Age-associated modifications of intestinal permeability and innate immunity in human small intestine

Clinical Science

Volumn 129, Issue 7, 2015, Pages 515-527

  Man, Angela L ^a   Bertelli, Eugenio ^b   Rentini, Silvia ^c   Regoli, Mari ^b   Briars, Graham ^d   Marini, Mario ^c   Watson, Alastair J M ^a,e   Nicoletti, Claudio ^a  

^a INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^b UNIVERSITY OF SIENA   (Italy)

^c UNIVERSITY HOSPITAL OF SIENA   (Italy)

^d NORFOLK AND NORWICH UNIVERSITY HOSPITAL   (United Kingdom)

^e UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

Aging; Infection; Innate immunity; Interleukin 6; Intestinal permeability; Intestine

Indexed keywords

CD40 ANTIGEN; CD86 ANTIGEN; CLAUDIN 2; CYTOKERATIN; FLAGELLIN; GAMMA INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; JUNCTIONAL ADHESION MOLECULE; MESSENGER RNA; OCCLUDIN; PROBIOTIC AGENT; PROTEIN ZO1; TOLL LIKE RECEPTOR 5; TUMOR NECROSIS FACTOR ALPHA; CULTURE MEDIUM; CYTOKINE;

ADULT; AGED; AGING; ARTICLE; CELL DIFFERENTIATION; CHILD; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DENSITOMETRY; ENZYME LINKED IMMUNOSORBENT ASSAY; EX VIVO STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INNATE IMMUNITY; INTESTINAL PERMEABILITY; INTESTINE EPITHELIUM CELL; INTESTINE FUNCTION; MICROSCOPY; ORGAN CULTURE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHOOL CHILD; SMALL INTESTINE; TERMINAL ILEUM; TISSUE LEVEL; UPREGULATION; WESTERN BLOTTING; AGE; BIOPSY; CACO 2 CELL LINE; CHEMISTRY; CULTURE MEDIUM; ENDOSCOPY; EPITHELIUM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; ILEUM; IMPEDANCE; METABOLISM; ORGAN CULTURE TECHNIQUE; YOUNG ADULT;

ADULT; AGE FACTORS; AGED; BIOPSY; CACO-2 CELLS; CHILD; CULTURE MEDIA, CONDITIONED; CYTOKINES; DENDRITIC CELLS; ELECTRIC IMPEDANCE; ENDOSCOPY; EPITHELIUM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; ILEUM; IMMUNITY, INNATE; ORGAN CULTURE TECHNIQUES; YOUNG ADULT;

EID: 84951907634     PISSN: 01435221     EISSN: 14708736     Source Type: Journal    
DOI: 10.1042/CS20150046     Document Type: Article

References (40)

