Development of an advanced primary human in vitro model of the small intestine

Tissue Engineering - Part C: Methods

Volumn 22, Issue 9, 2016, Pages 873-883

  Schweinlin, Matthias ^a   Wilhelm, Sabine ^a   Schwedhelm, Ivo ^a   Hansmann, Jan ^a   Rietscher, Rene ^b   Jurowich, Christian ^a   Walles, Heike ^a,c   Metzger, Marco ^a,c  

^a UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^b SAARLAND UNIVERSITY   (Germany)

^c FRAUNHOFER INSTITUTE FOR INTERFACIAL ENGINEERING AND BIOTECHNOLOGY IGB   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELLS; CYTOLOGY; ENZYME ACTIVITY; FIBROBLASTS; PHYSIOLOGICAL MODELS; TISSUE;

ENTEROENDOCRINE CELLS; EPITHELIAL BARRIER; EPITHELIAL CACO-2 CELLS; EXTRACELLULAR MATRICES; PERFUSION BIOREACTOR; RESEARCH AND DEVELOPMENT; SYNTHETIC MEMBRANES; TRANSPORT ACTIVITY;

SCAFFOLDS (BIOLOGY);

CHROMOGRANIN A; CLAUDIN 4; CYTOCHROME P450 3A4; CYTOKERATIN 18; DNA; MUCIN 1; MUCIN 2; UVOMORULIN;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOREACTOR; CELL DIFFERENTIATION; CELL SUBPOPULATION; COCULTURE; COLLAGEN FIBER; CONTROLLED STUDY; DNA ISOLATION; ENTEROENDOCRINE CELL; EXTRACELLULAR MATRIX; FEMALE; FIBROBLAST; FILTERS AND MEMBRANES; GENE EXPRESSION; GOBLET CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; INTESTINE CRYPT; INTESTINE EPITHELIUM CELL; MALE; NONHUMAN; PIG; PRIMARY CELL; PRIORITY JOURNAL; SHEAR STRESS; SMALL INTESTINAL TISSUE; SMALL INTESTINE MUCOSA; TISSUE ENGINEERING; TISSUE SCAFFOLD; UPREGULATION; BIOLOGICAL MODEL; CYTOLOGY; IN VITRO STUDY; INTESTINE MUCOSA; SMALL INTESTINE; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CELL DIFFERENTIATION; COCULTURE TECHNIQUES; FIBROBLASTS; HUMANS; IN VITRO TECHNIQUES; INTESTINAL MUCOSA; INTESTINE, SMALL; MODELS, BIOLOGICAL;

EID: 84988805128     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2016.0101     Document Type: Article

References (77)

