Explant culture of gastrointestinal tissue: A review of methods and applications

Cell Biology and Toxicology

Volumn 27, Issue 4, 2011, Pages 267-284

  Randall, Kevin J ^a   Turton, John ^b   Foster, John R ^a  

^a ASTRAZENECA   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Explant; Gastrointestinal; Organ culture; Toxicology

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 1BETA; TUMOR NECROSIS FACTOR ALPHA; XENOBIOTIC AGENT;

AGE; ANIMAL CELL CULTURE; ANOXIA; APOPTOSIS; BIOMEDICINE; BIOTECHNOLOGY; CELL DIFFERENTIATION; CELL DIVISION; CELL STRUCTURE; CELL VIABILITY; COLON MUCOSA; CULTURE MEDIUM; CYTOTOXICITY; DRUG RESEARCH; EMBRYONAL TISSUE; ENTERITIS; EPITHELIUM CELL; EXPLANT; GASTROINTESTINAL MUCOSA; GASTROINTESTINAL TOXICITY; GASTROINTESTINAL TRACT; HISTOPATHOLOGY; HUMAN; HUMAN CELL CULTURE; IN VIVO STUDY; INTESTINE CELL; INTESTINE MUCOSA; LIVING DONOR; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPRODUCIBILITY; REVIEW; SPECIES DIFFERENCE; TISSUE CULTURE TECHNIQUE; TISSUE METABOLISM; TISSUE PRESERVATION; TISSUE STRUCTURE;

ANIMALS; CELL DIFFERENTIATION; CULTURE MEDIA; GASTROINTESTINAL TRACT; HUMANS; MORPHOGENESIS; TISSUE CULTURE TECHNIQUES; XENOBIOTICS;

EID: 79959564815     PISSN: 07422091     EISSN: 15736822     Source Type: Journal    
DOI: 10.1007/s10565-011-9187-5     Document Type: Review

References (80)

