An endogenous nanomineral chaperones luminal antigen and peptidoglycan to intestinal immune cells

Nature Nanotechnology

Volumn 10, Issue 4, 2015, Pages 361-369

  Powell, Jonathan J ^a   Thomas McKay, Emma ^a   Thoree, Vinay ^a   Robertson, Jack ^a   Hewitt, Rachel E ^a   Skepper, Jeremy N ^b   Brown, Andy ^c   Hernandez Garrido, Juan Carlos ^d   Midgley, Paul A ^e   Gomez Morilla, Inmaculada ^f   Grime, Geoffrey W ^g   Kirkby, Karen J ^g,h   Mabbott, Neil A ⁱ   Donaldson, David S ⁱ   Williams, Ifor R ^j   Rios, Daniel ^j   Girardin, Stephen E ^k   Haas, Carolin T ^a   Bruggraber, Sylvaine F A ^a   Laman, Jon D ^l,m   Tanriver, Yakup ⁿ   Lombardi, Giovanna ^o   Lechler, Robert ^o   Thompson, Richard P H ^a,p   Pele, Laetitia C ^a   more..

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF LEEDS   (United Kingdom)

^d UNIVERSITY OF CÁDIZ   (Spain)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^g UNIVERSITY OF SURREY   (United Kingdom)

^h UNIVERSITY OF MANCHESTER   (United Kingdom)

ⁱ UNIVERSITY OF EDINBURGH   (United Kingdom)

^j EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^k UNIVERSITY OF TORONTO   (Canada)

^l ERASMUS MEDICAL CENTER   (Netherlands)

^m UNIVERSITY OF GRONINGEN   (Netherlands)

ⁿ UNIVERSITY OF FREIBURG   (Germany)

^o KING'S COLLEGE LONDON   (United Kingdom)

^p ROYAL COLLEGE OF PHYSICIANS   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGENS; CALCIUM PHOSPHATE; CYTOLOGY; LIGANDS; MACROMOLECULES; MAGNESIUM COMPOUNDS; MAMMALS; NANOPARTICLES;

BACTERIAL PEPTIDOGLYCAN; CALCIUM PHOSPHATE NANOPARTICLES; IMMUNE TOLERANCES; PARTICLE SCAVENGING; PEYER'S PATCHES; PHOSPHATE IONS; PROTEIN ANTIGENS; SMALL INTESTINE;

CELLS;

ANTIGEN; CALCIUM PHOSPHATE; CD11B ANTIGEN; CD68 ANTIGEN; CHAPERONE; GLYCOPROTEIN P 15095; HLA DR ANTIGEN; MAGNESIUM; NANOPARTICLE; PEPTIDOGLYCAN; PROGRAMMED DEATH 1 LIGAND 1; CALCIUM; MINERAL; PHOSPHATE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL TOLERANCE; INTESTINE CELL; KNOCKOUT MOUSE; MACROMOLECULE; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PEYER PATCH; PHENOTYPE; PRIORITY JOURNAL; WILD TYPE; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CHEMISTRY; CYTOLOGY; IMMUNOLOGY; INTESTINE; PARTICLE SIZE; ULTRASTRUCTURE;

ANIMALS; ANTIGENS; CALCIUM; CALCIUM PHOSPHATES; CELLS, CULTURED; HUMANS; INTESTINES; MICE; MICE, INBRED BALB C; MINERALS; MOLECULAR CHAPERONES; NANOPARTICLES; PARTICLE SIZE; PEPTIDOGLYCAN; PEYER'S PATCHES; PHOSPHATES;

EID: 84927125760     PISSN: 17483387     EISSN: 17483395     Source Type: Journal    
DOI: 10.1038/nnano.2015.19     Document Type: Article

References (44)

