The use of molecular imaging of gene expression by radiotracers in gene therapy

Expert Opinion on Biological Therapy

Volumn 11, Issue 10, 2011, Pages 1273-1285

  Richard Fiardo, Peggy ^a   Franken, Philippe R ^b   Harrington, Kevin J ^c   Vassaux, Georges ^a   Cambien, Béatrice ^b  

^a INSERM   (France)

^b Laboratoire TIRO   (France)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

Biosafety; Gene therapy; HSV tk; Molecular imaging; NIS; PET; SPECT; Transgene expression

Indexed keywords

(3 IODOBENZYL)GUANIDINE I 123; 3 (2 FLUOROETHYL)SPIPERONE; [2 [[2 [[[3 (4 CHLOROPHENYL) 8 METHYL 8 AZABICYCLO[3.2.1]OCT 2 YL]METHYL](2 MERCAPTOETHYL)AMINO]ETHYL]AMINO]ETHANETHIOLATO]OXOTECHNETIUM TC 99M; EDOTREOTIDE; EDOTREOTIDE Y 90; FIALURIDINE; FLUORODEOXYGLUCOSE F 18; GANCICLOVIR; PENTETREOTIDE IN 111; RACLOPRIDE C 11; RADIOPHARMACEUTICAL AGENT; THYMIDINE KINASE; UNCLASSIFIED DRUG;

GENE EXPRESSION; GENE THERAPY; HERPES SIMPLEX VIRUS 1; HUMAN; IN VIVO STUDY; MOLECULAR IMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; REPORTER GENE; REVIEW; SCINTILLATION CAMERA; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY;

ANIMALS; CLINICAL TRIALS AS TOPIC; DIAGNOSTIC IMAGING; GENE EXPRESSION; GENE THERAPY; HUMANS; MOLECULAR IMAGING; POSITRON-EMISSION TOMOGRAPHY; RADIOACTIVE TRACERS; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON;

ANIMALIA; SIMPLEXVIRUS;

EID: 80052447698     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.2011.588596     Document Type: Review

References (125)

