Ex Vivo Tumor Culture Systems for Functional Drug Testing and Therapy Response Prediction

References

• Moja L, Tagliabue L, Balduzzi S et al. Trastuzumab containing regimens for early breast cancer. Cochrane Database Syst. Rev. 4, CD006243 (2012).
   Web of Science ®Google Scholar
• Veale D, Ashcroft T, Marsh C, Gibson GJ, Harris AL. Epidermal growth factor receptors in non-small-cell lung cancer. Br. J. Cancer 55(5), 513–516 (1987).
   PubMed Web of Science ®Google Scholar
• Chang JC, Wooten EC, Tsimelzon A et al. Gene expression profiling for the prediction of therapeutic response to docetaxel in patients with breast cancer. Lancet 362(9381), 362–369 (2003).
   PubMed Web of Science ®Google Scholar
• De Marchi T, Liu NQ, Stingl C et al. 4-Protein signature predicting tamoxifen treatment outcome in recurrent breast cancer. Mol. Oncol. 10(1), 24–39 (2016).
   PubMed Web of Science ®Google Scholar
• Spentzos D, Levine DA, Kolia S et al. Unique gene expression profile based on pathologic response in epithelial ovarian cancer. J. Clin. Oncol. 23(31), 7911–7918 (2005).
   PubMed Web of Science ®Google Scholar
• Alizadeh AA, Aranda V, Bardelli A et al. Toward understanding and exploiting tumor heterogeneity. Nat. Med. 21(8), 846–853 (2015).
   PubMed Web of Science ®Google Scholar
• Marks DL, Olson RL, Fernandez-Zapico ME. Epigenetic control of the tumor microenvironment. Epigenomics 8(12), 1671–1687 (2016).
   PubMed Web of Science ®Google Scholar
• Kelly CM, Janjigian YY. The genomics and therapeutics of HER2-positive gastric cancer-from trastuzumab and beyond. J. Gastrointest. Oncol. 7(5), 750–762 (2016).
   PubMedGoogle Scholar
• Burdall SE, Hanby AM, Lansdown MR, Speirs V. Breast cancer cell lines: friend or foe? Breast Cancer Res. 5(2), 89–95 (2003).
   PubMed Web of Science ®Google Scholar
• Naipal KA, Raams A, Bruens ST et al. Attenuated XPC expression is not associated with impaired DNA repair in bladder cancer. PLoS ONE 10(4), e0126029 (2015).
   PubMed Web of Science ®Google Scholar
• Mukhopadhyay A, Elattar A, Cerbinskaite A et al. Development of a functional assay for homologous recombination status in primary cultures of epithelial ovarian tumor and correlation with sensitivity to poly(ADP-ribose) polymerase inhibitors. Clin. Cancer Res. 16(8), 2344–2351 (2010).
   PubMed Web of Science ®Google Scholar
• Mukhopadhyay A, Plummer ER, Elattar A et al. Clinicopathological features of homologous recombination-deficient epithelial ovarian cancers: sensitivity to PARP inhibitors, platinum, and survival. Cancer Res. 72(22), 5675–5682 (2012).
   PubMed Web of Science ®Google Scholar
• Greshock J, Bachman KE, Degenhardt YY et al. Molecular target class is predictive of in vitro response profile. Cancer Res. 70(9), 3677–3686 (2010).
   PubMed Web of Science ®Google Scholar
• Sos ML, Michel K, Zander T et al. Predicting drug susceptibility of non-small-cell lung cancers based on genetic lesions. J. Clin. Invest. 119(6), 1727–1740 (2009).
   PubMed Web of Science ®Google Scholar
• Lacroix M, Leclercq G. Relevance of breast cancer cell lines as models for breast tumours: an update. Breast Cancer Res. Treat. 83(3), 249–289 (2004).
   PubMed Web of Science ®Google Scholar
• Van Staveren WC, Solis DY, Hebrant A, Detours V, Dumont JE, Maenhaut C. Human cancer cell lines: experimental models for cancer cells in situ? For cancer stem cells? Biochim. Biophys. Acta 1795(2), 92–103 (2009).
