Synthetic small intestinal scaffolds for improved studies of intestinal differentiation

Biotechnology and Bioengineering

Volumn 111, Issue 6, 2014, Pages 1222-1232

  Costello, Cait M ^a   Hongpeng, Jia ^b   Shaffiey, Shahab ^b   Yu, Jiajie ^a   Jain, Nina K ^a   Hackam, David ^b   March, John C ^a  

^a Department of Biological and Environmental Engineering   (United States)

^b CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

Caco 2; Cadherin; Egf; Ht29; Lysozyme; Muc 2

Indexed keywords

CELL CULTURE; CELLS; ENZYMES; THREE DIMENSIONAL; TISSUE;

CACO-2; CADHERIN; EGF; HT29; MUC-2;

SCAFFOLDS (BIOLOGY);

TISSUE SCAFFOLD;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CACO 2 CELL LINE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SIZE; CELL STRUCTURE; CELL SURFACE; CELL TYPE; CONTROLLED STUDY; EPITHELIUM CELL; HT 29 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; INTESTINE CELL; INTESTINE CRYPT; INTESTINE EPITHELIUM; INTESTINE VILLUS; MICROENVIRONMENT; MOUSE; MUCUS; NONHUMAN; SMALL INTESTINE; COCULTURE; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; PROCEDURES; TISSUE SCAFFOLD;

MUS;

CACO-2 CELLS; COCULTURE TECHNIQUES; EPITHELIAL CELLS; HT29 CELLS; HUMANS; INTESTINE, SMALL; ORGAN CULTURE TECHNIQUES; TISSUE SCAFFOLDS;

EID: 84899628700     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.25180     Document Type: Article

References (77)

