Murine models to evaluate novel and conventional therapeutic strategies for cancer

American Journal of Pathology

Volumn 170, Issue 3, 2007, Pages 793-804

  Talmadge, James E ^a   Singh, Rakesh K ^a   Fidler, Isaiah J ^b   Raz, Avraham ^c  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c KARMANOS CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CELECOXIB; DOXORUBICIN; IMATINIB; RETINOIC ACID;

ASCITES TUMOR; CANCER MODEL; CHRONIC MYELOID LEUKEMIA; COLON CARCINOMA; CYTOTOXICITY; DRUG RESEARCH; HLA TYPING; HUMAN; INTESTINE TUMOR; NONHUMAN; PRIORITY JOURNAL; REVIEW; TOXICITY TESTING; TUMOR GROWTH; TUMOR XENOGRAFT; ANIMAL; DISEASE MODEL; DRUG SCREENING; METHODOLOGY; MOUSE; NEOPLASM;

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

EID: 34247876272     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2007.060929     Document Type: Review

References (87)

1. Jemal A, Siegel R, Ward E, Murray T, Xu J, Smigal C, Thun MJ: Cancer statistics, 2006. CA Cancer J Clin 2006, 56:106-130
2. Talmadge JE, Wolman SR, Fidler IJ: Evidence for the clonal origin of spontaneous metastases. Science 1982, 217:361-363
3. Talmadge JE, Fidler IJ: Cancer metastasis is selective or random depending on the parent tumour population. Nature 1982, 297:593-594
4. Talmadge JE, Benedict K, Madsen J, Fidler IJ: Development of biological diversity and susceptibility to chemotherapy in murine cancer metastases. Cancer Res 1984, 44:3801-3805
5. Schuh JC: Trials, tribulations, and trends in tumor modeling in mice. Toxicol Pathol 2004, 32(Suppl 1):53-66
6. Suggitt M, Bibby MC: 50 years of preclinical anticancer drug screening: empirical to target-driven approaches. Clin Cancer Res 2005, 11:971-981
7. Schein PS, Scheffler B: Barriers to efficient development of cancer therapeutics. Clin Cancer Res 2006, 12:3243-3248
8. 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, 40:802-820
9. Johnson JI, Decker S, Zaharevitz D, Rubinstein LV, Venditti JM, Schepartz S, Kalyandrug S, Christian M, Arbuck S, Hollingshead M, Sausville EA: Relationships between drug activity in NCl preclinical in vitro and in vivo models and early clinical trials. Br J Cancer 2001, 84:1424-1431
10. Fidler IJ: Orthotopic implantation of human colon carcinomas into nude mice provides a valuable model for the biology and therapy of metastasis. Cancer Metastasis Rev 1991, 10:229-243
11. Hoffman RM: Orthotopic metastatic mouse models for anticancer drug discovery and evaluation: a bridge to the clinic. Invest New Drugs 1999, 17:343-359
12. Hoffman R: Fertile seed and rich soil: the development of clinically relevant models of human cancer by surgical orthotopic implantation of intact tissues. Anticancer Drug Development Guide: Preclinical Screening, Clinical Trials, and Approval. Edited by BA Teicher. Totowa, Humana Press Inc., 1997, pp 127-144
13. Killion JJ, Radinsky R, Fidler IJ: Orthotopic models are necessary to predict therapy of transplantable tumors in mice. Cancer Metastasis Rev 1999, 17:279-284
14. Dexter DL, Diamond M, Creveling J, Chen SF: Chemotherapy of mammary carcinomas arising in ras transgenic mice. Invest New Drugs 1993, 11:161-168
15. Moser AR, Hegge LF, Cardiff RD: Genetic background affects susceptibility to mammary hyperplasias and carcinomas in Apc(min)/+ mice. Cancer Res 2001, 61:3480-3485
16. Stringer JR, Larson JS, Fischer JM, Medvedovic M, Hersh MN, Boivin GP, Stringer SL: Modeling variation in tumors in vivo. Proc Natl Acad Sci USA 2005, 102:2408-2413
17. Voskoglou-Nomikos T, Pater JL, Seymour L: Clinical predictive value of the in vitro cell line, human xenograft, and mouse allograft preclinical cancer models. Clin Cancer Res 2003, 9:4227-4239
18. Gellhorn A, Hirschberg E: Investigation of diverse systems for cancer chemotherapy screening. Cancer Res 1955, 15(Suppl 3):1-125
