Prioritizing therapeutic targets using patient-derived xenograft models

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1855, Issue 2, 2015, Pages 223-234

  Lodhia, K A ^a   Hadley, A M ^b   Haluska, P ^a   Scott, C L ^b,c  

^a MAYO CLINIC   (United States)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Genomics; Patient derived xenografts; Personalized medicine; Targeted therapy; Therapeutic targets

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; B RAF KINASE; CHLOROPLAST DNA; EPIDERMAL GROWTH FACTOR RECEPTOR 2; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PROTEIN P53; TUMOR MARKER;

BREAST CANCER; CANCER CELL LINE; CANCER CHEMOTHERAPY; CANCER MODEL; CANCER PROGNOSIS; CLONAL EVOLUTION; COLORECTAL CANCER; GENE AMPLIFICATION; GENE MUTATION; GENE OVEREXPRESSION; GENE TRANSLOCATION; GENETIC ASSOCIATION; HIGH GRADE SEROUS OVARIAN CANCER; HISTOLOGY; HUMAN; IMMUNE DEFICIENCY; IMMUNE SYSTEM; IMMUNOHISTOCHEMISTRY; LYMPHOMA; MELANOMA; MOLECULAR BIOLOGY; MOLECULARLY TARGETED THERAPY; NON SMALL CELL LUNG CANCER; NONHUMAN; OVARY CANCER; PATIENT DERIVED XENOGRAFT; PATIENT DERIVED XENOGRAFT AVATAR MODEL; PATIENT DERIVED XENOGRAFT SUPER AVATAR MODEL; PERSONALIZED MEDICINE; PREDICTION; PRIORITY JOURNAL; REVIEW; TREATMENT RESPONSE; TUMOR XENOGRAFT; ANIMAL; DISEASE MODEL; DRUG RESISTANCE; DRUG SCREENING; GENETICS; IMMUNOLOGY; MOUSE; NEOPLASMS; PATHOLOGY;

MUS;

ANIMALS; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; HUMANS; MICE; NEOPLASMS; PRECISION MEDICINE; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84925682623     PISSN: 0304419X     EISSN: 18792561     Source Type: Journal    
DOI: 10.1016/j.bbcan.2015.03.002     Document Type: Review

References (129)

1. Tursz T., Bernards R. Hurdles on the road to personalized medicine. Mol. Oncol. 2014.
2. Hidalgo M., Amant F., Biankin A.V., et al. Patient-derived xenograft models: an emerging platform for translational cancer research. Cancer Discov. 2014, 4(9):998-1013.
3. Romond E.H., Perez E.A., Bryant J., et al. Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. N. Engl. J. Med. 2005, 353(16):1673-1684.
4. Misale S., Yaeger R., Hobor S., et al. Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer. Nature 2012, 486(7404):532-536.
5. Mao M., Tian F., Mariadason J.M., et al. Resistance to BRAF inhibition in BRAF-mutant colon cancer can be overcome with PI3K inhibition or demethylating agents. Clin. Cancer Res. 2013, 19(3):657-667.
6. Lander E.S. Initial impact of the sequencing of the human genome. Nature 2011, 470(7333):187-197.
7. Ulahannan D., Kovac M.B., Mulholland P.J., Cazier J.B., Tomlinson I. Technical and implementation issues in using next-generation sequencing of cancers in clinical practice. Br. J. Cancer 2013, 109(4):827-835.
8. Gargis A.S., Kalman L., Berry M.W., et al. Assuring the quality of next-generation sequencing in clinical laboratory practice. Nat. Biotechnol. 2012, 30(11):1033-1036.
9. Sah S., Chen L., Houghton J., et al. Functional DNA quantification guides accurate next-generation sequencing mutation detection in formalin-fixed, paraffin-embedded tumor biopsies. Genome Med. 2013, 5(8):77.
10. Meric-Bernstam F., Farhangfar C., Mendelsohn J., Mills G.B. Building a personalized medicine infrastructure at a major cancer center. J. Clin. Oncol. 2013, 31(15):1849-1857.
