Login Register Cart 0
Generic placeholder image

Current Molecular Pharmacology

Editor-in-Chief

ISSN (Print): 1874-4672
ISSN (Online): 1874-4702

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Mini-Review Article

Tumor Organoid Model and Its Pharmacological Applications in Tumorigenesis Prevention

Author(s): Yuwei Qiang, Ninghua Yao, Fan Zuo, Shi Qiu, Xiaolei Cao* and Wenjie Zheng*

Volume 16, Issue 4, 2023

Published on: 17 October, 2022

Article ID: e030822207245 Pages: 13

DOI: 10.2174/1874467215666220803125822

Price: $65

Abstract

Cancer is a leading cause of death and a severe threat to global public health. Organoid, as a novel 3D in vitro model, has been applied in various tumor related studies due to its apparent advantages. The organoid is mainly constructed by Matrigel-depended 3D culture system, Air-Liquid Interface (ALI) culture, and Microfluidic culture or Organ-on-chips platform. For the application in carcinogenesis studies, the organoid model may favor depicting initiative hallmarks and identifying potential intervening targets, investigating driver genes of carcinogenesis, and identifying known or unknown risk or protective factors.

In this review, we discussed different organoid construction methods and their properties. We also noted that tumor organoids can portray initiative hallmarks and identify possible intervening targets, as well as explore carcinogenesis driver genes and uncover known or unknown risks or protective factors. Organoid systems have been used to identify tumor-preventive drugs such as oligomeric proanthocyanidins, Vitamin D, n-3 PUFAs, and pomegranate. The current evidence underscores the organoid model's potential importance in developing innovative tumorprevention techniques.

Keywords: Organoid, 3D model, tumorigenesis, pharmacology, oncogenic prevention, cancer.