   PubMed Web of Science ®Google Scholar
• Masters JR. Human cancer cell lines: fact and fantasy. Nat. Rev. Mol. Cell Biol. 1(3), 233–236 (2000).
   PubMed Web of Science ®Google Scholar
• Fong EL, Harrington DA, Farach-Carson MC, Yu H. Heralding a new paradigm in 3D tumor modeling. Biomaterials 108, 197–213 (2016).
   PubMed Web of Science ®Google Scholar
• Emerman JT, Pitelka DR. Maintenance and induction of morphological differentiation in dissociated mammary epithelium on floating collagen membranes. In Vitro 13(5), 316–328 (1977).
   PubMedGoogle Scholar
• Yin X, Mead BE, Safaee H, Langer R, Karp JM, Levy O. Engineering stem cell organoids. Cell Stem Cell 18(1), 25–38 (2016).
   PubMed Web of Science ®Google Scholar
• Jung P, Sato T, Merlos-Suarez A et al. Isolation and in vitro expansion of human colonic stem cells. Nat. Med. 17(10), 1225–1227 (2011).
   PubMed Web of Science ®Google Scholar
• Sato T, Stange DE, Ferrante M et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 141(5), 1762–1772 (2011).
   PubMed Web of Science ®Google Scholar
• Weeber F, Van De Wetering M, Hoogstraat M et al. Preserved genetic diversity in organoids cultured from biopsies of human colorectal cancer metastases. Proc. Natl Acad. Sci. USA 112(43), 13308–13311 (2015).
   PubMed Web of Science ®Google Scholar
• Bartfeld S, Bayram T, Van De Wetering M et al. In vitro expansion of human gastric epithelial stem cells and their responses to bacterial infection. Gastroenterology 148(1), 126–136; e126 (2015).
   PubMed Web of Science ®Google Scholar
• Boj SF, Hwang CI, Baker LA et al. Organoid models of human and mouse ductal pancreatic cancer. Cell 160(1–2), 324–338 (2015).
   PubMed Web of Science ®Google Scholar
• Broutier L, Andersson-Rolf A, Hindley CJ et al. Culture and establishment of self-renewing human and mouse adult liver and pancreas 3D organoids and their genetic manipulation. Nat. Protoc. 11(9), 1724–1743 (2016).
   PubMed Web of Science ®Google Scholar
• Walsh AJ, Cook RS, Sanders ME, Arteaga CL, Skala MC. Drug response in organoids generated from frozen primary tumor tissues. Sci. Rep. 6, 18889 (2016).
   PubMed Web of Science ®Google Scholar
• Van De Wetering M, Francies HE, Francis JM et al. Prospective derivation of a living organoid biobank of colorectal cancer patients. Cell 161(4), 933–945 (2015).
   PubMed Web of Science ®Google Scholar
• Skardal A, Devarasetty M, Rodman C, Atala A, Soker S. Liver-tumor hybrid organoids for modeling tumor growth and drug response in vitro. Ann. Biomed. Eng. 43(10), 2361–2373 (2015).
   PubMed Web of Science ®Google Scholar
• Alonso-Nocelo M, Abuin C, Lopez-Lopez R, De La Fuente M. Development and characterization of a three-dimensional co-culture model of tumor T cell infiltration. Biofabrication 8(2), 025002 (2016).
   PubMed Web of Science ®Google Scholar
• Bray LJ, Binner M, Holzheu A et al. Multi-parametric hydrogels support 3D in vitro bioengineered microenvironment models of tumour angiogenesis. Biomaterials 53, 609–620 (2015).
   PubMed Web of Science ®Google Scholar
• Majety M, Pradel LP, Gies M, Ries CH. Fibroblasts influence survival and therapeutic response in a 3D co-culture model. PLoS ONE 10(6), e0127948 (2015).
   PubMed Web of Science ®Google Scholar
• Subia B, Dey T, Sharma S, Kundu SC. Target specific delivery of anticancer drug in silk fibroin based 3D distribution model of bone-breast cancer cells. ACS Appl. Mater. Interfaces 7(4), 2269–2279 (2015).