11. Frampton G.M., Fichtenholtz A., Otto G.A., et al. Development and validation of a clinical cancer genomic profiling test based on massively parallel DNA sequencing. Nat. Biotechnol. 2013, 31(11):1023-1031.
12. Robson M. Multigene panel testing: planning the next generation of research studies in clinical cancer genetics. J. Clin. Oncol. 2014, 32(19):1987-1989.
13. Hoadley K.A., Yau C., Wolf D.M., et al. Multiplatform analysis of 12 cancer types reveals molecular classification within and across tissues of origin. Cell 2014, 158(4):929-944.
14. Cancer Genome Atlas Research N Integrated genomic analyses of ovarian carcinoma. Nature 2011, 474(7353):609-615.
15. Cancer Genome Atlas Research N Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008, 455(7216):1061-1068.
16. Cancer Genome Atlas Research N Comprehensive molecular characterization of gastric adenocarcinoma. Nature 2014, 513(7517):202-209.
17. Lawrence M.S., Stojanov P., Mermel C.H., et al. Discovery and saturation analysis of cancer genes across 21 tumour types. Nature 2014, 505(7484):495-501.
18. Gatta G., van der Zwan J.M., Casali P.G., et al. Rare cancers are not so rare: the rare cancer burden in Europe. Eur. J. Cancer 2011, 47(17):2493-2511.
19. Venditti J.M. Preclinical drug development: rationale and methods. Semin. Oncol. 1981, 8(4):349-361.
20. Johnson J.I., 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(10):1424-1431.
21. Ahmed A.A., Etemadmoghadam D., Temple J., et al. Driver mutations in TP53 are ubiquitous in high grade serous carcinoma of the ovary. J. Pathol. 2010, 221(1):49-56.
22. Knoops L., de Jong D. The role of the p53 pathway in the treatment of follicular lymphoma. Cell Cycle 2008, 7(4):436-439.
23. Chapman P.B., Hauschild A., Robert C., et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N. Engl. J. Med. 2011, 364(26):2507-2516.
24. Corcoran R.B., Ebi H., Turke A.B., et al. EGFR-mediated re-activation of MAPK signaling contributes to insensitivity of BRAF mutant colorectal cancers to RAF inhibition with vemurafenib. Cancer Discov. 2012, 2(3):227-235.
25. Prahallad A., Sun C., Huang S., et al. Unresponsiveness of colon cancer to BRAF(V600E) inhibition through feedback activation of EGFR. Nature 2012, 483(7387):100-103.
26. Bernards R. A missing link in genotype-directed cancer therapy. Cell 2012, 151(3):465-468.
27. Piccart-Gebhart M.J., Procter M., Leyland-Jones B., et al. Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. N. Engl. J. Med. 2005, 353(16):1659-1672.
28. Perez E.A., Romond E.H., Suman V.J., et al. Four-year follow-up of trastuzumab plus adjuvant chemotherapy for operable human epidermal growth factor receptor 2-positive breast cancer: joint analysis of data from NCCTG N9831 and NSABP B-31. J. Clin. Oncol. 2011, 29(25):3366-3373.
29. Slamon D.J., Leyland-Jones B., Shak S., et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N. Engl. J. Med. 2001, 344(11):783-792.
30. Cobleigh M.A., Vogel C.L., Tripathy D., et al. Multinational study of the efficacy and safety of humanized anti-HER2 monoclonal antibody in women who have HER2-overexpressing metastatic breast cancer that has progressed after chemotherapy for metastatic disease. J. Clin. Oncol. 1999, 17(9):2639-2648.
31. Bang Y.J., Van Cutsem E., Feyereislova A., et al. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet 2010, 376(9742):687-697.
32. Kato H., Arao T., Matsumoto K., et al. Gene amplification of EGFR, HER2, FGFR2 and MET in esophageal squamous cell carcinoma. Int. J. Oncol. 2013, 42(4):1151-1158.
33. Anglesio M.S., Kommoss S., Tolcher M.C., et al. Molecular characterization of mucinous ovarian tumours supports a stratified treatment approach with HER2 targeting in 19% of carcinomas. J. Pathol. 2013, 229(1):111-120.
