed Central
Google Scholar
Llorente-Esteban A, Manville RW, Reyna-Neyra A, Abbott GW, Amzel LM, Carrasco N. Allosteric regulation of mammalian Na(+)/I(-) symporter activity by perchlorate. Nat Struct Mol Biol. 2020;27(6):533–9.
Article
CAS
PubMed
Google Scholar
Spitzweg C, Bible KC, Hofbauer LC, Morris JC. Advanced radioiodine-refractory differentiated thyroid cancer: the sodium iodide symporter and other emerging therapeutic targets. Lancet Diabetes Endocrinol. 2014;2(10):830–42.
Article
CAS
PubMed
Google Scholar
Spitzweg C, Nelson PJ, Wagner E, Bartenstein P, Weber WA, Schwaiger M, et al. The sodium iodide symporter (NIS): novel applications for radionuclide imaging and treatment. Endocr Relat Cancer. 2021;28(10):T193–213.
Article
CAS
PubMed
Google Scholar
Willhauck MJ, Sharif Samani BR, Gildehaus FJ, Wolf I, Senekowitsch-Schmidtke R, Stark HJ, et al. Application of 188rhenium as an alternative radionuclide for treatment of prostate cancer after tumor-specific sodium iodide symporter gene expression. J Clin Endocrinol Metab. 2007;92(11):4451–8.
Article
CAS
PubMed
Google Scholar
Willhauck MJ, Samani BR, Wolf I, Senekowitsch-Schmidtke R, Stark HJ, Meyer GJ, et al. The potential of 211Astatine for NIS-mediated radionuclide therapy in prostate cancer. Eur J Nucl Med Mol Imaging. 2008;35(7):1272–81.
Article
CAS
PubMed
Google Scholar
Dadachova E, Bouzahzah B, Zuckier LS, Pestell RG. Rhenium-188 as an alternative to Iodine-131 for treatment of breast tumors expressing the sodium/iodide symporter (NIS). Nucl Med Biol. 2002;29(1):13–8.
Article
CAS
PubMed
Google Scholar
Dai G, Levy O, Carrasco N. Cloning and characterization of the thyroid iodide transporter. Nature. 1996;379(6564):458–60.
Article
CAS
PubMed
Google Scholar
Shimura H, Haraguchi K, Miyazaki A, Endo T, Onaya T. Iodide uptake and experimental 131I therapy in transplanted undifferentiated thyroid cancer cells expressing the Na+/I- symporter gene. Endocrinology. 1997;138(10):4493–6.
Article
CAS
PubMed
Google Scholar
Hager S, Wagner E. Bioresponsive polyplexes—chemically programmed for nucleic acid delivery. Expert Opin Drug Deliv. 2018;15(11):1067–83.
Article
CAS
PubMed
Google Scholar
Klutz K, Schaffert D, Willhauck MJ, Grunwald GK, Haase R, Wunderlich N, et al. Epidermal growth factor receptor-targeted (131)I-therapy of liver cancer following systemic delivery of the sodium iodide symporter gene. Mol Ther. 2011;19(4):676–85.
Article
CAS
PubMed
PubMed Central
Google Scholar
Lachelt U, Wagner E. Nucleic acid therapeutics using polyplexes: a journey of 50 years (and beyond). Chem Rev. 2015;115(19):11043–78.
Article
PubMed
CAS
Google Scholar
Schafer A, Pahnke A, Schaffert D, van Weerden WM, de Ridder CM, Rodl W, et al. Disconnecting the yin and yang relation of epidermal growth factor receptor (EGFR)-mediated delivery: a fully synthetic, EGFR-targeted gene transfer system avoiding receptor activation. Hum Gene Ther. 2011;22(12):1463–73.
Article
CAS
PubMed
PubMed Central
Google Scholar
Schmohl KA, Dolp P, Schug C, Knoop K, Klutz K, Schwenk N, et al. Reintroducing the sodium-iodide symporter to anaplastic thyroid carcinoma. Thyroid. 2017;27(12):1534–43.
Article
CAS
PubMed
Google Scholar
Schmohl KA, Gupta A, Grunwald GK, Trajkovic-Arsic M, Klutz K, Braren R, et al. Imaging and targeted therapy of pancreatic ductal adenocarcinoma using the theranostic sodium iodide symporter (NIS) gene. Oncotarget. 2017;8(20):33393–404.
Article
PubMed
PubMed Central
Google Scholar
Urnauer S, Muller AM, Schug C, Schmohl KA, Tutter M, Schwenk N, et al. EGFR-targeted nonviral NIS gene transfer for bioimaging and therapy of disseminated colon cancer metastases. Oncotarget. 2017;8(54):92195–208.
