Human gastric epithelial cells contribute to gastric immune regulation by providing retinoic acid to dendritic cells

Mucosal Immunology

Volumn 8, Issue 3, 2015, Pages 533-544

  Bimczok, D ^a   Kao, J Y ^b   Zhang, M ^b   Cochrun, S ^a   Mannon, P ^a   Peter, S ^a   Wilcox, C M ^a   Monkemuller K E ^a   Harris, P R ^c   Grams, J M ^d   Stahl, R D ^d   Smith, P D ^a,e   Smythies, L E ^a  

^a and Clinical Center   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^d University of Alabama at Birmingham   (United States)

^e BIRMINGHAM VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; CD103 ANTIGEN; RETINOIC ACID; RETINOL;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; DENDRITIC CELL; DISEASE COURSE; ENZYME ACTIVITY; EPITHELIUM CELL; GENE DISRUPTION; GENE EXPRESSION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREGULATION; IN VITRO STUDY; MALE; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STOMACH EPITHELIUM; ANIMAL; C57BL MOUSE; COCULTURE; FEMALE; HELICOBACTER INFECTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MUCOSAL IMMUNITY; PATHOGENICITY; PATHOLOGY; PRIMARY CELL CULTURE; STOMACH MUCOSA;

ALDEHYDE DEHYDROGENASE; ANIMALS; COCULTURE TECHNIQUES; EPITHELIAL CELLS; FEMALE; GASTRIC MUCOSA; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; IMMUNITY, MUCOSAL; MICE; MICE, INBRED C57BL; MONOCYTES; PRIMARY CELL CULTURE; TRETINOIN; VITAMIN A;

EID: 84928893261     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2014.86     Document Type: Article

References (60)