1. Abud HE, Watson N, Heath JK. Growth of intestinal epithelium in organ culture is dependent on EGF signalling. Exp Cell Res. 2005;303:252-62. (Pubitemid 40126260)
2. Autrup H, Barrett LA, Jackson FE, Jesudason ML, Stoner G, Phelps P, et al. Explant culture of human colon. Gastroenterology. 1978a;74:1248-57. (Pubitemid 8352852)
3. Autrup H, Stoner GD, Jackson F, Harris CC, Shamsuddin AK, Barrett LA, et al. Explant culture of rat colon: a model system for studying metabolism of chemical carcinogens. In Vitro. 1978b;14:868-77. (Pubitemid 9034370)
4. Bareiss PM, Metzger M, Sohn K, Rupp S, Frick JS, Autenrieth IB, et al. Organotypical tissue cultures from adult murine colon as an in vitro model of intestinal mucosa. Histochem Cell Biol. 2008;129:795-804.
5. Borsch G, Schmidt G. What's new in steroid and nonsteroid drug effects on gastroduodenal mucosa? Pathol Res Pract. 1985;180:437-44.
6. Brennan PC, McCullough JS, Carr KE. Variations in cell and structure populations along the length of murine small intestine. Cells Tissues Organs. 1999;164:221-6. (Pubitemid 29357198)
7. Broadhead CL, Bottrill K. Strategies for replacing animals in biomedical research. Mol Med Today. 1997;3:483-7. (Pubitemid 27505481)
8. Browning TH, Trier JS. Organ culture of mucosal biopsies of human small intestine. J Clin Invest. 1969;48:1423-32.
9. Brusko TM, Hulme MA, Myhr CB, Haller MJ, Atkinson MA. Assessing the in vitro suppressive capacity of regulatory T cells. Immunol Invest. 2007;36:607-28.
10. Buck V. Who will start the 3Rs ball rolling for animal welfare? Nature. 2007;446:856.
11. Bullen TF, Forrest S, Campbell F, Dodson AR, Hershman MJ, Pritchard DM, et al. Characterization of epithelial cell shedding from human small intestine. Lab Invest. 2006;86:1052-63. (Pubitemid 44423069)
12. Challacombe DN, Wheeler EE. Trophic action of epidermal growth factor on human duodenal mucosa cultured in vitro. Gut. 1991;32:991-3.
13. Cheng H, Bjerknes M. Whole population cell kinetics of mouse duodenal, jejunal, ileal, and colonic epithelia as determined by radioautography and flow cytometry. Anat Rec. 1982;203:251-64. (Pubitemid 12078926)
14. Cheng H, Bjerknes M. Cell production in mouse intestinal epithelium measured by stathmokinetic flow cytometry and coulter particle counting. Anat Rec. 1983;207:427-34. (Pubitemid 14205518)
15. Cheng H, Leblond CP. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. I. Columnar cell. Am J Anat. 1974;141:461-79.
16. Clayton RF, Rinaldi A, Kandyba EE, Edward M, Willberg C, Klenerman P, et al. Liver cell lines for the study of hepatocyte functions and immunological response. Liver Int. 2005;25:389-402.
17. Danielsen EM, Sjöström H, Norén O, Bro B, Dabelsteen E. Biosynthesis of intestinal microvillar proteins. Characterization of intestinal explants in organ culture and evidence for the existence of pro-forms of the microvillar enzymes. Biochem J. 1982;202:647-54.
18. De Kanter R, Monshouwer M, Meijer DKF, Groothuis GMM. Precision cut organ slices as a tool to study toxicity and metabolism of xenobiotics with special reference to non-hepatic tissues. Curr Drug Metab. 2002a;3:39-59. (Pubitemid 34296309)
19. De Kanter R, De Jager MH, Draaisma AL, Jurva JU, Olinga P, Meijer DKF, et al. Drug-metabolizing activity of human and rat liver, lung, kidney and intestine slices. Xenobiotica. 2002b;32:349-62. (Pubitemid 34624631)
20. De Kanter R, Monshouwer M, Draaisma AL, De Jager MH, De Graaf IAM, Proost JH, et al. Prediction of whole-body metabolic clearance of drugs through the combined use of slices from rat liver, lung, kidney, small intestine and colon. Xenobiotica. 2004;34:229-41. (Pubitemid 38478892)
