50 Years of preclinical anticancer drug screening: Empirical to target-driven approaches

Clinical Cancer Research

Volumn 11, Issue 3, 2005, Pages 971-981

  Suggitt, Marie ^a   Bibby, Michael C ^a  

^a UNIVERSITY OF BRADFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT;

CANCER; CANCER MODEL; CLONOGENIC ASSAY; DRUG SCREENING; GENETIC ENGINEERING; HOLLOW FIBER; HUMAN; METASTASIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUMOR CELL LINE; TUMOR MODEL; TUMOR XENOGRAFT;

ANIMALS; DISEASE MODELS, ANIMAL; DRUG SCREENING ASSAYS, ANTITUMOR; HUMANS; NEOPLASMS;

EID: 12944312687     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (136)

1. Gellhorn A, Hirschberg E. Investigation of diverse systems for cancer chemotherapy screening. Cancer Res 1955;15:1-125.
2. Goldin A, Venditti JM. Evaluation of chemical agents against carcinoma CA-755 in mice. Cancer Res 1961;21:617-91.
3. Stock CC, Clarke DA, Philips FS, Barclay RK. Cancer chemotherapy screening data. V. Sarcoma 180 screening data. Cancer Res 1960;1-92.
4. Oettel H, Wilheim G. Tests of compounds against Ehrlich tumour, sarcoma 180 and Walker carcino-sarcoma 256. Cancer Res 1955;2:129-44.
5. Goldin A, Venditti JM, Kline I, Mantel N. Evaluation of anti-leukemic agents employing advanced leukemia L1210 in mice. Cancer Res 1959;19:429-66.
6. Plowman J. Human tumour xenograft models in NCI drug development. In: Teicher B, editor. Anticancer drug development guide: preclinical screening, clinical trials, and approval: Humana Press Inc.; 1997. p. 101-25.
7. Geran RI, Greenberg NH, MacDonald MM, Schumacher AM, Abbott BJ. Cancer Chemother Rep 1972;3:1-103.
8. Ovejera A, Johnson RK, Goldin A. Cancer Chemother Rep 1975;5:111-25.
9. Venditti JM, Wesley RA, Plowman J. Current NCI preclinical antitumor screening in vivo: results of tumor panel screening, 1976-1982, and future directions. Adv Pharmacol Chemother 1984;20:1-20.
10. DeVita VT, Schein PS. The use of drugs in combination for the treatment of cancer: rationale and results. N Engl J Med 1973;288:998-1006.
11. Zubrod CG. Chemical Control of Cancer. Proc Natl Acad Sci U S A 1972;69:1042-7.
12. Flanagan SP. "Nude", a new hairless gene with pleiotropic effects in the mouse. Genet Res 1966;8:295-309.
13. Rygaard J, Povlsen CO. Heterotransplantation of a human malignant tumour to "Nude" mice. Acta Pathol Microbiol Scand 1969;77:758-60.
14. Bogden AE. A rapid screening method for testing chemotherapeutic agents against human tumour xenografts. In: Houchens D, Ovejera A, editors. Proceedings of the Symposium of the Use of Athymic (Nude) Mice in Cancer Research. New York, Stuttgart: Gustav Fischer; 1978. p. 231-50.
15. Bogden AE. The subrenal capsule assay: biological properties and testing capability. In: Fiebig HH, Burger AM, editors. Relevance of tumour models for anticancer drug development. Contrib Oncol. Vol. 54. Basel: Karger; 1999. p. 89-99.
16. Venditti JM. Drug evaluation branch program: report to screening contractors. Cancer Chemother Rep 1975;5:1-4.
17. Staquet MJ, Byar DP, Green SB, Rozencweig M. Clinical predictivity of transplantable tumor systems in the selection of new drugs for solid tumors: rationale for a three-stage strategy. Cancer Treat Rep 1983;67:753-65.
18. Venditti JM. Preclinical drug development: rationale and methods. Semin Oncol 1981;8:49-61.
19. Salmon SE, Hamburger AW, Soehnlen B, et al. Quantitation of differential sensitivity of human-tumor stem cells to anticancer drugs. N Engl J Med 1978;298:1321-7.
20. Hamburger AW, Salmon SE, Kim MB, et al. Direct cloning of human ovarian carcinoma cells in agar. Cancer Res 1978;38:3438-44.
