Long-lived pancreatic ductal adenocarcinoma slice cultures enable precise study of the immune microenvironment

References

• Cancer Facts & Figures 2016. Available at: http://www.cancer.org/acs/groups/content/@research/documents/…/acspc-047079.pdf.
   Google Scholar
• Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012; 62:10-29; PMID:22237781; https://doi.org/10.3322/caac.20138
   PubMed Web of Science ®Google Scholar
• Sener SF, Fremgen A, Menck HR, Winchester DP. Pancreatic cancer: a report of treatment and survival trends for 100,313 patients diagnosed from 1985-1995, using the National Cancer Database. J Am Coll Surg 1999; 189:1-7; PMID:10401733; https://doi.org/10.1016/S1072-7515(99)00075-7
   PubMed Web of Science ®Google Scholar
• Feig C, Gopinathan A, Neesse A, Chan DS, Cook N, Tuveson DA. The pancreas cancer microenvironment. Clin Cancer Res 2012; 18:4266-76; PMID:22896693; https://doi.org/10.1158/1078-0432.CCR-11-3114
   PubMed Web of Science ®Google Scholar
• Clark CE, Hingorani SR, Mick R, Combs C, Tuveson DA, Vonderheide RH. Dynamics of the immune reaction to pancreatic cancer from inception to invasion. Cancer Res 2007; 67:9518-27; PMID:17909062; https://doi.org/10.1158/0008-5472.CAN-07-0175
   PubMed Web of Science ®Google Scholar
• Shibuya KC, Goel VK, Xiong W, Sham JG, Pollack SM, Leahy AM, Whiting SH, Yeh MM, Yee C, Riddell SR et al. Pancreatic ductal adenocarcinoma contains an effector and regulatory immune cell infiltrate that is altered by multimodal neoadjuvant treatment. PLoS One 2014; 9:e96565; PMID:24794217; https://doi.org/10.1371/journal.pone.0096565
   PubMed Web of Science ®Google Scholar
• Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363:711-23; PMID:20525992; https://doi.org/10.1056/NEJMoa1003466
   PubMed Web of Science ®Google Scholar
• Robert C, Long GV, Brady B, Dutriaux C, Maio M, Mortier L, Hassel JC, Rutkowski P, McNeil C, Kalinka-Warzocha E et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med 2015; 372:320-30; PMID:25399552; https://doi.org/10.1056/NEJMoa1412082
   PubMed Web of Science ®Google Scholar
• Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012; 366:2455-65; PMID:22658128; https://doi.org/10.1056/NEJMoa1200694
   PubMed Web of Science ®Google Scholar
• Royal RE, Levy C, Turner K, Mathur A, Hughes M, Kammula US, Sherry RM, Topalian SL, Yang JC, Lowy I et al. Phase 2 trial of single agent Ipilimumab (anti-CTLA-4) for locally advanced or metastatic pancreatic adenocarcinoma. J Immunother 2010; 33:828-33; PMID:20842054; https://doi.org/10.1097/CJI.0b013e3181eec14c
   PubMed Web of Science ®Google Scholar
• Ino Y, Yamazaki-Itoh R, Shimada K, Iwasaki M, Kosuge T, Kanai Y, Hiraoka N. Immune cell infiltration as an indicator of the immune microenvironment of pancreatic cancer. Br J Cancer 2013; 108:914-23; PMID:23385730; https://doi.org/10.1038/bjc.2013.32
   PubMed Web of Science ®Google Scholar
• Fridman WH, Pages F, Sautes-Fridman C, Galon J. The immune contexture in human tumours: Impact on clinical outcome. Nat Rev Cancer 2012; 12:298-306; PMID:22419253; https://doi.org/10.1038/nrc3245
   PubMed Web of Science ®Google Scholar
