A microengineered collagen scaffold for generating a polarized crypt-villus architecture of human small intestinal epithelium

Biomaterials

Volumn 128, Issue , 2017, Pages 44-55

  Wang, Yuli ^a   Gunasekara, Dulan B ^a   Reed, Mark I ^a   DiSalvo, Matthew ^b   Bultman, Scott J ^c   Sims, Christopher E ^a   Magness, Scott T ^b   Allbritton, Nancy L ^a,b  

^a The University of North Carolina at Chapel Hill   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Crypt; Intestine; Microfabrication; Scaffold; Stem cell; Villus

Indexed keywords

CELL PROLIFERATION; CELLS; COLLAGEN; CYTOLOGY; MICROFABRICATION; PHYSIOLOGICAL MODELS; PHYSIOLOGY; SCAFFOLDS; STEM CELLS; STIFFNESS MATRIX; TISSUE;

CELLULAR COMPARTMENTS; CRYPT; DIFFERENTIATED CELLS; EXTRACELLULAR MATRICES; INTESTINAL EPITHELIUM; INTESTINE; PHYSIOLOGICAL FUNCTIONS; VILLUS;

SCAFFOLDS (BIOLOGY);

COLLAGEN; CROSS LINKING REAGENT; POLYETHYLENE GLYCOL DIMETHACRYLATE HYDROGEL;

ARTICLE; CELL COMPARTMENTALIZATION; CELL MIGRATION; CELL SELF-RENEWAL; CELL STRUCTURE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; INTESTINE CRYPT; PRIORITY JOURNAL; SMALL INTESTINE EPITHELIUM; TISSUE ENGINEERING; TISSUE SCAFFOLD; ANIMAL; CELL DIFFERENTIATION; CELL MOTION; CELL PROLIFERATION; CHEMISTRY; DRUG EFFECTS; INTESTINE MUCOSA; MOUSE; ORGANOID; PHYSIOLOGY; POROSITY; PROCEDURES; RAT; SMALL INTESTINE; TISSUE CULTURE TECHNIQUE;

ANIMALS; CELL COMPARTMENTATION; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; COLLAGEN; CROSS-LINKING REAGENTS; HUMANS; HYDROGEL, POLYETHYLENE GLYCOL DIMETHACRYLATE; INTESTINAL MUCOSA; INTESTINE, SMALL; MICE; ORGANOIDS; POROSITY; RATS; TISSUE CULTURE TECHNIQUES; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 85014819091     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2017.03.005     Document Type: Article

References (76)