21. Von Hoff DD, Harris GJ, Johnson G, Glaubiger D. Initial experience with the human tumor stem cell assay system: potential and problems. Prog Clin Biol Res 1980;48:113-24.
22. Shoemaker RH, Wolpert-DeFilippes MK, Kern DH, et al. Application of a human tumor colony-forming assay to new drug screening. Cancer Res 1985;45:2145-53.
23. Bertelsen CA, Sondak VK, Mann BD, Korn EL, Kern DH. Chemosensitivity testing of human solid tumors. A review of 1582 assays with 258 clinical correlations. Cancer 1984;53:1240-5.
24. Moon TE, Salmon SE, White CS, et al. Quantitative association between the in vitro human tumor stem cell assay and clinical response to cancer chemotherapy. Cancer Chemother Pharmacol 1981;6:211-8.
25. Tveit KM, Fodstad O, Lotsberg J, Vaage S, Pihl A. Colony growth and chemosensitivity in vitro of human melanoma biopsies. Relationship to clinical parameters. Int J Cancer 1982;29:533-8.
26. Von Hoff DD, Casper J, Bradley E, et al. Association between human tumor colony-forming assay results and response of an individual patient's tumor to chemotherapy. Am J Med 1981;70:1027-41.
27. Von Hoff DD, Clark GM, Stogdill BJ, et al. Prospective clinical trial of a human tumor cloning system. Cancer Res 1983;43:1926-31.
28. Salmon SE, Alberts DS, Durie BG, et al. Clinical correlations of drug sensitivity in the human tumor stem cell assay. Recent Results Cancer Res 1980;74:300-5.
29. Fiebig HH, Maier A, Burger AM. Clonogenic assay with established human tumour xenografts: correlation of in vitro to in vivo activity as a basis for anticancer drug discovery. Eur J Cancer 2004;40:802-20.
30. Selby P, Buick RN, Tannock I. A critical appraisal of the "human tumor stem-cell assay." N Engl J Med 1983;308:129-34.
31. Fiebig HH, Schmid JR, Bieser W, Henss H, Lohr GW. Colony assay with human tumor xenografts, murine tumors and human bone marrow. Potential for anticancer drug development. Eur J Cancer Clin Oncol 1987;23:937-48.
32. Roth T, Burger AM, Dengler W, Willmann H, Fiebig HH. Human tumour cell lines demonstrating characteristics of patient tumours as useful models for anticancer drug screening. In: Fiebig HH, Burger AM, editors. Relevance of tumour models for anticancer drug development. Contrib Oncol. Vol. 54. Basel: Karger; 1999. p. 145-56.
33. Alley MC, Scudiero DA, Monks A, et al. Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay. Cancer Res 1988;48:589-601.
34. Double JA, Bibby MC. Therapeutic index: a vital component in selection of anticancer agents for clinical trial. J Natl Cancer Inst 1989;81:988-94.
35. Corbett TH, Valeriote FA, Baker LH. Is the P388 murine tumour no longer adequate as a drug discovery model? Invest New Drugs 1987;5:3-20.
36. Boyd MR, Paull KD. Some practical considerations and applications of the National Cancer Institute In vitro anticancer drug discovery screen. Drug Dev Res 1995;34:91-109.
37. Holbeck SL. Update on NCI in vitro drug screen utilities. Eur J Cancer 2004;40:785-93.
38. Skehan P, Storeng R, Scudiero D, et al. New colorimetric cytotoxicity assay for anticancer-drug screening. J Natl Cancer Inst 1990;82:1107-12.
39. Paull KD, Shoemaker RH, Hodes L, et al. Display and analysis of patterns of differential activity of drugs against human tumor cell lines: development of mean graph and COMPARE algorithm. J Natl Cancer Inst 1989;81:1088-92.
40. Alvarez M, Paull K, Monks A, et al. Generation of a drug resistance profile by quantitation of Mdr-1/P-glycoprotein in the cell lines of the National Cancer Institute anticancer drug screen. J Clin Invest 1995;95:2205-14.
41. Hollingshead MG, Alley MC, Camalier RF, et al. In vivo cultivation of tumor cells in hollow fibers. Life Sci 1995;57:131-41.
42. Phillips RM, Bibby MC, Double JA. A critical appraisal of the predictive value of in vitro chemosensitivity assays. J Natl Cancer Inst 1990;82:1457-68.