1. Wolfe D, Mata M, Fink DJ. A human trial of HSV-mediated gene transfer for the treatment of chronic pain. Gene Ther 2009;11:455-60
2. Geus-Oei LF, Oyen WJ. Predictive and prognostic value of FDG-PET. Cancer Imaging 2008;8:70-80 (Pubitemid 351517292)
3. Kelly KA, Setlur SR, Ross R, et al. Detection of early prostate cancer using a hepsin-targeted imaging agent. Cancer Res 2008;68:2286-91 (Pubitemid 351521802)
4. Jacobs A, Voges J, Reszka R, et al. Positron-emission tomography of vector-mediated gene expression in gene therapy for gliomas. Lancet 2001;358:727-9 (Pubitemid 32823405)
5. Penuelas I, Mazzolini G, Boan JF, et al. Positron emission tomography imaging of adenoviral-mediated transgene expression in liver cancer patients. Gastroenterology 2005;128:1787-95 (Pubitemid 40824689)
6. Barton KN, Stricker H, Brown SL, et al. Phase I study of noninvasive imaging of adenovirus-mediated gene expression in the human prostate. Mol Ther 2008;16:1761-9
7. Sangro B, Mazzolini G, Ruiz M, et al. A Phase I clinical trial of thymidine kinase-based gene therapy in advanced hepatocellular carcinoma. Cancer Gene Ther 2010;17:837-43
8. Lipshutz GS, Gruber CA, Cao Y, et al. In utero delivery of adeno-associated viral vectors: intraperitoneal gene transfer produces long-term expression. Mol Ther 2001;3:284-92 (Pubitemid 32514643)
9. Sweeney TJ, Mailander V, Tucker AA, et al. Visualizing the kinetics of tumor-cell clearance in living animals. Proc Natl Acad Sci USA 1999;96:12044-9 (Pubitemid 29502855)
10. Nakajima A, Seroogy CM, Sandora MR, et al. Antigen-specific T cell-mediated gene therapy in collagen-induced arthritis. J Clin Invest 2001;107:1293-301 (Pubitemid 32494546)
11. Contag PR, Olomu IN, Stevenson DK, Contag CH. Bioluminescent indicators in living mammals. Nat Med 1998;4:245-7 (Pubitemid 28137381)
12. Contag CH, Contag PR, Mullins JI, et al. Photonic detection of bacterial pathogens in living hosts. Mol Microbiol 1995;18:593-603 (Pubitemid 26008843)
13. Contag CH, Spilman SD, Contag PR, et al. Visualizing gene expression in living mammals using a bioluminescent reporter. Photochem Photobiol 1997;66:523-31 (Pubitemid 127470201)
14. Contag CH, Bachmann MH. Advances in in vivo bioluminescence imaging of gene expression. Annu Rev Biomed Eng 2002;4:235-60 (Pubitemid 35217421)
15. Benaron DA, Contag PR, Contag CH. Imaging brain structure and function, infection and gene expression in the body using light. Philos Trans R Soc Lond B Biol Sci 1997;352:755-61 (Pubitemid 27354108)
16. Ray P, De A, Min JJ, et al. Imaging tri-fusion multimodality reporter gene expression in living subjects. Cancer Res 2004;64:1323-30 (Pubitemid 38235600)
17. Lockley M, Fernandez M, Wang Y, et al. Activity of the adenoviral E1A deletion mutant dl922-947 in ovarian cancer: comparison with E1A wild-type viruses, bioluminescence monitoring, and intraperitoneal delivery in icodextrin. Cancer Res 2006;66:989-98 (Pubitemid 43165967)
18. Rehemtulla A, Stegman LD, Cardozo SJ, et al. Rapid and quantitative assessment of cancer treatment response using in vivo bioluminescence imaging. Neoplasia 2000;2:491-5 (Pubitemid 32098683)
19. Edinger M, Cao YA, Hornig YS, et al. Advancing animal models of neoplasiathrough in vivo bioluminescence imaging. Eur J Cancer 2002;38:2128-36 (Pubitemid 35223250)
20. Wetterwald A, van der Pluijm G, Que I, et al. Optical imaging of cancer metastasis to bone marrow: a mouse model of minimal residual disease. Am J Pathol 2002;160:1143-53 (Pubitemid 34224600)
21. Shah K, Jacobs A, Breakefield XO, Weissleder R. Molecular imaging of gene therapy for cancer. Gene Ther 2004;11:1175-87 (Pubitemid 39136781)
22. Shah K, Tang Y, Breakefield X, Weissleder R. Real-time imaging of TRAIL-induced apoptosis of glioma tumors in vivo. Oncogene 2003;22:6865-72 (Pubitemid 37386686)
23. Bhaumik S, Gambhir SS. Optical imaging of renilla luciferase reporter gene expression in living mice. Proc Natl Acad Sci USA 2002;99:377-82 (Pubitemid 34060369)
