Theranostic potential of oncolytic vaccinia virus

Theranostics

Volumn 2, Issue 4, 2012, Pages 363-373

  Rojas, Juan J ^a   Thorne, Steve H ^a  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

Oncolytic vaccinia virus; Theranostics

Indexed keywords

GLV 1H68; IODINE 123; JX 594; LONTUCIREV; ONCOLYTIC VACCINIA VIRUS; ONCOLYTIC VIRUS; PENTETREOTIDE IN 111; PERRHENATE RE 188; PERRHENIC ACID RE 186; PERTECHNETIC ACID TC 99M; RADIOPHARMACEUTICAL AGENT; SODIUM IODIDE I 123; SODIUM IODIDE I 125; SODIUM IODIDE I 131; THYMIDINE KINASE; UNCLASSIFIED DRUG; VIROTHERAPY AGENT;

BIOLUMINESCENCE; BIOLUMINESCENCE IMAGING; FLUORESCENCE IMAGING; GENE DELETION; GENE EXPRESSION; HUMAN; IMAGING SYSTEM; IMMUNE RESPONSE; LIVER CELL CARCINOMA; MOLECULAR IMAGING; NONHUMAN; ONCOLYTIC VIROTHERAPY; PERSONALIZED MEDICINE; PHENOTYPE; POSITRON EMISSION TOMOGRAPHY; REPORTER GENE; REVIEW; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; TUMOR CELL DESTRUCTION; VIRUS REPLICATION; VIRUS STRAIN;

EID: 84864537130     PISSN: None     EISSN: 18387640     Source Type: Journal    
DOI: 10.7150/thno.3724     Document Type: Review

References (116)

1. Guo ZS, Thorne SH, Bartlett DL. Oncolytic virotherapy: Molecular targets in tumor-selective replication and carrier cell-mediated delivery of oncolytic viruses. Biochim Biophys Acta. 2008; doi:S0304-419X(08)00004-8 [pii] 10.1016/j.bbcan.2008.02.001.
2. Thorne SH, Hermiston T, Kirn D. Oncolytic virotherapy: approaches to tumor targeting and enhancing antitumor effects. Semin Oncol. 2005; 32: 537-48.
3. Kirn D, Martuza RL, Zwiebel J. Replication-selective virotherapy for cancer: Biological principles, risk management and future directions. Nat Med. 2001; 7: 781-7.
4. Harrington KJ, Vile RG, Melcher A, Chester J, Pandha HS. Clinical trials with oncolytic reovirus: moving beyond phase I into combinations with standard therapeutics. Cytokine Growth Factor Rev. 2010; 21: 91-8. doi:10.1016/j.cytogfr.2010.02.006.
5. Van Den Wollenberg DJ, Van Den Hengel SK, Dautzenberg IJ, Kranenburg O, Hoeben RC. Modification of mammalian reoviruses for use as oncolytic agents. Expert opinion on biological therapy. 2009; 9: 1509-20. doi:10.1517/14712590903307370.
6. Schirrmacher V, Fournier P. Newcastle disease virus: a promising vector for viral therapy, immune therapy, and gene therapy of cancer. Methods in molecular biology. 2009; 542: 565-605.
7. Barber GN. VSV-tumor selective replication and protein translation. Oncogene. 2005; 24: 7710-9. doi:10.1038/sj.onc.1209042.
8. Kirn DH, Thorne SH. Targeted and armed oncolytic poxviruses: a novel multi-mechanistic therapeutic class for cancer. Nat Rev Cancer. 2009; 9: 64-71. doi:nrc2545 [pii]10.1038/nrc2545.
9. Msaouel P, Iankov ID, Dispenzieri A, Galanis E. Attenuated Oncolytic Measles Virus Strains as Cancer Therapeutics. Curr Pharm Biotechnol. 2011.
10. Toth K, Wold WS. Increasing the efficacy of oncolytic adenovirus vectors. Viruses. 2010; 2: 1844-66. doi:10.3390/v2091844.
