Inflammation, innate immunity, and the intestinal stromal cell niche: Opportunities and challenges

Frontiers in Immunology

Volumn 6, Issue JUN, 2015, Pages

  Owens, Benjamin M J ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b SOMERVILLE COLLEGE   (United Kingdom)

Author keywords

Chronic inflammation; Intestinal inflammation; Intestinal innate immunity; Intestinal stromal cells; Stromal cells; Stromal immunology

Indexed keywords

COLLAGEN TYPE 6; COLONY STIMULATING FACTOR; CRYOPYRIN; CYTOKINE RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 33; LYMPHOTOXIN; MESSENGER RNA; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PODOPLANIN; PROSTAGLANDIN E2; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

BACTERIAL TRANSLOCATION; CELL METABOLISM; CELL POPULATION; DNA METHYLATION; ENTERITIS; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL MEMORY; IMMUNOREGULATION; INFLAMMATION; INFLAMMATORY BOWEL DISEASE; INNATE IMMUNITY; INTESTINE CELL; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; INTESTINE MUCOSA; MACROPHAGE; NATURAL KILLER CELL; REVIEW; RHEUMATOID ARTHRITIS; SALMONELLA; STROMA CELL; T LYMPHOCYTE; ULCERATIVE COLITIS;

EID: 84935064755     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00319     Document Type: Review

References (53)