1. [1] Volk, N., Lacy, B., Anatomy and physiology of the small bowel. Gastrointest. Endosc. Clin. N. Am. 27 (2017), 1–13.
2. [2] Wang, L., Murthy, S.K., Fowle, W.H., Barabino, G.A., Carrier, R.L., Influence of micro-well biomimetic topography on intestinal epithelial Caco-2 cell phenotype. Biomaterials 30 (2009), 6825–6834.
3. [3] Hall, J.E., Physiology, G., (eds.) Textbook of Medical Physiology, thirteenth ed., 2015, W.B. Saunders, Philadelphia.
4. [4] Pageot, L.P., Perreault, N., Basora, N., Francoeur, C., Magny, P., Beaulieu, J.F., Human cell models to study small intestinal functions: recapitulation of the crypt-villus axis. Microsc. Res. Tech. 49 (2000), 394–406.
5. [5] Sommer, F., Backhed, F., Know your neighbor: microbiota and host epithelial cells interact locally to control intestinal function and physiology. Bioessays 38 (2016), 455–464.
6. [6] von Martels, J.Z., Sadaghian Sadabad, M., Bourgonje, A.R., Blokzijl, T., Dijkstra, G., Faber, K.N., et al. The role of gut microbiota in health and disease: in vitro modeling of host-microbe interactions at the aerobe-anaerobe interphase of the human gut. Anaerobe 44 (April 2017), 3–12.
7. [7] Kaiko, G.E., Ryu, S.H., Koues, O.I., Collins, P.L., Solnica-Krezel, L., Pearce, E.J., et al. The colonic crypt protects stem cells from microbiota-derived metabolites. Cell 165 (2016), 1708–1720.
8. [8] Lynch, S.V., Pedersen, O., The human intestinal microbiome in health and disease. N. Engl. J. Med. 375 (2016), 2369–2379.
9. [9] Yeung, T.M., Chia, L.A., Kosinski, C.M., Kuo, C.J., Regulation of self-renewal and differentiation by the intestinal stem cell niche. Cell Mol. Life Sci. 68 (2011), 2513–2523.
10. [10] Yu, J., Carrier, R.L., March, J.C., Griffith, L.G., Three dimensional human small intestine models for ADME-Tox studies. Drug Discov. Today 19 (2014), 1587–1594.
11. [11] Stelzner, M., Helmrath, M., Dunn, J.C.Y., Henning, S.J., Houchen, C.W., Kuo, C., et al. A nomenclature for intestinal in vitro cultures. Am. J. Physiol. Gastrointest. Liver Physiol., 302, 2012 G1359–G63.
12. [12] Chen, Y., Lin, Y., Davis, K.M., Wang, Q., Rnjak-Kovacina, J., Li, C., et al. Robust bioengineered 3D functional human intestinal epithelium. Sci. Rep., 5, 2015, 13708.
13. [13] Chi, M., Yi, B., Oh, S., Park, D.J., Sung, J.H., Park, S., A microfluidic cell culture device (muFCCD) to culture epithelial cells with physiological and morphological properties that mimic those of the human intestine. Biomed. Microdevices, 17, 2015, 9966.
14. [14] 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 (2012), 2165–2174.
15. [15] Kim, H.J., Ingber, D.E., Gut-on-a-Chip microenvironment induces human intestinal cells to undergo villus differentiation. Integr. Biol. (Camb) 5 (2013), 1130–1140.
16. [16] Kim, S.H., Chi, M., Yi, B., Kim, S.H., Oh, S., Kim, Y., et al. Three-dimensional intestinal villi epithelium enhances protection of human intestinal cells from bacterial infection by inducing mucin expression. Integr. Biol. (Camb) 6 (2014), 1122–1131.
17. [17] Kim, S.H., Lee, J.W., Choi, I., Kim, Y.C., Lee, J.B., Sung, J.H., A microfluidic device with 3-d hydrogel villi scaffold to simulate intestinal absorption. J. Nanosci. Nanotechnol. 13 (2013), 7220–7228.
18. [18] Kimura, H., Ikeda, T., Nakayama, H., Sakai, Y., Fujii, T., An on-chip small intestine-liver model for pharmacokinetic studies. J. Lab. Autom. 20 (2015), 265–273.
19. [19] Koppes, A.N., Kamath, M., Pfluger, C.A., Burkey, D.D., Dokmeci, M., Wang, L., et al. Complex, multi-scale small intestinal topography replicated in cellular growth substrates fabricated via chemical vapor deposition of Parylene C. Biofabrication, 8, 2016, 035011.
