Drug resistance in the mouse cancer clinic

Drug Resistance Updates

Volumn 15, Issue 1-2, 2012, Pages 81-89

  Rottenberg, Sven ^a   Borst, Piet ^a  

^a ANTONI VAN LEEUWENHOEK HOSPITAL   (Netherlands)

Author keywords

ABCB1 P glycoprotein; BRCA1; Breast cancer; Genetic modifications; Predictive markers

Indexed keywords

ABC TRANSPORTER; BRCA1 PROTEIN; BRCA2 PROTEIN; CISPLATIN; DOCETAXEL; DOXORUBICIN; GEMCITABINE; IRINOTECAN; OLAPARIB; TOPOTECAN; VALSPODAR; VERAPAMIL;

BREAST CANCER; BREAST TUMOR; CANCER CELL CULTURE; CANCER CENTER; CANCER PATIENT; CANCER RESISTANCE; CANCER SURVIVAL; CAUSE OF DEATH; DISTANT METASTASIS; DNA REPAIR; ERADICATION THERAPY; HUMAN; LUNG ADENOCARCINOMA; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUMOR CELL;

EID: 84860662484     PISSN: 13687646     EISSN: 15322084     Source Type: Journal    
DOI: 10.1016/j.drup.2012.01.001     Document Type: Article

References (91)

1. M.W. Audeh, J. Carmichael, R.T. Penson, M. Friedlander, B. Powell, K.M. Bell-McGuinn, C. Scott, J.N. Weitzel, A. Oaknin, N. Loman, K. Lu, R.K. Schmutzler, U. Matulonis, M. Wickens, and A. Tutt Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer: a proof-of-concept trial Lancet 376 2010 245 251
2. P. Borst, S. Rottenberg, and J. Jonkers How do real tumors become resistant to cisplatin? Cell Cycle 7 2008 1353 1359
3. P. Borst, and L. Wessels Do predictive signatures really predict response to cancer chemotherapy? Cell Cycle 9 2010 4836 4840
4. P. Bouwman, A. Aly, J.M. Escandell, M. Pieterse, J. Bartkova, H. van der Gulden, S. Hiddingh, M. Thanasoula, A. Kulkarni, Q. Yang, B.G. Haffty, J. Tommiska, C. Blomqvist, R. Drapkin, D.J. Adams, H. Nevanlinna, J. Bartek, M. Tarsounas, S. Ganesan, and J. Jonkers 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers Nat. Struct. Mol. Biol. 17 6 2010 688 695
5. H.E. Bryant, N. Schultz, H.D. Thomas, K.M. Parker, D. Flower, E. Lopez, S. Kyle, M. Meuth, N.J. Curtin, and T. Helleday Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase Nature 434 2005 913 917
6. S.F. Bunting, E. Callen, N. Wong, H.T. Chen, F. Polato, A. Gunn, A. Bothmer, N. Feldhahn, O. Fernandez-Capetillo, L. Cao, X. Xu, C.X. Deng, T. Finkel, M. Nussenzweig, J.M. Stark, and A. Nussenzweig 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks Cell 141 2010 243 254
7. Cancer Genome Atlas Research Network Integrated genomic analyses of ovarian carcinoma Nature 474 2011 609 615
8. K.G. Chen, Y.C. Wang, M.E. Schaner, B. Francisco, G.E. Duran, D. Juric, L.M. Huff, H. Padilla-Nash, T. Ried, T. Fojo, and B.I. Sikic Genetic and epigenetic modeling of the origins of multidrug-resistant cells in a human sarcoma cell line Cancer Res. 65 2005 9388 9397
9. L.D. Cripe, H. Uno, E.M. Paietta, M.R. Litzow, R.P. Ketterling, J.M. Bennett, J.M. Rowe, H.M. Lazarus, S. Luger, and M.S. Tallman Zosuquidar, a novel modulator of P-glycoprotein, does not improve the outcome of older patients with newly diagnosed acute myeloid leukemia: a randomized, placebo-controlled trial of the Eastern Cooperative Oncology Group 3999 Blood 116 2010 4077 4085
