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Multicolor Imaging with Fluorescent Proteins in Mice

In Vivo Imaging with Fluorescent Proteins

  • Chapter
Reviews in Fluorescence 2008

Part of the book series: Reviews in Fluorescence 2008 ((RFLU,volume 2008))

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Abstract

The high extinction coefficients, quantum yields, and unique spectral properties of fluorescent proteins are optimal for imaging in live animals in real time. The important aspects of cancer in living animals, including tumor cell mobility, invasion, metastasis, and angiogenesis, can be imaged. Fluorescent proteins enable whole-body imaging of tumors on internal organs. Proteins which are spectrally distinct have allowed the color coding of cancer cells growing in vivo with distinction of different cell types, including host from tumor, with single-cell resolution. Individual cells can be multicolored to study nuclear–cytoplasmic dynamics in the living animal.

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References

  1. V. Verkhusha, K.A. Lukyanov, The molecular properties and applications of Anthozoa fluorescent proteins and chromoproteins. Nat. Biotech. 22, 289–296 (2004).

    CAS  Google Scholar 

  2. M. Zimmer, Green fluorescent protein (GFP): applications, structure and related photophysical behavior. Chem. Rev. 102, 759–781 (2002).

    CAS  PubMed  Google Scholar 

  3. A.K. Hadjantonakis, V.E. Papaioannou, Dynamic in vivo imaging and cell tracking using a histone fluorescent protein fusion in mice. BMC Biotechnol. 4, 33 (2004).

    PubMed  Google Scholar 

  4. T. Chishima, Y. Miyagi, X. Wang, H. Yamaoka, H. Shimada, A.R. Moossa, R.M. Hoffman, Cancer invasion and micrometastasis visualized in live tissue by green fluorescent protein expression. Cancer Res. 57, 2042–2047 (1997).

    CAS  PubMed  Google Scholar 

  5. M. Yang, E. Baranov, A.R. Moossa, S. Penman, R.M. Hoffman, Visualizing gene expression by whole-body fluorescence imaging. Proc. Natl. Acad. Sci. U S A 97, 12278–12282 (2000).

    CAS  PubMed  Google Scholar 

  6. M. Zhao, M. Yang, E. Baranov, X. Wang, S. Penman, A.R. Moossa, R.M. Hoffman, Spatial–temporal imaging of bacterial infection and antibiotic response in intact animals. Proc. Natl. Acad. Sci. U S A 98, 9814–9818 (2001).

    CAS  PubMed  Google Scholar 

  7. L. Li, J. Mignone, M. Yang, M. Matic, S. Penman, G. Enikolopov, R.M. Hoffman, Nestin expression in hair follicle sheath progenitor cells. Proc. Natl. Acad. Sci. U S A 100, 9958–9961 (2003).

    Google Scholar 

  8. Y. Amoh, L. Li, M. Yang, A.R. Moossa, K. Katsuoka, S. Penman, R.M. Hoffman, Nascent blood vessels in the skin arise from nestin-expressing hair follicle cells. Proc. Natl. Acad. Sci. U S A 101, 13291–13295 (2004).

    CAS  PubMed  Google Scholar 

  9. 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, R.M. Hoffman, Whole-body optical imaging of green fluorescent protein-expressing tumors and metastases. Proc. Natl. Acad. Sci. U S A 97, 1206–1211 (2000).

    CAS  PubMed  Google Scholar 

  10. M.H. Katz, S. Takimoto, D. Spivack, A.R. Moossa, R.M. Hoffman, M. Bouvet, A novel red fluorescent protein orthotopic pancreatic cancer model for the preclinical evaluation of chemotherapeutics. J. Surg. Res. 113, 151–160 (2003).

    CAS  PubMed  Google Scholar 

  11. M.H. Katz, M. Bouvet, S. Takimoto, D. Spivack, A.R. Moossa, R.M. Hoffman, Survival efficacy of adjuvant cytosine-analogue CS-682 in a fluorescent orthotopic model of human pancreatic cancer. Cancer Res. 64, 1828–1833 (2004).

    CAS  PubMed  Google Scholar 

  12. M.H. Katz, M. Bouvet, S. Takimoto, D. Spivack, A.R. Moossa, R.M. Hoffman, Selective antimetastatic activity of cytosine analog CS-682 in a red fluorescent protein orthotopic model of pancreatic cancer. Cancer Res. 63, 5521–5525 (2003).

    CAS  PubMed  Google Scholar 

  13. O. Peyruchaud, B. Winding, I. Pecheur, C.M. Serre, P. Delmas, P. Clezardin, Early detection of bone metastases in a murine model using fluorescent human breast cancer cells: application to the use of the bisphosphonate zoledronic acid in the treatment of osteolytic lesions. J. Bone Miner. Res. 16, 2027–2034 (2001).