21. Di Sabatino A, Pickard KM, Rampton D, Kruidenier L, Rovedatti L, Leakey NA, et al. Blockade of transforming growth factor beta upregulates T-box transcription factor T-bet, and increases T helper cell type 1 cytokine and matrix metalloproteinase-3 production in the human gut mucosa. Gut. 2008;57:605-12. (Pubitemid 351579972)
22. Dionne S, D'Agata ID, Hiscott J, Vanounou T, Seidman EG. Colonic explant production of IL-1and its receptor antagonist is imbalanced in inflammatory bowel disease (IBD). Clin Exp Immunol. 1998;112:435-42. (Pubitemid 28267424)
23. Dionne S, Laberge S, Deslandres C, Seidman EG. Modulation of cytokine release from colonic explants by bacterial antigens in inflammatory bowel disease. Clin Exp Immunol. 2003;133:108-14. (Pubitemid 36791948)
24. Emoto C, Yamazaki H, Yamasaki S, Shimada N, Nakajima M, Yokoi T. Use of everted sacs of mouse small intestine as enzyme sources for the study of drug oxidation activities in vitro. Xenobiotica. 2000;30:971-82.
25. Emoto C, Yamazaki H, Yamasaki S, Shimada N, Nakajima M, Yokoi T. Characterization of cytochrome P450 enzymes involved in drug oxidations in mouse intestinal microsomes. Xenobiotica. 2002;10:943-53.
26. Fara JW, Anderson LD, Casper AG, Myrback RE. Assessment and validation of animal models to evaluate topical effects of substances on gastrointestinal mucosa. Pharm Res. 1988;5:165-71.
27. Finney KJ, Ince P, Appleton DR, Sunter JP, Watson AJ. A comparison of crypt-cell proliferation in rat colonic mucosa in vivo and in vitro. J Anat. 1986;149:177-88.
28. Fischer A. A pure strain of cartilage cell in vitro. JEM. 1922;36:379-86.
29. Fletcher PS, Elliott J, Grivel JC, Margolis L, Anton P, McGowan I, et al. Ex vivo culture of human colorectal tissue for the evaluation of candidate microbicides. AIDS. 2006;20:1237-45. (Pubitemid 44030371)
30. Goyal RK, Hirano I. The enteric nervous system. New Engl J Med. 1996;334:1106-15. (Pubitemid 26120190)
31. Hearn CJ, Young HM, Ciampoli D, Lomax AEG, Newgreen D. Caternary cultures of embryonic gastrointestinal tract support organ morphogenesis, motility, neural crest cell migration, and cell differentiation. Dev Dynam. 1999;214:239-47. (Pubitemid 29117584)
32. Howdle PD. Organ culture of gastrointestinal mucosa - a technique for the study of the human gastrointestinal tract. Postgrad Med J. 1984;60:645-52. (Pubitemid 14008993)
33. Ito K, Iwatsubo T, Kanamitsu S, Nakajima Y, Sugiyama Y. Quantitative prediction of in vivo drug clearance and drug interactions from in vitro data on metabolism, together with binding and transport. Ann Rev Pharmacol Toxicol. 1998;38:461-99. (Pubitemid 28231503)
34. Jacobs JJ, Lehé C, Cammans KD, Das PK, Elliott GR. An in vitro model for detecting skin irritants: methyl green-pyronine staining of human skin explant cultures. Toxicol in Vitro. 2002;16:581-8. (Pubitemid 35229985)
35. Jarry A, Bach-Ngohou K, Masson D, Dejoie T, Lehur PA, Mosnier JF, et al. Human colonic myocytes are involved in postischemic inflammation through ADAM17-dependent TNFalpha production. Br J Pharmacol. 2006;147:64-72. (Pubitemid 43069097)
36. Jarry A, Bossard C, Bou-Hanna C, Masson D, Espaze E, Denis MG, et al. Mucosal IL-10 and tgf-beta play crucial roles in preventing lps-driven, ifn-gamma-mediated epithelial damage in human colon explants. J Clin Invest. 2008;118:1132-42. (Pubitemid 351364620)
37. Kararli TT. Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory animals. Biopharm Drug Dispos. 1995;16:351-80.
38. Kik MJ, Koninkx JF, van den Muysenberg A, Hendriksen F. Pathological effects of Phaseolus vulgaris isolectins on pig jejunal mucosa in organ culture. Gut. 1991;32:886-92.
39. Lehé CL, Jacobs JJ, Hua CM, Courtellemont P, Elliott GR, Das PK. Subtoxic concentrations of allergenic haptens induce LC migration and maturation in a human organotypic skin explant culture model: a novel method for identifying potential contact allergens. Exp Dermatol. 2006;15:421-31.
