An Integrative Approach to Precision Cancer Medicine Using Patient-Derived Xenografts |
Cho, Sung-Yup
(Department of Life Science, Ewha Womans University)
Kang, Wonyoung (Department of Life Science, Ewha Womans University) Han, Jee Yun (Department of Life Science, Ewha Womans University) Min, Seoyeon (Department of Life Science, Ewha Womans University) Kang, Jinjoo (Department of Life Science, Ewha Womans University) Lee, Ahra (Department of Life Science, Ewha Womans University) Kwon, Jee Young (Department of Life Science, Ewha Womans University) Lee, Charles (Department of Life Science, Ewha Womans University) Park, Hansoo (Department of Life Science, Ewha Womans University) |
1 | Pao, W., Miller, V., Zakowski, M., Doherty, J., Politi, K., Sarkaria, I., Singh, B., Heelan, R., Rusch, V., Fulton, L., et al. (2004). EGF receptor gene mutations are common in lung cancers from "never smokers" and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc. Natl. Acad. Sci. USA 101, 13306- 13311. DOI |
2 | Park, H., Cho, S.Y., Kim, H., Na, D., Han, J.Y., Chae, J., Park, C., Park, O.K., Min, S, Kang, J., et al. (2015). Genomic alterations in BCL2L1 and DLC1 contribute to drug sensitivity in gastric cancer. Proc. Natl. Acad. Sci. USA 112, 12492-12497. DOI |
3 | Quintas-Cardama, A., and Cortes, J. (2009). Molecular biology of bcr-abl1-positive chronic myeloid leukemia. Blood 113, 1619- 1630. DOI |
4 | Reyal, F., Guyader, C., Decraene, C., Lucchesi, C., Auger, N., Assayag, F., De Plater, L., Gentien, D., Poupon, M.F., Cottu, P., et al. (2012). Molecular profiling of patient-derived breast cancer xenografts. Breast Cancer Res. 14, R11. DOI |
5 | Reyes, G., Villanueva, A., Garcia, C., Sancho, F.J., Piulats, J., Lluis, F., and Capella, G. (1996). Orthotopic xenografts of human pancreatic carcinomas acquire genetic aberrations during dissemination in nude mice. Cancer Res. 56, 5713-5719. |
6 | Rongvaux, A., Willinger, T., Martinek, J., Strowig, T., Gearty, S.V., Teichmann, L.L., Saito, Y., Marches, F., Halene, S., Palucka, A.K., et al. (2014). Development and function of human innate immune cells in a humanized mouse model. Nat. Biotechnol. 32, 364-U230. DOI |
7 | Rosen, J.M., and Jordan, C.T. (2009). The increasing complexity of the cancer stem cell paradigm. Science 324, 1670-1673. DOI |
8 | Rosfjord, E., Lucas, J., Li, G., and Gerber, H.P. (2014). Advances in patient-derived tumor xenografts: From target identification to predicting clinical response rates in oncology. Biochem. Pharmacol. 91, 135-143. DOI |
9 | Von Hoff, D.D., Ramanathan, R.K., Borad, M.J., Laheru, D.A., Smith, L.S., Wood, T.E., Korn, R.L., Desai, N., Trieu, V., Iglesias, J.L., et al. (2011). Gemcitabine plus nab-paclitaxel is an active regimen in patients with advanced pancreatic cancer: a phase I/II trial. J. Clin. Oncol. 29, 4548-4554. DOI |
10 | Von Hoff, D.D., Ervin, T., Arena, F.P., Chiorean, E.G., Infante, J., Moore, M., Seay, T., Tjulandin, S.A., Ma, W.W., Saleh, M.N., et al. (2013). Increased survival in pancreatic cancer with nabpaclitaxel plus gemcitabine. N. Engl. J. Med. 369, 1691-1703. DOI |
11 | Weinstein, J.N., Collisson, E.A., Mills, G.B., Shaw, K.R.M., Ozenberger, B.A., Ellrott, K., Shmulevich, I., Sander, C., and Stuart, J.M. (2013). The cancer genome atlas pan-cancer analysis project. Nat. Genet. 45, 1113-1120. DOI |
