Xenograft models of the normal and malignant human breast

Translational Animal Models in Drug Discovery and Development

Volumn , Issue , 2012, Pages 122-138

  Lewis, Michael T ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Breast cancer; Drug discovery; Estrogen receptor; Human cancer cell; Immunocompromised mice; In vitro model; In vivo model; Progesterone receptor; Translational model; Xenograft

Indexed keywords

EID: 84882615820     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.2174/978160805469511201010122     Document Type: Chapter

References (104)

1. Allred DC, Harvey JM, Berardo M, Clark GM. Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Mod Pathol 1998; 11: 155-68.
2. Allred DC, Wu Y, Mao S, et al. Ductal carcinoma in situ and the emergence of diversity during breast cancer evolution. Clin Cancer Res 2008; 14: 370-8.
3. Shipitsin M, Campbell LL, Argani P, et al. Molecular definition of breast tumor heterogeneity. Cancer Cell 2007; 11: 259-73.
4. Sorlie T, Perou CM, Tibshirani R, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 2001; 98: 10869-74.
5. Herschkowitz JI, Simin K, Weigman VJ, et al. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol 2007; 8: R76.
6. Hu Z, Fan C, Oh DS, et al. The molecular portraits of breast tumors are conserved across microarray platforms. BMC Genomics 2006; 7: 96.
7. Perou CM, Sorlie T, Eisen MB, et al. Molecular portraits of human breast tumours. Nature 2000; 406: 747-52.
8. Marusyk A, Polyak K. Tumor heterogeneity: causes and consequences. Biochim Biophys Acta 2010; 1805: 105-17.
9. Park SY, Gonen M, Kim HJ, Michor F, Polyak K. Cellular and genetic diversity in the progression of in situ human breast carcinomas to an invasive phenotype. J Clin Invest 2010; 120: 636-44.
10. Park SY, Lee HE, Li H, Shipitsin M, Gelman R, Polyak K. Heterogeneity for stem cellrelated markers according to tumor subtype and histologic stage in breast cancer. Clin Cancer Res 2010; 16: 876-87.
11. Hollestelle A, Nagel JH, Smid M, et al. Distinct gene mutation profiles among luminal-type and basal-type breast cancer cell lines. Breast Cancer Res Treat 2010; 121: 53-64.
12. Neve RM, Chin K, Fridlyand J, et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006; 10: 515-27.
13. Chin K, DeVries S, Fridlyand J, et al. Genomic and transcriptional aberrations linked to breast cancer pathophysiologies. Cancer Cell 2006; 10: 529-41.
14. Hampton OA, Den Hollander P, Miller CA, et al. A sequence-level map of chromosomal breakpoints in the MCF-7 breast cancer cell line yields insights into the evolution of a cancer genome. Genome Res 2009; 19: 167-77.
15. Bonnefoi H, Potti A, Delorenzi M, et al. Validation of gene signatures that predict the response of breast cancer to neoadjuvant chemotherapy: a substudy of the EORTC 10994/BIG 00-01 clinical trial. Lancet Oncol 2007; 8: 1071-8.
16. Liedtke C, Wang J, Tordai A, et al. Clinical evaluation of chemotherapy response predictors developed from breast cancer cell lines. Breast Cancer Res Treat 2010; 121: 301-9.
17. Potti A, Dressman HK, Bild A, et al. Genomic signatures to guide the use of chemotherapeutics. Nat Med 2006; 12: 1294-300.
18. Salter KH, Acharya CR, Walters KS, et al. An integrated approach to the prediction of chemotherapeutic response in patients with breast cancer. PLoS One 2008; 3: e1908.
19. Kenny PA, Lee GY, Myers CA, et al. The morphologies of breast cancer cell lines in threedimensional assays correlate with their profiles of gene expression. Mol Oncol 2007; 1: 84-96.