    CAS  PubMed  Google Scholar 

  14. O. Peyruchaud, C-M. Serre, R. NicAmhlaoibh, P. Fournier, P. Clezardin, Angiostatin inhibits bone metastasis formation in nude mice through a direct anti-osteoclastic activity. J. Biol. Chem. 278, 45826–45832 (2003).

    CAS  PubMed  Google Scholar 

  15. T.R. Chaudhuri, J.M. Mountz, B.E. Rogers, E.E. Partridge, K.R. Zinn, Light-based imaging of green fluorescent protein-positive ovarian cancer xenografts during therapy. Gynecol. Oncol. 82, 581–589 (2001).

    CAS  PubMed  Google Scholar 

  16. T.R. Chaudhuri, Z. Cao, V.N. Krasnykh, A.V. Stargel, N. Belousova, E.E. Partridge, K.R. Zinn, Blood-based screening and light based imaging for the early detection and monitoring of ovarian cancer xenografts. Technol. Cancer Res. Treat. 2, 171–180 (2003).

    PubMed  Google Scholar 

  17. G. Choy, S. O'Connor, F.E. Diehn, N. Costouros, H.R. Alexander, P. Choyke, S.K.Libutti, Comparison of noninvasive fluorescent and bioluminescent small animal optical imaging. Biotechniques 35, 1022–1026, 1028–1030 (2003).

    PubMed  Google Scholar 

  18. M. Yang, E. Baranov, X.M. Li, J.W. Wang, P. Jiang, L. Li, A.R. Moossa, S. Penman, R.M. Hoffman, Whole-body and intravital optical imaging of angiogenesis in orthotopically implanted tumors. Proc. Natl. Acad. Sci. U S A 98, 2616–2621 (2001).

    CAS  PubMed  Google Scholar 

  19. M. Zhao, M. Yang, X-M. Li, P. Jiang, S. Li, M. Xu, R.M. Hoffman, Tumor-targeting bacterial therapy with amino acid auxotrophs of GFP-expressing Salmonella typhimurium. Proc. Natl. Acad. Sci U S A 102, 755–760 (2005).

    CAS  PubMed  Google Scholar 

  20. Y.A. Yu, S. Shabahang, T.M. Timiryasova, Q. Zhang, R. Beltz, I. Gentschev, W. Goebel, A.A. Szalay, Visualization of tumors and metastases in live animals with bacteria and vaccinia virus encoding light-emitting proteins. Nat. Biotechnol. 22, 313–320 (2004).

    CAS  PubMed  Google Scholar 

  21. M. Yang, E. Baranov, J-W. Wang, P. Jiang, X. Wang, F-X. Sun, M. Bouvet, A.R. Moossa, S. Penman, R.M. Hoffman, Direct external imaging of nascent cancer, tumor progression, angiogenesis, and metastasis on internal organs in the fluorescent orthotopic model. Proc. Natl. Acad. Sci. U S A 99, 3824–3829 (2002).

    CAS  PubMed  Google Scholar 

  22. A. Panoskaltsis-Mortari, A. Price, J.R. Hermanson, E. Taras, C. Lees, J.S. Serody, B.R. Blazar. In vivo imaging of graft-versus-host-disease in mice. Blood 103(9), 3590–3598 (2004).

    CAS  PubMed  Google Scholar 

  23. D.A. Tyas, T. Pratt, T.I. Simpson, J.O. Mason, D.J. Price, Identifying GFP-transgenic animals by flashlight. Biotechniques 34, 474–476 (2003).

    CAS  PubMed  Google Scholar 

  24. M. Yang, G. Luiken, E. Baranov, R.M. Hoffman, Facile whole-body imaging of internal fluorescent tumors in mice with an led flashlight. Biotechniques 39, 170–172 (2005).

    Google Scholar 

  25. E.B. Brown, R.B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, R.K. Jain, In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy. Nat. Med. 7, 864–868 (2001).

    CAS  PubMed  Google Scholar 

  26. R. Levenson, M. Yang, R.M. Hoffman, Whole-body dual-color differential fluorescence imaging of tumor angiogenesis enhanced by spectral unmixing. Proc. Am. Assoc. Cancer Res. 45, 46 (Abstract #202) (2004).

    Google Scholar 

  27. C.M. John, H. Leffler, B. Kahl-Knutsson, I. Svensson, G.A. Jarvis, Truncated Galectin-3 Inhibits tumor growth and metastasis in orthotopic nude mouse model of human breast cancer. Clin. Cancer Res. 9, 2374–2383, 2003.

