Improved targeting of ligand-modified adenovirus as a new near infrared fluorescence tumor imaging probe

Bioconjugate Chemistry

Volumn 22, Issue 4, 2011, Pages 567-581

  Shan, Lingling ^a   Xue, Jianpeng ^a   Guo, Jing ^a   Qian, Zhiyu ^b   Achilefu, Samuel ^c   Gu, Yueqing ^a  

^a CHINA PHARMACEUTICAL UNIVERSITY   (China)

^b NANJING UNIVERSITY OF AERONAUTICS AND ASTRONAUTICS   (China)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIAGNOSIS; FLUORESCENCE IMAGING; GENE THERAPY; GENE TRANSFER; INFRARED DEVICES; LIGANDS; PROBES; TOXICITY;

ACUTE TOXICITY; ADENOVIRUS VECTOR; DETERMINANT FACTORS; FOLIC ACIDS; IMAGING PROBE; IN-VIVO IMAGING; LOW TOXICITY; NEAR-INFRARED FLUORESCENCE; NEAR-INFRARED FLUORESCENT DYES; TUMOR IMAGING;

TUMORS;

ADENOVIRUS VECTOR; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; FLUORESCENT DYE; FOLIC ACID; FOLIC ACID ADENOVIRUS INDOCYANINE GREEN 02; INDOCYANINE GREEN; UNCLASSIFIED DRUG;

ACUTE TOXICITY; ANIMAL EXPERIMENT; ARTICLE; CHEMICAL STRUCTURE; CONJUGATION; CONTROLLED STUDY; CYTOTOXICITY; DIAGNOSTIC IMAGING; DRUG DISTRIBUTION; FLUORESCENCE IMAGING; GENE TARGETING; GENE THERAPY; GENE TRANSFER; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR TRANSPORT; MOLECULAR IMAGING; MOUSE; NEAR INFRARED FLUORESCENCE TUMOR IMAGING PROBE; NONHUMAN; SYNTHESIS; TUMOR CELL LINE; TUMOR DIAGNOSIS; TUMOR VOLUME; VIRUS CAPSID;

ADENOVIRIDAE; HUMAN ADENOVIRUS TYPE 5; MIRIDAE;

EID: 79955039899     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc100245t     Document Type: Article

References (65)

