Using in vivo bioluminescence imaging to shed light on cancer biology

Proceedings of the IEEE

Volumn 93, Issue 4, 2005, Pages 750-762

  Thorne, Steve H ^a   Contag, Christopher H ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Functional imaging; Molecular imaging; Multi modality

Indexed keywords

BIOLUMINESCENCE; BIOTECHNOLOGY; ENZYMES; GENES; OXYGEN; REAL TIME SYSTEMS; SIGNAL PROCESSING; SUBSTRATES; TUMORS;

FUNCTIONAL IMAGING; LIGHT-EMITTING ENZYMES; LUCIFERASES; MOLECULAR IMAGING; MULTI-MODALITY;

MEDICAL IMAGING;

EID: 20744449947     PISSN: 00189219     EISSN: None     Source Type: Journal    
DOI: 10.1109/JPROC.2005.844261     Document Type: Conference Paper

References (101)

1. C. H. Contag, P. R. Contag, J. I. Mullins, S. D. Spilman, D. K. Stevenson, and D. A. Benaron, "Photonic detection of bacterial pathogens in living hosts," Mol. Microbiol., vol. 18, pp. 593-603, 1995.
2. R. Hoffman, "Green fluorescent protein imaging of tumour growth, metastasis, and angiogenesis in mouse models," Lancet Oncol., vol. 3, pp. 546-556, 2002.
3. U. Mahmood and R. Weissleder, "Near-infrared optical imaging of proteases in cancer," Mol. Cancer Ther., vol. 2, pp. 489-496, 2003.
4. B. Chance, "Near-infrared (NIR) optical spectroscopy characterizes breast tissue hormonal and age status," Acad. Radiol., vol. 8, pp. 209-210, 2001.
5. D. A. Benaron, "The future of cancer imaging," Cancer Metastasis Rev., vol. 21, pp. 45-78, 2002.
6. C. Y. Dong, T. French, P. T. So, C. Buehler, K. M. Berland, and E. Gratton, "Fluorescence-lifetime imaging techniques for miroscopy," Methods Cell Biol., vol. 72, pp. 431-464, 2003.
7. B. J. Tromberg, N. Shah, R. Lanning, A. Cerussi, J. Espinoza, T. Pham, L. Svaasand, and J. Butler, "Non-invasive in vivo characterization of breast tumors using photon migration spectroscopy," Neoplasia, vol. 2, pp. 26-40, 2000.
8. J. W. Hastings, "Chemistries and colors of bioluminescent reactions: A review," Gene, vol. 173, pp. 5-11, 1996.
9. T. Wilson and J. W. Hastings, "Bioluminescence," Annu. Rev. Cell Dev. Biol., vol. 14, pp. 197-230, 1998.
10. S. K. Nordeen, "Luciferase reporter gene vectors for analysis of promoters and enhancers," Biotechniques, vol. 6, pp. 454-458, 1988.
11. G. A. Rutter, H. J. Kennedy, C. D. Wood, M. R. White, and J. M. Tavare, "Real-time imaging of gene expression in single living cells," Chem. Biol., vol. 5, pp. R285-R290, 1998.
12. C. E. Hooper, R. E. Ansorge, and J. G. Rushbrooke, "Low-light imaging technology in the life sciences," J. Biolumin. Chemilumin., vol. 9, pp. 113-122, 1994.
13. C. E. Hooper, R. E. Ansorge, H. M. Browne, and P. Tomkins, "CCD imaging of luciferase gene expression in single mammalian cells," J. Biolumin. Chemilumin., vol. 5, pp. 123-130, 1990.
14. W. F. Cheong, S. A. Prahl, and A. J. Welch, "A review of the optical properties of biological tissues," IEEE J. Quantum Electron., vol. 26, no. 12, pp. 2166-2185, Dec. 1990.
