Orthotopic metastatic mouse models for anticancer drug discovery and evaluation: A bridge to the clinic

Investigational New Drugs

Volumn 17, Issue 4, 1999, Pages 343-360

  Hoffman, Robert M ^a  

^a ANTICANCER INC   (United States)

Author keywords

Clinically relevant models; Green fluorescent protein; Immunodeficient mice; Metastasis; Surgical orthotopic implantation; Tumor imaging

Indexed keywords

ANTIMETASTATIC AGENT; ANTINEOPLASTIC AGENT; GREEN FLUORESCENT PROTEIN;

ARTICLE; BLADDER CANCER; BONE METASTASIS; BREAST CANCER; CANCER MODEL; CANCER TRANSPLANTATION; COLON CANCER; DRUG SCREENING; KIDNEY CANCER; LIVER METASTASIS; LUNG CANCER; LYMPH NODE METASTASIS; METASTASIS; METASTASIS POTENTIAL; MOUSE; NONHUMAN; OVARY CANCER; PANCREAS CANCER; PRIORITY JOURNAL; PROSTATE CANCER; STOMACH CANCER; TRANSGENIC MOUSE;

EID: 0033500248     PISSN: 01676997     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1006326203858     Document Type: Article

References (125)

1. Fu X, 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 USA 88: 9345-9349, 1991
2. Fu X, Theodorescu D, Kerbel RS, Hoffman RM: Extensive multi-organ metastasis following orthotopic on plantation of histologically-intact human bladder carcinoma tissue in nude mice. Int J Cancer 49: 938-939, 1991
3. Fu X, Hoffman RM: Human RT-4 bladder carcinoma is highly metastatic in nude mice and comparable to ras-H-transformed RT-4 when orthotopically onplanted as histologically-intact tissue. Int J Cancer 51: 989-991, 1992
4. Wang X, Fu X, Hoffman RM: A new patient-like metastatic model of human lung cancer constructed orthotopically with intact tissue via thoracotomy in immunodeficient mice. Int J Cancer 51: 992-995, 1992
5. Fu X, Guadagni F, Hoffman RM: A metastatic nude-mouse model of human pancreatic cancer constructed orthotopically from histologically-intact patient specimens. Proc Natl Acad Sci USA 89: 5645-5649, 1992
6. Hoffman RM: Patient-like models of human cancer in mice. Current Perspectives on Molecular & Cellular Oncology 1(B): 311-326, 1992
7. Kuo, T-H, Kubota T, Watanabe M, Furukawa T, Kase S, Tanino H, Nishibori K, Saikawa Y, Teramoto T, Ishibiki K, Kitajima M, Hoffman RM: Orthotopic reconstitution of human small-cell lung carcinoma after intravenous transplantation in SCID mice. Anticancer Res 12: 1407-1410, 1992
8. Fu X, Herrera H, Kubota T, Hoffman RM: Extensive liver metastasis from human colon cancer in nude and seid mice after orthotopic onplantation of histologically-intact human colon carcinoma tissue. Anticancer Res 12: 1395-1398, 1992
9. Wang X, Fu X, Hoffman RM: A patient-like metastasizing model of human lung adenocarcinoma constructed via thoracotomy in nude mice. Anticancer Res 12: 1399-1402, 1992
10. Wang X, Fu X, Kubota T, Hoffman RM: A new patient-like metastatic model of human small-cell lung cancer constructed orthotopically with intact tissue via thoracotomy in immunodeficient mice. Anticancer Res 12: 1403-1406, 1992
11. Fu X, Herrera H, Hoffman RM: Orthotopic growth and metastasis of human prostate carcinoma in nude mice after transplantation in nude mice. Int J Cancer 52: 987-990, 1992
12. Hoffman RM: Histoculture and the immunodeficient mouse come to the cancer clinic: rational approaches to individualizing cancer therapy and new drug evaluation review). Int J Oncol 1: 467-474, 1992
13. Furukawa T, Fu X, Kubota T, Watanabe M, Kitajima M, Hoffman RM: Nude mouse metastatic models of human stomach cancer constructed using orthotopic implantation of histologically-intact tissue. Cancer Research 53: 1204-1208, 1993