20. Weigelt B, Lo AT, Park CC, Gray JW, Bissell MJ. HER2 signaling pathway activation and response of breast cancer cells to HER2-targeting agents is dependent strongly on the 3D microenvironment. Breast Cancer Res Treat 2010; 122: 35-43.
21. Cardiff RD. Validity of mouse mammary tumour models for human breast cancer: comparative pathology. Microsc Res Tech 2001; 52: 224-30.
22. Clarke R. Human breast cancer cell line xenografts as models of breast cancer. The immunobiologies of recipient mice and the characteristics of several tumorigenic cell lines. Breast Cancer Res Treat 1996; 39: 69-86.
23. Kim JB, O'Hare MJ, Stein R. Models of breast cancer: is merging human and animal models the future?Breast Cancer Res 2004; 6: 22-30.
24. Rottenberg S, Pajic M, Jonkers J. Studying drug resistance using genetically engineered mouse models for breast cancer. Methods Mol Biol 2010; 596: 33-45.
25. Wu M, Jung L, Cooper AB, et al. Dissecting genetic requirements of human breast tumorigenesis in a tissue transgenic model of human breast cancer in mice. Proc Natl Acad Sci USA 2009; 106: 7022-7.
26. Becher OJ, Holland EC. Genetically engineered models have advantages over xenografts for preclinical studies. Cancer Res 2006; 66: 3355-8.
27. Sausville EA, Burger AM. Contributions of human tumor xenografts to anticancer drug development. Cancer Res 2006; 66: 3351-4.
28. Vargo-Gogola T, Rosen JM. Modeling breast cancer: one size does not fit all. Nat Rev Cancer 2007; 7: 659-72.
29. DeOme KB, Faulkin LJJ, Bern H. Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice. Cancer Res 1958; 19: 515-20.
30. Aamdal S, Fodstad O, Nesland JM, Pihl A. Characteristics of human tumour xenografts transplanted under the renal capsule of immunocompetent mice. Br J Cancer 1985; 51: 347-56.
31. Bogden AE, Haskell PM, LePage DJ, Kelton DE, Cobb WR, Esber HJ. Growth of human tumor xenografts implanted under the renal capsule of normal immunocompetent mice. Exp Cell Biol 1979; 47: 281-93.
32. Bogden AE, Kelton DE, Cobb WB, Esber HJ. A rapid screening method for testing chemotherapeutic agents against human tumor xenografts. In: Houchens DP, Ovejera AA. Symposium on the use of athymic (nude) mice in cancer research. 1978; pp. 231.
33. Eirew P, Stingl J, Raouf A. A method for quantifying normal human mammary epithelial stem cells with in vivo regenerative ability. Nat Med 2008; 14: 1384-9.
34. Brem SS, Jensen HM, Gullino PM. Angiogenesis as a marker of preneoplastic lesions of the human breast. Cancer 1978; 41: 239-244.
35. Gullino PM. Considerations on the preneoplastic lesions of the mammary gland. Am J Pathol 1977; 89: 413-30.
36. Bos PD, Zhang XH, Nadal C, et al. Genes that mediate breast cancer metastasis to the brain. Nature 2009; 459: 1005-9.
37. Kang Y, Siegel PM, Shu W, et al. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 2003; 3: 537-49.
38. Minn AJ, Gupta GP, Siegel PM, et al. Genes that mediate breast cancer metastasis to lung. Nature 2005; 436: 518-24.
39. Murphy P, Alexander P, Senior PV, Fleming J, Kirkham N, Taylor I. Mechanisms of organ selective tumour growth by bloodborne cancer cells. Br J Cancer 1988; 57: 19-31.
40. Palmieri D, Smith QR, Lockman PR, et al. Brain metastases of breast cancer. Breast Dis 2006; 26: 139-47.
41. Yi B, Williams PJ, Niewolna M, Wang Y, Yoneda T. Tumor-derived platelet-derived growth factor-BB plays a critical role in osteosclerotic bone metastasis in an animal model of human breast cancer. Cancer Res 2002; 62: 917-23.