15. B. W. Rice, M. D. Cable, and M. B. Nelson, "In vivo imaging of light-emitting probes," J. Biomed. Opt., vol. 6, pp. 432-440, 2001.
16. P. R. Contag, I. N. Olomu, D. K. Stevenson, and C. H. Contag, "Bioluminescent indicators in living mammals," Nat. Med., vol. 4, pp. 245-247, 1998.
17. S. Welsh and S. A. Kay, "Reporter gene expression for monitoring gene transfer," Curr. Opin. Biotechnol., vol. 8, pp. 617-622, 1997.
18. Y. A. Yu, T. Timiryasova, Q. Zhang, R. Beltz, and A. A. Szalay, "Optical imaging: Bacteria, viruses, and mammalian cells encoding light-emitting proteins reveal the locations of primary tumors and metastases in animals," Anal. Bioanal. Chem., vol. 377, pp. 964-972, 2003.
19. G. Choy, P. Choyke, and S. K. Libutti, "Current advances in molecular imaging: Noninvasive in vivo bioluminescent and fluorescent optical imaging in cancer research," Mol. Imaging, vol. 2, pp. 303-312, 2003.
20. T. C. Doyle, S. M. Burns, and C. H. Contag, "In vivo bioluminescence imaging for integrated studies of infection," Cell Microbiol., vol. 6, pp. 303-317, 2004.
21. J. Hardy, K. P. Francis, M. DeBoer, P. Chu, K. Gibbs, and C. H. Contag, "Extracellular replication of Listeria monocytogenes in the murine gall bladder," Science, vol. 303, pp. 851-853, 2004.
22. W. Zhang, J. Q. Feng, S. E. Harris, P. R. Contag, D. K. Stevenson, and C. H. Contag, "Rapid in vivo functional analysis of transgenes in mice using whole body imaging of luciferase expression," Transgenic Res., vol. 10, pp. 423-434, 2001.
23. T. J. Sweeney, V. Mailander, A. A. Tucker, A. B. Olomu, W. Zhang, Y. Cao, R. S. Negrin, and C. H. Contag, "Visualizing the kinetics of tumor-cell clearance in living animals," Proc. Natl. Acad. Sci. USA, vol. 96, pp. 12044-12049, 1999.
24. C. H. Contag, S. D. Spilman, P. R. Contag, M. Oshiro, B. Eames, P. Dennery, D. K. Stevenson, and D. A. Benaron, "Visualizing gene expression in living mammals using a bioluminescent reporter," Photochem. Photobiol., vol. 66, pp. 523-531, 1997.
25. A. Miyawaki, J. Llopis, R. Heim, J. M. McCaffery, J. A. Adams, M. Ikcura, and R. Y. Tsien, "Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin," Nature, vol. 388, pp. 882-887, 1997.
26. E. Forssell-Aronsson, E. Kjellen, S. Mattsson, and M. Hellstrom, "Medical imaging for improved tumour characterization, delineation and treatment verification," Acta Oncol., vol. 41, pp. 604-614, 2002.
27. A. Rangarajan and R. A. Weinberg, "Opinion: Comparative biology of mouse versus human cells: modeling human cancer in mice," Nat. Rev. Cancer, vol. 3, pp. 952-959, 2003.
28. R. Weissleder and U. Mahmood, "Molecular imaging," Radiology, vol. 219, pp. 316-333, 2001.
29. J. J. Min and S. S. Gambhir, "Gene therapy progress and prospects: Noninvasive imaging of gene therapy in living subjects," Gene Ther., vol. 11, pp. 115-125, 2004.
30. M. J. Paulus, S. S. Gleason, S. J. Kennel, P. R. Hunsicker, and D. K. Johnson, "High resolution X-ray computed tomography: An emerging tool for small animal cancer research," Neoplasia, vol. 2, pp. 62-70, 2000.