14. Furukawa T, Kubota T, Watanabe M, Kitajima M, Fu X, Hoffman RM: Orthotopic transplantation of histologically-intact clinical specimens of stomach cancer to nude mice: Correlation of metastatic sites in mouse and human. Int J Cancer 53: 608-612, 1993
15. Fu X, Hoffman RM: Human ovarian carcinoma metastatic models constructed in nude mice by orthotopic transplantation of histologically-intact patient specimens. Anticancer Res 13: 283-286, 1993
16. Furukawa T, Kubota T, Watanabe M, Kuo PH, Kase S, Saikawa Y, Tanino H, Teramoto T, Ishibiki K, Kitajima M, Hoffman RM: Immunochemotherapy prevents human colon cancer metastasis after orthotopic onplantation of histologically-intact tumor tissue in nude mice. Anticancer Res 13: 287-291, 1993
17. Kuo T-H, Kubota T, Watanabe M, Fujita S, Furukawa T, Teramoto T, Ishibiki K, Kitajima M, Hoffman RM: Early resection of primary orthotopically-growing human colon tumor in nude mouse prevents liver metastasis: Further evidence for patient-like hematogenous metastatic route. Anticancer Res 13: 293-298, 1993
18. Furukawa T, Kubota T, Watanabe M, Kitajima M, Hoffman RM: Differential chemosensitivity of local and metastatic human stomach cancer after orthotopic transplantation of histologically-intact tumor tissue in nude mice. Int J Cancer 54: 397-401, 1993
19. 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 53: 3070-3072, 1993
20. Kuo T-H, Kubota T, Watanabe M, Furukawa T, Kase S, Tanino H, Nishibori H, Saikawa Y, Ishibiki K, Kitajima M, Hoffman RM: Site-specific chemosensitivity of human small-cell lung carcinoma growing orthotopically compared to subcutaneously in SCID mice: The importance of orthotopic models to obtain relevant drug evaluation data. Anticancer Res 13: 627-630, 1993
21. Furukawa T, Kubota T, Watanabe M, Kuo T-H, Nishibori H, Kase S, Saikawa Y, Tanino H, Teramoto T, Ishibiki K, Kitajima M: A metastatic model of human colon cancer constructed using cecal implantation of cancer tissue in nude mice. Jpn J Surg 23: 420-423, 1993
22. Fu X, Le P, Hoffman RM: A metastatic orthotopic transplant nude-mouse model of human patient breast cancer. Anticancer Res 13: 901-904, 1993
23. Astoul P, Colt HG, Wang X, Hoffman RM: Metastatic human pleural ovarian cancer model constructed by orthotopic implantation of fresh histologically-intact patient carcinoma in nude mice. Anticancer Res 13: 1999-2002, 1993
24. Astoul P, Wang X, Hoffman RM: "Patient-Like" nude mouse models of human lung and pleural cancer (Review). Int J Oncology 3: 713-718, 1993
25. Kubota T, Inoue S, Furukawa T, Ishibiki K, Kitajima M, Kawamura E, Hoffman RM: Similarity of Serum - Tumor Pharmacokinetics of Antitumor Agents in Man and Nude Mice. Anticancer Research 13: 1481-1484, 1993
26. Astoul P, Colt HG, Wang X, Hoffman RM: A "patient-like" nude mouse model of parietal pleural human lung adenocarcinoma. Anticancer Res 14: 85-92, 1994
27. Astoul P, Colt HG, Wang X, Boutin C, Hoffman RM: A "patient-like" nude mouse metastatic model of advanced human pleural cancer. J Cell Biochem 56: 9-15, 1994
28. Wang X, Fu X, Brown PD, Crimmin MJ, Hoffman RM: Matrix metalloproteinase inhibitor BB-94 (Batimastat) inhibits human colon tumor growth and spread in a patient-like orthotopic model in nude mice. Cancer Res 54: 4726-4728, 1994
29. Hoffman RM: Orthotopic is orthodox: why are orthotopic-transplant metastatic models different from all other models? J Cell Biochem 56: 1-4, 1994
30. Togo S, Shimada H, Kubota T, Moossa AR, Hoffman RM: Seed to soil is a return trip in metastasis. Anticancer Res 15: 791-794, 1995