24. Becker A, Hessenius C, Licha K, et al. Receptor-targeted optical imaging of tumors with near-infrared fluorescent ligands. Nat Biotechnol 2001;19:327-31 (Pubitemid 32275340)
25. Smith BR, Johnson GA, Groman EV, Linney E. Magnetic resonance microscopy of mouse embryos. Proc Natl Acad Sci USA 1994;91:3530-3 (Pubitemid 24139463)
26. Jacobs RE, Fraser SE. Magnetic resonance microscopy of embryonic cell lineages and movements. Science 1994;263:681-4 (Pubitemid 24076295)
27. Vande Velde G, Baekelandt V, Dresselaers T, Himmelreich U. Magnetic resonance imaging and spectroscopy methods for molecular imaging. Q J Nucl Med Mol Imaging 2009;53:565-85
28. Moore A, Basilion JP, Chiocca EA, Weissleder R. Measuring transferring receptor gene expression by NMR imaging. Biochim Biophys Acta 1998;1402:239-49 (Pubitemid 28206918)
29. Shen T, Weissleder R, Papisov M, et al. Monocrystalline iron oxide nanocompounds (MION): physicochemical properties. Magn Reson Med 1993;29:599-604 (Pubitemid 23138048)
30. Weissleder R, Moore A, Mahmood U, et al. In vivo magnetic resonance imaging of transgene expression. Nat Med 2000;6:351-5
31. Genove G, DeMarco U, Xu H, et al. A new transgene reporter for in vivo magnetic resonance imaging. Nat Med 2005;11:450-4 (Pubitemid 40562338)
32. Deans AE, Wadghiri YZ, Bernas LM, et al. Cellular MRI contrast via coexpression of transferrin receptor and ferritin. Magn Reson Med 2006;56:51-9
33. Liu J, Cheng EC, Long RC, et al. Noninvasive monitoring of embryonic stem cells in vivo with MRI transgene reporter. Tissue Eng Part C Methods 2009;15:739-47
34. Ono K, Fuma K, Tabata K, Sawada M. Ferritin reporter used for gene expression imaging by magnetic resonance. Biochem Biophys Res Commun 2009;388:589-94
35. Kim HS, Cho HR, Choi SH, et al. In vivo imaging of tumor transduced with bimodal lentiviral vector encoding human ferritin and green fluorescent protein on a 1.5T clinical magnetic resonance scanner. Cancer Res 2010;70:7315-24
36. Aung W, Hasegawa S, Koshikawa-Yano M, et al. Visualization of in vivo electroporation-mediated transgene expression in experimental tumors by optical and magnetic resonance imaging. Gene Ther 2009;16:830-9
37. Vande Velde G, Rangarajan JR, Toelen J, et al. Evaluation of the specificity and sensitivity of ferritin as an MRI reporter gene in the mouse brain using lentiviral and adeno-associated viral vectors. Gene Ther 2011: published online 24 February 2011, doi:10.1038/gt.2011.2
38. Vassaux G, Groot-Wassink T. In vivo noninvasive imaging for gene therapy. J Biomed Biotechnol 2003;2003:92-101 (Pubitemid 36828263)
39. Penuelas I, Haberkorn U, Yaghoubi S, Gambhir SS. Gene therapy imaging in patients for oncological applications. Eur J Nucl Med Mol Imaging 2005;32(Suppl 2):S384-403 (Pubitemid 41796402)
40. Rosenthal MS, Cullom J, Hawkins W, et al. Quantitative SPECT imaging: a review and recommendations by the focus committee of the society of nuclear medicine computer and instrumentation council. J Nucl Med 1995;36:1489-513
41. Walker RC, Purnell GL, Jones-Jackson LB, et al. Introduction to PET imaging with emphasis on biomedical research. Neurotoxicology 2004;25:533-42 (Pubitemid 38739111)
42. Jansen FP, Vanderheyden JL. The future of SPECT in a time of PET. Nucl Med Biol 2007;34:733-5 (Pubitemid 47516659)
43. Briat A, Vassaux G. Preclinical applications of imaging for cancer gene therapy. Expert Rev Mol Med 2006;8:1-19 (Pubitemid 44070081)
44. Carlson SK, Classic KL, Hadac EM, et al. In vivo quantitation of intratumoral radioisotope uptake using micro-single photon emission computed tomography/ computed tomography. Mol Imaging Biol 2006;8:324-32 (Pubitemid 44741369)
45. Chatziioannou AF. PET scanners dedicated to molecular imaging of small animal models. Mol Imaging Biol 2002;4:47-63 (Pubitemid 34272710)
46. Sangro B, Qian C, Ruiz J, Prieto J. Tracing transgene expression in cancer gene therapy: a requirement for rational progress in the field. Mol Imaging Biol 2002;4:27-33 (Pubitemid 34272708)
