Coculture of primary human colon monolayer with human gut bacteria

Jianbo Zhang, Victor Hernandez-Gordillo, Martin Trapecar, Charles Wright, Mao Taketani, Kirsten Schneider, Wen Li Kelly Chen, Eric Stas, David T. Breault, Rebecca L. Carrier, Christopher A. Voigt, Linda G. Griffith

Published: 2021-06-27 DOI: 10.1038/s41596-021-00562-w

Coculture

Human colon monolayer

Gut bacteria

Microenvironment

Intestinal barrier

AI 解读

Supplementary information

Supplementary Information

Supplementary Fig. 1.

Supplementary Table 1

Growth curve of B. thetaiotaomicron MT768

Supplementary Table 2

Calculation of RPUL from OD600 and luminescence data. Related to Fig. 7e

Supplementary Table 3

The OD600 and luminescence signal for bacterial cells collected from top and bottom of the apical compartment in the transwell inserts

Efficient and safe single-cell cloning of human pluripotent stem cells using the CEPT cocktail

Profiling native pulmonary basement membrane stiffness using atomic force microscopy

Genetic circuit design automation with Cello 2.0

Synthesis of siRNA nanoparticles to silence plaque-destabilizing gene in atherosclerotic lesional macrophages

Scalable dual-omics profiling with single-nucleus chromatin accessibility and mRNA expression sequencing 2 (SNARE-seq2)

A practical guide to scanning light-field microscopy with digital adaptive optics

Effective high-throughput isolation of fully human antibodies targeting infectious pathogens

Improved sampling and DNA extraction procedures for microbiome analysis in food-processing environments

MOF-derived nanoporous carbons with diverse tunable nanoarchitectures

Tutorial: a statistical genetics guide to identifying HLA alleles driving complex disease