Article
PubMed
PubMed Central
Google Scholar
He D, Wagner E. Defined polymeric materials for gene delivery. Macromol Biosci. 2015;15(5):600–12.
Article
CAS
PubMed
Google Scholar
Kos P, Lachelt U, Herrmann A, Mickler FM, Doblinger M, He D, et al. Histidine-rich stabilized polyplexes for cMet-directed tumor-targeted gene transfer. Nanoscale. 2015;7(12):5350–62.
Article
CAS
PubMed
Google Scholar
Urnauer S, Morys S, Krhac Levacic A, Muller AM, Schug C, Schmohl KA, et al. Sequence-defined cMET/HGFR-targeted polymers as gene delivery vehicles for the theranostic sodium iodide symporter (NIS) gene. Mol Ther. 2016;24(8):1395–404.
Article
CAS
PubMed
PubMed Central
Google Scholar
Urnauer S, Schmohl KA, Tutter M, Schug C, Schwenk N, Morys S, et al. Dual-targeted NIS polyplexes-a theranostic strategy toward tumors with heterogeneous receptor expression. Gene Ther. 2019;26(3–4):93–108.
Article
CAS
PubMed
Google Scholar
Hagenhoff A, Bruns CJ, Zhao Y, von Luttichau I, Niess H, Spitzweg C, et al. Harnessing mesenchymal stem cell homing as an anticancer therapy. Expert Opin Biol Ther. 2016;16(9):1079–92.
Article
CAS
PubMed
Google Scholar
Melzer C, Yang Y, Hass R. Interaction of MSC with tumor cells. Cell Commun Signal. 2016;14(1):20.
Article
PubMed
PubMed Central
CAS
Google Scholar
Schmohl KA, Müller AM, Wechselberger A, Rühland S, Salb N, Schwenk N, et al. Thyroid hormones and tetrac: new regulators of tumour stroma formation via integrin αvβ3. Endocr Relat Cancer. 2015;22(6):941–52.
Article
CAS
PubMed
Google Scholar
Droujinine IA, Eckert MA, Zhao W. To grab the stroma by the horns: from biology to cancer therapy with mesenchymal stem cells. Oncotarget. 2013;4(5):651–64.
Article
PubMed
PubMed Central
Google Scholar
Niess H, von Einem JC, Thomas MN, Michl M, Angele MK, Huss R, et al. Treatment of advanced gastrointestinal tumors with genetically modified autologous mesenchymal stromal cells (TREAT-ME1): study protocol of a phase I/II clinical trial. BMC Cancer. 2015;15:237.
Article
PubMed
PubMed Central
CAS
Google Scholar
Knoop K, Kolokythas M, Klutz K, Willhauck MJ, Wunderlich N, Draganovici D, et al. Image-guided, tumor stroma-targeted 131I therapy of hepatocellular cancer after systemic mesenchymal stem cell-mediated NIS gene delivery. Mol Ther. 2011;19(9):1704–13.
Article
CAS
PubMed
PubMed Central
Google Scholar
Knoop K, Schwenk N, Dolp P, Willhauck MJ, Zischek C, Zach C, et al. Stromal targeting of sodium iodide symporter using mesenchymal stem cells allows enhanced imaging and therapy of hepatocellular carcinoma. Hum Gene Ther. 2013;24(3):306–16.
Article
CAS
PubMed
PubMed Central
Google Scholar
Knoop K, Schwenk N, Schmohl K, Muller A, Zach C, Cyran C, et al. Mesenchymal stem cell-mediated, tumor stroma-targeted radioiodine therapy of metastatic colon cancer using the sodium iodide symporter as theranostic gene. J Nucl Med. 2015;56(4):600–6.
Article
CAS
PubMed
Google Scholar
Schug C, Gupta A, Urnauer S, Steiger K, Cheung PF, Neander C, et al. A novel approach for image-guided (131)I therapy of pancreatic ductal adenocarcinoma using mesenchymal stem cell-mediated NIS gene delivery. Mol Cancer Res. 2019;17(1):310–20.
Article
CAS
PubMed
Google Scholar
Muller AM, Schmohl KA, Knoop K, Schug C, Urnauer S, Hagenhoff A, et al. Hypoxia-targeted 131I therapy of hepatocellular cancer after systemic mesenchymal stem cell-mediated sodium iodide symporter gene delivery. Oncotarget. 2016;7(34):54795–810.