31. Togo S, Shimada H, Kubota T, Moossa AR, Hoffman RM: Host organ specifically determines cancer progression. Cancer Res 55: 681-684, 1995
32. Kuo T-H, Kubota T, Watanabe M, Furukawa T, Teramoto T, Ishibiki K, Kitajimi M, Moossa AR, Penman S, Hoffman RM: Liver colonization competence governs colon cancer metastasis. Proc Natl Acad Sei USA 92: 12085-12089, 1995
33. Togo S, Wang X, Shimada H, Moossa AR, Hoffman RM: Cancer seed and soil can be highly selective: Human-patient colon tumor lung metastasis grows in nude mouse lung but not colon or subcutis. Anticancer Res 15: 795-798, 1995
34. Dutton G: AntiCancer Inc. scientists identify a key governing step in the metastasis of cancer. Genetic Engineering News 16: 1, January 15, 1996
35. Holzman D: Of mice and metastasis: a new for-profit model emerges J Natl Cancer Inst 88: 396-397, 1996
36. Leff DN: MetaMouse models colon cancer metastasis with clinical potential. BioWorld Today 7, 1 (January 8), 1996
37. Sun FX, Tang ZY, Liu KD, Ye SL, Xue Q, Gao DM, Ma ZC: Establishment of a metastatic model of human hepatocellular carcinoma in nude mice via orthotopic implantation of histologically intact tissues. Int J Cancer 66: 239-243, 1996
38. An Z, Wang X, Kubota T, Moossa AR, Hoffman RM: A clinical nude mouse metastatic model for highly malignant human pancreatic cancer. Anticancer Res 16: 627-632, 1996
39. Riordan T: A technique is said to ease attachment of tumors to mice, making them "little cancer patients". New York Times, "Patents" Column, March 4, 1996
40. Murray G, Duncan M, O'Neil P, Melvin W, Fothergill J: Matrix metalloproteinase-1 is associated with poor prognosis in colorectal cancer. Nature Med 2: 461-462, 1996
41. Hoffman RM: Fertile seed and rich soil: development of patient-like models of human cancer by surgical orthotopic implantation of intact tissue. Update Series: Comprehensive Textbook of Oncology 3: 1-10, Schimpff, S.C, et al, eds. Williams & Williams, Baltimore, 1996
42. Sun F-X, Tang Z-Y, Liu K-D, Xue Q, Gao D-M, Yu Y-Q, Zhou X-D, MaZ-C: Metastatic models of human liver cancer in nude mice orthotopically constructed by using histologically intact patient specimens. J Cancer Res Clin Oncol 122: 397-402, 1996
43. Astoul P, Wang X, Colt HG, Boulin C, Hoffman RM: A patient-like human malignant pleural mesothelioma nude-mouse model. Oncology Reports 3: 483-487, 1996
44. Colt HG, Astoul P, Wang X, Yi ES, Boulin C, Hoffman RM: Clinical course of human epithelial-type malignant pleural mesothelioma replicated in an orthotopic-transplant nude mouse model. Anticancer Res 16: 633-640, 1996
45. An Z, Wang X, Astoul P, Danays T, Hoffman RM: Interferon gamma is highly effective against orthotopically-implanted human pleural adenocarcinoma in nude mice. Anticancer Res 16: 2545-2551, 1996
46. Olbina G, Cieslak D, Ruzdijic S, Esler C, An Z, Wang X, Hoffman RM, Seifert W, Pietrzkowski Z: Reversible inhibition of IL-8 receptor B mRNA expression and proliferation in non-small cell lung cancer by antisense oligonucleotides. Anticancer Res 16: 3525-3530, 1996
47. An Z, Wang X, Willmott N, Chander SK, Tickle S, Docherty AJP, Mountain A, Millican AT, Morphy R, Porter JR, Epemolu RO, Kubota T, Moossa AR, Hoffman RM: Conversion of highly malignant colon cancer from an aggressive to a controlled disease by oral administration of a metalloproteinase inhibitor. Clin Exp Metastasis 15: 184-195, 1997
48. Hoffman RM: Fertile seed and rich soil: The development of clinically relevant models of human cancer by surgical orthotopic implantation of intact tissue. In: Teicher B (ed) Anticancer Drug Development Guide: Preclinical Screening Clinical Trials, and Approval. Totowa, NJ: Humana Press Inc., 127-144, 1997