47. Haberkorn U, Altmann A, Mier W, Eisenhut M. Impact of functional genomics and proteomics on radionuclide imaging. Semin Nucl Med 2004;34:4-22 (Pubitemid 38056400)
48. Banerjee D. Technology evaluation: gene therapy (mesothelioma), NCI. Curr Opin Mol Ther 1999;1:517-20 (Pubitemid 29420049)
49. Gambhir SS, Bauer E, Black ME, et al. 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 2000;97:2785-90 (Pubitemid 30159249)
50. Liang Q, Satyamurthy N, Barrio JR, et al. Noninvasive, quantitative imaging in living animals of a mutant dopamine D2 receptor reporter gene in which ligand binding is uncoupled from signal transduction. Gene Ther 2001;8:1490-8 (Pubitemid 32994660)
51. Qiao J, Doubrovin M, Sauter BV, et al. Tumor-specific transcriptional targeting of suicide gene therapy. Gene Ther 2002;9:168-75 (Pubitemid 34189576)
52. Tjuvajev JG, Avril N, Oku T, et al. Imaging herpes virus thymidine kinase gene transfer and expression by positron emission tomography. Cancer Res 1998;58:4333-41 (Pubitemid 28450034)
53. Bennett JJ, Tjuvajev J, Johnson P, et al. Positron emission tomographyimaging for herpes virus infection: Implications for oncolytic viral treatments of cancer. Nat Med 2001;7:859-63 (Pubitemid 32691643)
54. Hackman T, Doubrovin M, Balatoni J, et al. Imaging expression of cytosine deaminase-herpes virus thymidine kinase fusion gene (CD/TK) expression with [124I]FIAU and PET. Mol Imaging 2002;1:36-42
55. Vassaux G, Martin-Duque P. Use of suicide genes for cancer gene therapy: study of the different approaches. Expert Opin Biol Ther 2004;4:519-30 (Pubitemid 38480551)
56. MacLaren DC, Gambhir SS, Satyamurthy N, et al. Repetitive, non-invasive imaging of the dopamine D2 receptor as a reporter gene in living animals. Gene Ther 1999;6:785-91 (Pubitemid 29243651)
57. u-TETA- octreotide as a PET imaging agent for patients with neuroendocrine tumors. J Nucl Med 2001;42:213-21 (Pubitemid 32150511)
58. Henze M, Schuhmacher J, Hipp P, et al. PET imaging of somatostatin receptors using [68GA]DOTA-D-Phe1- Tyr3-octreotide: first results in patients with meningiomas. J Nucl Med 2001;42:1053-6 (Pubitemid 32595304)
59. Wester HJ, Schottelius M, Scheidhauer K, et al. PET imaging of somatostatin receptors: design, synthesis and preclinical evaluation of a novel 18F-labelled, carbohydrated analogue of octreotide. Eur J Nucl Med Mol Imaging 2003;30:117-22 (Pubitemid 36692901)
60. Zinn KR, Chaudhuri TR. The type 2 human somatostatin receptor as a platform for reporter gene imaging. Eur J Nucl Med Mol Imaging 2002;29:388-99 (Pubitemid 34253253)
61. Kogai T, Taki K, Brent GA. Enhancement of sodium/iodide symporter expression in thyroid and breast cancer. Endocr Relat Cancer 2006;13:797-826 (Pubitemid 44763258)
62. Hingorani M, Spitzweg C, Vassaux G, et al. The biology of the sodium iodide symporter and its potential for targeted gene delivery. Curr Cancer Drug Targets 2010;10:242-67
63. Spitzweg C, O'Connor MK, Bergert ER, et al. Treatment of prostate cancer by radioiodine therapy after tissue-specific expression of the sodium iodide symporter. Cancer Res 2000;60:6526-30
64. Boland A, Ricard M, Opolon P, et al. Adenovirus-mediated transfer of the thyroid sodium/iodide symporter gene into tumors for a targeted radiotherapy. Cancer Res 2000;60:3484-92 (Pubitemid 30482168)
65. Barton KN, Tyson D, Stricker H, et al. GENIS: gene expression of sodium iodide symporter for noninvasive imaging of gene therapy vectors and quantification of gene expression in vivo. Mol Ther 2003;8:508-18 (Pubitemid 37161473)
66. Montiel-Equihua CA, Martin-Duque P, de la Vieja A, et al. Targeting sodium/ iodide symporter gene expression for estrogen-regulated imaging and therapy in breast cancer. Cancer Gene Ther 2008;15:465-73 (Pubitemid 351822191)
67. +/I - symporter gene. Endocrinology 1997;138:4493-6 (Pubitemid 27408501)
