Luminal Microbes Promote Monocyte-Stem Cell Interactions Across a Healthy Colonic Epithelium

Journal of Immunology

Volumn 193, Issue 1, 2014, Pages 439-451

  Skoczek, Dagmara A ^a   Walczysko, Petr ^a   Horn, Nikki ^a   Parris, Alyson ^b   Clare, Simon ^c   Williams, Mark R ^b   Sobolewski, Anastasia ^a  

^a INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MYELOID DIFFERENTIATION FACTOR 88;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; CELL COUNT; CELL INTERACTION; CELL PROLIFERATION; COLITIS; CONTROLLED STUDY; EPITHELIOID CELL; EXPLANT; HOMEOSTASIS; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; IN VIVO STUDY; INTESTINE EPITHELIUM; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; MOLECULAR IMAGING; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STAINING; STEM CELL;

ANIMALS; ANTIGENS, LY; BACTERIA; CELL PROLIFERATION; FEMALE; HUMANS; INTESTINAL MUCOSA; MALE; MICE; MICE, TRANSGENIC; MONOCYTES; RECEPTORS, G-PROTEIN-COUPLED; STEM CELLS;

EID: 84903625205     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301497     Document Type: Article

References (61)

1. Barker, N., J. H. van Es, J. Kuipers, P. Kujala, M. van den Born, M. Cozijnsen, A. Haegebarth, J. Korving, H. Begthel, P. J. Peters, and H. Clevers. 2007. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449: 1003-1007. (Pubitemid 350014593)
2. Sato, T., D. E. Stange, M. Ferrante, R. G. Vries, J. H. Van Es, S. Van den Brink, W. J. Van Houdt, A. Pronk, J. Van Gorp, P. D. Siersema, and H. Clevers. 2011. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 141: 1762-1772.
3. Sato, T., R. G. Vries, H. J. Snippert, M. van de Wetering, N. Barker, D. E. Stange, J. H. van Es, A. Abo, P. Kujala, P. J. Peters, and H. Clevers. 2009. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459: 262-265.
4. Ootani, A., X. Li, E. Sangiorgi, Q. T. Ho, H. Ueno, S. Toda, H. Sugihara, K. Fujimoto, I. L. Weissman, M. R. Capecchi, and C. J. Kuo. 2009. Sustained in vitro intestinal epithelial culture within a Wnt-dependent stem cell niche. Nat. Med. 15: 701-706.
5. Shaker, A., and D. C. Rubin. 2010. Intestinal stem cells and epithelialmesenchymal interactions in the crypt and stem cell niche. Transl. Res. 156:180-187.
6. Chieppa, M., M. Rescigno, A. Y. Huang, and R. N. Germain. 2006. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J. Exp. Med. 203: 2841-2852. (Pubitemid 46026162)
7. Brown, S. L., T. E. Riehl, M. R. Walker, M. J. Geske, J. M. Doherty, W. F. Stenson, and T. S. Stappenbeck. 2007. Myd88-dependent positioning of Ptgs2-expressing stromal cells maintains colonic epithelial proliferation during injury. J. Clin. Invest. 117: 258-269. (Pubitemid 46048471)
8. Pull, S. L., J. M. Doherty, J. C. Mills, J. I. Gordon, and T. S. Stappenbeck. 2005. Activated macrophages are an adaptive element of the colonic epithelial progenitor niche necessary for regenerative responses to injury. Proc. Natl. Acad. Sci. USA 102: 99-104. (Pubitemid 40094435)
9. Rescigno, M. 2009. Gut commensal flora: tolerance and homeostasis. F1000 Biol. Rep. 1: 9.
10. Wlodarska, M., B. Willing, K. M. Keeney, A. Menendez, K. S. Bergstrom, N. Gill, S. L. Russell, B. A. Vallance, and B. B. Finlay. 2011. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect. Immun. 79: 1536-1545.
11. Rakoff-Nahoum, S., J. Paglino, F. Eslami-Varzaneh, S. Edberg, and R. Medzhitov. 2004. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241. (Pubitemid 38962578)