49. Chishima T, Miyagi Y, Wang X, Yamaoka H, Shimada H, Moossa AR, Hoffman RM: Cancer invasion and micrometastasis visualized in live tissue by green fluorescent protein expression. Cancer Res 57: 2042-2047, 1997
50. Inada T, Ichikawa A, Kubota T, Ogata Y, Moossa AR, Hoffman RM: 5-FU-induced apoptosis correlates with efficacy against human gastric and colon cancer xenografts in nude mice. Anticancer Res 17: 1965-1972, 1997
51. Chishima T, Miyagi Y, Wang X, Baranov E, Tan Y, Shimada H, Moossa AR, Hoffman RM: Metastatic patterns of lung cancer visualized live and in process by green fluorescent protein expression. Clin Exp Metastasis 15: 547-552, 1997
52. Chishima T, Miyagi Y, Wang X, Tan Y, Shimada H, Moossa AR, Hoffman RM: Visualization of the metastatic process by green fluorescent protein expression. Anticancer Res 17: 2377-2384, 1997
53. Chishima T, Yang M, Miyagi Y, Li L, Tan Y, Baranov E, Shimada H, Moossa AR, Penman S, Hoffman RM: Governing step of metastasis visualized in vitro. Proc Natl Acad Sci USA 94: 11573-11576, 1997
54. Tomikawa M, Kubota T, Matsuzaki SW, Takahasi S, Kitajima M, Moossa AR, Hoffman RM: Mitomycin C and cisplatin increase survival in a human pancreatic cancer metastatic model. Anticancer Res 17: 3623-3626, 1997
55. Chishima T, Miyagi Y, Li L, Tan Y, Baranov E, Yang M, Shimada H, Moossa AR, Hoffman RM: The use of histoculture and green fluorescent protein to visualize tumor cell host interaction. In Vitro Cell Dev Biol 33: 745-747, 1997
56. 3} in a metastatic model of human bladder cancer. Anticancer Res 17: 3239-3242, 1997
57. Dev SB, Nanda GS, An Z, Wang X, Hoffman RM, Hofmann GA: Effective electroporation therapy of human pancreatic tumors implanted in nude mice. Drug Delivery 4: 293-299, 1997
58. An Z, Wang X, Geller J, Moossa AR, Hoffman RM: Surgical orthotopic implantation allows high lung and lymph node metastatic expression of human prostate carcinoma cell line PC-3 in nude mice. Prostate 34: 169-174, 1998
59. Nanda GS, Sun FX, Hofmann GA, Hoffman RM, Dev SB: Electroporation therapy of human larynx tumors HEp-2 implanted in nude mice. Anticancer Res 18: 999-1004, 1998
60. Nanda GS, Sun FX, Hofmann GA, Hoffman RM, Dev SB: Electroporation enhances therapeutic efficacy of anticancer drugs: Treatment of human pancreatic tumor in animal model. Anticancer Res 18: 1361-1366, 1998
61. Yang M, Hasegawa S, Jiang P, Wang X, Tan Y, Chishima T, Shimada H, Moossa AR, Hoffman RM: Widespread skeletal metastatic potential of human lung cancer revealed by green fluorescent protein expression. Cancer Res 58: 4217-4221, 1998
62. Sun F-X, Sasson AR, Gamagami R, Jiang P, Moossa AR, Hoffman RH: An ultra-metastatic model of human colon cancer in nude mice. Clin Exp Metastasis 17(1): 41-48, 1999
63. Kiguchi K, Kubota T, Aoki D, Udagawa Y, Tamanouchi S, Saga M, Amemiya A, Sun F-X, Nozawa S, Moossa AR, Hoffman RM: A patient-like orthotopic implantation nude mouse model of highly metastatic human ovarian cancer. Clin Exp Metastasis 16: 75 1-756, 1999
64. Yang M, Jiang P, Sun FX, Hasegawa S, Baranov E, Chishima T, Shimada H, Moossa AR, Hoffman RM: A fluorescent orthotopic bone metastasis model of human prostate cancer. Cancer Res 59: 781-786, 1999
65. Wang X, An Z, Geller J, Hoffman RM: A high malignancy orthotopic nude mouse model of the human prostate cancer LNCaP. Prostate 39: 182-186, 1999
66. Kanai T, Konno H, Tanaka T, Matsumoto K, Baba M, Nakamura S, Baba S: Effect of angiogenesis inhibitor TNP-470 on the progression of human gastric cancer xenotransplanted into nude mice. Int J Cancer 71: 838-841, 1997
