Applications of nuclear-based imaging in gene and cell therapy: Probe considerations

Blasberg, 2003, Molecular-genetic imaging: current and future perspectives, J. Clin. Invest., 111, 1620, 10.1172/JCI18855 Peñuelas, 2005, Gene therapy imaging in patients for oncological applications, Eur. J. Nucl. Med. Mol. Imaging, 32, S384, 10.1007/s00259-005-1928-3 Vaquero, 2015, Positron emission tomography: current challenges and opportunities for technological advances in clinical and preclinical imaging systems, Annu. Rev. Biomed. Eng., 17, 385, 10.1146/annurev-bioeng-071114-040723 Khalil, 2011, Molecular SPECT imaging: an overview, Int. J. Mol. Imaging, 2011, 796025, 10.1155/2011/796025 Basu, 2011, Fundamentals of PET and PET/CT imaging, Ann. N Y Acad. Sci., 1228, 1, 10.1111/j.1749-6632.2011.06077.x Bailey, 2013, An evidence-based review of quantitative SPECT imaging and potential clinical applications, J. Nucl. Med., 54, 83, 10.2967/jnumed.112.111476 Lewis, 2019 Blasberg, 2002, Molecular-genetic imaging: a nuclear medicine-based perspective, Mol. Imaging, 1, 280, 10.1162/153535002760235472 Gambhir, 2000, Imaging transgene expression with radionuclide imaging technologies, Neoplasia, 2, 118, 10.1038/sj.neo.7900083 Yaghoubi, 2006, PET imaging of herpes simplex virus type 1 thymidine kinase (HSV1-tk) or mutant HSV1-sr39tk reporter gene expression in mice and humans using [18F]FHBG, Nat. Protoc., 1, 3069, 10.1038/nprot.2006.459 Pillarsetty, 2006, Synthesis and evaluation of [18F] labeled pyrimidine nucleosides for positron emission tomography imaging of herpes simplex virus 1 thymidine kinase gene expression, J. Med. Chem., 49, 5377, 10.1021/jm0512847 Zhang, 2014, Synthesis and evaluation of 18F-labeled benzylguanidine analogs for targeting the human norepinephrine transporter, Eur. J. Nucl. Med. Mol. Imaging, 41, 322, 10.1007/s00259-013-2558-9 Serganova, 2009, Multimodality imaging of TGFβ signaling in breast cancer metastases, FASEB J., 23, 2662, 10.1096/fj.08-126920 Dobrenkov, 2008, Monitoring the efficacy of adoptively transferred prostate cancer-targeted human T lymphocytes with PET and bioluminescence imaging, J. Nucl. Med., 49, 1162, 10.2967/jnumed.107.047324 Hong, 2010, In vivo imaging of RNA interference, J. Nucl. Med., 51, 169, 10.2967/jnumed.109.066878 Adonai, 2002, Ex vivo cell labeling with 64Cu-pyruvaldehyde-bis(N4-methylthiosemicarbazone) for imaging cell trafficking in mice with positron-emission tomography, Proc. Natl. Acad. Sci. USA, 99, 3030, 10.1073/pnas.052709599 Bansal, 2015, Novel 89Zr cell labeling approach for PET-based cell trafficking studies, EJNMMI Res., 5, 19, 10.1186/s13550-015-0098-y Kircher, 2003, In vivo high resolution three-dimensional imaging of antigen-specific cytotoxic T-lymphocyte trafficking to tumors, Cancer Res., 63, 6838 Read, 1990, In vivo traffic of indium-111-oxine labeled human lymphocytes collected by automated apheresis, J. Nucl. Med., 31, 999 Becker, 1988, Comparison of 99Tcm-HMPAO and 111In-oxine labelled granulocytes in man: first clinical results, Nucl. Med. Commun., 9, 435, 10.1097/00006231-198806000-00008 Daldrup-Link, 2011, MRI of tumor-associated macrophages with clinically applicable iron oxide nanoparticles, Clin. Cancer Res., 17, 5695, 10.1158/1078-0432.CCR-10-3420 Pérez-Medina, 2015, PET imaging of tumor-associated macrophages with 89Zr-labeled high-density lipoprotein nanoparticles, J. Nucl. Med., 56, 1272, 