Detecting host responses to microbial stimulation using primary epithelial organoids

References

• Zhou A, Yuan Y, Yang M, Huang Y, Li X, Li S, Yang S, Tang B. Crosstalk between the gut microbiota and epithelial cells under physiological and infectious conditions. Front Cell Infect Microbiol. 2022;12:832672. doi:10.3389/fcimb.2022.832672.
   PubMed Web of Science ®Google Scholar
• Rubert J, Schweiger PJ, Mattivi F, Tuohy K, Jensen KB, Lunardi A. Intestinal organoids: a tool for modelling diet–microbiome–host interactions. Trends Endocrinol Metab. 2020;31(11):848–15. doi:10.1016/j.tem.2020.02.004.
   PubMed Web of Science ®Google Scholar
• Kaiko GE, Ryu SH, Koues OI, Collins PL, Solnica-Krezel L, Pearce EJ, Pearce EL, Oltz EM, Stappenbeck TS. The colonic crypt protects stem cells from microbiota-derived metabolites. Cell. 2016;165(7):1708–1720. doi:10.1016/j.cell.2016.05.018.
   PubMed Web of Science ®Google Scholar
• Nakamura A, Kurihara S, Takahashi D, Ohashi W, Nakamura Y, Kimura S, Onuki M, Kume A, Sasazawa Y, Furusawa Y, et al. Symbiotic polyamine metabolism regulates epithelial proliferation and macrophage differentiation in the colon. Nat Commun. 2021;12(1):2105. doi:10.1038/s41467-021-22212-1.
   PubMed Web of Science ®Google Scholar
• Ehrlich AM, Pacheco AR, Henrick BM, Taft D, Xu G, Huda MN, Mishchuk D, Goodson ML, Slupsky C, Barile D, et al. Indole-3-lactic acid associated with Bifidobacterium-dominated microbiota significantly decreases inflammation in intestinal epithelial cells. BMC Microbiol. 2020;20(1):357. doi:10.1186/s12866-020-02023-y.
   PubMed Web of Science ®Google Scholar
• Wu SE, Hashimoto-Hill S, Woo V, Eshleman EM, Whitt J, Engleman L, Karns R, Denson LA, Haslam DB, Alenghat T, et al. Microbiota-derived metabolite promotes HDAC3 activity in the gut. Nature. 2020;586(7827):108–112. doi:10.1038/s41586-020-2604-2.
   PubMed Web of Science ®Google Scholar
• Schwarzer M, Gautam UK, Makki K, Lambert A, Brabec T, Joly A, Šrůtková D, Poinsot P, Novotná T, Geoffroy S, et al. Microbe-mediated intestinal NOD2 stimulation improves linear growth of undernourished infant mice. Sci. 2023;379(6634):826–833. doi:10.1126/science.ade9767.
   PubMed Web of Science ®Google Scholar
• Langerholc T, Maragkoudakis PA, Wollgast J, Gradisnik L, Cencic A. Novel and established intestinal cell line models - an indispensable tool in food science and nutrition. Trends Food Sci Technol. 2011;22:S11–S20. doi:10.1016/j.tifs.2011.03.010.
   PubMed Web of Science ®Google Scholar
• Sato T, Stange DE, Ferrante M, Vries RG, Van Es JH, Van den Brink S, et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and barrett’s epithelium. Gastroenterology. 2011;141:1762–1772. doi:10.1053/j.gastro.2011.07.050.
   PubMed Web of Science ®Google Scholar
• Schweiger PJ, Jensen KB. Modeling human disease using organotypic cultures. Curr Opin Cell Biol. 2016;43:22–29. doi:10.1016/j.ceb.2016.07.003.
   PubMed Web of Science ®Google Scholar
• Forbester JL, Goulding D, Vallier L, Hannan N, Hale C, Pickard D, Mukhopadhyay S, Dougan G. Interaction of Salmonella enterica serovar typhimurium with intestinal organoids derived from human induced pluripotent stem cells. Infect Immun. 2015;83(7):2926–2934. doi:10.1128/IAI.00161-15.