67. Konno H, Tanaka T, Kanai T, Masuyama K, Nakamura S, Baba S: Efficacy of an angiogenesis inhibitor, TNP-470, in xenotransplanted colorectal cancer with high metastatic potential. Cancer 77(8): 1736-1740, 1996
68. Konno H, Tanaka T, Matsuda I, Kanai T, Maruo Y, Nishino N, Nakamura S, Baba S: Comparison of the inhibitory effect of the angiogenesis inhibitor, TNP-470 and mitomycin C on the growth and liver metastasis of human colon cancer. Int J Cancer 11: 268-271, 1995
69. Konno H, Tanaka T, Baba M, Matsumoto K, Kamiya K, Nakamura S, Baba S, Arai T, Asano M, Suzuki H: Antitumor effect of angiogenesis inhibitors on colon cancer. Biotherapy 11: 993-996, 1997
70. Tanaka T, Konno H, Matsuda I, Nakamura S, Baba S: Prevention of hepatic metastasis of human colon cancer by angiogenesis inhibitor TNP-470. Cancer Res 55: 836-839, 1995
71. Konno H, Arai T, Tanaka T, Baba M, Matsumoto K, Kanai T, Nakamura S, Baba S, Naito T, Sugimura H, Yukita A, Asano M, Suzuki H: Antitumor effect of neutralizing antibody to vascular endothelial growth factor on liver metastasis of endocrine neoplasm. Jpn J Cancer Res 89: 933-939, 1998
72. Schabel FM: Animal Models as Predictive Systems in Cancer Chemotherapy Fundamental Concepts and Recent Advances, Year Book Publishers, pp. 323-355, 1975
73. Goldin A, Serpick AA, Mantel N: Experimental screening procedures and clinical predictability value. Cancer Chemother Rep 50: 173-218, 1966
74. Rygaard J, Povlsen CO: Heterotransplantation of a human malignant tumor to "nude" mice. Acta Pathol Microbiol Scan 77: 758-760, 1969
75. Ovejera A: The use of human tumor xenografts in large-scale drug screening. In Kalimann RF (ed) Rodent Tumor Model in Experimental Cancer Therapy, pp 218-220. Pergamon Press, NY, 1987
76. Fidler IJ: Critical factors in the biology of Human Cancer Metastases: twenty Eighth G.H.A Clowes memorial Award Lecture. Cancer Res 50: 6130-6138, 1990
77. Wilmans C, Fan D, O'Brian CA, Bucana CD, Fidler IJ: Orthotopic and ectopic organ environments differentially influence the sensitivity of murine colon carcinoma cells to doxorubicin and 5-fluorouracil. Int J Cancer 52: 98-104, 1992
78. An Z, Jiang P, Wang X, Moossa AR, Hoffman RM: Development of a high metastatic orthotopic model of human renal cell carcinoma in nude mice: Benefits of fragment implantation compared to cell-suspension injection. Clin Exp Metastasis 17: 265-270, 1999
79. Tanizawa A, Fujimori A, Fujimori Y et al.: Comparison of topoisomerase I inhibition, DNA damage, and cytotoxicity of camptothecin derivatives presently in clinical trials. J Natl Cancer Inst 86: 836-842, 1994
80. Cifuentes N, Pickren JW: Metastasis from carcinoma of mammary gland: an autopsy study. J Surg Oncol 11: 193-205, 1979
81. Mundy GR, Yoneda T: Facilitation and suppression of bone metastasis. Clin Orthop 312: 34-82, 1995
82. Guise TA: Parathyroid hormone-related protein and bone metastases. Cancer 80: 1572-1580, 1997
83. Olden K: Human tumor bone metastasis model in athymic nude rats. J Natl Cancer Inst 82: 340-341, 1990
84. Price JE, Polyzos A, Zhang RD, Daniels LM: Tumorigenicity and metastasis of human breast carcinoma cell lines in nude mice. Cancer Res 50: 717-721, 1990
85. Jia T, Liu YE, Liu J, Shi YE: Stimulation of breast cancer invasion and metastasis by synuclein-Γ. Cancer Res 5959: 742-747, 1999
86. Bagheri-Yarmand R, Kourbali Y, Rath AM, Vassy R, Martin A, Jozefonvicz J, Soria C, Lu H, Crepin, M: Carboxymethyl benzylamide dextran blocks angiogenesis of MDA-MB435 breast carcinoma xenograft in fat pad and its lung metastases in nude mice. Cancer Res 59: 507-510, 1999