43. Gorelik E, Ovejera A, Shoemaker R, et al. Microencapsulated tumor assay: new short-term assay for in vivo evaluation of the effects of anticancer drugs on human tumor cell lines. Cancer Res 1987;47:5739-47.
44. Lanza RP, Butler DH, Borland KM, et al. Xenotransplantation of canine, bovine, and porcine islets in diabetic rats without immunosuppression. Proc Natl Acad Sci U S A 1991;88:11100-4.
45. Lacy PE, Hegre OD, Gerasimidi-Vazeou A, Gentile FT, Dionne KE. Maintenance of nonnoglycemia in diabetic mice by subcutaneous xenografts of encapsulated islets. Science 1991;254:1785-4.
46. Decker S, Hollingshead M, Bonomi CA, Carter JP, Sausville EA. The hollow fibre model in cancer drug screening: the NCI experience. Eur J Cancer 2004;40:821-6.
47. Hall LA, Krauthauser CM, Wexler RS, et al. The hollow fiber assay: continued characterization with novel approaches. Anticancer Res 2000;20:903-11.
48. Suggitt M, Swaine DJ, Pettit GR, Bibby MC. Characterisation of the hollow fibre assay for the determination of microtubule disruption in vivo. Clin Cancer Res. 2004;10:6677-85.
49. Suggitt M, Bradshaw TD, Stevens MF, Bibby MC. 2-(4-amino-3-methylphenyl) benzothiazole prodrug ("Phortress") causes selective DNA damage in breast carcinoma cells cultured in the in vivo hollow fibre assay. AACR-NCI-EORTC International Conference, Molecular Targets and Cancer Therapeutics [abstract]. 2003 Nov 17-21; Boston, MA, USA.
50. Suggitt M, Bibby MC. Characterisation of the hollow fibre assay for the analysis of DNA damage using the comet assay [abstract]. Br J Cancer 2003;88:S31.
51. Bibby MC, Suggitt M, Cooper PA, Thurston DE. In vivo drug/target interaction of the novel pyrrolobenzodiazapine dimer SJG-136 revealed using the hollow fibre assay. AACR-NCI_EORTC International Conference, Molecular Targets and Cancer Therapeutics [abstract]. 2003 Nov 17-21; Boston, MA, USA.
52. Krauthauser CM, Hall LA, Wexler RS, et al. Regulation of gene expression and cell growth in vivo by tetracycline using the hollow fiber assay. Anticancer Res 2001;21:869-72.
53. Sadar MD, Akopian VA, Beraldi E. Characterization of a new in vivo hollow fiber model for the study of progression of prostate cancer to androgen dependence. Mol Cancer Ther 2002;1:629-37.
54. Jonsson E, Friberg LE, Karlsson MO, et al. In vivo activity of CHS 828 on hollow-fibre cultures of primary human tumour cells from patients. Cancer Lett 2001;162:193-200.
55. Hollingshead M, Plowman J, Alley M, Mayo J, Sausville E. The hollow fiber assay. In: Fiebig HH, Burger AM, editors. Relevance of tumour models for anticancer drug development. Contrib Oncol. Vol. 54. 1999.
56. Johnson JI, Decker S, Zaharevitz D, et al. Relationships between drug activity in NCI preclinical in vitro and in vivo models and early clinical trials. Br J Cancer 2001;84:1424-31.
57. Phillips RM, Pearce J, Loadman PM, et al. Angiogenesis in the hollow fiber tumor model influences drug delivery to tumor cells: implications for anticancer drug screening programs. Cancer Res 1998;58:5263-6.
58. Hollingshead MG, Bonomi CA, Borgel SD, et al. A potential role for imaging technology in anticancer efficacy evaluations. Eur J Cancer 2004;40:890-8.
59. Sausville EA, Feigal E. Evolving approaches to cancer drug discovery and development at the National Cancer Institute, USA. Ann Oncol 1999;10:1287-91.
60. Plowman J, Camalier R, Alley M, Sausville E, Schepartz S. US-NCI testing procedures. In: Fiebig HH, Burger AM, editors. Relevance of tumour models for anticancer drug development. Contrib Oncol. Vol. 54. Basel: Karger; 1999. p. 121-35.
61. Kelland LR. Of mice and men: values and liabilities of the athymic nude mouse model in anticancer drug development. Eur J Cancer 2004;40:827-36.
62. Scholz CC, Berger DP, Winterhalter BR, Henss H, Fiebig HH. Correlation of drug response in patients and in the clonogenic assay with solid human tumour xenografts. Eur J Cancer 1990;26:901-5.
