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Open Access 09-05-2024 | Positron Emission Tomography | Original Article

Imaging CAR-NK cells targeted to HER2 ovarian cancer with human sodium-iodide symporter-based positron emission tomography

Authors: Nourhan Shalaby, Ying Xia, John J Kelly, Rafael Sanchez-Pupo, Francisco Martinez, Matthew S Fox, Jonathan D Thiessen, Justin W Hicks, Timothy J Scholl, John A. Ronald

Published in: European Journal of Nuclear Medicine and Molecular Imaging

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Abstract

Chimeric antigen receptor (CAR) cell therapies utilize CARs to redirect immune cells towards cancer cells expressing specific antigens like human epidermal growth factor receptor 2 (HER2). Despite their potential, CAR T cell therapies exhibit variable response rates and adverse effects in some patients. Non-invasive molecular imaging can aid in predicting patient outcomes by tracking infused cells post-administration. CAR-T cells are typically autologous, increasing manufacturing complexity and costs. An alternative approach involves developing CAR natural killer (CAR-NK) cells as an off-the-shelf allogeneic product. In this study, we engineered HER2-targeted CAR-NK cells co-expressing the positron emission tomography (PET) reporter gene human sodium-iodide symporter (NIS) and assessed their therapeutic efficacy and PET imaging capability in a HER2 ovarian cancer mouse model.
NK-92 cells were genetically modified to express a HER2-targeted CAR, the bioluminescence imaging reporter Antares, and NIS. HER2-expressing ovarian cancer cells were engineered to express the bioluminescence reporter Firefly luciferase (Fluc). Co-culture experiments demonstrated significantly enhanced cytotoxicity of CAR-NK cells compared to naive NK cells. In vivo studies involving mice with Fluc-expressing tumors revealed that those treated with CAR-NK cells exhibited reduced tumor burden and prolonged survival compared to controls. Longitudinal bioluminescence imaging demonstrated stable signals from CAR-NK cells over time. PET imaging using the NIS-targeted tracer 18F-tetrafluoroborate ([18F]TFB) showed significantly higher PET signals in mice treated with NIS-expressing CAR-NK cells.
Overall, our study showcases the therapeutic potential of HER2-targeted CAR-NK cells in an aggressive ovarian cancer model and underscores the feasibility of using human-derived PET reporter gene imaging to monitor these cells non-invasively in patients.
Literature
3.
go back to reference Xin L, Xiao W, Che L, Liu J, Miccio L, Bianco V. u.c. Label-Free Assessment of the Drug Resistance of Epithelial Ovarian Cancer Cells in a Microfluidic Holographic Flow Cytometer Boosted through Machine Learning. 2021. gada [citēts 2022. gada 20. decembrī]; Iegūts no: https://doi.org/10.1021/acsomega.1c04204. Xin L, Xiao W, Che L, Liu J, Miccio L, Bianco V. u.c. Label-Free Assessment of the Drug Resistance of Epithelial Ovarian Cancer Cells in a Microfluidic Holographic Flow Cytometer Boosted through Machine Learning. 2021. gada [citēts 2022. gada 20. decembrī]; Iegūts no: https://​doi.​org/​10.​1021/​acsomega.​1c04204.
4.
go back to reference Itamochi H, Kigawa J. Clinical trials and future potential of targeted therapy for ovarian cancer. Itamochi H, Kigawa J. Clinical trials and future potential of targeted therapy for ovarian cancer.
5.
go back to reference Yan M, Schwaederle M, Arguello D, Millis SZ, Gatalica Z, Kurzrock R. HER2 expression status in diverse cancers: review of results from 37,992 patients. Cancer Metastasis Rev [Internets]. 2015. gada [citēts 2021. gada 9. novembrī];34:157. Iegūts no: /pmc/articles/PMC4368842/. Yan M, Schwaederle M, Arguello D, Millis SZ, Gatalica Z, Kurzrock R. HER2 expression status in diverse cancers: review of results from 37,992 patients. Cancer Metastasis Rev [Internets]. 2015. gada [citēts 2021. gada 9. novembrī];34:157. Iegūts no: /pmc/articles/PMC4368842/.
6.
go back to reference Pils D, Pinter A, Reibenwein J, Alfanz A, Horak P, Schmid BC. u.c. In ovarian cancer the prognostic influence of HER2/neu is not dependent on the CXCR4/SDF-1 signalling pathway. Br J Cancer 2007 963 [Internets]. 2007. gada [citēts 2021. gada 4. novembrī];96:485–91. Iegūts no: https://www.nature.com/articles/6603581. Pils D, Pinter A, Reibenwein J, Alfanz A, Horak P, Schmid BC. u.c. In ovarian cancer the prognostic influence of HER2/neu is not dependent on the CXCR4/SDF-1 signalling pathway. Br J Cancer 2007 963 [Internets]. 2007. gada [citēts 2021. gada 4. novembrī];96:485–91. Iegūts no: https://​www.​nature.​com/​articles/​6603581.