1. Ershler, W.B. (2003) Biological interactions of aging and anemia: a focus on cytokines. J. Am. Geriatr. Soc. 51, S18-S21
2. Gardner, I.D. (1980) The effect of aging on susceptibility to infection. Rev. Infect. Dis. 2, 801-810
3. Franceschi, C. and Campisi, J. (2014) Chronic inflammation (inflammageing) and its potential contribution to age-associated diseases. J. Gerontol. 69 Suppl1, S4-S9
4. Guigoz, Y., Dore, J. and Schiffrin, E.J. (2008) The inflammatory status of old age can be nurtured from the intestinal environment. Curr. Opin. Clin. Nutr. Metab. Care 11, 13-20
5. Man, A.L., Gicheva, N. and Nicoletti, C. (2014) The impact of ageing on the intestinal epithelial barrier and immune system. Cell Immunol. 289, 112-118
6. Turner, J.R. (2009) Intestinal mucosal barrier function inhealth and disease. Nat. Rev. Immunol. 9, 799-809
7. Bleau, C., Karelis, A.D., St-Pierre, D.H. and Lamontagne, L. (2014) Crosstalk between intestinal microbiota, adipose tissue and skeletal muscle as an early event in systemic low-grade inflammation and the development of obesity and diabetes. Diabetes Metab. Res. Rev., doi:10.1002/dmrr.2617
8. Maes, M., Kubera, M. and Leunis, J.C. (2008) The gut-brain barrier in major depression: intestinal mucosal dysfunction with an increased translocation of LPS from gram negative enterobacteria (leaky gut) plays a role in the inflammatory pathophysiology of depression. Neuro. Endocrinol. Lett. 9, 117-124
9. Forsyth, C.B., Shannon, K.M., Kordower, J.H., Voigt, R.M., Shaikh, M., Jaglin, J.A., Estes, J.D., Dodiya, H.B. and Keshavarzian, A. (2011) Increased intestinal permeability correlates with sigmoid mucosa alpha-synuclein staining and endotoxin exposure markers in early Parkinson's disease. PLoS One 6, e28032
10. Vrieze, A., de Groot, P.F., Kootte, R.S., Knaapen, M., van Nood, E. and Nieuwdorp, M. (2013) Fecal transplant: a safe and sustainable clinical therapy for restoring intestinal microbial balance in human disease? Best Pract. Res. Clin. Gastroenterol. 27, 127-137
11. Rera, M., Clark, R.I. and Walker, D.W. (2012) Intestinal barrier dysfunction links metabolic and inflammatory markers of aging to death in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 109, 21528-21533
12. Rimoldi, M., Chieppa, M., Salucci, V., Avogadri, F., Sonzogni, A., Sampietro, G.M., Nespoli, A., Viale, G., Allavena, P. and Rescigno, M. (2005) Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat. Immunol. 6, 507-514
13. Iliev, I.D., Mileti, E., Matteoli, G., Chieppa, M. and Rescigno, M. (2009) Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal. Immunol. 2, 340-350
14. Mowat, A.M. (2003) Anatomical basis of tolerance and immunity to intestinal antigens. Nat. Rev. Immunol. 4, 331-341
15. Sansonetti, P.J. (2004) War and peace at mucosal surfaces. Nat. Rev. Immunol. 4, 953-964
16. Greenwood-Van Meerveld, B., Tyler, K. and Keith, Jr, J.C. (2000) Recombinant human interleukin-1 modulates ion transport and mucosal inflammation in the small intestine and colon. Lab. Invest. 80, 1269-1280
17. Hicks, S., Candy, D.C. and Phillips, A.D. (1996) Adhesion of enteroaggregative Escherichia coli to pediatric intestinal mucosa in vitro. Infect Immun. 64, 4751-4760
18. El Asmar, R., Panigrahi, P., Bamford, P., Berti, I., Not, T., Coppa, G.V., Catassi, C. and Fasano, A. (2002) A. Host-dependent zonulin secretion causes the impairment of the small intestine barrier function after bacterial exposure. Gastroenterology 123, 1607-1615
19. Schuller, S., Lucas, M., Kaper, J.B., Girón, J.A. and Phillips, A.D. (2009) The ex vivo response of human intestinal mucosa to enteropathogenic E. coli infection. Cell Microbiol. 11, 1607-1615
20. Siddiqui, K.R., Laffon, S. and Powrie, F. (2010) E-cadherin marks a subset of inflammatory dendritic cells that promote T cell-mediated colitis. Immunity 23, 557-567
21. Hollander, D. and Tarnawski, H. (1985) Aging-associated increase in intestinal absorption of macromolecules. Gerontology 31, 133-137