12 | Wetterauer, C., Vlajnic, T., Schuler, J., Gsponer, J.R., Thalmann, G.N., Cecchini, M., Schneider, J., Zellweger, T., Pueschel, H., Bachmann, A., et al. (2015). Early development of human lymphomas in a prostate cancer xenograft program using triple knock-out immunocompromised mice. Prostate 75, 585-592. DOI |
13 | Whittle, J.R., Lewis, M.T., Lindeman, G.J., and Visvader, J.E. (2015). Patient-derived xenograft models of breast cancer and their predictive power. Breast Cancer Res. 17, 17. DOI |
14 | Williams, S.A., Anderson, W.C., Santaguida, M.T., and Dylla, S.J. (2013). Patient-derived xenografts, the cancer stem cell paradigm, and cancer pathobiology in the 21st century. Lab. Invest. 93, 970-982. DOI |
15 | Zhang, X.M., Claerhout, S., Prat, A., Dobrolecki, L.E., Petrovic, I., Lai, Q., Landis, M.D., Wiechmann, L., Schiff, R., Giuliano, M., et al. (2013). A Renewable tissue resource of phenotypically stable, biologically and ethnically diverse, patient-derived human breast cancer xenograft models. Cancer Res. 73, 4885-4897. DOI |
16 | Bertolini, G., Roz, L., Perego, P., Tortoreto, M., Fontanella, E., Gatti, L., Pratesi, G., Fabbri, A., Andriani, F., Tinelli, S., et al. (2009). Highly tumorigenic lung cancer CD133(+) cells display stem-like features and are spared by cisplatin treatment. Proc. Natl. Acad. Sci. USA 106, 16281-16286. DOI |
17 |
Agliano, A., Martin-Padura, I., Mancuso, P., Marighetti, P., Rabascio, C., Pruneri, G., Shultz, L.D., and Bertolini, F. (2008). Human acute leukemia cells injected in NOD/LtSz-scid/IL- |
18 | Aparicio, S., Hidalgo, M., and Kung, A.L. (2015). Examining the utility of patient-derived xenograft mouse models. Nat. Rev. Cancer 15, 311-316. DOI |
19 | Aytes, A., Mollevi, D.G., Martinez-Iniesta, M., Nadal, M., Vidal, A., Morales, A., Salazar, R., Capella, G., and Villanueva, A. (2012). Stromal interaction molecule 2 (STIM2) is frequently overexpressed in colorectal tumors and confers a tumor cell growth suppressor phenotype. Mol. Carcinog. 51, 746-753. DOI |
20 | Bell, D., Berchuck, A., Birrer, M., Chien, J., Cramer, D.W., Dao, F., Dhir, R., DiSaia, P., Gabra, H., Glenn, P., et al. (2011). Integrated genomic analyses of ovarian carcinoma. Nature 474, 609-615. DOI |
21 | Bertotti, A., Migliardi, G., Galimi, F., Sassi, F., Torti, D., Isella, C., Cora, D., Di Nicolantonio, F., Buscarino, M., Petti, C., et al. (2011). A molecularly annotated platform of patient-derived xenografts ("xenopatients") identifies HER2 as an effective therapeutic target in cetuximab-resistant colorectal cancer. Cancer Discov. 1, 508-523. DOI |
22 | Chen, K., Ahmed, S., Adeyi, O., Dick, J.E., and Ghanekar, A. (2012). Human solid tumor xenografts in immunodeficient mice are vulnerable to lymphomagenesis associated with Epstein-Barr virus. PLoS One 7, e39294. DOI |
23 | Choi, S.Y.C., Lin, D., Gout, P.W., Collins, C.C., Xu, Y., and Wang, Y.Z. (2014). Lessons from patient-derived xenografts for better in vitro modeling of human cancer. Adv. Drug Deliver. Rev. 79-80, 222-237. DOI |
