436
Views
1
CrossRef citations to date
0
Altmetric
Review

Organotypic-liver slide culture systems to explore the role of extracellular vesicles in pancreatic cancer metastatic behavior and guide new therapeutic approaches

ORCID Icon, , , ORCID Icon & ORCID Icon
Pages 937-946 | Received 09 Jan 2021, Accepted 30 Apr 2021, Published online: 21 May 2021

References

  • Rawla P, Sunkara T, Gaduputi V. Epidemiology of pancreatic cancer: global trends, etiology and risk factors. World J. Oncol. 2019;10(1):10–27.
  • McGuigan A, Kelly P, Turkington RC, et al. Pancreatic cancer: a review of clinical diagnosis, epidemiology, treatment and outcomes. World J Gastroenterol. 2018;24(43):4846–4861.
  • Zhang L, Sanagapalli S, Stoita A. Challenges in diagnosis of pancreatic cancer. World J Gastroenterol. 2018;24(19):2047–2060.
  • Singhi AD, Koay EJ, Chari ST, et al. Early detection of pancreatic cancer: opportunities and challenges. Gastroenterology. 2019;156(7):2024–2040.
  • Brodt P. Role of the microenvironment in liver metastasis: from pre- to prometastatic niches. Clin Cancer Res. 2016;22(24):5971–5982.
  • Peixoto RD, Speers C, McGahan CE, et al. Prognostic factors and sites of metastasis in unresectable locally advanced pancreatic cancer. Cancer Med. 2015;4(8):1171–1177.
  • Oweira H, Petrausch U, Helbling D, et al. Prognostic value of site-specific metastases in pancreatic adenocarcinoma: a surveillance epidemiology and end results database analysis. World J Gastroenterol. 2017;23(10):1872–1880.
  • Orth M, Metzger P, Gerum S, et al. Pancreatic ductal adenocarcinoma: biological hallmarks, current status, and future perspectives of combined modality treatment approaches, Radiat. Oncol 2019;14:141.
  • Das S, Batra SK. Pancreatic cancer metastasis: are we being pre-EMTed?. Curr Pharm Des. 2015;21(10):1249–1255.
  • Houg DS, Bijlsma MF. The hepatic pre-metastatic niche in pancreatic ductal adenocarcinoma, Mol. Cancer. 2018;17:95.
  • Fidler IJ, Poste G. The “seed and soil” hypothesis revisited. Lancet Oncol. 2008;9(8):808.
  • Costa-Silva B, Aiello NM, Ocean AJ, et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Bio. 2015;17(6):816–826. .
  • Karamitopoulou E. Tumour microenvironment of pancreatic cancer: immune landscape is dictated by molecular and histopathological features. Br J Cancer. 2019;121(1):5–14.
  • Ren B, Cui M, Yang G, et al. Tumor microenvironment participates in metastasis of pancreatic cancer. Mol Cancer. 2018;17(1):108.
  • Wortzel I, Dror S, Kenific CM, et al. Exosome-Mediated Metastasis: communication from a Distance. Dev Cell. 2019;49(3):347–360.
  • Mashouri L, Yousefi H, Aref AR, et al. Exosomes: composition, biogenesis, and mechanisms in cancer metastasis and drug resistance. Mol Cancer. 2019;18(1):75.
  • Whiteside TL. Tumor-Derived Exosomes and Their Role in Cancer Progression. In Adv. Clin. Chem.. Academic Press Inc.; 2016;74:103–141. DOI: 10.1016/bs.acc.2015.12.005.
  • Baglio SR, Lagerweij T, Pérez-Lanzón M, et al. Blocking tumor-educated MSC paracrine activity halts osteosarcoma progression, Clin. Cancer Res. 2017;23:3721–3733.
  • Abels ER, Breakefield XO. Introduction to extracellular vesicles: biogenesis, RNA cargo selection, content, release, and uptake. Cell Mol Neurobiol. 2016;36(3):301–312.
  • Liu D, Dong Z, Wang J, et al. The existence and function of mitochondrial component in extracellular vesicles. Mitochondrion. 2020;54:122–127.
  • Kogure A, Yoshioka Y, Ochiya T. Extracellular vesicles in cancer metastasis: potential as therapeutic targets and materials. Int J Mol Sci. 2020;21(12):4463.
  • Berenguer J, Lagerweij T, Zhao XW, et al. Glycosylated extracellular vesicles released by glioblastoma cells are decorated by CCL18 allowing for cellular uptake via chemokine receptor CCR8. J Extracell Vesicles. 2018;7(1):1446660.