20. [20] Pusch, J., Votteler, M., Gohler, S., Engl, J., Hampel, M., Walles, H., et al. The physiological performance of a three-dimensional model that mimics the microenvironment of the small intestine. Biomaterials 32 (2011), 7469–7478.
21. [21] Wang, L., Murthy, S.K., Barabino, G.A., Carrier, R.L., Synergic effects of crypt-like topography and ECM proteins on intestinal cell behavior in collagen based membranes. Biomaterials 31 (2010), 7586–7598.
22. [22] Yu, J., Peng, S., Luo, D., March, J.C., In vitro 3D human small intestinal villous model for drug permeability determination. Biotechnol. Bioeng. 109 (2012), 2173–2178.
23. [23] Esch, M.B., Sung, J.H., Yang, J., Yu, C., Yu, J., March, J.C., et al. On chip porous polymer membranes for integration of gastrointestinal tract epithelium with microfluidic ‘body-on-a-chip’ devices. Biomed. Microdevices 14 (2012), 895–906.
24. [24] 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 (2008), 741–746.
25. [25] Mahler, G.J., Esch, M.B., Glahn, R.P., Shuler, M.L., Characterization of a gastrointestinal tract microscale cell culture analog used to predict drug toxicity. Biotechnol. Bioeng. 104 (2009), 193–205.
26. [26] Ramadan, Q., Jafarpoorchekab, H., Huang, C., Silacci, P., Carrara, S., Koklu, G., et al. NutriChip: nutrition analysis meets microfluidics. Lab. Chip 13 (2013), 196–203.
27. [27] Artursson, P., Palm, K., Luthman, K., Caco-2 monolayers in experimental and theoretical predictions of drug transport. Adv. Drug Deliv. Rev. 46 (2001), 27–43.
28. [28] Larregieu, C.A., Benet, L.Z., Drug discovery and regulatory considerations for improving in silico and in vitro predictions that use Caco-2 as a surrogate for human intestinal permeability measurements. AAPS J. 15 (2013), 483–497.
29. [29] Hidalgo, I.J., Raub, T.J., Borchardt, R.T., Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability. Gastroenterology 96 (1989), 736–749.
30. [30] Sun, D., Lennernas, H., Welage, L.S., Barnett, J.L., Landowski, C.P., Foster, D., et al. Comparison of human duodenum and Caco-2 gene expression profiles for 12,000 gene sequences tags and correlation with permeability of 26 drugs. Pharm. Res. 19 (2002), 1400–1416.
31. [31] Maschmeyer, I., Hasenberg, T., Jaenicke, A., Lindner, M., Lorenz, A.K., Zech, J., et al. Chip-based human liver-intestine and liver-skin co-cultures–A first step toward systemic repeated dose substance testing in vitro. Eur. J. Pharm. Biopharm. 95 (2015), 77–87.
32. [32] Maschmeyer, I., Lorenz, A.K., Schimek, K., Hasenberg, T., Ramme, A.P., Hubner, J., et al. A four-organ-chip for interconnected long-term co-culture of human intestine, liver, skin and kidney equivalents. Lab. Chip 15 (2015), 2688–2699.
33. [33] Schweinlin, M., Wilhelm, S., Schwedhelm, I., Hansmann, J., Rietscher, R., Jurowich, C., et al. Development of an advanced primary human in vitro model of the small intestine. Tissue Eng. Part C Methods 22 (2016), 873–883.
34. [34] Mahla, R.S., Stem cells applications in regenerative medicine and disease therapeutics. Int. J. Cell Biol., 2016, 2016, 6940283.
35. [35] Miyoshi, H., Stappenbeck, T.S., In vitro expansion and genetic modification of gastrointestinal stem cells in spheroid culture. Nat. Protoc. 8 (2013), 2471–2482.
36. [36] Merker, S.R., Weitz, J., Stange, D.E., Gastrointestinal organoids: how they gut it out. Dev. Biol. 420 (2016), 239–250.
37. [37] In, J.G., Foulke-Abel, J., Estes, M.K., Zachos, N.C., Kovbasnjuk, O., Donowitz, M., Human mini-guts: new insights into intestinal physiology and host-pathogen interactions. Nat. Rev. Gastroenterol. Hepatol. 13 (2016), 633–642.
38. [38] Zachos, N.C., Kovbasnjuk, O., Foulke-Abel, J., In, J., Blutt, S.E., de Jonge, H.R., et al. Human enteroids/colonoids and intestinal organoids functionally recapitulate normal intestinal physiology and pathophysiology. J. Biol. Chem. 291 (2016), 3759–3766.