24 | Das Thakur, M., Salangsang, F., Landman, A.S., Sellers, W.R., Pryer, N.K., Levesque, M.P., Dummer, R., McMahon, M., and Stuart, D.D. (2013). Modelling vemurafenib resistance in melanoma reveals a strategy to forestall drug resistance. Nature 494, 251-255. DOI |
25 | DiMasi, J.A., Reichert, J.M., Feldman, L., and Malins, A. (2013). Clinical approval success rates for investigational cancer drugs. Clin. Pharmacol. Ther. 94, 329-335. DOI |
26 | de Groot, J.F., Fuller, G., Kumar, A.J., Piao, Y., Eterovic, K., Ji, Y.J., and Conrad, C.A. (2010). Tumor invasion after treatment of glioblastoma with bevacizumab: radiographic and pathologic correlation in humans and mice. Neuro. Oncol. 12, 233-242. DOI |
27 | Delitto, D., Pham, K., Vlada, A.C., Sarosi, G.A., Thomas, R.M., Behrns, K.E., Liu, C., Hughes, S.J., Wallet, S.M., and Trevino, J.G. (2015). Patient-derived xenograft models for pancreatic adenocarcinoma demonstrate retention of tumor morphology through incorporation of murine stromal elements. Am. J. Pathol. 185, 1297-1303. DOI |
28 | DeRose, Y.S., Wang, G.Y., Lin, Y.C., Bernard, P.S., Buys, S.S., Ebbert, M.T.W., Factor, R., Matsen, C., Milash, B.A., Nelson, E., et al. (2011). Tumor grafts derived from women with breast cancer authentically reflect tumor pathology, growth, metastasis and disease outcomes. Nat. Med. 17, 1514-1520 DOI |
29 | Ding, L., Ellis, M.J., Li, S.Q., Larson, D.E., Chen, K., Wallis, J., Harris, C.C., McLellan, M.D., Fulton, R.S., Fulton, L.L., et al. (2010). Genome remodelling in a basal-like breast cancer metastasis and xenograft. Nature 464, 999-1005. DOI |
30 | Dong, X., Guan, J., English, J.C., Flint, J., Yee, J., Evans, K., Murray, N., Macaulay, C., Ng, R.T., Gout, P.W., et al. (2010). Patientderived first generation xenografts of non-small cell lung cancers: promising tools for predicting drug responses for personalized chemotherapy. Clin. Cancer Res. 16, 1442-1451. DOI |
31 | Dowst, H., Pew, B., Watkins, C., McOwiti, A., Barney, J., Qu, S., Becnel, L. B. (2015). Acquire: an open-source comprehensive cancer biobanking system. Bioinformatics 31, 1655-1662. DOI |
32 | Gao, D., and Chen, Y. (2015). Organoid development in cancer genome discovery. Curr. Opin. Genet. Dev. 30, 42-48. DOI |
33 | Eirew, P., Steif, A., Khattra, J., Ha, G., Yap, D., Farahani, H., Gelmon, K., Chia, S., Mar, C., Wan, A., et al. (2015). Dynamics of genomic clones in breast cancer patient xenografts at single-cell resolution. Nature 518, 422-426. DOI |
34 |
Fernandez de Sanmamamed, M., Lopez Rodriguez, I., Schalper, K.A., Onate, C., Azpilikueta, A., Rodriguez-Ruiz, M.E., Morales- Kastresana, A., Labiano, S., Perez-Gracia, J.L., Martin-Algarra, S., et al. (2015). Nivolumab and urelumab enhance antitumor activity of human T lymphocytes engrafted in Rag2-/-IL2R |
35 | Fichtner, I., Rolff, J., Soong, R., Hoffmann, J., Hammer, S., Sommer, A., Becker, M., and Merk, J. (2008). Establishment of patientderived non-small cell lung cancer xenografts as models for the identification of predictive biomarkers. Clin. Cancer Res. 14, 6456-6468. DOI |
36 | Gao, H., Korn, J.M., Ferretti, S., Monahan, J.E., Wang, Y., Singh, M., Zhang, C., Schnell, C., Yang, G., Zhang, Y., et al. (2015). Highthroughput screening using patient-derived tumor xenografts to predict clinical trial drug response. Nat. Med. 21, 1318-1325. DOI |