40. Lindley RM, Hawcutt DB, Connell MG, Almond SL, Vannucchi MG, Faussone-Pellegrini MS, et al. Human and mouse enteric nervous system neurosphere transplants regulate the function of aganglionic embryonic distal colon. Gastroenterology. 2008;135:205-16.
41. Losonsky GA, Fantry GT, Reymann M, Lim Y. Validation of a gastrointestinal explant system for measurement of mucosal antibody production. Clin Diagn Lab Immunol. 1999;6:803-7. (Pubitemid 29529969)
42. Manzano M, Bueno P, Rueda R, Ramirez-Tortosa CL, Prieto PA, Lopez-Pedrosa JM. Intestinal toxicity induced by 5-fluorouracil in pigs: a new preclinical model. Chemotherapy. 2007;53:344-55. (Pubitemid 47415436)
43. Maximow A. Tissue cultures of young mammalian embryos. Contributions to Embryology. 1925;16:47-133.
44. Mazzarella G, Stefanile R, Camarca A, Giliberti P, Cosentini E, Marano C, et al. Gliadin activates HLA class I-restricted CD8+ T cells in celiac disease intestinal mucosa and induces the enterocyte apoptosis. Gastroenterology. 2008;134:1017-27. (Pubitemid 351451963)
45. Metzger M, Bareiss PM, Nikolov I, Skutella T, Just L. Three-dimensional slice cultures from murine fetal gut for investigations of the enteric nervous system. Dev Dyn. 2007;236:128-33. (Pubitemid 46095085)
46. Metzger M, Bareiss PM, Danker T, Wagner S, Hennenlotter J, Guenther E, et al. Expansion and differentiation of neural progenitors derived from the human adult enteric nervous system. Gastroenterology. 2009;137:2063-73.
47. Mitchell JD, Mitchell J, Peters TJ. Enzyme changes in human small bowel mucosa during culture in vitro. Gut. 1974;15:805-11.
48. Natarajan D, Grigoriou M, Marcos-Gutierrez CV, Atkins C, Pachnis V. Multipotential progenitors of the mammalian enteric nervous system capable of colonising aganglionic bowel in organ culture. Development. 1999;126:157-68. (Pubitemid 29045909)
49. Nigsch F, Klaffke W, Miret S. In vitro models for processes involved in intestinal absorption. Expert Opin Drug Metab Toxicol. 2007;3:545-56.
50. OECD. Final Report of the OECD Workshop on the Harmonisation of Validation and Acceptance Criteria for Alternative Toxicological Test Methods (Solna Report, 1996) as presented to the Seventh Meeting of the National Coordinators of the Test Guidelines Programme, 18-19 September 1996. ENV/MC/CHEM/TG(96)9. Paris: OECD, 1996
51. OECD. Final Report of the OECD Conference on the Validation and Regulatory Acceptance of New and Updated Methods in Hazard Assessment (Stockholm Report). ENV/JM/TG/M(2002)2. Paris: OECD, 2002.
52. Ootani A, Toda S, Fujimoto K, Sugihara H. An air-liquid interface promotes the differentiation of gastric surface mucous cells (GSM06) in culture. Biochem Biophys Res Commun. 2000;271:741-6. (Pubitemid 30444699)
53. Ootani A, Li X, Sangiorgi E, Ho QT, Ueno H, Toda S, et al. Sustained in vitro intestinal epithelial culture within a Wnt-dependent stem cell niche. Nat Med. 2009;15:701-6.
54. Ouellette AJ. Paneth cells and innate mucosal immunity. Curr Opin Gastroenterol. 2010;26:546-53.
55. Porter EM, Bevins CL, Ghosh D, Ganz T. The multifaceted Paneth cell. Cell Mol Life Sci. 2002;59:156-70. (Pubitemid 34117363)
56. Preynat-Seauve O, Suter DM, Tirefort D, Turchi L, Virolle T, Chneiweiss H, et al. Development of human nervous tissue upon differentiation of embryonic stem cells in three-dimensional culture. Stem Cells. 2009;27:509-20.
57. Quinlan JM, Yu WY, Hornsey MA, Tosh D, Slack JM. In vitro culture of embryonic mouse intestinal epithelium: cell differentiation and introduction of reporter genes. BMC Dev Biol. 2006;6:24.
58. Randall KJ, Foster JR. The demonstration of immunohistochemical biomarkers in methyl methacrylate-embedded plucked human hair follicles. Toxicol Pathol. 2007;35:952-7.