42. Lam P, Yang W, Amemiya Y, et al. A human bone NOD/SCID mouse model to distinguish metastatic potential in primary breast cancers. Cancer Biol Ther 2009; 8: 1010-7.
43. Flanagan SP. 'Nude', a new hairless gene with pleiotropic effects in the mouse. Genet Res 1966; 8: 295-309.
44. Kaushik A, Kelsoe G, Jaton JC. The nude mutation results in impaired primary antibody repertoire. Eur J Immunol 1995; 25: 631-4.
45. Wortis HH, Nehlsen S, Owen JJ. Abnormal development of the thymus in "nude" mice. J Exp Med 1971; 134: 681-92.
46. Kaestner KH, Knochel W, Martinez DE. Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev 2000; 14: 142-6.
47. Nehls M, Pfeifer D, Schorpp M, Hedrich H, Boehm T. New member of the winged-helix protein family disrupted in mouse and rat nude mutations. Nature 1994; 372: 103-7.
48. Osborne CK, Hobbs K, Clark GM. Effect of estrogens and antiestrogens on growth of human breast cancer cells in athymic nude mice. Cancer Res 1985; 45: 584-90.
49. Seibert K, Shafie SM, Triche TJ, et al. Clonal variation of MCF-7 breast cancer cells in vitro and in athymic nude mice. Cancer Res 1983; 43: 2223-39.
50. Popnikolov NK, Yang J, Guzman RC, et al. In vivo growth stimulation of collagen gel embedded normal human and mouse primary mammary epithelial cells. J Cell Physiol 1995; 163: 51-60.
51. Soule HD, McGrath CM. Estrogen responsive proliferation of clonal human breast carcinoma cells in athymic mice. Cancer Lett 1980; 10: 177-89.
52. Blunt T, Finnie NJ, Taccioli GE, et al. Defective DNA-dependent protein kinase activity is linked to V(D)J recombination and DNA repair defects associated with the murine scid mutation. Cell 1995; 80: 813-23.
53. Bosma GC, Custer RP, Bosma MJ. A severe combined immunodeficiency mutation in the mouse. Nature 1983; 301: 527-30.
54. Bosma GC, Fried M, Custer RP, Carroll A, Gibson DM, Bosma MJ. Evidence of functional lymphocytes in some (leaky) scid mice. J Exp Med 1988; 167, 1016-33.
55. Nonoyama S, Smith FO, Bernstein ID, Ochs HD. Strain-dependent leakiness of mice with severe combined immune deficiency. J Immunol 1993; 150: 3817-24.
56. Cashman JD, Lapidot T, Wang JC, et al. Kinetic evidence of the regeneration of multilineage hematopoiesis from primitive cells in normal human bone marrow transplanted into immunodeficient mice. Blood 1997; 89: 4307-16.
57. Pflumio F, Izac B, Katz A, Shultz LD, Vainchenker W, Coulombel L. Phenotype and function of human hematopoietic cells engrafting immune-deficient CB17-severe combined immunodeficiency mice and nonobese diabetic-severe combined immunodeficiency mice after transplantation of human cord blood mononuclear cells. Blood 1996; 88: 3731-40.
58. Shultz LD, Schweitzer PA, Christianson SW, et al. Multiple defects in innate and adaptive immunologic function in NOD/LtSz-scid mice. J Immunol 1995; 154: 180-91.
59. Ito M, Hiramatsu H, Kobayashi K, et al. NOD/SCID/gamma(c)(null) mouse: an excellent recipient mouse model for engraftment of human cells. Blood 2002; 100: 3175-82.
60. Shultz LD, Ishikawa F, Greiner DL. Humanized mice in translational biomedical research. Nat Rev Immunol 2007; 7: 118-30.
61. Shultz LD, Lyons BL, Burzenski LM, et al. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J Immunol 2005; 174: 6477-89.