63. Steel GG, Courtenay VD, Peckham MJ. The response to chemotherapy of a variety of human tumour xenografts. Br J Cancer 1983;47:1-13.
64. Nam NH, Parang K. Current targets for anticancer drug discovery. Curr Drug Targets 2003;4:159-79.
65. Bibby MC. Transplantable tumours in mice - the way forward. In: Burger AM, editor. Relevance of tumour models for anticancer drug development. Contrib Oncol. Vol. 54. Basel: Karger; 1999. p. 1-13.
66. Bibby MC. Orthotopic models of cancer for preclinical drug evaluation: advantages and disadvantages. Eur J Cancer 2004;40:852-7.
67. Kerbel RS. Human tumor xenografts as predictive preclinical models for anticancer drug activity in humans: better than commonly perceived - but they can be improved. Cancer Biol Ther 2003;2: S134-9.
68. Peterson JK, Houghton PJ. Integrating pharmacology and in vivo cancer models in preclinical and clinical drug development. Eur J Cancer 2004;40:837-44.
69. Fichtner I, Slisow W, Gill J, et al. Anticancer drug response and expression of molecular markers in early-passage xenotransplanted colon carcinomas. Eur J Cancer 2004;40:298-307.
70. Takimoto CH. Why drugs fail: of mice and men revisited. Clin Cancer Res 2001;7:229-30.
71. Paget S. Secondary growths of cancer of breast. Lancet 1889;1:571-3.
72. 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.
73. Fidler IJ, Naito S, Pathak S. Orthotopic implantation is essential for the selection, growth and metastasis of human renal cell cancer in nude mice [corrected]. Cancer Metastasis Rev 1990;9:149-65.
74. Hoffman RM. Fertile seed and rich soil: The development of clinically relevant models of human cancer by surgical orthotopic implantation of intact tissues. In: Teicher B, editor. Anticancer drug development guide: preclinical screening, clinical trials, and approval. Totowa, NJ: Humana Press, Inc.; 1997. p. 127-44.
75. Hoffman RM. Visualisation of metastasis in orthotopic mouse models with green fluorescent protein. In: Fiebig HH, Burger AM. editors. Relevance of tumour models for anticancer drug development. Contrib Oncol. Vol. 54. Basel: Karger; 1999. p. 81-7.
76. Killion JJ, Radinsky R, Fidler IJ. Orthotopic models are necessary to predict therapy of transplantable tumors in mice. Cancer Metastasis Rev 1999;17:279-84.
77. Kruger AE, Duray PH, Douglas K, et al. Approaches to preclinical screening of antiangiogenic agents. Semin Oncol 2001;28:570-6.
78. Tan MH, Holyoke ED, Goldrosen MH. Murine colon adenocarcinoma: syngeneic orthotopic transplantation and subsequent hepatic metastases. J Natl Cancer Inst 1977;59:1537-44.
79. Kuo TH, Kubota T, Watanabe M, et al. 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 1993;13:627-30.
80. Fidler IJ, Ellis LM. The implications of angiogenesis for the biology and therapy of cancer metastasis. Cell 1994;79:185-8.
81. Cowen SE, Bibby MC, Double JA. Characterisation of the vasculature within a murine adenocarcinoma growing in different sites to evaluate the potential of vascular therapies. Acta Oncol 1995;34:357-60.
82. 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 1994;54:4726-8.
83. Hoffman R. Green fluorescent protein imaging of tumour growth, metastasis, and angiogenesis in mouse models. Lancet Oncol 2002;3:546-56.
84. Huss WJ, Maddison LA, Greenberg NM. Autochthonous mouse models for prostate cancer: past, present and future. Semin Cancer Biol 2001;11:245-60.
85. Lin WC, Pretlow TP, Pretlow TG II, Culp LA. Bacterial lacZ gene as a highly sensitive marker to detect micrometastasis formation during tumor progression. Cancer Res 1990;50:2808-17.
86. El Hilali N, Rubio N, Martinez-Villacampa M, Blanco J. Combined noninvasive imaging and luminometric quantification of luciferase-labeled human prostate tumors and metastases. Lab Invest 2002;82:1563-71.
87. Berger MR. Autochthonous tumour models in rats: Is there a relevance for anticancer drug development. In: Fiebig HH, Burger AM, editors. Relevance of Tumour Models for Anticancer Drug Development. Contrib Oncol. Vol. 54. Basel: Karger; 1999. p. 15-27.
