Advances in imaging mouse tumour models in vivo

Journal of Pathology

Volumn 205, Issue 2, 2005, Pages 194-205

  Lyons, Scott K ^a  

^a Xenogen Corporation   (United States)

Author keywords

Imaging; Mouse model; Non invasive; Tumour

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; BIOLUMINESCENCE; COMPUTER; COMPUTER ASSISTED TOMOGRAPHY; DISEASE ACTIVITY; DISEASE MODEL; ECHOGRAPHY; FLUORESCENCE ANALYSIS; GENE EXPRESSION; IMAGE QUALITY; IMAGING SYSTEM; IN VITRO STUDY; IN VIVO STUDY; INTERMETHOD COMPARISON; MALIGNANT NEOPLASTIC DISEASE; METHODOLOGY; MICROSCOPY; MONITORING; MOUSE; NON INVASIVE MEASUREMENT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REPORTER GENE; REVIEW; SENSITIVITY AND SPECIFICITY; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; TRANSGENE; TREATMENT OUTCOME;

ANIMALS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, NEOPLASTIC; LUMINESCENT MEASUREMENTS; MAGNETIC RESONANCE IMAGING; MICE; NEOPLASMS, EXPERIMENTAL; TOMOGRAPHY, EMISSION-COMPUTED; TRANSGENES;

EID: 13644251904     PISSN: 00223417     EISSN: None     Source Type: Journal    
DOI: 10.1002/path.1697     Document Type: Review

References (94)