Graphical Abstract

[1]
Siegel, R.L.; Miller, K.D.; Fuchs, H.E.; Jemal, A. Cancer statistics, 2022. CA Cancer J. Clin., 2022, 72(1), 7-33.
[http://dx.doi.org/10.3322/caac.21708] [PMID: 35020204]
[2]
Aboulkheyr Es, H.; Montazeri, L.; Aref, A.R.; Vosough, M.; Baharvand, H. Personalized cancer medicine: An organoid approach. Trends Biotechnol., 2018, 36(4), 358-371.
[http://dx.doi.org/10.1016/j.tibtech.2017.12.005] [PMID: 29366522]
[3]
Ali, Z.; Vildevall, M.; Rodriguez, G.V.; Tandiono, D.; Vamvakaris, I.; Evangelou, G.; Lolas, G.; Syrigos, K.N.; Villanueva, A.; Wick, M.; Omar, S.; Erkstam, A.; Schueler, J.; Fahlgren, A.; Jensen, L.D. Zebrafish patient-derived xenograft models predict lymph node involvement and treatment outcome in non-small cell lung cancer. J. Exp. Clin. Cancer Res., 2022, 41(1), 58.
[http://dx.doi.org/10.1186/s13046-022-02280-x] [PMID: 35139880]
[4]
Gao, D.; Chen, Y. Organoid development in cancer genome discovery. Curr. Opin. Genet. Dev., 2015, 30, 42-48.
[http://dx.doi.org/10.1016/j.gde.2015.02.007] [PMID: 25796043]
[5]
Porter, R.J.; Murray, G.I.; McLean, M.H. Current concepts in tumour-derived organoids. Br. J. Cancer, 2020, 123(8), 1209-1218.
[http://dx.doi.org/10.1038/s41416-020-0993-5] [PMID: 32728094]
[6]
Mroz, E.A.; Rocco, J.W. Intra-tumor heterogeneity in head and neck cancer and its clinical implications. World J. Otorhinolaryngol. Head Neck Surg., 2016, 2(2), 60-67.
[http://dx.doi.org/10.1016/j.wjorl.2016.05.007] [PMID: 28642939]
[7]
Stanta, G.; Bonin, S. Overview on clinical relevance of intra-tumor heterogeneity. Front. Med. (Lausanne), 2018, 5, 85.
[http://dx.doi.org/10.3389/fmed.2018.00085] [PMID: 29682505]
[8]
Wang, S.; Gao, D.; Chen, Y. The potential of organoids in urological cancer research. Nat. Rev. Urol., 2017, 14(7), 401-414.
[http://dx.doi.org/10.1038/nrurol.2017.65] [PMID: 28534535]
[9]
Li, S.; Shen, D.; Shao, J.; Crowder, R.; Liu, W.; Prat, A.; He, X.; Liu, S.; Hoog, J.; Lu, C.; Ding, L.; Griffith, O.L.; Miller, C.; Larson, D.; Fulton, R.S.; Harrison, M.; Mooney, T.; McMichael, J.F.; Luo, J.; Tao, Y.; Goncalves, R.; Schlosberg, C.; Hiken, J.F.; Saied, L.; Sanchez, C.; Giuntoli, T.; Bumb, C.; Cooper, C.; Kitchens, R.T.; Lin, A.; Phommaly, C.; Davies, S.R.; Zhang, J.; Kavuri, M.S.; McEachern, D.; Dong, Y.Y.; Ma, C.; Pluard, T.; Naughton, M.; Bose, R.; Suresh, R.; McDowell, R.; Michel, L.; Aft, R.; Gillanders, W.; DeSchryver, K.; Wilson, R.K.; Wang, S.; Mills, G.B.; Gonzalez-Angulo, A.; Edwards, J.R.; Maher, C.; Perou, C.M.; Mardis, E.R.; Ellis, M.J. Endocrine-therapy-resistant ESR1 variants revealed by genomic characterization of breast-cancer-derived xenografts. Cell Rep., 2013, 4(6), 1116-1130.
[http://dx.doi.org/10.1016/j.celrep.2013.08.022] [PMID: 24055055]
[10]
Nguyen, R.; Bae, S.D.W.; Zhou, G.; Read, S.A.; Ahlenstiel, G.; George, J.; Qiao, L. Application of organoids in translational research of human diseases with a particular focus on gastrointestinal cancers. Biochim. Biophys. Acta Rev. Cancer, 2020, 1873(2), 188350.
[http://dx.doi.org/10.1016/j.bbcan.2020.188350] [PMID: 32007597]
[11]
Torre, L.A.; Siegel, R.L.; Ward, E.M.; Jemal, A. Global cancer incidence and mortality rates and trends - An update. Cancer Epidemiol. Biomarkers Prev., 2016, 25(1), 16-27.
[http://dx.doi.org/10.1158/1055-9965.EPI-15-0578] [PMID: 26667886]
[12]
Lou, Y.R.; Leung, A.W. Next generation organoids for biomedical research and applications. Biotechnol. Adv., 2018, 36(1), 132-149.
[http://dx.doi.org/10.1016/j.biotechadv.2017.10.005] [PMID: 29056474]
[13]
Li, X.; Nadauld, L.; Ootani, A.; Corney, D.C.; Pai, R.K.; Gevaert, O.; Cantrell, M.A.; Rack, P.G.; Neal, J.T.; Chan, C.W.; Yeung, T.; Gong, X.; Yuan, J.; Wilhelmy, J.; Robine, S.; Attardi, L.D.; Plevritis, S.K.; Hung, K.E.; Chen, C.Z.; Ji, H.P.; Kuo, C.J. Oncogenic transformation of diverse gastrointestinal tissues in primary organoid culture. Nat. Med., 2014, 20(7), 769-777.
[http://dx.doi.org/10.1038/nm.3585] [PMID: 24859528]
[14]
Matano, M.; Date, S.; Shimokawa, M.; Takano, A.; Fujii, M.; Ohta, Y.; Watanabe, T.; Kanai, T.; Sato, T. Modeling colorectal cancer using CRISPR-Cas9-mediated engineering of human intestinal organoids. Nat. Med., 2015, 21(3), 256-262.
[http://dx.doi.org/10.1038/nm.3802] [PMID: 25706875]
[15]
Drost, J.; van Jaarsveld, R.H.; Ponsioen, B.; Zimberlin, C.; van Boxtel, R.; Buijs, A.; Sachs, N.; Overmeer, R.M.; Offerhaus, G.J.; Begthel, H.; Korving, J.; van de Wetering, M.; Schwank, G.; Logtenberg, M.; Cuppen, E.; Snippert, H.J.; Medema, J.P.; Kops, G.J.; Clevers, H. Sequential cancer mutations in cultured human intestinal stem cells. Nature, 2015, 521(7550), 43-47.
[http://dx.doi.org/10.1038/nature14415] [PMID: 25924068]
[16]