    CAS  PubMed  Google Scholar 

  28. T. Chishima, Y. Miyagi, X. Wang, E. Baranov, Y. Tan, H. Shimada, A.R. Moossa, R.M. Hoffman, Metastatic patterns of lung cancer visualized live and in process by green fluorescent protein expression. Clin. Exp. Metastasis 15, 547–552 (1997).

    CAS  PubMed  Google Scholar 

  29. M.S. Huang, T.J. Wang, C.L. Liang, H.M. Huang, I.C. Yang, H. Yi-Jan, M. Hsiao, Establishment of fluorescent lung carcinoma metastasis model and its real-time microscopic detection in SCID mice. Clin. Exp. Metastasis 19, 359–68 (2002).

    CAS  PubMed  Google Scholar 

  30. C-Y. Li, S. Shan, Q. Huang, R.D. Braun, J. Lanzen, K. Hu, P. Lin, M.W. Dewhirst, Initial stages of tumor cell-induced angiogenesis: evaluation via skin window chambers in rodent models. J. Natl. Cancer Inst. 92, 143–147 (2000).

    CAS  PubMed  Google Scholar 

  31. A. Moore, E. Marecos, M. Simonova, R. Weissleder, A. Bogdanov Jr., Novel gliosarcoma cell line expressing green fluorescent protein: a model for quantitative assessment of angiogenesis. Microvasc. Res. 56, 145–153 (1998).

    CAS  PubMed  Google Scholar 

  32. A.B. Al-Mehdi, K. Tozawa, A.B. Fisher, L. Shientag, A. Lee, R.J. Muschel, Intravascular origin of metastasis from the proliferation of endothelium-attached tumor cells: a new model for metastasis. Nat. Med. 6, 100–102 (2000).

    CAS  PubMed  Google Scholar 

  33. C.W. Wong, C. Song, M.M. Grimes, W. Fu, M.W. Dewhirst, R.J. Muschel, A.B. Al-Mehdi, Intravascular location of breast cancer cells after spontaneous metastasis to the lung. Am. J. Pathol. 161, 749–753 (2002).

    PubMed  Google Scholar 

  34. S. Ito, H. Nakanishi, Y. Ikehara, T. Kato, Y. Kasai, K. Ito, S. Akiyama, A. Nakao, M. Tatematsu, Real-time observation of micrometastasis formation in the living mouse liver using a green fluorescent protein gene-tagged rat tongue carcinoma cell line. Int. J. Cancer 93, 212–217 (2001).

    CAS  PubMed  Google Scholar 

  35. O.R. Mook, J. Van Marle, H. Vreeling-Sindelarova, R. Jonges, W.M. Frederiks, C.J. Van Noorden, Visualization of early events in tumor formation of eGFP-transfected rat colon cancer cells in liver. Hepatology 38, 295–304 (2003).

    PubMed  Google Scholar 

  36. J.W. Sturm, M.A. Keese, B. Petruch, R.G. Bonninghoff, H. Zhang, N. Gretz, M. Hafner, S. Post, R.S. McCuskey, Enhanced green fluorescent protein-transfection of murine colon carcinoma cells: key for early tumor detection and quantification. Clin. Exp. Metastasis 20, 395–405 (2003).

    PubMed  Google Scholar 

  37. J-W. Wang, M. Yang, R.M. Hoffman, Visualizing portal vein metastatic trafficking to the liver with green fluorescent protein-expressing tumor cells. Anticancer Res. 24, 3699–3702 (2004).

    PubMed  Google Scholar 

  38. D. Fukumura, F. Yuan, W.L. Monsky, Y. Chen, R.K. Jain, Effect of host microenvironment on the microcirculation of human colon adenocarcinoma. Am. J. Pathol. 151, 679–688 (1997).

    CAS  PubMed  Google Scholar 

  39. D. Fukumura, R. Xavier, T. Sugiura, Y. Chen, E.C. Park, N. Lu, M. Selig, G. Nielsen, T. Taksir, R.K. Jain, B. Seed, Tumor induction of VEGF promoter activity in stromal cells. Cell 94, 715–725 (1998).

    CAS  PubMed  Google Scholar 

  40. C.W. Wong, A. Lee, L. Shientag, J. Yu, Y. Dong, G. Kao, A.B. Al-Mehdi, E.J. Bernhard, R.J. Muschel, Apoptosis: an early event in metastatic inefficiency. Cancer Res. 61, 333–338 (2001).