8.
go back to reference Vallera DA, Oh F, Kodal B, Hinderlie P, Geller MA, Miller JS. u.c. A HER2 tri-specific NK cell engager mediates efficient targeting of human ovarian cancer. Cancers (Basel). 2021. gada;13. Vallera DA, Oh F, Kodal B, Hinderlie P, Geller MA, Miller JS. u.c. A HER2 tri-specific NK cell engager mediates efficient targeting of human ovarian cancer. Cancers (Basel). 2021. gada;13.
9.
go back to reference Gajria D, Chandarlapaty S. HER2-amplified breast cancer: Mechanisms of trastuzumab resistance and novel targeted therapies. Expert Rev Anticancer Ther. 2011. gada;11:263–75. Gajria D, Chandarlapaty S. HER2-amplified breast cancer: Mechanisms of trastuzumab resistance and novel targeted therapies. Expert Rev Anticancer Ther. 2011. gada;11:263–75.
10.
go back to reference Wilken JA, Webster KT, Maihle NJ. Trastuzumab sensitizes ovarian cancer cells to EGFR-targeted therapeutics. J Ovarian Res. 2010. gada;3:1–9. Wilken JA, Webster KT, Maihle NJ. Trastuzumab sensitizes ovarian cancer cells to EGFR-targeted therapeutics. J Ovarian Res. 2010. gada;3:1–9.
11.
go back to reference Lanitis E, Dangaj D, Hagemann IS, Song DG, Best A, Sandaltzopoulos R. u.c. Primary Human ovarian epithelial Cancer cells broadly Express HER2 at immunologically-detectable levels. PLoS ONE. 2012. gada;7. Lanitis E, Dangaj D, Hagemann IS, Song DG, Best A, Sandaltzopoulos R. u.c. Primary Human ovarian epithelial Cancer cells broadly Express HER2 at immunologically-detectable levels. PLoS ONE. 2012. gada;7.
12.
go back to reference Sterner RC, Sterner RM. CAR-T cell therapy: current limitations and potential strategies. Blood Cancer J. 2021. gada;11. Sterner RC, Sterner RM. CAR-T cell therapy: current limitations and potential strategies. Blood Cancer J. 2021. gada;11.
13.
go back to reference Dai H, Wang Y, Lu X, Han W. Chimeric antigen receptors modified T-cells for cancer therapy. J Natl Cancer Inst. 2016. gada;108. Dai H, Wang Y, Lu X, Han W. Chimeric antigen receptors modified T-cells for cancer therapy. J Natl Cancer Inst. 2016. gada;108.
16.
go back to reference Xu J, Meng Q, Sun H, Zhang X, Yun J, Li B. u.c. HER2-specific chimeric antigen receptor-T cells for targeted therapy of metastatic colorectal cancer. Cell Death Dis. 2021. gada;12:1–11. Xu J, Meng Q, Sun H, Zhang X, Yun J, Li B. u.c. HER2-specific chimeric antigen receptor-T cells for targeted therapy of metastatic colorectal cancer. Cell Death Dis. 2021. gada;12:1–11.
17.
go back to reference Sun M, Shi H, Liu C, Liu J, Liu X, Sun Y. Construction and evaluation of a novel humanized HER2-specific chimeric receptor. Breast Cancer Res. 2014. gada;16:1–10. Sun M, Shi H, Liu C, Liu J, Liu X, Sun Y. Construction and evaluation of a novel humanized HER2-specific chimeric receptor. Breast Cancer Res. 2014. gada;16:1–10.
18.
go back to reference Song Y, Tong C, Wang Y, Gao Y, Dai H, Guo Y. u.c. Effective and persistent antitumor activity of HER2-directed CAR-T cells against gastric cancer cells in vitro and xenotransplanted tumors in vivo. Protein Cell. 2018. gada;9:867–78. Song Y, Tong C, Wang Y, Gao Y, Dai H, Guo Y. u.c. Effective and persistent antitumor activity of HER2-directed CAR-T cells against gastric cancer cells in vitro and xenotransplanted tumors in vivo. Protein Cell. 2018. gada;9:867–78.
19.
go back to reference Ahmed N, Brawley VS, Hegde M, Robertson C, Ghazi A, Gerken C. u.c. Human epidermal growth factor receptor 2 (HER2) - Specific chimeric antigen receptor - Modified T cells for the immunotherapy of HER2-positive sarcoma. J Clin Oncol. 2015. gada;33:1688–96. Ahmed N, Brawley VS, Hegde M, Robertson C, Ghazi A, Gerken C. u.c. Human epidermal growth factor receptor 2 (HER2) - Specific chimeric antigen receptor - Modified T cells for the immunotherapy of HER2-positive sarcoma. J Clin Oncol. 2015. gada;33:1688–96.
20.
go back to reference Ahmed N, Salsman VS, Kew Y, Shaffer D, Powell S, Zhang YJ. u.c. HER2-specific T cells target primary glioblastoma stem cells and induce regression of autologous experimental tumors. Clin Cancer Res. 2010. gada;16:474–85. Ahmed N, Salsman VS, Kew Y, Shaffer D, Powell S, Zhang YJ. u.c. HER2-specific T cells target primary glioblastoma stem cells and induce regression of autologous experimental tumors. Clin Cancer Res. 2010. gada;16:474–85.