Crespo, M.; Vilar, E.; Tsai, S.Y.; Chang, K.; Amin, S.; Srinivasan, T.; Zhang, T.; Pipalia, N.H.; Chen, H.J.; Witherspoon, M.; Gordillo, M.; Xiang, J.Z.; Maxfield, F.R.; Lipkin, S.; Evans, T.; Chen, S. Colonic organoids derived from human induced pluripotent stem cells for modeling colorectal cancer and drug testing. Nat. Med., 2017, 23(7), 878-884.
[http://dx.doi.org/10.1038/nm.4355] [PMID: 28628110]
[17]
Drost, J.; van Boxtel, R.; Blokzijl, F.; Mizutani, T.; Sasaki, N.; Sasselli, V.; de Ligt, J.; Behjati, S.; Grolleman, J.E.; van Wezel, T.; Nik-Zainal, S.; Kuiper, R.P.; Cuppen, E.; Clevers, H. Use of CRISPR-modified human stem cell organoids to study the origin of mutational signatures in cancer. Science, 2017, 358(6360), 234-238.
[http://dx.doi.org/10.1126/science.aao3130] [PMID: 28912133]
[18]
Sato, T.; Stange, D.E.; Ferrante, M.; Vries, R.G.; Van Es, J.H.; Van den Brink, S.; Van Houdt, W.J.; Pronk, A.; Van Gorp, J.; Siersema, P.D.; Clevers, H. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett’s epithelium. Gastroenterology, 2011, 141(5), 1762-1772.
[http://dx.doi.org/10.1053/j.gastro.2011.07.050] [PMID: 21889923]
[19]
Gao, M.; Lin, M.; Rao, M.; Thompson, H.; Hirai, K.; Choi, M.; Georgakis, G.V.; Sasson, A.R.; Bucobo, J.C.; Tzimas, D.; D’Souza, L.S.; Buscaglia, J.M.; Davis, J.; Shroyer, K.R.; Li, J.; Powers, S.; Kim, J. Development of patient-derived gastric cancer organoids from endoscopic biopsies and surgical tissues. Ann. Surg. Oncol., 2018, 25(9), 2767-2775.
[http://dx.doi.org/10.1245/s10434-018-6662-8] [PMID: 30003451]
[20]
Nuciforo, S.; Fofana, I.; Matter, M.S.; Blumer, T.; Calabrese, D.; Boldanova, T.; Piscuoglio, S.; Wieland, S.; Ringnalda, F.; Schwank, G.; Terracciano, L.M.; Ng, C.K.Y.; Heim, M.H. Organoid models of human liver cancers derived from tumor needle biopsies. Cell Rep., 2018, 24(5), 1363-1376.
[http://dx.doi.org/10.1016/j.celrep.2018.07.001] [PMID: 30067989]
[21]
Tiriac, H.; Bucobo, J.C.; Tzimas, D.; Grewel, S.; Lacomb, J.F.; Rowehl, L.M.; Nagula, S.; Wu, M.; Kim, J.; Sasson, A.; Vignesh, S.; Martello, L.; Munoz-Sagastibelza, M.; Somma, J.; Tuveson, D.A.; Li, E.; Buscaglia, J.M. Successful creation of pancreatic cancer organoids by means of EUS-guided fine-needle biopsy sampling for personalized cancer treatment. Gastrointest. Endosc., 2018, 87(6), 1474-1480.
[http://dx.doi.org/10.1016/j.gie.2017.12.032] [PMID: 29325707]
[22]
Broutier, L.; Mastrogiovanni, G.; Verstegen, M.M.; Francies, H.E.; Gavarró, L.M.; Bradshaw, C.R.; Allen, G.E.; Arnes-Benito, R.; Sidorova, O.; Gaspersz, M.P.; Georgakopoulos, N.; Koo, B.K.; Dietmann, S.; Davies, S.E.; Praseedom, R.K.; Lieshout, R.; IJzermans, J.N.M.; Wigmore, S.J.; Saeb-Parsy, K.; Garnett, M.J.; van der Laan, L.J.; Huch, M. Human primary liver cancer-derived organoid cultures for disease modeling and drug screening. Nat. Med., 2017, 23(12), 1424-1435.
[http://dx.doi.org/10.1038/nm.4438] [PMID: 29131160]
[23]
Fumagalli, A.; Drost, J.; Suijkerbuijk, S.J.; van Boxtel, R.; de Ligt, J.; Offerhaus, G.J.; Begthel, H.; Beerling, E.; Tan, E.H.; Sansom, O.J.; Cuppen, E.; Clevers, H.; van Rheenen, J. Genetic dissection of colorectal cancer progression by orthotopic transplantation of engineered cancer organoids. Proc. Natl. Acad. Sci. USA, 2017, 114(12), E2357-E2364.
[http://dx.doi.org/10.1073/pnas.1701219114] [PMID: 28270604]
[24]
Linkous, A.; Balamatsias, D.; Snuderl, M.; Edwards, L.; Miyaguchi, K.; Milner, T.; Reich, B.; Cohen-Gould, L.; Storaska, A.; Nakayama, Y.; Schenkein, E.; Singhania, R.; Cirigliano, S.; Magdeldin, T.; Lin, Y.; Nanjangud, G.; Chadalavada, K.; Pisapia, D.; Liston, C.; Fine, H.A. Modeling patient-derived glioblastoma with cerebral organoids. Cell Rep., 2019, 26(12), 3203-3211.e5.
[http://dx.doi.org/10.1016/j.celrep.2019.02.063] [PMID: 30893594]
[25]
Wang, K.; Yuen, S.T.; Xu, J.; Lee, S.P.; Yan, H.H.; Shi, S.T.; Siu, H.C.; Deng, S.; Chu, K.M.; Law, S.; Chan, K.H.; Chan, A.S.; Tsui, W.Y.; Ho, S.L.; Chan, A.K.; Man, J.L.; Foglizzo, V.; Ng, M.K.; Chan, A.S.; Ching, Y.P.; Cheng, G.H.; Xie, T.; Fernandez, J.; Li, V.S.; Clevers, H.; Rejto, P.A.; Mao, M.; Leung, S.Y. Whole-genome sequencing and comprehensive molecular profiling identify new driver mutations in gastric cancer. Nat. Genet., 2014, 46(6), 573-582.
[http://dx.doi.org/10.1038/ng.2983] [PMID: 24816253]
[26]
Boj, S.F.; Hwang, C.I.; Baker, L.A.; Chio, I.I.; Engle, D.D.; Corbo, V.; Jager, M.; Ponz-Sarvise, M.; Tiriac, H.; Spector, M.S.; Gracanin, A.; Oni, T.; Yu, K.H.; van Boxtel, R.; Huch, M.; Rivera, K.D.; Wilson, J.P.; Feigin, M.E.; Öhlund, D.; Handly-Santana, A.; Ardito-Abraham, C.M.; Ludwig, M.; Elyada, E.; Alagesan, B.; Biffi, G.; Yordanov, G.N.; Delcuze, B.; Creighton, B.; Wright, K.; Park, Y.; Morsink, F.H.; Molenaar, I.Q.; Borel Rinkes, I.H.; Cuppen, E.; Hao, Y.; Jin, Y.; Nijman, I.J.; Iacobuzio-Donahue, C.; Leach, S.D.; Pappin, D.J.; Hammell, M.; Klimstra, D.S.; Basturk, O.; Hruban, R.H.; Offerhaus, G.J.; Vries, R.G.; Clevers, H.; Tuveson, D.A. Organoid models of human and mouse ductal pancreatic cancer. Cell, 2015, 160(1-2), 324-338.