1. Kain MJ, Owens BM. Stromal cell regulation of homeostatic and inflammatory lymphoid organogenesis. Immunology (2013) 140:12-21. doi: 10.1111/imm.12119.
2. Owens BM, Simmons A. Intestinal stromal cells in mucosal immunity and homeostasis. Mucosal Immunol (2013) 6:224-34. doi:10.1038/mi.2012.125.
3. Hornef MW, Fulde M. Ontogeny of intestinal epithelial innate immune responses. Front Immunol (2014) 5:474. doi:10.3389/fimmu.2014.00474.
4. Powell DW, Pinchuk IV, Saada JI, Chen X, Mifflin RC. Mesenchymal cells of the intestinal lamina propria. Annu Rev Physiol (2011) 73:213-37. doi:10.1146/annurev.physiol.70.113006.100646.
5. Owens BM, Steevels TA, Dudek M, Walcott D, Sun MY, Mayer A, et al. CD90(+) stromal cells are non-professional innate immune effectors of the human colonic mucosa. Front Immunol (2013) 4:307. doi:10.3389/fimmu.2013.00307.
6. Otte JM, Rosenberg IM, Podolsky DK. Intestinal myofibroblasts in innate immune responses of the intestine. Gastroenterology (2003) 124:1866-78. doi:10.1016/S0016-5085(03)00403-7.
7. Kim YG, Kamada N, Shaw MH, Warner N, Chen GY, Franchi L, et al. The Nod2 sensor promotes intestinal pathogen eradication via the chemokine CCL2-dependent recruitment of inflammatory monocytes. Immunity (2011) 34:769-80. doi:10.1016/j.immuni.2011.04.013.
8. Barrera CA, Pinchuk IV, Saada JI, Suarez G, Bland DA, Beswick E, et al. Class II MHC-expressing myofibroblasts play a role in the immunopathogenesis associated with staphylococcal enterotoxins. Ann N Y Acad Sci (2004) 1029:313-8. doi:10.1196/annals.1309.022.
9. Saada JI, Pinchuk IV, Barrera CA, Adegboyega PA, Suarez G, Mifflin RC, et al. Subepithelial myofibroblasts are novel nonprofessional APCs in the human colonic mucosa. J Immunol (2006) 177:5968-79. doi:10.4049/jimmunol.177.9.5968.
10. Beswick EJ, Johnson JR, Saada JI, Humen M, House J, Dann S, et al. TLR4 activation enhances the PD-L1-mediated tolerogenic capacity of colonic CD90+ stromal cells. J Immunol (2014) 193:2218-29. doi:10.4049/jimmunol.1203441.
11. Pinchuk IV, Saada JI, Beswick EJ, Boya G, Qiu SM, Mifflin RC, et al. PD-1 ligand expression by human colonic myofibroblasts/fibroblasts regulates CD4+ T-cell activity. Gastroenterology (2008) 135:e1-2. doi:10.1053/j.gastro.2008.07.016.
12. Brown M, Hughes KR, Moossavi S, Robins A, Mahida YR. Toll-like receptor expression in crypt epithelial cells, putative stem cells and intestinal myofibroblasts isolated from controls and patients with inflammatory bowel disease. Clin Exp Immunol (2014) 178:28-39. doi:10.1111/cei.12381.
13. Vicente-Suarez I, Larange A, Reardon C, Matho M, Feau S, Chodaczek G, et al. Unique lamina propria stromal cells imprint the functional phenotype of mucosal dendritic cells. Mucosal Immunol (2015) 8:141-51. doi:10.1038/mi.2014.51.
14. Griseri T, McKenzie BS, Schiering C, Powrie F. Dysregulated hematopoietic stem and progenitor cell activity promotes interleukin-23-driven chronic intestinal inflammation. Immunity (2012) 37:1116-29. doi:10.1016/j.immuni.2012.08.025.
15. Lukacs-Kornek V, Malhotra D, Fletcher AL, Acton SE, Elpek KG, Tayalia P, et al. Regulated release of nitric oxide by nonhematopoietic stroma controls expansion of the activated T cell pool in lymph nodes. Nat Immunol (2011) 12:1096-104. doi:10.1038/ni.2112.
16. Khan O, Headley M, Gerard A, Wei W, Liu L, Krummel MF. Regulation of T cell priming by lymphoid stroma. PLoS One (2011) 6:e26138. doi:10.1371/journal.pone.0026138.
17. Song-Zhao GX, Srinivasan N, Pott J, Baban D, Frankel G, Maloy KJ. Nlrp3 activation in the intestinal epithelium protects against a mucosal pathogen. Mucosal Immunol (2014) 7:763-74. doi:10.1038/mi.2013.94.
18. Nordlander S, Pott J, Maloy KJ. NLRC4 expression in intestinal epithelial cells mediates protection against an enteric pathogen. Mucosal Immunol (2014) 7:775-85. doi:10.1038/mi.2013.95.