11. Kaur B, Chiocca EA, Cripe TP. Oncolytic HSV-1 Virotherapy: Clinical Experience and Opportunities for Progress. Curr Pharm Biotechnol. 2011.
12. Goetz C, Gromeier M. Preparing an oncolytic poliovirus recombinant for clinical application against glioblastoma multiforme. Cytokine Growth Factor Rev. 2010; 21: 197-203. doi:10.1016/j.cytogfr.2010.02.005.
13. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000; 100: 57-70.
14. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144: 646-74. doi:10.1016/j.cell.2011.02.013.
15. Kirn DH, Wang Y, Le Boeuf F, Bell J, Thorne SH. Targeting of interferon-beta to produce a specific, multi-mechanistic oncolytic vaccinia virus. PLoS Med. 2007; 4: e353. doi:07-PLME-RA-0571 [pii]10.1371/journal.pmed.0040353.
16. Guo ZS, Naik A, O'Malley ME, Popovic P, Demarco R, Hu Y, et al. The enhanced tumor selectivity of an oncolytic vaccinia lacking the host range and antiapoptosis genes SPI-1 and SPI-2. Cancer Research. 2005; 65: 9991-8. doi:10.1158/0008-5472.CAN-05-1630.
17. McCart JA, Ward JM, Lee J, Hu Y, Alexander HR, Libutti SK, et al. Systemic cancer therapy with a tumor-selective vaccinia virus mutant lacking thymidine kinase and vaccinia growth factor genes. Cancer Res. 2001; 61: 8751-7.
18. DeWeese TL, van der Poel H, Li S, Mikhak B, Drew R, Goemann M, et al. A phase I trial of CV706, a replication-competent, PSA selective oncolytic adenovirus, for the treatment of locally recurrent prostate cancer following radiation therapy. Cancer Res. 2001; 61: 7464-72.
19. Li Y, Yu DC, Chen Y, Amin P, Zhang H, Nguyen N, et al. A hepatocellular carcinoma-specific adenovirus variant, CV890, eliminates distant human liver tumors in combination with doxorubicin. Cancer Res. 2001; 61: 6428-36.
20. Yu DC, Chen Y, Dilley J, Li Y, Embry M, Zhang H, et al. Antitumor synergy of CV787, a prostate cancer-specific adenovirus, and paclitaxel and docetaxel. Cancer Res. 2001; 61: 517-25.
21. Rojas JJ, Guedan S, Searle PF, Martinez-Quintanilla J, Gil-Hoyos R, Alcayaga-Miranda F, et al. Minimal RB-responsive E1A promoter modification to attain potency, selectivity, and transgene-arming capacity in oncolytic adenoviruses. Mol Ther. 2010; 18: 1960-71. doi:mt2010173 [pii]10.1038/mt.2010.173.
22. Roelvink PW, Mi Lee G, Einfeld DA, Kovesdi I, Wickham TJ. Identification of a conserved receptor-binding site on the fiber proteins of CAR-recognizing adenoviridae. Science. 1999; 286: 1568-71.
23. Douglas JT, Rogers BE, Rosenfeld ME, Michael SI, Feng M, Curiel DT. Targeted gene delivery by tropism-modified adenoviral vectors. Nat Biotechnol. 1996; 14: 1574-8.
24. Peng KW, Donovan KA, Schneider U, Cattaneo R, Lust JA, Russell SJ. Oncolytic measles viruses displaying a single-chain antibody against CD38, a myeloma cell marker. Blood. 2003; 101: 2557-62.
25. Dock G. Rabies virus vaccination in a patient with cervical carcinoma. American Journal of Medical Science. 1904; 127: 563.
26. Southam CM, Moore AE. Clinical studies of viruses as antineoplastic agents with particular reference to Egypt 101 virus. Cancer. 1952; 5: 1025-34.