[http://dx.doi.org/10.1016/j.cell.2014.12.021] [PMID: 25557080]
[27]
Vela, I.; Chen, Y. Prostate cancer organoids: A potential new tool for testing drug sensitivity. Expert Rev. Anticancer Ther., 2015, 15(3), 261-263.
[http://dx.doi.org/10.1586/14737140.2015.1003046] [PMID: 25603995]
[28]
Sachs, N.; de Ligt, J.; Kopper, O.; Gogola, E.; Bounova, G.; Weeber, F.; Balgobind, A.V.; Wind, K.; Gracanin, A.; Begthel, H.; Korving, J.; van Boxtel, R.; Duarte, A.A.; Lelieveld, D.; van Hoeck, A.; Ernst, R.F.; Blokzijl, F.; Nijman, I.J.; Hoogstraat, M.; van de Ven, M.; Egan, D.A.; Zinzalla, V.; Moll, J.; Boj, S.F.; Voest, E.E.; Wessels, L.; van Diest, P.J.; Rottenberg, S.; Vries, R.G.J.; Cuppen, E.; Clevers, H. A living biobank of breast cancer organoids captures disease heterogeneity. Cell, 2018, 172(1-2), 373-386.e10.
[http://dx.doi.org/10.1016/j.cell.2017.11.010] [PMID: 29224780]
[29]
Li, X.; Francies, H.E.; Secrier, M.; Perner, J.; Miremadi, A.; Galeano-Dalmau, N.; Barendt, W.J.; Letchford, L.; Leyden, G.M.; Goffin, E.K.; Barthorpe, A.; Lightfoot, H.; Chen, E.; Gilbert, J.; Noorani, A.; Devonshire, G.; Bower, L.; Grantham, A.; MacRae, S.; Grehan, N.; Wedge, D.C.; Fitzgerald, R.C.; Garnett, M.J. Organoid cultures recapitulate esophageal adenocarcinoma heterogeneity providing a model for clonality studies and precision therapeutics. Nat. Commun., 2018, 9(1), 2983.
[http://dx.doi.org/10.1038/s41467-018-05190-9] [PMID: 30061675]
[30]
Schutgens, F.; Rookmaaker, M.B.; Margaritis, T.; Rios, A.; Ammerlaan, C.; Jansen, J.; Gijzen, L.; Vormann, M.; Vonk, A.; Viveen, M.; Yengej, F.Y.; Derakhshan, S.; de Winter-de Groot, K.M.; Artegiani, B.; van Boxtel, R.; Cuppen, E.; Hendrickx, A.P.A.; van den Heuvel-Eibrink, M.M.; Heitzer, E.; Lanz, H.; Beekman, J.; Murk, J.L.; Masereeuw, R.; Holstege, F.; Drost, J.; Verhaar, M.C.; Clevers, H. Tubuloids derived from human adult kidney and urine for personalized disease modeling. Nat. Biotechnol., 2019, 37(3), 303-313.
[http://dx.doi.org/10.1038/s41587-019-0048-8] [PMID: 30833775]
[31]
Sachs, N.; Papaspyropoulos, A.; Zomer-van Ommen, D.D.; Heo, I.; Böttinger, L.; Klay, D.; Weeber, F.; Huelsz-Prince, G.; Iakobachvili, N.; Amatngalim, G.D.; de Ligt, J.; van Hoeck, A.; Proost, N.; Viveen, M.C.; Lyubimova, A.; Teeven, L.; Derakhshan, S.; Korving, J.; Begthel, H.; Dekkers, J.F.; Kumawat, K.; Ramos, E.; van Oosterhout, M.F.; Offerhaus, G.J.; Wiener, D.J.; Olimpio, E.P.; Dijkstra, K.K.; Smit, E.F.; van der Linden, M.; Jaksani, S.; van de Ven, M.; Jonkers, J.; Rios, A.C.; Voest, E.E.; van Moorsel, C.H.; van der Ent, C.K.; Cuppen, E.; van Oudenaarden, A.; Coenjaerts, F.E.; Meyaard, L.; Bont, L.J.; Peters, P.J.; Tans, S.J.; van Zon, J.S.; Boj, S.F.; Vries, R.G.; Beekman, J.M.; Clevers, H. Long-term expanding human airway organoids for disease modeling. EMBO J., 2019, 38(4), e100300.
[http://dx.doi.org/10.15252/embj.2018100300] [PMID: 30643021]
[32]
Sadanandam, A.; Lyssiotis, C.A.; Homicsko, K.; Collisson, E.A.; Gibb, W.J.; Wullschleger, S.; Ostos, L.C.; Lannon, W.A.; Grotzinger, C.; Del Rio, M.; Lhermitte, B.; Olshen, A.B.; Wiedenmann, B.; Cantley, L.C.; Gray, J.W.; Hanahan, D. A colorectal cancer classification system that associates cellular phenotype and responses to therapy. Nat. Med., 2013, 19(5), 619-625.
[http://dx.doi.org/10.1038/nm.3175] [PMID: 23584089]
[33]
Guinney, J.; Dienstmann, R.; Wang, X.; de Reyniès, A.; Schlicker, A.; Soneson, C.; Marisa, L.; Roepman, P.; Nyamundanda, G.; Angelino, P.; Bot, B.M.; Morris, J.S.; Simon, I.M.; Gerster, S.; Fessler, E.; De Sousa, E. Melo, F.; Missiaglia, E.; Ramay, H.; Barras, D.; Homicsko, K.; Maru, D.; Manyam, G.C.; Broom, B.; Boige, V.; Perez-Villamil, B.; Laderas, T.; Salazar, R.; Gray, J.W.; Hanahan, D.; Tabernero, J.; Bernards, R.; Friend, S.H.; Laurent-Puig, P.; Medema, J.P.; Sadanandam, A.; Wessels, L.; Delorenzi, M.; Kopetz, S.; Vermeulen, L.; Tejpar, S. The consensus molecular subtypes of colorectal cancer. Nat. Med., 2015, 21(11), 1350-1356.
[http://dx.doi.org/10.1038/nm.3967] [PMID: 26457759]
[34]
Novellasdemunt, L.; Antas, P.; Li, V.S. Targeting Wnt signaling in colorectal cancer. A review in the theme: Cell signaling: proteins, pathways and mechanisms. Am. J. Physiol. Cell Physiol., 2015, 309(8), C511-C521.
[http://dx.doi.org/10.1152/ajpcell.00117.2015] [PMID: 26289750]
[35]
Fujii, M.; Shimokawa, M.; Date, S.; Takano, A.; Matano, M.; Nanki, K.; Ohta, Y.; Toshimitsu, K.; Nakazato, Y.; Kawasaki, K.; Uraoka, T.; Watanabe, T.; Kanai, T.; Sato, T. A colorectal tumor organoid library demonstrates progressive loss of niche factor requirements during tumorigenesis. Cell Stem Cell, 2016, 18(6), 827-838.
