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Recent Advances in Inflammation & Allergy Drug Discovery

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ISSN (Print): 2772-2708
ISSN (Online): 2772-2716

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Review Article

Modeling Inflammatory Bowel Disease by Intestinal Organoids

Author(s): Cristina Di Giorgio*, Rosalinda Roselli, Michele Biagioli, Martina Bordoni, Patrizia Ricci, Angela Zampella, Eleonora Distrutti, Annibale Donini and Stefano Fiorucci

Volume 17, Issue 1, 2023

Published on: 06 January, 2023

Page: [39 - 53] Pages: 15

DOI: 10.2174/2772270817666221121143853

Price: $65

Abstract

Inflammatory bowel disease (IBD) is a chronic and relapsing disease caused by a dysregulated immune response to host intestinal microbiota that occurs in genetically predisposed individuals. IBD encompasses two major clinical entities: ulcerative colitis (UC), limited to the colonic mucosa, and Crohn's disease (CD), which might affect any segment of the gastrointestinal tract. Despite the prevalence of IBD increasing worldwide, therapy remains suboptimal, largely because of the variability of causative mechanisms, raising the need to develop individualized therapeutic approaches targeted to each individual patient. In this context, patients-derived intestinal organoids represent an effective tool for advancing our understanding of IBD’s pathogenesis. Organoid 3D culture systems offer a unique model for dissecting epithelial mechanisms involved IBDs and testing individualized therapy, although the lack of a functional immune system and a microbiota, two driving components of the IBD pathogenesis, represent a major barrier to their exploitation in clinical medicine. In this review, we have examined how to improve the translational utility of intestinal organoids in IBD and how co-cultures of 3D or 2D organoids and immune cells and/or intestinal microbiota might help to overcome these limitations.

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[1]
Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007; 448(7152): 427-34.
[http://dx.doi.org/10.1038/nature06005] [PMID: 17653185]
[2]
Hanauer SB. Inflammatory bowel disease: Epidemiology, pathogenesis, and therapeutic opportunities. Inflamm Bowel Dis 2006; 12 (Suppl. 1): S3-9.
[http://dx.doi.org/10.1097/01.MIB.0000195385.19268.68] [PMID: 16378007]
[3]
Abraham C, Cho JH. Inflammatory bowel disease. N Engl J Med 2009; 361(21): 2066-78.
[http://dx.doi.org/10.1056/NEJMra0804647] [PMID: 19923578]
[4]
Stokkers PCF, Hommes DW. New cytokine therapeutics for inflammatory bowel disease. Cytokine 2004; 28(4-5): 167-73.
[http://dx.doi.org/10.1016/j.cyto.2004.07.012] [PMID: 15588691]
[5]
Szigethy E, McLafferty L, Goyal A. Inflammatory bowel disease. Child Adolesc Psychiatr Clin N Am 2010; 19(2): 301-18. [ix.
[http://dx.doi.org/10.1016/j.chc.2010.01.007] [PMID: 20478501]
[6]
Ng SC, Shi HY, Hamidi N, et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: A systematic review of population-based studies. Lancet 2017; 390(10114): 2769-78.
[http://dx.doi.org/10.1016/S0140-6736(17)32448-0] [PMID: 29050646]
[7]
Heyman MB, Kirschner BS, Gold BD, et al. Children with early-onset inflammatory bowel disease (IBD): Analysis of a pediatric IBD consortium registry. J Pediatr 2005; 146(1): 35-40.
[http://dx.doi.org/10.1016/j.jpeds.2004.08.043] [PMID: 15644819]
[8]
de Silva P, Korzenik J. The changing epidemiology of inflammatory bowel disease: Identifying new high-risk populations. Clin Gastroenterol Hepatol 2015; 13(4): 690-2.
[9]
Danese S, Fiocchi C. Etiopathogenesis of inflammatory bowel diseases. World J Gastroenterol 2006; 12(30): 4807-12.
[http://dx.doi.org/10.3748/wjg.v12.i30.4807] [PMID: 16937461]
[10]
Podolsky DK. Inflammatory bowel disease. N Engl J Med 2002; 347(6): 417-29.
[http://dx.doi.org/10.1056/NEJMra020831] [PMID: 12167685]
[11]
Lakatos PL. Environmental factors affecting inflammatory bowel disease: Have we made progress? Dig Dis 2009; 27(3): 215-25.
[http://dx.doi.org/10.1159/000228553] [PMID: 19786744]
[12]
Ardizzone S, Bianchi Porro G. Biologic therapy for inflammatory bowel disease. Drugs 2005; 65(16): 2253-86.
