Visualization of tumors and metastases in live animals with bacteria and vaccinia virus encoding light-emitting proteins

Nature Biotechnology

Volumn 22, Issue 3, 2004, Pages 313-320

  Yu, Yong A ^a,b   Shabahang, Shahrokh ^a   Timiryasova, Tatyana M ^a,b   Zhang, Qian ^b   Beltz, Richard ^a   Gentschev, Ivaylo ^c   Goebel, Werner ^c   Szalay, Aladar A ^a,c,d  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GENELUX CORPORATION   (United States)

^c Department of Microbiology ^*  (United States)

^d UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MUTATIONS; PATHOGENS;

BACTERIA; ENZYMES; ESCHERICHIA COLI; FLUORESCENCE; GENES; IMMUNOLOGY; TUMORS; VIRUSES;

BIOTECHNOLOGY;

BACTERIAL PROTEIN; GREEN FLUORESCENT PROTEIN; LIGHT EMITTING PROTEIN; LUCIFERASE; PHOTOPROTEIN; THYMIDINE KINASE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ADOLESCENT; ANAEROBIC GROWTH; ANIMAL CELL; ANIMAL MODEL; ARTICLE; AUXOTROPHIC MUTANT; BACTERIUM; CANCER DIAGNOSIS; CANCER THERAPY; ESCHERICHIA COLI; EXPERIMENTAL NEOPLASM; FEMALE; FLUORESCENCE; GENE; GENE AMPLIFICATION; GENE LOSS; IMAGING; IMMUNE DEFICIENCY; IMMUNOCOMPETENCE; LISTERIA MONOCYTOGENES; LUMINESCENCE; MALE; METASTASIS; MOUSE; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL; RAT; REAL TIME IMAGING; SALMONELLA TYPHIMURIUM; SOLID TUMOR; THYMIDINE KINASE GENE; TUMOR; TUMOR LOCALIZATION; VACCINIA VIRUS; VIBRIO CHOLERAE; VIRUS REPLICATION;

ANIMALS; BACTERIA; BIOLOGICAL ASSAY; CELL LINE, TUMOR; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; LUMINESCENT PROTEINS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; MICROSCOPY, FLUORESCENCE; NEOPLASM METASTASIS; NEOPLASM STAGING; NEOPLASMS; RATS; VACCINIA VIRUS;

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; LISTERIA; LISTERIA MONOCYTOGENES; MUS MUSCULUS; RODENTIA; SALMONELLA TYPHIMURIUM; VACCINIA VIRUS; VIBRIO; VIBRIO CHOLERAE;

EID: 1542336958     PISSN: 10870156     EISSN: None     Source Type: Journal    
DOI: 10.1038/nbt937     Document Type: Article

References (49)