1. Powell, J. J., Thoree, V. & Pele, L. C. Dietary microparticles and their impact on tolerance and immune responsiveness of the gastrointestinal tract. Br. J. Nutr. 98(Suppl 1), S59-S63 (2007).
2. Gomez-Morilla, I., Thoree, V., Powell, J. J., Kirkby, K. J. & Grime, G. W. Identification and quantitative analysis of calcium phosphate microparticles in intestinal tissue by nuclear microscopy. Nucl. Instrum. Methods Phys. Res. B 249, 665-669 (2006).
3. Powell, J. J., Faria, N., Thomas-McKay, E. & Pele, L. C. Origin and fate of dietary nanoparticles and microparticles in the gastrointestinal tract. J. Autoimmun. 34, J226-J233 (2010).
4. Lentner, C. (ed.) Geigy Scientific Tables 8th edn, Vol. 1 (CIBA-GEIGY Ltd, 1981).
5. Schedl, H. P., Osbaldiston, G. W. & Mills, I. H. Absorption, secretion, and precipitation of calcium in the small intestine of the dog. Am J Physiol 214, 814-819 (1968).
6. Jung, C., Hugot, J. P. & Barreau, F. Peyer's patches: the immune sensors of the intestine. Int. J. Inflam. 2010, 823710 (2010).
7. Mowat, A. M. & Bain, C. C. Mucosal macrophages in intestinal homeostasis and inflammation. J. Innate Immun. 3, 550-564 (2011).
8. Pele, L. C. et al. Low dietary calcium levels modulate mucosal caspase expression and increase disease activity in mice with dextran sulfate sodium induced colitis. J. Nutr. 137, 2475-2480 (2007).
9. Civitelli, R. & Ziambaras, K. Calcium and phosphate homeostasis: concerted interplay of new regulators. J. Endocrinol. Invest. 34, 3-7 (2011).
10. Neutra, M. R. & Kraehenbuhl, J. P. Transepithelial transport and mucosal defence I: the role of M cells. Trends Cell Biol. 2, 134-138 (1992).
11. Knoop, K. A. et al. RANKL is necessary and sufficient to initiate development of antigen-sampling M cells in the intestinal epithelium. J. Immunol. 183, 5738-5747 (2009).
12. Kimura, S. et al. Visualization of the entire differentiation process of murine M cells: suppression of their maturation in cecal patches. Mucosal Immunol. http://www.nature.com/mi/journal/vaop/ncurrent/full/mi201499a.html (2014).
13. Masahata, K. et al. Generation of colonic IgA-secreting cells in the caecal patch. Nature Commun. 5, 3704 (2014).
14. Szentkuti, L. Light microscopical observations on luminally administered dyes, dextrans, nanospheres and microspheres in the pre-epithelial mucus gel layer of the rat distal colon. J. Control. Rel. 46, 233-242 (1997).
15. Uskokovic, V. & Uskokovic, D. P. Nanosized hydroxyapatite and other calcium phosphates: chemistry of formation and application as drug and gene delivery agents. J. Biomed. Mater. Res B 96, 152-191 (2011).
16. Dorozhkin, S. V. Nanosized and nanocrystalline calcium orthophosphates. Acta Biomater. 6, 715-734 (2010).
17. Blander, J. M. & Medzhitov, R. Regulation of phagosome maturation by signals from toll-like receptors. Science 304, 1014-1018 (2004).
18. Blander, J. M. & Medzhitov, R. Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature 440, 808-812 (2006).
19. Chong, C. S. et al. Enhancement of T helper type 1 immune responses against hepatitis B virus core antigen by PLGA nanoparticle vaccine delivery. J. Control. Rel. 102, 85-99 (2005).
20. Heit, A., Schmitz, F., Haas, T., Busch, D. H. & Wagner, H. Antigen coencapsulated with adjuvants efficiently drive protective T cell immunity. Eur. J. Immunol. 37, 2063-2074 (2007).
21. Schlosser, E. et al. TLR ligands and antigen need to be coencapsulated into the same biodegradable microsphere for the generation of potent cytotoxic T lymphocyte responses. Vaccine 26, 1626-1637 (2008).
22. Klasen, I. S. et al. The presence of peptidoglycan-polysaccharide complexes in the bowel wall and the cellular responses to these complexes in Crohn's disease. Clin. Immunol. Immunopathol. 71, 303-308 (1994).