[http://dx.doi.org/10.2165/00003495-200565160-00002] [PMID: 16266194]
[13]
Hibi T, Ogata H. Novel pathophysiological concepts of inflammatory bowel disease. J Gastroenterol 2006; 41(1): 10-6.
[http://dx.doi.org/10.1007/s00535-005-1744-3] [PMID: 16501852]
[14]
Dethlefsen L, Huse S, Sogin ML, Relman DA. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 2008; 6(11): e280.
[http://dx.doi.org/10.1371/journal.pbio.0060280] [PMID: 19018661]
[15]
Theochari NA, Stefanopoulos A, Mylonas KS, Economopoulos KP. Antibiotics exposure and risk of inflammatory bowel disease: A systematic review. Scand J Gastroenterol 2018; 53(1): 1-7.
[http://dx.doi.org/10.1080/00365521.2017.1386711] [PMID: 29022402]
[16]
Ng SC, Tang W, Ching JY, et al. Incidence and phenotype of inflammatory bowel disease based on results from the Asia-pacific Crohn’s and colitis epidemiology study. Gastroenterology 2013; 145(1): 158-165.e2.
[http://dx.doi.org/10.1053/j.gastro.2013.04.007] [PMID: 23583432]
[17]
Maunder RG. Evidence that stress contributes to inflammatory bowel disease: Evaluation, synthesis, and future directions. Inflamm Bowel Dis 2005; 11(6): 600-8.
[http://dx.doi.org/10.1097/01.MIB.0000161919.42878.a0] [PMID: 15905709]
[18]
Loftus EV Jr. Clinical epidemiology of inflammatory bowel disease: Incidence, prevalence, and environmental influences. Gastroenterology 2004; 126(6): 1504-17.
[http://dx.doi.org/10.1053/j.gastro.2004.01.063] [PMID: 15168363]
[19]
Dethlefsen L, Relman DA. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci 2011; 108(S1): 4554-61.
[http://dx.doi.org/10.1073/pnas.1000087107]
[20]
Dolan KT, Chang EB. Diet, gut microbes, and the pathogenesis of inflammatory bowel diseases. Mol Nutr Food Res 2017; 61(1): 1600129.
[http://dx.doi.org/10.1002/mnfr.201600129] [PMID: 27346644]
[21]
Abreu MT, Fukata M, Arditi M. TLR signaling in the gut in health and disease. J Immunol 2005; 174(8): 4453-60.
[http://dx.doi.org/10.4049/jimmunol.174.8.4453] [PMID: 15814663]
[22]
Geremia A, Biancheri P, Allan P, Corazza GR, Di Sabatino A. Innate and adaptive immunity in inflammatory bowel disease. Autoimmun Rev 2014; 13(1): 3-10.
[http://dx.doi.org/10.1016/j.autrev.2013.06.004] [PMID: 23774107]
[23]
Duerr RH. Genome-wide association studies herald a new era of rapid discoveries in inflammatory bowel disease research. Gastroenterology 2007; 132: 2045-9.
[24]
Peters LA, Perrigoue J, Mortha A, Iuga A, Song WM, Neiman EM. A functional genomics predictive network model identifies regulators of inflammatory bowel disease. Nat Genet 2017; 49(10): 1437-49.
[http://dx.doi.org/10.1038/ng.3947]
[25]
Uhlig HH. Monogenic diseases associated with intestinal inflammation: Implications for the understanding of inflammatory bowel disease. Gut 2013; 62(12): 1795-805.
[http://dx.doi.org/10.1136/gutjnl-2012-303956] [PMID: 24203055]
[26]
Khor B, Gardet A, Xavier RJ. Genetics and pathogenesis of inflammatory bowel disease. Nature 2011; 474(7351): 307-17.
[http://dx.doi.org/10.1038/nature10209] [PMID: 21677747]
[27]
Anderson CA, Boucher G, Lees CW, et al. Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat Genet 2011; 43(3): 246-52.
[http://dx.doi.org/10.1038/ng.764] [PMID: 21297633]
[28]
Brand S. Crohn’s disease: Th1, Th17 or both? The change of a paradigm: New immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn’s disease. Gut 2009; 58(8): 1152-67.
[http://dx.doi.org/10.1136/gut.2008.163667] [PMID: 19592695]
[29]
Chalaris A, Adam N, Sina C, et al. Critical role of the disintegrin metalloprotease ADAM17 for intestinal inflammation and regeneration in mice. J Exp Med 2010; 207(8): 1617-24.
[http://dx.doi.org/10.1084/jem.20092366] [PMID: 20603312]
[30]
Lacher M, Fitze G, Helmbrecht J, et al. Hirschsprung-associated enterocolitis develops independently of NOD2 variants. J Pediatr Surg 2010; 45(9): 1826-31.
