Positron emission tomography reporter genes and reporter probes: Gene and cell therapy applications

Theranostics

Volumn 2, Issue 4, 2012, Pages 374-391

  Yaghoubi, Shahriar S ^a,b   Campbell, Dean O ^a   Radu, Caius G ^a   Czernin, Johannes ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CellSight Technologies Inc   (United States)

Author keywords

Genetically modified therapeutic cells; Imaging therapeutic transgenes or cells; PET imaging reporter genes; Positron emission tomography; Therapeutic transgenes

Indexed keywords

3 (2 FLUOROETHYL)SPIPERONE F 18; 3 METHYLSPIPERONE C 11; BETA GALACTOSIDASE; BETA GALACTOSIDASE C 11; CARBON 11; CARCINOEMBRYONIC ANTIGEN; CLEVUDINE; CLEVUDINE F 18; DEOXYCYTIDINE KINASE; FEAU F 18; FIALURIDINE; FIALURIDINE I 124; FLUORO 3 HYDROXYMETHYLBUTYL GUANINE F 18; FLUOROETHYLSPIPERONE; FLUOROETHYLSPIPERONE F 18; GALLIUM 68; IODINE 124; MACROGOL; MITOCHONDRIAL THYMIDINE KINASE 2; NORADRENALIN TRANSPORTER; NUCLEOSIDE ANALOG; PENCICLOVIR; RACLOPRIDE C 11; RADIOPHARMACEUTICAL AGENT; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; SODIUM IODIDE SYMPORTER; TETRAXETAN; THYMIDINE KINASE; UNCLASSIFIED DRUG; UNINDEXED DRUG; YTTRIUM 86;

CELL PROLIFERATION; CELL SURVIVAL; CELL THERAPY; DNA MODIFICATION; DRUG MECHANISM; GENE EXPRESSION; GENE THERAPY; HUMAN; IMMUNOGENICITY; KINETICS; MOLECULAR IMAGING; MOLECULAR PROBE; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; REPORTER GENE; REVIEW; RNA TRANSLATION; TRANSGENICS; VARICELLA ZOSTER VIRUS;

EID: 84864545156     PISSN: None     EISSN: 18387640     Source Type: Journal    
DOI: 10.7150/thno.3677     Document Type: Review

References (123)

1. Herzog RW, Cao O, Srivastava A. Two decades of clinical gene therapy-success is finally mounting. Discovery Medicine 2010; 9: 105-111.
2. Hackett PB, Largaespada DA, Cooper LJ. A transposon and transposase system for human application. Mol Ther 2010; 18: 674-683.
3. Al-Dosari MS, Gao X. Nonviral gene delivery: principle, limita-tions, and recent progress. AAPS J 2009; 11: 671-681.
4. Gambhir SS, Yaghoubi SS. Molecular Imaging With Reporter Genes. Cambridge University Press, 2010.
5. Acton PD, Zhou R. Imaging reporter genes for cell tracking with PET and SPECT. Quarterly Journal of Nuclear Medicine and Molecular Imaging 2005; 49: 349-360.
6. Herschman HR, MacLaren DC, Iyer M, Namavari M, Bobinski K, Green LA et al. Seeing is believing: non-invasive, quantitative and repetitive imaging of reporter gene expression in living animals, using positron emission tomography. J Neurosci Res 2000; 59: 699-705.
7. Peñuelas I, Yaghoubi SS, Prósper F, Gambhir SS. Clinical ap-plications of reporter gene technology. In: Yaghoubi SS, Gam-bhir SS (eds). Molecular Imaging With Reporter Genes. Cam-bridge University Press, 2010.
8. Serganova I, Blasberg R. Reporter gene imaging: potential im-pact on therapy. Nucl Med Biol 2005; 32: 763-780.
9. Yaghoubi SS, Gambhir SS. Gene therapy and imaging of transgene expression in living subjects. In: Yaghoubi SS, Gambhir SS, eds. Molecular Imaging With Reporter Genes. Cam-bridge University Press. 2010:227-238.