34. Herter-Sprie G.S., Greulich H., Wong K.K. Activating mutations in ERBB2 and their impact on diagnostics and treatment. Front. Oncol. 2013, 3:86.
35. Schoppmann S.F., Streubel B., Birner P. Amplification but not translocation of anaplastic lymphoma kinase is a frequent event in oesophageal cancer. Eur. J. Cancer 2013, 49(8):1876-1881.
36. Audeh M.W., Carmichael J., Penson R.T., et al. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer: a proof-of-concept trial. Lancet 2010, 376(9737):245-251.
37. Ledermann J., Harter P., Gourley C., et al. Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. N. Engl. J. Med. 2012, 366(15):1382-1392.
38. Ledermann J., Harter P., Gourley C., et al. Olaparib maintenance therapy in patients with platinum-sensitive relapsed serous ovarian cancer: a preplanned retrospective analysis of outcomes by BRCA status in a randomised phase 2 trial. Lancet Oncol. 2014, 15(8):852-861.
39. Patel A.G., Sarkaria J.N., Kaufmann S.H. Nonhomologous end joining drives poly(ADP-ribose) polymerase (PARP) inhibitor lethality in homologous recombination-deficient cells. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(8):3406-3411.
40. Du W., Elemento O. Cancer systems biology: embracing complexity to develop better anticancer therapeutic strategies. Oncogene 2014.
41. Tentler J.J., Tan A.C., Weekes C.D., et al. Patient-derived tumour xenografts as models for oncology drug development. Nat. Rev. Clin. Oncol. 2012, 9(6):338-350.
42. Ocana A., Pandiella A., Siu L.L., Tannock I.F. Preclinical development of molecular-targeted agents for cancer. Nat. Rev. Clin. Oncol. 2011, 8(4):200-209.
43. Morton C.L., Houghton P.J. Establishment of human tumor xenografts in immunodeficient mice. Nat. Protoc. 2007, 2(2):247-250.
44. Zhao B., Li L., Wang L., Wang C.Y., Yu J., Guan K.L. Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis. Genes Dev. 2012, 26(1):54-68.
45. Huang H.L., Hsing H.W., Lai T.C., et al. Trypsin-induced proteome alteration during cell subculture in mammalian cells. J. Biomed. Sci. 2010, 17:36.
46. Domcke S., Sinha R., Levine D.A., Sander C., Schultz N. Evaluating cell lines as tumour models by comparison of genomic profiles. Nat. Commun. 2013, 4:2126.
47. Buick R.N., Pullano R., Trent J.M. Comparative properties of five human ovarian adenocarcinoma cell lines. Cancer Res. 1985, 45(8):3668-3676.
48. Kerbel R.S. 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(4 Suppl. 1):S134-S139.
49. Topp M.D., Hartley L., Cook M., et al. Molecular correlates of platinum response in human high-grade serous ovarian cancer patient-derived xenografts. Mol. Oncol. 2014, 8(3):656-668.
50. Malaney P., Nicosia S.V., Dave V. One mouse, one patient paradigm: new avatars of personalized cancer therapy. Cancer Lett. 2014, 344(1):1-12.
51. Weroha S.J., Becker M.A., Enderica-Gonzalez S., et al. Tumorgrafts as in vivo surrogates for women with ovarian cancer. Clin. Cancer Res. 2014, 20(5):1288-1297.
52. Zhang X., Claerhout S., Prat A., et al. A renewable tissue resource of phenotypically stable, biologically and ethnically diverse, patient-derived human breast cancer xenograft models. Cancer Res. 2013, 73(15):4885-4897.
53. Simpson-Abelson M.R., Sonnenberg G.F., Takita H., et al. Long-term engraftment and expansion of tumor-derived memory T cells following the implantation of non-disrupted pieces of human lung tumor into NOD-scid IL2Rgamma(null) mice. J. Immunol. 2008, 180(10):7009-7018.
54. Yokota S.J., Facciponte J.G., Kelleher R.J., et al. Changes in ovarian tumor cell number, tumor vasculature, and T cell function monitored in vivo using a novel xenograft model. Cancer Immun. 2013, 13:11.