   PubMed Web of Science ®Google Scholar
• Hidalgo M, Amant F, Biankin AV et al. Patient-derived xenograft models: an emerging platform for translational cancer research. Cancer Discov. 4(9), 998–1013 (2014).
   PubMed Web of Science ®Google Scholar
• Williams SA, Anderson WC, Santaguida MT, Dylla SJ. Patient-derived xenografts, the cancer stem cell paradigm, and cancer pathobiology in the 21st century. Lab. Invest. 93(9), 970–982 (2013).
   PubMed Web of Science ®Google Scholar
• Kopetz S, Lemos R, Powis G. The promise of patient-derived xenografts: the best laid plans of mice and men. Clin. Cancer Res. 18(19), 5160–5162 (2012).
   PubMed Web of Science ®Google Scholar
• Kameya T, Shimosato Y, Tumuraya M, Ohsawa N, Nomura T. Human gastric choriocarcinoma serially transplanted in nude mice. J. Natl Cancer Inst. 56(2), 325–332 (1976).
   PubMedGoogle Scholar
• Bertotti A, Migliardi G, Galimi F et al. A molecularly annotated platform of patient-derived xenografts (‘xenopatients’) identifies HER2 as an effective therapeutic target in cetuximab-resistant colorectal cancer. Cancer Discov. 1(6), 508–523 (2011).
   PubMed Web of Science ®Google Scholar
• Daniel VC, Marchionni L, Hierman JS et al. A primary xenograft model of small-cell lung cancer reveals irreversible changes in gene expression imposed by culture in vitro. Cancer Res. 69(8), 3364–3373 (2009).
   PubMed Web of Science ®Google Scholar
• Derose YS, Wang G, Lin YC et al. Tumor grafts derived from women with breast cancer authentically reflect tumor pathology, growth, metastasis and disease outcomes. Nat. Med. 17(11), 1514–1520 (2011).
   PubMed Web of Science ®Google Scholar
• Zhao X, Liu Z, Yu L et al. Global gene expression profiling confirms the molecular fidelity of primary tumor-based orthotopic xenograft mouse models of medulloblastoma. Neuro Oncol. 14(5), 574–583 (2012).
   PubMed Web of Science ®Google Scholar
• Dowst H, Pew B, Watkins C et al. Acquire: an open-source comprehensive cancer biobanking system. Bioinformatics 31(10), 1655–1662 (2015).
   PubMed Web of Science ®Google Scholar
• Nardella C, Lunardi A, Patnaik A, Cantley LC, Pandolfi PP. The APL paradigm and the ‘co-clinical trial’ project. Cancer Discov. 1(2), 108–116 (2011).
   PubMed Web of Science ®Google Scholar
• Chen Z, Cheng K, Walton Z et al. A murine lung cancer co-clinical trial identifies genetic modifiers of therapeutic response. Nature 483(7391), 613–617 (2012).
   PubMed Web of Science ®Google Scholar
• Rubio-Viqueira B, Hidalgo M. Direct in vivo xenograft tumor model for predicting chemotherapeutic drug response in cancer patients. Clin. Pharmacol. Ther. 85(2), 217–221 (2009).
   PubMed Web of Science ®Google Scholar
• Pompili L, Porru M, Caruso C, Biroccio A, Leonetti C. Patient-derived xenografts: a relevant preclinical model for drug development. J. Exp. Clin. Cancer Res. 35(1), 189 (2016).
   PubMedGoogle Scholar
• Hidalgo M, Bruckheimer E, Rajeshkumar NV et al. A pilot clinical study of treatment guided by personalized tumorgrafts in patients with advanced cancer. Mol. Cancer Ther. 10(8), 1311–1316 (2011).
   PubMed Web of Science ®Google Scholar
• Horstmann E, Mccabe MS, Grochow L et al. Risks and benefits of phase 1 oncology trials, 1991 through 2002. N. Engl. J. Med. 352(9), 895–904 (2005).
   PubMed Web of Science ®Google Scholar
• Lawrence MG, Pook DW, Wang H et al. Establishment of primary patient-derived xenografts of palliative TURP specimens to study castrate-resistant prostate cancer. Prostate 75(13), 1475–1483 (2015).