68. Groot-Wassink T, Aboagye EO, Wang Y, et al. Noninvasive imaging of the transcriptional activities of human telomerase promoter fragments in mice. Cancer Res 2004;64:4906-11 (Pubitemid 38924536)
69. Cho YW, Park SA, Han TH, et al. In vivo tumor targeting and radionuclide imaging with self-assembled nanoparticles: mechanisms, key factors, and their implications. Biomaterials 2007;28:1236-47 (Pubitemid 44816372)
70. Raty JK, Liimatainen T, Unelma Kaikkonen M, et al. Non-invasive Imaging in Ge ne Therapy. Mol Ther 2007;15:1579-86
71. Jauregui-Osoro M, Sunassee K, Weeks AJ, et al. Synthesis and biological evaluation of [18F]tetrafluoroborate: a PET imaging agent for thyroid disease and reporter gene imaging of the sodium/iodide symporter. Eur J Nucl Med Mol Imaging 2010;37:2108-16
72. Willhauck MJ, Samani BR, Wolf I, et al. The potential of 211Astatine for NIS-mediated radionuclide therapy in prostate cancer. Eur J Nucl Med Mol Imaging 2008;35:1272-81
73. Kang JH, Chung JK, Lee YJ, et al. Establishment of a human hepatocellular carcinoma cell line highly expressing sodium iodide symporter for radionuclide gene therapy. J Nucl Med 2004;45:1571-6
74. Dadachova E, Nguyen A, Lin EY, et al. Treatment with rhenium-188- perrhenate and iodine-131 of NIS-expressing mammary cancer in a mouse model remarkably inhibited tumor growth. Nucl Med Biol 2005;32:695-700 (Pubitemid 41502974)
75. Shen DH, Marsee DK, Schaap J, et al. Effects of dose, intervention time, and radionuclide on sodium iodide symporter (NIS)-targeted radionuclide therapy. Gene Ther 2004;11:161-9 (Pubitemid 38159688)
76. Doubrovin M, Ponomarev V, Beresten T, et al. Imaging transcriptional regulation of p53-dependent genes with positron emission tomography in vivo. Proc Natl Acad Sci USA 2001;98:9300-5 (Pubitemid 32743911)
77. Kim SH, Chung HK, Kang JH, et al. Tumor-targeted radionuclide imaging and therapy based on human sodium iodide symporter gene driven by a modified telomerase reverse transcriptase promoter. Hum Gene Ther 2008;19:951-7
78. Brader P, Kelly KJ, Chen N, et al. Imaging a genetically engineered oncolytic vaccinia virus (GLV-1h99) using a human norepinephrine transporter reporter gene. Clin Cancer Res 2009;15:3791-801
79. Yaghoubi SS, Wu L, Liang Q, et al. Direct correlation between positron emission tomographic images of two reporter genes delivered by two distinct adenoviral vectors. Gene Ther 2001;8:1072-80 (Pubitemid 32970375)
80. Wildner O, Morris JC. The role of the E1B 55 kDa gene product in oncolytic adenoviral vectors expressing herpes simplex virus-tk: assessment of antitumor efficacy and toxicity. Cancer Res 2000;60:4167-74 (Pubitemid 30636600)
81. Dingli D, Peng KW, Harvey ME, et al. Image-guided radiovirotherapy for multiple myeloma using a recombinant measles virus expressing the thyroidal sodium iodide symporter. Blood 2004;103:1641-6 (Pubitemid 38268954)
82. Merron A, Peerlinck I, Martin-Duque P, et al. SPECT/CT imaging of oncolytic adenovirus propagation in tumours in vivo using the Na/I symporter as areporter gene. Gene Ther 2007;14:1731-8 (Pubitemid 350238450)
83. Msaouel P, Iankov ID, Allen C, et al. Noninvasive imaging and radiovirotherapy of prostate cancer using an oncolytic measles virus expressing the sodium iodide symporter. Mol Ther 2009;17:2041-8
84. Li H, Peng KW, Dingli D, et al. Oncolytic measles viruses encoding interferon beta and the thyroidal sodium iodide symporter gene for mesothelioma virotherapy. Cancer Gene Ther 2010;17:550-8
85. Merron A, Baril P, Martin-Duque P, et al. Assessment of the Na/I symporter as a reporter gene to visualize oncolytic adenovirus propagation in peritoneal tumours. Eur J Nucl Med Mol Imaging 2010;37:1377-85
86. Mullerad M, Eisenberg DP, Akhurst TJ, et al. Use of positron emission tomography to target prostate cancer gene therapy by oncolytic herpes simplex virus. Mol Imaging Biol 2006;8:30-5 (Pubitemid 44193400)