[http://dx.doi.org/10.1016/j.stem.2016.04.003] [PMID: 27212702]
[36]
de Sousa, E.M.; Vermeulen, L.; Richel, D.; Medema, J.P. Targeting Wnt signaling in colon cancer stem cells. Clin. Cancer Res., 2011, 17(4), 647-653.
[http://dx.doi.org/10.1158/1078-0432.CCR-10-1204] [PMID: 21159886]
[37]
Neal, J.T.; Kuo, C.J. Organoids as models for neoplastic transformation. Annu. Rev. Pathol., 2016, 11(1), 199-220.
[http://dx.doi.org/10.1146/annurev-pathol-012615-044249] [PMID: 26907527]
[38]
Lee, S.H.; Hu, W.; Matulay, J.T.; Silva, M.V.; Owczarek, T.B.; Kim, K.; Chua, C.W.; Barlow, L.J.; Kandoth, C.; Williams, A.B.; Bergren, S.K.; Pietzak, E.J.; Anderson, C.B.; Benson, M.C.; Coleman, J.A.; Taylor, B.S.; Abate-Shen, C.; McKiernan, J.M.; Al-Ahmadie, H.; Solit, D.B.; Shen, M.M. Tumor evolution and drug response in patient-derived organoid models of bladder cancer. Cell, 2018, 173(2), 515-528.e17.
[http://dx.doi.org/10.1016/j.cell.2018.03.017] [PMID: 29625057]
[39]
Cristobal, A.; van den Toorn, H.W.P.; van de Wetering, M.; Clevers, H.; Heck, A.J.R.; Mohammed, S. Personalized proteome profiles of healthy and tumor human colon organoids reveal both individual diversity and basic features of colorectal cancer. Cell Rep., 2017, 18(1), 263-274.
[http://dx.doi.org/10.1016/j.celrep.2016.12.016] [PMID: 28052255]
[40]
Tsai, S.; McOlash, L.; Palen, K.; Johnson, B.; Duris, C.; Yang, Q.; Dwinell, M.B.; Hunt, B.; Evans, D.B.; Gershan, J.; James, M.A. Development of primary human pancreatic cancer organoids, matched stromal and immune cells and 3D tumor microenvironment models. BMC Cancer, 2018, 18(1), 335.
[http://dx.doi.org/10.1186/s12885-018-4238-4] [PMID: 29587663]
[41]
Valent, P.; Bonnet, D.; De Maria, R.; Lapidot, T.; Copland, M.; Melo, J.V.; Chomienne, C.; Ishikawa, F.; Schuringa, J.J.; Stassi, G.; Huntly, B.; Herrmann, H.; Soulier, J.; Roesch, A.; Schuurhuis, G.J.; Wöhrer, S.; Arock, M.; Zuber, J.; Cerny-Reiterer, S.; Johnsen, H.E.; Andreeff, M.; Eaves, C. Cancer stem cell definitions and terminology: The devil is in the details. Nat. Rev. Cancer, 2012, 12(11), 767-775.
[http://dx.doi.org/10.1038/nrc3368] [PMID: 23051844]
[42]
Weiswald, L.B.; Bellet, D.; Dangles-Marie, V. Spherical cancer models in tumor biology. Neoplasia, 2015, 17(1), 1-15.
[http://dx.doi.org/10.1016/j.neo.2014.12.004] [PMID: 25622895]
[43]
Kenerson, H.L.; Sullivan, K.M.; Seo, Y.D.; Stadeli, K.M.; Ussakli, C.; Yan, X.; Lausted, C.; Pillarisetty, V.G.; Park, J.O.; Riehle, K.J.; Yeh, M.; Tian, Q.; Yeung, R.S. Tumor slice culture as a biologic surrogate of human cancer. Ann. Transl. Med., 2020, 8(4), 114.
[http://dx.doi.org/10.21037/atm.2019.12.88] [PMID: 32175407]
[44]
Yuki, K.; Cheng, N.; Nakano, M.; Kuo, C.J. Organoid models of tumor immunology. Trends Immunol., 2020, 41(8), 652-664.
[http://dx.doi.org/10.1016/j.it.2020.06.010] [PMID: 32654925]
[45]
Boucherit, N.; Gorvel, L.; Olive, D. 3D tumor models and their use for the testing of immunotherapies. Front. Immunol., 2020, 11, 603640.
[http://dx.doi.org/10.3389/fimmu.2020.603640] [PMID: 33362787]
[46]
Fujii, M.; Matano, M.; Toshimitsu, K.; Takano, A.; Mikami, Y.; Nishikori, S.; Sugimoto, S.; Sato, T. Human intestinal organoids maintain self-renewal capacity and cellular diversity in niche-inspired culture condition. Cell Stem Cell, 2018, 23(6), 787-793.e6.
[http://dx.doi.org/10.1016/j.stem.2018.11.016] [PMID: 30526881]
[47]
Sato, T.; Vries, R.G.; Snippert, H.J.; van de Wetering, M.; Barker, N.; Stange, D.E.; van Es, J.H.; Abo, A.; Kujala, P.; Peters, P.J.; Clevers, H. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature, 2009, 459(7244), 262-265.
[http://dx.doi.org/10.1038/nature07935] [PMID: 19329995]
[48]
Dijkstra, K.K.; Cattaneo, C.M.; Weeber, F.; Chalabi, M.; van de Haar, J.; Fanchi, L.F.; Slagter, M.; van der Velden, D.L.; Kaing, S.; Kelderman, S.; van Rooij, N.; van Leerdam, M.E.; Depla, A.; Smit, E.F.; Hartemink, K.J.; de Groot, R.; Wolkers, M.C.; Sachs, N.; Snaebjornsson, P.; Monkhorst, K.; Haanen, J.; Clevers, H.; Schumacher, T.N.; Voest, E.E. Generation of tumor-reactive T cells by co-culture of peripheral blood lymphocytes and tumor organoids. Cell, 2018, 174(6), 1586-1598.e12.
[http://dx.doi.org/10.1016/j.cell.2018.07.009] [PMID: 30100188]
[49]
Ootani, A.; Li, X.; Sangiorgi, E.; Ho, Q.T.; Ueno, H.; Toda, S.; Sugihara, H.; Fujimoto, K.; Weissman, I.L.; Capecchi, M.R.; Kuo, C.J. Sustained in vitro intestinal epithelial culture within a Wnt-dependent stem cell niche. Nat. Med., 2009, 15(6), 701-706.
[http://dx.doi.org/10.1038/nm.1951] [PMID: 19398967]
[50]