62. Christianson SW, Greiner DL, Schweitzer IB, et al. Role of natural killer cells on engraftment of human lymphoid cells and on metastasis of human T-lymphoblastoid leukemia cells in C57BL/6J-scid mice and in C57BL/6J-scid bg mice. Cell Immunol 1996; 171: 186-99.
63. Greiner DL, Shultz LD, Yates J, et al. Improved engraftment of human spleen cells in NOD/LtSz-scid/scid mice as compared with C.B-17-scid/scid mice. Am J Pathol 1995; 146: 888-902.
64. Roder J, Duwe A. The beige mutation in the mouse selectively impairs natural killer cell function. Nature 1979; 278: 451-3.
65. Xia Z, Taylor PR, Locklin RM, Gordon S, Cui Z, Triffitt JT. Innate immune response to human bone marrow fibroblastic cell implantation in CB17 scid/beige mice. J Cell Biochem 2006; 98: 966-80.
66. Gouon-Evans V, Lin EY, Pollard JW. Requirement of macrophages and eosinophils and their cytokines/chemokines for mammary gland development. Breast Cancer Res 2002; 4: 155-64.
67. Gouon-Evans V, Rothenberg ME, Pollard JW. Postnatal mammary gland development requires macrophages and eosinophils. Development 2000; 127: 2269-82.
68. Yang L, Huang J, Ren X, et al. Abrogation of TGF beta signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. Cancer Cell 2008; 13: 23-35.
69. Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, Papaioannou VE. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 1992; 68: 869-77.
70. Dewan MZ, Terunuma H, Ahmed S, et al. Natural killer cells in breast cancer cell growth and metastasis in SCID mice. Biomed Pharmacother 2005; 59S2: S375-9.
71. Hudson WA, Li Q, Le C, Kersey JH. Xenotransplantation of human lymphoid malignancies is optimized in mice with multiple immunologic defects. Leukemia 1998; 12: 2029-33.
72. Miller FR. Xenograft models of premalignant breast disease. J Mammary Gland Biol Neoplasia 2000; 5: 379-91.
73. Kuperwasser C, Chavarria T, Wu M, et al. Reconstruction of functionally normal and malignant human breast tissues in mice. Proc Natl Acad Sci USA 2004; 101: 4966-71.
74. Behbod F, Kittrell FS, LaMarca H, et al. An intraductal human-in-mouse transplantation model mimics the subtypes of ductal carcinoma in situ. Breast Cancer Res 2009; 11: R66.
75. Farnie G, Clarke RB, Spence K, et al. Novel cell culture technique for primary ductal carcinoma in situ: role of Notch and epidermal growth factor receptor signaling pathways. J Natl Cancer Inst 2007; 99: 616-27.
76. Deome KB, Faulkin LJ Jr., Bern HA, Blair PB. Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice. Cancer Res 1959; 19: 515-20.
77. Faulkin LJ Jr., Deome KB. Regulation of growth and spacing of gland elements in the mammary fat pad of the C3H mouse. J Natl Cancer Inst 1960; 24: 953-69.
78. Fichtner I, Becker M, Zeisig R, Sommer A. In vivo models for endocrine-dependent breast carcinomas: special considerations of clinical relevance. Eur J Cancer 2004; 40: 845-51.
79. 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.
80. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100: 3983-8.
81. Beckhove P, Schutz F, Diel IJ, et al. Efficient engraftment of human primary breast cancer transplants in nonconditioned NOD/Scid mice. Int J Cancer 2003; 105: 444-53.
82. Marangoni E, Vincent-Salomon A, Auger N, et al. A new model of patient tumor-derived breast cancer xenografts for preclinical assays. Clin Cancer Res 2007; 13: 3989-98.
83. McManus MJ, Welsch CW. DNA synthesis of benign human breast tumors in the untreated athymic "nude" mouse. An in vivo model to study hormonal influences on growth of human breast tissues. Cancer 1980; 45: 2160-5.