21.
go back to reference Rainusso N, Brawley VS, Ghazi A, Hicks MJ, Gottschalk S, Rosen JM. u.c. Immunotherapy targeting HER2 with genetically modified T cells eliminates tumor-initiating cells in osteosarcoma. Cancer Gene Ther. 2012. gada;19:212–7. Rainusso N, Brawley VS, Ghazi A, Hicks MJ, Gottschalk S, Rosen JM. u.c. Immunotherapy targeting HER2 with genetically modified T cells eliminates tumor-initiating cells in osteosarcoma. Cancer Gene Ther. 2012. gada;19:212–7.
22.
go back to reference Ahmed N, Ratnayake M, Savoldo B, Perlaky L, Dotti G, Wels WS. u.c. Regression of experimental medulloblastoma following transfer of HER2-specific T cells. Cancer Res. 2007. gada;67:5957–64. Ahmed N, Ratnayake M, Savoldo B, Perlaky L, Dotti G, Wels WS. u.c. Regression of experimental medulloblastoma following transfer of HER2-specific T cells. Cancer Res. 2007. gada;67:5957–64.
23.
go back to reference Hegde M, Joseph SK, Pashankar F, DeRenzo C, Sanber K, Navai S. u.c. Tumor response and endogenous immune reactivity after administration of HER2 CAR T cells in a child with metastatic rhabdomyosarcoma. Nat Commun [Internets]. 2020. gada [citēts 2024. gada 30. janvārī];11. Iegūts no: https://pubmed.ncbi.nlm.nih.gov/32669548/. Hegde M, Joseph SK, Pashankar F, DeRenzo C, Sanber K, Navai S. u.c. Tumor response and endogenous immune reactivity after administration of HER2 CAR T cells in a child with metastatic rhabdomyosarcoma. Nat Commun [Internets]. 2020. gada [citēts 2024. gada 30. janvārī];11. Iegūts no: https://​pubmed.​ncbi.​nlm.​nih.​gov/​32669548/​.
25.
go back to reference Vitanza NA, Johnson AJ, Wilson AL, Brown C, Yokoyama JK, Künkele A. u.c. Locoregional infusion of HER2-specific CAR T cells in children and young adults with recurrent or refractory CNS tumors: an interim analysis. Nat Med [Internets]. 2021. gada [citēts 2024. gada 30. janvārī];27:1544–52. Iegūts no: https://pubmed.ncbi.nlm.nih.gov/34253928/. Vitanza NA, Johnson AJ, Wilson AL, Brown C, Yokoyama JK, Künkele A. u.c. Locoregional infusion of HER2-specific CAR T cells in children and young adults with recurrent or refractory CNS tumors: an interim analysis. Nat Med [Internets]. 2021. gada [citēts 2024. gada 30. janvārī];27:1544–52. Iegūts no: https://​pubmed.​ncbi.​nlm.​nih.​gov/​34253928/​.
26.
go back to reference Sakemura R, Bansal A, Siegler EL, Hefazi M, Yang N, Khadka RH. u.c. Development of a Clinically Relevant Reporter for Chimeric Antigen Receptor T-cell Expansion, Trafficking, and Toxicity. Cancer Immunol Res [Internets]. 2021. gada [citēts 2022. gada 28. oktobrī];9:1035–46. Iegūts no: https://pubmed.ncbi.nlm.nih.gov/34244299/. Sakemura R, Bansal A, Siegler EL, Hefazi M, Yang N, Khadka RH. u.c. Development of a Clinically Relevant Reporter for Chimeric Antigen Receptor T-cell Expansion, Trafficking, and Toxicity. Cancer Immunol Res [Internets]. 2021. gada [citēts 2022. gada 28. oktobrī];9:1035–46. Iegūts no: https://​pubmed.​ncbi.​nlm.​nih.​gov/​34244299/​.
27.
go back to reference Zeng W, Zhang P. Resistance and recurrence of malignancies after CAR-T cell therapy. Exp Cell Res. 2022. gada;410:112971. Zeng W, Zhang P. Resistance and recurrence of malignancies after CAR-T cell therapy. Exp Cell Res. 2022. gada;410:112971.
30.
go back to reference Hu W, Wang G, Huang D, Sui M, Xu Y. Cancer Immunotherapy Based on Natural Killer Cells: Current Progress and New Opportunities. Front Immunol [Internets]. 2019. gada [citēts 2021. gada 4. novembrī];10:1205. Iegūts no: /pmc/articles/PMC6554437/. Hu W, Wang G, Huang D, Sui M, Xu Y. Cancer Immunotherapy Based on Natural Killer Cells: Current Progress and New Opportunities. Front Immunol [Internets]. 2019. gada [citēts 2021. gada 4. novembrī];10:1205. Iegūts no: /pmc/articles/PMC6554437/.
