Clinically-relevent orthotopic metastatic models of pancreatic cancer imageable with fluorescent genetic reporters

Minerva Chirurgica

Volumn 64, Issue 5, 2009, Pages 521-539

  Bouvet, M ^a   Hoffman, R M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ANTICANCER INC   (United States)

Author keywords

Cyan fluorescent protein; Green fluorescent proteins; Mice, nude; Pancreas; Pancreatic neoplasm; Red fluorescent protein

Indexed keywords

PHOTOPROTEIN;

ANIMAL; ARTICLE; BIOSYNTHESIS; CANCER TRANSPLANTATION; CHEMISTRY; DISEASE MODEL; GENETICS; HUMAN; METASTASIS; MOUSE; NUDE MOUSE; PANCREAS TUMOR; PATHOLOGY; SENSITIVITY AND SPECIFICITY;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; LUMINESCENT PROTEINS; MICE; MICE, NUDE; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; PANCREATIC NEOPLASMS; SENSITIVITY AND SPECIFICITY;

EID: 77249150173     PISSN: 00264733     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (79)

1. Bouvet M, Gamagami RA, Gilpin EA, Romeo O, Sasson A, Easter DW et al. Factors influencing survival after resection for periampullary neoplasms. Am J Surg 2000;180:13-7.
2. Katz MH, Bouvet M, Al-Refaie W, Gilpin EA, Moossa AR. Non-pancreatic periampullary adenocarcinomas: an explanation for favorable prognosis. Hepatogastroente-rology 2004;51:842-6.
3. Bouvet M, Binmoeller KF, Moossa AR. Diagnosis of adenocarcinoma of the pancreas. In: Cameron JL, editor. American Cancer Society Atlas of Clinical Oncology: pancreatic cancer. Hamilton, ON: BC Decker; 2001.
4. Moossa AR, Bouvet M, Gamagami R. The pancreas. In: Cuschieri A, Steele RJC, Moossa AR, editors. Essential surgical practice. 4th ed. London: Arnold Publishing; 2002. p. 477-525.
5. Katz MH, Savides TJ, Moossa AR, Bouvet M. An evidence-based approach to the diagnosis and staging of pancreatic cancer. Pancreatology 2005;5:576-90.
6. Bouvet M, Yang M, Nardin S, Wang X, Jiang P, Baranov E et al. Chronologically-specific metastatic targeting of human pancreatic tumors in orthotopic models. Clin Exp Metastasis 2000;18:213-8.
7. Bouvet M, Wang J, Nardin SR, Nassirpour R, Yang M, Baranov E et al. Real-time optical imaging of primary tumor growth and multiple metastatic events in a pancreatic cancer orthotopic model. Cancer Res 2002;62:1534-40.
8. Marincola FM, Drucker BJ, Siao DY, Hough KL, Holder WD Jr. The nude mouse as a model for the study of human pancreatic cancer. J Surg Res 1989;47:520-9.
9. Bruns CJ, Harbison MT, Kuniyasu H, Eue I, Fidler IJ. In vivo selection and characterization of metastatic variants from human pancreatic adenocarcinoma by using orthotopic implantation in nude mice. Neoplasia 1999; 1:50-62.
10. Vezeridis MP, Doremus CM, Tibbetts LM, Tzanakakis G, Jackson BT. Invasion and metastasis following orthotopic transplantation of human pancreatic cancer in the nude mouse. J Surg Oncol 1989;40:261-5.
11. Fu X, Guadagni F, Hoffman RM. A metastatic nude-mouse model of human pancreatic cancer constructed orthotopically with histologically intact patient specimens. Proc Natl Acad Sci U S A 1992;89:5645-9.
12. An Z, Wang X, Kubota T, Moossa AR, Hoffman RM. A clinical nude mouse metastatic model for highly malignant human pancreatic cancer. Anticancer Res 1996;16:627-31.
13. Furukawa T, Kubota T, Watanabe M, Kitajima M, Hoffman RM. A novel patient-like treatment model of human pancreatic cancer constructed using orthotopic transplantation of histologically intact human tumor tissue in nude mice. Cancer Res 1993;53:3070-2.
14. Kiguchi K, Kubota T, Aoki D, Udagawa Y, Yamanouchi S, Saga M et al. A patient-like orthotopic implantation nude mouse model of highly metastatic human ovarian cancer. Clin Exp Metastasis 1998;16:751-6.
15. Tomikawa M, Kubota T, Matsuzaki SW, Takahasi S, Kitajima M, Moossa AR et al. Mitomycin C and cisplatin increase survival in a human pancreatic cancer metastatic model. Anticancer Res 1997;17:3623-5.