19. Normand S, Delanoye-Crespin A, Bressenot A, Huot L, Grandjean T, Peyrin-Biroulet L, et al. Nod-like receptor pyrin domain-containing protein 6 (NLRP6) controls epithelial self-renewal and colorectal carcinogenesis upon injury. Proc Natl Acad Sci U S A (2011) 108:9601-6. doi:10.1073/pnas.1100981108.
20. El Marjou F, Janssen KP, Chang BH, Li M, Hindie V, Chan L, et al. Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis (2004) 39:186-93. doi:10.1002/gene.20042.
21. Armaka M, Apostolaki M, Jacques P, Kontoyiannis DL, Elewaut D, Kollias G. Mesenchymal cell targeting by TNF as a common pathogenic principle in chronic inflammatory joint and intestinal diseases. J Exp Med (2008) 205:331-7. doi:10.1084/jem.20070906.
22. Koliaraki V, Roulis M, Kollias G. Tpl2 regulates intestinal myofibroblast HGF release to suppress colitis-associated tumorigenesis. J Clin Invest (2012) 122:4231-42. doi:10.1172/JCI63917.
23. Peduto L, Dulauroy S, Lochner M, Späth GF, Morales MA, Cumano A, et al. Inflammation recapitulates the ontogeny of lymphoid stromal cells. J Immunol (2009) 182:5789-99. doi:10.4049/jimmunol.0803974.
24. Baptista AP, Olivier BJ, Goverse G, Greuter M, Knippenberg M, Kusser K, et al. Colonic patch and colonic SILT development are independent and differentially regulated events. Mucosal Immunol (2013) 6:511-21. doi:10.1038/mi.2012.90.
25. Onder L, Scandella E, Chai Q, Firner S, Mayer CT, Sparwasser T, et al. A novel bacterial artificial chromosome-transgenic podoplanin-cre mouse targets lymphoid organ stromal cells in vivo. Front Immunol (2011) 2:50. doi:10.3389/fimmu.2011.00050.
26. Roozendaal R, Mebius RE. Stromal cell-immune cell interactions. Annu Rev Immunol (2011) 29:23-43. doi:10.1146/annurev-immunol-031210-101357.
27. Driskell RR, Lichtenberger BM, Hoste E, Kretzschmar K, Simons BD, Charalambous M, et al. Distinct fibroblast lineages determine dermal architecture in skin development and repair. Nature (2013) 504:277-81. doi:10.1038/nature12783.
28. Bottini N, Firestein GS. Duality of fibroblast-like synoviocytes in RA: passive responders and imprinted aggressors. Nat Rev Rheumatol (2013) 9:24-33. doi:10.1038/nrrheum.2012.190.
29. Bechtel W, McGoohan S, Zeisberg EM, Müller GA, Kalbacher H, Salant DJ, et al. Methylation determines fibroblast activation and fibrogenesis in the kidney. Nat Med (2010) 16:544-50. doi:10.1038/nm.2135.
30. Li M, Riddle SR, Frid MG, El Kasmi KC, McKinsey TA, Sokol RJ, et al. Emergence of fibroblasts with a proinflammatory epigenetically altered phenotype in severe hypoxic pulmonary hypertension. J Immunol (2011) 187:2711-22. doi:10.4049/jimmunol.1100479.
31. McKaig BC, Hughes K, Tighe PJ, Mahida YR. Differential expression of TGF-beta isoforms by normal and inflammatory bowel disease intestinal myofibroblasts. Am J Physiol Cell Physiol (2002) 282:C172-82. doi:10.1152/ajpcell.00048.2001.
32. McKaig BC, McWilliams D, Watson SA, Mahida YR. Expression and regulation of tissue inhibitor of metalloproteinase-1 and matrix metalloproteinases by intestinal myofibroblasts in inflammatory bowel disease. Am J Pathol (2003) 162:1355-60. doi:10.1016/S0002-9440(10)63931-4.
33. McGettrick HM, Butler LM, Buckley CD, Rainger GE, Nash GB. Tissue stroma as a regulator of leukocyte recruitment in inflammation. J Leukoc Biol (2012) 91:385-400. doi:10.1189/jlb.0911458.
34. Schiering C, Krausgruber T, Chomka A, Fröhlich A, Adelmann K, Wohlfert EA, et al. The alarmin IL-33 promotes regulatory T-cell function in the intestine. Nature (2014) 513:564-8. doi:10.1038/nature13577.
35. Díaz-Jiménez D, Núñez LE, Beltrán CJ, Candia E, Suazo C, Alvarez-Lobos M, et al. Soluble ST2: a new and promising activity marker in ulcerative colitis. World J Gastroenterol (2011) 17:2181-90. doi:10.3748/wjg.v17.i17.2181.