1. VanDussen, K.L., Marinshaw, J.M., Shaikh, N., Miyoshi, H., Moon, C., Tarr, P.I., Ciorba, M.A., and Stappenbeck, T.S. Development of an enhanced human gastrointestinal epithelial culture system to facilitate patient-based assays. Gut 64, 911, 2015
2. Maloy, K.J., and Powrie, F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 474, 298, 2011
3. Sarmento, B., Andrade, F., da Silva, S.B., Rodrigues, F., das Neves, J., and Ferreira, D. Cell-based in vitro models for predicting drug permeability. Expert Opin Drug Metab Toxicol 8, 607, 2012
4. Artursson, P., Palm, K., and Luthman, K. Caco-2 monolayers in experimental and theoretical predictions of drug transport1. Adv Drug Deliv Rev 46, 27, 2001
5. Tran, Q.T., Gomez, G., Khare, S., Lawhon, S.D., Raffatellu, M., Baumler, A.J., Ajithdoss, D., Dhavala, S., and Adams, L.G. The Salmonella enterica serotype Typhi Vi capsular antigen is expressed after the bacterium enters the ileal mucosa. Infect Immun 78, 527, 2010
6. Raffatellu, M., Wilson, R.P., Chessa, D., Andrews-Polymenis, H., Tran, Q.T., Lawhon, S., Khare, S., Adams, L.G., and Baumler, A.J. SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica serotype typhimurium invasion of epithelial cells. Infect Immun 73, 146, 2005
7. Van Breemen, R.B., and Li, Y. Caco-2 cell permeability assays to measure drug absorption. Expert Opin Drug Metab Toxicol 1, 175, 2005
8. Sjöberg, Å ., Lutz, M., Tannergren, C., Wingolf, C., Borde, A., and Ungell, A.-L. Comprehensive study on regional human intestinal permeability and prediction of fraction absorbed of drugs using the Ussing chamber technique. Eur J Pharm Sci 48, 166, 2013
9. Sato, T., Stange, D.E., Ferrante, M., Vries, R.G.J., Van Es, J.H., Van den Brink, S., Van Houdt, W.J., Pronk, A., Van Gorp, J., Siersema, P.D., and Clevers, H. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 141, 1762, 2011
10. 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., and Clevers, H. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262, 2009
11. Pusch, J., Votteler, M., Gohler, S., Engl, J., Hampel, M., Walles, H., and Schenke-Layland, K. The physiological performance of a three-dimensional model that mimics the microenvironment of the small intestine. Biomaterials 32, 7469, 2011
12. Kim, H.J., Huh, D., Hamilton, G., and Ingber, D.E. Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab Chip 12, 2165, 2012
13. Lahar, N., Lei, N.Y., Wang, J., Jabaji, Z., Tung, S.C., Joshi, V., Lewis, M., Stelzner, M., Martiń, M.G., and Dunn, J.C.Y. Intestinal subepithelial myofibroblasts support in vitro and in vivo growth of human small intestinal epithelium. PLoS One 6, e26898, 2011
14. Miyoshi, H., and Stappenbeck, T.S. In vitro expansion and genetic modification of gastrointestinal stem cells in spheroid culture. Nat Protoc 8, 2471, 2013
15. Linke, K., Schanz, J., Hansmann, J., Walles, T., Brunner, H., and Mertsching, H. Engineered liver-like tissue on a capillarized matrix for applied research. Tissue Eng 13, 2699, 2007
16. Schanz, J., Pusch, J., Hansmann, J., and Walles, H. Vascularised human tissue models: a new approach for the refinement of biomedical research. J Biotechnol 148, 56, 2010
17. Milano, J., McKay, J., Dagenais, C., Foster-Brown, L., Pognan, F., Gadient, R., Jacobs, R.T., Zacco, A., Greenberg, B., and Ciaccio, P.J. Modulation of notch processing by g-secretase inhibitors causes intestinal goblet cell metaplasia and induction of genes known to specify gut secretory lineage differentiation. Toxicol Sci 82, 341, 2004
18. Van Es, J.H., Van Gijn, M.E., Riccio, O., Van den Born, M., Vooijs, M., Begthel, H., Cozijnsen, M., Robine, S., Winton, D.J., Radtke, F., and Clevers, H. Notch/[gamma]-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435, 959, 2005
19. Ogaki, S., Shiraki, N., Kume, K., and Kume, S. Wnt and notch signals guide embryonic stem cell differentiation into the intestinal lineages. Stem Cells 31, 1086, 2013
20. Fischer, A.H., Jacobson, K.A., Rose, J., and Zeller, R. Hematoxylin and eosin staining of tissue and cell sections. CSH Protoc 2008, pdb.prot4986, 2008
21. Chatelain, R., Willms, A., Biesterfeld, S., Auffermann, W., and Böcking, A. Automated Feulgen staining with a temperature-controlled staining machine. Anal Quant Cytol Histol 11, 211, 1989