19. Goldin A, Venditti JM, Kline I, Mantel N: Evaluation of anti-leukemic agents employing advanced leukemia L1210 in mice. Cancer Res 1959, 19:429-466
20. 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
21. Zubrod C: Chemical control of cancer. Proc Natl Acad Sci USA 1972, 69:1042-1047
22. Venditti JM, Wesley RA, Plowman J: Current NCl preclinical antitumor screening in vivo: results of tumor panel screening, 1976-1982, and future directions. Adv Pharmacol Chemother 1984, 20:1-20
23. Geran R, Greenberg N, MacDonald M, Schumacher A: Protocols for screening chemical agents and natural products against animal tumors and other biological systems. Cancer Chemother Rep 1972, 3:1-13
24. Ovejera A, Johnson R, Goldin A: Growth characteristics and chemotherapeutic response of intravenously implanted Lewis lung carcinoma. Cancer Chemother Rep 1975, 5:111-125
25. Bogden A: A rapid screening method for testing chemotherapeutic agents against human tumour xenografts. Proceedings of the Symposium of the Use of Athymic (Nude) Mice in Cancer Research. Edited by DOA Houchens. New York, Gustav Fischer, 1978, pp 231-250
26. Bogden AE: The subrenal capsule assay: biological properties and testing capability. Relevance of tumour models for anticancer drug development. Contributions to Oncology. Edited by HH Fiebig, BA Burger. Basel, Karger, 1999, pp 89-99
27. 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, 67:753-765
28. Venditti JM: Preclinical drug development: rationale and methods. Semin Oncol 1981, 8:349-361
29. Salmon SE, Hamburger AW, Soehnlen B, Durie BG, Alberts DS, Moon TE: Quantitation of differential sensitivity of human-tumor stem cells to anticancer drugs. N Engl J Med 1978, 298:1321-1327
30. 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, 48:113-124
31. Shoemaker RH, Wolpert-DeFilippes MK, Kern DH, Lieber MM, Makuch RW, Melnick NR, Miller WT, Salmon SE, Simon RM, Venditti JM: Application of a human tumor colony-forming assay to new drug screening. Cancer Res 1985, 45:2145-2153
32. 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, 53:1240-1245
33. Salmon SE, Alberts DS, Durie BG, Meyskens FL, Jones SE, Soehnlen B, Chen HS, Moon T: Clinical correlations of drug sensitivity in the human tumor stem cell assay. Recent Results Cancer Res 1980, 74:300-305
34. 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, 29:533-538
35. Von Hoff DD, Casper J, Bradley E, Sandbach J, Jones D, Makuch R: Association between human tumor colony-forming assay results and response of an individual patient's tumor to chemotherapy. Am J Med 1981, 70:1027-1041
36. Selby P, Buick RN, Tannock I: A critical appraisal of the "human tumor stem-cell assay." N Engl J Med 1983, 308:129-134
37. Alley MC, Scudiero DA, Monks A, Hursey ML, Czerwinski MJ, Fine DL, Abbott BJ, Mayo JG, Shoemaker RH, Boyd MR: Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay. Cancer Res 1988, 48:589-601
38. Sausville EA, Feigal E: Evolving approaches to cancer drug discovery and development at the National Cancer Institute, USA. Ann Oncol 1999, 10:1287-1291
39. Kelland LR: Of mice and men: values and liabilities of the athymic nude mouse model in anticancer drug development. Eur J Cancer 2004, 40:827-836
40. 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-S139
41. Peterson JK, Houghton PJ: Integrating pharmacology and in vivo cancer models in preclinical and clinical drug development. Eur J Cancer 2004, 40:837-844
42. Takimoto CH: Why drugs fail: of mice and men revisited. Clin Cancer Res 2001, 7:229-230
43. Habu S, Fukui H, Shimamura K, Kasai M, Nagai Y, Okumura K, Tamaoki N: In vivo effects of anti-asialo GM1. I. Reduction of NK activity and enhancement of transplanted tumor growth in nude mice. J Immunol 1981, 127:34-38