[http://dx.doi.org/10.1016/j.jpedsurg.2010.02.039] [PMID: 20850627]
[31]
Choy MC, Visvanathan K, De Cruz P. An overview of the innate and adaptive immune system in inflammatory bowel disease. Inflamm Bowel Dis 2017; 23(1): 2-13.
[http://dx.doi.org/10.1097/MIB.0000000000000955] [PMID: 27779499]
[32]
Fournier BM, Parkos CA. The role of neutrophils during intestinal inflammation. Mucosal Immunol 2012; 5(4): 354-66.
[http://dx.doi.org/10.1038/mi.2012.24] [PMID: 22491176]
[33]
Rigaud S, Fondanèche MC, Lambert N, et al. XIAP deficiency in humans causes an X-linked lymphoproliferative syndrome. Nature 2006; 444(7115): 110-4.
[http://dx.doi.org/10.1038/nature05257] [PMID: 17080092]
[34]
Muise AM, Xu W, Guo CH, et al. NADPH oxidase complex and IBD candidate gene studies: Identification of a rare variant in NCF2 that results in reduced binding to RAC2. Gut 2012; 61(7): 1028-35.
[http://dx.doi.org/10.1136/gutjnl-2011-300078] [PMID: 21900546]
[35]
Schäppi MG, Smith VV, Goldblatt D, Lindley KJ, Milla PJ. Colitis in chronic granulomatous disease. Arch Dis Child 2001; 84(2): 147-51.
[http://dx.doi.org/10.1136/adc.84.2.147] [PMID: 11159292]
[36]
Lopez-Herrera G, Tampella G, Pan-Hammarström Q, et al. Deleterious mutations in LRBA are associated with a syndrome of immune deficiency and autoimmunity. Am J Hum Genet 2012; 90(6): 986-1001.
[http://dx.doi.org/10.1016/j.ajhg.2012.04.015] [PMID: 22608502]
[37]
Visser G, Rake JP, Fernandes J, et al. Neutropenia, neutrophil dysfunction, and inflammatory bowel disease in glycogen storage disease type Ib: Results of the European Study on Glycogen Storage Disease Type I. J Pediatr 2000; 137(2): 187-91.
[http://dx.doi.org/10.1067/mpd.2000.105232] [PMID: 10931410]
[38]
Kühn R, Löhler J, Rennick D, Rajewsky K, Müller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 1993; 75(2): 263-74.
[http://dx.doi.org/10.1016/0092-8674(93)80068-P] [PMID: 8402911]
[39]
Shouval DS, Ouahed J, Biswas A, et al. Interleukin 10 receptor signaling: Master regulator of intestinal mucosal homeostasis in mice and humans. Adv Immunol 2014; 122: 177-210.
[http://dx.doi.org/10.1016/B978-0-12-800267-4.00005-5] [PMID: 24507158]
[40]
Moran CJ, Walters TD, Guo CH, et al. IL-10R polymorphisms are associated with very-early-onset ulcerative colitis. Inflamm Bowel Dis 2013; 19(1): 115-23.
[http://dx.doi.org/10.1002/ibd.22974] [PMID: 22550014]
[41]
Zeng Z, Mukherjee A, Zhang H. From genetics to epigenetics, roles of epigenetics in inflammatory bowel disease. Front Genet 2019; 10: 1017.
[http://dx.doi.org/10.3389/fgene.2019.01017] [PMID: 31737035]
[42]
Sambuy Y, De Angelis I, Ranaldi G, Scarino ML, Stammati A, Zucco F. The Caco-2 cell line as a model of the intestinal barrier: Influence of cell and culture-related factors on Caco-2 cell functional characteristics. Cell Biol Toxicol 2005; 21(1): 1-26.
[http://dx.doi.org/10.1007/s10565-005-0085-6] [PMID: 15868485]
[43]
O’Connell L, Winter DC. Organoids: Past learning and future directions. Stem Cells Dev 2020; 29(5): 281-9.
[http://dx.doi.org/10.1089/scd.2019.0227] [PMID: 31805828]
[44]
McKay DM, Philpott DJ, Perdue MH. Review article: In vitro models in inflammatory bowel disease research- A critical review. Aliment Pharmacol Ther 1997; 11 (Suppl. 3): 70-80.
[http://dx.doi.org/10.1111/j.1365-2036.1997.tb00811.x] [PMID: 9467981]
[45]
Mizoguchi A. Animal models of inflammatory bowel disease. Prog Mol Biol Transl Sci 2012; 105: 263-320.
[http://dx.doi.org/10.1016/B978-0-12-394596-9.00009-3] [PMID: 22137435]
[46]
Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 2009; 459(7244): 262-5.