33.
go back to reference Heipertz EL, Zynda ER, Stav-Noraas TE, Hungler AD, Boucher SE, Kaur N. u.c. current perspectives on off-the-Shelf Allogeneic NK and CAR-NK Cell therapies. Front Immunol [Internets]. 2021. Gada [citēts 2024. gada 30. janvārī];12. Iegūts no: /pmc/articles/PMC8671166/. Heipertz EL, Zynda ER, Stav-Noraas TE, Hungler AD, Boucher SE, Kaur N. u.c. current perspectives on off-the-Shelf Allogeneic NK and CAR-NK Cell therapies. Front Immunol [Internets]. 2021. Gada [citēts 2024. gada 30. janvārī];12. Iegūts no: /pmc/articles/PMC8671166/.
34.
go back to reference Suck G, Odendahl M, Nowakowska P, Seidl · Christian, Winfried ·, Wels S. u.c. NK-92: an off-the-shelf therapeutic for adoptive natural killer cell-based cancer immunotherapy. Cancer Immunol Immunother. 2016. gada;65:485–92. Suck G, Odendahl M, Nowakowska P, Seidl · Christian, Winfried ·, Wels S. u.c. NK-92: an off-the-shelf therapeutic for adoptive natural killer cell-based cancer immunotherapy. Cancer Immunol Immunother. 2016. gada;65:485–92.
35.
go back to reference Liu E, Marin D, Banerjee P, MacApinlac HA, Thompson P, Basar R. u.c. Use of CAR-transduced natural killer cells in CD19-positive lymphoid tumors. N Engl J Med. 2020. gada;382:545–53. Liu E, Marin D, Banerjee P, MacApinlac HA, Thompson P, Basar R. u.c. Use of CAR-transduced natural killer cells in CD19-positive lymphoid tumors. N Engl J Med. 2020. gada;382:545–53.
36.
go back to reference Valeri A, García-Ortiz A, Castellano E, Córdoba L, Maroto-Martín E, Encinas J. u.c. Overcoming tumor resistance mechanisms in CAR-NK cell therapy. Front Immunol. 2022. gada;13:1–28. Valeri A, García-Ortiz A, Castellano E, Córdoba L, Maroto-Martín E, Encinas J. u.c. Overcoming tumor resistance mechanisms in CAR-NK cell therapy. Front Immunol. 2022. gada;13:1–28.
38.
go back to reference Gong Y, Klein Wolterink RGJ, Wang J, Bos GMJ, Germeraad WTV. Chimeric antigen receptor natural killer (CAR-NK) cell design and engineering for cancer therapy. J Hematol Oncol. 2021. gada;14. Gong Y, Klein Wolterink RGJ, Wang J, Bos GMJ, Germeraad WTV. Chimeric antigen receptor natural killer (CAR-NK) cell design and engineering for cancer therapy. J Hematol Oncol. 2021. gada;14.
39.
go back to reference Marofi F, Al-Awad AS, Sulaiman Rahman H, Markov A, Abdelbasset WK, Ivanovna Enina Y. u.c. CAR-NK Cell: A New Paradigm in Tumor Immunotherapy. Front Oncol. 2021. gada;0:2078. Marofi F, Al-Awad AS, Sulaiman Rahman H, Markov A, Abdelbasset WK, Ivanovna Enina Y. u.c. CAR-NK Cell: A New Paradigm in Tumor Immunotherapy. Front Oncol. 2021. gada;0:2078.
43.
go back to reference Tang X, Yang L, Li Z, Nalin AP, Dai H, Xu T. u.c. First-in-man clinical trial of CAR NK-92 cells: safety test of CD33-CAR NK-92 cells in patients with relapsed and refractory acute myeloid leukemia. Am J Cancer Res [Internets]. 2018. gada [citēts 2022. gada 21. novembrī];8:1083. Iegūts no: /pmc/articles/PMC6048396/. Tang X, Yang L, Li Z, Nalin AP, Dai H, Xu T. u.c. First-in-man clinical trial of CAR NK-92 cells: safety test of CD33-CAR NK-92 cells in patients with relapsed and refractory acute myeloid leukemia. Am J Cancer Res [Internets]. 2018. gada [citēts 2022. gada 21. novembrī];8:1083. Iegūts no: /pmc/articles/PMC6048396/.
44.
go back to reference Pinz KG, Yakaboski E, Jares A, Liu H, Firor AE, Chen KH. u.c. Targeting T-cell malignancies using anti-CD4 CAR NK-92 cells. Oncotarget [Internets]. 2017. gada [citēts 2022. gada 21. novembrī];8:112783. Iegūts no: /pmc/articles/PMC5762550/. Pinz KG, Yakaboski E, Jares A, Liu H, Firor AE, Chen KH. u.c. Targeting T-cell malignancies using anti-CD4 CAR NK-92 cells. Oncotarget [Internets]. 2017. gada [citēts 2022. gada 21. novembrī];8:112783. Iegūts no: /pmc/articles/PMC5762550/.