10.2967/jnumed.115.158956 Tarkin, 2014, PET imaging of inflammation in atherosclerosis, Nat. Rev. Cardiol., 11, 443, 10.1038/nrcardio.2014.80 Kang, 2015, Combined fluorescence and magnetic resonance imaging of primary macrophage migration to sites of acute inflammation using near-infrared fluorescent magnetic nanoparticles, Mol. Imaging Biol., 17, 643, 10.1007/s11307-015-0830-z Nahrendorf, 2008, Nanoparticle PET-CT imaging of macrophages in inflammatory atherosclerosis, Circulation, 117, 379, 10.1161/CIRCULATIONAHA.107.741181 Grimm, 2007, [Cell tracking. Principles and applications], Radiologe, 47, 25, 10.1007/s00117-006-1449-5 Aicher, 2003, Assessment of the tissue distribution of transplanted human endothelial progenitor cells by radioactive labeling, Circulation, 107, 2134, 10.1161/01.CIR.0000062649.63838.C9 Brenner, 2004, 111In-labeled CD34+ hematopoietic progenitor cells in a rat myocardial infarction model, J. Nucl. Med., 45, 512 Zhou, 2005, In vivo detection of stem cells grafted in infarcted rat myocardium, J. Nucl. Med., 46, 816 Pittet, 2007, In vivo imaging of T cell delivery to tumors after adoptive transfer therapy, Proc. Natl. Acad. Sci. USA, 104, 12457, 10.1073/pnas.0704460104 Blocklet, 2003, 111In-oxine and 99mTc-HMPAO labelling of antigen-loaded dendritic cells: in vivo imaging and influence on motility and actin content, Eur. J. Nucl. Med. Mol. Imaging, 30, 440, 10.1007/s00259-002-1001-4 Bennink, 2005, Dedicated pinhole SPECT of intestinal neutrophil recruitment in a mouse model of dextran sulfate sodium-induced colitis, J. Nucl. Med., 46, 526 de Vries, 2010, Guidelines for the labelling of leucocytes with 99mTc-HMPAO, Eur. J. Nucl. Med. Mol. Imaging, 37, 842, 10.1007/s00259-010-1394-4 Lukawska, 2014, Imaging inflammation in asthma: real time, differential tracking of human neutrophil and eosinophil migration in allergen challenged, atopic asthmatics in vivo, EBioMedicine, 1, 173, 10.1016/j.ebiom.2014.10.014 Lukawska, 2014, Real-time differential tracking of human neutrophil and eosinophil migration in vivo, J. Allergy Clin. Immunol., 133, 233, 10.1016/j.jaci.2013.06.031 Stojanov, 2012, 18FFDG labeling of neural stem cells for in vivo cell tracking with positron emission tomography: inhibition of tracer release by phloretin, Mol. Imaging, 11, 1, 10.2310/7290.2011.00021 Meier, 2008, Tracking of 18FFDG-labeled natural killer cells to HER2/neu-positive tumors, Nucl. Med. Biol., 35, 579, 10.1016/j.nucmedbio.2008.02.006 Zhang, 2012, 18F-FDG cell labeling may underestimate transplanted cell homing: more accurate, efficient, and stable cell labeling with hexadecyl-4-[18F]fluorobenzoate for in vivo tracking of transplanted human progenitor cells by positron emission tomography, Cell Transplant., 21, 1821, 10.3727/096368911X637416 Swirski, 2006, Monocyte accumulation in mouse atherogenesis is progressive and proportional to extent of disease, Proc. Natl. Acad. Sci. USA, 103, 10340, 10.1073/pnas.0604260103 Avila-Rodriguez, 2017, Biodistribution and radiation dosimetry of [64Cu]copper dichloride: first-in-human study in healthy volunteers, EJNMMI Res., 7, 98, 10.1186/s13550-017-0346-4 Sato, 2020, In vivo tracking of adoptively transferred natural killer cells in rhesus macaques using 89zirconium-oxine cell labeling and PET imaging, Clin. Cancer Res., 26, 2573, 10.1158/1078-0432.CCR-19-2897 Weist, 2018, PET of adoptively transferred chimeric antigen receptor T cells with 