10. L. Da Silva, and S.R. Lakhani Pathology of hereditary breast cancer Mod. Pathol. 23 Suppl. 2 2010 S46 S51
11. P.W. Derksen, T.M. Braumuller, E. Van der Burg, M. Hornsveld, E. Mesman, J. Wesseling, P. Krimpenfort, and J. Jonkers Mammary-specific inactivation of E-cadherin and p53 impairs functional gland development and leads to pleomorphic invasive lobular carcinoma in mice Dis. Model. Mech. 4 2011 347 358
12. P.W. Derksen, X. Liu, F. Saridin, H. van der Gulden, J. Zevenhoven, B. Evers, J.R. van Beijnum, A.W. Griffioen, J. Vink, P. Krimpenfort, J.L. Peterse, R.D. Cardiff, A. Berns, and J. Jonkers Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis Cancer Cell 10 2006 437 449
13. J. Doles, T.G. Oliver, E.R. Cameron, G. Hsu, T. Jacks, G.C. Walker, and M.T. Hemann Suppression of Rev3, the catalytic subunit of Pol{zeta}, sensitizes drug-resistant lung tumors to chemotherapy Proc. Natl. Acad. Sci. U.S.A. 107 2010 20786 20791
14. R. Drost, P. Bouwman, S. Rottenberg, U. Boon, E. Schut, S. Klarenbeek, C. Klijn, I. Van der Heijden, H. van der Gulden, E. Wientjens, M. Pieterse, A. Catteau, P. Green, E. Solomon, J.R. Morris, and J. Jonkers BRCA1 RING function is essential for tumor suppression but dispensable for therapy resistance Cancer Cell 20 2011 797 809
15. S.L. Edwards, R. Brough, C.J. Lord, R. Natrajan, R. Vatcheva, D.A. Levine, J. Boyd, J.S. Reis-Filho, and A. Ashworth Resistance to therapy caused by intragenic deletion in BRCA2 Nature 451 2008 1111 1115
16. B.L. Emmink, W.J. van Houdt, R.G. Vries, F.J. Hoogwater, K.M. Govaert, A. Verheem, M.W. Nijkamp, E.J. Steller, C.R. Jimenez, H. Clevers, I.H. Borel Rinkes, and O. Kranenburg Differentiated human colorectal cancer cells protect tumor-initiating cells from irinotecan Gastroenterology 141 2011 269 278
17. B. Evers, R. Drost, E. Schut, M. de Bruin, E. Van der Burg, P.W. Derksen, H. Holstege, X. Liu, E. Van Drunen, H.B. Beverloo, G.C. Smith, N.M. Martin, A. Lau, M.J. O'Connor, and J. Jonkers Selective inhibition of BRCA2-deficient mammary tumor cell growth by AZD2281 and cisplatin Clin. Cancer Res. 14 2008 3916 3925
18. B. Evers, E.N. Speksnijder, E. Schut, M. Ciampricotti, M.J. Smalley, P.W. Derksen, J. Jonkers, and K.E. de Visser A tissue reconstitution model to study cancer cell-intrinsic and -extrinsic factors in mammary tumourigenesis J. Pathol. 220 2010 34 44
19. H. Farmer, N. McCabe, C.J. Lord, A.N. Tutt, D.A. Johnson, T.B. Richardson, M. Santarosa, K.J. Dillon, I. Hickson, C. Knights, N.M. Martin, S.P. Jackson, G.C. Smith, and A. Ashworth Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy Nature 434 2005 917 921
20. P.C. Fong, D.S. Boss, T.A. Yap, A. Tutt, P. Wu, M. Mergui-Roelvink, P. Mortimer, H. Swaisland, A. Lau, M.J. O'Connor, A. Ashworth, J. Carmichael, S.B. Kaye, J.H. Schellens, and J.S. de Bono Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers N. Engl. J. Med. 361 2009 123 134
21. P.C. Fong, T.A. Yap, D.S. Boss, C.P. Carden, M. Mergui-Roelvink, C. Gourley, J. De Greve, J. Lubinski, S. Shanley, C. Messiou, R. A'Hern, A. Tutt, A. Ashworth, J. Stone, J. Carmichael, J.H. Schellens, J.S. de Bono, and S.B. Kaye Poly(ADP)-ribose polymerase inhibition: frequent durable responses in BRCA carrier ovarian cancer correlating with platinum-free interval J. Clin. Oncol. 28 2010 2512 2519