1. Singh, R. and Kostarelos, K. (2009) Designer adenoviruses for nanomedicine and nanodiagnostics Trends. Biotechnol. 27, 220-229
2. McConnell, M. J. and Imperiale, M. J. (2004) Biology of adenovirus and its use as a vector for gene therapy Hum. Gene. Ther. 15, 1022-1033 (Pubitemid 39552284)
3. Ewert, K., Slack, N. L., Ahmad, A., Evans, H. M., Lin, A. J., Samuel, C. E., and Safinya, C. R. (2004) Cationic lipid-DNA complexes for gene therapy: understanding the relationship between complex structure and gene delivery pathways at the molecular level Curr. Med. Chem. 11, 133-149 (Pubitemid 38128841)
4. Everts, M., Saini, V., Leddon, J. L., Kok, R. J., Stoff-Khalili, M., Preuss, M. A., Millican, C. L., Perkins, G., Brown, J. M., Bagaria, H., Nikles, D. E., Johnson, D. T., Zharov, V. P., and Curiel, D. T. (2006) Covalently linked Au nanoparticles to a viral vector: potential for combined photothermal and gene cancer therapy Nano Lett. 6, 587-591
5. Anderson, E. A., Isaacman, S, Peabody, D. S., Wang, E. Y., Canary, J. W., and Kirshenbaum, K. (2006) Viral nanoparticles donning a paramagnetic coat: conjugation of MRI contrast agents to the MS2 capsid Nano Lett. 6, 1160-1164 (Pubitemid 44013476)
6. Huh, Y. M., Lee, E. S., Lee, J. H., Jun, Y. W., Kim, P. H., Yun, C. O., Kim, J. H., Suh, J. S., and Cheon, J. (2007) Hybrid nanoparticles for magnetic resonance imaging of target-specific viral gene delivery Adv. Mater. 19, 3109-3112 (Pubitemid 350044444)
7. Adam, J. F., Biston, M. C., Rousseau, J., Boudou, C., Charvet, A. M., Balosso, J., Estève, F., and Elleaume, H. (2008) Heavy element enhanced synchrotron stereotactic radiotherapy as a promising brain tumor treatment Phys. Med. 24, 92-97
8. Allen, M., Bulte, J. W., Liepold, L., Basu, G., Zywicke, H. A., Frank, J. A., Young, M., and Douglas, T. (2005) Paramagnetic viral nanoparticles as potential high-relaxivity magnetic resonance contrast agents Magn. Reson. Med. 54, 807-812 (Pubitemid 41457051)
9. Liniger, M., Zuniga, A., and Naim, H. Y. (2007) Use of viral vectors for the development of vaccines Expert Rev. Vaccines 6, 255-266 (Pubitemid 46613525)
10. Clarke, J. M., Morse, M. A., Lyerly, H. K., Clay, T., and Osada, T. (2010) Adenovirus vaccine immunotherapy targeting WT1-expressing tumors Expert Opin. Biol. 10, 875-873
11. Dash, R., Dmitriev, I., Su, Z. Z., Bhutia, S. K, Azab, B., Vozhilla, N., Yacoub, A., Dent, P., Curiel, D. T., Sarkar, D., and Fisher, P. B. (2010) Enhanced delivery of mda-7/IL-24 using a serotype chimeric adenovirus (Ad.5/3) improves therapeutic efficacy in low CAR prostate cancer cells Cancer Gene. Ther. 17, 447-456
12. Hemminki, A., Kanerva, A., Liu, B., Wang, M., Alvarez, R. D., Siegal, G. P., and Curiel, D. T. (2003) Modulation of Coxsackie adenovirus receptor expression for increased adenoviral transgene expression Cancer Res. 15, 847-853 (Pubitemid 36231986)
13. Wakayama, M., Abei, M., Kawashima, R., Seo, E., Fukuda, K., Ugai, H., Murata, T., Tanaka, N., Hyodo, I., Hamada, H., and Yokoyama, K. K. (2007) E1A, E1B double-restricted adenovirus with RGD-fiber modification exhibits enhanced oncolysis for CAR-deficient biliary cancers Clin. Cancer Res. 13, 3043-3050 (Pubitemid 46849581)
14. Bergelson, J. M., Cunningham, J. A., Droguett, G., Kurt-Jones, E. A., Krithivas, A., Hong, J. S., Horwitz, M. S., Crowell, R. L., and Finberg, R. W. (1997) Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5 Science 275, 1320-1323 (Pubitemid 27114163)
15. Coughlan, L., Vallath, S., Saha, A., Flak, M., McNeish, I. A., Vassaux, G., Marshall, J. F., Hart, I. R., and Thomas, G. J. (2009) In vivo retargeting of adenovirus type 5 to alphavbeta6 integrin results in reduced hepatotoxicity and improved tumor uptake following systemic delivery J. Virol. 83, 6416-6428