89Zr-oxine, J. Nucl. Med., 59, 1531, 10.2967/jnumed.117.206714 Sato, 2015, 89Zr-oxine complex PET cell imaging in monitoring cell-based therapies, Radiology, 275, 490, 10.1148/radiol.15142849 Man, 2019, In vivo pet tracking of 89Zr-labeled Vγ9Vδ2 T cells to mouse xenograft breast tumors activated with liposomal alendronate, Mol. Ther., 27, 219, 10.1016/j.ymthe.2018.10.006 Botti, 1997, Comparison of three different methods for radiolabelling human activated T lymphocytes, Eur. J. Nucl. Med., 24, 497 Rogers, 1999, In vivo localization of [111In]-DTPA-d-Phe1-octreotide to human ovarian tumor xenografts induced to express the somatostatin receptor subtype 2 using an adenoviral vector, Clin. Cancer Res., 5, 383 Shulkin, 1986, Iodine-123-4-amino-3-iodobenzylguanidine, a new sympathoadrenal imaging agent: comparison with iodine-123 metaiodobenzylguanidine, J. Nucl. Med., 27, 1138 Glowniak, 1993, Evaluation of metaiodobenzylguanidine uptake by the norepinephrine, dopamine and serotonin transporters, J. Nucl. Med., 34, 1140 Russell, 2007, Viruses as anticancer drugs, Trends Pharmacol. Sci., 28, 326, 10.1016/j.tips.2007.05.005 Russell, 2012, Oncolytic virotherapy, Nat. Biotechnol., 30, 658, 10.1038/nbt.2287 Mineta, 1995, Attenuated multi-mutated herpes simplex virus-1 for the treatment of malignant gliomas, Nat. Med., 1, 938, 10.1038/nm0995-938 Kooby, 1999, Oncolytic viral therapy for human colorectal cancer and liver metastases using a multi-mutated herpes simplex virus type-1 (G207), FASEB J., 13, 1325, 10.1096/fasebj.13.11.1325 Yoon, 2000, An oncolytic herpes simplex virus type 1 selectively destroys diffuse liver metastases from colon carcinoma, FASEB J., 14, 301, 10.1096/fasebj.14.2.301 Carew, 1999, Selective infection and cytolysis of human head and neck squamous cell carcinoma with sparing of normal mucosa by a cytotoxic herpes simplex virus type 1 (G207), Hum. Gene Ther., 10, 1599, 10.1089/10430349950017608 Toyoizumi, 1999, Combined therapy with chemotherapeutic agents and herpes simplex virus type 1 ICP34.5 mutant (HSV-1716) in human non-small cell lung cancer, Hum. Gene Ther., 10, 3013, 10.1089/10430349950016410 Advani, 1999, Replication-competent, nonneuroinvasive genetically engineered herpes virus is highly effective in the treatment of therapy-resistant experimental human tumors, Cancer Res., 59, 2055 Bennett, 2001, Positron emission tomography imaging for herpes virus infection: Implications for oncolytic viral treatments of cancer, Nat. Med., 7, 859, 10.1038/89991 Peñuelas, 2005, Positron emission tomography imaging of adenoviral-mediated transgene expression in liver cancer patients, Gastroenterology, 128, 1787, 10.1053/j.gastro.2005.03.024 Moolten, 1994, Drug sensitivity (“suicide”) genes for selective cancer chemotherapy, Cancer Gene Ther., 1, 279 Miller, 2016, The use of the NIS reporter gene for optimizing oncolytic virotherapy, Expert Opin. Biol. Ther., 16, 15, 10.1517/14712598.2016.1100162 Hasegawa, 2006, Dual therapy of ovarian cancer using measles viruses expressing carcinoembryonic antigen and sodium iodide symporter, Clin. Cancer Res., 12, 1868, 10.1158/1078-0432.CCR-05-1803 Dingli, 2004, Image-guided radiovirotherapy for multiple myeloma using a recombinant measles virus expressing the thyroidal sodium iodide symporter, Blood, 103, 1641, 10.1182/blood-2003-07-2233 Liu, 2010, Systemic therapy of disseminated myeloma in passively immunized mice using measles