22. K. Garber From human to mouse and back: 'tumorgraft' models surge in popularity J. Natl. Cancer Inst. 101 2009 6 8
23. I. Garrido-Laguna, M. Uson, N.V. Rajeshkumar, A.C. Tan, E. De Oliveira, C. Karikari, M.C. Villaroel, A. Solomon, G. Taylor, R. Sharma, R.H. Hruban, A. Maitra, D. Laheru, B. Rubio-Viqueira, A. Jimeno, and M. Hidalgo Tumor engraftment in nude mice and enrichment in stroma-related gene pathways predicts poor survival and resistance to gemcitabine in patients with pancreatic cancer Clin. Cancer Res. 17 2011 5793 5800
24. M. Graeser, A. McCarthy, C.J. Lord, K. Savage, M. Hills, J. Salter, N. Orr, M. Parton, I.E. Smith, J.S. Reis-Filho, M. Dowsett, A. Ashworth, and N.C. Turner A marker of homologous recombination predicts pathologic complete response to neoadjuvant chemotherapy in primary breast cancer Clin. Cancer Res. 16 2010 6159 6168
25. T. Hay, J.R. Matthews, L. Pietzka, A. Lau, A. Cranston, A.O. Nygren, A. Douglas-Jones, G.C. Smith, N.M. Martin, M. O'Connor, and A.R. Clarke Poly(ADP-ribose) polymerase-1 inhibitor treatment regresses autochthonous Brca2/p53-mutant mammary tumors in vivo and delays tumor relapse in combination with carboplatin Cancer Res. 69 2009 3850 3855
26. C. Hegedus, C. Ozvegy-Laczka, G. Szakacs, and B. Sarkadi Interaction of ABC multidrug transporters with anticancer protein kinase inhibitors: substrates and/or inhibitors? Curr. Cancer Drug Targets 9 2009 252 272
27. J. Heyer, L.N. Kwong, S.W. Lowe, and L. Chin Non-germline genetically engineered mouse models for translational cancer research Nat. Rev. Cancer 10 2010 470 480
28. M. Hidalgo, E. Bruckheimer, N.V. Rajeshkumar, I. Garrido-Laguna, E. De Oliveira, B. Rubio-Viqueira, S. Strawn, M.J. Wick, J. Martell, and D. Sidransky A pilot clinical study of treatment guided by personalized tumorgrafts in patients with advanced cancer Mol. Cancer Ther. 10 2011 1311 1316
29. C.C. Hofmeister, X. Yang, F. Pichiorri, P. Chen, D.M. Rozewski, A.J. Johnson, S. Lee, Z. Liu, C.L. Garr, E.M. Hade, J. Ji, L.J. Schaaf, D.M. Benson Jr., E.H. Kraut, W.J. Hicks, K.K. Chan, C.S. Chen, S.S. Farag, M.R. Grever, J.C. Byrd, and M.A. Phelps Phase I trial of lenalidomide and CCI-779 in patients with relapsed multiple myeloma: evidence for lenalidomide-CCI-779 interaction via P-glycoprotein J. Clin. Oncol. 29 2011 3427 3434
30. H. Holstege, H.M. Horlings, A. Velds, A. Langerod, A.L. Borresen-Dale, M.J. van de Vijver, P.M. Nederlof, and J. Jonkers BRCA1-mutated and basal-like breast cancers have similar aCGH profiles and a high incidence of protein truncating TP53 mutations BMC Cancer 10 2010 654
31. H. Holstege, E. van Beers, A. Velds, X. Liu, S.A. Joosse, S. Klarenbeek, E. Schut, R. Kerkhoven, C.N. Klijn, L.F. Wessels, P.M. Nederlof, and J. Jonkers Cross-species comparison of aCGH data from mouse and human BRCA1- and BRCA2-mutated breast cancers BMC Cancer 10 2010 455