22. Foot, N.C. The Masson trichrome staining methods in routine laboratory use. Stain Technol 8, 101, 1933
23. Burk, O., Arnold, K.A., Nussler, A.K., Schaeffeler, E., Efimova, E., Avery, B.A., Avery, M.A., Fromm, M.F., and Eichelbaum, M. Antimalarial artemisinin drugs induce cytochrome P450 and MDR1 expression by activation of xenosensors pregnane X receptor and constitutive androstane receptor. Mol Pharmacol 67, 1954, 2005
24. Wolbold, R., Klein, K., Burk, O., Nussler, A.K., Neuhaus, P., Eichelbaum, M., Schwab, M., and Zanger, U.M. Sex is a major determinant of CYP3A4 expression in human liver. Hepatology 38, 978, 2003
25. Artursson, P., and Karlsson, J. Correlation between oral drug absorption in humans and apparent drug permeability coefficients in human intestinal epithelial (Caco-2) cells. Biochem Biophys Res Commun 175, 880, 1991
26. Ma, W., Chen, M., Kaushal, S., McElroy, M., Zhang, Y., Ozkan, C., Bouvet, M., Kruse, C., Grotjahn, D., Ichim, T., and Minev, B. PLGA nanoparticle-mediated delivery of tumor antigenic peptides elicits effective immune responses. Int J Nanomed 7, 1475, 2012
27. Yamashita, S., Tanaka, Y., Endoh, Y., Taki, Y., Sakane, T., Nadai, T., and Sezaki, H. Analysis of drug permeation across Caco-2 monolayer: implication for predicting in vivo drug absorption. Pharm Res 14, 486, 1997
28. Rubas, W., Cromwell, M.E., Shahrokh, Z., Villagran, J., Nguyen, T.N., Wellton, M., Nguyen, T.H., and Mrsny, R.J. Flux measurements across Caco-2 monolayers may predict transport in human large intestinal tissue. J Pharm Sci 85, 165, 1996
29. Balimane, P.V., and Chong, S. Cell culture-based models for intestinal permeability: a critique. Drug Discov Today 10, 335, 2005
30. Mizutani, T., Nakamura, T., Morikawa, R., Fukuda, M., Mochizuki, W., Yamauchi, Y., Nozaki, K., Yui, S., Nemoto, Y., Nagaishi, T., Okamoto, R., Tsuchiya, K., and Watanabe, M. Real-time analysis of P-glycoprotein-mediated drug transport across primary intestinal epithelium threedimensionally cultured in vitro. Biochem Biophys Res Commun 419, 238, 2012
31. Bartfeld, S., and Clevers, H. Organoids as model for infectious diseases: culture of human and murine stomach organoids and microinjection of Helicobacter Pylori. J Vis Exp November 12, 2015. DOI: 10.3791/53359
32. Takenaka, T., Harada, N., Kuze, J., Chiba, M., Iwao, T., and Matsunaga, T. Human small intestinal epithelial cells differentiated from adult intestinal stem cells as a novel system for predicting oral drug absorption in humans. Drug Metab Dispos 42, 1947, 2014
33. Yamaura, Y., Chapron, B.D., Wang, Z., Himmelfarb, J., and Thummel, K.E. Functional comparison of human colonic carcinoma cell lines and primary small intestinal epithelial cells for investigations of intestinal drug permeability and first-pass metabolism. Drug Metab Dispos 44, 329, 2016
34. Kauffman, A.L., Gyurdieva, A.V., Mabus, J.R., Ferguson, C., Yan, Z., and Hornby, P.J. Alternative functional in vitro models of human intestinal epithelia. Front Pharmacol 4, 79, 2013
35. Roger, E., Kalscheuer, S., Kirtane, A., Guru, B.R., Grill, A.E., Whittum-Hudson, J., and Panyam, J. Folic acidfunctionalized nanoparticles for enhanced oral drug delivery. Mol Pharm 9, 2103, 2012
36. Brito Baleeiro, R., Schweinlin, M., Rietscher, R., Diedrich, A., Czaplewska, J.A., Metzger, M., Michael Lehr, C., Scherließ, R., Hanefeld, A., Gottschaldt, M., and Walden, P. Nanoparticle-based mucosal vaccines targeting tumorassociated antigens to human dendritic cells. J Biomed Nanotechnol 12, 1527, 2016
37. 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., and Clevers, H. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262, 2009
38. Pusch, J., Votteler, M., Gohler, S., Engl, J., Hampel, M., Walles, H., and Schenke-Layland, K. The physiological performance of a three-dimensional model that mimics the microenvironment of the small intestine. Biomaterials 32, 7469, 2011
39. Kim, H.J., Huh, D., Hamilton, G., and Ingber, D.E. Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab Chip 12, 2165, 2012