1. Aguirre AJ, Bardeesy N, Sinha M, et al. Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma. Genes Dev 2003; 17: 3112-3126.
2. Krimpenfort P, Quon KC, Mooi WJ, Loonstra A, Berns A. Loss of p16Ink4a confers susceptibility to metastatic melanoma in mice. Nature 2001; 413: 83-86.
3. Wang S, Gao J, Lei Q, et al. Prostate-specific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer. Cancer Cell 2003; 4: 209-221.
4. Artandi SE, Chang S, Lee SL, et al. Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice. Nature 2000; 406: 641-645.
5. Douma S, Van Laar T, Zevenhoven J, Meuwissen R, Van Garderen E, Peeper DS. Suppression of anoikis and induction of metastasis by the neurotrophic receptor TrkB. Nature 2004; 430: 1034-1039.
6. Bergers G, Javaherian K, Lo KM, Folkman J, Hanahan D. Effects of angiogenesis inhibitors on multistage carcinogenesis in mice. Science 1999; 284: 808-812.
7. Satchi-Fainaro R, Puder M, Davies JW, et al. Targeting angiogenesis with a conjugate of HPMA copolymer and TNP-470. Nature Med 2004; 10: 255-261.
8. Shah NP, Tran C, Lee FY, Chen P, Norris D, Sawyers CL. Overriding imatinib resistance with a novel ABL kinase inhibitor. Science 2004; 305: 399-401.
9. Romer JT, Kimura H, Magdaleno S, et al. Suppression of the Shh pathway using a small molecule inhibitor eliminates medulloblastoma in Ptc1(+/-) p53(-/-) mice. Cancer Cell 2004; 6 229-240.
10. Schmitt CA, Fridman JS, Yang M, Baranov E, Hoffman RM, Lowe SW. Dissecting p53 tumor suppressor functions in vivo. Cancer Cell 2002; 1: 289-298.
11. Wendel HG, De Stanchina E, Fridman JS, et al. Survival signalling by Akt and eIF4E in oncogenesis and cancer therapy. Nature 2004; 428: 332-337.
12. Weissleder R. Scaling down imaging: molecular mapping of cancer in mice. Nature Rev Cancer 2002; 2: 11-18.
13. Massoud TF, Gambhir SS. Molecular imaging in living subjects: seeing fundamental biological processes in a new light. Genes Dev 2003; 17: 545-580.
14. Goertzen AL, Meadors AK, Silverman RW, Cherry SR. Simultaneous molecular and anatomical imaging of the mouse in vivo. Phys Med Biol 2002; 47: 4315-4328.
15. Rehemtulla A, Hall DE, Stegman LD, et al. Molecular imaging of gene expression and efficacy following adenoviral-mediated brain tumor gene therapy. Mol Imaging 2002; 1: 43-55.
16. Ray P, De A, Min JJ, Tsien RY, Gambhir SS. Imaging tri-fusion multimodality reporter gene expression in living subjects. Cancer Res 2004; 64: 1323-1330.
17. Ponomarev V, Doubrovin M, Serganova I, et al. A novel triple-modality reporter gene for whole-body fluorescent, bioluminescent, and nuclear noninvasive imaging. Eur J Nucl Med Mol Imaging 2004; 31: 740-751.
18. Ichikawa T, Hogemann D, Saeki Y, et al. MRI of transgene expression: correlation to therapeutic gene expression. Neoplasia 2002; 4: 523-530.
19. Tung CH, Zeng Q, Shah K, Kim DE, Schellingerhout D, Weissleder R. In vivo imaging of beta-galactosidase activity using far red fluorescent switch. Cancer Res 2004; 64: 1579-1583.
20. Louie AY, Huber MM, Ahrens ET, et al. In vivo visualization of gene expression using magnetic resonance imaging. Nature Biotechnol 2000; 18: 321-325.
21. Jenkins DE, Oei Y, Hornig YS, et al. Bioluminescent imaging (BLI) to improve and refine traditional murine models of tumor growth and metastasis. Clin Exp Metastasis 2003; 20: 733-744.
22. Yang M, Li L, Jiang P, Moossa AR, Penman S, Hoffman RM. Dual-color fluorescence imaging distinguishes tumor cells from induced host angiogenic vessels and stromal cells. Proc Natl Acad Sci U S A 2003; 100: 14259-14262.
23. Adams JY, Johnson M, Sato M, et al. Visualization of advanced human prostate cancer lesions in living mice by a targeted gene transfer vector and optical imaging. Nature Med 2002; 8: 891-897.
24. Vooijs M, Jonkers J, Lyons S, Berns A. Noninvasive imaging of spontaneous retinoblastoma pathway-dependent tumors in mice. Cancer Res 2002; 62: 1862-1867.