31. K. Ishizu, T. Mukai, Y. Yonekura, M. Pagani, T. Fujita, Y. Magata, S. Nishizawa, N. Tamaki, H. Shibasaki, and J. Konishi, "Ultra-high resolution SPECT system using four pinhole collimators for small animal studies," J. Nucl. Med., vol. 36, pp. 2282-2287, 1995.
32. A. F. Chatziioannou, S. R. Cherry, Y. Shao, R. W. Silverman, K. Meadors, T. H. Farquhar, M. Pedarsani, and M. E. Phelps, "Performance evaluation of microPET: A high-resolution lutetium oxyorthosilicate PET scanner for animal imaging," J. Nucl. Med., vol. 40, pp. 1164-1175, 1999.
33. J. Ruff, F. Wiesmann, K. H. Hiller, S. Voll, M. von Kienlin, W. R. Bauer, E. Rommel, S. Neubauer, and A. Haase, "Magnetic resonance microimaging for noninvasive quantification of myocardial function and mass in the mouse," Magn. Reson. Med., vol. 40, pp. 43-48, 1998.
34. T. J. Meade, A. K. Taylor, and S. R. Bull, "New magnetic resonance contrast agents as biochemical reporters," Curr. Opin. Neurobiol., vol. 13, pp. 597-602, 2003.
35. N. Gaiano, J. D. Kohtz, D. H. Turnbull, and G. Fishell, "A method for rapid gain-of-function studies in the mouse embryonic nervous system," Nat. Neurosci., vol. 2, pp. 812-819, 1999.
36. F. S. Foster, P. N. Burns, D. H. Simpson, S. R. Wilson, D. A. Christopher, and D. E. Goertz, "Ultrasound for the visualization and quantification of tumor microcirculation," Cancer Metastasis Rev., vol. 19, pp. 131-138, 2000.
37. J. R. Lindner, "Molecular imaging with contrast ultrasound and targeted microbubbles," J. Nucl. Cardiol., vol 11, pp. 215-221, 2004.
38. V. V. Tuchin, Handbook of Optical Biomedical Diagnostics. Washington, DC: SPIE, 2002.
39. K. Licha, "Contrast agents for optical imaging," Topics Curr. Chem., vol. 222, pp. 1-29, 2002.
40. M. Yang, E. Baranov, P. Jiang, F. X. Sun, X. M. Li, L. Li, S. Hasegawa, M. Bouvet, M. Al-Tuwaijri, T. Chishima, H. Shimada, A. R. Moossa, S. Penman, and R. M. Hoffman, "Whole-body optical imaging of green fluorescent protein-expressing tumors and metastases," Proc. Natl. Acad. Sci. USA, vol. 97, pp. 1206-1211, 2000.
41. M. Yang, E. Baranov, A. R. Moossa, S. Penman, and R. M. Hoffman, "Visualizing gene expression by whole-body fluorescence imaging," Proc. Natl. Acad. Sci. USA, vol. 97, pp. 12278-12282, 2000.
42. B. Ballou, G. W. Fisher, J. S. Deng, T. R. Hakala, M. Srivastava, and D. L. Farkas, "Cyanine fluorochrome-labeled antibodies in vivo: Assessment of tumor imaging using Cy3, Cy5, Cy5.5, and Cy7," Cancer Detect. Prev., vol. 22, pp. 251-257, 1998.
43. B. Ramjiawan, R. E. Ariano, H. H. Manisch, P. Maiti, and M. Jackson, "Immunofluorescence imaging as a tool for studying the pharmacokinetics of a human monoclonal single chain fragment antibody," IEEE Trans. Med. Imag., vol. 21, no. 10, pp. 1317-1323, Oct. 2002.
44. C. Bremer, C. H. Tung, A. Bogdanov, Jr., and R. Weissleder, "Imaging of differential protease expression in breast cancers for detection of aggressive tumor phenotypes," Radiology, vol. 222, pp. 814-818, 2002.