37 | Garraway, L.A., Verweij, J., and Ballman, K.V. (2013). Precision oncology: an overview. J. Clin. Oncol. 31, 1803-1805. DOI |
38 | Garrido-Laguna, I., Uson, M., Rajeshkumar, N.V., Tan, A.C., de Oliveira, E., Karikari, C., Villaroel, M.C., Salomon, A., Taylor, G., Sharma, R., et al. (2011). Tumor engraftment in nude mice and enrichment in stroma-related gene pathways predict poor survival and resistance to gemcitabine in patients with pancreatic cancer. Clin. Cancer Res. 17, 5793-5800. DOI |
39 | Hidalgo, M., Bruckheimer, E., Rajeshkumar, N.V., Garrido-Laguna, I., De Oliveira, E., Rubio-Viqueira, B., Strawn, S., Wick, M.J., Martell, J., and Sidransky, D. (2011). A pilot clinical study of treatment guided by personalized tumorgrafts in patients with advanced cancer. Mol. Cancer Ther. 10, 1311-1316. DOI |
40 | Girotti, M.R., Lopes, F., Preece, N., Niculescu-Duvaz, D., Zambon, A., Davies, L., Whittaker, S., Saturno, G., Viros, A., Pedersen, M., et al. (2015). Paradox-breaking RAF inhibitors that also target SRC are effective in drug-resistant BRAF mutant melanoma. Cancer Cell 27, 85-96. DOI |
41 | Hidalgo, M., Amant, F., Biankin, A.V., Budinska, E., Byrne, A.T., Caldas, C., Clarke, R.B., de Jong, S., Jonkers, J., Maelandsmo, G.M., et al. (2014). Patient-derived xenograft models: an emerging platform for translational cancer research. Cancer Discov. 4, 998-1013. DOI |
42 | Hoffman, R.M. (2015). Patient-derived orthotopic xenografts: better mimic of metastasis than subcutaneous xenografts. Nat. Rev. Cancer 15, 451-452. DOI |
43 | John, T., Yanagawa, N., Kohler, D., Craddock, K.J., Bandarchi- Chamkhaleh, B., Pintilie, M., Sykes, J., To, C., Li, M., Panchal, D., et al. (2012). Characterization of lymphomas developing in immunodeficient mice implanted with primary human non-small cell lung cancer. J. Thorac. Oncol. 7, 1101-1108. DOI |
44 | Johnson, J.I., Decker, S., Zaharevitz, D., Rubinstein, L.V., Venditti, J., Schepartz, S., Kalyandrug, S., Christian, M., Arbuck, S., Hollingshead, M., et al. (2001). Relationships between drug activity in NCI preclinical in vitro and in vivo models and early clinical trials. Br. J. Cancer 84, 1424-1431. DOI |
45 | Keysar, S.B., Astling, D.P., Anderson, R.T., Vogler, B.W., Bowles, D.W., Morton, J.J., Paylor, J.J., Glogowska, M.J., Le, P.N., Eagles- Soukup, J.R., et al. (2013). A patient tumor transplant model of squamous cell cancer identifies PI3K inhibitors as candidate therapeutics in defined molecular bins. Mol. Oncol. 7, 776- 790. DOI |
46 | Joo, K.M., Kim, J., Jin, J., Kim, M., Seol, H.J., Muradov, J., Yang, H., Choi, Y.L., Park, W.Y., Kong, D.S., et al. (2013). Patient-specific orthotopic glioblastoma xenograft models recapitulate the histopathology and biology of human glioblastomas in situ. Cell Rep. 3, 260-273. DOI |
47 | Julien, S., Merino-Trigo, A., Lacroix, L., Pocard, M., Goere, D., Mariani, P., Landron, S., Bigot, L., Nemati, F., Dartigues, P., et al. (2012). Characterization of a large panel of patient-derived tumor xenografts representing the clinical heterogeneity of human colorectal cancer. Clin. Cancer Res. 18, 5314-5328. DOI |