10. Ray P, Bauer E, Iyer M, Barrio JR, Satyamurthy N, Phelps ME et al. Monitoring gene therapy with reporter gene imaging. Semin Nucl Med 2001; 31: 312-320.
11. 18F-FHBG in a patient with glioma. Nat Clin Pract Oncol 2009; 6: 53-58.
12. Penuelas I, Haberkorn U, Yaghoubi S, Gambhir S. Gene therapy imaging in patients for oncological applications. Eur J Nucl Med Mol Imaging 2005; 32: S384-S403.
13. Penuelas I, Mazzolini G, Boan JF, Sangro B, Marti-Climent J, Ruiz M et al. Positron emission tomography imaging of adeno-viral-mediated transgene expression in liver cancer patients. Gastroenterology 2005; 128: 1787-1795.
14. 123I-FIAU imaging of herpes simplex viral gene expression in the treatment of glioma. Nucl Med Commun 2006; 27: 611-617.
15. Jacobs A, Voges J, Reszka R, Lercher M, Grossmann A, Kracht L et al. Positron-emission tomography of vector-mediated gene expression in gene therapy for gliomas. Lancet 2001; 358: 727-729.
16. Barton KN, Stricker H, Brown SL, Elshaikh M, Aref I, Lu M et al. Phase I study of noninvasive imaging of adenovirus-mediated gene expression in the human prostate. Mol Ther 2008; 16: 1761-1769.
17. 18F]FHBG: A reporter probe for imaging herpes simplex virus type-1 thymidine kinase reporter gene expression. J Nucl Med 2001; 42: 1225-1234.
18. Gambhir SS, Bauer E, Black ME, Liang Q, Kokoris MS, Barrio JR 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. PNAS 2000; 97: 2785-2790.
19. Likar Y, Dobrenkov K, Olszewska M, Shenker L, Cai S, Hricak H et al. PET imaging of HSV1-tk mutants with acquired speci-ficity toward pyrimidine- and acycloguanosine-based radio-tracers. Eur J Nucl Med Mol Imaging 2009; 36: 1273-1282.
20. Likar Y, Dobrenkov K, Olszewska M, Vider E, Shenker L, Cai S et al. A new acycloguanosine-specific supermutant of herpes simplex virus type 1 thymidine kinase suitable for PET imaging and suicide gene therapy for potential use in patients treated with pyrimidine-based cytotoxic drugs. J Nucl Med 2008; 49: 713-720.
21. Hsieh C, Chen F, Wang H, Hwang J, Chang C, Lee Y et al. Generation of destabilized herpes simplex virus type 1 thymi-dine kinase as transcription reporter for PET reporter systems in molecular-genetic imaging. J Nucl Med 2008; 49: 142-150.
22. Hsieh C, Liu R, Wang H, Hwang J, Deng W, Chen J et al. In vitro evaluation of herpes simplex virus type 1 thymidine kinase reporter system in dynamic studies of transcriptional gene regulation. Nucl Med Biol 2006 Jul;33(5):653-60.
23. Najjar AM, Nishii R, Maxwell DS, Volgin A, Mukhopadhyay U, Bornmann WG et al. Molecular-genetic PET imaging using an HSV1-tk mutant reporter gene with enhanced specificity to acycloguanosine nucleoside analogs. J Nucl Med 2009; 50: 409-416.
24. Pantuck AJ, Berger F, Zisman A, Nguyen D, Tso CL, Matherly J et al. CL1-SR39: A noninvasive molecular imaging model of prostate cancer suicide gene therapy using positron emission tomography. J Urol 2002; 168: 1193-1198.
25. Pantuck AJ, Matherly J, Zisman A, Nguyen D, Berger F, Gambhir SS et al. Optimizing prostate cancer suicide gene therapy using herpes simplex virus thymidine kinase active site variants. Hum Gene Ther 2002; 13: 777-789.