[http://dx.doi.org/10.1038/nature07935]
[47]
Howitt MR, Lavoie S, Michaud M, et al. Tuft cells, taste-chemosensory cells, orchestrate parasite type 2 immunity in the gut. Science 2016; 351(6279): 1329-33.
[http://dx.doi.org/10.1126/science.aaf1648] [PMID: 26847546]
[48]
de Lau W, Kujala P, Schneeberger K, et al. Peyer’s patch M cells derived from Lgr5(+) stem cells require SpiB and are induced by RankL in cultured “miniguts”. Mol Cell Biol 2012; 32(18): 3639-47.
[http://dx.doi.org/10.1128/MCB.00434-12] [PMID: 22778137]
[49]
Lancaster MA, Knoblich JA. Organogenesis in a dish: Modeling development and disease using organoid technologies. Science 2014; 345(6194): 1247125.
[http://dx.doi.org/10.1126/science.1247125] [PMID: 25035496]
[50]
Bellono NW, Bayrer JR, Leitch DB, et al. Enterochromaffin cells are gut chemosensors that couple to sensory neural pathways. Cell 2017; 170(1): 185-198.e16.
[http://dx.doi.org/10.1016/j.cell.2017.05.034] [PMID: 28648659]
[51]
Takao K, Miyakawa T. Genomic responses in mouse models greatly mimic human inflammatory diseases. Proc Natl Acad Sci 2015; 112(4): 1167-72.
[http://dx.doi.org/10.1073/pnas.1401965111] [PMID: 25092317]
[52]
van de Wetering M, Francies HE, Francis JM, et al. Prospective derivation of a living organoid biobank of colorectal cancer patients. Cell 2015; 161(4): 933-45.
[http://dx.doi.org/10.1016/j.cell.2015.03.053] [PMID: 25957691]
[53]
McGuckin MA, Lindén SK, Sutton P, Florin TH. Mucin dynamics and enteric pathogens. Nat Rev Microbiol 2011; 9(4): 265-78.
[http://dx.doi.org/10.1038/nrmicro2538] [PMID: 21407243]
[54]
Buisine MP, Desreumaux P, Debailleul V, et al. Abnormalities in mucin gene expression in Crohn’s disease. Inflamm Bowel Dis 1999; 5(1): 24-32.
[http://dx.doi.org/10.1097/00054725-199902000-00004] [PMID: 10028446]
[55]
Salim SY, Söderholm JD. Importance of disrupted intestinal barrier in inflammatory bowel diseases. Inflamm Bowel Dis 2011; 17(1): 362-81.
[http://dx.doi.org/10.1002/ibd.21403] [PMID: 20725949]
[56]
Wallace KL, Zheng L-B, Kanazawa Y, Shih DQ. Immunopathology of inflammatory bowel disease. World J Gastroenterol 2014; 20(1): 6-21.
[http://dx.doi.org/10.3748/wjg.v20.i1.6] [PMID: 24415853]
[57]
Williams JM, Duckworth CA, Burkitt MD, Watson AJM, Campbell BJ, Pritchard DM. Epithelial cell shedding and barrier function: A matter of life and death at the small intestinal villus tip. Vet Pathol 2015; 52(3): 445-55.
[http://dx.doi.org/10.1177/0300985814559404] [PMID: 25428410]
[58]
Huch M, Gehart H, van Boxtel R, Hamer K, Blokzijl F, Verstegen MMA. Long-term culture of genome-stable bipotent stem cells from adult human liver. Cell 2014; 160(1-2): 299-312.
[59]
Beumer J, Puschhof J, Yengej FY, et al. BMP gradient along the intestinal villus axis controls zonated enterocyte and goblet cell states. Cell Rep 2022; 38(9): 110438.
[http://dx.doi.org/10.1016/j.celrep.2022.110438] [PMID: 35235783]
[60]
Sumigray KD, Terwilliger M, Lechler T. Morphogenesis and compartmentalization of the intestinal crypt. Dev Cell 2018; 45(2): 183-197.e5.
[http://dx.doi.org/10.1016/j.devcel.2018.03.024] [PMID: 29689194]
[61]
Kurokawa K, Hayakawa Y, Koike K. Plasticity of intestinal epithelium: Stem cell niches and regulatory signals. Int J Mol Sci 2020; 22(1): 357.
[http://dx.doi.org/10.3390/ijms22010357] [PMID: 33396437]
[62]
Crosnier C, Stamataki D, Lewis J. Organizing cell renewal in the intestine: Stem cells, signals and combinatorial control. Nat Rev Genet 2006; 7(5): 349-59.
[http://dx.doi.org/10.1038/nrg1840] [PMID: 16619050]
[63]
Dedhia PH, Bertaux-Skeirik N, Zavros Y, Spence JR. Organoid models of human gastrointestinal development and disease. Gastroenterology 2016; 150(5): 1098-112.