25. Serganova I, Doubrovin M, Vider J, et al. Molecular imaging of temporal dynamics and spatial heterogeneity of hypoxia-inducible factor-1 signal transduction activity in tumors in living mice. Cancer Res 2004; 64: 6101-6108.
26. Doubrovin M, Ponomarev V, Beresten T, et al. Imaging transcriptional regulation of p53-dependent genes with positron emission tomography in vivo. Proc Natl Acad Sci U S A 2001; 98: 9300-9305.
27. Iyer M, Wu L, Carey M, Wang Y, Smallwood A, Gambhir SS. Two-step transcriptional amplification as a method for imaging reporter gene expression using weak promoters. Proc Natl Acad Sci U S A 2001; 98: 14595-14600.
28. Sato M, Johnson M, Zhang L, et al. Optimization of adenoviral vectors to direct highly amplified prostate-specific expression for imaging and gene therapy. Mol Ther 2003; 8: 726-737.
29. Iyer M, Salazar FB, Lewis X, et al. Noninvasive imaging of enhanced prostate-specific gene expression using a two-step transcriptional amplification-based lentivirus vector. Mol Ther 2004; 10: 545-552.
30. Ray S, Paulmurugan R, Hildebrandt I, et al. Novel bidirectional vector strategy for amplification of therapeutic and reporter gene expression. Hum Gene Ther 2004; 15: 681-690.
31. Lyons SK, Meuwissen R, Krimpenfort P, Berns A. The generation of a conditional reporter that enables bioluminescence imaging of Cre/loxP-dependent tumorigenesis in mice. Cancer Res 2003; 63 7042-7046.
32. Jonkers J, Berns A. Conditional mouse models of sporadic cancer. Nature Rev Cancer 2002; 2: 251-265.
33. Sundaresan G, Paulmurugan R, Berger F, et al. MicroPET imaging of Cre-loxP-mediated conditional activation of a herpes simplex virus type 1 thymidine kinase reporter gene. Gene Ther 2004; 11 609-618.
34. Laxman B, Hall DE, Bhojani MS, et al. Noninvasive real-time imaging of apoptosis. Proc Natl Acad Sci U S A 2002; 99: 16551-16555.
35. Luker GD, Pica CM, Song J, Luker KE, Piwnica-Worms D. Imaging 26S proteasome activity and inhibition in living mice. Nature Med 2003; 9: 969-973.
36. Zhang GJ, Safran M, Wei W, et al. Bioluminescent imaging of Cdk2 inhibition in vivo. Nature Med 2004; 10: 643-648.
37. Luker GD, Sharma V, Pica CM, et al. Noninvasive imaging of protein - protein interactions in living animals. Proc Natl Acad Sci U S A 2002; 99: 6961-6966.
38. Luker GD, Sharma V, Pica CM, Prior JL, Li W, Piwnica-Worms D. Molecular imaging of protein-protein interactions: controlled expression of p53 and large T-antigen fusion proteins in vivo. Cancer Res 2003; 63: 1780-1788.
39. Paulmurugan R, Umezawa Y, Gambhir SS. Noninvasive imaging of protein-protein interactions in living subjects by using reporter protein complementation and reconstitution strategies. Proc Natl Acad Sci U S A 2002; 99: 15608-15613.
40. Paulmurugan R, Massoud TF, Huang J, Gambhir SS. Molecular imaging of drug-modulated protein-protein interactions in living subjects. Cancer Res 2004; 64: 2113-2119.
41. Luker KE, Piwnica-Worms D. Optimizing luciferase protein fragment complementation for bioluminescent imaging of protein-protein interactions in live cells and animals. Methods Enzymol 2004; 385: 349-360.
42. Moffat BA, Reddy GR, McConville P, et al. A novel polyacrylamide magnetic nanoparticle contrast agent for molecular imaging using MRI. Mol Imaging 2003; 2: 324-332.
43. Moore A, Medarova Z, Potthast A, Dai G. In vivo targeting of underglycosylated MUC-1 tumor antigen using a multimodal imaging probe. Cancer Res 2004; 64: 1821-1827.
44. Artemov D, Mori N, Ravi R, Bhujwalla ZM. Magnetic resonance molecular imaging of the HER-2/neu receptor. Cancer Res 2003; 63 2723-2727.
45. Weissleder R, Moore A, Mahmood U, et al. In vivo magnetic resonance imaging of transgene expression. Nature Med 2000; 6: 351-355.
46. Ross BD, Moffat BA, Lawrence TS, et al. Evaluation of cancer therapy using diffusion magnetic resonance imaging. Mol Cancer Ther 2003; 2: 581-587.
47. Griffin JL, Shockcor JP. Metabolic profiles of cancer cells. Nature Rev Cancer 2004; 4: 551-561.
48. Mandl SJ, Mari C, Edinger M, et al. Multi-modality imaging identifies key times for annexin V imaging as an early predictor of therapeutic outcome. Mol Imaging 2004; 3: 1-8.