87. McCart JA, Mehta N, Scollard D, et al. Oncolytic vaccinia virus expressing the human somatostatin receptor SSTR2: molecular imaging after systemic delivery using 111In-pentetreotide. Mol Ther 2004;10:553-61 (Pubitemid 39186116)
88. Rajecki M, Kangasmaki A, Laasonen L, et al. Sodium iodide symporter SPECT imaging of a patient treated with oncolytic adenovirus Ad5/3-Delta24- hNIS. Mol Ther 2011;19:629-31
89. Hakkarainen T, Rajecki M, Sarparanta M, et al. Targeted radiotherapy for prostate cancer with an oncolytic adenovirus coding for human sodium iodide symporter. Clin Cancer Res 2009;15:5396-403
90. Peerlinck I, Merron A, Baril P, et al. Targeted radionuclide therapy using a Wnt-targeted replicating adenovirus encoding the Na/I symporter. Clin Cancer Res 2009;15:6595-601
91. Goel A, Carlson SK, Classic KL, et al. Radioiodide imaging and radiovirotherapy of multiple myeloma using VSV(Delta51)-NIS, an attenuated vesicular stomatitis virus encoding the sodium iodide symporter gene. Blood 2007;110:2342-50 (Pubitemid 47523154)
92. Lassmann M, Hanscheid H, Chiesa C, et al. EANM Dosimetry Committee series on standard operational procedures for pre-therapeutic dosimetry I: blood and bone marrow dosimetry in differentiated thyroid cancer therapy. Eur J Nucl Med Mol Imaging 2008;35:1405-12
93. Hingorani M, White CL, Zaidi S, et al. Therapeutic effect of sodium iodide symporter gene therapy combined with external beam radiotherapy and targeted drugs that inhibit DNA repair. Mol Ther 2010;18:1599-605
94. Harrington KJ, Melcher A, Vassaux G, et al. Exploiting synergies between radiation and oncolytic viruses. Curr Opin Mol Ther 2008;10:362-70
95. Hingorani M, White CL, Zaidi S, et al. Radiation-mediated upregulation of gene expression from replication-defective adenoviral vectors: implications for sodium iodide symporter gene therapy . Clin Cancer Research 2008;14:4915-24
96. Hingorani M, White CL, Merron A, et al. Inhibition of repair of radiation-induced DNA damage enhances gene expression from replication-defective adenoviral vectors. Cancer Res 2008;68:9771-8
97. +/I-symporter in human glioma cells by adenovirus-mediated gene delivery. Gene Ther 2000;7:740-9 (Pubitemid 30255755)
98. +/I- symporters for radioiodide concentrator gene therapy. J Nucl Med 2000;41:1898-904
99. Faivre J, Clerc J, Gerolami R, et al. Long-term radioiodine retention and regression of liver cancer after sodium iodide symporter gene transfer in wistar rats. Cancer Res 2004;64:8045-51 (Pubitemid 39446941)
100. Dwyer RM, Schatz SM, Bergert ER, et al. A preclinical large animal model of adenovirus-mediated expression of the sodium-iodide symporter for radioiodide imaging and therapy of locally recurrent prostate cancer. Mol Ther 2005;12:835-41 (Pubitemid 41614478)
101. Dwyer RM, Bergert ER, O'Connor M K, et al. In vivo radioiodide imaging and treatment of breast cancer xenografts after MUC1-driven expression of the sodium iodide symporter. Clin Cancer Res 2005;11:1483-9 (Pubitemid 40315230)
102. Dwyer RM, Bergert ER, O'Connor MK, et al. Adenovirus-mediated and targeted expression of the sodium-iodide symporter permits in vivo radioiodide imaging and therapy of pancreatic tumors. Hum Gene Ther 2006;17:661-8 (Pubitemid 43967869)
103. Dwyer RM, Bergert ER, O'Connor MK, et al. Sodium iodide symporter-mediated radioiodide imaging and therapy of ovarian tumor xenografts in mice. Gene Ther 2006;13:60-6 (Pubitemid 41823852)
104. Hasegawa K, Pham L, O'Connor MK, et al. Dual therapy of ovarian cancer using measles viruses expressing carcinoembryonic antigen and sodium iodide symporter. Clin Cancer Res 2006;12:1868-75
105. Chen RF, Li ZH, Pan QH, et al. In vivo radioiodide imaging and treatment of pancreatic cancer xenografts after MUC1 promoter-driven expression of the human sodium-iodide symporter. Pancreatology 2007;7:505-13 (Pubitemid 47587630)
106. Spitzweg C, Baker CH, Bergert ER, et al. Image-guided radioiodide therapy of medullary thyroid cancer after carcinoembryonic antigen promoter-targeted sodium iodide symporter gene expression. Hum Gene Ther 2007;18:916-24 (Pubitemid 47587318)