45. D. Fukumura, R. Xavier, T. Sugiura, Y. Chen, E. C. Park, N. Lu, M. Selig, G. Nielsen, T. Taksir, R. K. Jain, and B. Seed, "Tumor induction of VEGF promoter activity in stromal cells," Cell, vol. 94, pp. 715-725, 1998.
46. R. R. Alfano, S. G. Demos, P. Galland, S. K. Gayen, Y. Guo, P. P. Ho, X. Liang, F. Liu, L. Wang, Q. Z. Wang, and W. B. Wang, "Time-resolved and nonlinear optical imaging for medical applications," Ann. NY Acad. Sci., vol. 838, pp. 14-28, 1998.
47. J. R. de Wet, K. V. Wood, M. DeLuca, D. R. Helinski, and S. Subramani, "Firefly luciferase gene: Structure and expression in mammalian cells," Mot. Cell. Biol., vol. 7, pp. 725-737, 1987.
48. K. V. Wood, Y. A. Lam, H. H. Seliger, and W. D. McElroy, "Complementary DNA coding click beetle luciferases can elicit bioluminescence of different colors," Science, vol. 244, pp. 700-702, 1989.
49. V. R. Viviani, E. J. Bechara, and Y. Ohmiya, "Cloning, sequence analysis, and expression of active Phrixothrix railroad-worms luciferases: Relationship between bioluminescence spectra and primary structures," Biochemistry, vol. 38, pp. 8271-8279, 1999.
50. W. W. Ward, General Aspects of Bioluminescence, in Chemi-and Bioluminescence, J. G. Burr, Ed. New York: Marcel Dekker, 1985, pp. 321-358.
51. W. W. Lorenz, R. O. McCann, M. Longiaru, and M. J. Cormier, "Isolation and expression of a cDNA encoding Renilla reniformis luciferase," Proc. Natl. Acad. Sci. USA, vol. 88, pp. 4438-4442, 1991.
52. S. Inouye, M. Noguchi, Y. Sakaki, Y. Takagi, T. Miyata, S. Iwanaga, and F. I. Tsuji, "Cloning and sequence analysis of cDNA for the luminescent protein aequorin," Proc. Natl. Acad. Sci. USA, vol. 82, pp. 3154-3158, 1985.
53. S. Frackman, M. Anhalt, and K. H. Nealson, "Cloning, organization, and expression of the bioluminescence genes of Xenorhabdus luminescens," J. Bacterial., vol. 172, pp. 5767-5773, 1990.
54. Z. Li, R. Szittner, and E. A. Meighen, "Subunit interactions and the role of the luxA polypeptide in controlling thermal stability and catalytic properties in recombinant luciferase hybrids," Biochim. Biophys. Acta, vol. 1158, pp. 137-145, 1993.
55. K. P. Francis, D. Joh, C. Bellinger-Kawahara, M. J. Hawkinson, T. F. Purchio, and P. R. Contag, "Monitoring bioluminescent staphylococcus aureus infections in living mice using a novel luxABCDE construct," Infect. Immun., vol. 68, pp. 3594-3600, 2000.
56. R. K. Gupta, S. S. Patterson, S. Ripp, M. L. Simpson, and G. S. Sayler, "Expression of the photorhabdus luminescens lux genes (luxA, B, C, D, and E) in saccharomyces cerevisiae," FEMS Yeast Res., vol. 4, pp. 305-313, 2003.
57. F. J. Janssen, "A study of the absorption and scattering factors of light in whole blood," Med. Biol. Eng., vol. 10, pp. 231-240, 1972.
58. R. Weissleder and V. Ntziachristos, "Shedding light onto live molecular targets," Nat. Med., vol. 9, pp. 123-128, 2003.
59. L. Resor, T. J. Bowen, and A. Wynshaw-Boris, "Unraveling human cancer in the mouse: Recent refinements to modeling and analysis," Hum. Mol. Genet., vol. 10, pp. 669-675, 2001.