查看全部

Sections

Figures

References

Supplementary information

Molly, K., Vande Woestyne, M. & Verstraete, W. Development of a 5-step multi-chamber reactor as a simulation of the human intestinal microbial ecosystem. Appl. Microbiol. Biotechnol. 39, 254–258 (1993).
Venema, K. & van den Abbeele, P. Experimental models of the gut microbiome. Best Pract. Res. Clin. Gastroenterol. 27, 115–126 (2013).
Molly, K., Woestyne, M. V., Smet, I. D. & Verstraete, W. Validation of the Simulator of the Human Intestinal Microbial Ecosystem (SHIME) reactor using microorganism-associated activities. Microb. Ecol. Health Dis. 7, 191–200 (1994).
Cinquin, C., Le Blay, G., Fliss, I. & Lacroix, C. New three-stage in vitro model for infant colonic fermentation with immobilized fecal microbiota. FEMS Microbiol. Ecol. 57, 324–336 (2006).
Trapecar, M., Goropevsek, A., Gorenjak, M., Gradisnik, L. & Slak Rupnik, M. A co-culture model of the developing small intestine offers new insight in the early immunomodulation of enterocytes and macrophages by Lactobacillus spp. through STAT1 and NF-kB p65 trans. PLoS ONE 9, e86297 (2014).
Kim, H. J., Li, H., Collins, J. J. & Ingber, D. E. Contributions of microbiome and mechanical deformation to intestinal bacterial overgrowth and inflammation in a human gut-on-a-chip. Proc. Natl Acad. Sci. 113, E7–E15 (2016).
Kim, H. J. & Ingber, D. E. Gut-on-a-Chip microenvironment induces human intestinal cells to undergo villus differentiation. Integr. Biol. (Camb) 5, 1130–1140 (2013).
Zhou, W. D. et al. Multifunctional bioreactor system for human intestine tissues. ACS Biomater. Sci. Eng. 4, 231–239 (2018).
Park, G. S. et al. Emulating host-microbiome ecosystem of human gastrointestinal tract in vitro. Stem Cell Rev. Rep. 13, 321–334 (2017).
Taketani, M. et al. Genetic circuit design automation for Bacteroides, applied to integrate signals from bile acid and antibiotic sensors. Nat. Biotechnol. 38, 962–969 (2020).
Riglar, D. T. et al. Engineered bacteria can function in the mammalian gut long-term as live diagnostics of inflammation. Nat. Biotechnol. 35, 653–658 (2017).
Kurtz, C. B. et al. An engineered E. coli Nissle improves hyperammonemia and survival in mice and shows dose-dependent exposure in healthy humans. Sci. Transl. Med. 11, eaau7975 (2019).
Isabella, V. M. et al. Development of a synthetic live bacterial therapeutic for the human metabolic disease phenylketonuria. Nat. Biotechnol. 36, 857–864 (2018).
Mimee, M., Tucker, A. C., Voigt, C. A. & Lu, T. K. Programming a human commensal bacterium, Bacteroides thetaiotaomicron, to sense and respond to stimuli in the murine gut microbiota. Cell Syst. 2, 214–214 (2016).
Tropini, C., Earle, K. A., Huang, K. C. & Sonnenburg, J. L. The gut microbiome: connecting spatial organization to function. Cell Host Microbe 21, 433–442 (2017).
Rawls, J. F., Mahowald, M. A., Ley, R. E. & Gordon, J. I. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 127, 423–433 (2006).
Arrieta, M. C., Walter, J. & Finlay, B. B. Human microbiota-associated mice: a model with challenges. Cell Host Microbe 19, 575–578 (2016).
Ulluwishewa, D. et al. Live Faecalibacterium prausnitzii in an apical anaerobic model of the intestinal epithelial barrier. Cell Microbiol. 17, 226–240 (2015).
Shin, W. et al. A robust longitudinal co-culture of obligate anaerobic gut microbiome with human intestinal epithelium in an anoxic-oxic interface-on-a-chip. Front. Bioeng. Biotechnol. 7, 13 (2019).
Fofanova, T. Y. et al. A novel human enteroid-anaerobe co-culture system to study microbial-host interaction under physiological hypoxia. Preprint at bioRxiv http://doi.org/10.1101/555755 (2019).
Shah, P. et al. A microfluidics-based in vitro model of the gastrointestinal human–microbe interface. Nat. Commun. 7, 11535–11535 (2016).
Chen, Y. et al. Robust bioengineered 3D functional human intestinal epithelium. Sci. Rep. 5, 13708 (2015).
Chen, Y., Zhou, W. D., Roh, T., Estes, M. K. & Kaplan, D. L. In vitro enteroid-derived three-dimensional tissue model of human small intestinal epithelium with innate immune responses. PLoS ONE 12, e0187880 (2017).
Jalili-Firoozinezhad, S. et al. A complex human gut microbiome cultured in an anaerobic intestine-on-a-chip. Nat. Biomed. Eng. 3, 520–531 (2019).
Sadabad, M. S. et al. A simple coculture system shows mutualism between anaerobic faecalibacteria and epithelial Caco-2 cells. Sci. Rep. 5, 17906 (2015).
Zhang, J. et al. Primary human colonic mucosal barrier crosstalk with super oxygen-sensitive Faecalibacterium prausnitzii in continuous culture. Med 2, 74–98 (2021).
Kozuka, K. et al. Development and characterization of a human and mouse intestinal epithelial cell monolayer platform. Stem Cell Rep. 9, 1976–1990 (2017).
Bhatt, A. P. et al. Nonsteroidal anti-inflammatory drug-induced leaky gut modeled using polarized monolayers of primary human intestinal epithelial cells. ACS Infect. Dis. 4, 46–52 (2018).