  • Tian H, Pang J, Qin K, et al. A novel Tissue-Based Liver–Kidney-on-a-Chip Can Mimic Liver Tropism of extracellular vesicles derived from breast cancer cells. Biotechnol. J. 2020;15(2):1900107.
  • Zhao H, Achreja A, Iessi E, et al. The key role of extracellular vesicles in the metastatic process. Biochim. Biophys. Acta - Rev. Cancer. 2018;1869(1):64–77.
  • Chin AR, Wang SE, Wang SE. Cancer-derived extracellular vesicles: the “soil conditioner” in breast cancer metastasis? HHS Public Access. Cancer Metastasis Rev. 2016;35(4):669–676.
  • Melo SA, Luecke LB, Kahlert C, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. (n.d.);523(7559):177–182.
  • Frampton AE, Mato Prado M, López-Jiménez E, et al. Glypican-1 is enriched in circulating-exosomes in pancreatic cancer and correlates with tumor burden. Oncotarget. 2018;9(27):19006–19013.
  • Chio IIC, Chio IIC, M. Ayres Pereira M. Metastasis in pancreatic ductal Adenocarcinoma: current standing and methodologies. Genes (Basel). 2019;11(1):6. .
  • Hingorani SR, Wang L, Multani AS, et al. Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell. 2005;7(5):469–483.
  • Liby KT, Royce DB, Risingsong R, et al. Synthetic triterpenoids prolong survival in a transgenic mouse model of pancreatic cancer. Cancer Prev Res. 2010;3(11):1427–1434.
  • Zhang G, Du YCN. Orthotopic pancreatic tumor mouse models of liver metastasis. In: Methods Mol. Biol.. Humana Press Inc; 2019;1882:309-320. DOI: 10.1007/978-1-4939-8879-2_27.
  • Avan A, Caretti V, Funel N, et al. Crizotinib inhibits metabolic inactivation of gemcitabine in c-Met-driven pancreatic carcinoma. Cancer Res. 2013;73(22):6745–6756.
  • Ouyang Y, Tang Y, Fu L, et al. Exosomes secreted by chronic hepatitis B patients with PNALT and liver inflammation grade ≥ A2 promoted the progression of liver cancer by transferring miR‐25‐3p to inhibit the co‐expression of TCF21 and HHIP. Cell Prolif. 2020;53(7). DOI:10.1111/cpr.12833.
  • Jiang K, Dong C, Yin Z, Li R, Mao J, Wang C, Zhang J, Gao Z, Liang R, Wang Q, Wang L. Exosome-derived ENO1 regulates integrin α6β4 expression and promotes hepatocellular carcinoma growth and metastasis. Cell Death Dis. 2020 Nov 12;11(11):972. doi:10.1038/s41419-020-03179-1.
  • Justus CR, Leffler N, Ruiz-Echevarria M, et al. In vitro cell migration and invasion assays. J Vis Exp. 2014;51046. DOI:10.3791/51046.
  • Xu H, Lyu X, Yi M, et al. Organoid technology and applications in cancer research. J Hematol Oncol. 2018;11(1):116.
  • Arnold J, Schattschneider J, Blechner C, et al. Tubulin Tyrosine Ligase like 4 (TTLL4) overexpression in breast cancer cells is associated with brain metastasis and alters exosome biogenesis. J Exp Clin Cancer Res. 2020;39(1). DOI:10.1186/s13046-020-01712-w.
  • Cruz VH, Arner EN, Du W, et al. Axl-mediated activation of TBK1 drives epithelial plasticity in pancreatic cancer. JCI Insight. 2019;4(9). DOI:10.1172/jci.insight.126117.
  • Cho J-H, Oh A-Y, Park S, et al. Loss of NF2 induces TGFβ receptor 1–mediated Noncanonical and Oncogenic TGFβ signaling: implication of the therapeutic effect of TGFβ receptor 1 inhibitor on NF2 syndrome. Mol Cancer Ther. 2018;17(11):2271–2284.
  • Karnoub AE, Dash AB, Vo AP, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature. 2007;449(7162):557–563.
  • Langhans SA. Three-dimensional in vitro cell culture models in drug discovery and drug repositioning. Front. Pharmacol. 2018;9:6.
  • Griffith LG, Swartz MA. Capturing complex 3D tissue physiology in vitro. Nat Rev Mol Cell Biol. 2006;7(3):211–224.
  • Ho WJ, Pham EA, Kim JW, et al. Incorporation of multicellular spheroids into 3-D polymeric scaffolds provides an improved tumor model for screening anticancer drugs. Cancer Sci. 2010;101(12):2637–2643.
  • Simian M, Bissell MJ. Organoids: a historical perspective of thinking in three dimensions. J Cell Biol. 2017;216(1):31–40.