44. Talmadge JE, Meyers KM, Prieur DJ, Starkey JR: Role of NK cells in tumour growth and metastasis in beige mice. Nature 1980, 284:622-624
45. Cespedes MV, Casanova I, Parreno M, Mangues R: Mouse models in oncogenesis and cancer therapy. Clin Transpl Oncol 2006, 8:318-329
46. Becher OJ, Holland EC: Genetically engineered models have advantages over xenografts for preclinical studies. Cancer Res 2006, 66:3355-3358
47. Sausville EA, Burger AM: Contributions of human tumor xenografts to anticancer drug development. Cancer Res 2006, 66:3351-3354
48. 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, 26:901-905
49. Steel GG, Courtenay VD, Peckham MJ: The response to chemotherapy of a variety of human tumour xenografts. Br J Cancer 1983, 47:1-13
50. Varney ML, Olsen KJ, Mosley RL, Bucana CD, Talmadge JE, Singh RK: Monocyte/macrophage recruitment, activation and differentiation modulate interleukin-8 production: a paracrine role of tumor-associated macrophages in tumor angiogenesis. In Vivo 2002, 16:471-477
51. Legrand N, Weijer K, Spits H: Experimental models to study development and function of the human immune system in vivo. J Immunol 2006, 176:2053-2058
52. Chang DH, Liu N, Klimek V, Hassoun H, Mazumder A, Nimer SD, Jagannath S, Dhodapkar MV: Enhancement of ligand-dependent activation of human natural killer T cells by lenalidomide: therapeutic implications. Blood 2006, 108:618-621
53. Thomsen M, Yacoub-Youssef H, Marcheix B: Reconstitution of a human immune system in immunodeficient mice: models of human alloreaction in vivo. Tissue Antigens 2005, 66:73-82
54. Gonzalez FJ, Yu AM: Cytochrome P450 and xenobiotic receptor humanized mice. Annu Rev Pharmacol Toxicol 2006, 46:41-64
55. Bogaards JJ, Bertrand M, Jackson P, Oudshoorn MJ, Weaver RJ, van Bladeren PJ, Walther B: Determining the best animal model for human cytochrome P450 activities: a comparison of mouse, rat, rabbit, dog, micropig, monkey and man. Xenobiotica 2000, 30:1131-1152
56. Macchiarini F, Manz MG, Palucka AK, Shultz LD: Humanized mice: are we there yet? J Exp Med 2005, 202:1307-1311
57. Casares N, Pequignot MO, Tesniere A, Ghiringhelli F, Roux S, Chaput N, Schmitt E, Hamai A, Hervas-Stubbs S, Obeid M, Coutant F, Metivier D, Pichard E, Aucouturier P, Pierron G, Garrido C, Zitvogel L, Kroemer G: Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med 2005, 202:1691-1701
58. Donelli MG, Rosso R, Garattini S: Selective chemotherapy in relation to the site of tumor transplantation. Int J Cancer 1967, 2:421-424
59. Wilmanns C, Fan D, O'Brian C, Radinsky R, Bucana C, Tsan R, Fidler I: Modulation of doxorubicin sensitivity and level of P-glycoprotein expression in human colon carcinoma cells by ectopic and orthotopic environments in nude mice. Int J Oncol 1993, 3:413-422
60. Bibby MC: Orthotopic models of cancer for preclinical drug evaluation: advantages and disadvantages. Eur J Cancer 2004, 40:852-857
61. 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
62. Tan MH, Holyoke ED, Goldrosen MH: Murine colon adenocarcinoma: syngeneic orthotopic transplantation and subsequent hepatic metastases. J Natl Cancer Inst 1977, 59:1537-1544
63. Brinster RL, Chen HY, Messing A, Van DT, Levine AJ, Palmiter RD: Transgenic mice harboring SV40 T-antigen genes develop characteristic brain tumors. Cell 1984, 37:367-379
64. Heineke J, Molkentin JD: Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol 2006, 7:589-600
65. Gossen M, Bujard H: Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci USA 1992, 89:5547-5551
66. Rego EM, He LZ, Warrell Jr RP, 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-RARalpha and PLZF-RARalpha oncoproteins. Proc Natl Acad Sci USA 2000, 97:10173-10178