• Collins MA, Bednar F, Zhang Y, Brisset JC, Galbán S, Galbán CJ, Rakshit S, Flannagan KS, Adsay NV, Pasca di Magliano M. Oncogenic Kras is required for both the initiation and maintenance of pancreatic cancer in mice. J Clin Invest 2012; 122:639-53; PMID:22232209; https://doi.org/10.1172/JCI59227
   PubMed Web of Science ®Google Scholar
• de Kanter R, Monshouwer M, Meijer DK, Groothuis GM. Precision-cut organ slices as a tool to study toxicity and metabolism of xenobiotics with special reference to non-hepatic tissues. Curr Drug Metab 2002; 3:39-59; PMID:11878310; https://doi.org/10.2174/1389200023338071
   PubMed Web of Science ®Google Scholar
• Guyot C, Lepreux S, Combe C, Sarrazy V, Billet F, Balabaud C, Bioulac-Sage P, Desmoulière A. Fibrogenic cell phenotype modifications during remodelling of normal and pathological human liver in cultured slices. Liver Int 2010; 30:1529-40; PMID:20846345; https://doi.org/10.1111/j.1478-3231.2010.02342.x
   PubMed Web of Science ®Google Scholar
• Gerlach MM, Merz F, Wichmann G, Kubick C, Wittekind C, Lordick F, Dietz A, Bechmann I. Slice cultures from head and neck squamous cell carcinoma: A novel test system for drug susceptibility and mechanisms of resistance. Br J Cancer 2014; 110:479-88; PMID:24263061; https://doi.org/10.1038/bjc.2013.700
   PubMed Web of Science ®Google Scholar
• Marciniak A, Cohrs CM, Tsata V, Chouinard JA, Selck C, Stertmann J, Reichelt S, Rose T, Ehehalt F, Weitz J et al. Using pancreas tissue slices for in situ studies of islet of Langerhans and acinar cell biology. Nat Protoc 2014; 9:2809-22; PMID:25393778; https://doi.org/10.1038/nprot.2014.195
   PubMed Web of Science ®Google Scholar
• Marciniak A, Selck C, Friedrich B, Speier S. Mouse pancreas tissue slice culture facilitates long-term studies of exocrine and endocrine cell physiology in situ. PLoS One 2013; 8:e78706; PMID:24223842; https://doi.org/10.1371/journal.pone.0078706
   PubMed Web of Science ®Google Scholar
• Rebours V, Albuquerque M, Sauvanet A, Ruszniewski P, Lévy P, Paradis V, Bedossa P, Couvelard A. Hypoxia pathways and cellular stress activate pancreatic stellate cells: Development of an organotypic culture model of thick slices of normal human pancreas. PLoS One 2013; 8:e76229; PMID:24098783; https://doi.org/10.1371/journal.pone.0076229
   PubMed Web of Science ®Google Scholar
• van Geer MA, Kuhlmann KF, Bakker CT, ten Kate FJ, Oude Elferink RP, Bosma PJ. Ex-vivo evaluation of gene therapy vectors in human pancreatic (cancer) tissue slices. World J Gastroenterol 2009; 15:1359-66; PMID:19294766; https://doi.org/10.3748/wjg.15.1359
   PubMed Web of Science ®Google Scholar
• Thornton EE, Krummel MF, Looney MR. Live imaging of the lung. Current Protocols in Cytometry 60:12.28:12.28.1–12.28.12; PMID:22470155; https://doi.org/10.1002/0471142956.cy1228s60
   PubMedGoogle Scholar
• Cummings RJ, Mitra S, Lord EM, Foster TH. Antibody-labeled fluorescence imaging of dendritic cell populations in vivo. J Biomed Opt 2008; 13:044041; PMID:19021368; https://doi.org/10.1117/1.2966122
   PubMed Web of Science ®Google Scholar
• Mastropasqua L, Nubile M, Lanzini M, Carpineto P, Ciancaglini M, Pannellini T, Di Nicola M, Dua HS. Epithelial dendritic cell distribution in normal and inflamed human cornea: In vivo confocal microscopy study. Am J Ophthalmol 2006; 142:736-44; PMID:17056357; https://doi.org/10.1016/j.ajo.2006.06.057