26. 18F]Fluoropenciclovir: An improved reporter probe for imaging HSV1-tk reporter gene expression in vivo using PET. J Nucl Med 2001; 42: 96-105.
27. 14C]FIAU for imaging of HSV1-tk reporter gene expression: adenoviral infection vs stable transfection. Eur J Nucl Med Mol Imaging 2003; 30: 1547-1560.
28. 18F]fluoro-3-hydroxymethylbutyl)guanine for in vivo measurement of suicide gene expression with PET. J Nucl Med 2001; 42: 1682-1690.
29. Alauddin MA, Shahinian A, Gordon EM, Conti PS. Direct comparison of radiolabeled probes FMAU, FHBG, and FHPG as PET imaging agents for HSV1-tk expression in human breast cancer model. Mol Imaging 2004; 3: 76-84.
30. 18F]FHBG): A new potential imaging agent for viral infection and gene therapy using PET. Nucl Med Biol 1998; 25: 175-180.
31. 18F]FEAU: A novel PET imaging agent for HSV1-tk/sr39tk re-porter gene expression. Mol Imaging Biol 2008; 10: 82-91.
32. Tjuvajev JG, Doubrovin M, Akhurst T, Cai S, Balatoni J, Alauddin MA et al. Comparison of radiolabeled nucleoside probes (FIAU, FHBG, and FHPG) for PET imaging of HSV1-tk gene expression. J Nucl Med 2002; 43: 1072-1083.
33. Johayem A, Raic-Malic S, Lazzati K, Schubiger PA, Scapozza L, Ametamey SM. Synthesis and characterization of a C(6) nucle-oside analogue for the in vivo imaging of the gene expression of Herpes Simplex virus type-1 thymidine kinase. Chemistry and Biodiversity 2006; 3: 274-282.
34. 18F-FHBG: A PET reporter probe for imaging Herpes Simplex virus type 1 thymidine ki-nase (HSV1-tk) or mutant HSV1-sr39tk's expression. J Nucl Med 2006; 47: 706-715.
35. 18F]FHBG. Nat Protoc 2007; 1: 3069-3075.
36. Yaghoubi SS, Barrio JR, Namavari M, Satyamurthy N, Phelps ME, Herschman HR et al. Imaging progress of herpes simplex virus type 1 thymidine kinase suicide gene therapy in living subjects with positron emission tomography. Cancer Gene Ther 2005; 12: 329-339.
37. Berger C, Flowers ME, Warren EH, Riddell SR. Analysis of transgene-specific immune responses that limit the in vivo per-sistence of adoptively transferred HSV-TK-modified donor T cells after allogeneic hematopoietic cell transplantation. Blood 2006; 107: 2294-2302.
38. Traversari C, Marktel S, Magnani Z, Mangia P, Russo V, Ciceri F et al. The potential immunogenicity of the TK suicide gene does not prevent full clinical benefit associated with the use of TK-transduced donor lymphocytes in HSCT for hematologic malignancies. Blood 2007; 109: 4708-4715.
39. 11C-labeled bicyclic nucleoside analogues as potential probes for imaging Varicella-Zoster virus thymidine kinase gene ex-pression using positron emission tomography. J Med Chem 2007; 50: 1041-1049.
40. 11C-labeled Beta-galactosyl triazoles as potential PET tracers for in vivo LacZ reporter gene imaging. Bioorg Med Chem Lett 2009; 17: 5117-5125.
41. Ghim CM, Lee SK, Takayama S, Mitchell RJ. The art of reporter proteins in science: past, present and future applications. BMB Reports 2010; 43: 451-460.
42. Gilad AA, Winnard Jr PT, Van Zijl PCM, Bulte JWM. Develop-ing MR reporter genes: promises and pitfalls. NMR Biomed 2007; 20: 275-290.