   PubMed Web of Science ®Google Scholar
• Pleguezuelos-Manzano C, Puschhof J, Rosendahl Huber A, van Hoeck A, Wood HM, Nomburg J, Gurjao C, Manders F, Dalmasso G, Stege PB, et al. Mutational signature in colorectal cancer caused by genotoxic pks(+) E. coli. Nature. 2020;580(7802):269–273. doi:10.1038/s41586-020-2080-8.
   PubMed Web of Science ®Google Scholar
• Leslie JL, Huang S, Opp JS, Nagy MS, Kobayashi M, Young VB, Spence JR. 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. doi:10.1128/IAI.02561-14.
   PubMed Web of Science ®Google Scholar
• Dheer R, Young VB. Stem-cell-derived models: tools for studying role of microbiota in intestinal homeostasis and disease. Curr Opin Gastroenterol. 2021;37(1):15–22. doi:10.1097/MOG.0000000000000691.
   PubMed Web of Science ®Google Scholar
• Wang Y, DiSalvo M, Gunasekara DB, Dutton J, Proctor A, Lebhar MS, Williamson IA, Speer J, Howard RL, Smiddy NM, et al. Self-renewing monolayer of primary colonic or rectal epithelial cells. Cell Mol Gastroenterol Hepatol. 2017;4(1):165–82 e7. doi:10.1016/j.jcmgh.2017.02.011.
   PubMed Web of Science ®Google Scholar
• Thorne CA, Chen IW, Sanman LE, Cobb MH, Wu LF, Altschuler SJ. Enteroid monolayers reveal an autonomous WNT and BMP circuit controlling intestinal epithelial growth and organization. Dev Cell. 2018;44(5):624–33 e4. doi:10.1016/j.devcel.2018.01.024.
   PubMed Web of Science ®Google Scholar
• Pond KW, Morris JM, Alkhimenok O, Varghese RP, Cabel CR, Ellis NA, Chakrabarti J, Zavros Y, Merchant JL, Thorne CA, et al. Live-cell imaging in human colonic monolayers reveals ERK waves limit the stem cell compartment to maintain epithelial homeostasis. Elife. 2022;11:11. doi:10.7554/eLife.78837.
   Web of Science ®Google Scholar
• Puschhof J, Pleguezuelos-Manzano C, Martinez-Silgado A, Akkerman N, Saftien A, Boot C, de Waal A, Beumer J, Dutta D, Heo I, et al. Intestinal organoid cocultures with microbes. Nat Protoc. 2021;16(10):4633–4649. doi:10.1038/s41596-021-00589-z.
   PubMed Web of Science ®Google Scholar
• Bornholdt J, Broholm C, Chen Y, Rago A, Sloth S, Hendel J, Melsæther C, Müller CV, Juul Nielsen M, Strickertsson J, et al. Personalized B cell response to the lactobacillus rhamnosus GG probiotic in healthy human subjects: a randomized trial. Gut Microbes. 2020;12(1):1–14. doi:10.1080/19490976.2020.1854639.
   PubMed Web of Science ®Google Scholar
• Meran L, Massie I, Campinoti S, Weston AE, Gaifulina R, Tullie L, Faull P, Orford M, Kucharska A, Baulies A, et al. Engineering transplantable jejunal mucosal grafts using patient-derived organoids from children with intestinal failure. Nat Med. 2020;26(10):1593–1601. doi:10.1038/s41591-020-1024-z.
   PubMed Web of Science ®Google Scholar
• Middendorp S, Schneeberger K, Wiegerinck CL, Mokry M, Akkerman RD, van Wijngaarden S, Clevers H, Nieuwenhuis EES. Adult stem cells in the small intestine are intrinsically programmed with their location-specific function. Stem Cells. 2014;32(5):1083–1091. doi:10.1002/stem.1655.