[http://dx.doi.org/10.1053/j.gastro.2015.12.042] [PMID: 26774180]
[64]
Spence JR, Mayhew CN, Rankin SA, et al. Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature 2011; 470(7332): 105-9.
[http://dx.doi.org/10.1038/nature09691] [PMID: 21151107]
[65]
Middendorp S, Schneeberger K, Wiegerinck CL, et al. Adult stem cells in the small intestine are intrinsically programmed with their location-specific function. Stem Cells 2014; 32(5): 1083-91.
[http://dx.doi.org/10.1002/stem.1655] [PMID: 24496776]
[66]
Sato T, Stange DE, Ferrante M, et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett’s epithelium. Gastroenterology 2011; 141(5): 1762-72.
[http://dx.doi.org/10.1053/j.gastro.2011.07.050] [PMID: 21889923]
[67]
Zachos NC, Kovbasnjuk O, Foulke-Abel J, et al. Human enteroids/colonoids and intestinal organoids functionally recapitulate normal intestinal physiology and pathophysiology. J Biol Chem 2016; 291(8): 3759-66.
[http://dx.doi.org/10.1074/jbc.R114.635995] [PMID: 26677228]
[68]
Degirmenci B, Valenta T, Dimitrieva S, Hausmann G, Basler K. GLI1-expressing mesenchymal cells form the essential Wnt-secreting niche for colon stem cells. Nature 2018; 558(7710): 449-53.
[http://dx.doi.org/10.1038/s41586-018-0190-3] [PMID: 29875413]
[69]
Mahe MM, Aihara E, Schumacher MA, Zavros Y, Montrose MH, Helmrath MA. Establishment of gastrointestinal epithelial organoids. Curr Protoc Mouse Biol 2014; 3(4): 217-40.
[70]
Di Giorgio C, Roselli R, Biagioli M, Marchianò S, Distrutti E, Bordoni M. Organoids as ex vivo culture system to investigate infection-host interaction in gastric pre-carcinogenesis Recent Adv Inflamm allergy drug Discov 2022.
[http://dx.doi.org/10.2174/2772270816666220105123702]
[71]
Eckburg PB, Bik EM, Bernstein CN, et al. Diversity of the human intestinal microbial flora. Science 2005; 308(5728): 1635-8.
[http://dx.doi.org/10.1126/science.1110591] [PMID: 15831718]
[72]
Arpaia N, Campbell C, Fan X, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013; 504(7480): 451-5.
[http://dx.doi.org/10.1038/nature12726] [PMID: 24226773]
[73]
Fiorucci S, Carino A, Baldoni M, Santucci L, Costanzi E, Graziosi L. Bile acid signaling in inflammatory bowel diseases. Dig Dis Sci 2020; 66(3): 674-93.
[74]
Biagioli M, Carino A, Cipriani S, et al. The bile acid receptor GPBAR1 regulates the M1/M2 phenotype of intestinal macrophages and activation of GPBAR1 rescues mice from murine colitis. J Immunol 2017; 199(2): 718-33.
[http://dx.doi.org/10.4049/jimmunol.1700183] [PMID: 28607110]
[75]
D’Amore C, Di Leva FSS, Sepe V, Renga B, Del Gaudio C, D’Auria MVV. Design, synthesis, and biological evaluation of potent dual agonists of nuclear and membrane bile acid receptors. J Med Chem 2014; 57(3): 937-54.
[76]
Renga B, Mencarelli A, Cipriani S, D’Amore C, Carino A, Bruno A. The bile acid sensor FXR is required for immune-regulatory activities of TLR-9 in intestinal inflammation. PLoS One 2013; 8(1): e54472.
[77]
Festa C, Renga B, D’Amore C, Sepe V, Finamore C, De Marino S. Exploitation of cholane scaffold for the discovery of potent and selective farnesoid X receptor (FXR) and G-protein coupled bile acid receptor 1 (GP-BAR1) ligands. J Med Chem 2014; 57(20): 8477-95.
[78]
Richard ML, Sokol H. The gut mycobiota: Insights into analysis, environmental interactions and role in gastrointestinal diseases. Nat Rev Gastroenterol Hepatol 2019; 16(6): 331-45.
[http://dx.doi.org/10.1038/s41575-019-0121-2] [PMID: 30824884]
[79]
Dotti I, Salas A. Potential use of human stem cell-derived intestinal organoids to study inflammatory bowel diseases. Inflamm Bowel Dis 2018; 24(12): 2501-9.
[PMID: 30169820]
[80]
Forbester JL, Goulding D, Vallier L, Hannan N, Hale C, Pickard D. Interaction of salmonella enterica serovar typhimurium with intestinal organoids derived from human induced pluripotent stem cells. Infect Immun 2015; 83(7): 2926-34.