84. Murthy MS, Scanlon EF, Jelachich ML, Klipstein S, Goldschmidt RA. Growth and metastasis of human breast cancers in athymic nude mice. Clin Exp Metastasis 1995; 13: 3-15.
85. Naundorf H, Fichtner I, Buttner B, Frege J. Establishment and characterization of a new human oestradiol-and progesterone-receptor-positive mammary carcinoma serially transplantable in nude mice. J Cancer Res Clin Oncol 1992; 119: 35-40.
86. Noel A, Borcy V, Bracke M, et al. Heterotransplantation of primary and established human tumour cells in nude mice. Anticancer Res 1995; 15: 1-7.
87. Outzen HC, Custer RP. Growth of human normal and neoplastic mammary tissues in the cleared mammary fat pad of the nude mouse. J Natl Cancer Inst 1975; 55: 1461-6.
88. Rae-Venter B, Reid LM. Growth of human breast carcinomas in nude mice and subsequent establishment in tissue culture. Cancer Res 1980; 40: 95-100.
89. Sakakibara T, Xu Y, Bumpers HL, et al. Growth and metastasis of surgical specimens of human breast carcinomas in SCID mice. Cancer J Sci Am 1996; 2: 291-300.
90. Sebesteny A, Taylor-Papadimitriou J, Ceriani R, Millis R, Schmitt C, Trevan D. Primary human breast carcinomas transplantable in the nude mouse. J Natl Cancer Inst 1979; 63: 1331-7.
91. Sheffield LG, Welsch CW. Transplantation of human breast epithelia to mammary-glandfree fat-pads of athymic nude mice: influence of mammotrophic hormones on growth of breast epithelia. Int J Cancer 1988; 41: 713-9.
92. Visonneau S, Cesano A, Torosian MH, Miller EJ, Santoli D. Growth characteristics and metastatic properties of human breast cancer xenografts in immunodeficient mice. Am J Pathol 1998; 152: 1299-311.
93. Bailey MJ, Gazet JC, Peckham MJ. Human breast-cancer xenografts in immune-suppressed mice. Br J Cancer 1980; 42: 524-9.
94. Proia DA, Kuperwasser C. Reconstruction of human mammary tissues in a mouse model. Nat Protoc 2006; 1: 206-14.
95. Wu M, Robinson MO. Human-in-mouse breast cancer model. Cell Cycle 2009; 8: 2317-8.
96. Ginestier C, Hur MH, Charafe-Jauffret E, et al. ALDH1 Is a Marker of Normal and Malignant Human Mammary Stem Cells and a Predictor of Poor Clinical Outcome. Cell Stem Cell 2007; 1: 555-67.
97. 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.
98. 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: 4227-39.
99. Boven E, Winograd B, Berger DP, et al. Phase II preclinical drug screening in human tumor xenografts: a first European multicenter collaborative study. Cancer Res 1992; 52: 5940-7.
100. 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.
101. Utama FE, LeBaron MJ, Neilson LM, et al. Human prolactin receptors are insensitive to mouse prolactin: implications for xenotransplant modeling of human breast cancer in mice. J Endocrinol 2006; 188: 589-601.
102. Utama FE, Tran TH, Ryder A, LeBaron MJ, Parlow AF, Rui H. Insensitivity of human prolactin receptors to nonhuman prolactins: relevance for experimental modeling of prolactin receptor-expressing human cells. Endocrinology 2009; 150: 1782-90.
103. Rong S, Bodescot M, Blair D, et al. Tumorigenicity of the met proto-oncogene and the gene for hepatocyte growth factor. Mol Cell Biol 1992; 12: 5152-8.
104. Rong S, Oskarsson M, Faletto D, et al. Tumorigenesis induced by coexpression of human hepatocyte growth factor and the human met protooncogene leads to high levels of expression of the ligand and receptor. Cell Growth Differ 1993; 4: 563-9.