   PubMed Web of Science ®Google Scholar
• Salmon H, Franciszkiewicz K, Damotte D, Dieu-Nosjean MC, Validire P, Trautmann A, Mami-Chouaib F, Donnadieu E. Matrix architecture defines the preferential localization and migration of T cells into the stroma of human lung tumors. J Clin Invest 2012; 122:899-910; PMID:22293174; https://doi.org/10.1172/JCI45817
   PubMed Web of Science ®Google Scholar
• Kong YM, Dahlke C, Xiang Q, Qian Y, Karp D, Scheuermann RH. Toward an ontology-based framework for clinical research databases. J Biomed Inform 2011; 44:48-58; PMID:20460173; https://doi.org/10.1016/j.jbi.2010.05.001
   PubMed Web of Science ®Google Scholar
• Neesse A, Michl P, Frese KK, Feig C, Cook N, Jacobetz MA, Lolkema MP, Buchholz M, Olive KP, Gress TM et al. Stromal biology and therapy in pancreatic cancer. Gut 2011; 60:861-8; PMID:20966025; https://doi.org/10.1136/gut.2010.226092
   PubMed Web of Science ®Google Scholar
• Kadaba R, Birke H, Wang J, Hooper S, Andl CD, Di Maggio F, Soylu E, Ghallab M, Bor D, Froeling FE et al. Imbalance of desmoplastic stromal cell numbers drives aggressive cancer processes. J Pathol 2013; 230:107-17; PMID:23359139; https://doi.org/10.1002/path.4172
   PubMed Web of Science ®Google Scholar
• De Monte L, Reni M, Tassi E, Clavenna D, Papa I, Recalde H, Braga M, Di Carlo V, Doglioni C, Protti MP. Intratumor T helper type 2 cell infiltrate correlates with cancer-associated fibroblast thymic stromal lymphopoietin production and reduced survival in pancreatic cancer. J Exp Med 2011; 208:469-78; PMID:21339327; https://doi.org/10.1084/jem.20101876
   PubMed Web of Science ®Google Scholar
• Davies EJ, Dong M, Gutekunst M, Närhi K, van Zoggel HJ, Blom S, Nagaraj A, Metsalu T, Oswald E, Erkens-Schulze S et al. Capturing complex tumour biology in vitro: Histological and molecular characterisation of precision cut slices. Sci Rep 2015; 5:17187; PMID:26647838; https://doi.org/10.1038/srep17187
   PubMed Web of Science ®Google Scholar
• Kang C, Qiao Y, Li G, Baechle K, Camelliti P, Rentschler S, Efimov IR. Human organotypic cultured cardiac slices: New platform for high throughput preclinical human trials. Sci Rep 2016; 6:28798; PMID:27356882; https://doi.org/10.1038/srep28798
   PubMed Web of Science ®Google Scholar
• Fujita H, Ohuchida K, Mizumoto K, Nakata K, Yu J, Kayashima T, Cui L, Manabe T, Ohtsuka T, Tanaka M. alpha-smooth muscle actin expressing stroma promotes an aggressive tumor biology in pancreatic ductal adenocarcinoma. Pancreas; November 2010; 39(8):1254-1262; PMID:20467342; https://doi.org/10.1097/MPA.0b013e3181dbf647
   PubMedGoogle Scholar
• Erkan M, Michalski CW, Rieder S, Reiser-Erkan C, Abiatari I, Kolb A, Giese NA, Esposito I, Friess H, Kleeff J. The activated stroma index is a novel and independent prognostic marker in pancreatic ductal adenocarcinoma. Clin Gastroenterol Hepatol 2008; 6:1155-61; PMID:18639493; https://doi.org/10.1016/j.cgh.2008.05.006
   PubMed Web of Science ®Google Scholar
• Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B et al. Fiji: An open-source platform for biological-image analysis. Nat Methods 2012; 9:676-82; PMID:22743772; https://doi.org/10.1038/nmeth.2019
   PubMed Web of Science ®Google Scholar