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Organoid research in digestive system tumors (Review)
- Authors:
- Xiaoxiao Yang
- Xuewen Xu
- Haitao Zhu
- Ming Wang
- Dongqing Wang
-
Affiliations: Department of Radiology, The Affiliated Hospital of Jiangsu University, Zhenjiang, Jiangsu 212031, P.R. China - Published online on: February 21, 2021 https://doi.org/10.3892/ol.2021.12569
- Article Number: 308
-
Copyright: © Yang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
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Lau H, Kranenburg O, Xiao H and Yu J: Organoid models of gastrointestinal cancers in basic and translational research. Nat Rev Gastroenterol Hepatol. 17:203–222. 2020. View Article : Google Scholar : PubMed/NCBI | |
Wei W, Zeng H, Zheng R, Zhang S, An L, Chen R, Wang S, Sun K, Matsuda T, Bray F and He J: Cancer registration in China and its role in cancer prevention and control. Lancet Oncol. 21:e342–e349. 2020. View Article : Google Scholar : PubMed/NCBI | |
Gähwiler BH, Capogna M, Debanne D, McKinney RA and Thompson SM: Organotypic slice cultures: A technique has come of age. Trends Neurosci. 20:471–477. 1997. View Article : Google Scholar : PubMed/NCBI | |
Fatehullah A, Tan SH and Barker N: Organoids as an in vitro model of human development and disease. Nat Cell Biol. 18:246–254. 2016. View Article : Google Scholar : PubMed/NCBI | |
Clevers H: Modeling development and disease with organoids. Cell. 165:1586–1597. 2016. View Article : Google Scholar : PubMed/NCBI | |
Dutta D, Heo I and Clevers H: Disease modeling in stem cell-derived 3D organoid systems. Trends Mol Med. 23:393–410. 2017. View Article : Google Scholar : PubMed/NCBI | |
Chen J, Lau BT, Andor N, Grimes SM, Handy C, Wood-Bouwens C and Ji HP: Single-cell transcriptome analysis identifies distinct cell types and niche signaling in a primary gastric organoid model. Sci Rep. 9:45362019. View Article : Google Scholar : PubMed/NCBI | |
Hartl L, Huelsz-Prince G, van Zon J and Tans SJ: Apical constriction is necessary for crypt formation in small intestinal organoids. Dev Biol. 450:76–81. 2019. View Article : Google Scholar : PubMed/NCBI | |
Artegiani B, van Voorthuijsen L, Lindeboom RGH, Seinstra D, Heo I, Tapia P, López-Iglesias C, Postrach D, Dayton T, Oka R, et al: Probing the tumor suppressor function of BAP1 in CRISPR-engineered human liver organoids. Cell Stem Cell. 24:927–943.e6. 2019. View Article : Google Scholar : PubMed/NCBI | |
Matsuura T, Maru Y, Izumiya M, Hoshi D, Kato S, Ochiai M, Hori M, Yamamoto S, Tatsuno K, Imai T, et al: Organoid-based ex vivo reconstitution of Kras-driven pancreatic ductal carcinogenesis. Carcinogenesis. 41:490–501. 2020. View Article : Google Scholar : PubMed/NCBI | |
Shu Y and Chua CW: An organoid assay for long-term maintenance and propagation of mouse prostate luminal epithelial progenitors and cancer cells. Methods Mol Biol. 1940:231–254. 2019. View Article : Google Scholar : PubMed/NCBI | |
Gao D and Chen Y: Organoid development in cancer genome discovery. Curr Opin Genet Dev. 30:42–48. 2015. View Article : Google Scholar : PubMed/NCBI | |
Schumacher D, Andrieux G, Boehnke K, Keil M, Silvestri A, Silvestrov M, Keilholz U, Haybaeck J, Erdmann G, Sachse C, et al: Heterogeneous pathway activation and drug response modelled in colorectal-tumor-derived 3D cultures. PLoS Genet. 15:e10080762019. View Article : Google Scholar : PubMed/NCBI | |
Corrò C, Novellasdemunt L and Li VSW: A brief history of organoids. Am J Physiol Cell Physiol. 319:C151–C165. 2020. View Article : Google Scholar : PubMed/NCBI | |
Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, van Es JH, Abo A, Kujala P, Peters PJ and Clevers H: Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature. 459:262–265. 2009. View Article : Google Scholar : PubMed/NCBI | |