[http://dx.doi.org/10.1128/IAI.00161-15]
[81]
Boccellato F, Woelffling S, Imai-Matsushima A, et al. Polarised epithelial monolayers of the gastric mucosa reveal insights into mucosal homeostasis and defence against infection. Gut 2019; 68(3): 400-13.
[http://dx.doi.org/10.1136/gutjnl-2017-314540] [PMID: 29467166]
[82]
Rajan A, Vela L, Zeng XL, et al. Novel segment- and host-specific patterns of enteroaggregative Escherichia coli adherence to human intestinal enteroids. MBio 2018; 9(1): e02419-17.
[http://dx.doi.org/10.1128/mBio.02419-17] [PMID: 29463660]
[83]
Saxena K, Blutt SE, Ettayebi K, et al. Human intestinal enteroids: A new model to study human rotavirus infection, host restriction, and pathophysiology. J Virol 2016; 90(1): 43-56.
[http://dx.doi.org/10.1128/JVI.01930-15] [PMID: 26446608]
[84]
Bartfeld S, Bayram T, van de Wetering M, Huch M, Begthel H, Kujala P. In vitro expansion of human gastric epithelial stem cells and their responses to bacterial infection. Gastroenterology 2014; 148(1): 126-36.
[85]
Co JY, Margalef-Català M, Li X, et al. Controlling epithelial polarity: A human enteroid model for host-pathogen interactions. Cell Rep 2019; 26(9): 2509-2520.e4.
[http://dx.doi.org/10.1016/j.celrep.2019.01.108] [PMID: 30811997]
[86]
Wang AZ, Ojakian GK, Nelson WJ. Steps in the morphogenesis of a polarized epithelium. II. Disassembly and assembly of plasma membrane domains during reversal of epithelial cell polarity in multicellular epithelial (MDCK) cysts. J Cell Sci 1990; 95(1): 153-65.
[http://dx.doi.org/10.1242/jcs.95.1.153] [PMID: 2351700]
[87]
Co JY, Margalef-Català M, Monack DM, Amieva MR. Controlling the polarity of human gastrointestinal organoids to investigate epithelial biology and infectious diseases. Nat Protoc 2021; 16(11): 5171-92.
[http://dx.doi.org/10.1038/s41596-021-00607-0] [PMID: 34663962]
[88]
Li Y, Yang N, Chen J, et al. Next-generation porcine intestinal organoids: An apical-out organoid model for swine enteric virus infection and immune response investigations. J Virol 2020; 94(21): e01006-20.
[http://dx.doi.org/10.1128/JVI.01006-20] [PMID: 32796075]
[89]
Wang Y, DiSalvo M, Gunasekara DB, et al. Self-renewing monolayer of primary colonic or rectal epithelial cells. Cell Mol Gastroenterol Hepatol 2017; 4(1): 165-182.e7.
[http://dx.doi.org/10.1016/j.jcmgh.2017.02.011] [PMID: 29204504]
[90]
Angus HCK, Butt AG, Schultz M, Kemp RA. Intestinal organoids as a tool for inflammatory bowel disease research. Front Med 2020; 6: 334.
[http://dx.doi.org/10.3389/fmed.2019.00334] [PMID: 32010704]
[91]
Kozuka K, He Y, Koo-McCoy S, et al. Development and characterization of a human and mouse intestinal epithelial cell monolayer platform. Stem Cell Reports 2017; 9(6): 1976-90.
[http://dx.doi.org/10.1016/j.stemcr.2017.10.013] [PMID: 29153987]
[92]
Platt AM, Mowat AM. Mucosal macrophages and the regulation of immune responses in the intestine. Immunol Lett 2008; 119(1-2): 22-31.
[http://dx.doi.org/10.1016/j.imlet.2008.05.009] [PMID: 18601952]
[93]
Kamada N, Hisamatsu T, Okamoto S, et al. Unique CD14 intestinal macrophages contribute to the pathogenesis of Crohn disease via IL-23/IFN-gamma axis. J Clin Invest 2008; 118(6): 2269-80.
[PMID: 18497880]
[94]
Noel G, Baetz NW, Staab JF, et al. A primary human macrophage-enteroid co-culture model to investigate mucosal gut physiology and host-pathogen interactions. Sci Rep 2017; 7(1): 45270.
[http://dx.doi.org/10.1038/srep45270] [PMID: 28345602]
[95]
Gaudino SJ, Kumar P. Cross-talk between antigen presenting cells and T cells impacts intestinal homeostasis, bacterial infections, and tumorigenesis. Front Immunol 2019; 10: 360.