48 | Kimple, R.J., Harari, P.M., Torres, A.D., Yang, R.Z., Soriano, B.J., Yu, M., Armstrong, E.A., Blitzer, G.C., Smith, M.A., Lorenz, L.D., et al. (2013). Development and characterization of HPV-positive and HPV-negative head and neck squamous cell carcinoma tumorgrafts. Clin. Cancer Res. 19, 855-864. DOI |
49 | Koboldt, D.C., Fulton, R.S., McLellan, M.D., Schmidt, H., Kalicki- Veizer, J., McMichael, J.F., Fulton, L.L., Dooling, D.J., Ding, L., Mardis, E.R., et al. (2012). Comprehensive molecular portraits of human breast tumours. Nature 490, 61-70. DOI |
50 | Kopetz, S., Lemos, R., and Powis, G. (2012). The promise of patient- derived xenografts: the best laid plans of mice and men. Clin. Cancer Res. 18, 5160-5162. DOI |
51 | Kung, A.L. (2007). Practices and pitfalls of mouse cancer models in drug discovery. Adv. Cancer Res. 96, 191-212. |
52 | Lin, D., Wyatt, A. W., Xue, H., Wang, Y., Dong, X., Haegert, A., Wu, R., Brahmbhatt, S., Mo, F., Jong, L., et al. (2014). High fidelity patient-derived xenografts for accelerating prostate cancer discovery and drug development. Cancer Res. 74, 1271-1283. DOI |
53 | Lai, A., Tran, A., Nghiemphu, P.L., Pope, W.B., Solis, O.E., Selch, M., Filka, E., Yong, W.H., Mischel, P.S., Liau, L.M., et al. (2011). Phase II study of bevacizumab plus temozolomide during and after radiation therapy for patients with newly diagnosed glioblastoma multiforme. J. Clin. Oncol. 29, 142-148. DOI |
54 | Landis, M.D., Lehmann, B.D., Pietenpol, J.A., and Chang, J.C. (2013). Patient-derived breast tumor xenografts facilitating personalized cancer therapy. Breast Cancer Res. 15, 201. DOI |
55 | Li, S.Q., Shen, D., Shao, J.Y., Crowder, R., Liu, W.B., Prat, A., He, X.P., Liu, S.Y., Hoog, J., Lu, C., et al. (2013). Endocrine-therapyresistant ESR1 variants revealed by genomic characterization of breast-cancer-derived xenografts. Cell Rep. 4, 1116-1130. DOI |
56 | Macconaill, L.E., and Garraway, L.A. (2010). Clinical implications of the cancer genome. J. Clin. Oncol. 28, 5219-5228. DOI |
57 | Marangoni, E., Vincent-Salomon, A., Auger, N., Degeorges, A., Assayag, F., de Cremoux, P., de Plater, L., Guyader, C., De Pinieux, G., Judde, J.G., et al. (2007). A new model of patient tumorderived breast cancer xenografts for preclinical assays. Clin. Cancer Res. 13, 3989-3998. DOI |
58 | Masso-Valles, D., Jauset, T., Serrano, E., Sodir, N.M., Pedersen, K., Affara, N.I., Whitfield, J.R., Beaulieu, M.E., Evan, G.I., Elias, L., et al. (2015). Ibrutinib exerts potent antifibrotic and antitumor activities in mouse models of pancreatic adenocarcinoma. Cancer Res. 75, 1675-1681. DOI |
59 | Morton, C.L., and Houghton, P.J. (2007). Establishment of human tumor xenografts in immunodeficient mice. Nat. Protoc. 2, 247- 250. DOI |
60 | Mattie, M., Christensen, A., Chang, M.S., Yeh, W., Said, S., Shostak, Y., Capo, L., Verlinsky, A., An, Z.L., Joseph, I., et al. (2013). Molecular characterization of patient-derived human pancreatic tumor xenograft models for preclinical and translational development of cancer therapeutics. Neoplasia 15, 1124-1136. |
61 | Morton, J.J., Bird, G., Keysar, S.B., Astling, D.P., Lyons, T.R., Anderson, R.T., Glogowska, M.J., Estes, P., Eagles, J.R., Le, P.N., et al. (2015). XactMice: humanizing mouse bone marrow enables microenvironment reconstitution in a patient-derived xenograft model of head and neck cancer. Oncogene (Epub ahead of print). |