32. P.J. Houghton, C.L. Morton, C. Tucker, D. Payne, E. Favours, C. Cole, R. Gorlick, E.A. Kolb, W. Zhang, R. Lock, H. Carol, M. Tajbakhsh, C.P. Reynolds, J.M. Maris, J. Courtright, S.T. Keir, H.S. Friedman, C. Stopford, J. Zeidner, J. Wu, T. Liu, C.A. Billups, J. Khan, S. Ansher, J. Zhang, and M.A. Smith The pediatric preclinical testing program: description of models and early testing results Pediatr. Blood Cancer 49 2007 928 940
33. I.J. Huijbers, P. Krimpenfort, A. Berns, and J. Jonkers Rapid validation of cancer genes in chimeras derived from established genetically engineered mouse models BioEssays 33 2011 701 710
34. J. Jonkers, and A. Berns Conditional mouse models of sporadic cancer Nat. Rev. Cancer 2 2002 251 265
35. J. Jonkers, R. Meuwissen, H. van der Gulden, H. Peterse, M. Van der Valk, and A. Berns Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer Nat. Genet. 29 2001 418 425
36. R.L. Juliano, and V. Ling A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants Biochim. Biophys. Acta 455 1976 152 162
37. L.R. Kelland Of mice and men: values and liabilities of the athymic nude mouse model in anticancer drug development Eur. J. Cancer 40 2004 827 836
38. R.J. Kelly, D. Draper, C.C. Chen, R.W. Robey, W.D. Figg, R.L. Piekarz, X. Chen, E.R. Gardner, F.M. Balis, A.M. Venkatesan, S.M. Steinberg, T. Fojo, and S.E. Bates A pharmacodynamic study of docetaxel in combination with the P-glycoprotein antagonist tariquidar (XR9576) in patients with lung, ovarian, and cervical cancer Clin. Cancer Res. 17 2011 569 580
39. R.S. Kerbel 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. 2 2003 S134 S139
40. Kim, W.Y., Sharpless, N.E., in press. Drug efficacy testing in mice. Curr. Top. Microbiol. Immunol.
41. U. Kortmann, J.N. McAlpine, H. Xue, J. Guan, G. Ha, S. Tully, S. Shafait, A. Lau, A.N. Cranston, M.J. O'Connor, D.G. Huntsman, Y. Wang, and C.B. Gilks Tumor growth inhibition by olaparib in BRCA2 germline-mutated patient-derived ovarian cancer tissue xenografts Clin. Cancer Res. 17 2011 783 791
42. M. Kriege, C. Seynaeve, H. Meijers-Heijboer, J.M. Collee, M.B. Menke-Pluymers, C.C. Bartels, M.M. Tilanus-Linthorst, J. Blom, E. Huijskens, A. Jager, A. van den Ouweland, B. van Geel, M.J. Hooning, C.T. Brekelmans, and J.G. Klijn Sensitivity to first-line chemotherapy for metastatic breast cancer in BRCA1 and BRCA2 mutation carriers J. Clin. Oncol. 27 2009 3764 3771
43. G.D. Kruh, Y. Guo, E. Hopper-Borge, M.G. Belinsky, and Z.S. Chen ABCC10, ABCC11, and ABCC12 Pflugers Arch. 453 2007 675 684
44. R.J. Leary, I. Kinde, F. Diehl, K. Schmidt, C. Clouser, C. Duncan, A. Antipova, C. Lee, K. McKernan, F.M. De La Vega, K.W. Kinzler, B. Vogelstein, L.A. Diaz Jr., and V.E. Velculescu Development of personalized tumor biomarkers using massively parallel sequencing Sci. Transl. Med. 2 2010 20ra14
45. M. Leggas, M. Adachi, G.L. Scheffer, D. Sun, P. Wielinga, G. Du, K.E. Mercer, Y. Zhuang, J.C. Panetta, B. Johnston, R.J. Scheper, C.F. Stewart, and J.D. Schuetz Mrp4 confers resistance to topotecan and protects the brain from chemotherapy Mol. Cell. Biol. 24 2004 7612 7621