60. A. Rehemtulla, D. E. Hall, L. D. Stegman, U. Prasad, G. Chen, M. S. Bhojani, T. L. Chenevert, and B. D. Ross, "Molecular imaging of gene expression and efficacy following adenoviral-mediated brain tumor gene therapy," Mol. Imaging, vol. 1, pp. 43-55, 2002.
61. G. S. Lipshutz, C. A. Gruber, Y. Cao, J. Hardy, C. H. Contag, and K. M. Gaensler, "In utero delivery of adeno-associated viral vectors: Intraperitoneal gene transfer produces long-term expression," Mol. Ther., vol. 3, pp. 284-292, 2001.
62. S. Bhaumik and S. S. Gambhir, "Optical imaging of Renilla luciferase reporter gene expression in living mice," Proc. Natl. Acad. Sci. USA, vol. 99, pp. 377-382, 2002.
63. H. Zhao, T. C. Doyle, R. J. Wong, Y. Cao, D. K. Stevenson, D. Piwnica-Worms, and C. H. Contag, "Characterization of coelenterazine analogs for measurement of Renilla luciferase activity in live cells and living animals," Mol. Imaging, vol. 3, pp. 43-54, 2004.
64. K. Hori, J. M. Anderson, W. W. Ward, and M. J. Cormier, "Renilla luciferin as the substrate for calcium induced photoprotein bioluminescence. Assignment of luciferin tautomers in aequorin and mnemiopsin," Biochemistry, vol. 14, pp. 2371-2376, 1975.
65. M. Oshiro and B. Moomaw, "Cooled vs. intensified vs. electron bombardment CCD cameras-applications and relative advantages," Methods Cell. Biol., vol. 72, pp. 133-156, 2003.
66. M. Edinger, Y. A. Cao, Y. S. Hornig, D. E. Jenkins, M. R. Verneris, M. H. Bachmann, R. S. Negrin, and C. H. Contag, "Advancing animal models of neoplasia through in vivo bioluminescence imaging," Eur. J. Cancer, vol. 38, pp. 2128-2136, 2002.
67. M. Edinger, T. J. Sweeney, A. A. Tucker, A. B. Olomu, R. S. Negrin, and C. H. Contag, "Noninvasive assessment of tumor cell proliferation in animal models," Neoplasia, vol. 1, pp. 303-310, 1999.
68. A. Rehemtulla, L. D. Stegman, S. J. Cardozo, S. Gupta, D. E. Hall, C. H. Contag, and B. D. Ross, "Rapid and quantitative assessment of cancer treatment response using in vivo bioluminescence imaging," Neoplasia, vol. 2, pp. 491-495, 2000.
69. M. Iyer, M. Berenji, N. S. Templeton, and S. S. Gambhir, "Noninvasive imaging of cationic lipid-mediated delivery of optical and PET reporter genes in living mice," Mol. Ther., vol. 6, pp. 555-562, 2002.
70. M. Edinger, Y. A. Cao, M. R. Verneris, M. H. Bachmann, C. H. Contag, and R. S. Negrin, "Revealing lymphoma growth and the efficacy of immune cell therapies using in vivo bioluminescence imaging," Blood, vol. 101, pp. 640-648, 2003.
71. S. Zeamari, G. Rumping, B. Floot, S. Lyons, and F. A. Stewart, "In vivo bioluminescence imaging of locally disseminated colon carcinoma in rats," Br. J. Cancer, vol. 90, pp. 1259-1264, 2004.
72. D. E. Jenkins, Y. Oei, Y. S. Hornig, S. F. Yu, J. Dusich, T. Purchio, and P. R. Contag, "Bioluminescent imaging (BLI) to improve and refine traditional murine models of tumor growth and metastasis," Clin. Exp. Metastasis, vol. 20, pp. 733-744, 2003.