1. Andersson AS, Brink J, Lidberg U, Sutherland DS. 2003. Influence of systematically varied nanoscale topography on the morphology of epithelial cells. IEEE Trans Nanobiosci 2(2):49-57.
2. Anselme K, Bigerelle M. 2011. Role of materials surface topography on mammalian cell response. Int Mater Rev 56(4):243-266.
3. Atreya R, Mudter J, Finotto S, Mullberg J, Jostock T, Wirtz S, Schutz M, Bartsch B, Holtmann M, Becker C, Strand D, Czaja J, Schlaak JF, Lehr HA, Autschbach F, Schurmann G, Nishimoto N, Yoshizaki K, Ito H, Kishimoto T, Galle PR, Rose-John S, Neurath MF. 2000. Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: Evidence in Crohn disease and experimental colitis in vivo. Nat Med 6(5):583-588.
4. Ayabe T, Satchell DP, Pesendorfer P, Tanabe H, Wilson CL, Hagen SJ, Ouellette AJ. 2002. Activation of Paneth cell alpha-defensins in mouse small intestine. J Biol Chem 277(7):5219-5228.
5. Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, Ouellette AJ. 2000. Secretion of microbicidal alpha-defensins by intestinal Paneth cells in response to bacteria. Nat Immunol 1(2):113-118.
6. Barnard JA, Beauchamp RD, Russell WE, Dubois RN, Coffey RJ. 1995. Epidermal growth factor-related peptides and their relevance to gastrointestinal pathophysiology. Gastroenterology 108(2):564-580.
7. Barrila J, Radtke AL, Crabbe A, Sarker SF, Herbst-Kralovetz MM, Ott CM, Nickerson CA. 2010. Organotypic 3D cell culture models: Using the rotating wall vessel to study host-pathogen interactions. Nat Rev Microbiol 8(11):791-801.
8. Basson MD, Modlin IM, Madri JA. 1992. Human enterocyte (CACO-2) migration is modulated invitro by extracellular-matrix composition and epidermal growth-factor. J Clin Invest 90(1):15-23.
9. Beatty MW, Ojha AK, Cook JL, Alberts LR, Mahanna GK, Iwasaki LR, Nickel JC. 2002. Small intestinal submucosa versus salt-extracted polyglycolic acid-poly-L-lactic acid: A comparison of neocartilage formed in two scaffold materials. Tissue Eng 8(6):955-968.
10. Beckstead BL, Pan S, Bhrany AD, Bratt-Leal AM, Ratner BD, Giachelli CM. 2005. Esophageal epithelial cell interaction with synthetic and natural scaffolds for tissue engineering. Biomaterials 26(31):6217-6228.
11. Bentrup KHz, Ramamurthy R, Ott CM, Emami K, Nelman-Gonzalez M, Wilson JW, Richter EG, Goodwin TJ, Alexander JS, Pierson DL, et al. 2006. Three-dimensional organotypic models of human colonic epithelium to study the early stages of enteric salmonellosis. Microb Infect 8(7):1813-1825.
12. Bernardo D, Sanchez B, Al-Hassi HO, Mann ER, Urdaci MC, Knight SC, Margolles A. 2012. Microbiota/host crosstalk biomarkers: Regulatory response of human intestinal dendritic cells exposed to lactobacillus extracellular encrypted peptide. PLoS ONE 7(5):e36262.
13. Bernet MF, Brassart D, Neeser JR, Servin AL. 1994. Lactobacillus-acidophilus la-1 binds to cultured human intestinal-cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria. Gut 35(4):483-489.
14. Bettinger CJ, Langer R, Borenstein JT. 2009. Engineering substrate topography at the micro- and nanoscale to control cell function. Angewandte Chemie Int Edn 48(30):5406-5415.
15. Brown RA, Phillips JB. 2007. Cell responses to biomimetic protein scaffolds used in tissue repair and engineering. Int Rev Cytol 262(262):75-150.
16. Cao Y, Mitchell G, Messina A, Price L, Thompson E, Penington A, Morrison W, O'Connor A, Stevens G, Cooper-White J. 2006. The influence of architecture on degradation and tissue ingrowth into three-dimensional poly(lactic-co-glycolic acid) scaffolds in vitro and in vivo. Biomaterials 27(14):2854-2864.
17. Chen X, Zhao J, Gregersen H. 2008. The villi contribute to the mechanics in the guinea pig small intestine. J Biomech 41(4):806-812.