88. Macleod KF, Jacks T. Insights into cancer from transgenic mouse models. J Pathol 1999;187:43-60.
89. Stewart TA, Pattengale PK, Leder P. Spontaneous mammary adenocarcinomas in transgenic mice that carry and express MTV/myc fusion genes. Cell 1984;38:627-37.
90. Adams JM, Cory S. Transgenic models for haemopoietic malignancies. Biochim Biophys Acta 1991;1072:9-31.
91. Knudson AG. Antioncogenes and human cancer. Proc Natl Acad Sci U S A 1993;90:10914-21.
92. Jacks T, Remington L, Williams BO, et al. Tumor spectrum analysis in p53-mutant mice. Curr Biol 1994;4:1-7.
93. Lavigueur A, Maltby V, Mock D, et al. High incidence of lung, bone, and lymphoid tumors in transgenic mice overexpressing mutant alleles of the p53 oncogene. Mol Cell Biol 1989;9:3982-91.
94. Jacks T, Fazeli A, Schmitt EM, et al. Effects of an Rb mutation in the mouse. Nature 1992;359:295-300.
95. Donehower LA, Harvey M, Slagle BL, et al. Mice deficient for p53 are developrnentally normal but susceptible to spontaneous tumours. Nature 1992;356:215-21.
96. Purdie CA, Harrison DJ, Peter A, et al. Tumour incidence, spectrum and ploidy in mice with a large deletion in the p53 gene. Oncogene 1994;9:603-9.
97. Moser AR, Mattes EM, Dove WF, et al. ApcMin, a mutation in the murine Apc gene, predisposes to mammary carcinomas and focal alveolar hyperplasias. Proc Natl Acad Sci U S A 1993;90:8977-81.
98. Jacks T, Shih T, Schmitt E. Tumourigenic and developmental consequences of a targeted Nf1 mutation in the mouse. Nature Genet 1994;3:353-61.
99. Herzig M, Christofori G. Recent advances in cancer research: mouse models of tumorigenesis. Biochim Biophys Acta 2002;1602:97-113.
100. Clarke AR. Manipulating the germline: its impact on the study of carcinogenesis. Carcinogenesis 2000;21:435-41.
101. Hann B, Balmain A. Building "validated" mouse models of human cancer. Curr Opin Cell Biol 2001;13:778-84.
102. Shoemaker AR, Gould KA, Luongo C, Moser AR, Dove WF. Studies of neoplasia in the Min mouse. Biochim Biophys Acta 1997;1332:F25-48.
103. Aszterbaum M, Epstein J, Oro A, et al. Ultraviolet and ionizing radiation enhance the growth of BCCs and trichoblastomas in patched heterozygous knockout mice. Nat Med 1999;5:1285-91.
104. Wasan HS, Novelli M, Bee J, Bodmer WF. Dietary fat influences on polyp phenotype in multiple intestinal neoplasia mice. Proc Natl Acad Sci U S A 1997;94:3308-13.
105. Kavanaugh C, Green JE. The use of genetically altered mice for breast cancer prevention studies. J Nutr 2003;133:2404-9S.
106. Vogelstein B, Kinzler KW. The multistep nature of cancer. Trends Genet 1993;9:138-41.
107. Sinn E, Muller W, Pattengale P, et al. Coexpression of MMTV/v-Ha-ras and MMTV/c-myc genes in transgenic mice: synergistic action of oncogenes in vivo. Cell 1987;49:465-75.
108. Hanahan D. Heritable formation of pancreatic β-cell tumours in transgenic mice expressing recombinant insulin/simian virus 40 oncogenes. Nature 1985;315:115-22.
109. Perl AK, Wilgenbus P, Dahl U, Semb H, Christofori G. A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature 1998;392:190-3.
110. Naik P, Karrim J, Hanahan D. The rise and fall of apoptosis during multistage tumorigenesis: down-modulation contributes to tumor progression from angiogenic progenitors. Genes Dev 1996;10:2105-16.
111. Parangi S, Dietrich W, Christofori G, Lander ES, Hanahan D. Tumor suppressor loci on mouse chromosomes 9 and 16 are lost at distinct stages of tumorigenesis in a transgenic model of islet cell carcinoma. Cancer Res 1995;55:6071-6.