12. Fukata, M., K. S. Michelsen, R. Eri, L. S. Thomas, B. Hu, K. Lukasek, C. C. Nast, J. Lechago, R. Xu, Y. Naiki, et al. 2005. Toll-like receptor-4 is required for intestinal response to epithelial injury and limiting bacterial translocation in a murine model of acute colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 288: G1055-G1065. (Pubitemid 40563149)
13. Lee, J., J. M. Gonzales-Navajas, and E. Raz. 2008. The "polarizing-tolerizing" mechanism of intestinal epithelium: its relevance to colonic homeostasis. Semin. Immunopathol. 30: 3-9.
14. Lee, J., J. H. Mo, K. Katakura, I. Alkalay, A. N. Rucker, Y. T. Liu, H. K. Lee, C. Shen, G. Cojocaru, S. Shenouda, et al. 2006. Maintenance of colonic homeostasis by distinctive apical TLR9 signalling in intestinal epithelial cells. Nat. Cell Biol. 8: 1327-1336. (Pubitemid 44835107)
15. Duerkop, B. A., S. Vaishnava, and L. V. Hooper. 2009. Immune responses to the microbiota at the intestinal mucosal surface. Immunity 31: 368-376.
16. Pedron, T., C. Mulet, C. Dauga, L. Frangeul, C. Chervaux, G. Grompone, and P. J. Sansonetti. 2012. A crypt-specific core microbiota resides in the mouse colon. MBio 3(3).
17. Barnett, A. M., N. C. Roy, W. C. McNabb, and A. L. Cookson. 2012. The interactions between endogenous bacteria, dietary components and the mucus layer of the large bowel. Food Funct. 3: 690-699.
18. Seno, H., H. Miyoshi, S. L. Brown, M. J. Geske, M. Colonna, and T. S. Stappenbeck. 2009. Efficient colonic mucosal wound repair requires Trem2 signaling. Proc. Natl. Acad. Sci. USA 106: 256-261.
19. Willenborg, S., T. Lucas, G. van Loo, J. A. Knipper, T. Krieg, I. Haase, B. Brachvogel, M. Hammerschmidt, A. Nagy, N. Ferrara, et al. 2012. CCR2 recruits an inflammatory macrophage subpopulation critical for angiogenesis in tissue repair. Blood 120: 613-625.
20. Shechter, R., A. London, C. Varol, C. Raposo, M. Cusimano, G. Yovel, A. Rolls, M. Mack, S. Pluchino, G. Martino, et al. 2009. Infiltrating blood-derived macrophages are vital cells playing an anti-inflammatory role in recovery from spinal cord injury in mice. PLoS Med. 6: e1000113.
21. Tsilingiri, K., T. Barbosa, G. Penna, F. Caprioli, A. Sonzogni, G. Viale, and M. Rescigno. 2012. Probiotic and postbiotic activity in health and disease: comparison on a novel polarised ex-vivo organ culture model. Gut 61: 1007-1015.
22. Johansson, M. E., J. K. Gustafsson, K. E. Sjöberg, J. Petersson, L. Holm, H. Sjövall, and G. C. Hansson. 2010. Bacteria penetrate the inner mucus layer before inflammation in the dextran sulfate colitis model. PLoS ONE 5: e12238.
23. Norrander, J., T. Kempe, and J. Messing. 1983. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene 26: 101-106. (Pubitemid 14209690)
24. Reynolds, A., A. Parris, L. A. Evans, S. Lindqvist, P. Sharp, M. Lewis, R. Tighe, and M. R. Williams. 2007. Dynamic and differential regulation of NKCC1 by calcium and cAMP in the native human colonic epithelium. J. Physiol. 582: 507-524. (Pubitemid 47040541)
25. Lindqvist, S., J. Hernon, P. Sharp, N. Johns, S. Addison, M. Watson, R. Tighe, S. Greer, J. Mackay, M. Rhodes, et al. 2002. The colon-selective spasmolytic otilonium bromide inhibits muscarinic M(3) receptor-coupled calcium signals in isolated human colonic crypts. Br. J. Pharmacol. 137: 1134-1142. (Pubitemid 35440754)
26. Reynolds, A., N. Wharton, A. Parris, E. Mitchell, A. Sobolewski, C. Kam, L. Bigwood, A. El Hadi, A. Müunsterberg, M. Lewis, et al. 2014. Canonical Wnt signals combined with suppressed TGFb/BMP pathways promote renewal of the native human colonic epithelium. Gut 63: 610-621.