27. Martuza RL, Malick A, Markert JM, Ruffner KL, Coen DM. Experimental therapy of human glioma by means of a genetically engineered virus mutant. Science. 1991; 252: 854-6.
28. Bischoff JR, Kirn DH, Williams A, Heise C, Horn S, Muna M, et al. An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science. 1996; 274: 373-6.
29. Heise C, Sampson-Johannes A, Williams A, McCormick F, Von Hoff DD, Kirn DH. ONYX-015, an E1B gene-attenuated adenovirus, causes tumor-specific cytolysis and antitumoral efficacy that can be augmented by standard chemotherapeutic agents. Nat Med. 1997; 3: 639-45.
30. Nemunaitis J, Khuri F, Ganly I, Arseneau J, Posner M, Vokes E, et al. Phase II trial of intratumoral administration of ONYX-015, a replication-selective adenovirus, in patients with refractory head and neck cancer. J Clin Oncol. 2001; 19: 289-98.
31. Galanis E, Okuno SH, Nascimento AG, Lewis BD, Lee RA, Oliveira AM, et al. Phase I-II trial of ONYX-015 in combination with MAP chemotherapy in patients with advanced sarcomas. Gene Ther. 2005; 12: 437-45.
32. Breitbach CJ, Burke J, Jonker D, Stephenson J, Haas AR, Chow LQ, et al. Intravenous delivery of a multi-mechanistic cancer-targeted oncolytic poxvirus in humans. Nature. 2011; 477: 99-102. doi:10.1038/nature10358.
33. Park BH, Hwang T, Liu TC, Sze DY, Kim JS, Kwon HC, et al. Use of a targeted oncolytic poxvirus, JX-594, in patients with refractory primary or metastatic liver cancer: a phase I trial. Lancet Oncol. 2008; 9: 533-42. doi:S1470-2045(08)70107-4 [pii]10.1016/S1470-2045(08)70107-4.
34. Schmidt C. Amgen spikes interest in live virus vaccines for hard-to-treat cancers. Nature biotechnology. 2011; 29: 295-6. doi:10.1038/nbt0411-295.
35. Senzer NN, Kaufman HL, Amatruda T, Nemunaitis M, Reid T, Daniels G, et al. Phase II clinical trial of a granulocyte-macrophage colony-stimulating factor-encoding, second-generation oncolytic herpesvirus in patients with unresectable metastatic melanoma. J Clin Oncol. 2009; 27: 5763-71. doi:JCO.2009.24.3675 [pii]10.1200/JCO.2009.24.3675.
36. Breitbach CJ, Thorne SH, Bell JC, Kirn DH. Targeted and Armed Oncolytic Poxviruses for Cancer: The Lead Example of JX-594. Curr Pharm Biotechnol. 2011.
37. Thorne SH. Immunotherapeutic potential of oncolytic vaccinia virus. Immunol Res. 2011; 50: 286-93. doi:10.1007/s12026-011-8211-4.
38. Breitbach CJ, Paterson JM, Lemay CG, Falls TJ, McGuire A, Parato KA, et al. Targeted inflammation during oncolytic virus therapy severely compromises tumor blood flow. Mol Ther. 2007; 15: 1686-93. doi:6300215 [pii]10.1038/sj.mt.6300215.
39. Liu TC, Hwang T, Park BH, Bell J, Kirn DH. The targeted oncolytic poxvirus JX-594 demonstrates antitumoral, antivascular, and anti-HBV activities in patients with hepatocellular carcinoma. Mol Ther. 2008; 16: 1637-42. doi:mt2008143 [pii]10.1038/mt.2008.143.
40. Hermiston T. Fighting fire with fire: attacking the complexity of human tumors with armed therapeutic viruses. Curr Opin Mol Ther. 2002; 4: 334-42.
41. Hermiston TW, Kuhn I. Armed therapeutic viruses: strategies and challenges to arming oncolytic viruses with therapeutic genes. Cancer Gene Ther. 2002; 9: 1022-35.