45.
go back to reference Gong J, Maki G, Klingemann H. Characterization of a human cell line (NK-92) with phenotypical and functional characteristics of activated natural killer cells. Leukemia. 1994. gada. Gong J, Maki G, Klingemann H. Characterization of a human cell line (NK-92) with phenotypical and functional characteristics of activated natural killer cells. Leukemia. 1994. gada.
47.
go back to reference Minn I, Huss DJ, Ahn HH, Chinn TM, Park A, Jones J. u.c. Imaging CAR T cell therapy with PSMA-targeted positron emission tomography. Sci Adv. 2019. gada;5:eaaw5096. Minn I, Huss DJ, Ahn HH, Chinn TM, Park A, Jones J. u.c. Imaging CAR T cell therapy with PSMA-targeted positron emission tomography. Sci Adv. 2019. gada;5:eaaw5096.
48.
go back to reference Sellmyer MA, Richman SA, Lohith K, Hou C, Weng CC, Mach RH. u.c. imaging CAR T cell trafficking with eDHFR as a PET reporter Gene. Mol Ther [Internets]. 2020. gada [citēts 2022. gada 20. decembrī];28:42. Iegūts no: /pmc/articles/PMC6953896/. Sellmyer MA, Richman SA, Lohith K, Hou C, Weng CC, Mach RH. u.c. imaging CAR T cell trafficking with eDHFR as a PET reporter Gene. Mol Ther [Internets]. 2020. gada [citēts 2022. gada 20. decembrī];28:42. Iegūts no: /pmc/articles/PMC6953896/.
49.
go back to reference Keu KV, Witney TH, Yaghoubi S, Rosenberg J, Kurien A, Magnusson R. u.c. Reporter gene imaging of targeted T cell immunotherapy in recurrent glioma. Sci Transl Med. 2017. gada;9. Keu KV, Witney TH, Yaghoubi S, Rosenberg J, Kurien A, Magnusson R. u.c. Reporter gene imaging of targeted T cell immunotherapy in recurrent glioma. Sci Transl Med. 2017. gada;9.
50.
go back to reference Yaghoubi SS, Jensen MC, Satyamurthy N, Budhiraja S, Paik D, Czernin J. u.c. non-invasive detection of therapeutic cytolytic T cells with [18F]FHBG Positron Emission Tomography in a glioma patient. Nat Clin Pract Oncol [Internets]. 2009. gada [citēts 2024. gada 30. janvārī];6:53. Iegūts no: /pmc/articles/PMC3526373/. Yaghoubi SS, Jensen MC, Satyamurthy N, Budhiraja S, Paik D, Czernin J. u.c. non-invasive detection of therapeutic cytolytic T cells with [18F]FHBG Positron Emission Tomography in a glioma patient. Nat Clin Pract Oncol [Internets]. 2009. gada [citēts 2024. gada 30. janvārī];6:53. Iegūts no: /pmc/articles/PMC3526373/.
51.
go back to reference Volpe A, Lang C, Lim L, Man F, Kurtys E, Ashmore-Harris C. u.c. Spatiotemporal PET Imaging Reveals Differences in CAR-T Tumor Retention in Triple-Negative Breast Cancer Models. Mol Ther. 2020. gada;28:2271–85. Volpe A, Lang C, Lim L, Man F, Kurtys E, Ashmore-Harris C. u.c. Spatiotemporal PET Imaging Reveals Differences in CAR-T Tumor Retention in Triple-Negative Breast Cancer Models. Mol Ther. 2020. gada;28:2271–85.
52.
go back to reference Sakemura R, Cox MJ, Bansal A, Roman CM, Hefazi M, Vernon CJ. u.c. Dynamic Imaging of Chimeric Antigen Receptor T Cells with [18F]Tetrafluoroborate Positron Emission Tomography/Computed Tomography. J Vis Exp [Internets]. 2022. gada [citēts 2024. gada 30. janvārī];2022. Iegūts no: https://pubmed.ncbi.nlm.nih.gov/35253798/. Sakemura R, Cox MJ, Bansal A, Roman CM, Hefazi M, Vernon CJ. u.c. Dynamic Imaging of Chimeric Antigen Receptor T Cells with [18F]Tetrafluoroborate Positron Emission Tomography/Computed Tomography. J Vis Exp [Internets]. 2022. gada [citēts 2024. gada 30. janvārī];2022. Iegūts no: https://​pubmed.​ncbi.​nlm.​nih.​gov/​35253798/​.
53.
go back to reference Yaghoubi SS, Campbell DO, Radu CG, Czernin J. Positron emission tomography reporter genes and reporter probes: Gene and cell therapy applications. Theranostics. 2012. lpp. 374–91. Yaghoubi SS, Campbell DO, Radu CG, Czernin J. Positron emission tomography reporter genes and reporter probes: Gene and cell therapy applications. Theranostics. 2012. lpp. 374–91.