87. Kurebayashi J, Nukatsuka M, Fujioka A, Saito H, Takeda S, Unemi N, Fukumori N, Kurosumi M, Sonoo H, Dickson RB: Postsurgical oral administration of uracil and tegafur inhibits progression of micrometastasis of human breast cancer cells in nude mice. Clin Cancer Res 3: 653-659, 1997
88. Thompson EW, Brunner N, Torri J, Johnson MD, Boulay V, Wright A, Lippman ME, Steeg PS, Clarke R: The invasive and metastatic properties of hormone-independent but hormone-responsive variants of MCF-7 human breast cancer cells. Clin Exp Metastasis 11: 15-26, 1993
89. Arguello FB, Baggs RB, Frantz CN: A murine model of experimental metastasis to bone and bone marrow. Cancer Res 48: 6876-6881, 1988
90. Sasaki A, Boyce BF, Story B, Wright KR, Chapman M, Boyce R, Mundy GR, Yoneda T: Bisphosphonate risedronate reduces metastatic human breast cancer burden in bone in nude mice. Cancer Res 55: 3551-3557, 1995
91. Morinaga Y, Fujita N, Ohishi K, Tsuruo T: Stimulation of interleukin-11 production from osteoblast-like cells by transforming growth factor-P and tumor cell factors. Int J Cancer 71: 422-428, 1997
92. Guise TA, Yin JJ, Taylor SD, Kumagai Y, Dallas M, Boyce BF, Yoneda T, Mundy GR: Evidence of causal role of parathyroid hormone-related protein in the pathogenesis of human breast cancer-mediated osteolysis. J Clin Invest 98: 1544-1549, 1996
93. Sung V, Gilles C, Murray A, Clarke R, Aaron AD, Azumi N, Thompson EW: The LCC1S-MB human breast cancer cell line expresses osteopontin and exhibits an invasive and metastatic phenotype. Exp Cell Res 241: 273-284, 1998
94. Wang CY, Chang YW: A model for osseous metastasis of human breast cancer established by intrafemur injection of the MDA-MB-435 cells in nude mice. Anticancer Res 17: 2471-2474, 1997
95. Stephenson RA, Dinney CPN, Gohji K, Ordonez NC, Kilion JJ, Fidler IJ: Metastasis model for human prostate cancer using orthotopic implantation in nude mice. J Natl Cancer Inst 84: 951-957, 1992
96. Pettaway CA, Pathak S, Greene G, Ramirez E, Wilson MR, Killion JJ, Fidler IJ: Selection of highly metastatic variants of different human prostatic carcinomas using orthotopic implantation in nude mice. Clin Cancer Res 2: 1627-1636, 1996
97. Saito N, Gleave ME, Bruchovshy N, Rennie PS, Beraldi E, Sullivan LD: A metastatic and androgen-sensitive human prostate cancer model using intraprostatic inoculation of LNCaP cells in SCID mice. Cancer Res 57: 1584-1589, 1997
98. Rembrink K, Romijn JC, van der Kwast TH, Rubben H, Schroder FH: Orthotopic implantation of human prostate cancer cell lines: a clinically-relevant animal model for metastatic prostate cancer. Prostate 31: 168-174, 1997
99. Thalmann GN, Anezinis PE, Chang SM, Zhau HE, Kim EE, Hopwood VL, Pathak S, Eschenbach ACV, Chung WK: Androgen-independent cancer progression and bone metastasis in the LNCaP model of human cancer. Cancer Res 54: 2577-2581, 1994
100. Lin WC, Pretlow TP, Pretlow TG, Culp LA: Bacterial lacZ gene as a highly sensitive marker to detect micrometastasis formation during tumor progression. Cancer Res 50: 2808-2817, 1990
101. Lin WC, Culp LA: Altered establishment/clearance mechanisms during experimental micrometastasis with live and/or disabled bacterial lacZ-tagged tumor cells. Invasion & Metastasis 12: 197-209, 1992
102. Morin J, Hastings J: Energy transfer in a bioluminescent system. J Cell Physiol 77: 313-318, 1972
103. Chalfie M, Tu Y, Euskirchen G, Ward, WW, Prasher DC: Green fluorescent protein as a marker for gene expression. Science 263: 802-805, 1994