42. Mastrangelo MJ, Maguire HC, Jr., Eisenlohr LC, Laughlin CE, Monken CE, McCue PA, et al. Intratumoral recombinant GM-CSF-encoding virus as gene therapy in patients with cutaneous melanoma. Cancer Gene Ther. 1999; 6: 409-22.
43. Smith GL, Moss B. Infectious poxvirus vectors have capacity for at least 25 000 base pairs of foreign DNA. Gene. 1983; 25: 21-8.
44. Moss B. Vaccinia virus: a tool for research and vaccine development. Science. 1991; 252: 1662-7.
45. Moss B. Genetically engineered poxviruses for recombinant gene expression, vaccination, and safety. Proc Natl Acad Sci U S A. 1996; 93: 11341-8.
46. Fenner F, Henderson DA, Arita I, Jezek Z, Ladnyi ID. Smallpox and its eradication. Geneva: World Health Organization; 1988.
47. Cono J, Casey CG, Bell DM. Smallpox vaccination and adverse reactions. Guidance for clinicians. MMWR Recomm Rep. 2003; 52: 1-28.
48. Wittek R. Vaccinia immune globulin: current policies, preparedness, and product safety and efficacy. Int J Infect Dis. 2006; 10: 193-201. doi:S1201-9712(06)00040-3 [pii]10.1016/j.ijid.2005.12.001.
49. Buller RM, Palumbo GJ. Poxvirus pathogenesis. Microbiol Rev. 1991; 55: 80-122.
50. Thorne SH, Hwang TH, O'Gorman WE, Bartlett DL, Sei S, Kanji F, et al. Rational strain selection and engineering creates a broad-spectrum, systemically effective oncolytic poxvirus, JX-963. J Clin Invest. 2007; 117: 3350-8. doi:10.1172/JCI32727.
51. Davison AJ, Moss B. Structure of vaccinia virus late promoters. J Mol Biol. 1989; 210: 771-84.
52. Davison AJ, Moss B. Structure of vaccinia virus early promoters. J Mol Biol. 1989; 210: 749-69.
53. Puhlmann M, Brown CK, Gnant M, Huang J, Libutti SK, Alexander HR, et al. Vaccinia as a vector for tumor-directed gene therapy: biodistribution of a thymidine kinase-deleted mutant. Cancer Gene Ther. 2000; 7: 66-73.
54. Hengstschlager M, Knofler M, Mullner EW, Ogris E, Wintersberger E, Wawra E. Different regulation of thymidine kinase during the cell cycle of normal versus DNA tumor virus-transformed cells. J Biol Chem. 1994; 269: 13836-42.
55. Buller RM, Chakrabarti S, Moss B, Fredrickson T. Cell proliferative response to vaccinia virus is mediated by VGF. Virology. 1988; 164: 182-92.
56. Kim JH, Oh JY, Park BH, Lee DE, Kim JS, Park HE, et al. Systemic Armed Oncolytic and Immunologic Therapy for Cancer with JX-594, a Targeted Poxvirus Expressing GM-CSF. Mol Ther. 2006; 14: 361-70.
57. Yu YA, Timiryasova T, Zhang Q, Beltz R, Szalay AA. Optical imaging: bacteria, viruses, and mammalian cells encoding light-emitting proteins reveal the locations of primary tumors and metastases in animals. Anal Bioanal Chem. 2003; 377: 964-72.
58. Zhang Q, Yu YA, Wang E, Chen N, Danner RL, Munson PJ, et al. Eradication of solid human breast tumors in nude mice with an intravenously injected light-emitting oncolytic vaccinia virus. Cancer Res. 2007; 67: 10038-46. doi:67/20/10038 [pii]10.1158/0008-5472.CAN-07-0146.
59. Kirn DH, Wang Y, Liang W, Contag CH, Thorne SH. Enhancing poxvirus oncolytic effects through increased spread and immune evasion. Cancer Res. 2008; 68: 2071-5. doi:68/7/2071 [pii]10.1158/0008-5472.CAN-07-6515.
