Epithelial cell extrusion leads to breaches in the intestinal epithelium

Inflammatory Bowel Diseases

Volumn 19, Issue 5, 2013, Pages 912-921

  Liu, Julia J ^a   Davis, Elisabeth M ^a   Wine, Eytan ^a   Lou, Yuefei ^a   Rudzinski, Jan K ^b   Alipour, Misagh ^a   Boulanger, Pierre ^a   Thiesen, Aducio L ^a   Sergi, Consolato ^a   Fedorak, Richard N ^a   Muruve, Daniel ^a   Madsen, Karen L ^a   Irvin, Randall T ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Bacteria; Barrier function; Caspase 1; Cell extrusion; Confocal endomicroscopy; Epithelial integrity; Inflammasome; Inflammatory bowel disease; Interleukin 1 beta; Intestinal epithelial cells; Mucosa; Pyroptosis; Small intestine

Indexed keywords

CASPASE 3; CASPASE 7; GREEN FLUORESCENT PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA CONVERTING ENZYME; MICROSPHERE;

ANIMAL EXPERIMENT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOCHEMISTRY; ENZYME ACTIVATION; EPITHELIUM CELL; ESCHERICHIA COLI; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; INTESTINE; INTESTINE BIOPSY; INTESTINE EPITHELIUM; INTESTINE MUCOSA PERMEABILITY; MICROORGANISM; MONOLAYER CULTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; STAINING; WILD TYPE;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CASE-CONTROL STUDIES; CASPASE 1; CASPASE 3; CELL DIFFERENTIATION; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; CELL SURFACE EXTENSIONS; CELLS, CULTURED; CYTOKINES; EPITHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; INFLAMMATORY BOWEL DISEASES; INTERLEUKIN-10; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT;

EID: 84876404676     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0b013e3182807600     Document Type: Article

References (50)