27. Francke, A., J. Herold, S. Weinert, R. H. Strasser, and R. C. Braun-Dullaeus. 2011. Generation of mature murine monocytes from heterogeneous bone marrow and description of their properties. J. Histochem. Cytochem. 59: 813-825.
28. Fukuda, S., M. Nagano, T. Yamashita, K. Kimura, I. Tsuboi, G. Salazar, S. Ueno, M. Kondo, T. Kunath, T. Oshika, and O. Ohneda. 2013. Functional endothelial progenitor cells selectively recruit neurovascular protective monocyte-derived F4/80(+)/Ly6c(+) macrophages in a mouse model of retinal degeneration. Stem Cells 31: 2149-2161.
29. Hansson, G. C., and M. E. Johansson. 2010. The inner of the two Muc2 mucindependent mucus layers in colon is devoid of bacteria. Gut Microbes 1: 51-54.
30. Henderson, R. B., J. A. Hobbs, M. Mathies, and N. Hogg. 2003. Rapid recruitment of inflammatory monocytes is independent of neutrophil migration. Blood 102: 328-335. (Pubitemid 36759673)
31. Lee, P. Y., J. X. Wang, E. Parisini, C. C. Dascher, and P. A. Nigrovic. 2013. Ly6 family proteins in neutrophil biology. J. Leukoc. Biol. 94: 585-594.
32. Rose, S., A. Misharin, and H. Perlman. 2012. A novel Ly6C/Ly6G-based strategy to analyze the mouse splenic myeloid compartment. Cytometry A 81:343-350.
33. Gordon, H. A., and E. Bruckner-Kardoss. 1961. Effect of normal microbial flora on intestinal surface area. Am. J. Physiol. 201: 175-178.
34. Glaister, J. R. 1973. Factors affecting the lymphoid cells in the small intestinal epithelium of the mouse. Int. Arch. Allergy Appl. Immunol. 45: 719-730.
35. Petnicki-Ocwieja, T., T. Hrncir, Y. J. Liu, A. Biswas, T. Hudcovic, H. Tlaskalova-Hogenova, and K. S. Kobayashi. 2009. Nod2 is required for the regulation of commensal microbiota in the intestine. Proc. Natl. Acad. Sci. USA 106: 15813-15818.
36. Cliffe, L. J., N. E. Humphreys, T. E. Lane, C. S. Potten, C. Booth, and R. K. Grencis. 2005. Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science 308: 1463-1465. (Pubitemid 40791299)
37. Swirski, F. K., M. Nahrendorf, M. Etzrodt, M. Wildgruber, V. Cortez-Retamozo, P. Panizzi, J. L. Figueiredo, R. H. Kohler, A. Chudnovskiy, P. Waterman, et al. 2009. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 325: 612-616.
38. Reinecker, H. C., E. Y. Loh, D. J. Ringler, A. Mehta, J. L. Rombeau, and R. P. MacDermott. 1995. Monocyte-chemoattractant protein 1 gene expression in intestinal epithelial cells and inflammatory bowel disease mucosa. Gastroenterology 108: 40-50.
39. Zigmond, E., C. Varol, J. Farache, E. Elmaliah, A. T. Satpathy, G. Friedlander, M. Mack, N. Shpigel, I. G. Boneca, K. M. Murphy, et al. 2012. Ly6C hi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity 37: 1076-1090.
40. Dunay, I. R., R. A. Damatta, B. Fux, R. Presti, S. Greco, M. Colonna, and L. D. Sibley. 2008. Gr1(+) inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii. Immunity 29: 306-317.
41. Carlin, L. M., E. G. Stamatiades, C. Auffray, R. N. Hanna, L. Glover, G. Vizcay-Barrena, C. C. Hedrick, H. T. Cook, S. Diebold, and F. Geissmann. 2013. Nr4a1-dependent Ly6C(low) monocytes monitor endothelial cells and orchestrate their disposal. Cell 153: 362-375.
42. Rosas, M., B. Thomas, M. Stacey, S. Gordon, and P. R. Taylor. 2010. The myeloid 7/4-antigen defines recently generated inflammatory macrophages and is synonymous with Ly-6B. J. Leukoc. Biol. 88: 169-180.
43. Bain, C. C., C. L. Scott, H. Uronen-Hansson, S. Gudjonsson, O. Jansson, O. Grip, M. Guilliams, B. Malissen, W. W. Agace, and A. M. Mowat. 2013. Resident and pro-inflammatory macrophages in the colon represent alternative context-dependent fates of the same Ly6Chi monocyte precursors. Mucosal Immunol. 6: 498-510.