36. Whitaker JW, Shoemaker R, Boyle DL, Hillman J, Anderson D, Wang W, et al. An imprinted rheumatoid arthritis methylome signature reflects pathogenic phenotype. Genome Med (2013) 5:40. doi:10.1186/gm444.
37. Russell SB, Russell JD, Trupin KM, Gayden AE, Opalenik SR, Nanney LB, et al. Epigenetically altered wound healing in keloid fibroblasts. J Invest Dermatol (2010) 130:2489-96. doi:10.1038/jid.2010.162.
38. Neumann E, Lefevre S, Zimmermann B, Gay S, Muller-Ladner U. Rheumatoid arthritis progression mediated by activated synovial fibroblasts. Trends Mol Med (2010) 16:458-68. doi:10.1016/j.molmed.2010.07.004.
39. Karouzakis E, Gay RE, Michel BA, Gay S, Neidhart M. DNA hypomethylation in rheumatoid arthritis synovial fibroblasts. Arthritis Rheum (2009) 60:3613-22. doi:10.1002/art.25018.
40. Ai R, Whitaker JW, Boyle DL, Tak PP, Gerlag DM, Wang W, et al. DNA methylome signature in early rheumatoid arthritis synoviocytes compared with longstanding rheumatoid arthritis synoviocytes. Arthritis Rheumatol (2015). doi:10.1002/art.39123.
41. Angiolilli C, Grabiec AM, Ferguson BS, Ospelt C, Malvar Fernandez B, van Es IE, et al. Inflammatory cytokines epigenetically regulate rheumatoid arthritis fibroblast-like synoviocyte activation by suppressing HDAC5 expression. Ann Rheum Dis (2014). doi:10.1136/annrheumdis-2014-205635.
42. Klein K, Kabala PA, Grabiec AM, Gay RE, Kolling C, Lin LL, et al. The bromodomain protein inhibitor I-BET151 suppresses expression of inflammatory genes and matrix degrading enzymes in rheumatoid arthritis synovial fibroblasts. Ann Rheum Dis (2014). doi:10.1136/annrheumdis-2014-205809.
43. Ospelt C, Reedquist KA, Gay S, Tak PP. Inflammatory memories: is epigenetics the missing link to persistent stromal cell activation in rheumatoid arthritis? Autoimmun Rev (2011) 10:519-24. doi:10.1016/j.autrev.2011.04.001.
44. Patel R, Filer A, Barone F, Buckley CD. Stroma: fertile soil for inflammation. Best Pract Res Clin Rheumatol (2014) 28:565-76. doi:10.1016/j.berh.2014.10.022.
45. Quintin J, Cheng S-C, van der Meer JW, Netea MG. Innate immune memory: towards a better understanding of host defense mechanisms. Curr Opin Immunol (2014) 29C:1-7. doi:10.1016/j.coi.2014.02.006.
46. Netea MG, Quintin J, van der Meer JWM. Trained immunity: a memory for innate host defense. Cell Host Microbe (2011) 9:355-61. doi:10.1016/j.chom.2011.04.006.
47. Saeed S, Quintin J, Kerstens HH, Rao NA, Aghajanirefah A, Matarese F, et al. Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity. Science (2014) 345:1251086-1251086. doi:10.1126/science.1251086.
48. Cheng SC, Quintin J, Cramer RA, Shepardson KM, Saeed S, Kumar V, et al. mTOR- and HIF-1 -mediated aerobic glycolysis as metabolic basis for trained immunity. Science (2014) 345:1250684-1250684. doi:10.1126/science.1250684.
49. Ruchti C, Haller D, Nuber M, Cottier H. Regional differences in renewal rates of fibroblasts in young adult female mice. Cell Tissue Res (1983) 232:625-36. doi:10.1007/BF00216434.
50. Ifrim DC, Quintin J, Joosten LA, Jacobs C, Jansen T, Jacobs L, et al. Trained immunity or tolerance: opposing functional programs induced in human monocytes after engagement of various pattern recognition receptors. Clin Vaccine Immunol (2014) 21:534-45. doi:10.1128/CVI. 00688-13.
51. Owens BMJ, Kaye PM. Stromal cell induction of regulatory dendritic cells. Front Immun (2012) 3:262. doi:10.3389/fimmu.2012.00262.
52. Calon A, Lonardo E, Berenguer-Llergo A, Espinet E, Hernando-Momblona X, Iglesias M, et al. Stromal gene expression defines poor-prognosis subtypes in colorectal cancer. Nat Genet (2015) 47(4):320-9. doi:10.1038/ng.3225.
53. Isella C, Terrasi A, Bellomo SE, Petti C, Galatola G, Muratore A, et al. Stromal contribution to the colorectal cancer transcriptome. Nat Genet (2015) 47(4):312-9. doi:10.1038/ng.3224.