54.
go back to reference Ahn BC. Sodium iodide symporter for nuclear molecular imaging and gene ther-apy: From bedside to bench and back [Internets]. Theranostics. Ivyspring International Publisher; 2012 [citēts 2020. gada 7. augustā]. lpp. 392–402. Iegūts no: /pmc/articles/PMC3337731/?report = abstract. Ahn BC. Sodium iodide symporter for nuclear molecular imaging and gene ther-apy: From bedside to bench and back [Internets]. Theranostics. Ivyspring International Publisher; 2012 [citēts 2020. gada 7. augustā]. lpp. 392–402. Iegūts no: /pmc/articles/PMC3337731/?report = abstract.
56.
go back to reference Hammill JA, VanSeggelen H, Helsen CW, Denisova GF, Evelegh C, Tantalo DGM. u.c. Designed ankyrin repeat proteins are effective targeting elements for chimeric antigen receptors. J Immunother Cancer [Internets]. 2015. gada;3:1–11. Iegūts no: https://doi.org/10.1186/s40425-015-0099-4. Hammill JA, VanSeggelen H, Helsen CW, Denisova GF, Evelegh C, Tantalo DGM. u.c. Designed ankyrin repeat proteins are effective targeting elements for chimeric antigen receptors. J Immunother Cancer [Internets]. 2015. gada;3:1–11. Iegūts no: https://​doi.​org/​10.​1186/​s40425-015-0099-4.
57.
go back to reference Liu S, Nyström NN, Kelly JJ, Hamilton AM, Fu Y, Ronald JA. Molecular Imaging Reveals a High Degree of Cross-Seeding of Spontaneous Metastases in a Novel Mouse Model of Synchronous Bilateral Breast Cancer. Mol Imaging Biol. 2022. gada;24:104–14. Liu S, Nyström NN, Kelly JJ, Hamilton AM, Fu Y, Ronald JA. Molecular Imaging Reveals a High Degree of Cross-Seeding of Spontaneous Metastases in a Novel Mouse Model of Synchronous Bilateral Breast Cancer. Mol Imaging Biol. 2022. gada;24:104–14.
59.
go back to reference Turtle CJ, Hay KA, Hanafi LA, Li D, Cherian S, Chen X. u.c. durable molecular remissions in chronic lymphocytic leukemia treated with CD19-Specific chimeric Antigen receptor–modified T cells after failure of Ibrutinib. J Clin Oncol [Internets]. 2017. gada [citēts 2022. gada 20. decembrī];35:3010. Iegūts no: /pmc/articles/PMC5590803/. Turtle CJ, Hay KA, Hanafi LA, Li D, Cherian S, Chen X. u.c. durable molecular remissions in chronic lymphocytic leukemia treated with CD19-Specific chimeric Antigen receptor–modified T cells after failure of Ibrutinib. J Clin Oncol [Internets]. 2017. gada [citēts 2022. gada 20. decembrī];35:3010. Iegūts no: /pmc/articles/PMC5590803/.
60.
go back to reference Porter DL, Hwang WT, Frey NV, Lacey SF, Shaw PA, Loren AW. u.c. Chimeric antigen receptor T cells persist and induce sustained remissions in relapsed refractory chronic lymphocytic leukemia. Sci Transl Med [Internets]. 2015. gada [citēts 2022. gada 20. decembrī];7:303ra139. Iegūts no: /pmc/articles/PMC5909068/. Porter DL, Hwang WT, Frey NV, Lacey SF, Shaw PA, Loren AW. u.c. Chimeric antigen receptor T cells persist and induce sustained remissions in relapsed refractory chronic lymphocytic leukemia. Sci Transl Med [Internets]. 2015. gada [citēts 2022. gada 20. decembrī];7:303ra139. Iegūts no: /pmc/articles/PMC5909068/.
61.
go back to reference Locke FL, Ghobadi A, Jacobson CA, Miklos DB, Lekakis LJ, Oluwole OO. u.c. Long-term safety and activity of axicabtagene ciloleucel in refractory large B-cell lymphoma (ZUMA-1): a single-arm, multicentre, phase 1–2 trial. Lancet Oncol. 2019. gada;20:31–42. Locke FL, Ghobadi A, Jacobson CA, Miklos DB, Lekakis LJ, Oluwole OO. u.c. Long-term safety and activity of axicabtagene ciloleucel in refractory large B-cell lymphoma (ZUMA-1): a single-arm, multicentre, phase 1–2 trial. Lancet Oncol. 2019. gada;20:31–42.
62.
go back to reference Locke FL, Neelapu SS, Bartlett NL, Siddiqi T, Chavez JC, Hosing CM. u.c. Phase 1 Results of ZUMA-1: A Multicenter Study of KTE-C19 Anti-CD19 CAR T Cell Therapy in Refractory Aggressive Lymphoma. Mol Ther. 2017. gada;25:285–95. Locke FL, Neelapu SS, Bartlett NL, Siddiqi T, Chavez JC, Hosing CM. u.c. Phase 1 Results of ZUMA-1: A Multicenter Study of KTE-C19 Anti-CD19 CAR T Cell Therapy in Refractory Aggressive Lymphoma. Mol Ther. 2017. gada;25:285–95.