[http://dx.doi.org/10.3389/fimmu.2019.00360] [PMID: 30894857]
[96]
Duchmann R, Kaiser I, Hermann E, Mayet W, Ewe K. BÜSchenfelde K-HMZ. Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease (IBD). Clin Exp Immunol 2008; 102(3): 448-55.
[http://dx.doi.org/10.1111/j.1365-2249.1995.tb03836.x] [PMID: 8536356]
[97]
Tindemans I, Joosse ME, Samsom JN. Dissecting the heterogeneity in T-cell mediated inflammation in IBD. Cells 2020; 9(1): 110.
[http://dx.doi.org/10.3390/cells9010110] [PMID: 31906479]
[98]
Nozaki K, Mochizuki W, Matsumoto Y, et al. Co-culture with intestinal epithelial organoids allows efficient expansion and motility analysis of intraepithelial lymphocytes. J Gastroenterol 2016; 51(3): 206-13.
[http://dx.doi.org/10.1007/s00535-016-1170-8] [PMID: 26800996]
[99]
Rouch JD, Scott A, Lei NY, et al. Development of functional microfold (M) cells from intestinal stem cells in primary human enteroids. PLoS One 2016; 11(1): e0148216.
[http://dx.doi.org/10.1371/journal.pone.0148216] [PMID: 26820624]
[100]
Goldberg R, Prescott N, Lord GM, MacDonald TT, Powell N. The unusual suspects—innate lymphoid cells as novel therapeutic targets in IBD. Nat Rev Gastroenterol Hepatol 2015; 12(5): 271-83.
[http://dx.doi.org/10.1038/nrgastro.2015.52] [PMID: 25971811]
[101]
Forkel M, Mjösberg J. Dysregulation of group 3 innate lymphoid cells in the pathogenesis of inflammatory bowel disease. Curr Allergy Asthma Rep 2016; 16(10): 73.
[http://dx.doi.org/10.1007/s11882-016-0652-3] [PMID: 27645534]
[102]
Lindemans CA, Calafiore M, Mertelsmann AM, et al. Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature 2015; 528(7583): 560-4.
[http://dx.doi.org/10.1038/nature16460] [PMID: 26649819]
[103]
Lenti MV, Di Sabatino A. Intestinal fibrosis. Mol Aspects Med 2019; 65: 100-9.
[http://dx.doi.org/10.1016/j.mam.2018.10.003] [PMID: 30385174]
[104]
Rodansky ES, Johnson LA, Huang S, Spence JR, Higgins PDR. Intestinal organoids: A model of intestinal fibrosis for evaluating anti-fibrotic drugs. Exp Mol Pathol 2015; 98(3): 346-51.
[http://dx.doi.org/10.1016/j.yexmp.2015.03.033] [PMID: 25828392]
[105]
Bein A, Shin W, Jalili-Firoozinezhad S, et al. Microfluidic organ-on-a-chip models of human intestine. Cell Mol Gastroenterol Hepatol 2018; 5(4): 659-68.
[http://dx.doi.org/10.1016/j.jcmgh.2017.12.010] [PMID: 29713674]
[106]
Sidar B, Jenkins BR, Huang S, Spence JR, Walk ST, Wilking JN. Long-term flow through human intestinal organoids with the gut organoid flow chip (GOFlowChip). Lab Chip 2019; 19(20): 3552-62.
[http://dx.doi.org/10.1039/C9LC00653B] [PMID: 31556415]
[107]
Jalili-Firoozinezhad S, Gazzaniga FS, Calamari EL, et al. A complex human gut microbiome cultured in an anaerobic intestine-on-a-chip. Nat Biomed Eng 2019; 3(7): 520-31.
[http://dx.doi.org/10.1038/s41551-019-0397-0] [PMID: 31086325]
[108]
Kim HJ, Huh D, Hamilton G, Ingber DE. Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab Chip 2012; 12(12): 2165-74.
[http://dx.doi.org/10.1039/c2lc40074j] [PMID: 22434367]
[109]
Kasendra M, Tovaglieri A, Sontheimer-Phelps A, et al. Development of a primary human small intestine on a chip using biopsy-derived organoids. Sci Rep 2018; 8(1): 2871.
[http://dx.doi.org/10.1038/s41598-018-21201-7] [PMID: 29440725]
[110]
Roh TT, Chen Y, Paul HT, Guo C, Kaplan DL. 3D bioengineered tissue model of the large intestine to study inflammatory bowel disease. Biomaterials 2019; 225: 119517.
[http://dx.doi.org/10.1016/j.biomaterials.2019.119517] [PMID: 31580968]
[111]
Neurath MF. Current and emerging therapeutic targets for IBD. Nat Rev Gastroenterol Hepatol 2017; 14(5): 269-78.
