Epithelial Cell Shedding and Barrier Function: A Matter of Life and Death at the Small Intestinal Villus Tip

Veterinary Pathology

Volumn 52, Issue 3, 2015, Pages 445-455

  Williams, J M ^a   Duckworth, C A ^a   Burkitt, M D ^a   Watson, A J M ^b   Campbell, B J ^a   Pritchard, D M ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

bacterial; digestive tract; genetically engineered mice; imaging; immunohistochemistry; immunologic; inflammation; nutritional

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); MUS;

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TUMOR NECROSIS FACTOR;

ANIMAL; APOPTOSIS; CYTOLOGY; HUMAN; INTESTINE MUCOSA; MICROVILLUS; MOUSE; PATHOLOGY; PHYSIOLOGY; SMALL INTESTINE;

ANIMALS; APOPTOSIS; HUMANS; INTESTINAL MUCOSA; INTESTINE, SMALL; MICE; MICROVILLI; NF-KAPPA B; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84930173219     PISSN: 03009858     EISSN: 15442217     Source Type: Journal    
DOI: 10.1177/0300985814559404     Document Type: Article

References (85)

1. Arrieta MC,Madsen K,Doyle J, et al.Reducing small intestinal permeability attenuates colitis in the IL10 gene-deficient mouse.Gut. 2009;58 (1): 41-48
2. Aziz Q,Doré J,Emmanuel A, et al.Gut microbiota and gastrointestinal health: current concepts and future directions.Neurogastroenterol Motil. 2013;25 (1): 4-15
3. Backhed F,Ding H,Wang T, et al.The gut microbiota as an environmental factor that regulates fat storage.Proc Natl Acad Sci USA. 2004;101 (44): 15718-15723
4. Barker N,van Es JH,Kuipers J, et al.Identification of stem cells in small intestine and colon by marker gene Lgr5.Nature. 2007;449 (7165): 1003-1007
5. Beaulieu JF.Differential expression of the VLA family of integrins along the crypt-villus axis in the human small intestine.J Cell Sci. 1992;102 (3): 427-436
6. Black RA,Rauch CT,Kozlosky CJ, et al.A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells.Nature. 1997;385 (6618): 729-733
7. Blikslager AT.Life in the gut without oxygen: adaptive mechanisms and inflammatory bowel disease.Gastroenterology. 2008;134 (1): 346-348
8. Brown CC,Baker DC,Barker IKPathology of Domestic Animals. 5th ed. Edinburgh, UK: Elsevier Saunders; 2007:69–78.Maxie MG, ed. Edinburgh, UK: Elsevier Saunders; 2007:69-78.
9. Bullen TF,Forrest S,Campbell F, et al.Characterization of epithelial cell shedding from human small intestine.Lab Invest. 2006;86 (10): 1052-1063
10. Burrin DG,Stoll B,Guan X, et al.Glucagon-like peptide 2 dose-dependently activates intestinal cell survival and proliferation in neonatal piglets.Endocrinology. 2005;146 (1): 22-32
11. Cani PD,Amar J,Iglesias MA, et al.Metabolic endotoxemia initiates obesity and insulin resistance.Diabetes. 2007;56 (7): 1761-1772
12. Casellas F,Aguade S,Soriano B, et al.Intestinal permeability to Tc-99m-diethylenetriaminopentaacetic acid in inflammatory bowel-disease.Am J Gastroenterol. 1986;81 (9): 767-770
13. Cheng H,Leblond CP.Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine: V. Unitarian theory of the origin of the four epithelial cell types.Am J Anat. 1974;141 (4): 537-561
14. Coopersmith CM,Stromberg PE,Davis CG, et al.Sepsis from Pseudomonas aeruginosa pneumonia decreases intestinal proliferation and induces gut epithelial cell cycle arrest.Crit Care Med. 2003;31 (6): 1630-1637
15. Coopersmith CM,Stromberg PE,Dunne WM, et al.Inhibition of intestinal epithelial apoptosis and survival in a murine model of pneumonia-induced sepsis.JAMA. 2002;287 (13): 1716-1721
16. Crouser ED,Julian MW,Weinstein DM, et al.Endotoxin-induced ileal mucosal injury and nitric oxide dysregulation are temporally dissociated.Am J Respir Crit Care Med. 2000;161 (5): 1705-1712
17. de Silva PSA,Nguyen DD,Sauk J, et al.Long-term outcome of a third anti-TNF monoclonal antibody after the failure of two prior anti-TNFs in inflammatory bowel disease.Aliment Pharmacol Ther. 2012;36 (5): 459-466