63.
go back to reference Maude SL, Laetsch TW, Buechner J, Rives S, Boyer M, Bittencourt H. u.c. Tisagenlecleucel in Children and Young Adults with B-Cell Lymphoblastic Leukemia. N Engl J Med. 2018. gada;378:439–48. Maude SL, Laetsch TW, Buechner J, Rives S, Boyer M, Bittencourt H. u.c. Tisagenlecleucel in Children and Young Adults with B-Cell Lymphoblastic Leukemia. N Engl J Med. 2018. gada;378:439–48.
66.
go back to reference Jiang Y, Li Y, Zhu B. T-cell exhaustion in the tumor microenvironment. Cell Death Dis [Internets]. 2015. gada [citēts 2022. gada 20. decembrī];6:e1792. Iegūts no: /pmc/articles/PMC4669840/. Jiang Y, Li Y, Zhu B. T-cell exhaustion in the tumor microenvironment. Cell Death Dis [Internets]. 2015. gada [citēts 2022. gada 20. decembrī];6:e1792. Iegūts no: /pmc/articles/PMC4669840/.
68.
go back to reference Del Bufalo F, De Angelis B, Caruana I, Del Baldo G, De Ioris MA, Serra A. u.c. GD2-CART01 for Relapsed or Refractory High-Risk Neuroblastoma. N Engl J Med. 2023. gada;388:1284–95. Del Bufalo F, De Angelis B, Caruana I, Del Baldo G, De Ioris MA, Serra A. u.c. GD2-CART01 for Relapsed or Refractory High-Risk Neuroblastoma. N Engl J Med. 2023. gada;388:1284–95.
70.
go back to reference Chu J, Oh Y, Sens A, Ataie N, Dana H, Macklin JJ. u.c. A bright cyan-excitable orange fluorescent protein facilitates dual-emission microscopy and enhances bioluminescence imaging in vivo. Nat Biotechnol. 2016. gada;34:760–7. Chu J, Oh Y, Sens A, Ataie N, Dana H, Macklin JJ. u.c. A bright cyan-excitable orange fluorescent protein facilitates dual-emission microscopy and enhances bioluminescence imaging in vivo. Nat Biotechnol. 2016. gada;34:760–7.
71.
go back to reference Vedvyas Y, Shevlin E, Zaman M, Min IM, Amor-Coarasa A, Park S. u.c. longitudinal PET imaging demonstrates biphasic CAR T cell responses in survivors. JCI Insight. 2016. gada;1. Vedvyas Y, Shevlin E, Zaman M, Min IM, Amor-Coarasa A, Park S. u.c. longitudinal PET imaging demonstrates biphasic CAR T cell responses in survivors. JCI Insight. 2016. gada;1.
74.
go back to reference O’Doherty J, Jauregui-Osoro M, Brothwood T, Szyszko T, Marsden PK, O’Doherty MJ. 18F-Tetrafluoroborate, a PET Probe for Imaging Sodium/Iodide Symporter Expression: Whole-Body Biodistribution, Safety, and Radiation Dosimetry in Thyroid Cancer Patients. J Nucl Med [Internets]. 2017;58:1666–71. Iegūts no:. http://www.ncbi.nlm.nih.gov/pubmed/28385795. gada [citēts 2019. O’Doherty J, Jauregui-Osoro M, Brothwood T, Szyszko T, Marsden PK, O’Doherty MJ. 18F-Tetrafluoroborate, a PET Probe for Imaging Sodium/Iodide Symporter Expression: Whole-Body Biodistribution, Safety, and Radiation Dosimetry in Thyroid Cancer Patients. J Nucl Med [Internets]. 2017;58:1666–71. Iegūts no:. http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​28385795. gada [citēts 2019.
75.
go back to reference Emami-Shahri N, Foster J, Kashani R, Gazinska P, Cook C, Sosabowski J. u.c. Clinically compliant spatial and temporal imaging of chimeric antigen receptor T-cells. Nat Commun. 2018. gada;9:1–12. Emami-Shahri N, Foster J, Kashani R, Gazinska P, Cook C, Sosabowski J. u.c. Clinically compliant spatial and temporal imaging of chimeric antigen receptor T-cells. Nat Commun. 2018. gada;9:1–12.
76.
go back to reference Seo JH, Jeon YH, Lee YJ, Yoon GS, Won D-I, Ha J-H. u.c. Trafficking macrophage migration using reporter gene imaging with human sodium iodide symporter in animal models of inflammation. J Nucl Med. 2010. gada;51:1637–43. Seo JH, Jeon YH, Lee YJ, Yoon GS, Won D-I, Ha J-H. u.c. Trafficking macrophage migration using reporter gene imaging with human sodium iodide symporter in animal models of inflammation. J Nucl Med. 2010. gada;51:1637–43.
77.
go back to reference Lee SB, Lee HW, Lee H, Jeon YH, Lee SW, Ahn BC. u.c. Tracking dendritic cell migration into lymph nodes by using a novel PET probe 18F-tetrafluoroborate for sodium/iodide symporter. EJNMMI Res. 2017. gada;7. Lee SB, Lee HW, Lee H, Jeon YH, Lee SW, Ahn BC. u.c. Tracking dendritic cell migration into lymph nodes by using a novel PET probe 18F-tetrafluoroborate for sodium/iodide symporter. EJNMMI Res. 2017. gada;7.