22. Suzuki, T., Yoshinaga, N. and Tanabe, S. (2011) Interleukin-6 (IL-6) regulates Claudin-2 expression and tight junction permeability in intestinal epithelium. J. Biol. Chem. 286, 31263-31271
23. Van Itallie, C.M., Holmes, J., Bridges, A., Gookin, J.L., Coccaro, M.R., Proctor, W., Colegio, O.R. and Anderson, J.M. (2008) The density of small tight junction pores varies among cell types and is increased by expression of claudin-2. J. Cell Sci. 121, 298-305
24. Tran, L. and Greenwood-Van Meerveld, B. (2013) Age-associated remodeling of the intestinal epithelial barrier. J. Gerontol. A Biol. Sci. Med. Sci. 68, 1045-1056
25. Eckmann, L., Kagnoff, M.F. and Fierer, J. (1993) Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infect Immun. 61, 4569-4574
26. Pagnini, C., Saeed, R., Bamias, G., Arseneau, K.O., Pizarro, T.T. and Cominelli, F. (2010) Probiotics promote gut health through stimulation of epithelial innate immunity. Proc. Natl. Acad. Sci. U.S.A. 107, 454-459
27. Mann, E.R., Bernardo, D., English, N.R., Landy, J., Al-Hassi, H.O., Peake, S.T., Man, R., Elliott, T.R., Spranger, H., Lee, G.H. et al. (2015) Compartment-specific immunity in the human gut: properties and functions of dendritic cells in the colon versus the ileum. Gut, doi: 10.1136/gutjnl-2014-307916
28. Al-Sadi, R., Ye, D., Boivin, M., Guo, S., Hashimi, M., Ereifej, L. and Ma, T.Y. (2014) Interleukin-6 modulation of intestinal epithelial tight junction permeability is mediated by JNK pathway activation of claudin-2 gene. PLoS One 9, e85345
29. Heller, F., Florian, P., Bojarski, C., Richter, J., Christ, M., Hillenbrand, B., Mankertz, J., Gitter, A.H., Bürgel, N., Fromm, M. et al. (2015) Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology 129, 550-564
30. Fujino, S., Andoh, A., Bamba, S., Ogawa, A., Hata, K., Araki, Y., Bamba, T. and Fujiyama, Y. (2003) Increased expression of interleukin 17 in inflammatory bowel disease. Gut 52, 65-70
31. Mankertz, J., Amasheh, M., Krug, S. M, Fromm, A., Amasheh, S., Hillenbrand, B., Tavalali, S., Fromm, M. and Schulzke, J.D. (2009) TNF-a up-regulates claudin-2 expression in epithelial HT-29/B6 cells via phosphatidylinositol-3-kinase signaling. Cell Tissue Res. 336, 67-77
32. Ershler, W.B. and Keller, ET. (2000) Age-associated increased interleukin-6 gene expression, late-life diseases, and frailty. Annu. Rev. Med. 51, 245-270
33. Roubenoff, R. (2014) The cytokine for gerontologist has some company. J. Gerontol. A Biol. Sci. Med. Sci. 69, 163-164
34. Sanders, J.L., Ding, V., Arnold, A.M., Kaplan, R.C., Cappola, A.R., Kizer, J.R., Boudreau, R.M., Cushman, M. and Newman, A.B. (2014) Do changes in circulating biomarkers track with each other and with functional changes in older adults? J. Gerontol. A Biol. Sci. Med. Sci. 68, 174-181
35. Ivanov, I.I., Atarashi, K., Manel, N., Brodie, E.L., Shima, T., Karaoz, U., Wei, D., Goldfarb, K.C., Santee, C.A., Lynch, S.V. et al. (2009) Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139, 485-498
36. Claesson, J., Jeffery, IB., Conde, S., Power, S.E., O'Connor, E.M., Cusack, S., Harris, H.M., Coakley, M., Lakshminarayanan, B., O'Sullivan, O. et al. (2012) Gut microbiota composition correlates with diet and health in the elderly. Nature 488, 178-184
37. Kimura, A. and Kishimoto, T. (2010) IL-6: regulator of Treg/Th17 balance. Eur. J. Immunol. 40, 830-835
38. Schmitt, V., Rink, L. and Uciechowski, P. (2013) The Th17/Treg balance is disturbed during aging. Exp. Gerontol. 48, 1379-1386
39. Perona-Wright, G., Jenkins, S.J., O'Connor, R.A., Zienkiewicz, D., McSorley, H.J., Maizels, R.M., Anderton, S.M. and MacDonald, AS. (2009) A pivotal role for CD40-mediated IL-6 production by dendritic cells during IL-17 induction in vivo. J. Immunol. 182, 2808-2815
40. Sánchez-Muñoz, F., Fonseca-Camarillo, G., Villeda-Ramírez, M.A., Miranda-Pérez, E., Mendivil, E.J., Barreto-Zúñiga, R., Uribe, M., Bojalil, R., Domínguez-López, A. and Yamamoto-Furusho, J.K. (2011) Transcript levels of toll-like receptors 5, 8 and 9 correlate with inflammatory activity in ulcerative colitis. BMC Gastroenterol. 11, 138-142