46. Q.Q. Li, J.D. Xu, W.J. Wang, X.X. Cao, Q. Chen, F. Tang, Z.Q. Chen, X.P. Liu, and Z.D. Xu Twist1-mediated adriamycin-induced epithelial-mesenchymal transition relates to multidrug resistance and invasive potential in breast cancer cells Clin. Cancer Res. 15 2009 2657 2665
47. E. Libby, and R. Hromas Dismounting the MDR horse Blood 116 2010 4037 4038
48. E.H. Lips, L. Mulder, J. Hannemann, N. Laddach, M.T. Vrancken Peeters, M.J. van de Vijver, J. Wesseling, P.M. Nederlof, and S. Rodenhuis Indicators of homologous recombination deficiency in breast cancer and association with response to neoadjuvant chemotherapy Ann. Oncol. 22 2011 870 876
49. X. Liu, H. Holstege, H. van der Gulden, M. Treur-Mulder, J. Zevenhoven, A. Velds, R.M. Kerkhoven, M.H. Van Vliet, L.F.A. Wessels, J.L. Peterse, A. Berns, and J. Jonkers Somatic loss of BRCA1 and p53 in mice induces mammary tumors with pathologic and molecular features of human BRCA1-mutated basal-like breast cancer Proc. Natl. Acad. Sci. U.S.A. 104 2007 12111 12116
50. C. Loveday, C. Turnbull, E. Ramsay, D. Hughes, E. Ruark, J.R. Frankum, G. Bowden, B. Kalmyrzaev, M. Warren-Perry, K. Snape, J.W. Adlard, J. Barwell, J. Berg, A.F. Brady, C. Brewer, G. Brice, C. Chapman, J. Cook, R. Davidson, A. Donaldson, F. Douglas, L. Greenhalgh, A. Henderson, L. Izatt, A. Kumar, F. Lalloo, Z. Miedzybrodzka, P.J. Morrison, J. Paterson, M. Porteous, M.T. Rogers, S. Shanley, L. Walker, D. Eccles, D.G. Evans, A. Renwick, S. Seal, C.J. Lord, A. Ashworth, J.S. Reis-Filho, A.C. Antoniou, and N. Rahman Germline mutations in RAD51D confer susceptibility to ovarian cancer Nat. Genet. 43 2011 879 882
51. E. Marangoni, A. Vincent-Salomon, N. Auger, A. Degeorges, F. Assayag, P. de Cremoux, L. de Plater, C. Guyader, G. De Pinieux, J.G. Judde, M. Rebucci, C. Tran-Perennou, X. Sastre-Garau, B. Sigal-Zafrani, O. Delattre, V. Dieras, and M.F. Poupon A new model of patient tumor-derived breast cancer xenografts for preclinical assays Clin. Cancer Res. 13 2007 3989 3998
52. E.M. Michalak, and J. Jonkers Studying therapy response and resistance in mouse models for BRCA1-deficient breast cancer J. Mammary Gland Biol. Neoplasia 16 2011 41 50
53. L.A. Mickley, J.-S. Lee, Z. Weng, Z. Zhan, M. Alvarez, W. Wilson, S.E. Bates, and T. Fojo Genetic polymorphism in MDR-1: a tool for examining allelic expression in normal cells, unselected and drug-selected cell lines, and human tumors Blood 91 1998 1749 1756
54. L.A. Mickley, B.A. Spengler, T.A. Knutsen, J.L. Biedler, and A.T. Fojo Gene rearrangement: a novel mechanism for MDR-1 gene activation J. Clin. Invest. 99 1997 1947 1957
55. K. Olive, M. Jacobetz, C. Davidson, A. Gopinathan, D. McIntyre, D. Honess, B. Madhu, M. Goldgraben, M. Caldwell, D. Allard, K. Frese, G. Denicola, C. Feig, C. Combs, S. Winter, H. Ireland-Zecchini, S. Reichelt, W. Howat, A. Chang, M. Dhara, L. Wang, F. Rückert, R. Grützmann, C. Pilarsky, K. Izeradjene, S. Hingorani, P. Huang, S. Davies, W. Plunkett, M. Egorin, R. Hruban, N. Whitebread, K. McGovern, J. Adams, C. Iacobuzio-Donahue, J. Griffiths, and D. Tuveson Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer Science 324 2009 1457 1461