18. Deitch EA,Berg R,Specian R.Endotoxin promotes the translocation of bacteria from the gut.Arch Surg. 1987;122 (2): 185-190
19. Deitch EA,Specian RD,Berg RD.Endotoxin-induced bacterial translocation and mucosal permeability: role of xanthine oxidase, complement activation, and macrophage products.Crit Care Med. 1991;19 (6): 785-791
20. Duckworth CA,Watson AJ.Analysis of epithelial cell shedding and gaps in the intestinal epithelium.Methods Mol Biol. 2011;763:105-114
21. Everard A,Belzer C,Geurts L, et al.Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity.Proc Natl Acad Sci USA. 201 3;110 (22): 9066-9071
22. Foster DM,Stauffer SH,Stone MR, et al.Proteasome inhibition of pathologic shedding of enterocytes to defend barrier function requires X-linked inhibitor of apoptosis protein and nuclear factor kappaB.Gastroenterology. 2012;143 (1): 133-144
23. Fouquet S,Lugo-Martinez VH,Faussat AM, et al.Early loss of E-cadherin from cell-cell contacts is involved in the onset of Anoikis in enterocytes.J Biol Chem. 2004;279 (41): 43061-43069
24. Gadjeva M,Wang Y,Horwitz BH.NF-κB p50 and p65 subunits control intestinal homeostasis.Eur J Immunol. 2007;37 (9): 2509-2517
25. Gamer LW,Nove J,Rosen V.Return of the Chalones.Dev Cell. 2003;4 (2): 143-144
26. Garside P,Bunce C,Tomlinson RC, et al.Analysis of enteropathy induced by tumour necrosis factor alpha.Cytokine. 1993;5 (1): 24-30
27. Gatt M,Reddy BS,Macfie J.Review article: bacterial translocation in the critically ill—evidence and methods of prevention.Aliment Pharmacol Ther. 2007;25 (7): 741-757
28. Gelberg HBPathologic Basis of Veterinary Disease. 4th ed. St Louis, MO: Elsevier Mosby; 2007:342–360.McGavin MDZachary JF, ed. St Louis, MO: Elsevier Mosby; 2007:342-360.
29. Guan Y,Watson AJ,Marchiando AM, et al.Redistribution of the tight junction protein ZO-1 during physiologic shedding of mouse intestinal epithelial cells.Am J Physiol Cell Physiol. 201 1;300 (6): C1404-C1414
30. Guma M,Stepniak D,Shaked H, et al.Constitutive intestinal NF-kappaB does not trigger destructive inflammation unless accompanied by MAPK activation.J Exp Med. 2011;208 (9): 1889-1900
31. Han H,Iwanaga T,Fujita T.Species-differences in the process of apoptosis in epithelial cells of the small intestine: an ultrastructural and cytochemical study of luminal cell elements.Arch Histol Cytol. 1993;56 (1): 83-90
32. Han X,Fink MP,Yang R, et al.Increased iNOS activity is essential for intestinal epithelial tight junction dysfunction in endotoxemic mice.Shock. 2004;21 (3): 261-270
33. Ikeda H,Suzuki Y,Suzuki M, et al.Apoptosis is a major mode of cell death caused by ischaemia and ischaemia/reperfusion injury to the rat intestinal epithelium.Gut. 1998;42 (4): 530-537
34. Jackson GDF,Dai W,Sewell WA.Bile mediates intestinal pathology in endotoxemia in rats.Infect Immun. 2000;68 (8): 4714-4719
35. Johansson ME,Sjovall H,Hansson GC.The gastrointestinal mucus system in health and disease.Nat Rev Gastroenterol Hepatol. 2013;10 (6): 352-361
36. Julian MW,Bao S,Knoell DL, et al.Intestinal epithelium is more susceptible to cytopathic injury and altered permeability than the lung epithelium in the context of acute sepsis.Int J Exp Pathol. 2011;92 (5): 366-376
37. Kaur P,Potten CS.Circadian variation in migration velocity in small intestinal epithelium.Cell Tissue Kinet. 1986;19 (6): 591-599
38. Kiesslich R,Duckworth CA,Moussata D, et al.Local barrier dysfunction identified by confocal laser endomicroscopy predicts relapse in inflammatory bowel disease.Gut. 2012;61 (8): 1146-1153
39. Kiesslich R,Goetz M,Angus EM, et al.Identification of epithelial gaps in human small and large intestine by confocal endomicroscopy.Gastroenterology. 2007;133 (6): 1769-1778