16. Kyriazis AP, DiPersio L, Michael GJ, Pesce AJ, Stinnett JD. Growth patterns and metastatic behavior of human tumors growing in athymic mice. Cancer Res 1978;38:3186-90.
17. Fidler IJ. Critical factors in the biology of human cancer metastasis: twenty-eighth G.H.A. Clowes memorial award lecture. Cancer Res 1990;50:6130-8.
18. Fidler IJ. Rationale and methods for the use of nude mice to study the biology and therapy of human cancer metastasis. Cancer Metastasis Rev 1986;5:29-49.
19. Miller FR, Medina D, Heppner GH. Preferential growth of mammary tumors in intact mammary fatpads. Cancer Res 1981;41:3863-7.
20. Sordat B, Wang WR. Human colorectal tumor xenografts in nude mice: expression of malignancy. Behring Inst Mitt 1984;(74):291-300.
21. Morikawa K, Walker SM, Nakajima M, Pathak S, Jessup JM, Fidler IJ. Influence of organ environment on the growth, selection, and metastasis of human colon carcinoma cells in nude mice. Cancer Res 1988;48: 6863-71.
22. Hoffman RM. Orthotopic metastatic mouse models for anticancer drug discovery and evaluation: a bridge to the clinic. Invest New Drugs 1999;17:343-59.
23. Tan MH, Chu TM. Characterization of the tumorigenic and metastatic properties of a human pancreatic tumor cell line (AsPC-1) implanted orthotopically into nude mice. Tumour Biol 1985;6:89-98.
24. US Patents 5, 284 and 5,569,812 Reissue RE:39,337.
25. Lin WC, Pretlow TP, Pretlow TG 2nd, Culp LA. Bacterial lacZ gene as a highly sensitive marker to detect micrometastasis formation during tumor progression. Cancer Res 1990;50:2808-17.
26. Fukumura D, Yuan F, Monsky WL, Chen Y, Jain RK. Effect of host microenvironment on the microcirculation of human colon adenocarcinoma. Am J Pathol 1997;151:679-88.
27. Chambers AF, MacDonald IC, Schmidt EE, Koop S, Morris VL, Khokha R et al. Steps in tumor metastasis: new concepts from intravital videomicroscopy. Cancer Metastasis Rev 1995;14:279-301.
28. Weissleder R, Tung CH, Mahmood U, Bogdanov A Jr. In vivo imaging of tumors with protease-activated near-infrared fluorescent probes. Nat Biotechnol 1999;17: 375-8.
29. Sweeney TJ, Mailander V, Tucker AA, Olomu AB, Zhang W, Cao Y et al. Visualizing the kinetics of tumor-cell clearance in living animals. Proc Natl Acad Sci U S A 1999;96:12044-9.
30. Cheng L, Fu J, Tsukamoto A, Hawley RG. Use of green fluorescent protein variants to monitor gene transfer and expression in mammalian cells. Nat Biotechnol 1996;14:606-9.
31. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC. Green fluorescent protein as a marker for gene expression. Science 1994;263:802-5.
32. Astoul P, Colt HG, Wang X, Hoffman RM. A "patientlike" nude mouse model of parietal pleural human lung adenocarcinoma. Anticancer Res 1994;14:85-91.
33. Yang F, Moss LG, Phillips GN Jr. The molecular structure of green fluorescent protein. Nat Biotechnol 1996;14:1246-51.
34. Prasher DC, Eckenrode VK, Ward WW, Prendergast FG, Cormier MJ. Primary structure of the Aequorea victoria green-fluorescent protein. Gene 1992;111: 229-33.
35. Zolotukhin S, Potter M, Hauswirth WW, Guy J, Muzyczka N. A "humanized" green fluorescent protein cDNA adapted for high-level expression in mammalian cells. J Virol 1996;70:4646-54.
36. Heim R, Cubitt AB, Tsien RY. Improved green fluorescence. Nature 1995;373:663-4.
37. Delagrave S, Hawtin RE, Silva CM, Yang MM, Youvan DC. Red-shifted excitation mutants of the green fluorescent protein. Biotechnology (N Y) 1995;13:151-4.
38. Cormack BP, Valdivia RH, Falkow S. FACS-optimized mutants of the green fluorescent protein (GFP). Gene 1996;173:33-8.
39. Budinger TF, Benaron DA, Koretsky AP. Imaging transgenic animals. Annu Rev Biomed Eng 1999;1:611-48.
40. Flotte TR, Beck SE, Chesnut K, Potter M, Poirier A, Zolotukhin S. A fluorescence video-endoscopy technique for detection of gene transfer and expression. Gene Ther 1998;5:166-73.