   PubMed Web of Science ®Google Scholar
• Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, van den Born M, Barker N, Shroyer NF, van de Wetering M, Clevers H, et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature. 2011;469(7330):415–418. doi:10.1038/nature09637.
   PubMed Web of Science ®Google Scholar
• Korinek V, Barker N, Moerer P, van Donselaar E, Huls G, Peters PJ, Clevers H. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking tcf-4. Nat Genet. 1998;19(4):379–383. doi:10.1038/1270.
   PubMed Web of Science ®Google Scholar
• Jung P, Sommer C, Barriga FM, Buczacki SJ, Hernando-Momblona X, Sevillano M, Duran-Frigola M, Aloy P, Selbach M, Winton D, et al. Isolation of human colon stem cells using surface expression of PTK7. Stem Cell Rep. 2015;5(6):979–987. doi:10.1016/j.stemcr.2015.10.003.
   PubMed Web of Science ®Google Scholar
• Beaulieu JF, Vachon PH. Reciprocal expression of laminin A-chain isoforms along the crypt-villus axis in the human small intestine. Gastroenterology. 1994;106(4):829–839. doi:10.1016/0016-5085(94)90740-4.
   PubMed Web of Science ®Google Scholar
• Castro-Herrera VM, Rasmussen C, Wellejus A, Miles EA, Calder PC. In vitro effects of live and heat-inactivated Bifidobacterium animalis subsp. Lactis, BB-12 and lactobacillus rhamnosus GG on Caco-2 cells. Nutrients. 2020;12(6):12. doi:10.3390/nu12061719.
   Web of Science ®Google Scholar
• Friedrich M, Pohin M, Powrie F. Cytokine networks in the pathophysiology of inflammatory bowel disease. Immunity. 2019;50(4):992–1006. doi:10.1016/j.immuni.2019.03.017.
   PubMed Web of Science ®Google Scholar
• Hugenholtz F, de Vos WM. Mouse models for human intestinal microbiota research: a critical evaluation. Cell Mol Life Sci. 2018;75(1):149–160. doi:10.1007/s00018-017-2693-8.
   PubMed Web of Science ®Google Scholar
• Elzinga J, van der Oost J, de Vos WM, Smidt H, de Vos WM. The use of defined microbial communities to model host-microbe interactions in the human gut. Microbiol Mol Biol Rev. 2019;83(2). doi:10.1128/MMBR.00054-18.
   PubMed Web of Science ®Google Scholar
• Hill DR, Huang S, Nagy MS, Yadagiri VK, Fields C, Mukherjee D, Bons B, Dedhia PH, Chin AM, Tsai Y-H, et al. Bacterial colonization stimulates a complex physiological response in the immature human intestinal epithelium. Elife. 2017;6:6. doi:10.7554/eLife.29132.
   Web of Science ®Google Scholar
• Hall AB, Tolonen AC, Xavier RJ. Human genetic variation and the gut microbiome in disease. Nat Rev Genet. 2017;18(11):690–699. doi:10.1038/nrg.2017.63.
   PubMed Web of Science ®Google Scholar
• Vlachogiannis G, Hedayat S, Vatsiou A, Jamin Y, Fernandez-Mateos J, Khan K, Lampis A, Eason K, Huntingford I, Burke R, et al. Patient-derived organoids model treatment response of metastatic gastrointestinal cancers. Sci. 2018;359(6378):920–926. doi:10.1126/science.aao2774.
   PubMed Web of Science ®Google Scholar
• Dekkers JF, Wiegerinck CL, de Jonge HR, Bronsveld I, Janssens HM, de Winter-de Groot KM, Brandsma AM, de Jong NWM, Bijvelds MJC, Scholte BJ, et al. A functional CFTR assay using primary cystic fibrosis intestinal organoids. Nat Med. 2013;19(7):939–945. doi:10.1038/nm.3201.