1. Atherton, J.C. & Blaser, M.J. Coadaptation of Helicobacter pylori and humans: ancient history, modern implications. J. Clin. Invest. 119, 2475-2487 (2009).
2. Bimczok, D., Grams, J.M., Stahl, R.D., Waites, K.B., Smythies, L.E. & Smith, P.D. Stromal regulation of human gastric dendritic cells restricts the Th1 response to Helicobacter pylori. Gastroenterology 141, 929-938 (2011).
3. Yang, I., Nell, S. & Suerbaum, S. Survival in hostile territory: the microbiota of the stomach. FEMS Microbiol. Rev. 37, 736-761 (2013).
4. Bik, E.M. et al. Molecular analysis of the bacterial microbiota in the human stomach. Proc. Natl. Acad. Sci. USA 103, 732-737 (2006).
5. Iwata, M. Retinoic acid production by intestinal dendritic cells and its role in T-cell trafficking. Semin. Immunol. 21, 8-13 (2009).
6. Agace, W. W. & Persson, E. K. Howvitamin Ametabolizing dendritic cells are generated in the gut mucosa. Trends Immunol. 33, 42-48 (2012).
7. Pino-Lagos, K., Benson, M.J. & Noelle, R.J. Retinoic acid in the immune system. Ann. N.Y. Acad. Sci 1143, 170-187 (2008).
8. del Rio, M.L., Bernhardt, G., Rodriguez-Barbosa, J.I. & Forster, R. Development and functional specialization of CD103+ dendritic cells. Immunol. Rev. 234, 268-281 (2010).
9. Gyongyosi, A. et al. RDH10, RALDH2, and CRABP2 are required components of PPARgamma-directed ATRA synthesis and signaling in human dendritic cells. J. Lipid Res. 54, 2458-2474 (2013).
10. Edele, F. et al. Cutting edge: instructive role of peripheral tissue cells in the imprinting of Tcell homing receptor patterns. J. Immunol. 181, 3745-3749 (2008).
11. Ohoka, Y., Yokota-Nakatsuma, A., Maeda, N., Takeuchi, H. & Iwata, M. Retinoic acid and GM-CSF coordinately induce retinal dehydrogenase 2 (RALDH2) expression through cooperation between the RAR/RXR complex and Sp1 in dendritic cells. PLoS One 9, e96512 (2014).
12. Matsumoto, M., Yokoyama, H., Suzuki, H., Shiraishi-Yokoyama, H. & Hibi, T. Retinoic acid formation from retinol in the human gastric mucosa: role of class IV alcohol dehydrogenase and its relevance to morphological changes. Am. J. Physiol. Gastrointest. Liver Physiol. 289, G429-G433 (2005).
13. Jaensson-Gyllenback, E. et al. Bile retinoids imprint intestinal CD103+ dendritic cells with the ability to generate gut-tropic T cells. Mucosal Immunol 4, 438-447 (2011).
14. Lee, S.A., Belyaeva, O.V., Wu, L. & Kedishvili, N.Y. Retinol dehydrogenase 10 but not retinol/sterol dehydrogenase(s) regulates the expression of retinoic acid-responsive genes in human transgenic skin raft culture. J. Biol. Chem. 286, 13550-13560 (2011).
15. Balmer, J.E. & Blomhoff, R. Gene expression regulation by retinoic acid. J. Lipid Res. 43, 1773-1808 (2002).
16. Yan, Z.H., Noonan, S., Nagy, L., Davies, P.J. & Stein, J.P. Retinoic acid induction of the tissue transglutaminase promoter is mediated by a novel response element. Mol. Cell Endocrinol. 120, 203-212 (1996).
17. Chiocca, E.A., Davies, P.J. & Stein, J.P. The molecular basis of retinoic acid action. Transcriptional regulation of tissue transglutaminase gene expression in macrophages. J. Biol. Chem. 263, 11584-11589 (1988).
18. Gundemir, S., Colak, G., Tucholski, J. & Johnson, G.V. Transglutaminase 2: a molecular Swiss army knife. Biochim. Biophys. Acta. 1823, 406-419 (2012).
19. McDonald, K.G. et al. Epithelial expression of the cytosolic retinoid chaperone cellular retinol binding protein II is essential for in vivo imprinting of local gut dendritic cells by lumenal retinoids. Am. J. Pathol. 180, 984-997 (2012).
20. Borel, P. et al. Processing of vitamin A and E in the human gastrointestinal tract. Am. J. Physiol. Gastrointest. Liver Physiol. 280, G95-G103 (2001).
21. Napoli, J.L. Biosynthesis and metabolism of retinoic acid: roles of CRBP and CRABP in retinoic acid: roles of CRBP and CRABP in retinoic acid homeostasis. J. Nutr. 123 (2 Suppl), 362-366 (1993).
22. O'Byrne, S.M. & Blaner, W.S. Retinol and retinyl esters: biochemistry and physiology. J. Lipid Res. 54, 1731-1743 (2013).
23. Iliev, I.D. et al. Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells. Gut 58, 1481-1489 (2009).
24. Wagner, M., Han, B. & Jessell, T.M. Regional differences in retinoid release from embryonic neural tissue detected by an in vitro reporter assay. Development 116, 55-66 (1992).
25. Uematsu, S. et al. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat. Immunol. 9, 769-776 (2008).
26. Bimczok, D. et al. Human primary gastric dendritic cells induce a Th1 response to H. pylori. Mucosal Immunol 3, 260-269 (2010).
27. Meredith, M.M. et al. Expression of the zinc finger transcription factor zDC (Zbtb46, Btbd4) defines the classical dendritic cell lineage. J. Exp. Med. 209, 1153-1165 (2012).
28. Yokota, A. et al. GM-CSF and IL-4 synergistically trigger dendritic cells to acquire retinoic acid-producing capacity. Int. Immunol. 21, 361-377 (2009).
29. Iwata, M., Hirakiyama, A., Eshima, Y., Kagechika, H., Kato, C. & Song, S.Y. Retinoic acid imprints gut-homing specificity on Tcells. Immunity 21, 527-538 (2004).
30. Michetti, M., Kelly, C.P., Kraehenbuhl, J.P., Bouzourene, H. & Michetti, P. Gastric mucosal alpha(4)beta(7)-integrin-positive CD4 T lymphocytes and immune protection against helicobacter infection in mice. Gastroenterology 119, 109-118 (2000).