    CAS  PubMed  Google Scholar 

  41. Y.S. Chang, E. di Tomaso, D.M. McDonald, R. Jones, R.K. Jain, L.L. Munn, Mosaic blood vessels in tumors: frequency of cancer cells in contact with flowing blood. Proc. Natl. Acad. Sci. U S A 97, 14608–14613 (2000).

    CAS  PubMed  Google Scholar 

  42. J.B. Wyckoff, J.G. Jones, J.S. Condeelis, J.E. Segall, A critical step in metastasis: in vivo analysis of intravasation at the primary tumor. Cancer Res. 60, 2504–2511 (2000).

    CAS  PubMed  Google Scholar 

  43. F. Ahmed, J. Wyckoff, E.Y. Lin, W. Wang, Y. Wang, L. Hennighausen, J. Miyazaki, J. Jones, J.W. Pollard, J.S. Condeelis, J.E. Segall, GFP expression in the mammary gland for imaging of mammary tumor cells in transgenic mice. Cancer Res. 62(24), 7166–7169 (2002).

    CAS  PubMed  Google Scholar 

  44. A.B. Glinskii, B.A. Smith, P. Jiang, X.M. Li, M. Yang, R.M. Hoffman, G.V. Glinsky, Viable circulating metastatic cells produced in orthotopic but not ectopic prostate cancer models. Cancer Res. 63, 4239–4243 (2003).

    CAS  PubMed  Google Scholar 

  45. O. Berezovskaya, A.D. Schimmer, A.B. Glinskii, C. Pinilla, R.M. Hoffman, J.C. Reed, G.V. Glinky, Increased expression of apoptosis inhibitor protein XIAP contributes to anoikis resistance of circulating metastatic human prostate cancer cells. Cancer Res. 65, 2378–2386 (2005).

    CAS  PubMed  Google Scholar 

  46. N. Yamamoto, P. Jiang, M. Yang, M. Xu, K. Yamauchi, H. Tsuchiya, K. Tomita, G.M. Wahl, A.R. Moossa, R.M. Hoffman, Cellular dynamics visualized in live cells in vitro and in vivo by differential dual-color nuclear-cytoplasmic fluorescent-protein expression. Cancer Res. 64, 4251–4256 (2004).

    CAS  PubMed  Google Scholar 

  47. K. Yamauchi, M. Yang, P. Jiang, N. Yamamoto, M. Xu, Y. Amoh, K. Tsuji, M. Bouvet, H. Tsuchiya, K. Tomita, A.R. Moossa, R.M. Hoffman, Real-time in vivo dual-color imaging of intracapillary cancer cell and nucleus deformation and migration. Cancer Res. 65, 4246–4252 (2005).

    CAS  PubMed  Google Scholar 

  48. N. Yamamoto, M. Yang, P. Jiang, M. Xu, H. Tsuchiya, K. Tomita, A.R. Moossa, R.M. Hoffman, Determination of clonality of metastasis by cell-specific color-coded fluorescent-protein imaging. Cancer Res. 63, 7785–7790 (2003).

    CAS  PubMed  Google Scholar 

  49. N. Yamamoto, M. Yang, P. Jiang, M. Xu, H. Tsuchiya, K. Tomita, A.R. Moossa, R.M. Hoffman, Real-time imaging of individual fluorescent protein color-coded metastatic colonies in vivo. Clin. Exp. Metastasis 20(7), 633–638 (2003).

    CAS  PubMed  Google Scholar 

  50. M. Okabe, M. Ikawa, K. Kominami, T. Nakanishi, Y. Nishimune, “Green mice” as a source of ubiquitous green cells. FEBS Lett. 407, 313–319 (1997).

    CAS  PubMed  Google Scholar 

  51. M. Yang, J. Reynoso, P. Jiang, L. Li, A.R. Moossa, R.M. Hoffman, Transgenic nude mouse with ubiquitous green fluorescent protein expression as a host for human tumors. Cancer Res. 64, 8651–8656 (2004).

    CAS  PubMed  Google Scholar 

  52. M. Yang, L. Li, P. Jiang, A.R. Moossa, S. Penman, R.M. Hoffman, Dual-color fluorescence imaging distinguishes tumor cells from induced host angiogenic vessels and stromal cells. Proc. Natl. Acad. Sci. U S A 100, 14259–14262 (2003).

    CAS  PubMed  Google Scholar 

  53. Y. Amoh, L. Li, M. Yang, P. Jiang, A.R. Moossa, K. Katsuoka, R.M. Hoffman, Hair-follicle-derived blood vessels vascularize tumors in skin and are inhibited by doxorubicin. Cancer Res, 65, 2337–2343 (2005).