40. Lahar, N., Lei, N.Y., Wang, J., Jabaji, Z., Tung, S.C., Joshi, V., Lewis, M., Stelzner, M., Martiń, M.G., and Dunn, J.C.Y. Intestinal subepithelial myofibroblasts support in vitro and in vivo growth of human small intestinal epithelium. PLoS One 6, e26898, 2011
41. Miyoshi, H., and Stappenbeck, T.S. In vitro expansion and genetic modification of gastrointestinal stem cells in spheroid culture. Nat Protoc 8, 2471, 2013
42. Linke, K., Schanz, J., Hansmann, J., Walles, T., Brunner, H., and Mertsching, H. Engineered liver-like tissue on a capillarized matrix for applied research. Tissue Eng 13, 2699, 2007
43. Schanz, J., Pusch, J., Hansmann, J., and Walles, H. Vascularised human tissue models: a new approach for the refinement of biomedical research. J Biotechnol 148, 56, 2010
44. Milano, J., McKay, J., Dagenais, C., Foster-Brown, L., Pognan, F., Gadient, R., Jacobs, R.T., Zacco, A., Greenberg, B., and Ciaccio, P.J. Modulation of notch processing by g-secretase inhibitors causes intestinal goblet cell metaplasia and induction of genes known to specify gut secretory lineage differentiation. Toxicol Sci 82, 341, 2004
45. Van Es, J.H., Van Gijn, M.E., Riccio, O., Van den Born, M., Vooijs, M., Begthel, H., Cozijnsen, M., Robine, S., Winton, D.J., Radtke, F., and Clevers, H. Notch/[gamma]-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435, 959, 2005
46. Ogaki, S., Shiraki, N., Kume, K., and Kume, S. Wnt and notch signals guide embryonic stem cell differentiation into the intestinal lineages. Stem Cells 31, 1086, 2013
47. Fischer, A.H., Jacobson, K.A., Rose, J., and Zeller, R. Hematoxylin and eosin staining of tissue and cell sections. CSH Protoc 2008, pdb.prot4986, 2008
48. Chatelain, R., Willms, A., Biesterfeld, S., Auffermann, W., and Böcking, A. Automated Feulgen staining with a temperature-controlled staining machine. Anal Quant Cytol Histol 11, 211, 1989
49. Foot, N.C. The Masson trichrome staining methods in routine laboratory use. Stain Technol 8, 101, 1933
50. Burk, O., Arnold, K.A., Nussler, A.K., Schaeffeler, E., Efimova, E., Avery, B.A., Avery, M.A., Fromm, M.F., and Eichelbaum, M. Antimalarial artemisinin drugs induce cytochrome P450 and MDR1 expression by activation of xenosensors pregnane X receptor and constitutive androstane receptor. Mol Pharmacol 67, 1954, 2005
51. Wolbold, R., Klein, K., Burk, O., Nussler, A.K., Neuhaus, P., Eichelbaum, M., Schwab, M., and Zanger, U.M. Sex is a major determinant of CYP3A4 expression in human liver. Hepatology 38, 978, 2003
52. Artursson, P., and Karlsson, J. Correlation between oral drug absorption in humans and apparent drug permeability coefficients in human intestinal epithelial (Caco-2) cells. Biochem Biophys Res Commun 175, 880, 1991
53. Ma, W., Chen, M., Kaushal, S., McElroy, M., Zhang, Y., Ozkan, C., Bouvet, M., Kruse, C., Grotjahn, D., Ichim, T., and Minev, B. PLGA nanoparticle-mediated delivery of tumor antigenic peptides elicits effective immune responses. Int J Nanomed 7, 1475, 2012
54. Yamashita, S., Tanaka, Y., Endoh, Y., Taki, Y., Sakane, T., Nadai, T., and Sezaki, H. Analysis of drug permeation across Caco-2 monolayer: implication for predicting in vivo drug absorption. Pharm Res 14, 486, 1997
55. Rubas, W., Cromwell, M.E., Shahrokh, Z., Villagran, J., Nguyen, T.N., Wellton, M., Nguyen, T.H., and Mrsny, R.J. Flux measurements across Caco-2 monolayers may predict transport in human large intestinal tissue. J Pharm Sci 85, 165, 1996
56. Balimane, P.V., and Chong, S. Cell culture-based models for intestinal permeability: a critique. Drug Discov Today 10, 335, 2005
57. Mizutani, T., Nakamura, T., Morikawa, R., Fukuda, M., Mochizuki, W., Yamauchi, Y., Nozaki, K., Yui, S., Nemoto, Y., Nagaishi, T., Okamoto, R., Tsuchiya, K., and Watanabe, M. Real-time analysis of P-glycoprotein-mediated drug transport across primary intestinal epithelium threedimensionally cultured in vitro. Biochem Biophys Res Commun 419, 238, 2012
58. Bartfeld, S., and Clevers, H. Organoids as model for infectious diseases: culture of human and murine stomach organoids and microinjection of Helicobacter Pylori. J Vis Exp November 12, 2015. DOI: 10.3791/53359