Article
PubMed
PubMed Central
Google Scholar
Schug C, Urnauer S, Jaeckel C, Schmohl KA, Tutter M, Steiger K, et al. TGFB1-driven mesenchymal stem cell-mediated NIS gene transfer. Endocr Relat Cancer. 2019;26(1):89–101.
Article
CAS
PubMed
Google Scholar
Klopp AH, Spaeth EL, Dembinski JL, Woodward WA, Munshi A, Meyn RE, et al. Tumor irradiation increases the recruitment of circulating mesenchymal stem cells into the tumor microenvironment. Cancer Res. 2007;67(24):11687–95.
Article
CAS
PubMed
PubMed Central
Google Scholar
Schug C, Sievert W, Urnauer S, Muller AM, Schmohl KA, Wechselberger A, et al. External beam radiation therapy enhances mesenchymal stem cell-mediated sodium-iodide symporter gene delivery. Hum Gene Ther. 2018;29(11):1287–300.
Article
CAS
PubMed
Google Scholar
Schug C, Kitzberger C, Sievert W, Spellerberg R, Tutter M, Schmohl KA, et al. Radiation-induced amplification of TGFB1-induced mesenchymal stem cell-mediated sodium iodide symporter (NIS) gene (131)I therapy. Clin Cancer Res. 2019;25(19):5997–6008.
Article
CAS
PubMed
Google Scholar
Tutter M, Schug C, Schmohl KA, Urnauer S, Kitzberger C, Schwenk N, et al. Regional hyperthermia enhances mesenchymal stem cell recruitment to tumor stroma: implications for mesenchymal stem cell-based tumor therapy. Mol Ther. 2021;29(2):788–803.
Article
CAS
PubMed
Google Scholar
Tutter M, Schug C, Schmohl KA, Urnauer S, Schwenk N, Petrini M, et al. Effective control of tumor growth through spatial and temporal control of theranostic sodium iodide symporter (NIS) gene expression using a heat-inducible gene promoter in engineered mesenchymal stem cells. Theranostics. 2020;10(10):4490–506.
Article
CAS
PubMed
PubMed Central
Google Scholar
Ravera S, Reyna-Neyra A, Ferrandino G, Amzel LM, Carrasco N. The sodium/iodide symporter (NIS): molecular physiology and preclinical and clinical applications. Annu Rev Physiol. 2017;79:261–89.
Article
CAS
PubMed
PubMed Central
Google Scholar
Jiang H, DeGrado TR. [(18)F]Tetrafluoroborate ([(18)F]TFB) and its analogs for PET imaging of the sodium/iodide symporter. Theranostics. 2018;8(14):3918–31.
Article
CAS
PubMed
PubMed Central
Google Scholar
Samnick S, Al-Momani E, Schmid JS, Mottok A, Buck AK, Lapa C. Initial clinical investigation of [18F]tetrafluoroborate PET/CT in comparison to [124I]iodine PET/CT for imaging thyroid cancer. Clin Nucl Med. 2018;43(3):162–7.
Article
PubMed
Google Scholar
Portulano C, Paroder-Belenitsky M, Carrasco N. The Na+/I- symporter (NIS): mechanism and medical impact. Endocr Rev. 2014;35(1):106–49.
Article
CAS
PubMed
Google Scholar
Dittmann M, Gonzalez Carvalho JM, Rahbar K, Schafers M, Claesener M, Riemann B, et al. Incremental diagnostic value of [(18)F]tetrafluoroborate PET-CT compared to [(131)I]iodine scintigraphy in recurrent differentiated thyroid cancer. Eur J Nucl Med Mol Imaging. 2020;47(11):2639–46.
Article
PubMed
PubMed Central
CAS
Google Scholar
Jauregui-Osoro M, Sunassee K, Weeks AJ, Berry DJ, Paul RL, Cleij M, et al. Synthesis and biological evaluation of [(18)F]tetrafluoroborate: a PET imaging agent for thyroid disease and reporter gene imaging of the sodium/iodide symporter. Eur J Nucl Med Mol Imaging. 2010;37(11):2108–16.
Article
CAS
PubMed
PubMed Central
Google Scholar
Khoshnevisan A, Jauregui-Osoro M, Shaw K, Torres JB, Young JD, Ramakrishnan NK, et al. [(18)F]tetrafluoroborate as a PET tracer for the sodium/iodide symporter: the importance of specific activity. EJNMMI Res. 2016;6(1):34.