43. Louie AY, Huber MM, Ahrens ET, Rothbacher U, Moats R, Jacobs RE et al. In vivo visualization of gene expression using magnetic resonance imaging. Nat Biotechnol 2000; 18: 321-325.
44. Serganova I, Ponomarev V, Blasberg R. Human reporter genes: potential use in clinical studies. Nucl Med Biol 2007; 34: 791-807.
45. MacLaren DC, Gambhir SS, Satyamurthy N, Barrio JR, Sharf-stein S, Toyokuni T et al. Repetitive, non-invasive imaging of the dopamine D2 receptor as a reporter gene in living animals. Gene Ther 1999; 6: 785-791.
46. Hwang DW, Kang JH, Chang YS, Jeong JM, Chung J, Lee MC et al. Development of a dual membrane protein reporter system using sodium iodide symporter and mutant dopamine D2 receptor transgenes. J Nucl Med 2007; 48: 588-595.
47. Liang Q, Satyamurthy N, Barrio JR, Toyokuni T, Phelps ME, Gambhir SS 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: 1490-1498.
48. Satyamurthy N, Barrio J, Bida G, Huang S, Mazziotta J, Phelps M. 3-(2'-[18F]fluoroethyl)Spiperone, a potent dopamine antag-onist: synthesis, structural analysis and in vivo utilization in human. Appl Radiat Isotopes 1990; 41: 113-129.
49. Furukawa T, Lohith TG, Takamatsu S, Mori T, Tanaka T, Fujibayashi Y. Potential of the FES-hERL PET reporter gene system - Basic evaluation for gene therapy monitoring. Nucl Med Biol 2006; 33: 145-151.
50. Lohith TG, Furukawa T, Mori T, Kobayashi M, Fujibayashi Y. Basic evaluation of FES-hERL PET tracer-reporter gene system for in vivo monitoring of adenoviral-mediated gene therapy. Mol Imaging Biol 2008; 10: 245-252.
51. Chaudhuri TR, Rogers BE, Buchsbaum DJ, Mountz JM, Zinn KR. A noninvasive reporter system to image adenoviral-mediated gene transfer to ovarian cancer xenografts. Gynecol Oncol 2001; 83: 432-438.
52. 188Re. J Nucl Med 2000; 41: 887-895.
53. Zinn KR, Chaudhuri TR, Buchsbaum DJ, Mountz JM, Rogers BE. Detection and measurement of in vitro gene transfer by gamma camera imaging. Gene Ther 2001; 8: 291-299.
54. Rogers BE, Chaudhuri TR, Reynolds PN, Manna DD, Zinn KR. Non-invasive gamma camera imaging of gene transfer using an adenoviral vector encoding an epitope-tagged receptor as a reporter. Gene Ther 2003; 10: 105-114.
55. Kenanova V, Barat B, Olafsen T, Chatziioannou A, Herschman HR, Braun J et al. Recombinant carcinoembryonic antigen as a reporter gene for molecular imaging. Eur J Nucl Med Mol Imaging 2009; 36: 104-114.
56. Wei LH, Olafsen T, Radu CG, Hildebrandt IJ, McCoy MR, Phelps ME et al. Engineered antibody fragments with infinite affinity as reporter genes for PET imaging. J Nucl Med 2008; 49: 1828-1835.
57. Kang HJ, Chung J, Lee YJ, Kim K, Jeong JM, Lee DS et al. Eval-uation of transcriptional activity of the oestrogen receptor with sodium iodide symporter as an imaging reporter gene. Nucl Med Commun 2006; 27: 773-777.
58. Cho J-Y. A transporter gene (sodium iodide symporter) for dual purposes in gene therapy: Imaging and therapy. Curr Gene Ther 2002; 2: 393-402.