    CAS  PubMed  Google Scholar 

  54. Y. Amoh, M. Yang, L. Li, J. Reynoso, M. Bouvet, A.R. Moossa, K. Katsuoka, R.M. Hoffman, Nestin-linked-green fluorescent protein transgenic nude mouse for imaging human tumor angiogenesis. Cancer Res 65, 5352–5357 (2005).

    Google Scholar 

  55. D.G. Duda, D. Fukumura, L.L. Munn, M.F. Booth, E.B. Brown, P. Huang, B. Seed, R.K. Jain, Differential transplantability of tumor-associated stromal cells. Cancer Res. 64, 5920–5924 (2004).

    CAS  PubMed  Google Scholar 

  56. J. Morin, J. Hastings, Energy transfer in a bioluminescent system. J. Cell Physiol. 77, 313–318 (1971).

    CAS  PubMed  Google Scholar 

  57. B. Cormack, R. Valdivia, S. Falkow, FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173, 33–38 (1996).

    CAS  PubMed  Google Scholar 

  58. A. Crameri, E.A. Whitehorn, E. Tate, W.P.C. Stemmer, Improved green fluorescent protein by molecular evolution using DNA shuffling. Nat. Biotechnol. 14, 315–319 (1996).

    CAS  PubMed  Google Scholar 

  59. S. Delagrave, R.E. Hawtin, C.M. Silva, M.M. Yang, D.C. Youvan, Red-shifted excitation mutants of the green fluorescent protein. Biotechnology 13, 151–154 (1995).

    CAS  PubMed  Google Scholar 

  60. R. Heim, A.B. Cubitt, R.Y. Tsien, Improved green fluorescence. Nature 373, 663–664 (1995).

    CAS  PubMed  Google Scholar 

  61. S. Zolotukhin, M. Potter, W.W. Hauswirth, J. Guy, N. Muzyczka, A “humanized” green fluorescent protein cDNA adapted for high-level expression in mammalian cells. J. Virol. 70, 4646–4654 (1996).

    CAS  PubMed  Google Scholar 

  62. C.W. Cody, D.C. Prasher, V.M. Welstler, F.G. Prendergast, W.W. Ward, Chemical structure of the hexapeptide chromophore of the Aequorea green fluorescent protein. Biochemistry 32, 1212–1218 (1993).

    CAS  PubMed  Google Scholar 

  63. S.E. Ilyin, M.C. Flynn, C.R. Plata-Salaman, Fiber-optic monitoring coupled with confocal microscopy for imaging gene expression in vitro and in vivo. J. Neurosci. Methods 108, 91–96 (2001).

    CAS  PubMed  Google Scholar 

  64. K. Kelly, H. Alencar, M. Funovics, U. Mahmood, R. Weissleder, Detection of invasive colon cancer using a novel, targeted, library-derived fluorescent peptide. Cancer Res. 64, 6247–6251 (2004).

    CAS  PubMed  Google Scholar 

  65. S.F. Stanziale, B.M. Stiles, A. Bhargava, S.A. Kerns, N. Kalakonda, Y. Fong, Oncolytic herpes simplex virus-1 mutant expressing green fluorescent protein can detect and treat peritoneal cancer. Hum. Gene Ther. 15, 609–618 (2004).

    CAS  PubMed  Google Scholar 

  66. S. Wack, A. Hajri, F. Heisel, M. Sowinska, C. Berger, M. Whelan, J. Marescaux, M. Aprahamian, Feasibility, sensitivity, and reliability of laser-induced fluorescence imaging of green fluorescent protein-expressing tumors in vivo. Mol. Ther. 7, 765–773 (2003).

    CAS  PubMed  Google Scholar 

  67. J.S. Burgos, M. Rosol, R.A. Moats, V. Khankaldyyan, D.B. Kohn, M.D. Nelson Jr., W.E. Laug, Time course of bioluminescent signal in orthotopic and heterotopic brain tumors in nude mice. Biotechniques 34, 1184–1188 (2003).

    CAS  PubMed  Google Scholar 

  68. T.J. Sweeney, V. Mailander, A.A. Tucker, A.B. Olomu, W. Zhang, Y. Cao, R.S. Negrin, C.H. Contag, Visualizing the kinetics of tumor-cell clearance in living animals. Proc. Natl. Acad. Sci. U S A 96, 12044–12049 (1999).

    CAS  PubMed  Google Scholar 

  69. C.H. Contag, D. Jenkins, P.R. Contag, R.S. Negrin, Use of reporter genes for optical measurements of neoplastic disease in vivo. Neoplasia 2, 41–52 (2000).