  • Sato T, Vries RG, Snippert HJ, et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature. 2009;459(7244):262–265.
  • Apáti Á, Varga N, Berecz T, et al. Application of human pluripotent stem cells and pluripotent stem cell-derived cellular models for assessing drug toxicity. Expert Opin Drug Metab Toxicol. 2019;15(1):61–75.
  • Prior N, Inacio P, Huch M. Liver organoids: from basic research to therapeutic applications. Gut. 2019;68(12):2228–2237.
  • Padmanaban V, Grasset EM, Neumann NM, et al. Organotypic culture assays for murine and human primary and metastatic-site tumors. Nat Protoc. 2020;15(8):2413–2442.
  • D’angelo E, Natarajan D, Sensi F, et al. Patient-Derived Scaffolds of Colorectal Cancer Metastases as an Organotypic 3D model of the liver metastatic microenvironment. Cancers (Basel). 2020;12(2):364.
  • Markus J, Landry T, Stevens Z, et al. Human small intestinal organotypic culture model for drug permeation, inflammation, and toxicity assays. Vitr. Cell. Dev. Biol. - Anim. 2020. DOI:10.1007/s11626-020-00526-6.
  • Humpel C. Organotypic brain slice cultures: a review. Neuroscience. 2015;305:86–98.
  • Worboys PD, Bradbury A, Houston JB. Kinetics of drug metabolism in rat liver slices. Drug Metab Dispos. 1997;25(4):460–467.
  • Sivakumar R, Chan M, Shin S, et al. Organotypic tumor slice cultures provide a versatile platform for immuno-oncology and drug discovery. OncoImmunology. 2019;8(12):e1670019.
  • Eisemann T, Costa B, Strelau J, et al. An advanced glioma cell invasion assay based on organotypic brain slice cultures. BMC Cancer. 2018;18(1):103.
  • Rodrigues G, Hoshino A, Kenific CM, et al. Tumour exosomal CEMIP protein promotes cancer cell colonization in brain metastasis. Nat Cell Bio. 2019;21(11):1403–1412.
  • Martin SZ, Wagner DC, Hörner N, et al. Ex vivo tissue slice culture system to measure drug-response rates of hepatic metastatic colorectal cancer. BMC Cancer. 2019;19(1):1030.
  • Suckert T, Rassamegevanon T, Müller J, et al. Applying tissue slice culture in cancer Research-Insights from preclinical proton radiotherapy. Cancers (Basel). 2020;12(6):1589.
  • Wu X, Roberto JB, Knupp A, et al. Precision-cut human liver slice cultures as an immunological platform. J Immunol Methods. 2018;455:71–79.
  • Koch A, Saran S, Tran DDH, et al. Murine precision-cut liver slices (PCLS): a new tool for studying tumor microenvironments and cell signaling ex vivo. Cell Commun Signal. 2014;12(1):73.
  • Jiang X, Seo YD, Sullivan KM, et al. Establishment of slice cultures as a tool to study the cancer immune microenvironment. In: Methods Mol. Biol. Humana Press Inc; 2019;1884:283-295. DOI: 10.1007/978-1-4939-8885-3_20.
  • Michael A, Falgari G, Annels N, et al. Organotypic slice ovarian cancer model as a platform to test novel therapeutics. Ann Oncol. 2016;27:vi535.
  • Misra S, Moro CF, Del Chiaro M, et al. Ex vivo organotypic culture system of precision-cut slices of human pancreatic ductal adenocarcinoma. Sci Rep. 2019;9(1). DOI:10.1038/s41598-019-38603-w.
  • Lim CY, Chang JH, Lee WS, et al. Organotypic slice cultures of pancreatic ductal adenocarcinoma preserve the tumor microenvironment and provide a platform for drug response. Pancreatology. 2018;18(8):913–927.
  • Kenerson HL, Sullivan KM, Seo YD, et al. Tumor slice culture as a biologic surrogate of human cancer. Ann. Transl. Med. 2020;8(4):114.
  • Haykal MM, Nahmias C, Varon C, et al. Organotypic modeling of the tumor landscape. Front Cell Dev Biol. 2020;8:1406.
  • Spennati G, Horowitz LF, McGarry DJ, et al. Organotypic platform for studying cancer cell metastasis. Exp Cell Res. 2021;401(2):112527.
  • Blazquez R, Pukrop T. 3D coculture model of the brain Parenchyma-Metastasis interface of brain metastasis. Methods Mol Biol. 2017;1612:213–222.
  • Palma E, Doornebal EJ, Chokshi S. Precision-cut liver slices: a versatile tool to advance liver research. Hepatol Int. 2019;13(1):51–57.