59. Cho J-Y, Shen DHY, Yang W, Williams B, Buckwalter TLF, La Perle KMD et al. In vivo imaging and radioiodine therapy fol-lowing sodium iodide symporter gene transfer in animal model of intracerebral gliomas. Gene Ther 2002; 9: 1139-1145.
60. Chung J. Sodium iodide symporter: Its role in nuclear medicine. J Nucl Med 2002; 43: 1188-1200.
61. Goel A, Carlson SK, Classic KL, Greiner S, Naik S, Power AT 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: 2342-2350.
62. 124I-MIBG. J Nucl Med 2007; 48: 827-836.
63. Ponomarev V, Doubrovin M, Shavrin A, Serganova I, Beresten T, Ageyeva L et al. A human-derived reporter gene for nonin-vasive imaging in humans: mitochondrial thymidine kinase type 2. J Nucl Med 2007; 48: 819-826.
64. Campbell DO, Yaghoubi SS, Su Y, Lee JT, Auerbach MS, Herschman H et al. Structure-guided engineering of human thymidine kinase 2 as a positron emission tomography reporter gene for enhanced phosphorylation of a non-natural thymidine analog reporter probe. J Biol Chem In Press.
65. Likar Y, Zurita J, Dobrenkov K, Shenker L, Cai S, Neschadim A et al. A new pyrimidine-specific reporter gene: a mutated hu-man deoxycytidine kinase suitable for PET during treatment with acycloguanosine-based cytotoxic drugs. J Nucl Med 2010; 51: 1395-1403.
66. Chuang KH, Wang HE, Cheng TC, Tzou SC, Tseng WL, Hung WC et al. Development of a universal anti-polyethylene glycol reporter gene for noninvasive imaging of PEGylated probes. J Nucl Med 2010; 51: 933-941.
67. Lendvai G, Estrada S, Bergstrom M. Radiolabelled oligonucleotides for imaging of gene expression with PET. Curr Med Chem 2009; 16: 4445-4461.
68. Deng W, Yang WK, Lai W, Liu R, Hwang J, Yang D et al. Non-invasive in vivo imaging with radiolabelled FIAU for monitoring cancer gene therapy using herpes simplex virus type 1 thymidine kinase and ganciclovir. Eur J Nucl Med Mol Imaging 2004; 31: 99-109.
69. Haberkorn U, Altmann A, Morr I, Germann C, Oberdorfer F, Van Kaick G. Multitracer studies during gene therapy of hepatoma cells with Herpes Simplex Virus Thymidine Kinase and Ganciclovir. J Nucl Med 1997; 38: 1048-1054.
70. Kuruppu D, Brownell AL, Zhu A, Yu M, Wang X, Kulu Y et al. Positron emission tomography of herpes simplex virus 1 oncolysis. Cancer Res 2007; 67: 3295-3300.
71. Lanuti M, Gao G, Force SD, Chang MY, El Kouri C, Amin KM et al. Evaluation of an E1E4-Deleted adenovirus expressing the herpes simplex thymidine kinase suicide gene in cancer gene therapy. Hum Gene Ther 1999; 10: 463-475.
72. Yaghoubi S. Imaging reporter transgene expression in living subjects using positron emission tomography. Los Angeles: University of California, Los Angeles. 2002.
73. Yaghoubi SS, Wu L, Liang Q, Toyokuni T, Barrio JR, Namavari M et al. Direct correlation between positron emission tomographic images of two reporter genes delivered by two distinct adenoviral vectors. Gene Ther 2001; 8: 1072-1080.
74. Yaghoubi SS, Gambhir SS. Monitoring p53 therapeutic transgene expression in mice by imaging the expression of a linked HSV1-sr39tk PET reporter transgene. J Nucl Med 2003; 44: 30P [Abstract#95].
75. Yu Y, Annala AJ, Barrio JR, Toyokuni T, Satyamurthy N, Namavari M et al. Quantification of target gene expression by imaging reporter gene expression in living animals. Nat Med 2000; 6: 933-937.