55. Dolmans M.M., Marinescu C., Saussoy P., Van Langendonckt A., Amorim C., Donnez J. Reimplantation of cryopreserved ovarian tissue from patients with acute lymphoblastic leukemia is potentially unsafe. Blood 2010, 116(16):2908-2914.
56. Bankert R.B., Balu-Iyer S.V., Odunsi K., et al. Humanized mouse model of ovarian cancer recapitulates patient solid tumor progression, ascites formation, and metastasis. PLoS ONE 2011, 6(9):e24420.
57. DeRose Y.S., Wang G., Lin Y.C., et al. Tumor grafts derived from women with breast cancer authentically reflect tumor pathology, growth, metastasis and disease outcomes. Nat. Med. 2011, 17(11):1514-1520.
58. Visonneau S., Cesano A., Torosian M.H., Miller E.J., Santoli D. Growth characteristics and metastatic properties of human breast cancer xenografts in immunodeficient mice. Am. J. Pathol. 1998, 152(5):1299-1311.
59. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. U. S. A. 2003, 100(7):3983-3988.
60. Beckhove P., Schutz F., Diel I.J., et al. Efficient engraftment of human primary breast cancer transplants in nonconditioned NOD/Scid mice. Int. J. Cancer 2003, 105(4):444-453.
61. Liu H., Patel M.R., Prescher J.A., et al. Cancer stem cells from human breast tumors are involved in spontaneous metastases in orthotopic mouse models. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(42):18115-18120.
62. Walters D.M., Stokes J.B., Adair S.J., et al. Clinical, molecular and genetic validation of a murine orthotopic xenograft model of pancreatic adenocarcinoma using fresh human specimens. PLoS ONE 2013, 8(10):e77065.
63. Metildi C.A., Kaushal S., Hoffman R.M., Bouvet M. In vivo serial selection of human pancreatic cancer cells in orthotopic mouse models produces high metastatic variants irrespective of Kras status. J. Surg. Res. 2013, 184(1):290-298.
64. Perez-Torras S., Vidal-Pla A., Miquel R., et al. Characterization of human pancreatic orthotopic tumor xenografts suitable for drug screening. Cell. Oncol. (Dordr) 2011, 34(6):511-521.
65. Qiu W., Su G.H. Development of orthotopic pancreatic tumor mouse models. Methods Mol. Biol. 2013, 980:215-223.
66. Chai M.G., Kim-Fuchs C., Angst E., Sloan E.K. Bioluminescent orthotopic model of pancreatic cancer progression. J. Vis. Exp. 2013, 76.
67. Kim M.P., Evans D.B., Wang H., Abbruzzese J.L., Fleming J.B., Gallick G.E. Generation of orthotopic and heterotopic human pancreatic cancer xenografts in immunodeficient mice. Nat. Protoc. 2009, 4(11):1670-1680.
68. Kudo-Saito C., Wansley E.K., Gruys M.E., Wiltrout R., Schlom J., Hodge J.W. Combination therapy of an orthotopic renal cell carcinoma model using intratumoral vector-mediated costimulation and systemic interleukin-2. Clin. Cancer Res. 2007, 13(6):1936-1946.
69. Norian L.A., Kresowik T.P., Rosevear H.M., et al. Eradication of metastatic renal cell carcinoma after adenovirus-encoded TNF-related apoptosis-inducing ligand (TRAIL)/CpG immunotherapy. PLoS ONE 2012, 7(2):e31085.
70. Sicklick J.K., Leonard S.Y., Babicky M.L., et al. Generation of orthotopic patient-derived xenografts from gastrointestinal stromal tumor. J. Transl. Med. 2014, 12:41.
71. Tracz A., Mastri M., Lee C.R., Pili R., Ebos J.M. Modeling spontaneous metastatic renal cell carcinoma (mRCC) in mice following nephrectomy. J. Vis. Exp. 2014, 86.
72. Hillman G.G., Wang Y., Che M., et al. Progression of renal cell carcinoma is inhibited by genistein and radiation in an orthotopic model. BMC Cancer 2007, 7:4.