18. Choi RS, Vacanti JP. 1997. Preliminary studies of tissue-engineered intestine using isolated epithelial organoid units on tubular synthetic biodegradable scaffolds. Transpl Proc 29(1-2):848-851.
19. Clark JA, Doelle SM, Halpern MD, Saunders TA, Holubec H, Dvorak K, Boitano SA, Dvorak B. 2006. Intestinal barrier failure during experimental necrotizing enterocolitis: Protective effect of EGF treatment. Am J Physiol Gastrointes Liver Physiol 291(5):G938-G949.
20. Clark P, Connolly P, Curtis ASG, Dow JAT, Wilkinson CDW. 1991. Cell guidance by ultrafine topography in vitro. J Cell Sci 99(Pt1):71-77.
21. Cross HS, Quaroni A. 1991. Inhibition of sucrase-isomaltase expression by egf in the human colon adenocarcinoma cells CACO-2. Am J Physiol 261(6):C1173-C1183.
22. Darfeuille-Michaud A, Boudeau J, Bulois P, Neut C, Glasser AL, Barnich N, Bringer MA, Swidsinski A, Beaugerie L, Colombel JF. 2004. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 127(2):412-421.
23. Day RM. 2006. Epithelial stem cells and tissue engineered intestine. Curr Stem Cell Res Ther 1(1):113-120.
24. Fan MZ, Stoll B, Jiang R, Burrin DG. 2001. Enterocyte digestive enzyme activity along the crypt-villus and longitudinal axes in the neonatal pig small intestine. J Anim Sci 79(2):371-381.
25. Ferruzza S, Rossi C, Scarino ML, Sambuy Y. 2012. A protocol for in situ enzyme assays to assess the differentiation of human intestinal Caco-2 cells. Toxicol In Vitro 26(8):1274-1251.
26. Goodwin TJ, Schroeder WF, Wolf DA, Moyer MP. 1993. Rotating-wall vessel coculture of small-intestine as a prelude to tissue modeling: Aspects of simulated microgravity. Proc Soc Exp Biol Med 202(2):181-192.
27. Grikscheit TC, Ochoa ER, Ramsanahie A, Alsberg E, Mooney D, Whang EE, Vacanti JP. 2003. Tissue-engineered large intestine resembles native colon with appropriate in vitro physiology and architecture. Ann Surg 238(1):35-41.
28. Grikscheit TC, Siddique A, Ochoa ER, Srinivasan A, Alsberg E, Hodin RA, Vacanti JP. 2004. Tissue-engineered small intestine improves recovery after massive small bowel resection. Ann Surg 240(5):748-754.
29. Guan LM, Davies JE. 2004. Preparation and characterization of a highly macroporous biodegradable composite tissue engineering scaffold. J Biomed Mater Res Part A 71A(3):480-487.
30. Hidalgo IJ, Raub TJ, Borchardt RT. 1989. Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability. Gastroenterology 96(3):736-749.
31. Hilgers AR, Conradi RA, Burton PS. 1990. Caco-2 Cell Monolayers as a Model for Drug Transport Across the Intestinal Mucosa. Pharm Res 7(9):902-910.
32. Ho MH, Kuo PY, Hsieh HJ, Hsien TY, Hou LT, Lai JY, Wang DM. 2004. Preparation of porous scaffolds by using freeze-extraction and freeze-gelation methods. Biomaterials 25(1):129-138.
33. Piechocka IK, van Oosten AS, Breuls RG, Koenderink GH. 2011. Rheology of heterotypic collagen networks. Biomacromolecules. 2797-2805.
34. Kaeffer B. 2002. Mammalian intestinal epithelial cells in primary culture: A mini-review. In Vitro Cell Dev Biol Anim 38(3):123-134.
35. Kelly SM, Hunter JO. 1990. Epidermal growth-factor stimulates synthesis and secretion of mucus glycoproteins in human gastric-mucosa. Clin Sci 79(5):425-427.
36. Kim HJ, Huh D, Hamilton G, Ingber DE. 2012. Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab Chip 12(12):2165-2174.
37. Lesuffleur T, Barbat A, Dussaulx E, Zweibaum A. 1990. Growth adaptation to methotrexate of HT-29 human colon carcinoma cells is associated with their ability to differentiate into columnar absorptive and mucus-secreting cells. Cancer Res 50(19):6334-6343.
38. Leung L, Chan C, Baek S, Naguib H. 2008. Comparison of morphology and mechanical properties of PLGA bioscaffolds. Biomed Mater 3(2):025006.