16. Wu, H., Dmitriev, I., Kashentseva, E., Seki, T., Wang, M., and Curiel, D., T. (2002) Construction and characterization of adenovirus serotype 5 packaged by serotype 3 hexon J. Virol. 76, 12775-12782 (Pubitemid 35386961)
17. Li, J., Le, L., Sibley, D. A., Mathis, J. M., and Curiel, D. T. (2005) Genetic incorporation of HSV-1 thymidine kinase into the adenovirus protein IX for functional display on the virion Virology 338, 247-258 (Pubitemid 41019191)
18. Shashkova, E. V., May, S. M., Doronin, K., and Barry, M. A. (2009) Expanded anticancer therapeutic window of hexon-modified oncolytic adenovirus Mol. Ther. 17, 2121-2130
19. Singh, R., Tian, B., and Kostarelos, K. (2008) Artificial envelopment of nonenveloped viruses: enhancing adenovirus tumor targeting in vivo FASEB. J. 22, 3389-3402
20. Eto, Y., Yoshioka, Y., Asavatanabodee, R., Kida, S., Maeda, M., Mukai, Y., Mizuguchi, H., Kawasaki, K, Okada., N., and Nakagawa, S. (2009) Transduction of adenovirus vectors modified with cell-penetrating peptides Peptides 30, 1548-1552
21. Destito, G., Yeh, R., Rae, C. S., Finn, M. G., and Manchester, M. (2007) Folic acid-mediated targeting of cowpea mosaic virus particles to tumor cells Chem. Biol. 14, 1152-1162 (Pubitemid 47603227)
22. Sega, E. I. and Low, P. S. (2008) Tumor detection using folate receptor-targeted imaging agents Cancer Metastasis Rev. 27, 655-664
23. Arote, R. B., Hwang, S. K., Lim, H. T., Kim, T. H., Jere., D., Jiang, H. L., Kim, Y. K., Cho, M. H., and Cho, C. S. (2010) The therapeutic efficiency of FP-PEA/TAM67 gene complexes via folate receptor-mediated endocytosis in a xenograft mice model Biomaterials 31, 2435-2445
24. Leamon, C. P. and Low, P. S. (1991) Delivery of macromolecules into living cells: A method that exploits folate receptor endocytosis Proc. Natl. Acad. Sci. U.S.A. 88, 5572-5576 (Pubitemid 21914787)
25. Okarvi, S. M. and Jammaz, I. A. (2006) Preparation and in vitro and in vivo evaluation of technetium-99m-labeled folate and methotrexate conjugates as tumor imaging agents Cancer Biother. Radiopharm. 21, 49-60
26. Chapkin, R. S., Kamen, B. A., Callaway, E.S., Davidson, L. A., George, N. I., Wang, N., Lupton, J. R., and Finnell, R. H. (2009) Use of a novel genetic mouse model to investigate the role of folate in colitis-associated colon cancer J. Nutr. Biochem. 20, 649-655
27. Retnakumari, A., Setua, S., Menon, D., Ravindran, P., Muhammed, H., Pradeep, T., Nair, S., and Koyakutty, M. (2010) Molecular-receptor-specific, non-toxic, near-infrared-emitting Au cluster-protein nanoconjugates for targeted cancer imaging Nanotechnology 5, 055103
28. Ke, J. H., Lin, J. J., Carey, J. R., Chen, J. S., Chen, C. Y., and Wang, L. F. (2010) A specific tumor-targeting magnetofluorescent nanoprobe for dual-modality molecular imaging Biomaterials 31, 1707-1715
29. Liu, F., Deng, D., Chen, X., Qian, Z., Achilefu, S., and Gu, Y. Folate-polyethylene glycol conjugated near-infrared fluorescence probe with high targeting affinity and sensitivity for in vivo early tumor diagnosis. Mol. Imaging Biol. 2010, not supplied.
30. Zhang, J., Deng, D., Qian, Z., Liu, F., Chen, X., An, L., and Gu, Y. (2010) The targeting behavior of folate-nanohydrogel evaluated by near infrared imaging system in tumor-bearing mouse model Pharm. Res. 27, 46-55
31. Pierce, M. C., Javier, D. J., and Richards-Kortum, R. (2008) Optical contrast agents and imaging systems for detection and diagnosis of cancer Int. J. Cancer 123, 1979-1990
32. Keramidas, M., Josserand, V., Righini, C. A., Wenk, C., Faure, C., and Coll, J. L. (2010) Intraoperative near-infrared image-guided surgery for peritoneal carcinomatosis in a preclinical experimental model Br. J. Surg. 97, 737-743