62 | Muzny, D.M., Bainbridge, M.N., Chang, K., Dinh, H.H., Drummond, J.A., Fowler, G., Kovar, C.L., Lewis, L.R., Morgan, M.B., Newsham, I.F., et al. (2012). Comprehensive molecular characterization of human colon and rectal cancer. Nature 487, 330-337. DOI |
63 | Nardella, C., Lunardi, A., Patnaik, A., Cantley, L.C., and Pandolfi, P.P. (2011). The APL paradigm and the "co-clinical trial" project. Cancer Discov. 1, 108-116. DOI |
64 | Nemati, F., Sastre-Garau, X., Laurent, C., Couturier, J., Mariani, P., Desjardins, L., Piperno-Neumann, S., Lantz, O., Asselain, B., Plancher, C., et al. (2010). Establishment and characterization of a panel of human uveal melanoma xenografts derived from primary and/or metastatic tumors. Clin. Cancer Res. 16, 2352- 2362. DOI |
65 | Ostman, A. (2012). The tumor microenvironment controls drug sensitivity. Nat. Med. 18, 1332-1334. DOI |
66 | Siolas, D., and Hannon, G.J. (2013). Patient-derived tumor xenografts: transforming clinical samples into mouse models. Cancer Res. 73, 5315-5319. DOI |
67 | Schatton, T., Murphy, G.F., Frank, N.Y., Yamaura, K., Waaga- Gasser, A.M., Gasser, M., Zhan, Q., Jordan, S., Duncan, L.M., Weishaupt, C., et al. (2008). Identification of cells initiating human melanomas. Nature 451, 345-349. DOI |
68 | Scott, C.L., Becker, M.A., Haluska, P., and Samimi, G. (2013). Patient- derived xenograft models to improve targeted therapy in epithelial ovarian cancer treatment. Front. Oncol. 3, 295. |
69 | Shaw, A.T., Yeap, B.Y., Solomon, B.J., Riely, G.J., Gainor, J., Engelman, J.A., Shapiro, G.I., Costa, D.B., Ou, S.H.I., Butaney, M., et al. (2011). Effect of crizotinib on overall survival in patients with advanced non-small-cell lung cancer harbouring ALK gene rearrangement: a retrospective analysis. Lancet Oncol. 12, 1004-1012. DOI |
70 | Slamon, D., Eiermann, W., Robert, N., Pienkowski, T., Martin, M., Press, M., Mackey, J., Glaspy, J., Chan, A., Pawlicki, M., et al. (2011). Adjuvant trastuzumab in HER2-positive breast cancer. N. Engl. J. Med. 365, 1273-1283. DOI |
71 | Tentler, J.J., Tan, A.C., Weekes, C.D., Jimeno, A., Leong, S., Pitts, T.M., Arcaroli, J.J., Messersmith, W.A., and Eckhardt, S.G. (2012). Patient-derived tumour xenografts as models for oncology drug development. Nat. Rev. Clin. Oncol. 9, 338-350. DOI |
72 | Verhaak, R.G.W., Hoadley, K.A., Purdom, E., Wang, V., Qi, Y., Wilkerson, M.D., Miller, C.R., Ding, L., Golub, T., Mesirov, J.P., et al. (2010). Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17, 98-110. DOI |
73 | Zhao, X.M., Liu, Z.G., Yu, L.T., Zhang, Y.J., Baxter, P., Voicu, H., Gurusiddappa, S., Luan, J., Su, J.M., Leung, H.C.E., et al. (2012). Global gene expression profiling confirms the molecular fidelity of primary tumor-based orthotopic xenograft mouse models of medulloblastoma. Neuro. Oncol. 14, 574-583. DOI |
74 | Zhang, L.H., Liu, Y.Q., Wang, X.H., Tang, Z.Y., Li, S.X., Hu, Y., Zong, X.L., Wu, X.J., Bu, Z.D., Wu, A.W., et al. (2015). The extent of in flammatory infiltration in primary cancer tissues is associated with lymphomagenesis in immunodeficient mice. Sci. Rep. 5, 9447. DOI |
![]() |