Article
PubMed
PubMed Central
CAS
Google Scholar
O’Doherty J, Jauregui-Osoro M, Brothwood T, Szyszko T, Marsden PK, O’Doherty MJ, et al. (18)F-Tetrafluoroborate, a PET probe for imaging sodium/iodide symporter expression: whole-body biodistribution, safety, and radiation dosimetry in thyroid cancer patients. J Nucl Med. 2017;58(10):1666–71.
Article
CAS
PubMed
Google Scholar
Jiang H, Schmit NR, Koenen AR, Bansal A, Pandey MK, Glynn RB, et al. Safety, pharmacokinetics, metabolism and radiation dosimetry of (18)F-tetrafluoroborate ((18)F-TFB) in healthy human subjects. EJNMMI Res. 2017;7(1):90.
Article
PubMed
PubMed Central
CAS
Google Scholar
Jiang H, Bansal A, Pandey MK, Peng KW, Suksanpaisan L, Russell SJ, et al. Synthesis of 18F-tetrafluoroborate via radiofluorination of boron trifluoride and evaluation in a murine C6-glioma tumor model. J Nucl Med. 2016;57(9):1454–9.
Article
CAS
PubMed
PubMed Central
Google Scholar
Nagarajah J, Le M, Knauf JA, Ferrandino G, Montero-Conde C, Pillarsetty N, et al. Sustained ERK inhibition maximizes responses of BrafV600E thyroid cancers to radioiodine. J Clin Investig. 2016;126(11):4119–24.
Article
PubMed
PubMed Central
Google Scholar
Diocou S, Volpe A, Jauregui-Osoro M, Boudjemeline M, Chuamsaamarkkee K, Man F, et al. [(18)F]tetrafluoroborate-PET/CT enables sensitive tumor and metastasis in vivo imaging in a sodium iodide symporter-expressing tumor model. Sci Rep. 2017;7(1):946.
Article
CAS
PubMed
PubMed Central
Google Scholar
Verburg FA, Giovanella L, Hoffmann M, Iakovou I, Mihailovic J, Ovcaricek PP, et al. New! F-18-based PET/CT for sodium-iodine-symporter-targeted imaging! Eur J Nucl Med Mol Imaging. 2020;47(11):2484–6.
Article
PubMed
PubMed Central
Google Scholar
Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, et al. The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol. 2016;131(6):803–20.
Article
PubMed
Google Scholar
Guo R, Xi Y, Zhang M, Miao Y, Zhang M, Li B. Human sodium iodide transporter gene-mediated imaging and therapy of mouse glioma, comparison between (188)Re and (131)I. Oncol Lett. 2018;15(3):3911–7.
PubMed
PubMed Central
Google Scholar
Cho JY, Shen DH, Yang W, Williams B, Buckwalter TL, La Perle KM, et al. In vivo imaging and radioiodine therapy following sodium iodide symporter gene transfer in animal model of intracerebral gliomas. Gene Ther. 2002;9(17):1139–45.
Article
CAS
PubMed
Google Scholar
Opyrchal M, Allen C, Iankov I, Aderca I, Schroeder M, Sarkaria J, et al. Effective radiovirotherapy for malignant gliomas by using oncolytic measles virus strains encoding the sodium iodide symporter (MV-NIS). Hum Gene Ther. 2012;23(4):419–27.
Article
CAS
PubMed
Google Scholar
Spellerberg R, Benli-Hoppe T, Kitzberger C, Berger S, Schmohl KA, Schwenk N, et al. Selective sodium iodide symporter (NIS) gene therapy of glioblastoma mediated by EGFR-targeted lipopolyplexes. Mol Ther Oncolytics. 2021;23:432–46.
Article
CAS
PubMed
PubMed Central
Google Scholar
Ho AL, Grewal RK, Leboeuf R, Sherman EJ, Pfister DG, Deandreis D, et al. Selumetinib-enhanced radioiodine uptake in advanced thyroid cancer. N Engl J Med. 2013;368(7):623–32.
Article
CAS
PubMed
PubMed Central
Google Scholar
Jentzen W, Hoppenbrouwers J, van Leeuwen P, van der Velden D, van de Kolk R, Poeppel TD, et al. Assessment of lesion response in the initial radioiodine treatment of differentiated thyroid cancer using 124I PET imaging. J Nucl Med. 2014;55(11):1759–65.
Article
CAS
PubMed
Google Scholar
Castillo-Rivera F, Ondo-Mendez A, Guglielmi J, Guigonis JM, Jing L, Lindenthal S, et al. Tumor microenvironment affects exogenous sodium/iodide symporter expression. Transl Oncol. 2021;14(1):100937.
Article
CAS
PubMed
Google Scholar