virus-infected cell carriers, Mol. Ther., 18, 1155, 10.1038/mt.2010.43 Msaouel, 2009, Noninvasive imaging and radiovirotherapy of prostate cancer using an oncolytic measles virus expressing the sodium iodide symporter, Mol. Ther., 17, 2041, 10.1038/mt.2009.218 Blechacz, 2006, Engineered measles virus as a novel oncolytic viral therapy system for hepatocellular carcinoma, Hepatology, 44, 1465, 10.1002/hep.21437 Penheiter, 2010, Sodium iodide symporter (NIS)-mediated radiovirotherapy for pancreatic cancer, AJR Am. J. Roentgenol., 195, 341, 10.2214/AJR.09.3672 Merron, 2007, SPECT/CT imaging of oncolytic adenovirus propagation in tumours in vivo using the Na/I symporter as a reporter gene, Gene Ther., 14, 1731, 10.1038/sj.gt.3303043 Dingli, 2003, Genetically targeted radiotherapy for multiple myeloma, Blood, 102, 489, 10.1182/blood-2002-11-3390 Likar, 2010, A new pyrimidine-specific reporter gene: a mutated human deoxycytidine kinase suitable for PET during treatment with acycloguanosine-based cytotoxic drugs, J. Nucl. Med., 51, 1395, 10.2967/jnumed.109.074344 McCracken, 2015, Noninvasive detection of tumor-infiltrating T cells by PET reporter imaging, J. Clin. Invest., 125, 1815, 10.1172/JCI77326 Vedvyas, 2016, Longitudinal PET imaging demonstrates biphasic CAR T cell responses in survivors, JCI Insight, 1, e90064, 10.1172/jci.insight.90064 Moroz, 2015, Comparative analysis of T cell imaging with human nuclear reporter genes, J. Nucl. Med., 56, 1055, 10.2967/jnumed.115.159855 Miyagawa, 2008, Imaging of HSV-tk reporter gene expression: comparison between [18F]FEAU, [18F]FFEAU, and other imaging probes, J. Nucl. Med., 49, 637, 10.2967/jnumed.107.046227 Rao, 2007, Sodium iodide symporter (hNIS) permits molecular imaging of gene transduction in cardiac transplantation, Transplantation, 84, 1662, 10.1097/01.tp.0000295932.26883.ba Mayer-Kuckuk, 2006, Molecular imaging reveals skeletal engraftment sites of transplanted bone marrow cells, Cell Transplant., 15, 75, 10.3727/000000006783982278 Ashmore-Harris, 2019, Reporter gene-engineering of human induced pluripotent stem cells during differentiation renders in vivo traceable hepatocyte-like cells accessible, Stem Cell Res. (Amst.), 41, 101599, 10.1016/j.scr.2019.101599 Koehne, 2003, Serial in vivo imaging of the targeted migration of human HSV-TK-transduced antigen-specific lymphocytes, Nat. Biotechnol., 21, 405, 10.1038/nbt805 Dotti, 2009, Repetitive noninvasive monitoring of HSV1-tk-expressing T cells intravenously infused into nonhuman primates using positron emission tomography and computed tomography with 18F-FEAU, Mol. Imaging, 8, 230, 10.2310/7290.2009.00022 Doubrovin, 2007, In vivo imaging and quantitation of adoptively transferred human antigen-specific T cells transduced to express a human norepinephrine transporter gene, Cancer Res., 67, 11959, 10.1158/0008-5472.CAN-07-1250 Volpe, 2020, Spatiotemporal PET imaging reveals differences in CAR-T tumor retention in triple-negative breast cancer models, Mol. Ther., 28, 2271, 10.1016/j.ymthe.2020.06.028 O’Doherty, 2017, 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., 58, 1666, 10.2967/jnumed.117.192252 Ponomarev, 2001, Imaging TCR-dependent NFAT-mediated T-cell activation with positron emission tomography in vivo, Neoplasia, 3, 480, 10.1038/sj.neo.7900204 Mayer-Kuckuk, 2002, Cells exposed to antifolates show increased cellular levels of proteins fused to dihydrofolate reductase: a method to modulate gene expression, Proc. Natl. Acad. Sci. USA, 99, 3400, 10.1073/pnas.062036899 Alauddin, 1996, 9-[(3-[18F]-fluoro-1-hydroxy-2-propoxy)methyl]guanine ([18F]-FHPG): a potential imaging agent of viral infection and gene therapy using PET, Nucl. Med. Biol., 23, 787, 10.1016/0969-8051(96)00075-3 Alauddin, 1998, Synthesis and preliminary evaluation of 9-(4-[18F]-fluoro-3-hydroxymethylbutyl)guanine ([18F]FHBG): a new potential imaging agent for viral infection and gene therapy using PET, Nucl. Med. Biol., 25, 175, 10.1016/S0969-8051(97)00160-1 Gambhir, 1999, Imaging adenoviral-directed reporter gene expression in living animals with positron emission tomography, Proc. Natl. Acad. Sci. USA, 96, 2333, 10.1073/pnas.96.5.2333 Gambhir, 2000, A mutant herpes simplex virus type 1 thymidine kinase reporter gene shows improved sensitivity for imaging reporter gene expression with positron emission tomography, Proc. Natl. Acad. Sci. USA, 97, 2785, 10.1073/pnas.97.6.2785 Haberkorn, 1998, Ganciclovir uptake in human mammary carcinoma cells expressing herpes simplex virus thymidine kinase, Nucl. Med. Biol., 25, 367, 10.1016/S0969-8051(97)00210-2 Alauddin, 2004, Synthesis of 2′-deoxy-2′-[18F]fluoro-5-bromo-1-β-d-arabinofuranosyluracil ([18F]-FBAU) and 2′-deoxy-2′-[18F]fluoro-5-chloro-1-β-d-arabinofuranosyl-uracil ([18F]-FCAU), and their biological evaluation as markers for gene expression, Nucl. Med. Biol., 31, 399, 10.1016/j.nucmedbio.2003.12.008 Fuchigami, 2020, Synthesis and characterization of 9-(4-[18F]fluoro-3-(hydroxymethyl)butyl)-2-(phenylthio)-6-oxopurine as a novel PET agent for mutant herpes simplex virus type 1 thymidine kinase reporter gene imaging, Mol. Imaging Biol., 22, 1151, 10.1007/s11307-020-01517-5 Yaghoubi, 2001, Human pharmacokinetic and dosimetry studies of [18F]FHBG: a reporter probe for imaging herpes simplex virus type-1 thymidine kinase reporter gene expression, J. Nucl. Med., 42, 1225 Tjuvajev, 2002, Comparison of radiolabeled nucleoside probes (FIAU, FHBG, and FHPG) for PET imaging of HSV1-tk gene expression, J. Nucl. Med., 43, 1072 Yaghoubi, 2009, Noninvasive detection of therapeutic cytolytic T cells with 18F-FHBG PET in a patient with glioma, Nat. Clin. Pract. Oncol., 6, 53, 10.1038/ncponc1278 Keu, 2017, Reporter gene imaging of targeted T cell immunotherapy in recurrent glioma, Sci. Transl. Med., 9, eaag2196, 10.1126/scitranslmed.aag2196 Likar, 2009, PET imaging of HSV1-tk mutants with acquired specificity toward pyrimidine- and acycloguanosine-based radiotracers, Eur. J. Nucl. Med. Mol. Imaging, 36, 1273, 10.1007/s00259-009-1089-x Kircher, 2011, Noninvasive cell-tracking methods, Nat. Rev. Clin. Oncol., 8, 677, 10.1038/nrclinonc.2011.141 Minn, 2014, Molecular-genetic imaging of cancer, Adv. Cancer Res., 124, 131, 10.1016/B978-0-12-411638-2.00004-5 Hoekstra, 2015, Assessing T lymphocyte function and differentiation by genetically encoded reporter systems, Trends Immunol., 36, 392, 10.1016/j.it.2015.05.008 Cherry, 2018, Total-body PET: maximizing sensitivity to create new opportunities for clinical research and patient care, J. Nucl. Med., 59, 3, 10.2967/jnumed.116.184028 Shao, 1997, Simultaneous PET and MR imaging, Phys. Med. Biol., 42, 1965, 10.1088/0031-9155/42/10/010 Slates, 1999, A study of artefacts in simultaneous PET and MR imaging using a prototype MR compatible PET scanner, Phys. Med. Biol., 44, 2015, 10.1088/0031-9155/44/8/312