    CAS  PubMed  Google Scholar 

  70. P. Ray, A. De, J-J. Min, R.Y. Tsien, S.S. Gambhir, Imaging tri-fusion multimodality reporter gene expression in living subjects. Cancer Res. 64, 1323–1330 (2004).

    CAS  PubMed  Google Scholar 

  71. R. Weissleder, C.H. Tung, U. Mahmood, A. Bogdanov Jr., In vivo imaging of tumors with protease-activated near-infrared fluorescent probes. Nat. Biotechnol. 17, 375–378 (1999).

    CAS  PubMed  Google Scholar 

  72. C. Bremer, C.H. Tung, R. Weissleder, In vivo molecular target assessment of matrix metalloproteinase inhibition. Nat. Med. 7, 743–748 (2001).

    CAS  PubMed  Google Scholar 

  73. T. Jiang, E.S. Olson, Q.T. Nguyen, M. Roy, P.A. Jennings, R.Y. Tsien, Tumor imaging by means of proteolytic activation of cell-penetrating peptides. Proc. Natl. Acad. Sci. U S A 101, 17867–17872 (2004).

    CAS  PubMed  Google Scholar 

  74. D.M. Chudakov, V.V. Belousov, A.G. Zaraisky, V.V. Novoselov, D.B. Staroverov, D.B. Zorov, S. Lukyanov, K.A. Lukyanov, Kindling fluorescent proteins for precise in vivo photolabeling. Nat. Biotechnol. 21, 191–194 (2003).

    CAS  PubMed  Google Scholar 

  75. D.M. Chudakov, V.V. Verkhusha, D.B. Staroverov, E.A. Souslova, S. Lukyanov, K.A. Lukyanov, Photoswitchable cyan fluorescent protein for protein tracking. Nat. Biotechnol. 22, 1435–1439 (2004).

    CAS  PubMed  Google Scholar 

  76. P.G. Wilmann, J. Petersen, R.J. Devenish, M. Prescott, J. Rossjohn, Variations on the GFP Chromophore: a polypeptide fragmentation within the chromophore revealed in the 2.1-a crystal structure of a nonfluorescent chromoprotein from Anemonia sulcata. J. Biol. Chem. 280, 2401–2404 (2005).

    CAS  PubMed  Google Scholar 

  77. R. Ando, H. Mizuno, A. Miyawaki, Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting. Science 306, 1370–1373 (2004).

    CAS  PubMed  Google Scholar 

  78. K. Vintersten, C. Monetti, M. Gertsenstein, P. Zhang, L. Laszlo, S. Biechele, A. Nagy, Mouse in red: red fluorescent protein expression in mouse ES cells, embryos, and adult animals. Genesis 40, 241–246 (2004).

    CAS  PubMed  Google Scholar 

  79. K. Takeuchi, A. Sereemaspun, T. Inagaki, Y. Hakamata, T. Kaneko, T. Murakami, M. Takahashi, E. Kobayashi, S. Ookawara, Morphologic characterization of green fluorescent protein in embryonic, neonatal, and adult transgenic rats. Anat. Rec. A Discov. Mol. Cell Evol. Biol. 274, 883–886 (2003).

    PubMed  Google Scholar 

  80. Y. Sato, Y. Igarashi, Y. Hakamata, T. Murakami, T. Kaneko, M. Takahashi, N. Seo, E. Kobayashi, Establishment of Alb-DsRed2 transgenic rat for liver regeneration research. Biochem. Biophys. Res. Commun. 311, 478–481 (2003).

    CAS  PubMed  Google Scholar 

  81. M. Stroh, J.P. Zimmer, D.G. Duda, T.S. Levchenko, K.S. Cohen, E.B. Brown, D.T. Scadden, V.P. Torchilin, M.G. Bawendi, D. Fukumura, R.K. Jain, Quantum dots spectrally distinguish multiple species within the tumor milieu in vivo. Nat. Med. 11, 678–682 (2005).

    Google Scholar 

  82. N.C. Shaner, R.E. Campbell, P.A. Steinbach, B.N. Giepmans, A.E. Palmer, R.Y. Tsien, Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. Red fluorescent protein. Nat. Biotechnol. 22, 1567–1572 (2004).

    CAS  PubMed  Google Scholar 

  83. X. Gao, L. Yang, J.A. Petros, F.F. Marshall, J.W. Simons, S. Nie, In vivo molecular and cellular imaging with quantum dots. Curr. Opin. Biotechnol. 16(1), 63–72 (2005).