60. Guo ZS, Naik A, O'Malley ME, Popovic P, Demarco R, Hu Y, et al. The enhanced tumor selectivity of an oncolytic vaccinia lacking the host range and antiapoptosis genes SPI-1 and SPI-2. Cancer Res. 2005; 65: 9991-8.
61. Chen NG, Szalay AA. Oncolytic Vaccinia Virus: A theranostic agent for cancer. Future Virol. 2010; 5: 763-84.
62. Thorne SH, Contag CH. Combining immune cell and viral therapy for the treatment of cancer. Cell Mol Life Sci. 2007; 64: 1449-51. doi:10.1007/s00018-007-6550-z.
63. Contag CH, Sikorski R, Negrin RS, Schmidt T, Fan AC, Bachireddy P, et al. Definition of an enhanced immune cell therapy in mice that can target stem-like lymphoma cells. Cancer Research. 2010; 70: 9837-45. doi:10.1158/0008-5472.CAN-10-2650.
64. Thorne SH, Liang W, Sampath P, Schmidt T, Sikorski R, Beilhack A, et al. Targeting localized immune suppression within the tumor through repeat cycles of immune cell-oncolytic virus combination therapy. Molecular therapy: the journal of the American Society of Gene Therapy. 2010; 18: 1698-705. doi:10.1038/mt.2010.140.
65. Baril P, Martin-Duque P, Vassaux G. Visualization of gene expression in the live subject using the Na/I symporter as a reporter gene: applications in biotherapy. Br J Pharmacol. 2010; 159: 761-71. doi:BPH412 [pii]10.1111/j.1476-5381.2009.00412.x.
66. Negrin RS, Contag CH. In vivo imaging using bioluminescence: a tool for probing graft-versus-host disease. Nat Rev Immunol. 2006; 6: 484-90. doi:nri1879 [pii]10.1038/nri1879.
67. Zhao H, Doyle TC, Coquoz O, Kalish F, Rice BW, Contag CH. Emission spectra of bioluminescent reporters and interaction with mammalian tissue determine the sensitivity of detection in vivo. J Biomed Opt. 2005; 10: 41210.
68. Contag CH, Contag PR, Mullins JI, Spilman SD, Stevenson DK, Benaron DA. Photonic detection of bacterial pathogens in living hosts. Mol Microbiol. 1995; 18: 593-603.
69. Contag CH, Spilman SD, Contag PR, Oshiro M, Eames B, Dennery P, et al. Visualizing gene expression in living mammals using a bioluminescent reporter. Photochem Photobiol. 1997; 66: 523-31.
70. 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.
71. Cao YA, Wagers AJ, Beilhack A, Dusich J, Bachmann MH, Negrin RS, et al. Shifting foci of hematopoiesis during reconstitution from single stem cells. Proc Natl Acad Sci U S A. 2004; 101: 221-6.
72. Weissleder R. Scaling down imaging: molecular mapping of cancer in mice. Nat Rev Cancer. 2002; 2: 11-8. doi:10.1038/nrc701.
73. Maxwell IH, Chapman JT, Scherrer LC, Spitzer AL, Leptihn S, Maxwell F, et al. Expansion of tropism of a feline parvovirus to target a human tumor cell line by display of an alpha(v) integrin binding peptide on the capsid. Gene Ther. 2001; 8: 324-31. doi:10.1038/sj.gt.3301399.
74. Nanda D, Vogels R, Havenga M, Avezaat CJ, Bout A, Smitt PS. Treatment of malignant gliomas with a replicating adenoviral vector expressing herpes simplex virus-thymidine kinase. Cancer Res. 2001; 61: 8743-50.
75. Rivera AA, Wang M, Suzuki K, Uil TG, Krasnykh V, Curiel DT, et al. Mode of transgene expression after fusion to early or late viral genes of a conditionally replicating adenovirus via an optimized internal ribosome entry site in vitro and in vivo. Virology. 2004; 320: 121-34. doi:10.1016/j.virol.2003.11.028S0042682203008742 [pii].