33. Keramidas, R., Tung, C. H., Mahmood, U., and Bogdanov, A., Jr. (1999) In vivo imaging of tumors with protease-activated near-infrared fluorescent probes Nat. Biotechnol. 17, 375-378 (Pubitemid 29166041)
34. Hsu, A. R., Hou, L. C., Veeravagu, A., Greve, J. M., Vogel, H, Tse, V., and Chen, X. (2006) In vivo near-infrared fluorescence imaging of integrin alphavbeta3 in an orthotopic glioblastoma model Mol. Imaging Biol. 8, 315-323 (Pubitemid 44741368)
35. Ogawa, M., Regino, C. A., Choyke, P. L., and Kobayashi, H. (2009) In vivo target-specific activatable near-infrared optical labeling of humanized monoclonal antibodies Mol. Cancer Ther. 8, 232-239
36. Björnsson, O. G., Murphy, R., and Chadwick, V. S. (1982) Physiochemical studies of indocyanine green (ICG): absorbance/concentration relationship, pH tolerance and assay precision in various solvents Experientia 38, 1441-1442
37. Zou, P., Xu, S., Povoski, S. P., Wang, A., Johnson, M. A., Martin, E. W., Jr., Subramaniam, V., Xu, R., and Sun, D. (2009) Near-infrared fluorescence labeled anti-TAG-72 monoclonal antibodies for tumor imaging in colorectal cancer xenograft mice Mol. Pharmaceutics 6, 428-440
38. Xiao, W., Yao, N., Peng, L., Liu, R., and Lam, K. S. (2009) Near-infrared optical imaging in glioblastoma xenograft with ligand-targeting alpha3 integrin Eur. J. Nucl. Med. Mol. Imaging 36, 94-103
39. Leopold, P. L., Ferris, B., Grinberg, I., Worgall, S., Hackett, N. R., and Crystal, R. G. (1998) Fluorescent virions: dynamic tracking of the pathway of adenoviral gene transfer vectors in living cells Hum. Gene. Ther. 9, 367-378 (Pubitemid 28085024)
40. Oh, I. K., Mok, H., and Park, T. G. (2006) Folate immobilized and PEGylated adenovirus for retargeting to tumor cells Bioconjugate Chem. 17, 721-727 (Pubitemid 43794382)
41. Schumacher, A., Horvat, S., Woischwill, C., Wolff, G., and Witt, C. (2009) Co-expression of p21 (Waf1/Cip1) in adenovirus vectors improves expression of a second transgene Gene Ther. 16, 574-578
42. Wang, W., Jin, B., Li, W., Xu, C. X., Cui, F. A., Liu, B., Yan, Y. F., Liu, X. X., and Wang, X. L. (2009) Targeted antitumor effect induced by hTERT promoter mediated ODC antisense adenovirus Mol. Biol. Rep. 30, 176-181
43. Yong, R. L., Shinojima, N., Fueyo, J., Gumin, J., Vecil, G. G., Marini, F. C., Bogler, O., Andreeff, M., and Lang, F. F. (2009) Human bone marrow-derived mesenchymal stem cells for intravascular delivery of oncolytic adenovirus Delta24-RGD to human gliomas Cancer Res. 69, 8932-8940
44. Mueller, H., Kassack, M. U., and Wiese, M. (2004) Comparison of the usefulness of the MTT, ATP, and calcein assays to predict the potency of cytotoxici agents in various human cancer cell lines J. Biomol. Screen. 9, 506-515
45. Gao, J., Chen, K., Xie, R., Xie, J., Yan, Y., Cheng, Z., Peng, X., and Chen, X. (2010) In vivo tumor-targeted fluorescence imaging using near-infrared of non-cadmium quantum dots Bioconjugate Chem. 21, 604-609
46. Cheng, Z., Wu, Y., Xiong, Z., Gambhir, S, S., and Chen, X. (2005) Near-infrared fluorescent RGD peptides for optical imaging of integrin alphavbeta3 expression in living mice Bioconjugate Chem. 16, 1433-1441 (Pubitemid 41681509)
47. Zhang, J., Chen, H., Xu, L., and Gu, Y. (2008) The targeted behavior of thermally responsive nanohydrogel evaluated by NIR system in mouse model J. Controlled Release 131, 34-40
48. Johnson, M., Huyn, S., Burton, J., Sato, M., and Wu, L. (2006) Differential biodistribution of adenoviral vector in vivo as monitored by bioluminescence imaging and quantitative polymerase chain reaction Hum. Gene. Ther. 17, 1262-1269 (Pubitemid 44975142)
49. Awasthi, V., Meinken, G., Springer, K., Srivastava, S. C., and Freimuth, P. (2004) Biodistribution of radioiodinated adenovirus fiber protein knob domain after intravenous injection in mice J. Virol. 78, 6431-6438 (Pubitemid 38715941)