112. Bergers G, Hanahan D, Coussens LM. Angiogenesis and apoptosis are cellular parameters of neoplastic progression in transgenic mouse models of tumorigenesis. Int J Dev Biol 1998;42:995-1002.
113. Cavallaro U, Christofori G. Molecular mechanisms of tumor angiogenesis and tumor progression. J Neurooncol 2000;50:63-70.
114. Balmain A, Ramsden M, Bowden GT, Smith J. Activation of the mouse cellular Harvey-ras gene in chemically induced benign skin papillomas. Nature 1984;307:658-60.
115. Tuveson DA, Jacks T. Technologically advanced cancer modeling in mice. Curr Opin Genet Dev 2002;12:105-10.
116. Van Dyke T, Jacks T. Cancer modeling in the modern era: progress and challenges. Cell 2002;108:135-44.
117. Lewandoski M. Conditional control of gene expression in the mouse. Nat Rev Genet 2001;2:743-55.
118. Resor L, Bowen TJ, Wynshaw-Boris A. Unraveling human cancer in the mouse: recent refinements to modeling and analysis. Hum Mol Genet 2001;10:669-75.
119. Liyanage M, Coleman A, du Manoir S, et al. Multicolour spectral karyotyping of mouse chromosomes. Nat Genet 1996;14:312-5.
120. Pinkel D, Segraves R, Sudar D, et al. High resolution analysis of DNA copy number variation using comparative genomic hybridization to microarrays. Nat Genet 1998;20:207-11.
121. Le Y, Sauer B. Conditional gene knockout using Cre recombinase. Mol Biotechnol 2001;17:269-75.
122. Lakso M, Sauer B, Mosinger B Jr, et al. Targeted oncogene activation by site-specific recombination in transgenic mice. Proc Natl Acad Sci U S A 1992;89:6232-6.
123. Johnson L, Mercer K, Greenbaum D, et al. Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 2001;410:1111-6.
124. Fisher GH, Orsulic S, Holland E, et al. Development of a flexible and specific gene delivery system for production of murine tumor models. Oncogene 1999;18:5253-60.
125. Weiss B, Shannon K. Mouse cancer models as a platform for performing preclinical therapeutic trials. Curr Opin Genet Dev 2003;13:84-9.
126. Jacks T. Tumor suppressor gene mutations in mice. Annu Rev Genet 1996;30:603-36.
127. Harlow E. Retinoblastoma. For our eyes only. Nature 1992;359:270-1.
128. Kohl NE, Omer CA, Conner MW, et al. Inhibition of farnesyl-transferase induces regression of mammary and salivary carcinomas in ras transgenic mice. Nat Med 1995;1:792-7.
129. Lenferink AE, Simpson JF, Shawver LK, et al. Blockade of the epidermal growth factor receptor tyrosine kinase suppresses tumorigenesis in MMTV/Neu + MMTV/TGF-α bigenic mice. Proc Natl Acad Sci U S A 2000;97:9609-14.
130. Levis M, Allebach J, Tse KF, et al. A FLT3-targeted tyrosine kinase inhibitor is cytotoxic to leukemia cells in vitro and in vivo. Blood 2002;99:3885-91.
131. Bergers G, Javaherian K, Lo KM, Folkman J, Hanahan D. Effects of angiogenesis inhibitors on multistage carcinogenesis in mice. Science 1999;284:808-12.
132. Bergers G, Brekken R, McMahon G, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000;2:737-44.
133. Huss WJ, Barrios RJ, Greenberg NM. SU5416 selectively impairs angiogenesis to induce prostate cancer-specific apoptosis. Mol Cancer Ther 2003;2:611-6.
134. Rego EM, He LZ, Warrell RP Jr, Wang ZG, Pandolfi PP. Retinoic acid (RA) and As2O3 treatment in transgenic models of acute promyelocytic leukemia (APL) unravel the distinct nature of the leukemogenic process induced by the PML-RARα and PLZF-RARα oncoproteins. Proc Natl Acad Sci U S A 2000;97:10173-8.
135. Lallemand-Breitenbach V, Guillemin MC, Janin A, et al. Retinoic acid and arsenic synergize to eradicate leukemic cells in a mouse model of acute promyelocytic leukemia. J Exp Med 1999;189:1043-52.
136. Bearss DJ, Subler MA, Hundley JE, et al. Genetic determinants of response to chemotherapy in transgenic mouse mammary and salivary tumors. Oncogene 2000;19:1114-22.