73. T. J. Rosol, S. H. Tannehill-Gregg, B. E. LeRoy, S. Mandl, and C. H. Contag, "Animal models of bone metastasis," Cancer, vol. 97, pp. 748-757, 2003.
74. C. Scheffold, M. Kornacker, Y. C. Scheffold, C. H. Contag, and R. S. Negrin, "Visualization of effective tumor targeting by CD8+ natural killer T cells redirected with bispecific antibody F(ab′)(2)HER2xCD3," Cancer Res, vol. 62, pp. 5785-5791, 2002.
75. P. E. Andreotti, G. Caceres, R. Zamkina, and M. Dauphinee, "Luminescence applications for chemotherapeutic drug development," Recent Results Cancer Res., vol. 161, pp. 3-12, 2003.
76. S. Wang and W. S. El-Deiry, "Requirement of p53 targets in chemosensitization of colonie carcinoma to death ligand therapy," Proc. Natl. Acad. Sci. USA, vol. 100, pp. 15 095-15 100, 2003.
77. G. D. Luker, C. M. Pica, J. Song, K. E. Luker, and D. Piwnica-Worms, "Imaging 26S proteasome activity and inhibition in living mice," Nat. Med., vol. 9, pp. 969-973, 2003.
78. J. T. Nguyen, H. Machado, and H. R. Herschman, "Repetitive, noninvasive imaging of cyclooxygenase-2 gene expression in living mice," Mol. Imaging Biol., vol. 5, pp. 248-256, 2003.
79. M. Eilers, D. Picard, K. R. Yamamoto, and J. M. Bishop, "Chimaeras of myc oncoprotein and steroid receptors cause hormone-dependent transformation of cells," Nature, vol. 340, pp. 66-68, 1989.
80. B. Laxman, D. E. Hall, M. S. Bhojani, D. A. Hamstra, T. L. Chenevert, B. D. Ross, and A. Rehemtulla, "Noninvasive real-time imaging of apoptosis," Proc. Natl. Acad. Sci. USA, vol. 99, pp. 16551-16555, 2002.
81. T. Monsees, W. Miska, and R. Geiger, "Synthesis and characterization of a bioluminogenic substrate for alpha-chymotrypsin," Anal. Biochem., vol. 221, pp. 329-334, 1994.
82. F. Tronche, E. Casanova, M. Turiault, I. Sahly, and C. Kellendonk, "When reverse genetics meets physiology: The use of site-specific recombinases in mice," FEBS Lett., vol. 529, pp. 116-121, 2002.
83. R. Kuhn and R. M. Torres, "Cre/loxP recombination system and gene targeting," Methods Mol. Biol., vol. 180, pp. 175-204, 2002.
84. S. K. Lyons, R. Meuwissen, P. Krimpenfort, and A. Berns, "The generation of a conditional reporter that enables bioluminescence imaging of Cre/loxP-dependent tumorigenesis in mice," Cancer Res., vol. 63, pp. 7042-7046, 2003.
85. M. Safran, W. Y. Kim, A. L. Kung, J. W. Homer, R. A. DePinho, and W. G. Kaelin, Jr., "Mouse reporter strain for noninvasive bioluminescent imaging of cells that have undergone cre-mediated recombination," Mol. Imaging, vol. 2, pp. 297-302, 2003.
86. D. Kirn, R. L. Martuza, and J. Zwiebel, "Replication-selective virotherapy for cancer: Biological principles, risk management and future directions," Nat. Med., vol. 7, pp. 781-787, 2001.
87. K. Shah, Y. Tang, X. Breakefield, and R. Weissleder, "Real-time imaging of TRAIL-induced apoptosis of glioma tumors in vivo," Oncogene, vol. 22, pp. 6865-6872, 2003.
88. I. J. Hildebrandt, M. Iyer, E. Wagner, and S. S. Gambhir, "Optical imaging of transferrin targeted PEI/DNA complexes in living subjects," Gene Ther., vol. 10, pp. 758-764, 2003.