Vlachogiannis, G.; Hedayat, S.; Vatsiou, A.; Jamin, Y.; Fernández-Mateos, J.; Khan, K.; Lampis, A.; Eason, K.; Huntingford, I.; Burke, R.; Rata, M.; Koh, D.M.; Tunariu, N.; Collins, D.; Hulkki-Wilson, S.; Ragulan, C.; Spiteri, I.; Moorcraft, S.Y.; Chau, I.; Rao, S.; Watkins, D.; Fotiadis, N.; Bali, M.; Darvish-Damavandi, M.; Lote, H.; Eltahir, Z.; Smyth, E.C.; Begum, R.; Clarke, P.A.; Hahne, J.C.; Dowsett, M.; de Bono, J.; Workman, P.; Sadanandam, A.; Fassan, M.; Sansom, O.J.; Eccles, S.; Starling, N.; Braconi, C.; Sottoriva, A.; Robinson, S.P.; Cunningham, D.; Valeri, N. Patient-derived organoids model treatment response of metastatic gastrointestinal cancers. Science, 2018, 359(6378), 920-926.
[http://dx.doi.org/10.1126/science.aao2774] [PMID: 29472484]
[51]
Neal, J.T.; Li, X.; Zhu, J.; Giangarra, V.; Grzeskowiak, C.L.; Ju, J.; Liu, I.H.; Chiou, S.H.; Salahudeen, A.A.; Smith, A.R.; Deutsch, B.C.; Liao, L.; Zemek, A.J.; Zhao, F.; Karlsson, K.; Schultz, L.M.; Metzner, T.J.; Nadauld, L.D.; Tseng, Y.Y.; Alkhairy, S.; Oh, C.; Keskula, P.; Mendoza-Villanueva, D.; De La Vega, F.M.; Kunz, P.L.; Liao, J.C.; Leppert, J.T.; Sunwoo, J.B.; Sabatti, C.; Boehm, J.S.; Hahn, W.C.; Zheng, G.X.Y.; Davis, M.M.; Kuo, C.J. Organoid modeling of the tumor immune microenvironment. Cell, 2018, 175(7), 1972-1988.
[http://dx.doi.org/10.1016/j.cell.2018.11.021] [PMID: 30550791]
[52]
Whitesides, G.M. The origins and the future of microfluidics. Nature, 2006, 442(7101), 368-373.
[http://dx.doi.org/10.1038/nature05058] [PMID: 16871203]
[53]
Buchanan, C.; Rylander, M.N. Microfluidic culture models to study the hydrodynamics of tumor progression and therapeutic response. Biotechnol. Bioeng., 2013, 110(8), 2063-2072.
[http://dx.doi.org/10.1002/bit.24944] [PMID: 23616255]
[54]
Torabi, S.; Li, L.; Grabau, J.; Sands, M.; Berron, B.J.; Xu, R.; Trinkle, C.A. Cassie-baxter surfaces for reversible, barrier-free integration of microfluidics and 3D cell culture. Langmuir, 2019, 35(32), 10299-10308.
[http://dx.doi.org/10.1021/acs.langmuir.9b01163] [PMID: 31291112]
[55]
Nalluri, H.; Subramanian, S.; Staley, C. Intestinal organoids: A model to study the role of microbiota in the colonic tumor microenvironment. Future Microbiol., 2020, 15(16), 1583-1594.
[http://dx.doi.org/10.2217/fmb-2019-0345] [PMID: 33215543]
[56]
Lannagan, T.R.M.; Lee, Y.K.; Wang, T.; Roper, J.; Bettington, M.L.; Fennell, L.; Vrbanac, L.; Jonavicius, L.; Somashekar, R.; Gieniec, K.; Yang, M.; Ng, J.Q.; Suzuki, N.; Ichinose, M.; Wright, J.A.; Kobayashi, H.; Putoczki, T.L.; Hayakawa, Y.; Leedham, S.J.; Abud, H.E.; Yilmaz, O.H.; Marker, J.; Klebe, S.; Wirapati, P.; Mukherjee, S.; Tejpar, S.; Leggett, B.A.; Whitehall, V.L.J.; Worthley, D.L.; Woods, S.L. Genetic editing of colonic organoids provides a molecularly distinct and orthotopic preclinical model of serrated carcinogenesis. Gut, 2019, 68(4), 684-692.
[http://dx.doi.org/10.1136/gutjnl-2017-315920] [PMID: 29666172]
[57]
Bartfeld, S.; Bayram, T.; van de Wetering, M.; Huch, M.; Begthel, H.; Kujala, P.; Vries, R.; Peters, P.J.; Clevers, H. In vitro expansion of human gastric epithelial stem cells and their responses to bacterial infection. Gastroenterology, 2015, 148(1), 126-136.e6.
[http://dx.doi.org/10.1053/j.gastro.2014.09.042] [PMID: 25307862]
[58]
Ishida, H.; Sugimoto, S.; Kawakubo, H.; Kim, J.; Kitagawa, Y.; Sekine, S.; Koo, B.K.; Kanai, T.; Sato, T. Divergent routes toward Wnt and R-spondin niche independency during human gastric carcinogenesis. Cell, 2018, 174(4), 856-869.e17.
[http://dx.doi.org/10.1016/j.cell.2018.07.027] [PMID: 30096312]
[59]
Comprehensive molecular characterization of gastric adenocarcinoma. Nature, 2014, 513(7517), 202-209.
[http://dx.doi.org/10.1038/nature13480] [PMID: 25079317]
[60]
Kunze, B.; Wein, F.; Fang, H.Y.; Anand, A.; Baumeister, T.; Strangmann, J.; Gerland, S.; Ingermann, J.; Münch, N.S.; Wiethaler, M.; Sahm, V.; Hidalgo-Sastre, A.; Lange, S.; Lightdale, C.J.; Bokhari, A.; Falk, G.W.; Friedman, R.A.; Ginsberg, G.G.; Iyer, P.G.; Jin, Z.; Nakagawa, H.; Shawber, C.J.; Nguyen, T.; Raab, W.J.; Dalerba, P.; Rustgi, A.K.; Sepulveda, A.R.; Wang, K.K.; Schmid, R.M.; Wang, T.C.; Abrams, J.A.; Quante, M. Notch signaling mediates differentiation in Barrett’s esophagus and promotes progression to adenocarcinoma. Gastroenterology, 2020, 159(2), 575-590.
[http://dx.doi.org/10.1053/j.gastro.2020.04.033] [PMID: 32325086]
[61]
Sethi, N.S.; Kikuchi, O.; Duronio, G.N.; Stachler, M.D.; McFarland, J.M.; Ferrer-Luna, R.; Zhang, Y.; Bao, C.; Bronson, R.; Patil, D.; Sanchez-Vega, F.; Liu, J.B.; Sicinska, E.; Lazaro, J.B.; Ligon, K.L.; Beroukhim, R.; Bass, A.J. Early TP53 alterations engage environmental exposures to promote gastric premalignancy in an integrative mouse model. Nat. Genet., 2020, 52(2), 219-230.
[http://dx.doi.org/10.1038/s41588-019-0574-9] [PMID: 32025000]
[62]