56. T.G. Oliver, K.L. Mercer, L.C. Sayles, J.R. Burke, D. Mendus, K.S. Lovejoy, M.H. Cheng, A. Subramanian, D. Mu, S. Powers, D. Crowley, R.T. Bronson, C.A. Whittaker, A. Bhutkar, S.J. Lippard, T. Golub, J. Thomale, T. Jacks, and E.A. Sweet-Cordero Chronic cisplatin treatment promotes enhanced damage repair and tumor progression in a mouse model of lung cancer Genes Dev. 24 2010 837 852
57. M. Pajic, J.K. Iyer, A. Kersbergen, E. Van der Burg, A.O. Nygren, J. Jonkers, P. Borst, and S. Rottenberg Moderate increase in Mdr1a/1b expression causes in vivo resistance to doxorubicin in a mouse model for hereditary breast cancer Cancer Res. 69 2009 6396 6404
58. M. Pajic, A. Kersbergen, F. van Diepen, A. Pfauth, J. Jonkers, P. Borst, and S. Rottenberg Tumor-initiating cells are not enriched in cisplatin-surviving BRCA1;p53-deficient mammary tumor cells in vivo Cell Cycle 9 2010 3780 3791
59. K.J. Patel, and I.F. Tannock The influence of P-glycoprotein expression and its inhibitors on the distribution of doxorubicin in breast tumors BMC Cancer 9 2009 356
60. K. Politi, and W. Pao How genetically engineered mouse tumor models provide insights into human cancers J. Clin. Oncol. 29 2011 2273 2281
61. P.K. Premsrirut, L.E. Dow, S.Y. Kim, M. Camiolo, C.D. Malone, C. Miething, C. Scuoppo, J. Zuber, R.A. Dickins, S.C. Kogan, K.R. Shroyer, R. Sordella, G.J. Hannon, and S.W. Lowe A rapid and scalable system for studying gene function in mice using conditional RNA interference Cell 145 2011 145 158
62. R.W. Robey, P.R. Massey, L. Amiri-Kordestani, and S.E. Bates ABC transporters: unvalidated therapeutic targets in cancer and the CNS Anticancer Agents Med. Chem. 10 2010 625 633
63. S. Rottenberg, J.E. Jaspers, A. Kersbergen, E. Van der Burg, A.O. Nygren, S.A. Zander, P.W. Derksen, M. de Bruin, J. Zevenhoven, A. Lau, R. Boulter, A. Cranston, M.J. O'Connor, N.M. Martin, P. Borst, and J. Jonkers High sensitivity of BRCA1-deficient mammary tumors to the PARP inhibitor AZD2281 alone and in combination with platinum drugs Proc. Natl. Acad. Sci. U.S.A. 105 2008 17079 17084
64. S. Rottenberg, and J. Jonkers Modeling therapy resistance in genetically engineered mouse cancer models Drug Resist. Updat. 11 2008 51 60
65. S. Rottenberg, A.O.H. Nygren, M. Pajic, F.W.B. Van Leeuwen, I. Van der Heijden, K. Van de Wetering, X. Liu, K.E. de Visser, K.G. Gilhuijs, O. Van Tellingen, J.P. Schouten, J. Jonkers, and P. Borst Selective induction of chemotherapy resistance of mammary tumors in a conditional mouse model for hereditary breast cancer Proc. Natl. Acad. Sci. U.S.A. 104 2007 12117 12122
66. P. Ruff, D.A. Vorobiof, J.P. Jordaan, G.S. Demetriou, S.D. Moodley, A.L. Nosworthy, I.D. Werner, J. Raats, and L.J. Burgess A randomized, placebo-controlled, double-blind phase 2 study of docetaxel compared to docetaxel plus zosuquidar (LY335979) in women with metastatic or locally recurrent breast cancer who have received one prior chemotherapy regimen Cancer Chemother. Pharmacol. 64 2009 763 768
67. W. Sakai, E.M. Swisher, B.Y. Karlan, M.K. Agarwal, J. Higgins, C. Friedman, E. Villegas, C. Jacquemont, D.J. Farrugia, F.J. Couch, N. Urban, and T. Taniguchi Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers Nature 451 2008 1116 1120