41. Fu XY, Besterman JM, Monosov A, Hoffman RM. Models of human metastatic colon cancer in nude mice orthotopically constructed by using histologically intact patient specimens. Proc Natl Acad Sci U S A 1991;88:9345-9.
42. Sun FX, Sasson AR, Jiang P, An Z, Gamagami R, Li L et al. An ultra-metastatic model of human colon cancer in nude mice. Clin Exp Metastasis 1999;17:41-8.
43. Chishima T, Miyagi Y, Wang X, Yamaoka H, Shimada H, Moossa AR et al. Cancer invasion and micrometastasis visualized in live tissue by green fluorescent protein expression. Cancer Res 1997;57:2042-7.
44. Chishima T, Miyagi Y, Wang X, Baranov E, Tan Y, Shimada H et al. Metastatic patterns of lung cancer visualized live and in process by green fluorescence protein expression. Clin Exp Metastasis 1997;15:547-52.
45. Chishima T, Miyagi Y, Wang X, Tan Y, Shimada H, Moossa A et al. Visualization of the metastatic process by green fluorescent protein expression. Anticancer Res 1997;17:2377-84.
46. Chishima T, Miyagi Y, Li L, Tan Y, Baranov E, Yang M et al. Use of histoculture and green fluorescent protein to visualize tumor cell host interaction [letter]. In Vitro Cell Dev Biol Anim 1997;33:745-7.
47. Chishima T, Yang M, Miyagi Y, Li L, Tan Y, Baranov E et al. Governing step of metastasis visualized in vitro. Proc Natl Acad Sci U S A 1997;94:11573-6.
48. Yang M, Hasegawa S, Jiang P, Wang X, Tan Y, Chishima T et al. Widespread skeletal metastatic potential of human lung cancer revealed by green fluorescent protein expression. Cancer Res 1998;58:4217-21.
49. Yang M, Jiang P, Sun FX, Hasegawa S, Baranov E, Chishima T et al. A fluorescent orthotopic bone metastasis model of human prostate cancer. Cancer Res 1999;59:781-6.
50. Yang M, Jiang P, An Z, Baranov E, Li L, Hasegawa S et al. Genetically fluorescent melanoma bone and organ metastasis models. Clin Cancer Res 1999;5:3549-59.
51. Yang M, Baranov E, Jiang P, Sun FX, Li XM, LI L et al. Whole-body optical imaging of green fluorescent protein-expressing tumors and metastases. Proc Natl Acad Sci U S A 2000;97:1206-11.
52. Yang M, Baranov E, Moossa AR, Penman S, Hoffman RM. Visualizing gene expression by whole-body fluorescence imaging. Proc Natl Acad Sci U S A 2000;97:12278-82.
53. Yang M, Baranov E, Li XM, Wang JW, Jiang P, Li L et al. Whole-body and intravital optical imaging of angiogenesis in orthotopically implanted tumors. Proc Natl Acad Sci U S A 2001;98:2616-21.
54. Yang M, Baranov E, Wang JW, Jiang P, Wang X, Sun FX et al. 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 2002;99:3824-9.
55. Hoffman RM. The multiple uses of fluorescent proteins to visualize cancer in vivo. Nat Rev Cancer 2005;5:796-806.
56. Katz MH, Takimoto S, Spivack D, Moossa AR, Hoffman RM, Bouvet M. A novel red fluorescent protein orthotopic pancreatic cancer model for the preclinical evaluation of chemotherapeutics. J Surg Res 2003;113:151-60.
57. Katz MH, Spivack DE, Takimoto S, Fang B, Burton DW, Moossa AR et al. Gene therapy of pancreatic cancer with green fluorescent protein and tumor necrosis factor-related apoptosis-inducing ligand fusion gene expression driven by a human telomerase reverse transcriptase promoter. Ann Surg Oncol 2003;10:762-72.
58. Katz MH, Takimoto S, Spivack D, Moossa AR, Hoffman RM, Bouvet M. An imageable highly metastatic orthotopic red fluorescent protein model of pancreatic cancer. Clin Exp Metastasis 2004;21:7-12.
59. Tsuji K, Yang M, Jiang P, Maitra A, Kaushal S, Yamauchi K et al. Common bile duct injection as a novel method for establishing red fluorescent protein (RFP)-expressing human pancreatic cancer in nude mice. JOP 2006;7:193-9.
60. Bouvet M, Spernyak J, Katz MH, Mazurchuk RV, Takimoto S, Bernacki R et al. High correlation of whole-body red fluorescent protein imaging and magnetic resonance imaging on an orthotopic model of pancreatic cancer. Cancer Res 2005;65:9829-33.