23. Schrijver, I. A. et al. Bacterial peptidoglycan and immune reactivity in the central nervous system in multiple sclerosis. Brain 124, 1544-1554 (2001).
24. Boskey, A. L. & Posner, A. S. Magnesium stabilization of amorphous calcium phosphate: a kinetic study. Mater. Res. Bull. 9, 907-916 (1974).
25. Termine, J. D., Peckauskas, R. A. & Posner, A. S. Calcium phosphate formation in vitro. II. Effects of environment on amorphous-crystalline transformation. Arch. Biochem. Biophys. 140, 318-325 (1970).
26. Hewitt, R. E. et al. Immuno-inhibitory PD-L1 can be induced by a peptidoglycan/NOD2 mediated pathway in primary monocytic cells and is deficient in Crohn's patients with homozygous NOD2 mutations. Clin. Immunol. 143, 162-169 (2012).
27. Davies, J. M., MacSharry, J. & Shanahan, F. Differential regulation of Toll-like receptor signalling in spleen and Peyer's patch dendritic cells. Immunology 131, 438-448 (2010).
28. Stroo, I. et al. Phenotyping of Nod1/2 double deficient mice and characterization of Nod1/2 in systemic inflammation and associated renal disease. Biol. Open. 1, 1239-1247 (2012).
29. Francisco, L. M., Sage, P. T. & Sharpe, A. H. The PD-1 pathway in tolerance and autoimmunity. Immunol. Rev. 236, 219-242 (2010).
30. Van Heel, D. A. et al. Muramyl dipeptide and toll-like receptor sensitivity in NOD2-associated Crohn's disease. Lancet 365, 1794-1796 (2005).
31. Gullberg, E. & Soderholm, J. D. Peyer's patches and M cells as potential sites of the inflammatory onset in Crohn's disease. Ann. NY Acad. Sci. 1072, 218-232 (2006).
32. Fukaya, T. et al. Crucial roles of B7-H1 and B7-DC expressed on mesenteric lymph node dendritic cells in the generation of antigen-specific CD4+Foxp3+ regulatory T cells in the establishment of oral tolerance. Blood 116, 2266-2276 (2010).
33. Scandiuzzi, L. et al. Tissue-expressed B7-H1 critically controls intestinal inflammation. Cell. Rep. 6, 625-632 (2014).
34. Reynoso, E. D. et al. Intestinal tolerance is converted to autoimmune enteritis upon PD-1 ligand blockade. J. Immunol. 182, 2102-2112 (2009).
35. Awaad, A., Nakamura, M. & Ishimura, K. Imaging of size-dependent uptake and identification of novel pathways in mouse Peyer's patches using fluorescent organosilica particles. Nanomedicine 8, 627-636 (2012).
36. Sass, W., Dreyer, H. P. & Seifert, J. Rapid insorption of small particles in the gut. Am. J. Gastroenterol. 85, 255-260 (1990).
37. Davies, K. M., Rafferty, K. & Heaney, R. P. Determinants of endogenous calcium entry into the gut. Am. J. Clin. Nutr. 80, 919-923 (2004).
38. Cross, K. J., Huq, N. L., Palamara, J. E., Perich, J. W. & Reynolds, E. C. Physicochemical characterization of casein phosphopeptide-amorphous calcium phosphate nanocomplexes. J. Biol. Chem. 280, 15362-15369 (2005).
39. De Kruif, C. G., Huppertz, T., Urban, V. S. & Petukhov, A. V. Casein micelles and their internal structure. Adv. Colloid Interface Sci. 171-172, 36-52 (2012).
40. McGann, T. C. et al. Amorphous calcium phosphate in casein micelles of bovine milk. Calcif. Tissue Int. 35, 821-823 (1983).
41. Minniti, F. et al. Breast-milk characteristics protecting against allergy. Endocr. Metab. Immune Disord. Drug Targets 14, 9-15 (2014).
42. Schneider, C. A., Rasband,W. S. & Eliceiri, K.W. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671-675 (2012).
43. Bilton, M., Brown, A. P. & Milne, S. J. Investigating the optimum conditions for the formation of calcium oxide, used for CO2 sequestration, by thermal decomposition of calcium acetate. Electron Microscopy and Analysis Group Conference 2011 (Emag 2011) 371 (2012).
44. Bres, E. F., Hutchison, J. L., Senger, B., Voegel, J. C. & Frank, R. M. HREM study of irradiation damage in human dental enamel crystals. Ultramicroscopy 35, 305-322 (1991).