1. Abelmann, H.W. in Cancer as I See It (Philosophical Library, Inc., New York, 1951).
2. Llinares, P. et al. Infected atrial myxoma simulating infective endocarditis. Enferm. Infecc. Microbiol. Clin. 11, 378-381 (1993).
3. Liao, W.Y. et al. Bacteriology of infected cavitating lung tumor. Am. J. Respir. Crit. Care Med. 161, 1750-1753 (2000).
4. Di Virgilio, G., Lavenda, N. & Siegel, D. Viral particles in human breast cancer. Oncologia 19, 341-348 (1965).
5. Williamson, A.L., Jaskiesicz, K. & Gunning, A. The detection of human papillomavirus in oesophageal lesions. Anticancer Res. 11, 263-265 (1991).
6. Liu, B. et al. Identification of a proviral structure in human breast cancer. Cancer Res. 61, 1754-1759 (2001).
7. Chang, F., Syrjanen, S., Shen, Q., Wang, L. & Syrjanen, K. Screening for human papillomavirus infections in esophageal squamous cell carcinomas by in situ hybridization. Cancer 72, 2525-2530 (1993).
8. Lemmon, M.J. et al. Anaerobic bacteria as a gene delivery system that is controlled by the tumor microenvironment. Gene Ther. 4, 791-796 (1997).
9. Pawelek, J.M., Low, K.B., & Bermudes, D. Tumor-targeted Salmonella as a novel anti-cancer vector. Cancer Res. 57, 4537-4544 (1997).
10. Sauter, B.V., Martinet, O., Zhang, W., Mandeli, J. & Woo, S.L.C. Adenovirus-mediated gene transfer of endostatin in vivo results in high level of transgene expression and inhibition of tumor growth and metastases. Proc. Natl. Acad. Sci. USA 97, 4802-4807 (2000).
11. Gordon, E.M. et al. Systemic administration of a matrix-targeted retroviral vector is efficacious for cancer gene therapy in mice. Hum. Gene Ther. 12, 193-204 (2001).
12. Block, A. et al. Gene therapy of metastatic colon carcinoma: regression of multiple hepatic metastases by adenoviral expression of bacterial cytosine deaminase. Cancer Gene Ther. 7, 438-445 (2000).
13. Chen, C.T. et al. Antiangiogenic gene therapy for cancer via systemic administration of adenoviral vectors expressing secretable endostatin. Hum. Gene Ther. 11, 1983-1996 (2000).
14. Gnant, M.F.X. et al. Tumor-specific gene delivery using recombinant vaccinia virus in a rabbit model of liver metastases. J. Natl. Cancer Inst. 91, 1744-1750 (1999).
15. Gnant, M.F., Puhlmann, M., Bartlett, D.L. & Alexander, H.R. Jr. Regional versus systemic delivery of recombinant vaccinia virus as suicide gene therapy for murine liver metastases. Ann. Surg. 230, 352-360 (1999).
16. McCart, J.A. et al. Complex interactions between the replicating oncolytic effect and the enzyme/prodrug effect of vaccinia-mediated tumor regression. Gene Ther. 7, 1217-1223 (2000).
17. Puhlmann, M. et al. Vaccinia as a vector for tumor-directed gene therapy: biodistribution of a thymidine kinase-deleted mutant. Cancer Gene Ther. 7, 66-73 (2000).
18. Belas, R. et al. Bacterial bioluminescence: isolation and expression of the luciferase genes from Vibrio harveyi. Science 218, 791-793 (1982).
19. De Wet, J.R., Wood, K.V., Deluca, M., Helinski, D.R. & Subramani, S. Firefly luciferase gene: structure and expression in mammalian cells. Mol. Cell. Biol. 7, 725-737 (1987).
20. Prasher, D.C., McCann, R.O., Longiaru, M. & Cormier, M.J. Sequence comparisons of complementary DNAs encoding aequorin isotypes. Biochem. 26, 1326-1332 (1987).
21. Foran, D.R. & Brown, W.M. Nucleotide sequence of the LuxA and LuxB genes of the bioluminescent marine bacterium Vibrio fischeri. Nucleic Acids Res. 16, 777 (1988).
22. Escher, A., O'Kane, D.J., Lee, J., & Szalay, A.A. Bacterial luciferase αβ fusion protein is fully active as a monomer and highly sensitive in vivo to elevated temperature. Proc Natl. Acad. Sci. USA 86, 6528-6532 (1989).
23. Lorenz, W.W., McCann, R.O., Longiaru, M. & Cormier, M.J. Isolation and expression of a cDNA encoding Renilla reniformis luciferase. Proc. Natl. Acad. Sci. USA 88, 4438-4442 (1991).
24. Prasher, D.C., Eckenrode, V.K., Ward, W.W., Prendergast, F.G. & Cormier, M.J. Primary structure of the Aequorea victoria green-fluorescent protein. Gene 111, 229-233 (1992).
25. Engebrecht, J., Simon, M. & Silverman, M. Measuring gene expression with light. Science 227, 1345-1347 (1985).
26. Legocki, R.P., Legocki, M., Baldwin, T.O. & Szalay, A.A. Bioluminescence in soybean root nodules: demonstration of a general approach to assay gene expression in vivo using bacterial luciferase. Proc. Natl. Acad. Sci. USA 83, 9080-9084 (1986).
27. Chalfie, M., Tu, Y., Euskirchen, G., Ward, W.W. & Prasher, D.C. Green fluorescent protein as a marker for gene expression. Science 263, 802-805 (1994).