73. Mathieu A., Remmelink M., D'Haene N., et al. Development of a chemoresistant orthotopic human nonsmall cell lung carcinoma model in nude mice: analyses of tumor heterogeneity in relation to the immunohistochemical levels of expression of cyclooxygenase-2, ornithine decarboxylase, lung-related resistance protein, prostaglandin E synthetase, and glutathione-S-transferase-alpha (GST)-alpha, GST-mu, and GST-pi. Cancer 2004, 101(8):1908-1918.
74. Mordant P., Loriot Y., Lahon B., et al. Bioluminescent orthotopic mouse models of human localized non-small cell lung cancer: feasibility and identification of circulating tumour cells. PLoS ONE 2011, 6(10):e26073.
75. Justilien V., Fields A.P. Utility and applications of orthotopic models of human non-small cell lung cancer (NSCLC) for the evaluation of novel and emerging cancer therapeutics. Curr. Protoc. Pharmacol. 2013, 62(Unit 14):27.
76. Onn A., Isobe T., Itasaka S., et al. Development of an orthotopic model to study the biology and therapy of primary human lung cancer in nude mice. Clin. Cancer Res. 2003, 9(15):5532-5539.
77. Rozenberg G.I., Monahan K.B., Torrice C., Bear J.E., Sharpless N.E. Metastasis in an orthotopic murine model of melanoma is independent of RAS/RAF mutation. Melanoma Res. 2010, 20(5):361-371.
78. Mueller A.J., Maniotis A.J., Freeman W.R., et al. An orthotopic model for human uveal melanoma in SCID mice. Microvasc. Res. 2002, 64(2):207-213.
79. Bobek V., Kolostova K., Pinterova D., et al. A clinically relevant, syngeneic model of spontaneous, highly metastatic B16 mouse melanoma. Anticancer Res. 2010, 30(12):4799-4803.
80. Landis M.D., Lehmann B.D., Pietenpol J.A., Chang J.C. Patient-derived breast tumor xenografts facilitating personalized cancer therapy. Breast Cancer Res. 2013, 15(1):201.
81. Kelland L. The resurgence of platinum-based cancer chemotherapy. Nat. Rev. Cancer 2007, 7(8):573-584.
82. Telli M. Optimizing chemotherapy in triple-negative breast cancer: the role of platinum. Am. Soc. Clin. Oncol. Educ. Book 2014, e37-e42.
83. Garralda E., Paz K., Lopez-Casas P.P., et al. Integrated next-generation sequencing and avatar mouse models for personalized cancer treatment. Clin. Cancer Res. 2014, 20(9):2476-2484.
84. Ishikawa F. Modeling normal and malignant human hematopoiesis in vivo through newborn NSG xenotransplantation. Int. J. Hematol. 2013, 98(6):634-640.
85. Eggermont A.M., Robert C. Melanoma: smart therapeutic strategies in immuno-oncology. Nat. Rev. Clin. Oncol. 2014, 11(4):181-182.
86. Odunsi K., Old L.J. Tumor infiltrating lymphocytes: indicators of tumor-related immune responses. Cancer Immun. 2007, 7:3.
87. Finn O.J. Immuno-oncology: understanding the function and dysfunction of the immune system in cancer. Ann. Oncol. 2012, 23(Suppl. 8):viii6-viii9.
88. Wognum A.W., Eaves A.C., Thomas T.E. Identification and isolation of hematopoietic stem cells. Arch. Med. Res. 2003, 34(6):461-475.
89. Notta F., Doulatov S., Laurenti E., Poeppl A., Jurisica I., Dick J.E. Isolation of single human hematopoietic stem cells capable of long-term multilineage engraftment. Science 2011, 333(6039):218-221.
90. Furness S.G., McNagny K. Beyond mere markers: functions for CD34 family of sialomucins in hematopoiesis. Immunol. Res. 2006, 34(1):13-32.
91. Quintana E., Shackleton M., Sabel M.S., Fullen D.R., Johnson T.M., Morrison S.J. Efficient tumour formation by single human melanoma cells. Nature 2008, 456(7222):593-598.
92. Shultz L.D., Brehm M.A., Garcia-Martinez J.V., Greiner D.L. Humanized mice for immune system investigation: progress, promise and challenges. Nat. Rev. Immunol. 2012, 12(11):786-798.