39. [39] Sato, T., Vries, R.G., Snippert, H.J., van de Wetering, M., Barker, N., Stange, D.E., et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature, 459, 2009 262–U147.
40. [40] Bhatia, S.N., Ingber, D.E., Microfluidic organs-on-chips. Nat. Biotechnol. 32 (2014), 760–772.
41. [41] Lancaster, M.A., Knoblich, J.A., Organogenesis in a dish: modeling development and disease using organoid technologies. Science, 345, 2014, 1247125.
42. [42] van de Wetering, M., Francies, H.E., Francis, J.M., Bounova, G., Iorio, F., Pronk, A., et al. Prospective derivation of a living organoid biobank of colorectal cancer patients. Cell 161 (2015), 933–945.
43. [43] Sato, T., Stange, D.E., Ferrante, M., Vries, R.G.J., van Es, J.H., van den Brink, S., et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 141 (2011), 1762–1772.
44. [44] Yin, X.L., Farin, H.F., van Es, J.H., Clevers, H., Langer, R., Karp, J.M., Niche-independent high-purity cultures of Lgr5(+) intestinal stem cells and their progeny. Nat. Methods 11 (2014), 106–112.
45. [45] Liu, Y.W., Gan, L.H., Carlsson, D.J., Fagerholm, P., Lagali, N., Watsky, M.A., et al. A simple, cross-linked collagen tissue substitute for corneal implantation. Invest. Ophthalmol. Vis. Sci. 47 (2006), 1869–1875.
46. [46] Engler, A.J., Rehfeldt, F., Sen, S., Discher, D.E., Microtissue elasticity: measurements by atomic force microscopy and its influence on cell differentiation. Wang, Y.L., Discher, D.E., (eds.) Cell Mechanics, 2007, 521–545.
47. [47] Pai, J.H., Wang, Y., Salazar, G.T., Sims, C.E., Bachman, M., Li, G.P., et al. Photoresist with low fluorescence for bioanalytical applications. Anal. Chem. 79 (2007), 8774–8780.
48. [48] Hu, S.W., Ren, X.Q., Bachman, M., Sims, C.E., Li, G.P., Allbritton, N., Surface modification of poly(dimethylsiloxane) microfluidic devices by ultraviolet polymer grafting. Anal. Chem. 74 (2002), 4117–4123.
49. [49] Yang, C.R., Enhanced physicochemical properties of collagen by using EDC/NHS-crosslinking. Bull. Mat. Sci. 35 (2012), 913–918.
50. [50] Vrana, N.E., Builles, N., Kocak, H., Gulay, P., Justin, V., Malbouyres, A., et al. EDC/NHS cross-linked collagen foams as scaffolds for artificial corneal stroma. J. Biomater. Sci. Polym. Ed. 18 (2007), 1527–1545.
51. [51] Schuijers, J., van der Flier, L.G., van Es, J., Clevers, H., Robust cre-mediated recombination in small intestinal stem cells utilizing the Olfm4 locus. Stem Cell Rep. 3 (2014), 234–241.
52. [52] Van der Flier, L.G., Haegebarth, A., Stange, D.E., Van de Wetering, M., Clevers, H., OLFM4 is a robust marker for stem cells in human intestine and marks a subset of colorectal cancer cells. Gastroenterology 137 (2009), 15–17.
53. [53] Szpak, P., Fish bone chemistry and ultrastructure: implications for taphonomy and stable isotope analysis. J. Archaeol. Sci. 38 (2011), 3358–3372.
54. [54] Louvard, D., Kedinger, M., Hauri, H.P., The differentiating intestinal epithelial cell: establishment and maintenance of functions through interactions between cellular structures. Annu. Rev. Cell Biol. 8 (1992), 157–195.
55. [55] Beaulieu, J.F., Differential expression of the VLA family of integrins along the crypt-villus axis in the human small intestine. J. Cell Sci. 102 (1992), 427–436.
56. [56] Atuma, C., Strugala, V., Allen, A., Holm, L., The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. Am. J. Physiol. Gastrointest. Liver Physiol., 280, 2001 G922–G9.
57. [57] Ulluwishewa, D., Anderson, R.C., McNabb, W.C., Moughan, P.J., Wells, J.M., Roy, N.C., Regulation of tight junction permeability by intestinal bacteria and dietary components. J. Nutr. 141 (2011), 769–776.