76. Yamamoto S, Deckter LA, Kasai K, Chiocca EA, Saeki Y. Imaging immediate-early and strict-late promoter activity during oncolytic herpes simplex virus type 1 infection and replication in tumors. Gene Ther. 2006; 13: 1731-6. doi:3302831 [pii]10.1038/sj.gt.3302831.
77. Veerapong J, Bickenbach KA, Shao MY, Smith KD, Posner MC, Roizman B, et al. Systemic delivery of (gamma1)34.5-deleted herpes simplex virus-1 selectively targets and treats distant human xenograft tumors that express high MEK activity. Cancer Res. 2007; 67: 8301-6. doi:67/17/8301 [pii]10.1158/0008-5472.CAN-07-1499.
78. Msaouel P, Iankov ID, Allen C, Morris JC, von Messling V, Cattaneo R, et al. Engineered measles virus as a novel oncolytic therapy against prostate cancer. Prostate. 2009; 69: 82-91. doi:10.1002/pros.20857.
79. Moussavi M, Fazli L, Tearle H, Guo Y, Cox M, Bell J, et al. Oncolysis of prostate cancers induced by vesicular stomatitis virus in PTEN knockout mice. Cancer Res. 2010; 70: 1367-76. doi:0008-5472.CAN-09-2377[pii]10.1158/0008-5472.CAN-09-2377.
80. Thorne SH, Negrin RS, Contag CH. Synergistic antitumor effects of immune cell-viral biotherapy. Science. 2006; 311: 1780-4.
81. Ong HT, Hasegawa K, Dietz AB, Russell SJ, Peng KW. Evaluation of T cells as carriers for systemic measles virotherapy in the presence of antiviral antibodies. Gene Ther. 2007; 14: 324-33. doi:3302880 [pii]10.1038/sj.gt.3302880.
82. Davydova J, Gavrikova T, Brown EJ, Luo X, Curiel DT, Vickers SM, et al. In vivo bioimaging tracks conditionally replicative adenoviral replication and provides an early indication of viral antitumor efficacy. Cancer Sci. 2010; 101: 474-81. doi:CAS1407 [pii]10.1111/j.1349-7006.2009.01407.x.
83. Yu YA, Shabahang S, Timiryasova TM, Zhang Q, Beltz R, Gentschev I, et al. Visualization of tumors and metastases in live animals with bacteria and vaccinia virus encoding light-emitting proteins. Nat Biotechnol. 2004; 22: 313-20.
84. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC. Green fluorescent protein as a marker for gene expression. Science. 1994; 263: 802-5.
85. Song KY, Wong J, Gonzalez L, Sheng G, Zamarin D, Fong Y. Antitumor efficacy of viral therapy using genetically engineered Newcastle disease virus [NDV(F3aa)-GFP] for peritoneally disseminated gastric cancer. J Mol Med (Berl). 2010; 88: 589-96. doi:10.1007/s00109-010-0605-6.
86. Ebert O, Shinozaki K, Huang TG, Savontaus MJ, Garcia-Sastre A, Woo SL. Oncolytic vesicular stomatitis virus for treatment of orthotopic hepatocellular carcinoma in immune-competent rats. Cancer Res. 2003; 63: 3605-11.
87. Stanziale SF, Stiles BM, Bhargava A, Kerns SA, Kalakonda N, Fong Y. Oncolytic herpes simplex virus-1 mutant expressing green fluorescent protein can detect and treat peritoneal cancer. Hum Gene Ther. 2004; 15: 609-18. doi:10.1089/104303404323142051.
88. Allen C, Vongpunsawad S, Nakamura T, James CD, Schroeder M, Cattaneo R, et al. Retargeted oncolytic measles strains entering via the EGFRvIII receptor maintain significant antitumor activity against gliomas with increased tumor specificity. Cancer Res. 2006; 66: 11840-50. doi:66/24/11840 [pii]10.1158/0008-5472.CAN-06-1200.