67. Brain J, Saksena A, Laneuville P: The kinase inhibitor STI571 reverses the Bcr-Abl induced point mutation frequencies observed in pre-leukemic P190(Bcr-Abl) transgenic mice. Leuk Res 2002, 26:1011-1016
68. Shoemaker AR, Gould KA, Luongo C, Moser AR, Dove WF: Studies of neoplasia in the Min mouse. Biochim Biophys Acta 1997, 1332:F25-F48
69. Macleod KF, Jacks T: Insights into cancer from transgenic mouse models. J Pathol 1999, 187:43-60
70. Sharpless NE, DePinho RA: The mighty mouse: genetically engineered mouse models in cancer drug development. Nat Rev Drug Discov 2006, 5:741-754
71. Basu GD, Pathangey LB, Tinder TL, Lagioia M, Gendler SJ, Mukherjee P: Cyclooxygenase-2 inhibitor induces apoptosis in breast cancer cells in an in vivo model of spontaneous metastatic breast cancer. Mol Cancer Res 2004, 2:632-642
72. Lallemand-Breitenbach V, Guillemin MC, Janin A, Daniel MT, Degos L, Kogan SC, Bishop JM, de The H: Retinoic acid and arsenic synergize to eradicate leukemic cells in a mouse model of acute promyelocytic leukemia. J Exp Med 1999, 189:1043-1052
73. Bearss DJ, Subler MA, Hundley JE, Troyer DA, Salinas RA, Windle JJ: Genetic determinants of response to chemotherapy in transgenic mouse mammary and salivary tumors. Oncogene 2000, 19:1114-1122
74. Weiss B, Shannon K: Mouse cancer models as a platform for performing preclinical therapeutic trials. Curr Opin Genet Dev 2003, 13:84-89
75. Jacks T: Tumor suppressor gene mutations in mice. Annu Rev Genet 1996, 30:603-636
76. Hann B, Balmain A: Building 'validated' mouse models of human cancer. Curr Opin Cell Biol 2001, 13:778-784
77. Van Dyke T, Jacks T: Cancer modeling in the modern era: progress and challenges. Cell 2002, 108:135-144
78. Berger M: Is there a relevance for anticancer drug development. Relevance of Tumour Models for Anticancer Drug Development. Contributions to Oncology. Edited by HH Fiebig, BA Burger. Basel, Karger, 1999, pp 15-27
79. Talmadge JE, Lenz BF, Klabansky R, Simon R, Riggs C, Guo S, Oldham RK, Fidler IJ: Therapy of autochthonous skin cancers in mice with intravenously injected liposomes containing muramyltripeptide. Cancer Res 1986, 46:1160-1163
80. Schwartz B, Birk Y, Raz A, Madar Z: Nutritional-pharmacological combinations - a novel approach to reducing colon cancer incidence. Eur J Nutr 2004, 43:221-229
81. Corpet DE, Pierre F: How good are rodent models of carcinogenesis in predicting efficacy in humans? A systematic review and meta-analysis of colon chemoprevention in rats, mice and men. Eur J Cancer 2005, 41:1911-1922
82. Schipper H, Goh CR, Wang TL: Shifting the cancer paradigm: must we kill to cure? J Clin Oncol 1995, 13:801-807
83. Freireich EJ, Gehan EA, Rall DP, Schmidt LH, Skipper HE: Quantitative comparison of toxicity of anticancer agents in mouse, rat, hamster, dog, monkey, and man. Cancer Chemother Rep 1966, 50:219-244
84. Burtles SS, Newell DR, Henrar RE, Connors TA: Revisions of general guidelines for the preclinical toxicology of new cytotoxic anticancer agents in Europe. The Cancer Research Campaign (CRC) Phase I/II Clinical Trials Committee and the European Organization for Research and Treatment of Cancer (EORTC) New Drug Development Office. Eur J Cancer 1995, 31A:408-410
85. Newell DR, Burtles SS, Fox BW, Jodrell DI, Connors TA: Evaluation of rodent-only toxicology for early clinical trials with novel cancer therapeutics. Br J Cancer 1999, 81:760-768
86. Balmain A: Cancer as a complex genetic trait: tumor susceptibility in humans and mouse models. Cell 2002, 108:145-152
87. Siemann DW: Satisfactory and unsatisfactory tumor models factors influencing the selection of a tumor model for experimental evaluation. Rodent Tumor Models in Experimental Cancer Therapy. Edited by RF Kallman, Elmsford, Pergamon Books, Inc., 1987