49. Janssen ML, Oyen WJ, Dijkgraaf I, et al. Tumor targeting with radiolabeled alpha(v)beta(3) integrin binding peptides in a nude mouse model. Cancer Res 2002; 62: 6146-6151.
50. Chen X, Liu S, Hou Y, et al. MicroPET imaging of breast cancer alpha(v)-integrin expression with (64)Cu-labeled dimeric RGD peptides. Mol Imaging Biol 2004; 6: 350-359.
51. Smith-Jones PM, Solit DB, Akhurst T, Afroze F, Rosen N, Larson SM. Imaging the pharmacodynamics of HER2 degradation in response to Hsp90 inhibitors. Nature Biotechnol 2004; 22: 701-706.
52. Visser GW, van der Wilt CL, Wedzinga R, Peters GJ, Herscheid JD. 18F-radiopharmacokinetics of [18F]-5-fluorouracil in a mouse bearing two colon tumors with a different 5-fluorouracil sensitivity: a study for a correlation with oncological results. Nucl Med Biol 1996; 23 333-342.
53. Collingridge DR, Carroll VA, Glaser M, et al. The development of [(124)I]iodinated-VG76e: a novel tracer for imaging vascular endothelial growth factor in vivo using positron emission tomography. Cancer Res 2002; 62: 5912-5919.
54. Gambhir SS, Bauer E, Black ME, et al. A mutant herpes simplex virus type 1 thymidine kinase reporter gene shows improved sensitivity for imaging reporter gene expression with positron emission tomography. Proc Natl Acad Sci U S A 2000; 97: 2785-2790.
55. Gambhir SS, Barrio JR, Phelps ME, et al. Imaging adenoviral-directed reporter gene expression in living animals with positron emission tomography. Proc Natl Acad Sci U S A 1999; 96 2333-2338.
56. De A, Lewis XZ, Gambhir SS. Noninvasive imaging of lentiviral-mediated reporter gene expression in living mice. Mol Ther 2003; 7: 681-691.
57. Dubey P, Su H, Adonai N, et al. Quantitative imaging of the T cell antitumor response by positron-emission tomography. Proc Natl Acad Sci U S A 2003; 100: 1232-1237.
58. Koehne G, Doubrovin M, Doubrovina E, et al. Serial in vivo imaging of the targeted migration of human HSV-TK-transduced antigen-specific lymphocytes. Nature Biotechnol 2003; 21: 405-413.
59. Sharma V, Luker GD, Piwnica-Worms D. Molecular imaging of gene expression and protein function in vivo with PET and SPECT. J Magn Reson Imaging 2002; 16: 336-351.
60. Groot-Wassink T, Aboagye EO, Wang Y, Lemoine NR, Keith WN, Vassaux G. Noninvasive imaging of the transcriptional activities of human telomerase promoter fragments in mice. Cancer Res 2004; 64: 4906-4911.
61. Contag CH, Ross BD. It's not just about anatomy: in vivo bioluminescence imaging as an eyepiece into biology. J Magn Reson Imaging 2002; 16: 378-387.
62. Bhaumik S, Walls Z, Puttaraju M, Mitchell LG, Gambhir SS. Molecular imaging of gene expression in living subjects by spliceosome-mediated RNA trans-splicing. Proc Natl Acad Sci U S A 2004; 101: 8693-8698.
63. Massoud TF, Paulmurugan R, Gambhir SS. Molecular imaging of homodimeric protein-protein interactions in living subjects. FASEB J 2004; 18: 1105-1107.
64. Jenkins DE, Yu SF, Hornig YS, Purchio T, Contag PR. In vivo monitoring of tumor relapse and metastasis using bioluminescent PC-3M-luc-C6 cells in murine models of human prostate cancer. Clin Exp Metastasis 2003; 20: 745-756.
65. Rehemtulla A, Stegman LD, Cardozo SJ, et al. Rapid and quantitative assessment of cancer treatment response using in vivo bioluminescence imaging. Neoplasia 2000; 2: 491-495.
66. Bhaumik S, Gambhir SS. Optical imaging of Renilla luciferase reporter gene expression in living mice. Proc Natl Acad Sci U S A 2002; 99: 377-382.
67. Shah K, Tang Y, Breakefield X, Weissleder R. Real-time imaging of TRAIL-induced apoptosis of glioma tumors in vivo. Oncogene 2003; 22: 6865-6872.
68. Pichler A, Prior JL, Piwnica-Worms D. Imaging reversal of multidrug resistance in living mice with bioluminescence: MDR1 P-glycoprotein transports coelenterazine. Proc Natl Acad Sci U S A 2004; 101: 1702-1707.
69. Troy T, Jekic-McMullen D, Sambucetti L, Rice B. Quantitative comparison of the sensitivity of detection of fluorescent and bioluminescent reporters in animal models. Mol Imaging 2004; 3 9-23.