58. [58] VanDussen, K.L., Carulli, A.J., Keeley, T.M., Patel, S.R., Puthoff, B.J., Magness, S.T., et al. Notch signaling modulates proliferation and differentiation of intestinal crypt base columnar stem cells. Development 139 (2012), 488–497.
59. [59] Olsauskas-Kuprys, R., Zlobin, A., Osipo, C., Gamma secretase inhibitors of Notch signaling. Oncotargets Ther. 6 (2013), 943–955.
60. [60] van Es, J.H., van Gijn, M.E., Riccio, O., van den Born, M., Vooijs, M., Begthel, H., et al. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435 (2005), 959–963.
61. [61] Cayo, M.A., Cayo, A.K., Jarjour, S.M., Chen, H., Sodium butyrate activates Notch1 signaling, reduces tumor markers, and induces cell cycle arrest and apoptosis in pheochromocytoma. Am. J. Transl. Res. 1 (2009), 178–183.
62. [62] Davie, J.R., Inhibition of histone deacetylase activity by butyrate. J. Nutr., 133, 2003 2485S–93S.
63. [63] Benjamin, J., Makharia, G., Ahuja, V., Rajan, K.D.A., Kalaivani, M., Gupta, S.D., et al. Glutamine and whey protein improve intestinal permeability and morphology in patients with Crohn's disease: a randomized controlled trial. Dig. Dis. Sci. 57 (2012), 1000–1012.
64. [64] Attayek, P.J., Ahmad, A.A., Wang, Y., Williamson, I., Sims, C.E., Magness, S.T., et al. In vitro polarization of colonoids to create an intestinal stem cell compartment. PLoS One, 11, 2016, e0153795.
65. [65] Heath, J.P., Epithelial cell migration in the intestine. Cell Biol. Int. 20 (1996), 139–146.
66. [66] Moutairou, K., Fritsch, P., Meslin, J.C., Poncy, J.L., Metivier, H., Masse, R., Epithelial cell migration on small intestinal villi in the neonatal rat. Comparison between [3H] thymidine and cytoplasmic labelling after Pu-citrate ingestion. Biol. Cell. 65 (1989), 265–269.
67. [67] Lai, Y.Z., Asthana, A., Kisaalita, W.S., Biomarkers for simplifying HTS 3D cell culture platforms for drug discovery: the case for cytokines. Drug Discov. Today 16 (2011), 293–297.
68. [68] Wypych, G., Handbook of Polymers. 2012, Toronto ChemTec Publishing.
69. [69] Fuard, D., Tzvetkova-Chevolleau, T., Decossas, S., Tracqui, P., Schiavone, P., Optimization of poly-di-methyl-siloxane (PDMS) substrates for studying cellular adhesion and motility. Microelectron. Eng. 85 (2008), 1289–1293.
70. [70] 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. U. S. A. 113 (2016), E7–E15.
71. [71] Costello, C.M., Jia, H.P., Shaffiey, S., Yu, J.J., Jain, N.K., Hackam, D., et al. Synthetic small intestinal scaffolds for improved studies of intestinal differentiation. Biotechnol. Bioeng. 111 (2014), 1222–1232.
72. [72] Shaffiey, S.A., Jia, H.P., Keane, T., Costello, C., Wasserman, D., Quidgley, M., et al. Intestinal stem cell growth and differentiation on a tubular scaffold with evaluation in small and large animals. Regen. Med. 11 (2016), 45–61.
73. [73] Jabaji, Z., Sears, C.M., Brinkley, G.J., Lei, N.Y., Joshi, V.S., Wang, J., et al. Use of collagen gel as an alternative extracellular matrix for the in vitro and in vivo growth of murine small intestinal epithelium. Tissue Eng. Part C Methods 19 (2013), 961–969.
74. [74] Jabaji, Z., Brinkley, G.J., Khalil, H.A., Sears, C.M., Lei, N.Y., Lewis, M., et al. Type I collagen as an extracellular matrix for the in vitro growth of human small intestinal epithelium. PLoS One, 2014, 9.
75. [75] DuFort, C.C., Paszek, M.J., Weaver, V.M., Balancing forces: architectural control of mechanotransduction. Nat. Rev. Mol. Cell Biol. 12 (2011), 308–319.
76. [76] Sung, J.H., Yu, J.J., Luo, D., Shuler, M.L., March, J.C., Microscale 3-D hydrogel scaffold for biomimetic gastrointestinal (GI) tract model. Lab a Chip 11 (2011), 389–392.