76. Anton M, Wittermann C, Haubner R, Simoes M, Reder S, Essien B et al. Coexpression of herpesviral thymidine kinase reporter gene and VEGF gene for noninvasive monitoring of therapeutic gene transfer: an in vitro evaluation. J Nucl Med 2004; 45: 1743-1746.
77. Chen IY, Gheysens O, Ray S, Wang Q, Padmanabhan P, Paulmurugan R et al. Indirect imaging of cardiac-specific transgene expression using a bidirectional two-step transcriptional amplification strategy. Gene Ther 2010.
78. Chen IY, Wu JC, Min J, Sundaresan G, Lewis X, Liang Q et al. Micro-positron emission tomography imaging of cardiac gene expression in rats using bicistronic adenoviral vector-mediated gene delivery. Circulation 2004; 109: 1415-1420.
79. Wang Y, Iyer M, Annala AJ, Chappell S, Mauro V, Gambhir SS. Noninvasive monitoring of target gene expression by imaging reporter gene expression in living animals using improved bicistronic vectors. J Nucl Med 2005; 46: 667-674.
80. Sun X, Annala AJ, Yaghoubi SS, Barrio JR, Nguyen KN, Toyokuni T et al. Quantitative imaging of gene induction in living animals. Gene Ther 2001; 8: 1572-1579.
81. Wang Y, Iyer M, Annala A, Wu L, Carey M, Gambhir SS. Non-invasive indirect imaging of vascular endothelial growth factor gene expression using bioluminescence imaging in living transgenic mice. Physiol Genomics 2006; 24: 173-180.
82. Ray P, Wu AM, Gambhir SS. Optical bioluminescence and positron emission tomography imaging of a novel fusion reporter gene in tumor xenografts of living mice. Cancer Res 2003; 63: 1160-1165.
83. Ray P, De A, Min J, Tsien RY, Gambhir SS. Imaging tri-fusion multimodality reporter gene expression in living subjects. Cancer Res 2004; 64: 1323-1330.
84. Ray P, Gambhir SS. Multimodality imaging of reporter genes. In: Yaghoubi SS, Gambhir SS, eds. Molecular Imaging With Reporter Genes. Cambridge University Press. 2010: 113-126.
85. Ray P, Tsien R, Gambhir SS. Construction and validation of improved triple fusion reporter gene vectors for molecular imaging of living subjects. Cancer Res 2007; 67: 3085-3093.
86. Kesarwala AH, Prior JL, Sun J, Harpstrite SE, Sharma V, Piwnica-Worms D. Second-generation triple reporter for bio-luminescence, micro-positron emission tomography, and fluorescence imaging. Mol Imaging 2006; 5: 465-474.
87. Jacobs A, Dubrovin M, Hewett J, Sena-Esteves M, Tan CW, Slack M et al. Functional coexpression of HSV-1 thymidine kinase and green fluorescent protein: implications for noninvasive imaging of transgene expression. Neoplasia 1999; 1: 154-161.
88. Ponomarev V, Doubrovin M, Serganova I, Vider J, Shavrin A, Beresten T et al. A novel triple-modality reporter gene for whole-body fluorescent, bioluminescent, and nuclear noninvasive imaging. Eur J Nucl Med Mol Imaging 2004; 31: 740-751.
89. Wu JC, Chen IY, Wang Y, Tseng JR, Chhabra A, Salek M et al. Molecular Imaging of the kinetics of vascular endothelial growth factor gene expression in ischemic myocardium. Circulation 2004; 110: 685-691.
90. Morstyn G, Sheridan W (eds). Cell therapy: stem cell transplantation, gene therapy, and cellular immunotherapy. Cambridge University Press: Cambridge, 1996.