Lee, J.; Snyder, E.R.; Liu, Y.; Gu, X.; Wang, J.; Flowers, B.M.; Kim, Y.J.; Park, S.; Szot, G.L.; Hruban, R.H.; Longacre, T.A.; Kim, S.K. Reconstituting development of pancreatic intraepithelial neoplasia from primary human pancreas duct cells. Nat. Commun., 2017, 8(1), 14686.
[http://dx.doi.org/10.1038/ncomms14686] [PMID: 28272465]
[63]
Seino, T.; Kawasaki, S.; Shimokawa, M.; Tamagawa, H.; Toshimitsu, K.; Fujii, M.; Ohta, Y.; Matano, M.; Nanki, K.; Kawasaki, K.; Takahashi, S.; Sugimoto, S.; Iwasaki, E.; Takagi, J.; Itoi, T.; Kitago, M.; Kitagawa, Y.; Kanai, T.; Sato, T. Human pancreatic tumor organoids reveal loss of stem cell niche factor dependence during disease progression. Cell Stem Cell, 2018, 22(3), 454-467.e6.
[http://dx.doi.org/10.1016/j.stem.2017.12.009] [PMID: 29337182]
[64]
Ryan, B.M.; Faupel-Badger, J.M. The hallmarks of premalignant conditions: A molecular basis for cancer prevention. Semin. Oncol., 2016, 43(1), 22-35.
[http://dx.doi.org/10.1053/j.seminoncol.2015.09.007] [PMID: 26970122]
[65]
Dutta, D.; Heo, I.; Clevers, H. Disease modeling in stem cell-derived 3D organoid systems. Trends Mol. Med., 2017, 23(5), 393-410.
[http://dx.doi.org/10.1016/j.molmed.2017.02.007] [PMID: 28341301]
[66]
Leslie, J.L.; Huang, S.; Opp, J.S.; Nagy, M.S.; Kobayashi, M.; Young, V.B.; Spence, J.R. Persistence and toxin production by clostridium difficile within human intestinal organoids result in disruption of epithelial paracellular barrier function. Infect. Immun., 2015, 83(1), 138-145.
[http://dx.doi.org/10.1128/IAI.02561-14] [PMID: 25312952]
[67]
Ranjan, A.; Ramachandran, S.; Gupta, N.; Kaushik, I.; Wright, S.; Srivastava, S.; Das, H.; Srivastava, S.; Prasad, S.; Srivastava, S.K. Role of phytochemicals in cancer prevention. Int. J. Mol. Sci., 2019, 20(20), E4981.
[http://dx.doi.org/10.3390/ijms20204981] [PMID: 31600949]
[68]
Fan, Y.Y.; Davidson, L.A.; Callaway, E.S.; Wright, G.A.; Safe, S.; Chapkin, R.S. A bioassay to measure energy metabolism in mouse colonic crypts, organoids, and sorted stem cells. Am. J. Physiol. Gastrointest. Liver Physiol., 2015, 309(1), G1-G9.
[http://dx.doi.org/10.1152/ajpgi.00052.2015] [PMID: 25977509]
[69]
Bhasin, N.; Alleyne, D.; Gray, O.A.; Kupfer, S.S.; Vitamin, D. Vitamin D regulation of the uridine phosphorylase 1 gene and uridine-induced DNA damage in colon in African Americans and European Americans. Gastroenterology, 2018, 155(4), 1192-1204.e9.
[http://dx.doi.org/10.1053/j.gastro.2018.06.049] [PMID: 29964038]
[70]
Ravindranathan, P.; Pasham, D.; Balaji, U.; Cardenas, J.; Gu, J.; Toden, S.; Goel, A. Mechanistic insights into anticancer properties of oligomeric proanthocyanidins from grape seeds in colorectal cancer. Carcinogenesis, 2018, 39(6), 767-777.
[http://dx.doi.org/10.1093/carcin/bgy034] [PMID: 29684110]
[71]
Toden, S.; Ravindranathan, P.; Gu, J.; Cardenas, J.; Yuchang, M.; Goel, A. Oligomeric proanthocyanidins (OPCs) target cancer stem-like cells and suppress tumor organoid formation in colorectal cancer. Sci. Rep., 2018, 8(1), 3335.
[http://dx.doi.org/10.1038/s41598-018-21478-8] [PMID: 29463813]
[72]
Zhu, X.; Tian, X.; Yang, M.; Yu, Y.; Zhou, Y.; Gao, Y.; Zhang, L.; Li, Z.; Xiao, Y.; Moses, R.E.; Li, X.; Zhang, B. Procyanidin B2 promotes intestinal injury repair and attenuates colitis-associated tumorigenesis via suppression of oxidative stress in mice. Antioxid. Redox Signal., 2021, 35(2), 75-92.
[http://dx.doi.org/10.1089/ars.2019.7911] [PMID: 32940048]
[73]
Fan, Y.Y.; Davidson, L.A.; Callaway, E.S.; Goldsby, J.S.; Chapkin, R.S. Differential effects of 2- and 3-series E-prostaglandins on in vitro expansion of Lgr5+ colonic stem cells. Carcinogenesis, 2014, 35(3), 606-612.
[http://dx.doi.org/10.1093/carcin/bgt412] [PMID: 24336194]
[74]
Afaq, F.; Zaid, M.A.; Khan, N.; Dreher, M.; Mukhtar, H. Protective effect of pomegranate-derived products on UVB-mediated damage in human reconstituted skin. Exp. Dermatol., 2009, 18(6), 553-561.
[http://dx.doi.org/10.1111/j.1600-0625.2008.00829.x] [PMID: 19320737]
[75]
Wu, H.; Xie, S.; Miao, J.; Li, Y.; Wang, Z.; Wang, M.; Yu, Q. Lactobacillus reuteri maintains intestinal epithelial regeneration and repairs damaged intestinal mucosa. Gut Microbes, 2020, 11(4), 997-1014.
[http://dx.doi.org/10.1080/19490976.2020.1734423] [PMID: 32138622]
[76]
Iwama, T.; Fujiya, M.; Konishi, H.; Tanaka, H.; Murakami, Y.; Kunogi, T.; Sasaki, T.; Takahashi, K.; Ando, K.; Ueno, N.; Kashima, S.; Moriichi, K.; Tanabe, H.; Okumura, T. Bacteria-derived ferrichrome inhibits tumor progression in sporadic colorectal neoplasms and colitis-associated cancer. Cancer Cell Int., 2021, 21(1), 21.
[http://dx.doi.org/10.1186/s12935-020-01723-9] [PMID: 33407519]
[77]