59. Robertson JM, Grant G, Allen-Vercoe E, Woodward MJ, Pusztai A, Flint HJ. Adhesion of Salmonella enterica var Enteritidis strains lacking fimbriae and flagella to rat ileal explants cultured at the air interface or submerged in tissue culture medium. J Med Microbiol. 2000;49:691-6. (Pubitemid 30623900)
60. Rouet-Benzineb P, Rouyer-Fessard C, Jarry A, Avondo V, Pouzet C, Yanagisawa M, et al. Orexins acting at native OX(1) receptor in colon cancer and neuroblastoma cells or at recombinant OX(1) receptor suppress cell growth by inducing apoptosis. J Biol Chem. 2004;279:45875-86.
61. Rowland IR, Mallett AK, Wise A. The effect of diet on the mammalian gut flora and its metabolic activities. Crit Rev Toxicol. 1985;16:31-103.
62. Sambruy Y, Ferruzza S, Ranaldi G, De Angelis I. Intestinal cell culture models: applications in toxicology and pharmacology. Cell Biol Toxicol. 2001;17:301-17.
63. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature. 2009;459:262-5.
64. Schiff LJ. Organ cultures of rat and hamster colon. In Vitro. 1975;11:46-9.
65. Seeber JW, Zorn-Kruppa M, Lombardi-Borgia S, Scholz H, Manzer AK, Rusche B, et al. Characterisation of human corneal epithelial cell cultures maintained under serum-free conditions. Altern Lab Anim. 2008;36:569-83.
66. Shamsuddin AK, Barrett LA, Autrup H, Harris CC, Trump BF. Long-term organ culture of adult rat colon. Pathol Res Pract. 1978;163:362-72. (Pubitemid 9123386)
67. Simon-Assmann P, Turck N, Sidhoum-Jenny M, Gradwohl G, Kedinger M. In vitro models of intestinal epithelial cell differentiation. Cell Biol Toxicol. 2007;23:241-56.
68. Snippert HJ, van der Flier LG, Sato T, van Es JH, van den Born M, Kroon-Veenboer C, et al. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell. 2010;142:134-44.
69. Stoppini L, Buchs PA, Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods. 1991;37:173-82.
70. Strangeways TSP, Fell HB. Experimental studies on the differentiation of embryonic tissues growing in vivo and in vitro. I. The development of the undifferentiated limb-bud (a) when subcutaneously grafted into the post-embryonic chick and (b) when cultivated in vitro. Proc R Soc Lond B. 1926;99:340-66.
71. Takemoto K, Yamazaki H, Tanaka Y, Nakajima M, Yokoi T. Catalytic activities of cytochrome P450 enzymes and UDP-glucuronosyltransferases involved in drug metabolism in rat everted sacs and intestinal microsomes. Xenobiotica. 2003;33:43-55. (Pubitemid 36071762)
72. Tham DM, Whitin JC, Kim KK, Zhu SX, Cohen HJ. Expression of extracellular glutathione peroxidase in human and mouse gastrointestinal tract. Am J Physiol. 1998;275:G1463-71.
73. Thomson D. Some further researches on the cultivation of tissues in vitro. Proc R Soc Med. 1914;7:21-46.
74. Trowell OA. The culture of mature organs in a synthetic medium. Exp Cell Res. 1959;16:118-47.
75. Wheeler EE, Challacombe DN. The trophic action of growth hormone, insulin-like growth factor-I, and insulin on human duodenal mucosa cultured in vitro. Gut. 1997;40:57-60. (Pubitemid 27079751)
76. Yeh TH, Tsai CH, Chen YS, Hsu WC, Cheng CH, Hsu CJ, et al. Increased communication among nasal epithelial cells in air-liquid interface culture. Laryngoscope. 2007;117:1439-44.
77. Young B, Heath JW. Wheater's functional histology. 4th ed. London: Churchill Livingstone; 2000. p. 249-73.
78. Zachrisson K, Neopikhanov V, Wretlind B, Uribe A. Mitogenic action of tumour necrosis factor-alpha and interleukin-8 on explants of human duodenal mucosa. Cytokine. 2001;15:148-55. (Pubitemid 34587496)
79. Zak O, O'Reilly T. Animal models in the evaluation of antimicrobial agents. Antimicrob Agents Chemother. 1991;35:1527-31.
80. Zimmermann GS, Neurohr C, Villena-Hermoza H, Hatz R, Behr J. Anti-inflammatory effects of antibacterials on human bronchial epithelial cells. Respir Res. 2009;29:10-89.