68. A.H. Schinkel, U. Mayer, E. Wagenaar, C.A.A.M. Mol, L. Van Deemter, J.J.M. Smit, M.A. Van der Valk, A.C. Voordouw, H. Spits, O. Van Tellingen, J.M.J.M. Zijlmans, W.E. Fibbe, and P. Borst Normal viability and altered pharmacokinetics in mice lacking mdr1-type (drug-transporting) P-glycoproteins Proc. Natl. Acad. Sci. U.S.A. 94 1997 4028 4033
69. K.W. Scotto Transcriptional regulation of ABC drug transporters Oncogene 22 2003 7496 7511
70. J. Seibler, A. Kleinridders, B. Kuter-Luks, S. Niehaves, J.C. Bruning, and F. Schwenk Reversible gene knockdown in mice using a tight, inducible shRNA expression system Nucleic Acids Res. 35 2007 e54
71. S.V. Sharma, D.Y. Lee, B. Li, M.P. Quinlan, F. Takahashi, S. Maheswaran, U. McDermott, N. Azizian, L. Zou, M.A. Fischbach, K.K. Wong, K. Brandstetter, B. Wittner, S. Ramaswamy, M. Classon, and J. Settleman A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations Cell 141 2010 69 80
72. N.E. Sharpless, and R.A. DePinho The mighty mouse: genetically engineered mouse models in cancer drug development Nat. Rev. Drug Discov. 5 2006 741 754
73. D.P. Silver, A.L. Richardson, A.C. Eklund, Z.C. Wang, Z. Szallasi, Q. Li, N. Juul, C.O. Leong, D. Calogrias, A. Buraimoh, A. Fatima, R.S. Gelman, P.D. Ryan, N.M. Tung, A. De Nicolo, S. Ganesan, A. Miron, C. Colin, D.C. Sgroi, L.W. Ellisen, E.P. Winer, and J.E. Garber Efficacy of neoadjuvant Cisplatin in triple-negative breast cancer J. Clin. Oncol. 28 2010 1145 1153
74. A. Singh, and J. Settleman EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer Oncogene 29 2010 4741 4751
75. M. Singh, A. Lima, R. Molina, P. Hamilton, A.C. Clermont, V. Devasthali, J.D. Thompson, J.H. Cheng, H. Bou Reslan, C.C. Ho, T.C. Cao, C.V. Lee, M.A. Nannini, G. Fuh, R.A. Carano, H. Koeppen, R.X. Yu, W.F. Forrest, G.D. Plowman, and L. Johnson Assessing therapeutic responses in Kras mutant cancers using genetically engineered mouse models Nat. Biotechnol. 28 2010 585 593
76. E.M. Swisher, W. Sakai, B.Y. Karlan, K. Wurz, N. Urban, and T. Taniguchi Secondary BRCA1 mutations in BRCA1-mutated ovarian carcinomas with platinum resistance Cancer Res. 68 2008 2581 2586
77. G. Szakacs, J.K. Paterson, J.A. Ludwig, C. Booth-Genthe, and M.M. Gottesman Targeting multidrug resistance in cancer Nat. Rev. Drug Discov. 5 2006 219 234
78. N. Turner, A. Tutt, and A. Ashworth Hallmarks of 'BRCAness' in sporadic cancers Nat. Rev. Cancer 4 2004 814 819
79. A. Tutt, M. Robson, J.E. Garber, S.M. Domchek, M.W. Audeh, J.N. Weitzel, M. Friedlander, B. Arun, N. Loman, R.K. Schmutzler, A. Wardley, G. Mitchell, H. Earl, M. Wickens, and J. Carmichael Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and advanced breast cancer: a proof-of-concept trial Lancet 376 2010 235 244
80. V. Vafaizadeh, P. Klemmt, C. Brendel, K. Weber, C. Doebele, K. Britt, M. Grez, B. Fehse, S. Desrivieres, and B. Groner Mammary epithelial reconstitution with gene-modified stem cells assigns roles to Stat5 in luminal alveolar cell fate decisions, differentiation, involution, and mammary tumor formation Stem Cells 28 2010 928 938