89. M. Akiyama, S. Thorne, D. Kim, P. W. Roelvink, D. A. Einfeld, C. R. King, and T. J. Wickham, "Ablating CAR and integrin binding in adenovirus vectors reduces nontarget organ transduction and permits sustained bloodstream persistence following intraperitoneal administration," Mol. Ther., vol. 9, pp. 218-230, 2004.
90. J. Y. Adams, M. Johnson, M. Sato, F. Berger, S. S. Gambhir, M. Carey, M. L. Iruela-Arispe, and L. Wu, "Visualization of advanced human prostate cancer lesions in living mice by a targeted gene transfer vector and optical imaging," Nat. Med., vol. 8, pp. 891-897, 2002.
91. M. Sato, M. Johnson, L. Zhang, B. Zhang, K. Le, S. S. Gambhir, M. Carey, and L. Wu, "Optimization of adenoviral vectors to direct highly amplified prostate-specific expression for imaging and gene therapy" Mol. Ther., vol. 8, pp. 726-737, 2003.
92. Y. A. Yu, S. Shabahang, T. M. Timiryasova, Q. Zhang, R. Beltz, I. Gentschev, W. Goebel, and A. A. Szalay, "Visualization of tumors and metastases in live animals with bacteria and vaccinia virus encoding light-emitting proteins," Nat. Biotechnol., vol. 22, pp. 313-320, 2004.
93. M. R. Verneris, M. Karami, J. Baker, A. Jayaswal, and R. S. Negrin, "Role of NKG2D signaling in the cytotoxicity of activated and expanded CD8+ T cells," Blood, vol. 103, pp. 3065-3072, 2004.
94. C. H. Contag and M. H. Bachmann, "Advances in in vivo bioluminescence imaging of gene expression," Annu. Rev. Biomed. Eng., vol. 4, pp. 235-260, 2002.
95. Y. A. Cao, A. J. Wagers, A. Beilhack, J. Dusich, M. H. Bachmann, R. S. Negrin, I. L. Weissman, and C. H. Contag, "Shifting foci of hematopoiesis during reconstitution from single stem cells," Proc. Natl. Acad. Sci. USA, vol. 101, pp. 221-226, 2004.
96. A. Pichler, J. L. Prior, and D. Piwnica-Worms, "Imaging reversal of multidrug resistance in living mice with bioluminescence: MDR1 P-glycoprotein transports coelenterazine," Proc. Natl. Acad. Sci. USA, vol. 101, pp. 1702-1707, 2004.
97. P. Ray, A. De, J. J. Min, R. Y. Tsien, and S. S. Gambhir, "Imaging tri-fusion multimodality reporter gene expression in living subjects," Cancer Res., vol. 64, pp. 1323-1330, 2004.
98. N. Kajiyama and E. Nakano, "Isolation and characterization of mutants of firefly luciferase which produce different colors of light," Protein Eng., vol. 4, pp. 691-693, 1991.
99. Y. Xu, D. W. Piston, and C. H. Johnson, "A bioluminescence resonance energy transfer (BRET) system: Application to interacting circadian clock proteins," Proc. Natl. Acad. Sci. USA, vol. 96, pp. 151-156, 1999.
100. Y. Wang, Y. A. Yu, S. Shabahang, G. Wang, and A. A. Szalay, "Renilla luciferase-Aequorea GFP (Ruc-GFP) fusion protein, a noveldual reporter for real-time imaging of gene expression in cell cultures and in live animals," Mol. Genet. Genomics, vol. 268, pp. 160-168, 2002.
101. Y. Wang, G. Wang, D. J. O'Kane, and A. A. Szalay, "A study of protein-protein interactions in living cells using luminescence resonance energy transfer (LRET) from Renilla luciferase to Aequorea GFP," Mol. Gen. Genet., vol. 264, pp. 578-587, 2001.