  • Wurdinger T, Badr C, Pike L, et al. A secreted luciferase for ex vivo monitoring of in vivo processes. Nat Methods. 2008;5(2):171–173.
  • Maftouh M, Belo AI, Avan A, et al. Galectin-4 expression is associated with reduced lymph node metastasis and modulation of Wnt/β-catenin signalling in pancreatic adenocarcinoma. Oncotarget. 2014;30(14):5335–5349.
  • Firuzi O, Che PP, El Hassouni B, et al. Role of c-MET inhibitors in overcoming drug resistance in spheroid models of primary human pancreatic cancer and stellate cells. Cancers (Basel). 2019;11(5):638.
  • De Graaf IAM, Olinga P, De Jager MH, et al. Preparation and incubation of precision-cut liver and intestinal slices for application in drug metabolism and toxicity studies. Nat Protoc. 2010;5(9):1540–1551.
  • Starokozhko V, Vatakuti S, Schievink B, et al. Maintenance of drug metabolism and transport functions in human precision-cut liver slices during prolonged incubation for 5 days. Arch Toxicol. 2017;91(5):2079–2092.
  • Kruepunga N, Hakvoort TBM, Hikspoors JPJM, et al. Anatomy of rodent and human livers: what are the differences? Biochim Biophys Acta - Mol Basis Dis. 2019;1865(5):869–878.
  • Odom DT, Dowell RD, Jacobsen ES, et al. Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Nature Genetics. 2007;39(6):730–732.
  • Zimmermann M, Lampe J, Lange S, et al. Improved reproducibility in preparing precision-cut liver tissue slices. Cytotechnology. 2009;61(3):145–152.
  • Pearen MA, Lim HK, Gratte FD, et al. Murine precision-cut liver slices as an ex vivo model of liver biology. J Vis Exp. 2020;2020:e60992.
  • Rebours V, Albuquerque M, Sauvanet A, et al. A. Couvelard, Hypoxia pathways and cellular stress activate pancreatic stellate cells: development of an Organotypic culture model of thick slices of normal human pancreas. 2013;8(9):e76229. DOI: 10.1371/journal.pone.0076229.
  • Obatomi DK, Brant S, Anthonypillai V, et al. Optimizing preincubation conditions for precision-cut rat kidney and liver tissue slices: effect of culture media and antioxidants. Toxicol Vitr. 1998;12(6):725–737.
  • Catania JR, McGarrigle BP, Rittenhouse-Olson K, et al. Induction of CYP2B and CYP2E1 in precision-cut rat liver slices cultured in defined medium. Toxicol Vitr. 2007;21(1):109–115.
  • Van Midwoud PM, Merema MT, Verweij N, et al. Hydrogel embedding of precision-cut liver slices in a microfluidic device improves drug metabolic activity. Biotechnol Bioeng. 2011;108(6):1404–1412.
  • Gandolfi AJ, Wijeweera J, Brendel K. Use of precision-cut liver slices as an in vitro tool for evaluating liver function. In Toxicol.. Pathol SAGE Publications Inc. 1996;24(1):58–61. DOI: 10.1177/019262339602400108.
  • Marquardt A, Halle S, Seckert CK, et al. Single cell detection of latent cytomegalovirus reactivation in host tissue. J Gen Virol. 2011;92(6):1279–1291.
  • Stoff-Khalili MA, Stoff A, Rivera AA, et al. Preclinical evaluation of transcriptional targeting strategies for carcinoma of the breast in a tissue slice model system. Breast Cancer Res. 2005;7(6):R1141.
  • Savelyev SA, Larsson KC, Johansson AS, et al. Slice preparation, organotypic tissue culturing and luciferase recording of clock gene activity in the suprachiasmatic nucleus. J Vis Exp. 2010. DOI:10.3791/2439.
  • Nave R, Fisher R, Zech K. In vitro metabolism of ciclesonide in human lung and liver precision-cut tissue slices. Biopharm. Drug Dispos. 2006;27(4):197–207.
  • Westra IM, Mutsaers HAM, Luangmonkong T, et al. Human precision-cut liver slices as a model to test antifibrotic drugs in the early onset of liver fibrosis. Toxicol Vitr. 2016;35:77–85.
  • Tannenbaum J, Bennett BT. Russell and Burch’s 3Rs then and now: the need for clarity in definition and purpose. J Am Assoc Lab Anim Sci. 2015;5(4): 120–132. /pmc/articles/PMC4382615/?report=abstract (accessed January 6, 2021.
  • Giovannetti CL, Van Der Borden CL, Frampton AE, et al., E. Never let it go: stopping key mechanisms underlying metastasis to fight pancreatic cancer. Semin Cancer Biol. 2017;44:43–59. Epub 2017 Apr 22.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.