93. Rongvaux A., Willinger T., Martinek J., et al. Development and function of human innate immune cells in a humanized mouse model. Nat. Biotechnol. 2014, 32(4):364-372.
94. Werner-Klein M., Proske J., Werno C., et al. Immune humanization of immunodeficient mice using diagnostic bone marrow aspirates from carcinoma patients. PLoS ONE 2014, 9(5):e97860.
95. Wege A.K., Schmidt M., Ueberham E., et al. Co-transplantation of human hematopoietic stem cells and human breast cancer cells in NSG mice: a novel approach to generate tumor cell specific human antibodies. MAbs 2014, 6(4):968-977.
96. Chen K., Ahmed S., Adeyi O., Dick J.E., Ghanekar A. Human solid tumor xenografts in immunodeficient mice are vulnerable to lymphomagenesis associated with Epstein-Barr virus. PLoS ONE 2012, 7(6):e39294.
97. John T., Yanagawa N., Kohler D., et al. Characterization of lymphomas developing in immunodeficient mice implanted with primary human non-small cell lung cancer. J. Thorac. Oncol. 2012, 7(7):1101-1108.
98. Zenger E., Abbey N.W., Weinstein M.D., et al. Injection of human primary effusion lymphoma cells or associated macrophages into severe combined immunodeficient mice causes murine lymphomas. Cancer Res. 2002, 62(19):5536-5542.
99. Shibata S., Asano T., Ogura A., et al. SCID-bg mice as xenograft recipients. Lab. Anim. 1997, 31(2):163-168.
100. Bosma M.J., Carroll A.M. The SCID mouse mutant: definition, characterization, and potential uses. Annu. Rev. Immunol. 1991, 9:323-350.
101. Green M., Rogers D., Russell P., et al. The SCID/Beige mouse as a model to investigate protection against Yersinia pestis. FEMS Immunol. Med. Microbiol. 1999, 23(2):107-113.
102. Shultz L.D., Lyons B.L., Burzenski L.M., 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(10):6477-6489.
103. Dainiak M.B., Kumar A., Galaev I.Y., Mattiasson B. Methods in cell separations. Adv. Biochem. Eng. Biotechnol. 2007, 106:1-18.
104. Rudnicka D., Oszmiana A., Finch D.K., et al. Rituximab causes a polarization of B cells that augments its therapeutic function in NK-cell-mediated antibody-dependent cellular cytotoxicity. Blood 2013, 121(23):4694-4702.
105. Cang S., Mukhi N., Wang K., Liu D. Novel CD20 monoclonal antibodies for lymphoma therapy. J. Hematol. Oncol. 2012, 5:64.
106. Dienstmann R., Rodon J., Tabernero J. Optimal design of trials to demonstrate the utility of genomically-guided therapy: putting precision cancer medicine to the test. Mol. Oncol. 2014.
107. Dong X., Guan J., English J.C., et al. Patient-derived first generation xenografts of non-small cell lung cancers: promising tools for predicting drug responses for personalized chemotherapy. Clin. Cancer Res. 2010, 16(5):1442-1451.
108. Garber K. Personal mouse colonies give hope for pancreatic cancer patients. J. Natl. Cancer Inst. 2007, 99(2):105-107.
109. Zhou Y., Zhu S., Cai C., et al. High-throughput screening of a CRISPR/Cas9 library for functional genomics in human cells. Nature 2014, 509(7501):487-491.
110. Wei Y., Xu F., Li P. Technology-driven and evidence-based genomic analysis for integrated pediatric and prenatal genetics evaluation. J. Genet. Genomics 2013, 40(1):1-14.
111. Giles F.J., DeAngelo D.J., Baccarani M., et al. Optimizing outcomes for patients with advanced disease in chronic myelogenous leukemia. Semin. Oncol. 2008, 35(1 Suppl. 1):S1-S17. (quiz S18-20).
112. Fichtner I., Rolff J., Soong R., et al. Establishment of patient-derived non-small cell lung cancer xenografts as models for the identification of predictive biomarkers. Clin. Cancer Res. 2008, 14(20):6456-6468.