39. Li SR, La Carrubba V, Piccarolo S, Sannino D, Brucato V. 2004. Preparation and properties of poly(L-lactic acid) scaffolds by thermally induced phase separation from a ternary polymer-solvent system. Polymer Int 53(12):2079-2085.
40. Lin HR, Kuo CJ, Yang CY, Shaw SY, Wu YJ. 2002. Preparation of macroporous biodegradable PLGA scaffolds for cell attachment with the use of mixed salts as porogen additives. J Biomed Mater Res 63(3):271-279.
41. Lin PW, Simon PO, Gewirtz AT, Neish AS, Ouellette AJ, Madara JL, Lencer WI. 2004. Paneth cell cryptdins act in vitro as apical paracrine regulators of the innate inflammatory response. J Biol Chem 279(19):19902-19907.
42. Lu L, Peter SJ, Lyman MD, Lai HL, Leite SM, Tamada JA, Uyama S, Vacanti JP, Langer R, Mikos AG. 2000. In vitro and in vivo degradation of porous poly(DL-lactic-co-glycolic acid) foams. Biomaterials 21(18):1837-1845.
43. Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, Yachimec C, Doyle J, Jewell L, De Simone C. 2001. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 121(3):580-591.
44. Maierhofer C, Rohmer K, Wittmann V. 2007. Probing multivalent carbohydrate-lectin interactions by an enzyme-linked lectin assay employing covalently immobilized carbohydrates. Bioorg Med Chem 15(24):7661-7676.
45. Manning AP, Thompson WG, Heaton KW, Morris AF. 1978. Towards positive diagnosis of the irritable bowel. BMJ 2(6138):653-654.
46. Matsumoto H, Erickson RH, Gum JR, Yoshioka M, Gum E, Kim YS. 1990. Biosynthesis of alkaline-phosphatase during differentiation of the human colon cancer cell-line Caco-2. Gastroenterology 98(5):1199-2085.
47. Mattioli-Belmonte M, Vozzi G, Kyriakidou K, Pulieri E, Lucarini G, Vinci B, Pugnaloni A, Biagini G, Ahluwalia A. 2008. Rapid-prototyped and salt-leached PLGA scaffolds condition cell morpho-functional behavior. J Biomed Mater Res Part A 85A(2):466-476.
48. Molladavoodi S, Gorbet M, Medley J, Kwon HJ. 2013. Investigation of microstructure, mechanical properties and cellular viability of poly(L-lactic acid) tissue engineering scaffolds prepared by different thermally induced phase separation protocols. J Mech Behav Biomed Mater 17:186-197.
49. Moon HW. 1978. Mechanisms in pathogenesis of diarrhea - review. J Am Vet Med Assoc 172(4):443-448.
50. Murray JA. 1999. The widening spectrum of celiac disease. Am J Clin Nutr 69(3):354-365.
51. Nematollahi M, Hamilton DW, Jaeger NJ, Brunette DM. 2009. Hexagonal micron scale pillars influence epithelial cell adhesion, morphology, proliferation, migration, and cytoskeletal arrangement. J Biomed Mater Res Part A 91A(1):149-157.
52. Nickerson CA, Richter EG, Ott CM. 2007. Studying host-pathogen interactions in 3D: Organotypic models for infectious disease and drug development. J Neuroimmune Pharmacol 2(1):26-31.
53. Okuyama H, Urao M, Lee D, Drongowski RA, Coran AG. 1998. The effect of epidermal growth factor on bacterial translocation in newborn rabbits. J Pediatr Surg 33(2):225-228.
54. Ouellette AJ. 1997. Paneth cells and innate immunity in the crypt microenvironment. Gastroenterology 113(5):1779-1784.
55. Pavia FC, La Carrubba V, Brucato V. 2013. Polymeric scaffolds based on blends of poly-L-lactic acid (PLLA) with poly-D-L-lactic acid (PLA) prepared via thermally induced phase separation (TIPS): Demixing conditions and morphology. Polym Bull 70(2):563-578.
56. Pinto M, Robineleon S, Appay MD, Kedinger M, Triadou N, Dussaulx E, Lacroix B, Simonassmann P, Haffen K, Fogh J, et al. 1983. Enterocyte-like differentiation and polarization of the human-colon carcinoma cell-line CACO-2 in culture. Biol Cell 47(3):82-92.
57. Salzman NH, Chou MM, de Jong H, Liu L, Porter EM, Paterson Y. 2003. Enteric salmonella infection inhibits Paneth cell antimicrobial peptide expression. Infect Immun 71(3):1109-1115.
58. 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. 2011. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469(7330):415-418.
59. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, van Es JH, Abo A, Kujala P, Peters PJ, et al. 2009. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459(7244):262-U147.
60. Scheving LA, Shiurba RA, Nguyen TD, Gray GM. 1989. Epidermal growth-factor receptor of the intestinal enterocyte - localization to laterobasal but not brush-border membrane. J Biol Chem 264(3):1735-1741.
61. Schulzke JD, Bentzel CJ, Schulzke I, Riecken EO, Fromm M. 1998. Epithelial tight junction structure in the jejunum of children with acute and treated celiac sprue. Pediatr Res 43(4):435-441.
62. Shi GX, Cai Q, Wang CY, Lu N, Wang SG, Bei JZ. 2002. Fabrication and biocompatibility of cell scaffolds of poly(L-lactic acid) and poly(L-lactic-co-glycolic acid). Polym Adv Technol 13(3-4):227-232.
63. Simon-Assman P, Turck N, Sidhoum-Jenny M, Gradwohl G, Kedinger M. 2007. In vitro models of intestinal epithelial cell differentiation. Cell Biol Toxicol 23(4):241-256.
64. Skardal A, Sarker SF, Crabbe A, Nickerson CA, Prestwich GD. 2010. The generation of 3D tissue models based on hyaluronan hydrogel-coated microcarriers within a rotating wall vessel bioreactor. Biomaterials 31(32):8426-8435.
65. Spence JR, Mayhew CN, Rankin SA, Kuhar MF, Vallance JE, Tolle K, Hoskins EE, Kalinichenko VV, Wells SI, Zorn AM, et al. 2011. Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature 470(7332):105-U120.
66. Spurrier RG, Grikscheit TC. 2013. Tissue engineering the small intestine. Clinical Gastroenterol Hepatol 11(4):354-358.
67. Steidler L, Hans W, Schotte L, Neirynck S, Obermeier F, Falk W, Fiers W, Remaut E. 2000. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science 289(5483):1352-1355.
68. Sung JH, Yu J, Luo D, Shuler ML, March JC. 2011. Microscale 3D hydrogel scaffold for biomimetic gastrointestinal (GI) tract model. Lab Chip 11(3):389-392.
69. Uhlig HH, Powrie F. 2009. Mouse models of intestinal inflammation as tools to understand the pathogenesis of inflammatory bowel disease. Eur J Immunol 39(8):2021-2026.
70. Walter E, Janich S, Roessler BJ, Hilfinger JM, Amidon GL. 1996. HT29-MTX/Caco-2 cocultures as an in vitro model for the intestinal epithelium: In vitro in vivo correlation with permeability data from rats and humans. J Pharm Sci 85(10):1070-1076.
71. Wang L, Murthy SK, Barabino GA, Carrier RL. 2010. Synergic effects of crypt-like topography and ECM proteins on intestinal cell behavior in collagen based membranes. Biomaterials 31(29):7586-7598.
72. Wang L, Murthy SK, Fowle WH, Barabino GA, Carrier RL. 2009. Influence of micro-well biomimetic topography on intestinal epithelial Caco-2 cell phenotype. Biomaterials 30(36):6825-6834.
73. Wikman A, Karlsson J, Carlstedt I, Artursson P. 1993. A drug absorption-model based on the mucus layer producing human intestinal goblet cell-line HT29-H. Pharm Res 10(6):843-852.
74. Wright NA, Poulsom R, Stamp GWH, Hall PA, Jeffery RE, Longcroft JM, Rio MC, Tomasetto C, Chambon P. 1990. Epidermal growth-factor (egf uro) induces expression of regulatory peptides in damaged human gastrointestinal tissues. J Pathol 162(4):279-284.
75. Yang Y, Zhao J, Zhao Y, Wen L, Yuan X, Fan Y. 2008. Formation of porous PLGA scaffolds by a combining method of thermally induced phase separation and porogen leaching. J Appl Polym Sci 109(2):1232-1241.
76. Yu J, Peng S, Luo D, March JC. 2012. In vitro 3D human small intestinal villous model for drug permeability determination. Biotechnol Bioeng 109(9):2173-2178.
77. Zoghbi S, Trompette A, Claustre J, El Homsi M, Garzon J, Scoazec JY, Plaisancie P. 2006. beta-Casomorphin-7 regulates the secretion and expression of gastrointestinal mucins through a mu-opioid pathway. Am J Physiol Gastrointest Liver Physiol 290(6):G1105-G1113.