31. Segal, E.D., Lange, C., Covacci, A., Tompkins, L.S. & Falkow, S. Induction of host signal transduction pathways by Helicobacter pylori. Proc. Natl. Acad. Sci. USA 94, 7595-7599 (1997).
32. Bamford, K.B. et al. Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype. Gastroenterology 114, 482-492 (1998).
33. Harris, P.R. et al. Helicobacter pylori gastritis in children is associatedwith a regulatory T-cell response. Gastroenterology 134, 491-499 (2008).
34. Robinson, K. et al. Helicobacter pylori-induced peptic ulcer disease is associated with inadequate regulatory T cell responses. Gut 57, 1375-1385 (2008).
35. Serrano, C. et al. Downregulated Th17 responses are associated with reduced gastritis in Helicobacter pylori-infected children. Mucosal Immunol 6, 950-959 (2013).
36. Lampen, A., Meyer, S., Arnhold, T. & Nau, H. Metabolism of vitamin A and its active metabolite all-trans-retinoic acid in small intestinal enterocytes. J. Pharmacol. Exp. Ther. 295, 979-985 (2000).
37. McGrane, M.M. Vitamin A regulation of gene expression: molecular mechanism of a prototype gene. J Nutr. Biochem. 18, 497-508 (2007).
38. Tang, X.H. & Gudas, L.J. Retinoids, retinoic acid receptors, and cancer. Annu. Rev. Pathol 6, 345-364 (2011).
39. Strate, I., Min, T.H., Iliev, D. & Pera, E.M. Retinol dehydrogenase 10 is a feedback regulator of retinoic acid signalling during axis formation and patterning of the central nervous system. Development 136, 461-472 (2009).
40. Pinaire, J. et al. Identification of a retinoid receptor response element in the human aldehyde dehydrogenase-2 promoter. Alcohol Clin. Exp. Res. 27, 1860-1866 (2003).
41. Sun, C.M. et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204, 1775-1785 (2007).
42. Coombes, J.L. et al. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J. Exp. Med. 204, 1757-1764 (2007).
43. Iliev, I.D., Mileti, E., Matteoli, G., Chieppa, M. & Rescigno, M. Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal Immunol 2, 340-350 (2009).
44. Manicassamy, S. et al. Toll-like receptor 2-dependent induction of vitamin A-metabolizing enzymes in dendritic cells promotes Tregulatory responses and inhibits autoimmunity. Nat. Med 15, 401-409 (2009).
45. Szatmari, I. et al. PPARgamma controls CD1d expression by turning on retinoic acid synthesis in developing human dendritic cells. J. Exp. Med. 203, 2351-2362 (2006).
46. Nagy, T.A. et al. Helicobacter pylori induction of eosinophil migration is mediated by the cag pathogenicity island via microbial-epithelial interactions. Am. J. Pathol. 178, 1448-1452 (2011).
47. Harrison, E.H. Mechanisms of digestion and absorption of dietary vitamin A. Annu. Rev. Nutr. 25, 87-103 (2005).
48. Cassani, B., Villablanca, E.J., De Calisto, J., Wang, S. & Mora, J.R. Vitamin A and immune regulation: role of retinoic acid in gut-associated dendritic cell education, immune protection and tolerance. Mol. Aspects Med. 33, 63-76 (2012).
49. Watchmaker, P.B. et al. Comparative transcriptional and functional profiling defines conserved programs of intestinal DC differentiation in humans and mice. Nat. Immunol. 15, 98-108 (2014).
50. Robinson, P.W., Green, S.J., Carter, C., Coadwell, J. & Kilshaw, P.J. Studies on transcriptional regulation of the mucosal T-cell integrin alpha Ebeta7 (CD103). Immunology 103, 146-154 (2001).
51. Guilliams, M. et al. Skin-draining lymph nodes contain dermis-derived CD103(-) dendritic cells that constitutively produce retinoic acid and induce Foxp3(+) regulatory T cells. Blood 115, 1958-1968 (2010).
52. Epplein, M. et al. Helicobacter pylori prevalence and circulating micronutrient levels in a low-income United States population. Cancer Prev. Res. (Phila) 4, 871-878 (2011).
53. Ozturk, Y., Buyukgebiz, B., Arslan, N., Ozer, E. & Lebe, B. Serum vitamin A and total carotene concentrations in well-nourished children with Helicobacter pylori infection. J. Pediatr. Gastroenterol. Nutr. 36, 502-504 (2003).
54. Hu, K.W., Chen, F.H., Ge, J.F., Cao, L.Y. & Li, H. Retinoid receptors in gastric cancer: expression and influence on prognosis. Asian Pac. J. Cancer Prev. 13, 1809-1817 (2012).
55. Kim, J.H., Choi, Y.K., Kwon, H.J., Yang, H.K., Choi, J.H. & Kim, D.Y. Downregulation of gelsolin and retinoic acid receptor beta expression in gastric cancer tissues through histone deacetylase 1. J. Gastroenterol. Hepatol. 19, 218-224 (2004).
56. Smoot, D.T., Sewchand, J., Young, K., Desbordes, B.C., Allen, C.R. & Naab, T. A method for establishing primary cultures of human gastric epithelial cells. Methods Cell. Sci 22, 133-136 (2000).
57. Bimczok, D. et al. Helicobacter pylori infection inhibits phagocyte clearance of apoptotic gastric epithelial cells. J. Immunol. 190, 6626-6634 (2013).
58. Sun, X. et al. TLR2 mediates Helicobacter pylori-induced tolerogenic immune response in mice. PLoS One 8, e74595 (2013).
59. Pfaffl, M.W. A new mathematical model for relative quantification in realtime RT-PCR. Nucleic Acids Res. 29, e45 (2001).
60. Napoli, J.L. & Horst, R.L. Quantitative analyses of naturally occurring retinoids. Methods Mol. Biol. 89, 29-40 (1998).