Development of a primary human Small Intestine-on-a-Chip using biopsy-derived organoids

Scientific Reports

Volumn 8, Issue 1, 2018, Pages

  Kasendra, Magdalena ^a,j   Tovaglieri, Alessio ^a,b   Sontheimer Phelps, Alexandra ^a,c   Jalili Firoozinezhad, Sasan ^a,d   Bein, Amir ^a   Chalkiadaki, Angeliki ^a   Scholl, William ^a   Zhang, Cheng ^e   Rickner, Hannah ^f   Richmond, Camilla A ^f,g   Li, Hu ^e   Breault, David T ^f,g,h   Ingber, Donald E ^a,f,i  

^a HARVARD UNIVERSITY   (United States)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF FREIBURG   (Germany)

^d INSTITUTO SUPERIOR TÉCNICO   (Portugal)

^e MAYO GRADUATE SCHOOL   (United States)

^f BOSTON CHILDREN S HOSPITAL   (United States)

^g HARVARD MEDICAL SCHOOL   (United States)

^h HARVARD STEM CELL INSTITUTE   (United States)

ⁱ HARVARD UNIVERSITY   (United States)

^j Emulate Inc   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BIOPSY; CELL PROLIFERATION; CYTOLOGY; EPITHELIUM CELL; HUMAN; LAB ON A CHIP; ORGANOID; SMALL INTESTINE;

BIOPSY; CELL PROLIFERATION; EPITHELIAL CELLS; HUMANS; INTESTINE, SMALL; LAB-ON-A-CHIP DEVICES; ORGANOIDS;

EID: 85042054523     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-018-21201-7     Document Type: Article

References (57)