78.
go back to reference Liu S, Su Y, Lin MZ, Ronald JA. Brightening up Biology: Advances in Luciferase Systems for in Vivo Imaging. ACS Chem Biol. 2021. gada;16:2707–18. Liu S, Su Y, Lin MZ, Ronald JA. Brightening up Biology: Advances in Luciferase Systems for in Vivo Imaging. ACS Chem Biol. 2021. gada;16:2707–18.
79.
go back to reference Jochems C, Hodge JW, Fantini M, Fujii R, Morillon YM, Greiner JW. u.c. An NK cell line (haNK) expressing high levels of granzyme and engineered to express the high affinity CD16 allele. Oncotarget. 2016. gada;7:86359–73. Jochems C, Hodge JW, Fantini M, Fujii R, Morillon YM, Greiner JW. u.c. An NK cell line (haNK) expressing high levels of granzyme and engineered to express the high affinity CD16 allele. Oncotarget. 2016. gada;7:86359–73.
80.
go back to reference Klingemann H, Boissel L, Toneguzzo F. Characterization of interleukin-15 gene-modified human natural killer cells: implications for adoptive cellular immunotherapy. Front. Immunol. Frontiers Media S.A.; 2016. Klingemann H, Boissel L, Toneguzzo F. Characterization of interleukin-15 gene-modified human natural killer cells: implications for adoptive cellular immunotherapy. Front. Immunol. Frontiers Media S.A.; 2016.
81.
go back to reference Marin V, Cribioli E, Philip B, Tettamanti S, Pizzitola I, Biondi A. u.c. Comparison of different suicide-gene strategies for the safety improvement of genetically manipulated T cells. Hum Gene Ther Methods. 2012. gada;23:376–86. Marin V, Cribioli E, Philip B, Tettamanti S, Pizzitola I, Biondi A. u.c. Comparison of different suicide-gene strategies for the safety improvement of genetically manipulated T cells. Hum Gene Ther Methods. 2012. gada;23:376–86.
82.
go back to reference Dahlke J, Schott JW, Barbosa PV, Klatt D, Selich A, Lachmann N. u.c. Efficient genetic safety switches for future application of ipsc-derived cell transplants. J Pers Med. 2021. gada;11. Dahlke J, Schott JW, Barbosa PV, Klatt D, Selich A, Lachmann N. u.c. Efficient genetic safety switches for future application of ipsc-derived cell transplants. J Pers Med. 2021. gada;11.
83.
go back to reference Penheiter AR, Russell SJ, Carlson SK. The Sodium Iodide Symporter (NIS) as an Imaging Reporter for Gene, Viral, and Cell-based Therapies. Curr Gene Ther [Internets]. 2012. gada [citēts 2020. gada 24. novembrī];12:33. Iegūts no: /pmc/articles/PMC3367315/?report = abstract. Penheiter AR, Russell SJ, Carlson SK. The Sodium Iodide Symporter (NIS) as an Imaging Reporter for Gene, Viral, and Cell-based Therapies. Curr Gene Ther [Internets]. 2012. gada [citēts 2020. gada 24. novembrī];12:33. Iegūts no: /pmc/articles/PMC3367315/?report = abstract.
84.
go back to reference Ahmed KA, Davis BJ, Wilson TM, Wiseman GA, Federspiel MJ, Morris JC. Progress in Gene Therapy for Prostate Cancer. Front Oncol. 2012. gada;2:1–7. Ahmed KA, Davis BJ, Wilson TM, Wiseman GA, Federspiel MJ, Morris JC. Progress in Gene Therapy for Prostate Cancer. Front Oncol. 2012. gada;2:1–7.
87.
go back to reference Kelly JJ, Saee-Marand M, Nyström NN, Evans MM, Chen Y, Martinez FM. Safe harbor-targeted CRISPR-Cas9 homology-independent targeted integration for multimodality reporter gene-based cell tracking. Sci Adv [Internets]. 2021;7:eabc3791. Iegūts no:. http://advances.sciencemag.org/. gada [citēts 2021. Kelly JJ, Saee-Marand M, Nyström NN, Evans MM, Chen Y, Martinez FM. Safe harbor-targeted CRISPR-Cas9 homology-independent targeted integration for multimodality reporter gene-based cell tracking. Sci Adv [Internets]. 2021;7:eabc3791. Iegūts no:. http://​advances.​sciencemag.​org/​. gada [citēts 2021.
Metadata
Title
Imaging CAR-NK cells targeted to HER2 ovarian cancer with human sodium-iodide symporter-based positron emission tomography
Authors
Nourhan Shalaby
Ying Xia
John J Kelly
Rafael Sanchez-Pupo
Francisco Martinez
Matthew S Fox
Jonathan D Thiessen
Justin W Hicks
Timothy J Scholl
John A. Ronald
Publication date
09-05-2024
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nuclear Medicine and Molecular Imaging
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-024-06722-w