   PubMed Web of Science ®Google Scholar
• Moon HG, Oh K, Lee J et al. Prognostic and functional importance of the engraftment-associated genes in the patient-derived xenograft models of triple-negative breast cancers. Breast Cancer Res. Treat. 154(1), 13–22 (2015).
   PubMed Web of Science ®Google Scholar
• Bergamaschi A, Hjortland GO, Triulzi T et al. Molecular profiling and characterization of luminal-like and basal-like in vivo breast cancer xenograft models. Mol. Oncol. 3(5–6), 469–482 (2009).
   PubMed Web of Science ®Google Scholar
• Dangles-Marie V, Pocard M, Richon S et al. Establishment of human colon cancer cell lines from fresh tumors versus xenografts: comparison of success rate and cell line features. Cancer Res. 67(1), 398–407 (2007).
   PubMed Web of Science ®Google Scholar
• Cassidy JW, Caldas C, Bruna A. Maintaining tumor heterogeneity in patient-derived tumor xenografts. Cancer Res. 75(15), 2963–2968 (2015).
   PubMed Web of Science ®Google Scholar
• Shultz LD, Brehm MA, Garcia-Martinez JV, Greiner DL. Humanized mice for immune system investigation: progress, promise and challenges. Nat. Rev. Immunol. 12(11), 786–798 (2012).
   PubMed Web of Science ®Google Scholar
• Bousquet J, Meunier JM. [Organotypic culture, on natural and artificial media, of fragments of the adult rat hypophysis]. C. R. Seances Soc. Biol. Fil. 156, 65–67 (1962).
   PubMedGoogle Scholar
• Loffredo Sampaolo C. [Chick embryo heart in organotypic culture] Il cuore di embrioni di pollo in coltura organotipica. Boll. Soc. Ital. Biol. Sper. 32(12), 1580–1582 (1956).
   PubMedGoogle Scholar
• Krumdieck CL. Development of a live tissue microtome: reflections of an amateur machinist. Xenobiotica 43(1), 2–7 (2013).
   PubMed Web of Science ®Google Scholar
• Arman AC, Sampath AP. Patch clamp recordings from mouse retinal neurons in a dark-adapted slice preparation. J. Vis. Exp. (43), doi:10.3791/2107 (2010).
   PubMedGoogle Scholar
• Blauer M, Tammela TL, Ylikomi T. A novel tissue-slice culture model for non-malignant human prostate. Cell Tissue Res. 332(3), 489–498 (2008).
   PubMed Web of Science ®Google Scholar
• Laughlin AM, Welsh TH, Jr, Love CC et al. In vitro culture of precision-cut testicular tissue as a novel tool for the study of responses to LH. In vitro Cell. Dev. Biol. Anim. 46(1), 45–53 (2010).
   PubMed Web of Science ®Google Scholar
• Zimmermann M, Lampe J, Lange S et al. Improved reproducibility in preparing precision-cut liver tissue slices. Cytotechnology 61(3), 145–152 (2009).
   PubMed Web of Science ®Google Scholar
• Carranza-Torres IE, Guzman-Delgado NE, Coronado-Martinez C et al. Organotypic culture of breast tumor explants as a multicellular system for the screening of natural compounds with antineoplastic potential. BioMed. Res. Int. 2015, 618021 (2015).
   PubMed Web of Science ®Google Scholar
• Merz F, Gaunitz F, Dehghani F et al. Organotypic slice cultures of human glioblastoma reveal different susceptibilities to treatments. Neuro Oncol. 15(6), 670–681 (2013).
   PubMed Web of Science ®Google Scholar
• Naipal KA, Verkaik NS, Ameziane N et al. Functional ex vivo assay to select homologous recombination-deficient breast tumors for PARP inhibitor treatment. Clin. Cancer Res. 20(18), 4816–4826 (2014).
   PubMed Web of Science ®Google Scholar
• Davies EJ, Dong M, Gutekunst M et al. Capturing complex tumour biology in vitro: histological and molecular characterisation of precision cut slices. Sci. Rep. 5, 17187 (2015).