   PubMed Web of Science ®Google Scholar
• Henrick BM, Rodriguez L, Lakshmikanth T, Pou C, Henckel E, Arzoomand A, Olin A, Wang J, Mikes J, Tan Z, et al. Bifidobacteria-mediated immune system imprinting early in life. Cell. 2021;184(15):3884–98 e11. doi:10.1016/j.cell.2021.05.030.
   PubMed Web of Science ®Google Scholar
• Van den Berge K, Soneson C, Robinson MD, Clement L. stageR: a general stage-wise method for controlling the gene-level false discovery rate in differential expression and differential transcript usage. Genome Biol. 2017;18(1):151. doi:10.1186/s13059-017-1277-0.
   PubMedGoogle Scholar
• Zheng GX, Terry JM, Belgrader P, Ryvkin P, Bent ZW, Wilson R, Ziraldo SB, Wheeler TD, McDermott GP, Zhu J, et al. Massively parallel digital transcriptional profiling of single cells. Nat Commun. 2017;8(1):14049. doi:10.1038/ncomms14049.
   PubMed Web of Science ®Google Scholar
• La Manno G, Soldatov R, Zeisel A, Braun E, Hochgerner H, Petukhov V, Lidschreiber K, Kastriti ME, Lönnerberg P, Furlan A, et al. RNA velocity of single cells. Nature. 2018;560(7719):494–498. doi:10.1038/s41586-018-0414-6.
   PubMed Web of Science ®Google Scholar
• Wolf FA, Angerer P, Theis FJ. SCANPY: large-scale single-cell gene expression data analysis. Genome Biol. 2018;19(1):15. doi:10.1186/s13059-017-1382-0.
   PubMed Web of Science ®Google Scholar
• Bergen V, Lange M, Peidli S, Wolf FA, Theis FJ. Generalizing RNA velocity to transient cell states through dynamical modeling. Nat Biotechnol. 2020;38(12):1408–1414. doi:10.1038/s41587-020-0591-3.
   PubMed Web of Science ®Google Scholar
• McGinnis CS, Murrow LM, Gartner ZJ. DoubletFinder: doublet Detection in single-cell RNA sequencing data using artificial nearest neighbors. Cell Syst. 2019;8(4):329–37 e4. doi:10.1016/j.cels.2019.03.003.
   PubMed Web of Science ®Google Scholar
• Wolock SL, Lopez R, Klein AM. Scrublet: computational identification of cell doublets in single-cell transcriptomic data. Cell Syst. 2019;8(4):281–91 e9. doi:10.1016/j.cels.2018.11.005.
   PubMed Web of Science ®Google Scholar
• Merlos-Suarez A, Barriga FM, Jung P, Iglesias M, Cespedes MV, Rossell D, Sevillano M, Hernando-Momblona X, da Silva-Diz V, Muñoz P, et al. The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell. 2011;8(5):511–524. doi:10.1016/j.stem.2011.02.020.
   PubMed Web of Science ®Google Scholar
• Tirosh I, Izar B, Prakadan SM, Wadsworth MH 2nd, Treacy D, Trombetta JJ, Rotem A, Rodman C, Lian C, Murphy G, et al. Dissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-seq. Sci. 2016;352(6282):189–196. doi:10.1126/science.aad0501.
   PubMed Web of Science ®Google Scholar
• Polanski K, Young MD, Miao Z, Meyer KB, Teichmann SA, Park JE, Berger B. BBKNN: fast batch alignment of single cell transcriptomes. Bioinformatics. 2020;36(3):964–965. doi:10.1093/bioinformatics/btz625.
   PubMed Web of Science ®Google Scholar
• Traag VA, Waltman L, van Eck NJ. From Louvain to Leiden: guaranteeing well-connected communities. Sci Rep. 2019;9(1):5233. doi:10.1038/s41598-019-41695-z.
   PubMed Web of Science ®Google Scholar