91. Gupta R, Losordo DW. Challenges in the translation of cardio-vascular cell therapy. J Nucl Med 2010; 51: 122S-127S.
92. Salem ML, Cole DJ. Dendritic cell recovery post-lymphodepletion: a potential mechanism for anti-cancer adoptive T cell therapy and vaccination. Cancer Immunol Immunother 2010; 59: 341-353.
93. June CH. Adoptive T cell therapy for cancer in the clinic. The Journal of Clinical Investigation 2007; 117: 1466-1476.
94. Olasz EB, Lang L, Seidel J, Green MV, Eckelman WC, Katz SI. Fluorine-18 labeled mouse bone marrow-derived dendritic cells can be detected in vivo by high resolution projection imaging. J Immunol Methods 2002; 260: 137-148.
95. Ahrens ET, Flores R, Xu H, Morel PA. In vivo imaging platform for tracking immunotherapeutic cells. Nat Biotechnol 2005; 23: 983-987.
96. Kircher MF, Allport JR, Graves EE, Love V, Josephson L, Lichtman AH et al. In vivo high resolution three-dimensional imaging of antigen-specific cytotoxic T-lymphocyte trafficking to tumors. Cancer Res 2003; 63: 6838-6846.
97. Morse MA, Coleman RE, Akabani G, Niehaus N, Coleman D, Lyerly HK. Migration of human dendritic cells after injection in patients with metastatic malignancies. Cancer Res 1999; 59: 56-58.
98. Adonai N, Nguyen KN, Walsh J, Iyer M, Toyokuni T, Phelps ME et al. Ex vivo cell labeling with 64Cu-pyruvaldehyde-bis(N4-methylthiosemicarbazone) for imaging cell trafficking in mice with positron-emission tomography. PNAS 2002; 99: 3030-3035.
99. Verdijk P, Scheenen TWJ, Lesterhuis WJ, Gambarota G, Veltien AA, Walczak P et al. Sensitivity of magnetic resonance imaging of dendritic cells for in vivo tracking of cellular cancer vaccines. Int J Cancer 2006; 120: 978-984.
100. Vuu K, Xie J, McDonald MA, Bernardo M, Hunter F, Zhang Y et al. Gadolinium-Rhodamine nanoparticles for cell labeling and tracking via magnetic resonance and optical imaging. Bioconjug Chem 2005; 16: 995-999.
101. Chung J, Kang JH, Kang KW. Reporter gene imaging with PET/SPECT. In: Gambhir SS, Yaghoubi SS, eds. Molecular Im-aging With Reporter Genes. Cambridge University Press. 2010: 70-87.
102. Yaghoubi SS, Creusot RJ, Ray P, Fathman CG, Gambhir SS. Multimodality imaging of T-cell hybridoma trafficking in collagen-induced arthritic mice: image-based estimation of the number of cells accumulating in mouse paws. Journal of Bio-medical Optics 2007; 12: 064025_064021-064011.
103. Waerzeggers Y, Klein M, Miletic H, Himmelreich U, Li H, Monfared P et al. Multimodal imaging of neural progenitor cell fate in rodents. Mol Imaging Biol 2008; 7: 77-91.
104. Cao F, Lin S, Xie X, Ray P, Patel M, Zhang X et al. In vivo visu-alization of embryonic stem cell survival, proliferation, and migration after cardiac delivery. Circulation 2006; 113: 1005-1014.
105. Wu JC, Chen IY, Sundaresan G, Min J, De A, Qiao J et al. Molecular imaging of cardiac cell transplantation in living animals using optical bioluminescence and positron emission tomography. Circulation 2003; 108: 1302-1305.
106. -/- mice by positron-emission tomography. J Immunol 2006; 176: 4459-4467.
107. Su H, Forbes A, Gambhir SS, Braun J. Quantitation of cell number by a positron emission tomography reporter gene strategy. Mol Imaging Biol 2004; 6: 139-148.
108. Kim S, Doudet DJ, Studenov AR, Nian C, Ruth TJ, Gambhir SS et al. Quantitative micro positron emission tomography (PET) imaging for the in vivo determination of pancreatic islet graft survival. Nat Med 2006; 12: 1423-1428.