40. Krause WJ.Intestinal mucosa of the platypus.Ornithorhynchus anatinus. Anat Rec. 1975;181 (2): 251-265
41. Lachat J-J,Gonçalves R.Influence of autonomic denervation upon the kinetics of the ileal epithelium of the rat.Cell Tissue Res. 1978;192 (2): 285-297
42. Lai CW,Sun TL,Lo W, et al.Shedding-induced gap formation contributes to gut barrier dysfunction in endotoxemia.J Trauma Acute Care Surg. 2013;74 (1): 203-213
43. Lau KS,Juchheim AM,Cavaliere KR, et al.In vivo systems analysis identifies spatial and temporal aspects of the modulation of TNF-alpha-induced apoptosis and proliferation by MAPKs.Sci Signal. 2011;4 (165): ra16
44. Lee JS.Epithelial cell extrusion during fluid transport in canine small intestine.Am J Physiol. 1977;232 (4): E408-E414
45. 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 (3): 240-245
46. Lobo SM,De Backer D,Sun QH, et al.Gut mucosal damage during endotoxic shock is due to mechanisms other than gut ischemia.J Appl Physiol. 2004;96 (2): 829-829
47. Madara JL.Maintenance of the macromolecular barrier at cell extrusion sites in intestinal epithelium: physiological rearrangement of tight junctions.J Membr Biol. 1990;116 (2): 177-184
48. 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 (4): 1208-1218
49. Marshman E,Booth C,Potten CS.The intestinal epithelial stem cell.BioEssays. 2002;24 (1): 91-98
50. Mayhew TM,Myklebust R,Whybrow A, et al.Epithelial integrity, cell death and cell loss in mammalian small intestine.Histol Histopathol. 1999;14 (1): 257-267
51. McAllister CS,Lakhdari O,Pineton de Chambrun G, et al.TLR3, TRIF, and caspase 8 determine double-stranded RNA-induced epithelial cell death and survival in vivo.J Immunol. 2013;190 (1): 418-427
52. Meddings J.What role does intestinal permeability have in IBD pathogenesis?.Inflamm Bowel Dis. 2008;14:S138-S139
53. Meyerholz DK,Stabel TJ,Ackermann MR, et al.Early epithelial invasion by Salmonella enterica Serovar Typhimurium DT104 in the swine ileum.Vet Pathol. 2002;39 (6): 712-720
54. Moore R,Carlson S,Madara JL.Villus contraction aids repair of intestinal epithelium after injury.Am J Physiol Gastrointest Liver Physiol. 1989;257 (2): G274-G283
55. 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 (3): 513-523
56. Nelson DE,Ihekwaba AE,Elliott M, et al.Oscillations in NF-kappaB signaling control the dynamics of gene expression.Science. 2004;306 (5696): 704-708
57. Nikitas G,Deschamps C,Disson O, et al.Transcytosis of Listeriamonocytogenes across the intestinal barrier upon specific targeting of goblet cell accessible E-cadherin.J Exp Med. 2011;208 (11): 2263-2277
58. Pendyala S,Walker JM,Holt PR.A high-fat diet is associated with endotoxemia that originates from the gut.Gastroenterology. 2012;142 (5): 1100-1101
59. Pentecost M,Otto G,Theriot JA, et al.Listeria monocytogenes invades the epithelial junctions at sites of cell extrusion.PLoS Pathog. 2006;2 (1): e3
60. Peschon JJ,Torrance DS,Stocking KL, et al.TNF receptor-deficient mice reveal divergent roles for p55 and p75 in several models of inflammation.J Immunol. 1998;160 (2): 943-952
61. Pfeffer K,Matsuyama T,Kundig TM, et al.Mice deficient for the 55 kd tumor necrosis factor receptor are resistant to endotoxic shock, yet succumb to L. monocytogenes infection.Cell. 1993;73 (3): 457-467
62. Piguet PF,Vesin C,Guo J, et al.TNF-induced enterocyte apoptosis in mice is mediated by the TNF receptor 1 and does not require p53.Eur J Immunol. 1998;28 (11): 3499-3505
63. Potten CS.A comprehensive study of the radiobiological response of the murine (BDF1) small intestine.Int J Radiat Biol. 1990;58 (6): 925-973
64. Rera M,Clark RI,Walker DW.Intestinal barrier dysfunction links metabolic and inflammatory markers of aging to death in Drosophila.Proc Natl Acad Sci USA. 2012;109 (52): 21528-21533