   PubMed Web of Science ®Google Scholar
• Gerlach MM, Merz F, Wichmann G et al. Slice cultures from head and neck squamous cell carcinoma: a novel test system for drug susceptibility and mechanisms of resistance. Br. J. Cancer 110(2), 479–488 (2014).
   PubMed Web of Science ®Google Scholar
• Koerfer J, Kallendrusch S, Merz F et al. Organotypic slice cultures of human gastric and esophagogastric junction cancer. Cancer Med. 5(7), 1444–1453 (2016).
   PubMed Web of Science ®Google Scholar
• Vaira V, Fedele G, Pyne S et al. Preclinical model of organotypic culture for pharmacodynamic profiling of human tumors. Proc. Natl Acad. Sci. USA 107(18), 8352–8356 (2010).
   PubMed Web of Science ®Google Scholar
• Naipal KA, Verkaik NS, Sanchez H et al. Tumor slice culture system to assess drug response of primary breast cancer. BMC Cancer 16, 78 (2016).
   PubMed Web of Science ®Google Scholar
• Toniatti C, Jones P, Graham H, Pagliara B, Draetta G. Oncology drug discovery: planning a turnaround. Cancer Discov. 4(4), 397–404 (2014).
   PubMed Web of Science ®Google Scholar
• Rubin EH, Gilliland DG. Drug development and clinical trials – the path to an approved cancer drug. Nat. Rev. Clin. Oncol. 9(4), 215–222 (2012).
   PubMed Web of Science ®Google Scholar
• Van Der Kuip H, Murdter TE, Sonnenberg M et al. Short term culture of breast cancer tissues to study the activity of the anticancer drug taxol in an intact tumor environment. BMC Cancer 6, 86 (2006).
   PubMed Web of Science ®Google Scholar
• Hammond EM, Asselin MC, Forster D, O'connor JP, Senra JM, Williams KJ. The meaning, measurement and modification of hypoxia in the laboratory and the clinic. Clin. Oncol. (R. Coll. Radiol.) 26(5), 277–288 (2014).
   PubMed Web of Science ®Google Scholar
• Majumder B, Baraneedharan U, Thiyagarajan S et al. Predicting clinical response to anticancer drugs using an ex vivo platform that captures tumour heterogeneity. Nat. Commun. 6, 6169 (2015).
   PubMed Web of Science ®Google Scholar
• Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U, Stein H. Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J. Immunol. 133(4), 1710–1715 (1984).
   PubMed Web of Science ®Google Scholar
• Zhang W, Lee WY, Zilberberg J. Tissue engineering platforms to replicate the tumor microenvironment of multiple myeloma. Methods Mol. Biol. 1513, 171–191 (2017).
   PubMedGoogle Scholar
• Lee DH, Bae CY, Kwon S, Park JK. User-friendly 3D bioassays with cell-containing hydrogel modules: narrowing the gap between microfluidic bioassays and clinical end-users’ needs. Lab Chip 15(11), 2379–2387 (2015).
   PubMed Web of Science ®Google Scholar
• Bersini S, Jeon JS, Dubini G et al. A microfluidic 3D in vitro model for specificity of breast cancer metastasis to bone. Biomaterials 35(8), 2454–2461 (2014).
   PubMed Web of Science ®Google Scholar
• Lu YT, Pendharkar GP, Lu CH, Chang CM, Liu CH. A microfluidic approach towards hybridoma generation for cancer immunotherapy. Oncotarget 6(36), 38764–38776 (2015).
   PubMedGoogle Scholar
• Han B, Qu C, Park K, Konieczny SF, Korc M. Recapitulation of complex transport and action of drugs at the tumor microenvironment using tumor-microenvironment-on-chip. Cancer Lett. 380(1), 319–329 (2016).
   PubMed Web of Science ®Google Scholar
• Bakmand T, Troels-Smith AR, Dimaki M et al. Fluidic system for long-term in vitro culturing and monitoring of organotypic brain slices. Biomed. Microdev. 17(4), 71 (2015).
   PubMed Web of Science ®Google Scholar
• Holliday DL, Moss MA, Pollock S et al. The practicalities of using tissue slices as preclinical organotypic breast cancer models. J. Clin. Pathol. 66(3), 253–255 (2013).
   PubMed Web of Science ®Google Scholar