59. Takenaka, T., Harada, N., Kuze, J., Chiba, M., Iwao, T., and Matsunaga, T. Human small intestinal epithelial cells differentiated from adult intestinal stem cells as a novel system for predicting oral drug absorption in humans. Drug Metab Dispos 42, 1947, 2014
60. Yamaura, Y., Chapron, B.D., Wang, Z., Himmelfarb, J., and Thummel, K.E. Functional comparison of human colonic carcinoma cell lines and primary small intestinal epithelial cells for investigations of intestinal drug permeability and first-pass metabolism. Drug Metab Dispos 44, 329, 2016
61. Kauffman, A.L., Gyurdieva, A.V., Mabus, J.R., Ferguson, C., Yan, Z., and Hornby, P.J. Alternative functional in vitro models of human intestinal epithelia. Front Pharmacol 4, 79, 2013
62. Roger, E., Kalscheuer, S., Kirtane, A., Guru, B.R., Grill, A.E., Whittum-Hudson, J., and Panyam, J. Folic acidfunctionalized nanoparticles for enhanced oral drug delivery. Mol Pharm 9, 2103, 2012
63. Brito Baleeiro, R., Schweinlin, M., Rietscher, R., Diedrich, A., Czaplewska, J.A., Metzger, M., Michael Lehr, C., Scherließ, R., Hanefeld, A., Gottschaldt, M., and Walden, P. Nanoparticle-based mucosal vaccines targeting tumorassociated antigens to human dendritic cells. J Biomed Nanotechnol 12, 1527, 2016
64. Desai, M.P., Labhasetwar, V., Walter, E., Levy, R.J., and Amidon, G.L. The mechanism of uptake of biodegradable microparticles in Caco-2 cells is size dependent. Pharm Res 14, 1568, 1997
65. Panyam, J., Sahoo, S.K., Prabha, S., Bargar, T., and Labhasetwar, V. Fluorescence and electron microscopy probes for cellular and tissue uptake of poly(D, L-lactide-coglycolide) nanoparticles. Int J Pharm 262, 1, 2003
66. Mertsching, H., Schanz, J., Steger, V., Schandar, M., Schenk, M., Hansmann, J., Dally, I., Friedel, G., and Walles, T. Generation and transplantation of an autologous vascularized bioartificial human tissue. Transplantation 88, 203, 2009
67. Shi, L., and Ronfard, V. Biochemical and biomechanical characterization of porcine small intestinal submucosa (SIS): a mini review. Int J Burns Trauma 3, 173, 2013
68. Schuijers, J., Junker, Jan P., Mokry, M., Hatzis, P., Koo, B.-K., Sasselli, V., Van DerFlier, Laurens G., Cuppen, E., Van Oudenaarden, A., and Clevers, H. Ascl2 acts as an Rspondin/Wnt-responsive switch to control stemness in intestinal crypts. Cell Stem Cell 16, 158, 2015
69. Muendoerfer, M., Schaefer, U.F., Koenig, P., Walk, J.S., Loos, P., Balbach, S., Eichinger, T., and Lehr, C.-M. Online monitoring of transepithelial electrical resistance (TEER) in an apparatus for combined dissolution and permeation testing. Int J Pharm 392, 134, 2010
70. Shahin, K., and Doran, P. Shear and compression bioreactor for cartilage synthesis. In: Doran P.M., ed. Cartilage Tissue Engineering. New York: Springer, 2015, p. 221
71. Rebelo, S.P., Costa, R., Silva, M.M., Marcelino, P., Brito, C., and Alves, P.M. Three-dimensional co-culture of human hepatocytes and mesenchymal stem cells: improved functionality in long-term bioreactor cultures. J Tissue Eng Regen Med 2015. [Epub ahead of print]. DOI: 10.1002/term.2099
72. Jeong, S.I., Kwon, J.H., Lim, J.I., Cho, S.-W., Jung, Y., Sung, W.J., Kim, S.H., Kim, Y.H., Lee, Y.M., Kim, B.-S., Choi, C.Y., and Kim, S.-J. Mechano-active tissue engineering of vascular smooth muscle using pulsatile perfusion bioreactors and elastic PLCL scaffolds. Biomaterials 26, 1405, 2005
73. Paine, M.F., Hart, H.L., Ludington, S.S., Haining, R.L., Rettie, A.E., and Zeldin, D.C. The human intestinal cytochrome P450 pie. Drug Metab Dispos 34, 880, 2006
74. Berginc, K., Zakelj, S., Levstik, L., Ursic, D., and Kristl, A. Fluorescein transport properties across artificial lipid membranes, Caco-2 cell monolayers and rat jejunum. Eur J Pharm Biopharm 66, 281, 2007
75. Bock, U., Flototto, T., and Haltner, E. Validation of cell culture models for the intestine and the blood-brain barrier and comparison of drug permeation. Altex 21 Suppl 3, 57, 2004
76. Kratz, J.M., Teixeira, M.R., Koester, L.S., and Simões, C.M.O. An HPLC-UV method for the measurement of permeability of marker drugs in the Caco-2 cell assay. Braz J Med Biol Res 44, 531, 2011
77. McGuckin, M.A., Lindén, S.K., Sutton, P., and Florin, T.H. Mucin dynamics and enteric pathogens. Nat Rev Micro 9, 265, 2011