65. Ritsma L,Ellenbroek SIJ,Zomer A, et al.Intestinal crypt homeostasis revealed at single-stem-cell level by in vivo live imaging.Nature. 2014;507 (7492): 362-365
66. Roulis M,Armaka M,Manoloukos M, et al.Intestinal epithelial cells as producers but not targets of chronic TNF suffice to cause murine Crohn-like pathology.Proc Natl Acad Sci USA. 2011;108 (13): 5396-5401
67. Rupani B,Caputo FJ,Watkins AC, et al.Relationship between disruption of the unstirred mucus layer and intestinal restitution in loss of gut barrier function after trauma hemorrhagic shock.Surgery. 2007;141 (4): 481-489
68. Sato T,Clevers H.Growing self-organizing mini-guts from a single intestinal stem cell: mechanism and applications.Science. 2013;340 (6137): 1190-1194
69. Sherry B,Jue DM,Zentella A, et al.Characterization of high molecular weight glycosylated forms of murine tumor necrosis factor.Biochem Biophys Res Commun. 1990;173 (3): 1072-1078
70. Shi S,Wang H,Gao H, et al.Increased gap density predicts weakness of the epithelial barrier in vivo by confocal laser endomicroscopy in indomethacin-induced enteropathy.Dig Dis Sci. 2014;59 (7): 1398-1405
71. Shirkey TW,Siggers RH,Goldade BG, et al.Effects of commensal bacteria on intestinal morphology and expression of proinflammatory cytokines in the gnotobiotic pig.Exp Biol Med (Maywood). 2006;231 (8): 1333-1345
72. Sodhi C,Levy R,Gill R, et al.DNA attenuates enterocyte Toll-like receptor 4-mediated intestinal mucosal injury after remote trauma.Am J Physiol Gastrointest Liver Physiol. 2011;300 (5): G862-G873
73. Song HL,Lu S,Liu P.Tumor necrosis factor-alpha induces apoptosis of enterocytes in mice with fulminant hepatic failure.World J Gastroenterol. 2005;11 (24): 3701-3709
74. Song J,Wolf SE,Herndon DN, et al.Second hit post burn increased proximal gut mucosa epithelial cells damage.Shock. 2008;30 (2): 184-188
75. Steinbrecher KA,Harmel-Laws E,Sitcheran R, et al.Loss of epithelial RelA results in deregulated intestinal proliferative/apoptotic homeostasis and susceptibility to inflammation.J Immunol. 2008;180 (4): 2588-2599
76. Suzuki Y,Mori K,Iwanaga T.Intraepithelial gamma delta T cells are closely associated with apoptotic enterocytes in the bovine intestine.Arch Histol Cytol. 1997;60 (4): 319-328
77. Taylor CT,Dzus AL,Colgan SP.Autocrine regulation of epithelial permeability by hypoxia: role for polarized release of tumor necrosis factor alpha.Gastroenterology. 1998;114 (4): 657-668
78. van der Flier LG,Clevers H.Stem cells, self-renewal, and differentiation in the intestinal epithelium.Annu Rev Physiol. 2009;71 (1): 241-260
79. van Es JH,Clevers H.Paneth cells.Curr Biol. 20 14;24 (12): R547-R548
80. Vandenbroucke RE,Dejonckheere E,Van Hauwermeiren F, et al.Matrix metalloproteinase 13 modulates intestinal epithelial barrier integrity in inflammatory diseases by activating TNF.EMBO Mol Med. 2013;5 (7): 1000-1016
81. Vollmar B,Menger M.Intestinal ischemia/reperfusion: microcirculatory pathology and functional consequences.Langenbecks Arch Surg. 2011;396 (1): 13-29
82. Wang F,Wang F,Zou Z, et al.Active deformation of apoptotic intestinal epithelial cells with adhesion-restricted polarity contributes to apoptotic clearance.Lab Invest. 2011;91 (3): 462-471
83. Watson AJ,Chu S,Sieck L, et al.Epithelial barrier function in vivo is sustained despite gaps in epithelial layers.Gastroenterology. 2005;129 (3): 902-912
84. Williams JM,Duckworth CA,Watson AJ, et al.A mouse model of pathological small intestinal epithelial cell apoptosis and shedding induced by systemic administration of lipopolysaccharide.Dis Model Mech. 2013;6 (6): 1388-1399
85. Wu S,Rhee KJ,Zhang M, et al.Bacteroides fragilis toxin stimulates intestinal epithelial cell shedding and gamma-secretase-dependent E-cadherin cleavage.J Cell Sci. 2007;120 (pt 11): 1944-1952