109. Kim SJ, Doudet D, Ruth TJ, Gambhir SS, McIntosh CHS. Quantitative in vivo imaging of transplanted islets using micro positron emission tomography scanning. Nat Med 2006; 12: 1423-1428.
110. Kim YJ, Dubey P, Ray P, Gambhir SS, Witte ON. Multimodality imaging of lymphocytic migration using lentiviral-based transduction of a tri-fusion reporter gene. Mol Imaging Biol 2004; 6: 331-340.
111. Lu Y, Dang H, Middleton B, Zhang Z, Washburn L, Stout DB et al. Noninvasive imaging of islet grafts using positron-emission tomography. PNAS 2006; 103: 11294-11299.
112. Dubey P, Su H, Adonai N, Du S, Rosato A, Braun J et al. Quantitative imaging of T cell antitumor response by positron-emission tomography. PNAS 2003; 100: 1232-1237.
113. Shu CJ, Guo S, Kim YJ, Shelly SM, Nijagal A, Ray P et al. Visu-alization of a primary anti-tumor immune response by positron emission tomography. PNAS 2005; 102: 17412-17417.
114. Shu CJ, Radu CG, Shelly SM, Vo DD, Prins R, Ribas A et al. Quantitative PET reporter gene imaging of CD8+ T cells specific for a melanoma-expressed self-antigen. Int Immunol 2009; 21: 155-165.
115. Cao F, Drukker M, Lin S, Sheikh A, Xie X, Li Z et al. Molecular imaging of embryonic stem cell misbehavior and suicide gene ablation. Cloning and Stem Cells 2007; 9: 107-117.
116. Dobrenkov K, Olszewska M, Likar Y, Shenker L, Gunset G, Cai S et al. Monitoring the efficacy of adoptively transferred prostate cancer-targeted human T lymphocytes with PET and bio-luminescence imaging. J Nucl Med 2008; 49: 1162-1170.
117. Koehne G, Doubrovin M, Doubrovina E, Zanzonico P, Gallardo HF, Ivanova A et al. Serial in vivo imaging of the targeted migration of human HSV-TK-transduced antigen-specific lym-phocytes. Nat Biotechnol 2003; 21: 405-413.
118. Lo W, Hsu C, Wu ATH, Yang L, Chen W, Chiu W et al. A novel cell-based therapy for contusion spinal cord injury using GDNF-delivering NIH3T3 cells with dual reporter genes monitored by molecular imaging. J Nucl Med 2008; 49: 1512-1519.
119. Doubrovin MM, Doubrovina E, Zanzonico P, Sadelain M, Larson SM, O'Reilly RJ. In vivo imaging and quantitation of adoptively transferred human antigen-specific T cells transduced to express a human norepinephrine transporter gene. Cancer Res 2007; 67: 11959-11969.
120. Dotti G, Tian M, Savoldo B, Najjar A, Cooper LJN, Jackson J et al. 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 2009; 8: 230-237.
121. Qiao H, Surti S, Choi SR, Raju K, Zhang H, Ponde DE et al. Death and Proliferation Time Course of Stem Cells Trans-planted in the Myocardium. Mol Imaging Biol 2009; 11: 408-414.
122. Terrovitis J, Kwok KF, Lautamaki R, Engles JM, Barth AS, Kizana E et al. Ectopic expression of the sodium-iodide symporter enables imaging of transplanted cardiac stem cells in vivo by single-photon emission computed tomography or positron emission tomography. J Am Coll Cardiol 2008; 52: 1652-1660.
123. Willmann JK, Paulmurugan R, Rodriguez-Porcel M, Stein W, Brinton TJ, Connolly AJ et al. Imaging Gene Expression in Human Mesenchymal Stem Cells: From Small to Large Animals. Radiology 2009; 252: 117-127.