28. Langridge, W.H.R. et al. A luciferase marker gene system to monitor gene expression in bacteria, plant and virus infected animal cells. Proceedings of the VIIth Int. Symp. on Bio & Chemiluminescence, Banff, Canada, March 14-18, 1993 (eds. Szalay, A.A. et al.) 222-226 (Wiley, Chichester, UK, 1993).
29. O'Kane, D.J. et al. Visualization of bioluminescence as a marker of gene expression in Rhizobium-infected soybean root nodules. J. Plant Mol. Biol. 10, 387-399 (1988).
30. Wang, G., Mayerhofer, R., Langridge, W.H.R., & Szalay, A.A. in Proceedings of the VIIth Int. Symp. on Bio & Chemiluminescence, Banff, Canada, March 14-18, 1993 (eds. Szalay, A.A. et al.) 232-238 (Wiley, Chichester, UK, 1993).
31. Giacomin, L.T. & Szalay, A.A. Expression of a PALI promoter luciferase gene fusion in Arabidopsis thaliana in response to infection by phytopathogenic bacteria. Plant Sci. 116, 59-72 (1996).
32. Lee, C.Y., Szittner, R. & Meighen, E.A. The luxgenes of the luminous bacterial symbiont, Photobacterium leiognathi, of the ponyfish. Nucleotide sequence, difference in gene organization and high expression in mutant Escherichia coli. Eur. J. Biochem. 201, 161-167 (1991).
33. Meighen, E.A. & Szittner, R. Multiple repetitive elements organization of the fux operons of luminescent terrestrial bacteria. J. Bacteriol. 174, 5371-5381 (1992).
34. Fernandez-Pinas, F. & Wolk, C.P. Expression of luxCD-E in Anabaena sp. can replace the use of exogenous aldehyde for in vivo localization of transcription by luxAB. Gene 150, 169-174 (1994).
35. Contag, C.H. et al. Photonic detection of bacterial pathogens in living hosts. Mol. Microbiol. 18, 593-603 (1995).
36. Shabahang, S. & Szalay, A.A. in Proceedings of the 11th International Symposium on Bioluminescence and Chemiluminescence, Pacific Grove, CA, September 6-10, 2000 (eds. Case, J.F. et al.) 449-452 (World Scientific, Singapore, 2001).
37. Wang, Y., Wang, G., O'Kane, D.J. & Szalay, A.A. in Proceedings of the 9th International Symposium on Bioluminescence and Chemiluminescence, Woods Hole, MA, October 4-8, 1996 (eds. Hastings, J.W. et al.) 419-422 (Wiley, Chichester, UK, 1996).
38. Wang, Y., Wang, G., O'Kane D.J. & Szalay A.A. Chemiluminescence energy transfer to study protein-protein interaction in living cells. Mol. Gen. Genet. 264, 578-587 (2001).
39. Wang, Y, Yu Y., Shabahang, S., Wang, G. & Szalay, A.A. Functional Renilla luciferase-Aequorea GFP (RUC-GFP) fusion protein as a novel dual reporter for imaging of gene expression in cell cultures and in live animals. Mol. Gen. Genet. 268, 160-168 (2002).
40. Timiryasova, T., Yu, Y.A., Shabahang, S., Fodor, I. & Szalay, A.A. in Proceedings of the 11th International Symposium on Bioluminescence and Chemiluminescence, Pacific Grove, CA, September 6-10, 2000 (eds. Case, J.F. et al.) 457-460 (World Scientific, Singapore, 2001).
41. Gebauer, G., Jager, W. & Lang, N. mRNA expression of components of the insulin-like growth factor system in breast cancer cell lines, tissues, and metastatic breast cancer cells. Anticancer Res. 18, 1191-1195 (1998).
42. Padera, T.P. et al. Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 296, 1883-1886 (2002).
43. Mose, J.R. & Mose, G. Oncolysis by Clostridia. I. Activity of Clostridium butyricum (M-55) and other nonpathogenic Clostridia against the Ehrlich carcinoma. Cancer Res. 24, 212-216 (1964).
44. Dang, L.H., Bettegowda, C., Huso, D.L., Kinzler, K.W. & Vogelstein, B. Combination bacteriolytic therapy for the treatment of experimental tumors. Proc. Natl. Acad. Sci. USA 98, 15155-15160 (2001).
45. Yazawa, K., Fujimori, M., Amano, J., Kano, Y. & Taniguchi, S. Bifidobacterium longum as a delivery system for cancer gene therapy: selective localization and growth in hypoxic tumors. Cancer Gene Ther. 7, 269-274 (2000).
46. Sznol, M., Lin, S.L., Bermudes, D., Zheng, L.M. & King, I. Use of preferentially replicating bacteria for the treatment of cancer. J. Clin. Invest. 105, 1027-1030 (2000).
47. Ramshaw, I., Ruby, J., Ramsay, A., Ada, G. & Karupiah, G. Expression of cytokines by recombinant vaccinia virus: a model for studying cytokines in virus infections in vivo. Immun. Rev. 127, 157-182 (1992).
48. Gnant, M.F.X., Puhlmann, M., Alexander H.R. & Bartlett, D.L. Systemic administration of a recombinant vaccinia virus expressing the cytosine deaminase gene and subsequent treatment with 5-fluorocytosine leads to tumor-specific gene expression and prolongation of survival in mice. Cancer Res. 59, 3396-3403 (1999).
49. Voisey, C.R. & Marincs, F. Elimination of internal restriction enzyme sites from a bacterial luminescence (luxCDABE) operon. Biotechniques 24, 56-58 (1998).