[http://dx.doi.org/10.1038/nrgastro.2016.208] [PMID: 28144028]
[112]
Mencarelli A, Cipriani S, Francisci D, Santucci L, Baldelli F, Distrutti E. Highly specific blockade of CCR5 inhibits leukocyte trafficking and reduces mucosal inflammation in murine colitis. Sci Rep 2016; 6: 30802.
[http://dx.doi.org/10.1038/srep30802]
[113]
Jakubczyk D. Leszczyńska K, Górska S. The effectiveness of probiotics in the treatment of Inflammatory Bowel Disease (IBD)—A critical review. Nutrients 2020; 12(7): 1973.
[http://dx.doi.org/10.3390/nu12071973] [PMID: 32630805]
[114]
Mencarelli A, Distrutti E, Renga B, Cipriani S, Palladino G, Booth C. Development of non-antibiotic macrolide that corrects inflammation-driven immune dysfunction in models of inflammatory bowel diseases and arthritis. Eur J Pharmacol 2011; 665(1-3): 29-39.
[http://dx.doi.org/10.1016/j.ejphar.2011.04.036]
[115]
Annaházi A, Molnár T. Optimal endpoint of therapy in IBD: An update on factors determining a successful drug withdrawal. Gastroenterol Res Pract 2015; 2015: 1-18.
[http://dx.doi.org/10.1155/2015/832395] [PMID: 26199624]
[116]
Weiser M, Simon JM, Kochar B, et al. Molecular classification of Crohn’s disease reveals two clinically relevant subtypes. Gut 2018; 67(1): 36-42.
[http://dx.doi.org/10.1136/gutjnl-2016-312518] [PMID: 27742763]
[117]
Cleynen I, Boucher G, Jostins L, et al. Inherited determinants of Crohn’s disease and ulcerative colitis phenotypes: A genetic association study. Lancet 2016; 387(10014): 156-67.
[http://dx.doi.org/10.1016/S0140-6736(15)00465-1] [PMID: 26490195]
[118]
d’Aldebert E, Quaranta M, Sébert M, et al. Characterization of human colon organoids from inflammatory bowel disease patients. Front Cell Dev Biol 2020; 8: 363.
[http://dx.doi.org/10.3389/fcell.2020.00363] [PMID: 32582690]
[119]
Suzuki K, Murano T, Shimizu H, et al. Single cell analysis of Crohn’s disease patient-derived small intestinal organoids reveals disease activity-dependent modification of stem cell properties. J Gastroenterol 2018; 53(9): 1035-47.
[http://dx.doi.org/10.1007/s00535-018-1437-3] [PMID: 29374777]
[120]
Hibiya S, Tsuchiya K, Hayashi R, et al. Long-term inflammation transforms intestinal epithelial cells of colonic organoids. J Crohn’s Colitis 2017; 11(5): 621-30.
[PMID: 28453760]
[121]
O’Connell L, Winter DC, Aherne CM. The role of organoids as a novel platform for modeling of inflammatory bowel disease. Front Pediatr 2021; 9: 624045.
[http://dx.doi.org/10.3389/fped.2021.624045] [PMID: 33681101]
[122]
Howell KJ, Kraiczy J, Nayak KM, et al. DNA methylation and transcription patterns in intestinal epithelial cells from pediatric patients with inflammatory bowel diseases differentiate disease subtypes and associate with outcome. Gastroenterology 2018; 154(3): 585-98.
[http://dx.doi.org/10.1053/j.gastro.2017.10.007] [PMID: 29031501]
[123]
Ventham NT, Kennedy NA, Nimmo ER, Satsangi J. Beyond gene discovery in inflammatory bowel disease: The emerging role of epigenetics. Gastroenterology 2013; 145(2): 293-308.
[http://dx.doi.org/10.1053/j.gastro.2013.05.050] [PMID: 23751777]
[124]
Cooke J, Zhang H, Greger L, et al. Mucosal genome-wide methylation changes in inflammatory bowel disease. Inflamm Bowel Dis 2012; 18(11): 2128-37.
[http://dx.doi.org/10.1002/ibd.22942] [PMID: 22419656]
[125]
Yu DH, Gadkari M, Zhou Q, et al. Postnatal epigenetic regulation of intestinal stem cells requires DNA methylation and is guided by the microbiome. Genome Biol 2015; 16(1): 211.
[http://dx.doi.org/10.1186/s13059-015-0763-5] [PMID: 26420038]
[126]
Hill DR, Spence JR. Gastrointestinal organoids: Understanding the molecular basis of the host–microbe interface. Cell Mol Gastroenterol Hepatol 2017; 3(2): 138-49.
[http://dx.doi.org/10.1016/j.jcmgh.2016.11.007] [PMID: 28275681]

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