104. Cheng L, Fu J, Tsukamoto A, Hawley RG: Use of green fluorescent protein variants to monitor gene transfer and expression in mammalian cells. Nature Biotechnol 14: 606-609,1996
105. Prasher DC, Eckenrode VK, Ward WW, Prendergast FG, Cormier MJ: Primary structure of the Aequorea victoria green-fluorescent protein. Gene 111: 229-233, 1992
106. Yang F, Miss LG, Phillips GN Jr: The molecular structure of green fluorescent protein. Nature Biotechnol 14: 1252-1256, 1996
107. Cody CW, Prasher DC, Welstler VM, Prendergast FG, Ward WW: Chemical structure of the hexapeptide chromophore of the Aequorea green fluorescent protein. Biochemistry 32: 1212-1218, 1993
108. Heim R, Cubitt AB, Tsien RY: Improved green fluorescence. Nature 373: 663-664, 1995
109. Delagrave S, Hawtin RE, Silva CM, Yang MM, Youvan DC: Red-shifted excitation mutants of the green fluorescent protein. Bio/Technology 13: 151-154, 1995
110. Cormack B, Valdivia R, Falkow S: FAGS-optimized mutants of the green fluorescent protein (GFP). Gene 173: 33-38, 1996
111. Zolotukhin S, Potter M, Hauswirth WW, Guy J, Muzycka N: 'Humanized' green fluorescent protein cDNA adapted for high-level expression in mammalian cells. J Virology 70: 4646-4654, 1996
112. Wang X, Fu X, Hoffman RM: A new patient-like metastatic model of human lung cancer constructed orthotopically with intact tissue via thoracotomy in immunodeficient mice. Int J Cancer 51: 992-995, 1992
113. Naumov GN, Wilson SM, MacDonald IC, Schmidt EE, Morris VL, Groom AC, Hoffman RM, Chambers AF: 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
114. Kan Z, Liu T-J: Video microscopy of tumor metastasis: using the green fluorescent protein (GFP) gene as a cancer-cell-labeling system. Clin Exp Meta 17: 49-55, 1999
115. Stewart TA, Pattengale PK, Leder P: Spontaneous mammary adenocarcinomas in transgenic mice that carry and express MTV/myc fusion genes. Cell 38: 627-637, 1984
116. Sinn E, Muller W, Pattengale P, Tepler I, Wallace R, Leder P: Coexpression of MMTV/v-Ha-ras and MMTV/c-myc genes in transgenic mice: synergistic action of oncogenes in vivo. Cell 49: 465-475, 1987
117. Guy CT, Cardiff RD, Muller WJ: Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol 12: 954-961, 1992
118. Ritland SR, Rowse GJ, Chang Y, Gendler SJ: Loss of Heterozygosity Analysis in Primary Mammary Tumors and Lung Metastases of MMTV-MTAg and MMTV-neu Transgenic Mice. Cancer Res 57: 3520-3525, 1997
119. Guy CT, Webster MA, Schaller M, Parsons TJ, Cardiff RD, Muller, WJ: Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc Natl Acad Sei USA 89: 10578-10582, 1992
120. Leder A, Pattengale PK, Kuo A, Stewart TA, Leder P: Consequences of Widespread Deregulation of the c-myc Gene in Transgenic Mice: Multiple Neoplasms and Normal Development. Cell 45: 485-495, 1986
121. Greenberg NM, DeMayo F, Finegold MJ, Medina D, Tilley WD, Aspinall JO, Cunha GR, Donjacour AA, Matusik RJ, Rosen JM: Prostate cancer in a transgenic mouse. Proc Natl Acad Sci USA 92: 3439-3443, 1995
122. Gingrich JR, Barrios RJ, Morton RA, Boyce BF, DeMayo FJ, Finegold MJ, Angelopoulou R, Rosen JM, Greenberg NM: Metastatic prostate cancer in a transgenic mouse. Cancer Res 56: 4096-4102, 1996
123. Gingrich JR, Barrios RJ, Kattan MW, Nahm HS, Finegold MJ, Greenberg NM: Androgen-independent Prostate Cancer Progression in the TRAMP Model Cancer Res 57: 4687-4691, 1997
124. Zhu Y, Richardson JA, Parada LF, Graff JM: Smad3 Mutant Mice Develop Metastatic Colorectal Cancer. Cell 94: 703-714, 1998
125. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA Jr, Butel JS, Bradley A: Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumors. Nature 356: 215-221, 1992