50. Liu, Q. and Muruve, D. A. (2003) Molecular basis of the inflammatory response to adenovirus vectors Gene Ther. 10, 935-940 (Pubitemid 36722427)
51. Danielsson, A., Elgue, G., Nilsson, B. M., Nilsson, B., Lambris, J. D., Tötterman, T. H., Kochanek, S., Kreppel, F., and Essand, M. (2010) An ex vivo loop system models the toxicity and efficacy of PEGylated and unmodified adenovirus serotype 5 in whole human blood Gene Ther. 17, 752-762
52. Lubaroff, D. M., Konety, B. R., Link, B., Gerstbrein, J., Madsen, T., Shannon, M., Howard, J., Paisley, J., Boeglin, D., Ratliff, T. L., and Williams, R. D. (2009) Phase I clinical trial of an adenovirus/prostate-specific antigen vaccine for prostate cancer: safety and immunologic results Clin. Cancer Res. 15, 7375-7380
53. Zaiss, A. K., Machado, H. B., and Herschman, H. R. (2009) The influence of innate and pre-existing immunity on adenovirus therapy J. Cell. Biochem. 108, 778-790
54. Ohashi, M., Yoshida, K., Kushida, M., Miura, Y., Ohnami, S., Ikarashi, Y., Kitade, Y., Yoshida, T., and Aoki, K. (2005) Adenovirus-mediated interferon alpha gene transfer induces regional direct cytotoxicity and possible systemic immunity against pancreatic cancer Br. J. Cancer 93, 441-449 (Pubitemid 43080018)
55. Smith, J. S., Xu, Z., and Byrnes, A. P. (2008) A quantitative assay for measuring clearance of adenovirus vectors by Kupffer cells J. Virol. Methods 147, 54-60 (Pubitemid 350250848)
56. Ebisch, I. M., Thomas, C. M., Peters, W. H., Braat, D. D., and Steegers-Theunissen, R. P. (2006) The importance of folate, zinc and antioxidants in the pathogenesis and prevention of subfertility Hum. Reprod. Update 13, 163-174 (Pubitemid 46323193)
57. Bistulfi, G., Vandette, E., Matsui, S., and Smiraglia, D. J. (2010) Mild folate deficiency induces genetic and epigenetic instability and phenotype changes in prostate cancer cells BMC Biol. 21, 8-6
58. Herbort, C. P. (2009) Fluorescein and indocyanine green angiography for uveitis Middle East Afr. J. Ophthalmol. 16, 168-187
59. Ebisch, R. D., Jr. and Pascarella, A. Retinal angiomatous proliferation successfully treated with indocyanine green dye-enhanced photocoagulation. Ophthalmic Surg. Lasers Imaging 2010, not supplied.
60. Lozier, J. N., Csako, G., Mondoro, T. H., Krizek, D. M., Metzger, M. E., Costello, R., Vostal, J. G., Rick, M. E., Donahue, R. E, and Morgan, R. A. (2002) Toxicity of a first-generation adenoviral vector in rhesus macaques Hum. Gene. Ther. 13, 113-124 (Pubitemid 34075175)
61. Shayakhmetov, D. M., Gaggar, A., Ni, S., Li, Z. Y., and Lieber, A. (2005) Adenovirus binding to blood factors results in liver cell infection and hepatotoxicity J. Virol. 79, 7478-7491 (Pubitemid 40756784)
62. Koizumi, N., Yamaguchi, T., Kawabata, K., Sakurai, F., Sasaki, T., Watanabe, Y., Hayakawa, T., and Mizuguchi, H. (2007) Fiber-modified adenovirus vectors decrease liver toxicity through reduced IL-6 production J. Immunol. 178, 1767-1773 (Pubitemid 46154648)
63. McDonald, D., Stockwin, L., Matzow, T., Blair, Zajdel, M. E, and Blair, G. E. (1999) Coxsackie and adenovirus receptor (CAR)-dependent and major histocompatibility complex (MHC) class I-independent uptake of recombinant adenoviruses into human tumor cells Gene Ther. 6, 1512-1519 (Pubitemid 29465509)
64. Kim, M., Zinn, K. R., Barnett, B. G., Sumerel, L. A., Krasnykh, V., Curiel, D. T., and Douglas, J. T. (2002) The therapeutic efficacy of adenoviral vectors for cancer gene therapy is limited by a low level of primary adenovirus receptors on tumor cells Eur. J. Cancer 38, 1917-26 (Pubitemid 35247478)
65. Chen, H., Wang, Y., Xu, J., Ji, J., Zhang, J., Hu, Y., and Gu, Y. (2008) Non-invasive near infrared fluorescence imaging of CdHgTe quantum dots in mouse model J. Fluoresc. 18, 801-811