81. M.A. Vollebergh, E.H. Lips, P.M. Nederlof, L.F. Wessels, M.K. Schmidt, E.H. van Beers, S. Cornelissen, M. Holtkamp, F.E. Froklage, E.G. de Vries, J.G. Schrama, J. Wesseling, M.J. van de Vijver, H. Van Tinteren, M. de Bruin, M. Hauptmann, S. Rodenhuis, and S.C. Linn An aCGH classifier derived from BRCA1-mutated breast cancer and benefit of high-dose platinum-based chemotherapy in HER2-negative breast cancer patients Ann. Oncol. 22 2011 1561 1570
82. J.C. Walrath, J.J. Hawes, T. Van Dyke, and K.M. Reilly Genetically engineered mouse models in cancer research Adv. Cancer Res. 106 2010 113 164
83. J.W. Watters, C. Cheng, P.K. Majumder, R. Wang, S. Yalavarthi, C. Meeske, L. Kong, W. Sun, J. Lin, J. Heyer, C. Ware, C. Winter, J.F. Reilly, T. Demuth, S. Clark, M.I. Chiu, M.O. Robinson, N. Kohl, and K. Kannan De novo discovery of a gamma-secretase inhibitor response signature using a novel in vivo breast tumor model Cancer Res. 69 2009 8949 8957
84. B. Weigelt, B. Kreike, and J.S. Reis-Filho Metaplastic breast carcinomas are basal-like breast cancers: a genomic profiling analysis Breast Cancer Res. Treat. 117 2009 273 280
85. M. Wu, L. Jung, A.B. Cooper, C. Fleet, L. Chen, L. Breault, K. Clark, Z. Cai, S. Vincent, S. Bottega, Q. Shen, A. Richardson, M. Bosenburg, S.P. Naber, R.A. DePinho, C. Kuperwasser, and M.O. Robinson Dissecting genetic requirements of human breast tumorigenesis in a tissue transgenic model of human breast cancer in mice Proc. Natl. Acad. Sci. U.S.A. 106 2009 7022 7027
86. J. Yuan, K.C. Cheng, R.L. Johnson, R. Huang, S. Pattaradilokrat, A. Liu, R. Guha, D.A. Fidock, J. Inglese, T.E. Wellems, C.P. Austin, and X.Z. Su Chemical genomic profiling for antimalarial therapies, response signatures, and molecular targets Science 333 2011 724 729
87. S.A. Zander, A. Kersbergen, E. Van der Burg, N. de Water, O. Van Tellingen, S. Gunnarsdottir, J.E. Jaspers, M. Pajic, A.O. Nygren, J. Jonkers, P. Borst, and S. Rottenberg Sensitivity and acquired resistance of BRCA1;p53-deficient mouse mammary tumors to the topoisomerase I inhibitor topotecan Cancer Res. 70 2010 1700 1710
88. L. Zender, W. Xue, J. Zuber, C.P. Semighini, A. Krasnitz, B. Ma, P. Zender, S. Kubicka, J.M. Luk, P. Schirmacher, W.R. McCombie, M. Wigler, J. Hicks, G.J. Hannon, S. Powers, and S.W. Lowe An oncogenomics-based in vivo RNAi screen identifies tumor suppressors in liver cancer Cell 135 2008 852 864
89. Y. Zhou, W.M. Rideout III, T. Zi, A. Bressel, S. Reddypalli, R. Rancourt, J.K. Woo, J.W. Horner, L. Chin, M.I. Chiu, M. Bosenberg, T. Jacks, S.C. Clark, R.A. DePinho, M.O. Robinson, and J. Heyer Chimeric mouse tumor models reveal differences in pathway activation between ERBB family- and KRAS-dependent lung adenocarcinomas Nat. Biotechnol. 28 2010 71 78
90. L. Zitvogel, L. Apetoh, F. Ghiringhelli, and G. Kroemer Immunological aspects of cancer chemotherapy Nat. Rev. Immunol. 8 2008 59 73
91. J. Zuber, I. Radtke, T.S. Pardee, Z. Zhao, A.R. Rappaport, W. Luo, M.E. McCurrach, M.M. Yang, M.E. Dolan, S.C. Kogan, J.R. Downing, and S.W. Lowe Mouse models of human AML accurately predict chemotherapy response Genes Dev. 23 2009 877 889