    CAS  PubMed  Google Scholar 

  84. J. Lovric, H.S. Bazzi, Y. Cuie, G.R. Fortin, F.M. Winnik, D. Maysinger, Differences in subcellular distribution and toxicity of green and red emitting CdTe quantum dots. J. Mol. Med. 83(5), 377–385 (2005).

    PubMed  Google Scholar 

  85. A. Shiohara, A. Hoshino, K. Hanaki, K. Suzuki, K. Yamamoto, On the cyto-toxicity caused by quantum dots. Microbiol. Immunol. 48(9), 669–675 (2004).

    CAS  PubMed  Google Scholar 

  86. E.B. Voura, J.K. Jaiswal, H. Mattoussi, S.M. Simon, Tracking metastatic tumor cell extravasation with quantum dot nanocrystals and fluorescence emission-scanning microscopy. Nat. Med. 10(9), 993–998 (2004).

    CAS  PubMed  Google Scholar 

  87. J.W. Sturm, R. Magdeburg, K. Berger, B. Petruch, S. Samel, R. Bonninghoff, M. Keese, M. Hafner, S. Post, Influence of TNFA on the formation of liver metastases in a syngeneic mouse model. Int. J. Cancer 107, 11–21 (2003).

    CAS  PubMed  Google Scholar 

  88. C.A. Schmitt, J.S. Fridman, M. Yang, E. Baranov, R.M. Hoffman, S.W. Lowe, Dissecting p53 tumor suppressor functions in vivo. Cancer Cell 1, 289–298 (2002).

    CAS  PubMed  Google Scholar 

  89. C.A. Schmitt, J.S. Fridman, M. Yang, S. Lee, E. Baranov, R.M. Hoffman, S.W. Lowe, Senescence program controlled by p53 and p16INK4a contributes to the outcome of cancer therapy. Cell 109, 335–346 (2002).

    CAS  PubMed  Google Scholar 

  90. V. Bobek, K. Kolostova, D. Pinterov, M. Boubelik, P. Jiang, M. Yang, R.M. Hoffman, Syngeneic lymph-node-targeting model of green fluorescent protein-expressing Lewis lung carcinoma. Clin. Exp. Metastasis 21, 705–708 (2004).

    CAS  PubMed  Google Scholar 

  91. G.N. Naumov, S.M. Wilson, I.C. MacDonald, E.E. Schmidt, V.L. Morris, A.C. Groom, R.M. Hoffman, A.F. Chambers, Cellular expression of green fluorescent protein, coupled with high-resolution in vivo videomicroscopy, to monitor steps in tumor metastasis. J. Cell Sci. 112, 1835–1842 (1999).

    CAS  PubMed  Google Scholar 

  92. K.L. Farina, J.B. Wyckoff, J. Rivera, H. Lee, J.E. Segall, J.S. Condeelis, J.G. Jones, Cell motility of tumor cells visualized in living intact primary tumors using green fluorescent protein. Cancer Res. 58, 2528–2532 (1998).

    CAS  PubMed  Google Scholar 

  93. J-Y. Lu, H.C. Chen, R.Y. Chu, T.C. Lin, P.I. Hsu, M.S. Huang, C.J. Tseng, M. Hsiao, Establishment of red fluorescent protein-tagged HeLa tumor metastasis models: determination of DsRed2 insertion effects and comparison of metastatic patterns after subcutaneous, intraperitoneal, or intravenous injection. Clin. Exp. Metastasis 20, 121–133 (2003).

    CAS  PubMed  Google Scholar 

  94. Y. Amoh, L. Li, K. Katsuoka, S. Penman, R.M. Hoffman, Multipotent nestin-positive, keratin-negative hair-follicle-bulge stem cells can form neurons. Proc. Natl. Acad. Sci. U S A 102, 5530–5534 (2005).

    CAS  PubMed  Google Scholar 

  95. M.A. Funovics, H. Alencar, H.S. Su, K. Khazaie, R. Weissleder, U. Mahmood, Miniaturized multichannel near infrared endoscope for mouse imaging. Mol. Imag. 2, 350–357 (2003).

    Google Scholar 

  96. T. Fukada, K. Inoue, T. Urano, K. Sugimoto, Visualization of chromosomes and nuclear envelope in living cells for molecular dynamics studies. Biotechniques 37, 552–556 (2004).

    CAS  PubMed  Google Scholar 

  97. W. Denk, J.H. Strickler, W.W. Webb, Two-photon laser scanning fluorescence microscopy. Science 248, 73–76 (1990).

    CAS  PubMed  Google Scholar 

  98. J. Condeelis, J.E. Segall, Intravital imaging of cell movement in tumours. Nat. Rev. Cancer 3, 921–930 (2003).

    CAS  PubMed  Google Scholar 

  99. S. Hasegawa, M. Yang, T. Chishima, Y. Miyagi, H. Shimada, A.R. Moossa, R.M. Hoffman, In vivo tumor delivery of the green fluorescent protein gene to report future occurrence of metastasis. Cancer Gene Ther. 7, 1336–1340 (2000).