1. Shanks, N., Greek, R. &Greek, J. Are animal models predictive for humans? Philos. Ethics. Humanit. Med. 4, 2 (2009).
2. Sato, T. et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262-5 (2009).
3. Sato, T. et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 141, 1762-72 (2011).
4. Vandussen, K. L. et al. Development of an enhanced human gastrointestinal epithelial culture system to facilitate patient-based assays. https://doi.org/10.1136/gutjnl-2013-306651 (2014).
5. Sasai, Y., Eiraku, M. &Suga, H. In vitro organogenesis in three dimensions: self-organising stem cells. Development 139, 4111-21 (2012).
6. Sato, T. &Clevers, H. Growing self-organizing mini-guts from a single intestinal stem cell: mechanism and applications. Science 340, 1190-4 (2013).
7. Wells, J. M. &Spence, J. R. How to make an intestine. Development 141, 752-60 (2014).
8. Fatehullah, A., Tan, S. H. &Barker, N. Organoids as an in vitro model of human development and disease. Nat. Cell Biol. 18, 246-54 (2016).
9. Bhatia, S. N. &Ingber, D. E. Microfluidic organs-on-chips. Nat. Biotechnol. 32, 760-72 (2014).
10. Ingber, D. E. Reverse Engineering Human Pathophysiology with Organs-on-Chips. Cell 164, 1105-9 (2016).
11. Huh, D. et al. Reconstituting organ-level lung functions on a chip. Science 328, 1662-8 (2010).
12. Baudoin, R., Griscom, L., Monge, M., Legallais, C. &Leclerc, E. Development of a renal microchip for in vitro distal tubule models. Biotechnol. Prog. 23, 1245-53 (2007).
13. Jang, K.-J. et al. Human kidney proximal tubule-on-A-chip for drug transport and nephrotoxicity assessment. Integr. Biol. (Camb) 5, 1119-29 (2013).
14. Leclerc, E., Sakai, Y. &Fujii, T. Microfluidic PDMS (polydimethylsiloxane) bioreactor for large-scale culture of hepatocytes. Biotechnol. Prog. 20, 750-5 (2004).
15. Powers, M. J. et al. A microfabricated array bioreactor for perfused 3D liver culture. Biotechnol. Bioeng. 78, 257-69 (2002).
16. Tilles, A. W., Baskaran, H., Roy, P., Yarmush, M. L. &Toner, M. Effects of oxygenation and flow on the viability and function of rat hepatocytes cocultured in a microchannel flat-plate bioreactor. Biotechnol. Bioeng. 73, 379-89 (2001).
17. Grosberg, A., Alford, P. W., McCain, M. L. &Parker, K. K. Ensembles of engineered cardiac tissues for physiological and pharmacological study: heart on a chip. Lab Chip 11, 4165-73 (2011).
18. Park, J. et al. Three-dimensional brain-on-A-chip with an interstitial level of flow and its application as an in vitro model of Alzheimer's disease. Lab Chip 15, 141-50 (2015).
19. Kim, H. J., Huh, D., Hamilton, G. &Ingber, D. E. Human gut-on-A-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab Chip 12, 2165-74 (2012).
20. Kim, H. J. &Ingber, D. E. Gut-on-A-Chip microenvironment induces human intestinal cells to undergo villus differentiation. Integr. Biol. (Camb). 5, 1130-40 (2013).
21. 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. USA 113, E7-15 (2016).
22. Imura, Y., Asano, Y., Sato, K. &Yoshimura, E. A microfluidic system to evaluate intestinal absorption. Anal. Sci. 25, 1403-7 (2009).
23. Kimura, H., Yamamoto, T., Sakai, H., Sakai, Y. &Fujii, T. An integrated microfluidic system for long-term perfusion culture and on-line monitoring of intestinal tissue models. Lab Chip 8, 741-6 (2008).
24. Shah, P. et al. A microfluidics-based in vitro model of the gastrointestinal human-microbe interface. Nat. Commun. 7, 11535 (2016).
25. Yissachar, N. et al. An Intestinal Organ Culture System Uncovers a Role for the Nervous System in Microbe-Immune Crosstalk. Cell 168, 1135-1148.e12 (2017).
26. Tsilingiri, K., Sonzogni, A., Caprioli, F. &Rescigno, M. A novel method for the culture and polarized stimulation of human intestinal mucosa explants. J. Vis. Exp. e4368 https://doi.org/10.3791/4368 (2013).
27. Sato, T. et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262-265 (2009).
28. Zietek, T., Rath, E., Haller, D. &Daniel, H. Intestinal organoids for assessing nutrient transport, sensing and incretin secretion. Sci. Rep. 5, 16831 (2015).
29. Darwich, A. S., Aslam, U., Ashcroft, D. M. &Rostami-Hodjegan, A. Meta-analysis of the turnover of intestinal epithelia in preclinical animal species and humans. Drug Metab. Dispos. 42, 2016-2022 (2014).
30. Umar, S. I. S. Cells. Curr Gastroenterol Rep 12, 340-348 (2011).
31. Elnasharty, M. A., Abou-Ghanema, I. I., Sayed-Ahmed, A. &Mucosal-Submucosal, A. A. E. Changes in Rabbit Duodenum during Development. In International Journal of Biological, Biomolecular, Agricultural, Food and Biotechnological Engineering 7, 500-508 (2013).
32. Hassan, S. A. &Moussa, E. A. Light and scanning electron microscopy of the small intestine of goat (Capra hircus). J. Cell Anim. Biol. Full 9, 1-8 (2015).
33. Skrzypek, T. et al. Light and scanning electron microscopy evaluation of the postnatal small intestinal mucosa development in pigs. J. Physiol. Pharmacol. 56(Suppl 3), 71-87 (2005).
34. Charney, A. N. &Donowitz, M. Functional significance of intestinal Na +-K+-ATPase: in vivo ouabain inhibition. Am. J. Physiol. 234, E629-36 (1978).
35. Barker, N. et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. 449, (2007).
36. Yan, K. S. et al. The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations. Proc. Natl. Acad. Sci. USA 109, 466-71 (2012).
37. Tappenden, K. A. Pathophysiology of short bowel syndrome: considerations of resected and residual anatomy. JPEN. J. Parenter. Enteral Nutr. 38, 14S-22S (2014).
38. Battle, M. A. et al. GATA4 is essential for jejunal function in mice. Gastroenterology 135, 1676-1686.e1 (2008).
39. Kim, H. J. Human gut-on-A-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab Chip Lab on a Chip. https://doi.org/10.1039/c2lc40074j (2015).
40. Shim, K.-Y. et al. Microfluidic gut-on-A-chip with three-dimensional villi structure. Biomed. Microdevices 19, 37 (2017).
41. Wang, Y. et al. A microengineered collagen scaffold for generating a polarized crypt-villus architecture of human small intestinal epithelium. Biomaterials 128, 44-55 (2017).
42. Valenta, T. et al. Wnt Ligands Secreted by Subepithelial Mesenchymal Cells Are Essential for the Survival of Intestinal Stem Cells and Gut Homeostasis. Cell Rep. 15, 911-918 (2016).
43. Stzepourginski, I. et al. CD34 + mesenchymal cells are a major component of the intestinal stem cells niche at homeostasis and after injury. Proc. Natl. Acad. Sci. USA 114, E506-E513 (2017).
44. Huh, D. et al. A human disease model of drug toxicity-induced pulmonary edema in a lung-on-A-chip microdevice. Sci. Transl. Med. 4, 159ra147 (2012).
45. Workman, M. J. et al. Enhanced utilization of induced pluripotent stem cell-derived human intestinal organoids using microengineered Chips. Cell. Mol. Gastroenterol. Hepatol. https://doi.org/10.1016/j.jcmgh.2017.12.008 (2017).
46. Ferruzza, S., Rossi, C., Scarino, M. L. &Sambuy, Y. A protocol for in situ enzyme assays to assess the differentiation of human intestinal Caco-2 cells. Toxicol. In Vitro 26, 1247-51 (2012).
47. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-82 (2012).
48. Schneider, C. A., Rasband, W. S. &Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-5 (2012).
49. Rueden, C. T. et al. ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinformatics 18, 529 (2017).
50. Piccolo, S. R., Withers, M. R., Francis, O. E., Bild, A. H. &Johnson, W. E. Multiplatform single-sample estimates of transcriptional activation. Proc. Natl. Acad. Sci. USA 110, 17778-83 (2013).
51. Piccolo, S. R. et al. A single-sample microarray normalization method to facilitate personalized-medicine workflows. Genomics 100, 337-44 (2012).
52. Ritchie, M. E. et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015).
53. Pavlidis, P. &Noble, W. S. Analysis of strain and regional variation in gene expression in mouse brain. Genome Biol. 2, RESEARCH0042 (2001).
54. Lance, G. N. &Williams, W. T. Mixed-data classificatory programs. I. Agglomerative Systems. Aust. Comput. J. (1967).
55. Edgar, R., Domrachev, M. &Lash, A. E. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207-10 (2002).
56. Eichler, G. S., Huang, S. &Ingber, D. E. Gene Expression Dynamics Inspector (GEDI): for integrative analysis of expression profiles. Bioinformatics 19, 2321-2 (2003).
57. Barrett, T. et al. NCBI GEO: archive for functional genomics data sets-update. Nucleic Acids Res. 41, D991-5 (2013).