Neal J, Li X, Zhu J, Giangarra V, Grzeskowiak CL, Ju J, Liu IH, Chiou SH, Salahudeen AA, Smith AR, et al: Organoid modeling of the tumor immune microenvironment. Cell. 175:1972–1988.e16. 2018. View Article : Google Scholar : PubMed/NCBI | |
Wild CP, Weiderpass E and Stewart BW: World Cancer Report: Cancer Research for Cancer Prevention. World Health Organisation; Geneva, Switzerland: pp. 23–33. 2020, PubMed/NCBI | |
Liu HD, Xia BR, Jin MZ and Lou G: Organoid of ovarian cancer: genomic analysis and drug screening. Clinical and Translational Oncology. 22:1240–1251. 2020. View Article : Google Scholar : PubMed/NCBI | |
Bartfeld S, Bayram T, van de Wetering M, Huch M, Begthel H, Kujala P, Vries R, Peters PJ and Clevers H: In vitro expansion of human gastric epithelial stem cells and their responses to bacterial infection. Gastroenterology. 148:126–136.e6. 2015. View Article : Google Scholar : PubMed/NCBI | |
Bertaux-Skeirik N, Centeno J, Gao J, Gabre J and Zavros Y: Oncogenic transformation of human-derived gastric organoids. Methods Mol Biol. 1576:205–213. 2019. View Article : Google Scholar : PubMed/NCBI | |
Nagle PW, Plukker JTM, Muijs CT, van Luijk P and Coppes RP: Patient-derived tumor organoids for prediction of cancer treatment response. Semin Cancer Biol. 53:258–264. 2018. View Article : Google Scholar : PubMed/NCBI | |
Wenzel C, Riefke B, Gründemann S, Krebs A, Christian S, Prinz F, Osterland M, Golfier S, Räse S, Ansari N, et al: 3D high-content screening for the identification of compounds that target cells in dormant tumor spheroid regions. Exp Cell Res. 323:131–143. 2014. View Article : Google Scholar : PubMed/NCBI | |
Arena S, Corti G, Durinikova E, Montone M, Reilly NM, Russo M, Lorenzato A, Arcella P, Lazzari L, Rospo G, et al: A subset of colorectal cancers with cross-sensitivity to olaparib and oxaliplatin. Clin Cancer Res. 26:1372–1384. 2020. View Article : Google Scholar : PubMed/NCBI | |
Yao Y, Xu X, Yang L, Zhu J, Wan J, Shen L, Xia F, Fu G, Deng Y, Pan M, et al: Patient-derived organoids predict chemoradiation responses of locally advanced rectal cancer. Cell Stem Cell. 26:17–26.e6. 2020. View Article : Google Scholar : PubMed/NCBI | |
Skardal A, Shupe T and Atala A: Organoid-on-a-chip and body-on-a-chip systems for drug screening and disease modeling. Drug Discov Today. 21:1399–1411. 2016. View Article : Google Scholar : PubMed/NCBI | |
Saito Y: Establishment of an organoid bank of biliary tract and pancreatic cancers and its application for personalized therapy and future treatment. J Gastroenterol Hepatol. 34:1906–1910. 2019. View Article : Google Scholar : PubMed/NCBI | |
van de Wetering M, Francies HE, Francis JM, Bounova G, Iorio F, Pronk A, van Houdt W, van Gorp J, Taylor-Weiner A, Kester L, et al: Prospective derivation of a living organoid biobank of colorectal cancer patients. Cell. 161:933–945. 2015. View Article : Google Scholar : PubMed/NCBI | |
Kondo J and Inoue MJC: Application of cancer organoid model for drug screening and personalized therapy. Cells. 8:4702019. View Article : Google Scholar | |
Broutier L, Mastrogiovanni G, Verstegen MM, Francies HE, Gavarró LM, Bradshaw CR, Allen GE, Arnes-Benito R, Sidorova O, Gaspersz MP, et al: Human primary liver cancer-derived organoid cultures for disease modeling and drug screening. Nat Med. 23:1424–1435. 2017. View Article : Google Scholar : PubMed/NCBI | |
Fong ELS, Toh TB, Lin QXX, Liu Z, Hooi L, Mohd Abdul Rashid MB, Benoukraf T, Chow EK, Huynh TH and Yu H: Generation of matched patient-derived xenograft in vitro-in vivo models using 3D macroporous hydrogels for the study of liver cancer. Biomaterials. 159:229–240. 2018. View Article : Google Scholar : PubMed/NCBI | |