    CAS  PubMed  Google Scholar 

  100. K. Kaneko, M. Yano, T. Yamano, T. Tsujinaka, H. Miki, Y. Akiyama, M. Taniguchi, Y. Fujiwara, Y. Doki, M. Inoue, H. Shiozaki, Y. Kaneda, M. Monden, Detection of peritoneal micrometastases of gastric carcinoma with green fluorescent protein and carcinoembryonic antigen promoter. Cancer Res 61, 5570–5574 (2001).

    CAS  PubMed  Google Scholar 

  101. Y. Sato, N. Yamauchi, M. Takahashi, K. Sasaki, J. Fukaura, H. Neda, S. Fujii, M. Hirayama, Y. Itoh, Y. Koshita, K. Kogawa, J. Kato, S. Sakamaki, Y. Niitsu, In vivo gene delivery to tumor cells by transferrin–streptavidin–DNA conjugate. FASEB J 14, 2108–2118 (2000).

    CAS  PubMed  Google Scholar 

  102. N. Varda-Bloom, A. Shaish, A. Gonen, K. Levanon, S. Greenbereger, S. Ferber, H. Levkovitz, D. Castel, I. Goldberg, A. Afek, Y. Kopolovitc, D. Harats, Tissue-specific gene therapy directed to tumor angiogenesis. Gene Ther. 8, 819–827 (2001).

    CAS  PubMed  Google Scholar 

  103. H. Kishimoto, M. Zhao, K. Hayashi, Y. Urata, N. Tanaka, T. Fujiwara, S. Penman, R.M. Hoffman, In vivo internal tumor illumination by telomerase-dependent adenoviral GFP for precise surgical navigation. Proc. Natl. Acad. Sci. USA 106, 14514–14517 (2009).

    CAS  PubMed  Google Scholar 

  104. B.R. Jasny. Green surgery. Science 325, 1321 (2009).

    Google Scholar 

  105. D. Shcherbo, E.M. Merzlyak, T.V. Chepurnykh, A.F. Fradkov, G.V. Ermakova, E.A. Solovieva, K.A. Lukyanov, E.A. Bogdanova, A.G. Zaraisky, S. Lukyanov, D.M. Chudakov. Bright far-red fluorescent protein for whole-body imaging. Nature Methods 4, 741–746 (2007).

    CAS  PubMed  Google Scholar 

  106. R.M. Hoffman, A better fluorescent protein for whole-body imaging. Trends Biotechnol 26, 1–4 (2008).

    CAS  PubMed  Google Scholar 

  107. A. Sakaue-Sawano, H. Kurokawa, T. Morimura, A. Hanyu, H. Hama, H. Osawa, S. Kashiwagi, K. Fukami, T. Miyata, H. Miyoshi, T. Imamura, M. Ogawa, H. Masai, A. Miyawaki, Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 132, 487–498 (2008).

    CAS  PubMed  Google Scholar 

  108. J. Livet, T.A. Weissman, H. Kang, R.W. Draft, J. Lu, R.A. Bennis, J.R. Sanes, J.W. Lichtman, Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450, 56–63 (2007).

    CAS  PubMed  Google Scholar 

  109. O. Shimomura, Discovery of Green Fluorescent Protein (GFP) (Nobel Lecture). Angew. Chem. Int. Ed. 48, 5590–5602 (2009).

    CAS  Google Scholar 

  110. M. Chalfie, GFP: Lighting up life (Nobel Lecture). Angew. Chem. Int. Ed. 48, 5603–5611 (2009).

    CAS  Google Scholar 

  111. R.Y. Tsien, Constructing and exploiting the fluorescent protein paintbox (Nobel Lecture). Angew. Chem. Int. Ed. 48, 5612–5626 (2009).

    CAS  Google Scholar 

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  1. AntiCancer, Inc, San Diego, CA, 92111, USA

    Robert M. Hoffman

  2. Department of Surgery, University of California, San Diego, CA, 92103, USA

    Robert M. Hoffman

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    Chris D. Geddes

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Hoffman, R.M. (2010). Multicolor Imaging with Fluorescent Proteins in Mice. In: Geddes, C.D. (eds) Reviews in Fluorescence 2008. Reviews in Fluorescence 2008, vol 2008. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-1260-2_11

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