113. Zhang J., Zhang L., Su X., et al. Translating the therapeutic potential of AZD4547 in FGFR1-amplified non-small cell lung cancer through the use of patient-derived tumor xenograft models. Clin. Cancer Res. 2012, 18(24):6658-6667.
114. Zhang X.C., Zhang J., Li M., et al. Establishment of patient-derived non-small cell lung cancer xenograft models with genetic aberrations within EGFR, KRAS and FGFR1: useful tools for preclinical studies of targeted therapies. J. Transl. Med. 2013, 11:168.
115. Kortmann U., McAlpine J.N., Xue H., et al. Tumor growth inhibition by olaparib in BRCA2 germline-mutated patient-derived ovarian cancer tissue xenografts. Clin. Cancer Res. 2011, 17(4):783-791.
116. Das Thakur M., Salangsang F., Landman A.S., et al. Modelling vemurafenib resistance in melanoma reveals a strategy to forestall drug resistance. Nature 2013, 494(7436):251-255.
117. 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(13):3989-3998.
118. Ma C.X., Cai S., Li S., et al. Targeting Chk1 in p53-deficient triple-negative breast cancer is therapeutically beneficial in human-in-mouse tumor models. J. Clin. Invest. 2012, 122(4):1541-1552.
119. Dave B., Landis M.D., Tweardy D.J., et al. Selective small molecule Stat3 inhibitor reduces breast cancer tumor-initiating cells and improves recurrence free survival in a human-xenograft model. PLoS ONE 2012, 7(8):e30207.
120. Oakes S.R., Vaillant F., Lim E., et al. Sensitization of BCL-2-expressing breast tumors to chemotherapy by the BH3 mimetic ABT-737. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(8):2766-2771.
121. Vaillant F., Merino D., Lee L., et al. Targeting BCL-2 with the BH3 mimetic ABT-199 in estrogen receptor-positive breast cancer. Cancer Cell 2013, 24(1):120-129.
122. Julien S., Merino-Trigo A., Lacroix L., et al. Characterization of a large panel of patient-derived tumor xenografts representing the clinical heterogeneity of human colorectal cancer. Clin. Cancer Res. 2012, 18(19):5314-5328.
123. Pawaskar D.K., Straubinger R.M., Fetterly G.J., et al. Synergistic interactions between sorafenib and everolimus in pancreatic cancer xenografts in mice. Cancer Chemother. Pharmacol. 2013, 71(5):1231-1240.
124. Rubio-Viqueira B., Jimeno A., Cusatis G., et al. An in vivo platform for translational drug development in pancreatic cancer. Clin. Cancer Res. 2006, 12(15):4652-4661.
125. Cao P., Maira S.M., Garcia-Echeverria C., Hedley D.W. Activity of a novel, dual PI3-kinase/mTor inhibitor NVP-BEZ235 against primary human pancreatic cancers grown as orthotopic xenografts. Br. J. Cancer 2009, 100(8):1267-1276.
126. Al-Ejeh F., Pajic M., Shi W., et al. Gemcitabine and CHK1 inhibition potentiate EGFR-directed radioimmunotherapy against pancreatic ductal adenocarcinoma. Clin. Cancer Res. 2014, 20(12):3187-3197.
127. Sivanand S., Pena-Llopis S., Zhao H., et al. A validated tumorgraft model reveals activity of dovitinib against renal cell carcinoma. Sci. Transl. Med. 2012, 4(137):137ra175.
128. Su B., Zhao W., Shi B., et al. Let-7d suppresses growth, metastasis, and tumor macrophage infiltration in renal cell carcinoma by targeting COL3A1 and CCL7. Mol. Cancer 2014, 13:206.
129. Stewart EG R., Bradley C., Griffiths L.M., Benavente C., Twarog N.R., Miller G.M., Caufield W., Freeman B.B., Bahrami A., Pappo A., Wu J., Loh S., Karlstrom A., Calabrese C., Gordon B., Tsurkan L., Hatfield M.J., Potter P.M., Snyder S.M., Thiagarajan S., Shirinifard A., Sablauer A., Shelat A., Dyer M.A. Targeting the DNA repair pathway in Ewing sarcoma. Cell Rep. 2014, 9:829-840.