70. Schmitt CA, Fridman JS, Yang M, et al. A senescence program controlled by p53 and p16INK4a contributes to the outcome of cancer therapy. Cell 2002; 109: 335-346.
71. Joyce JA, Baruch A, Chehade K, et al. Cathepsin cysteine proteases are effectors of invasive growth and angiogenesis during multistage tumorigenesis. Cancer Cell 2004; 5: 443-453.
72. Yang M, Baranov E, Jiang P, et al. Whole-body optical imaging of green fluorescent protein-expressing tumors and metastases. Proc Natl Acad Sci U S A 2000; 97: 1206-1211.
73. Mahasreshti PJ, Kataram M, Wang MH, et al. Intravenous delivery of adenovirus-mediated soluble FLT-1 results in liver toxicity. Clin Cancer Res 2003; 9: 2701-2710.
74. Yamamoto N, Yang M, Jiang P, et al. Determination of clonality of metastasis by cell-specific color-coded fluorescent-protein imaging. Cancer Res 2003; 63: 7785-7790.
75. Fukumura D, Xavier R, Sugiura T, et al. Tumor induction of VEGF promoter activity in stromal cells. Cell 1998; 94: 715-725.
76. Ke S, Wen X, Gurfinkel M, et al. Near-infrared optical imaging of epidermal growth factor receptor in breast cancer xenografts. Cancer Res 2003; 63: 7870-7875.
77. Citrin D, Scott T, Sproull M, Menard C, Tofilon PJ, Camphausen K. In vivo tumor imaging using a near-infrared-labeled endostatin molecule. Int J Radiat Oncol Biol Phys 2004; 58: 536-541.
78. Kelly K, Alencar H, Funovics M, Mahmood U, Weissleder R. Detection of invasive colon cancer using a novel, targeted, library-derived fluorescent peptide. Cancer Res 2004; 64: 6247-6251.
79. Bremer C, Tung CH, Weissleder R. In vivo molecular target assessment of matrix metalloproteinase inhibition. Nature Med 2001; 7: 743-748.
80. Marten K, Bremer C, Khazaie K, et al. Detection of dysplastic intestinal adenomas using enzyme-sensing molecular beacons in mice. Gastroenterology 2002; 122: 406-414.
81. Messerli SM, Prabhakar S, Tang Y, et al. A novel method for imaging apoptosis using a caspase-1 near-infrared fluorescent probe. Neoplasia 2004; 6: 95-105.
82. Shah K, Tung CH, Chang CH, et al. In vivo imaging of HIV protease activity in amplicon vector-transduced gliomas. Cancer Res 2004; 64: 273-278.
83. Law B, Curino A, Bugge TH, Weissleder R, Tung CH. Design, synthesis, and characterization of urokinase plasminogen-activator-sensitive near-infrared reporter. Chem Biol 2004; 11: 99-106.
84. Larson DR, Zipfel WR, Williams RM, et al. Water-soluble quantum dots for multiphoton fluorescence imaging in vivo. Science 2003; 300: 1434-1436.
85. Ballou B, Lagerholm BC, Ernst LA, Bruchez MP, Waggoner AS. Noninvasive imaging of quantum dots in mice. Bioconjug Chem 2004; 15: 79-86.
86. Wu X, Liu H, Liu J, et al. Immunofluorescent labeling of cancer marker Her2 and other cellular targets with semiconductor quantum dots. Nature Biotechnol 2003; 21: 41-46.
87. Gao X, Cui Y, Levenson RM, Chung LW, Nie S. In vivo cancer targeting and imaging with semiconductor quantum dots. Nature Biotechnol 2004; 22: 969-976.
88. Akerman ME, Chan WC, Laakkonen P, Bhatia SN, Ruoslahti E. Nanocrystal targeting in vivo. Proc Natl Acad Sci U S A 2002; 99 12617-12621.
89. Kim S, Lim YT, Soltesz EG, et al. Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping. Nature Biotechnol 2004; 22: 93-97.
90. Graves EE, Weissleder R, Ntziachristos V. Fluorescence molecular imaging of small animal tumor models. Curr Mol Med 2004; 4: 419-430.
91. Ntziachristos V, Schellenberger EA, Ripoll J, et al. Visualization of antitumor treatment by means of fluorescence molecular tomography with an annexin V-Cy5.5 conjugate. Proc Natl Acad Sci U S A 2004; 101: 12294-12299.
92. Jain RK, Munn LL, Fukumura D. Dissecting tumour pathophysiology using intravital microscopy. Nature Rev Cancer 2002; 2: 266-276.
93. Condeelis J, Segall JE. Intravital imaging of cell movement in tumours. Nature Rev Cancer 2003; 3: 921-930.
94. Holland EC. Mouse models of human cancer as tools in drug development. Cancer Cell 2004; 6: 197-198.