Siegel RL, Miller KD and Jemal A: Cancer statistics, 2016. CA Cancer J Clin. 66:7–30. 2016. View Article : Google Scholar : PubMed/NCBI | |
Zhang HC and Kuo CJ: Personalizing pancreatic cancer organoids with hPSCs. Nat Med. 21:1249–1251. 2015. View Article : Google Scholar : PubMed/NCBI | |
Boj SF, Hwang CI, Baker LA, Chio II, Engle DD, Corbo V, Jager M, Ponz-Sarvise M, Tiriac H, Spector MS, et al: Organoid models of human and mouse ductal pancreatic cancer. Cell. 160:324–338. 2015. View Article : Google Scholar : PubMed/NCBI | |
Patman G: Pancreatic cancer: From normal to metastases-a whole gamut of pancreatic organoids. Nat Rev Gastroenterol Hepatol. 12:612015. View Article : Google Scholar : PubMed/NCBI | |
Huang L, Holtzinger A, Jagan I, BeGora M, Lohse I, Ngai N, Nostro C, Wang R, Muthuswamy LB, Crawford HC, et al: Ductal pancreatic cancer modeling and drug screening using human pluripotent stem cell- and patient-derived tumor organoids. Nat Med. 21:1364–1371. 2015. View Article : Google Scholar : PubMed/NCBI | |
Chio IIC, Jafarnejad SM, Ponz-Sarvise M, Park Y, Rivera K, Palm W, Wilson J, Sangar V, Hao Y, Öhlund D, et al: NRF2 promotes tumor maintenance by modulating mRNA translation in pancreatic cancer. Cell. 166:963–976. 2016. View Article : Google Scholar : PubMed/NCBI | |
Öhlund D, Handly-Santana A, Biffi G, Elyada E, Almeida AS, Ponz-Sarvise M, Corbo V, Oni TE, Hearn SA, Lee EJ, et al: Distinct populations of inflammatory fibroblasts and myofibroblasts in pancreatic cancer. J Exp Med. 214:579–596. 2017. View Article : Google Scholar : PubMed/NCBI | |
Lesina M, Kurkowski MU, Ludes K, Rose-John S, Treiber M, Klöppel G, Yoshimura A, Reindl W, Sipos B, Akira S, et al: Stat3/Socs3 activation by IL-6 transsignaling promotes progression of pancreatic intraepithelial neoplasia and development of pancreatic cancer. Cancer Cell. 19:456–469. 2011. View Article : Google Scholar : PubMed/NCBI | |
Roe JS, Hwang CI, Somerville TDD, Milazzo JP, Lee EJ, Da Silva B, Maiorino L, Tiriac H, Young CM, Miyabayashi K, et al: Enhancer reprogramming promotes pancreatic cancer metastasis. Cell. 170:875–888.e20. 2017. View Article : Google Scholar : PubMed/NCBI | |
Tiriac H, Bucobo J, Tzimas D, Grewel S, Lacomb JF, Rowehl LM, Nagula S, Wu M, Kim J, Sasson A, et al: Successful creation of pancreatic cancer organoids by means of EUS-guided fine-needle biopsy sampling for personalized cancer treatment. Gastrointest Endosc. 87:1474–1480. 2018. View Article : Google Scholar : PubMed/NCBI | |
Seino T, Kawasaki S, Shimokawa M, Tamagawa H, Toshimitsu K, Fujii M, Ohta Y, Matano M, Nanki K, Kawasaki K, et al: Human pancreatic tumor organoids reveal loss of stem cell niche factor dependence during disease progression. Cell Stem Cell. 22:454–467. 2018. View Article : Google Scholar : PubMed/NCBI | |
Frappart PO, Walter K, Gout J, Beutel AK, Morawe M, Arnold F, Breunig M, Barth TF, Marienfeld R, Schulte L, et al: Pancreatic cancer-derived organoids-a disease modeling tool to predict drug response. United European Gastroenterol J. 8:594–606. 2020. View Article : Google Scholar : PubMed/NCBI | |
Múnera JO, Sundaram N, Rankin SA, Hill D, Watson C, Mahe M, Vallance JE, Shroyer NF, Sinagoga KL, Zarzoso-Lacoste A, et al: Differentiation of human pluripotent stem cells into colonic organoids via transient activation of BMP signaling. Cell Stem Cell. 21:51–64. 2017. View Article : Google Scholar : PubMed/NCBI | |
Webber JP, Spary LK, Sanders AJ, Chowdhury R, Jiang WG, Steadman R, Wymant J, Jones AT, Kynaston H, Mason MD, et al: Differentiation of tumour-promoting stromal myofibroblasts by cancer exosomes. Oncogene. 34:290–302. 2015. View Article : Google Scholar : PubMed/NCBI | |