61. Katz MH, Bouvet M, Takimoto S, Spivack D, Moossa AR, Hoffman RM. Selective antimetastatic activity of cytosine analog CS-682 in a red fluorescent protein orthotopic model of pancreatic cancer. Cancer Res 2003;63:5521-5.
62. Katz MH, Bouvet M, Takimoto S, Spivack D, Moossa AR, Hoffman RM. Survival efficacy of adjuvant cytosine-analogue CS-682 in a fluorescent orthotopic model of human pancreatic cancer. Cancer Res 2004;64:1828-33.
63. Amoh Y, Li L, Tsuji K, Moossa AR, Katsuoka K, Hoffman RM et al. Dual-color imaging of nascent blood vessels vascularizing pancreatic cancer in an orthotopic model demonstrates antiangiogenesis efficacy of gemcitabine. J Surg Res 2006;132:164-9.
64. Amoh Y, Nagakura C, Maitra A, Moossa AR, Katsuoka K, Hoffman RM et al. Dual-color imaging of nascent angiogenesis and its inhibition in liver metastases of pancreatic cancer. Anticancer Res 2006;26:3237-42.
65. 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: 14259-62.
66. Saito N, Zhao M, Li L, Baranov E, Yang M, Ohta Y et al. High efficiency genetic modification of hair follicles and growing hair shafts. Proc Natl Acad Sci U S A 2002;99:13120-4.
67. Lee NC, Bouvet M, Nardin S, Jiang P, Baranov E, Rashidi B et al. Antimetastatic efficacy of adjuvant gemcitabine in a pancreatic cancer orthotopic model. Clin Exp Metastasis 2000;18:379-84.
68. Hoffman RM, Yang M. Whole-body imaging with fluorescent proteins. Nat Protoc 2006;1:1429-38.
69. Yang M, Jiang P, Hoffman RM. Whole-body subcellular multicolor imaging of tumor-host interaction and drug response in real time. Cancer Res 2007;67: 5195-200.
70. Makale M, McElroy M, O'Brien P, Hoffman RM, Guo S, Bouvet M et al. Extended-working-distance multiphoton micromanipulation microscope for deep-penetration imaging in live mice and tissue. J Biomed Opt 2009;14:024032.
71. Snyder CS, Kaushal S, Kono Y, Iran Cao HS, Hoffman RM, Bouvet M. Complementarity of ultrasound and fluorescence imaging in an orthotopic mouse model of pancreatic cancer. BMC Cancer 2009;9:106.
72. Nagakura C, Hayashi K, Zhao M, Yamauchi K, Yamamoto N, Tsuchiya H et al. Efficacy of a Genetically-modified Salmonella typhimurium in an Orthotopic Human Pancreatic Cancer in Nude Mice. Anticancer Res 2009;29:1873-8.
73. Zhao M, Geller J, Ma H, Yang M, Penman S, Hoffman RM. Monotherapy with a tumor-targeting mutant of Salmonella typhimurium cures orthotopic metastatic mouse models of human prostate cancer. Proc Natl Acad Sci U S A 2007;104:10170-4.
74. Zhao M, Yang M, Li XM, Jiang P, Baranov E, Li S et al. Tumor-targeting bacterial therapy with amino acid auxotrophs of GFP-expressing Salmonella typhimurium. Proc Natl Acad Sci U S A 2005;102:755-60.
75. Zhao M, Yang M, Ma H, U X, Tan X, Li S et al. Targeted therapy with a Salmonella typhimurium leucine-arginine auxotroph cures orthotopic human breast tumors in nude mice. Cancer Res 2006;66:7647-52.
76. Yam C, Zhao M, Hayashi K, Ma H, Kishimoto H, McElroy M et al. Monotherapy with a tumor-targeting mutant of S. typhimurium inhibits liver metastasis in a mouse model of pancreatic cancer. J Surg Res 2009 [In press].
77. Hadjantonakis AK, Macmaster S, Nagy A. Embryonic stem cells and mice expressing different GFP variants for multiple non-invasive reporter usage within a single animal. BMC Biotechnol 2002;2:11.
78. Tran Cao HS, Kimura H, Kaushal S, Snyder CS, Reynoso J, Hoffman RM et al. The cyan fluorescent protein (CFP) transgenic mouse as a model for imaging pancreatic exocrine cells. JOP 2009;10:152-6.
79. Tran Cao HS, Reynoso J, Yang M, Kimura H, Kaushal S, Snyder CS et al. Development of the transgenic cyan fluorescent protein (CFP)-expressing nude mouse for "Technicolor" cancer imaging. J Cell Biochem 2009; 107:328-34.