Bougen-Zhukov, N.; Nouri, Y.; Godwin, T.; Taylor, M.; Hakkaart, C.; Single, A.; Brew, T.; Permina, E.; Chen, A.; Black, M.A.; Guilford, P. Allosteric AKT inhibitors target synthetic lethal vulnerabilities in E-cadherin-deficient cells. Cancers (Basel), 2019, 11(9), E1359.
[http://dx.doi.org/10.3390/cancers11091359] [PMID: 31540244]
[78]
Reyes-Uribe, L.; Wu, W.; Gelincik, O.; Bommi, P.V.; Francisco-Cruz, A.; Solis, L.M.; Lynch, P.M.; Lim, R.; Stoffel, E.M.; Kanth, P.; Samadder, N.J.; Mork, M.E.; Taggart, M.W.; Milne, G.L.; Marnett, L.J.; Vornik, L.; Liu, D.D.; Revuelta, M.; Chang, K.; You, Y.N.; Kopelovich, L.; Wistuba, I.I.; Lee, J.J.; Sei, S.; Shoemaker, R.H.; Szabo, E.; Richmond, E.; Umar, A.; Perloff, M.; Brown, P.H.; Lipkin, S.M.; Vilar, E. Naproxen chemoprevention promotes immune activation in Lynch syndrome colorectal mucosa. Gut, 2021, 70(3), 555-566.
[http://dx.doi.org/10.1136/gutjnl-2020-320946] [PMID: 32641470]
[79]
Chen, K.; Sheng, J.; Ma, B.; Cao, W.; Hernanda, P.Y.; Liu, J.; Boor, P.P.C.; Tjon, A.S.W.; Felczak, K.; Sprengers, D.; Pankiewicz, K.W.; Metselaar, H.J.; Ma, Z.; Kwekkeboom, J.; Peppelenbosch, M.P.; Pan, Q. Suppression of hepatocellular carcinoma by mycophenolic acid in experimental models and in patients. Transplantation, 2019, 103(5), 929-937.
[http://dx.doi.org/10.1097/TP.0000000000002647] [PMID: 30747839]
[80]
Westmeier, D.; Posselt, G.; Hahlbrock, A.; Bartfeld, S.; Vallet, C.; Abfalter, C.; Docter, D.; Knauer, S.K.; Wessler, S.; Stauber, R.H. Nanoparticle binding attenuates the pathobiology of gastric cancer-associated Helicobacter pylori. Nanoscale, 2018, 10(3), 1453-1463.
[http://dx.doi.org/10.1039/C7NR06573F] [PMID: 29303193]
[81]
Serra, A.; Macià, A.; Romero, M.P.; Valls, J.; Bladé, C.; Arola, L.; Motilva, M.J. Bioavailability of procyanidin dimers and trimers and matrix food effects in in vitro and in vivo models. Br. J. Nutr., 2010, 103(7), 944-952.
[http://dx.doi.org/10.1017/S0007114509992741] [PMID: 20003617]
[82]
Giovannucci, E. Epidemiological evidence for vitamin D and colorectal cancer. J. Bone Miner. Res., 2007, 22(S2), 81-85.
[http://dx.doi.org/10.1359/jbmr.07s206] [PMID: 18290728]
[83]
Feldman, D.; Krishnan, A.V.; Swami, S.; Giovannucci, E.; Feldman, B.J. The role of vitamin D in reducing cancer risk and progression. Nat. Rev. Cancer, 2014, 14(5), 342-357.
[http://dx.doi.org/10.1038/nrc3691] [PMID: 24705652]
[84]
Fernández-Barral, A.; Costales-Carrera, A.; Buira, S.P.; Jung, P.; Ferrer-Mayorga, G.; Larriba, M.J.; Bustamante-Madrid, P.; Domínguez, O.; Real, F.X.; Guerra-Pastrián, L.; Lafarga, M.; García-Olmo, D.; Cantero, R.; Del Peso, L.; Batlle, E.; Rojo, F.; Muñoz, A.; Barbáchano, A. Vitamin D differentially regulates colon stem cells in patient-derived normal and tumor organoids. FEBS J., 2020, 287(1), 53-72.
[http://dx.doi.org/10.1111/febs.14998] [PMID: 31306552]
[85]
Alleyne, D.; Witonsky, D.B.; Mapes, B.; Nakagome, S.; Sommars, M.; Hong, E.; Muckala, K.A.; Di Rienzo, A.; Kupfer, S.S. Colonic transcriptional response to 1α25(OH)2 vitamin D3 in African- and European-Americans. J. Steroid Biochem. Mol. Biol., 2017, 168, 49-59.
[http://dx.doi.org/10.1016/j.jsbmb.2017.02.001] [PMID: 28163244]
[86]
F’guyer, S.; Afaq, F.; Mukhtar, H. Photochemoprevention of skin cancer by botanical agents. Photodermatol. Photoimmunol. Photomed., 2003, 19(2), 56-72.
[http://dx.doi.org/10.1034/j.1600-0781.2003.00019.x] [PMID: 12945805]
[87]
Richmond, E.; Viner, J.L. Chemoprevention of skin cancer. Semin. Oncol. Nurs., 2003, 19(1), 62-69.
[http://dx.doi.org/10.1053/sonu.2003.50004] [PMID: 12638382]
[88]
Lansky, E.P.; Newman, R.A. Punica granatum (pomegranate) and its potential for prevention and treatment of inflammation and cancer. J. Ethnopharmacol., 2007, 109(2), 177-206.
[http://dx.doi.org/10.1016/j.jep.2006.09.006] [PMID: 17157465]
[89]
Khan, N.; Afaq, F.; Kweon, M.H.; Kim, K.; Mukhtar, H. Oral consumption of pomegranate fruit extract inhibits growth and progression of primary lung tumors in mice. Cancer Res., 2007, 67(7), 3475-3482.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-3941] [PMID: 17389758]
[90]
Tilg, H.; Moschen, A.R. Food, immunity, and the microbiome. Gastroenterology, 2015, 148(6), 1107-1119.
[http://dx.doi.org/10.1053/j.gastro.2014.12.036] [PMID: 25575570]
[91]
Tan, J.; McKenzie, C.; Potamitis, M.; Thorburn, A.N.; Mackay, C.R.; Macia, L. The role of short-chain fatty acids in health and disease. Adv. Immunol., 2014, 121, 91-119.
[http://dx.doi.org/10.1016/B978-0-12-800100-4.00003-9] [PMID: 24388214]
[92]
Tsilimigras, M.C.; Fodor, A.; Jobin, C. Carcinogenesis and therapeutics: The microbiota perspective. Nat. Microbiol., 2017, 2(3), 17008.
[http://dx.doi.org/10.1038/nmicrobiol.2017.8] [PMID: 28225000]

Rights & Permissions Print Cite
Article Metrics
67
3
© 2024 Bentham Science Publishers | Privacy Policy