Usui T, Sakurai M, Enjoji S, Kawasaki H, Umata K, Ohama T, Fujiwara N, Yabe R, Tsuji S, Yamawaki H, et al: Establishment of a novel model for anticancer drug resistance in three-dimensional primary culture of tumor microenvironment. Stem Cells Int. 2016:70538722016. View Article : Google Scholar : PubMed/NCBI | |
Lannagan TRM, Lee YK, Wang T, Roper J, Bettington ML, Fennell L, Vrbanac L, Jonavicius L, Somashekar R, Gieniec K, et al: Genetic editing of colonic organoids provides a molecularly distinct and orthotopic preclinical model of serrated carcinogenesis. Gut. 68:684–692. 2019. View Article : Google Scholar : PubMed/NCBI | |
Nadauld LD, Garcia S, Natsoulis G, Bell JM, Miotke L, Hopmans ES, Xu H, Pai RK, Palm C, Regan JF, et al: Metastatic tumor evolution and organoid modeling implicate TGFBR2 as a cancer driver in diffuse gastric cancer. Genome Biol. 15:4282014. View Article : Google Scholar : PubMed/NCBI | |
Li X, Nadauld L, Ootani A, Corney DC, Pai RK, Gevaert O, Cantrell MA, Rack PG, Neal JT, Chan CW, et al: Oncogenic transformation of diverse gastrointestinal tissues in primary organoid culture. Nat Med. 20:769–777. 2014. View Article : Google Scholar : PubMed/NCBI | |
Seidlitz T, Merker SR, Rothe A, Zakrzewski F, von Neubeck C, Grützmann K, Sommer U, Schweitzer C, Schölch S, Uhlemann H, et al: Human gastric cancer modelling using organoids. Gut. 68:207–217. 2019. View Article : Google Scholar : PubMed/NCBI | |
Vlachogiannis G, Hedayat S, Vatsiou A, Jamin Y, Fernández-Mateos J, Khan K, Lampis A, Eason K, Huntingford I, Burke R, et al: Patient-derived organoids model treatment response of metastatic gastrointestinal cancers. Science. 359:920–926. 2018. View Article : Google Scholar : PubMed/NCBI | |
Singh A, Poling HM, Spence JR, Wells JM and Helmrath MA: Gastrointestinal organoids: A next-generation tool for modeling human development. Am J Physiol Gastrointest Liver Physiol. 319:G375–G381. 2020. View Article : Google Scholar : PubMed/NCBI | |
Xu H, Lyu X, Yi M, Zhao W, Song Y and Wu K: Organoid technology and applications in cancer research. J Hematol Oncol. 11:1162018. View Article : Google Scholar : PubMed/NCBI | |
Foulke-Abel J, In J, Kovbasnjuk O, Zachos NC, Ettayebi K, Blutt SE, Hyser JM, Zeng XL, Crawford SE, Broughman JR, et al: Human enteroids as an ex-vivo model of host-pathogen interactions in the gastrointestinal tract. Exp Biol Med (Maywood). 239:1124–1134. 2014. View Article : Google Scholar : PubMed/NCBI | |
Sachs N, Tsukamoto Y, Kujala P, Peters PJ and Clevers H: Intestinal epithelial organoids fuse to form self-organizing tubes in floating collagen gels. Development. 144:1107–1112. 2017. View Article : Google Scholar : PubMed/NCBI | |
Fong EL, Wan X, Yang J, Morgado M, Mikos AG, Harrington DA, Navone NM and Farach-Carson MC: A 3D in vitro model of patient-derived prostate cancer xenograft for controlled interrogation of in vivo tumor-stromal interactions. Biomaterials. 77:164–172. 2016. View Article : Google Scholar : PubMed/NCBI | |
Zhang S, Wan Z and Kamm RD: Vascularized organoids on a chip: Strategies for engineering organoids with functional vasculature. Lab Chip. 21:473–488. 2021. View Article : Google Scholar : PubMed/NCBI | |
Zhang C, Jin M, Zhao J, Chen J and Jin W: Organoid models of glioblastoma: Advances, applications and challenges. Am J Cancer Res. 10:2242–2257. 2020.PubMed/NCBI | |
Date S and Sato T: Mini-gut organoids: Reconstitution of the stem cell niche. Annu Rev Cell Dev Biol. 31:269–289. 2015. View Article : Google Scholar : PubMed/NCBI | |
Kim J, Koo BK and Knoblich JA: Human organoids: Model systems for human biology and medicine. Nat Rev Mol Cell Biol. 21:571–584. 2020. View Article : Google Scholar : PubMed/NCBI |