44. Rivollier, A., J. He, A. Kole, V. Valatas, and B. L. Kelsall. 2012. Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J. Exp. Med. 209: 139-155.
45. Yona, S., and S. Jung. 2010. Monocytes: subsets, origins, fates and functions. Curr. Opin. Hematol. 17: 53-59.
46. Auffray, C., D. Fogg, M. Garfa, G. Elain, O. Join-Lambert, S. Kayal, S. Sarnacki, A. Cumano, G. Lauvau, and F. Geissmann. 2007. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317:666-670. (Pubitemid 47229966)
47. Arnold, L., A. Henry, F. Poron, Y. Baba-Amer, N. van Rooijen, A. Plonquet, R. K. Gherardi, and B. Chazaud. 2007. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med. 204: 1057-1069. (Pubitemid 46798150)
48. Abraham, C., and J. H. Cho. 2009. Inflammatory bowel disease. N. Engl. J. Med. 361: 2066-2078.
49. Barrett, J. C., S. Hansoul, D. L. Nicolae, J. H. Cho, R. H. Duerr, J. D. Rioux, S. R. Brant, M. S. Silverberg, K. D. Taylor, M. M. Barmada, et al NIDDK IBD Genetics Consortium; Belgian-French IBD Consortium; Wellcome Trust Case Control Consortium. 2008. Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease. Nat. Genet. 40: 955-962.
50. Strober, W., and T. Watanabe. 2011. NOD2, an intracellular innate immune sensor involved in host defense and Crohn's disease. Mucosal Immunol. 4: 484-495.
51. Hiemstra, I. H., G. Bouma, D. Geerts, G. Kraal, and J. M. den Haan. 2012. Nod2 improves barrier function of intestinal epithelial cells via enhancement of TLR responses. Mol. Immunol. 52: 264-272.
52. Coulombe, F., S. Fiola, S. Akira, Y. Cormier, and J. Gosselin. 2012. Muramyl dipeptide induces NOD2-dependent Ly6C(high) monocyte recruitment to the lungs and protects against influenza virus infection. PLoS ONE 7: e36734.
53. Kim, Y. G., N. Kamada, M. H. Shaw, N. Warner, G. Y. Chen, L. Franchi, and G. Núñez. 2011. The Nod2 sensor promotes intestinal pathogen eradication via the chemokine CCL2-dependent recruitment of inflammatory monocytes. Immunity 34: 769-780.
54. Osusky, R., and S. J. Ryan. 1996. Retinal pigment epithelial cell proliferation:potentiation by monocytes and serum. Graefes Arch. Clin. Exp. Ophthalmol. 234 (Suppl. 1): S76-S82.
55. Itzkovitz, S., A. Lyubimova, I. C. Blat, M. Maynard, J. van Es, J. Lees, T. Jacks, H. Clevers, and A. van Oudenaarden. 2011. Single-molecule transcript counting of stem-cell markers in the mouse intestine. Nat. Cell Biol. 14: 106-114.
56. Yui, S., T. Nakamura, T. Sato, Y. Nemoto, T. Mizutani, X. Zheng, S. Ichinose, T. Nagaishi, R. Okamoto, K. Tsuchiya, et al. 2012. Functional engraftment of colon epithelium expanded in vitro from a single adult Lgr5+ stem cell. Nat. Med. 18: 618-623.
57. McDole, J. R., L. W. Wheeler, K. G. McDonald, B. Wang, V. Konjufca, K. A. Knoop, R. D. Newberry, and M. J. Miller. 2012. Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine. Nature 483:345-349.
58. Osuský, R., P. Malik, and S. J. Ryan. 1997. Retinal pigment epithelium cells promote the maturation of monocytes to macrophages in vitro. Ophthalmic Res. 29: 31-36. (Pubitemid 27153821)
59. Rimoldi, M., M. Chieppa, M. Vulcano, P. Allavena, and M. Rescigno. 2004. Intestinal epithelial cells control dendritic cell function. Ann. N. Y. Acad. Sci. 1029: 66-74. (Pubitemid 40298517)
60. Iliev, I. D., E. Mileti, G. Matteoli, M. Chieppa, and M. Rescigno. 2009. Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal Immunol. 2: 340-350.
61. Iliev, I. D., I. Spadoni, E. Mileti, G. Matteoli, A. Sonzogni, G. M. Sampietro, D. Foschi, F. Caprioli, G. Viale, and M. Rescigno. 2009. Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells. Gut 58:1481-1489.