Wilke, et al. in In vitro culture of cryptosporidium parvum using stem cell-derived intestinal epithelial monolayers (eds Mead, J. R. & Arrowood, M. J.) Ch. 20, 351–372 (Springer, 2020).
Madden, L. R. et al. Bioprinted 3D primary human intestinal tissues model aspects of native physiology and ADME/Tox functions. iScience 2, 156–167 (2018).
Freire, R. et al. Human gut derived-organoids provide model to study gluten response and effects of microbiota-derived molecules in celiac disease. Sci Rep. 9, 7029 (2019).
Wang, Y. et al. Self-renewing monolayer of primary colonic or rectal epithelial cells. Cell Mol. Gastroenterol. Hepatol. 4, 165–182 e167 (2017).
Hubatsch, I., Ragnarsson, E. G. & Artursson, P. Determination of drug permeability and prediction of drug absorption in Caco-2 monolayers. Nat. Protoc. 2, 2111–2119 (2007).
Kasendra, M. et al. Development of a primary human Small Intestine-on-a-Chip using biopsy-derived organoids. Sci. Rep. 8, 2871 (2018).
Kasendra, M. et al. Duodenum Intestine-Chip for preclinical drug assessment in a human relevant model. eLife http://doi.org/10.7554/eLife.50135 (2020).
Wang, Y. et al. In vitro generation of mouse colon crypts. ACS Biomater. Sci. Eng. 3, 2502–2513 (2017).
Hinman, S. S., Wang, Y., Kim, R. & Allbritton, N. L. In vitro generation of self-renewing human intestinal epithelia over planar and shaped collagen hydrogels. Nat. Protoc. 16, 352–382 (2021).
Wang, Y. et al. Analysis of interleukin 8 secretion by a stem-cell-derived human-intestinal-epithelial-monolayer platform. Anal. Chem. 90, 11523–11530 (2018).
Zamora, C. Y. et al. Application of a gut-immune co-culture system for the study of N-glycan-dependent host–pathogen interactions of Campylobacter jejuni. Glycobiology 30, 374–381 (2020).
Noel, G. et al. A primary human macrophage-enteroid co-culture model to investigate mucosal gut physiology and host-pathogen interactions. Sci. Rep. 7, 45270 (2017).
Ettayebi, K. et al. Replication of human noroviruses in stem cell–derived human enteroids. Science 353, 1387–1393 (2016).
Costantini, V. et al. Human norovirus replication in human intestinal enteroids as model to evaluate virus inactivation. Emerg. Infect. Dis. 24, 1453–1464 (2018).
Kim, R. et al. An in vitro intestinal platform with a self-sustaining oxygen gradient to study the human gut/microbiome interface. Biofabrication 12, 015006 (2019).
Dutta, D., Heo, I. & Clevers, H. Disease modeling in stem cell-derived 3D organoid systems. Trends Mol. Med. 23, 393–410 (2017).
Hernandez-Gordillo, V. et al. Fully synthetic matrices for in vitro culture of primary human intestinal enteroids and endometrial organoids. Biomaterials http://doi.org/10.1016/j.biomaterials.2020.120125 (2020).
Sato, T. et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262–265 (2009).
Spence, J. R. et al. Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature 470, 105–109 (2011).
McCracken, K. W., Howell, J. C., Wells, J. M. & Spence, J. R. Generating human intestinal tissue from pluripotent stem cells in vitro. Nat. Protoc. 6, 1920–1928 (2011).
Williamson, I. A. et al. A high-throughput organoid microinjection platform to study gastrointestinal microbiota and luminal physiology. Cell Mol. Gastroenterol. Hepatol. 6, 301–319 (2018).
Kester, J. C. et al. Clostridioides difficile–associated antibiotics alter human mucosal barrier functions by microbiome-independent mechanisms. Antimicrob. Agents Chemother. http://doi.org/10.1128/AAC.01404-19 (2020).
In, J. et al. Enterohemorrhagic Escherichia coli reduce mucus and intermicrovillar bridges in human stem cell-derived colonoids. Cell Mol. Gastroenterol. Hepatol. 2, 48–62 e43 (2016).
Trapecar, M. et al. Gut-liver physiomimetics reveal paradoxical modulation of IBD-related inflammation by short-chain fatty acids. Cell Syst. 10, 223–239 (2020).
Ozdemir, T., Fedorec, A. J. H., Danino, T. & Barnes, C. P. Synthetic biology and engineered live biotherapeutics: toward increasing system complexity. Cell Syst. 7, 5–16 (2018).
Murakami, K. et al. Bile acids and ceramide overcome the entry restriction for GII.3 human norovirus replication in human intestinal enteroids. Proc. Natl Acad. Sci. 117, 1700 (2020).
Maier, E., Anderson, R. C., Altermann, E. & Roy, N. C. Live Faecalibacterium prausnitzii induces greater TLR2 and TLR2/6 activation than the dead bacterium in an apical anaerobic co-culture system. Cell. Microbiol. 20, e12805 (2018).
VanDussen, K. L., Sonnek, N. M. & Stappenbeck, T. S. L-WRN conditioned medium for gastrointestinal epithelial stem cell culture shows replicable batch-to-batch activity levels across multiple research teams. Stem Cell Res. 37, 101430 (2019).
Srinivasan, B. et al. TEER measurement techniques for in vitro barrier model systems. J. Lab. Autom. 20, 107–126 (2015).