107. Carlson SK, Classic KL, Hadac EM, et al. Quantitative molecular imaging of viral therapy for pancreatic cancer using an engineered measles virus expressing the sodium-iodide symporter reporter gene. AJR Am J Roentgenol 2009;192:279-87
108. Ma XJ, Huang R, Kuang AR. AFP promoter enhancer increased specific expression of the human sodium iodide symporter (hNIS) for targeted radioiodine therapy of hepatocellular carcinoma. Cancer Invest 2009;27:673-81
109. Chisholm EJ, Vassaux G, Martin-Duque P, et al. Cancer-specific transgene expression mediated by systemic injection of nanoparticles. Cancer Res 2009;69:2655-62
110. Klutz K, Russ V, Willhauck MJ, et al. Targeted radioiodine therapy of neuroblastoma tumors following systemic nonviral delivery of the sodium iodide symporter gene. Clin Cancer Res 2009;15:6079-86
111. Penheiter AR, Wegman TR, Classic KL, et al. Sodium iodide symporter (NIS)- mediated radiovirotherapy for pancreatic cancer. AJR Am J Roentgenol 2010;195:341-9
112. Trujillo MA, Oneal MJ, McDonough S, et al. A probasin promoter, conditionally replicating adenovirus that expresses the sodium iodide symporter (NIS) for radiovirotherapy of prostate cancer. Gene Ther 2010;17:1325-32
113. Watanabe Y, Horie S, Funaki Y, et al. Delivery of Na/I symporter gene into skeletal muscle using nanobubbles and ultrasound: visualization of gene expression by PET. J Nucl Med 2010;51:951-8
114. Liang Q, Nguyen K, Satyamurthy N, et al. Monitoring adenoviral DNA delivery, using a mutant herpes simplex virus type 1 thymidine kinase gene as a PET reporter gene. Gene Ther 2002;9:1659-66 (Pubitemid 36104609)
115. Liang Q, Gotts J, Satyamurthy N, et al. Noninvasive, repetitive, quantitative measurement of gene expression from a bicistronic message by positron emission tomography, following gene transfer with adenovirus. Mol Ther 2002;6:73-82 (Pubitemid 36124273)
116. Burton JB, Johnson M, Sato M, et al.Adenovirus-mediated gene expression imaging to directly detect sentinel lymph node metastasis of prostate cancer. Nat Med 2008;14:882-8
117. Sato M, Figueiredo ML, Burton JB, et al. Configurations of a two-tiered amplified gene expression system in adenoviral vectors designed to improve the specificity of in vivo prostate cancer imaging. Gene Ther 2008;15:583-93
118. Lan X, Liu Y, He Y, et al. Autoradiography study and SPECT imaging of reporter gene HSV1-tk expression in heart. Nucl Med Biol;37:371-80
119. Auricchio A, Acton PD, Hildinger M, et al. In vivo quantitative noninvasive imaging of gene transfer by single-photon emission computerized tomography. Hum Gene Ther 2003;14:255-61 (Pubitemid 36423444)
120. Umegaki H, Ishiwata K, Ogawa O, et al. Longitudinal follow-up study of adenoviral vector-mediated gene transfer of dopamine D2 receptors in the striatum in young, middle-aged, and aged rats: a positron emission tomography study. Neuroscience 2003;121:479-86 (Pubitemid 37176935)
121. Rogers BE, Zinn KR, Lin CY, et al. Targeted radiotherapy with [90Y]-SMT 487 in mice bearing human nonsmall cell lung tumor xenografts induced to express human somatostatin receptor subtype 2 with an adenoviral vector. Cancer 2002;94(4 Suppl):1298-305 (Pubitemid 34150893)
122. Rogers BE, Parry JJ, Andrews R, et al. MicroPET imaging of gene transfer with a somatostatin receptor-based reporter gene and 94mTc-Demotate 1. J Nucl Med 2005;46:1889-97 (Pubitemid 46196652)
123. Cotugno G, Aurilio M, Annunziata P, et al. Non-invasive repetitive imaging of somatostatin receptor 2 gene transfer with positron emission tomography. Hum Gene Ther 2011;22:189-96
124. Singh SP, Han L, Murali R, et al. SSTR2-based reporters for assessing gene transfer into non-small cell lung cancer: evaluation using an intrathoracic mouse model. Hum Gene Ther 2011;22:55-64
125. Chen R, Parry JJ, Akers WJ, et al. Multimodality imaging of gene transfer with a receptor-based reporter gene. J Nucl Med;51:1456-63