1. Mayhew TM, Myklebust R, Whybrow A, et al. Epithelial integrity, cell death and cell loss in mammalian small intestine. Histol Histopathol. 1999;14:257-267.
2. Rosenblatt J, Raff MC, Cramer LP. An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr Biol. 2001;11:1847-1857.
3. Watson AJ, Chu S, Sieck L, et al. Epithelial barrier function in vivo is sustained despite gaps in epithelial layers. Gastroenterology. 2005;129:902-912.
4. Myklebust R, Mayhew TM. Further evidence of species variation in mechanisms of epithelial cell loss in mammalian small intestine: ultrastructural studies on the reindeer (Rangifer tarandus) and seal (Phoca groenlandica). Cell Tissue Res. 1998;291:513-523.
5. Sato T, Vries RG, Snippert HJ, et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature. 2009;459:262-265.
6. Bullen TF, Forrest S, Campbell F, et al. Characterization of epithelial cell shedding from human small intestine. Lab Invest. 2006;86:1052-1063.
7. Shibahara T, Sato N, Waguri S, et al. The fate of effete epithelial cells at the villus tips of the human small intestine. Arch Histol Cytol. 1995;58:205-219.
8. Knodler LA, Vallance BA, Celli J, et al. Dissemination of invasive Salmonella via bacterial-induced extrusion of mucosal epithelia. Proc Natl Acad Sci USA. 2010;107:17733-17738.
9. Thornberry NA, Bull HG, Calaycay JR, et al. A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature. 1992;356:768-774.
10. Martinon F, Burns K, Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell. 2002;10:417-426.
11. Franchi L, Munoz-Planillo R, Nunez G. Sensing and reacting to microbes through the inflammasomes. Nat Immunol. 2012;13:325-332.
12. Kroemer G, Galluzzi L, Vandenabeele P, et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 2009;16:3-11.
13. Fink SL, Bergsbaken T, Cookson BT. Anthrax lethal toxin and Salmonella elicit the common cell death pathway of caspase-1-dependent pyroptosis via distinct mechanisms. Proc Natl Acad Sci USA. 2008;105:4312-4317.
14. Miao EA, Leaf IA, Treuting PM, et al. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol. 2010;11:1136-1142.
15. Labbe K, Saleh M. Cell death in the host response to infection. Cell Death Differ. 2008;15:1339-1349.
16. Bergsbaken T, Fink SL, Cookson BT. Pyroptosis: host cell death and inflammation. Nat Rev Microbiol. 2009;7:99-109.
17. Dinarello CA. Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol. 2009;27:519-550.
18. Mahida YR, Wu K, Jewell DP. Enhanced production of interleukin 1-beta by mononuclear cells isolated from mucosa with active ulcerative colitis of Crohn's disease. Gut. 1989;30:835-838.
19. Ligumsky M, Simon PL, Karmeli F, et al. Role of interleukin 1 in inflammatory bowel disease-enhanced production during active disease. Gut. 1990;31:686-689.
20. Brynskov J, Tvede N, Andersen CB, et al. Increased concentrations of interleukin 1 beta, interleukin-2, and soluble interleukin-2 receptors in endoscopical mucosal biopsy specimens with active inflammatory bowel disease. Gut. 1992;33:55-58.
21. Hirota SA, Ng J, LuengA, et al.NLRP3 inflammasome plays a key role in the regulation of intestinal homeostasis. Inflamm Bowel Dis. 2010;17:1359-1372.
22. Zaki MH, Boyd KL, Vogel P, et al. The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis. Immunity. 2010;32:379-391.
23. Villani AC, Lemire M, Fortin G, et al. Common variants in the NLRP3 region contribute to Crohn's disease susceptibility. Nat Genet. 2009;41:71-76.
24. Strober W, Fuss I, Mannon P. The fundamental basis of inflammatory bowel disease. J Clin Invest. 2007;117:514-521.
25. Swidsinski A, Ladhoff A, Pernthaler A, et al. Mucosal flora in inflammatory bowel disease. Gastroenterology. 2002;122:44-54.
26. Moussata D, Goetz M, Gloeckner A, et al. Confocal laser endomicroscopy is a new imaging modality for recognition of intramucosal bacteria in inflammatory bowel disease in vivo. Gut. 2011;60:26-33.
27. Keita AV, Salim SY, Jiang T, et al. Increased uptake of non-pathogenic E. coli via the follicle-associated epithelium in longstanding ileal Crohn's disease. J Pathol. 2008;215:135-144.
28. Duchmann R, Kaiser I, Hermann E, et al, Meyer zum Buschenfelde KH. Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease (IBD). Clin Exp Immunol. 1995;102:448-455.
29. Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol. 2009;9:799-809.
30. Guan Y, Watson AJ, Marchiando AM, et al. Redistribution of the tight junction protein ZO-1 during physiological shedding of mouse intestinal epithelial cells. Am J Physiol Cell Physiol. 2011;300:C1404-C1414.
31. Kiesslich R, Goetz M, Angus EM, et al. Identification of epithelial gaps in human small and large intestine by confocal endomicroscopy. Gastroenterology. 2007;133:1769-1778.
32. Liu JJ, Madsen KL, Boulanger P, et al. Mind the gaps: confocal endomicroscopy showed increased density of small bowel epithelial gaps in inflammatory bowel disease. J Clin Gastroenterol. 2011;45:240-245.
33. Giltner CL, van Schaik EJ, Audette GF, et al. The Pseudomonas aeruginosa type IV pilin receptor binding domain functions as an adhesin for both biotic and abiotic surfaces. Mol Microbiol. 2006;59:1083-1096.
34. Kilimann KV, Hartmann C, Vogel RF, et al. Differential inactivation of glucose- and glutamate dependent acid resistance of Escherichia coli TMW 2.497 by high-pressure treatments. Syst Appl Microbiol. 2005;28:663-671.
35. Dupaul-Chicoine J, Yeretssian G, Doiron K, et al. Control of intestinal homeostasis, colitis, and colitis-associated colorectal cancer by the inflammatory caspases. Immunity. 2010;32:367-378.
36. Limpanussorn J, Simon L, Dayan AD. Transepithelial transport of large particles in rat: a new model for the quantitative study of particle uptake. J Pharm Pharmacol. 1998;50:753-760.
37. Liu JJ, Rudzinski JK, Mah SJ, et al. Epithelial gaps in a rodent model of inflammatory bowel disease: a quantitative validation study. Clin Transl Gastroenterol. 2011;2:doi:10.1038/ctg.2011.2.
38. Mariathasan S, Weiss DS, Newton K, et al. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature. 2006;440:228-232.
39. Garcia-Calvo M, Peterson EP, Leiting B, et al. Inhibition of human caspases by peptide-based and macromolecular inhibitors. J Biol Chem. 1998;273:32608-32613.
40. Weiser MM, Ryzowicz S, Soroka CJ, et al. Synthesis of intestinal basement membrane. Immunol Invest. 1989;18:417-430.
41. Arlehamn CS, Evans TJ. Pseudomonas aeruginosa pilin activates the inflammasome. Cell Microbiol. 2011;13:388-401.
42. Nazli A, Yang PC, Jury J, et al. Epithelia under metabolic stress perceive commensal bacteria as a threat. Am J Pathol. 2004;164:947-957.
43. Leonard F, Collnot EM, Lehr CM. A three-dimensional coculture of enterocytes, monocytes and dendritic cells to model inflamed intestinal mucosa in vitro. Mol Pharm. 2010;7:2103-2119.
44. Marchiando AM, Shen L, Graham WV, et al. The epithelial barrier is maintained by in vivo tight junction expansion during pathologic intestinal epithelial shedding. Gastroenterology. 2011;140:1208-1218 e1-2.
45. Kummer JA, Broekhuizen R, Everett H, et al. Inflammasome components NALP 1 and 3 show distinct but separate expression profiles in human tissues suggesting a site-specific role in the inflammatory response. J Histochem Cytochem. 2007;55:443-452.
46. Zaki MH, Lamkanfi M, Kanneganti TD. The Nlrp3 inflammasome: contributions to intestinal homeostasis. Trends Immunol. 2011;32:171-179.
47. Liu Z, Zaki MH, Vogel P, et al. Role of inflammasomes in host defense against Citrobacter rodentium infection. J Biol Chem. 2012;287:16955-16964.
48. Siegmund B, Lehr HA, Fantuzzi G, et al. IL-1 beta -converting enzyme (caspase-1) in intestinal inflammation. Proc Natl Acad Sci USA. 2001;98: 13249-13254.
49. Bauer C, Loher F, Dauer M, et al. The ICE inhibitor pralnacasan prevents DSS-induced colitis in C57BL/6 mice and suppresses IP-10 mRNA but not TNF-alpha mRNA expression. Dig Dis Sci. 2007;52:1642-1652.
50. Allen IC, TeKippe EM, Woodford RM, et al. The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitis-associated cancer. J Exp Med. 2010;207:1045-1056.