89. Funston GM, Kallioinen SE, de Felipe P, Ryan MD, Iggo RD. Expression of heterologous genes in oncolytic adenoviruses using picornaviral 2A sequences that trigger ribosome skipping. J Gen Virol. 2008; 89: 389-96. doi:89/2/389 [pii]10.1099/vir.0.83444-0.
90. Ilyin SE, Flynn MC, Plata-Salaman CR. Fiber-optic monitoring coupled with confocal microscopy for imaging gene expression in vitro and in vivo. J Neurosci Methods. 2001; 108: 91-6. doi:S0165-0270(01)00379-X [pii].
91. Li P, Chen CH, Li S, Givi B, Yu Z, Zamarin D, et al. Therapeutic effects of a fusogenic newcastle disease virus in treating head and neck cancer. Head Neck. 2011; 33: 1394-9. doi:10.1002/hed.21609.
92. Shcherbo D, Merzlyak EM, Chepurnykh TV, Fradkov AF, Ermakova GV, Solovieva EA, et al. Bright far-red fluorescent protein for whole-body imaging. Nat Methods. 2007; 4: 741-6. doi:nmeth1083 [pii]10.1038/nmeth1083.
93. Diallo JS, Roy D, Abdelbary H, De Silva N, Bell JC. Ex vivo infection of live tissue with oncolytic viruses. J Vis Exp. 2011; doi:2854 [pii]10.3791/2854.
94. Kishimoto H, Zhao M, Hayashi K, Urata Y, Tanaka N, Fujiwara T, et al. In vivo internal tumor illumination by telomerase-dependent adenoviral GFP for precise surgical navigation. Proc Natl Acad Sci U S A. 2009; 106: 14514-7. doi:0906388106 [pii]10.1073/pnas.0906388106.
95. Adusumilli PS, Eisenberg DP, Chun YS, Ryu KW, Ben-Porat L, Hendershott KJ, et al. Virally directed fluorescent imaging improves diagnostic sensitivity in the detection of minimal residual disease after potentially curative cytoreductive surgery. J Gastrointest Surg. 2005; 9: 1138-46. doi:S1091-255X(05)00556-1 [pii]10.1016/j.gassur.2005.06.029.
96. Kelly KJ, Brader P, Woo Y, Li S, Chen N, Yu YA, et al. Real-time intraoperative detection of melanoma lymph node metastases using recombinant vaccinia virus GLV-1h68 in an immunocompetent animal model. Int J Cancer. 2009; 124: 911-8. doi:10.1002/ijc.24037.
97. Eisenberg DP, Adusumilli PS, Hendershott KJ, Chung S, Yu Z, Chan MK, et al. Real-time intraoperative detection of breast cancer axillary lymph node metastases using a green fluorescent protein-expressing herpes virus. Ann Surg. 2006; 243: 824-30. doi:10.1097/01.sla.0000219738.56896.c000000658- 200606000-00013 [pii].
98. Vassaux G, Groot-Wassink T. In Vivo Noninvasive Imaging for Gene Therapy. J Biomed Biotechnol. 2003; 2003: 92-101. doi:10.1155/S1110724303209050S1110724303209050 [pii].
99. Jacobs A, Tjuvajev JG, Dubrovin M, Akhurst T, Balatoni J, Beattie B, et al. Positron emission tomography-based imaging of transgene expression mediated by replication-conditional, oncolytic herpes simplex virus type 1 mutant vectors in vivo. Cancer Res. 2001; 61: 2983-95.
100. 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: 3295-300. doi:67/7/3295 [pii]10.1158/0008-5472.CAN-06-4062.
101. Tseng JC, Zanzonico PB, Levin B, Finn R, Larson SM, Meruelo D. Tumor-specific in vivo transfection with HSV-1 thymidine kinase gene using a Sindbis viral vector as a basis for prodrug ganciclovir activation and PET. J Nucl Med. 2006; 47: 1136-43. doi:47/7/1136 [pii].
102. Dempsey MF, Wyper D, Owens J, Pimlott S, Papanastassiou V, Patterson J, et al. Assessment of 123I-FIAU imaging of herpes simplex viral gene expression in the treatment of glioma. Nucl Med Commun. 2006; 27: 611-7. doi:00006231-200608000-00003 [pii].
103. McCart JA, Mehta N, Scollard D, Reilly RM, Carrasquillo JA, Tang N, 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.
104. al-Tikriti MS, Baldwin RM, Zea-Ponce Y, Sybirska E, Zoghbi SS, Laruelle M, et al. Comparison of three high affinity SPECT radiotracers for the dopamine D2 receptor. Nucl Med Biol. 1994; 21: 179-88.
105. Brader P, Kelly KJ, Chen N, Yu YA, Zhang Q, Zanzonico P, 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. doi:1078-0432.CCR-08-3236[pii]10.1158/1078-0432.CCR-08-323.
106. Penheiter AR, Griesmann GE, Federspiel MJ, Dingli D, Russell SJ, Carlson SK. Pinhole micro-SPECT/CT for noninvasive monitoring and quantitation of oncolytic virus dispersion and percent infection in solid tumors. Gene Ther. 2011; doi:gt2011107 [pii]10.1038/gt.2011.107.
107. Msaouel P, Iankov ID, Allen C, Aderca I, Federspiel MJ, Tindall DJ, 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. doi:mt2009218 [pii]10.1038/mt.2009.218.
108. 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: 2342-50. doi:blood-2007-01-065573 [pii]10.1182/blood-2007-01-065573.
109. Hakkarainen T, Rajecki M, Sarparanta M, Tenhunen M, Airaksinen AJ, Desmond RA, et al. Targeted radiotherapy for prostate cancer with an oncolytic adenovirus coding for human sodium iodide symporter. Clin Cancer Res. 2009; 15: 5396-403. doi:1078-0432.CCR-08-2571[pii]10.1158/1078-0432.CCR-08-257.
110. Merron A, Baril P, Martin-Duque P, de la Vieja A, Tran L, Briat A, 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. doi:10.1007/s00259-009-1379-3.
111. Haddad D, Chen NG, Zhang Q, Chen CH, Yu YA, Gonzalez L, et al. Insertion of the human sodium iodide symporter to facilitate deep tissue imaging does not alter oncolytic or replication capability of a novel vaccinia virus. J Transl Med. 2011; 9: 36. doi:1479-5876-9-36 [pii]10.1186/1479-5876-9-36.
112. 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: 1761-9. doi:mt2008172 [pii]10.1038/mt.2008.172.
113. Rajecki M, Kangasmaki A, Laasonen L, Escutenaire S, Hakkarainen T, Haukka J, et al. Sodium iodide symporter SPECT imaging of a patient treated with oncolytic adenovirus Ad5/3-Delta24-hNIS. Mol Ther. 2011; 19: 629-31. doi:mt201131 [pii]10.1038/mt.2011.31.
114. Brader P, Kelly K, Gang S, Shah JP, Wong RJ, Hricak H, et al. Imaging of lymph node micrometastases using an oncolytic herpes virus and [F]FEAU PET. PLoS One. 2009; 4: e4789. doi:10.1371/journal.pone.0004789.
115. Dingli D, Peng KW, Harvey ME, Greipp PR, O'Connor MK, Cattaneo R, et al. Image-guided radiovirotherapy for multiple myeloma using a recombinant measles virus expressing the thyroidal sodium iodide symporter. Blood. 2004; 103: 1641-6. doi:10.1182/blood-2003-07-22332003-07-2233 [pii].
116. Mitrofanova E, Unfer R, Vahanian N, Link C. Rat sodium iodide symporter allows using lower dose of 131I for cancer therapy. Gene Ther. 2006; 13: 1052-6. doi:3302758 [pii]10.1038/sj.gt.3302758.