Exosome-like nanoparticles from intestinal mucosal cells carry prostaglandin E2 and suppress activation of liver NKT cells

Journal of Immunology

Volumn 190, Issue 7, 2013, Pages 3579-3589

  Deng, Zhong Bin ^a   Zhuang, Xiaoying ^a   Ju, Songwen ^a   Xiang, Xiaoyu ^a   Mu, Jingyao ^a   Liu, Yuelong ^b   Jiang, Hong ^a   Zhang, Lifeng ^a   Mobley, James ^c   McClain, Craig ^a   Feng, Wenke ^a   Grizzle, William ^b   Yan, Jun ^a   Miller, Donald ^a   Kronenberg, Mitchell ^d   Zhang, Huang Ge ^a,e  

^a University of Louisville School of Medicine   (United States)

^b University of Alabama at Birmingham   (United States)

^c University of Alabama at Birmingham   (United States)

^d LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; GAMMA INTERFERON; INTERLEUKIN 4; NANOPARTICLE; PROSTAGLANDIN E RECEPTOR 4; PROSTAGLANDIN E2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INTERACTION; CLONAL ANERGY; CONTROLLED STUDY; EXOSOME; IMMUNOMODULATION; INTESTINE MUCOSA; LIVER CELL; LIVER INJURY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE MIGRATION; MOUSE; MUCOSA CELL; MUCUS; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS INHIBITION;

ANIMALS; CELL-DERIVED MICROPARTICLES; CLONAL ANERGY; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DINOPROSTONE; DISEASE MODELS, ANIMAL; EXOSOMES; GALACTOSYLCERAMIDES; HEPATITIS, AUTOIMMUNE; HUMANS; INTESTINAL MUCOSA; LIVER; LYMPHOCYTE ACTIVATION; MALE; MICE; NATURAL KILLER T-CELLS; SIGNAL TRANSDUCTION;

EID: 84875438397     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203170     Document Type: Article

References (51)

1. Crispe, I. N. 2009. The liver as a lymphoid organ. Annu. Rev. Immunol. 27: 147-163.
2. Adams, D. H., and B. Eksteen. 2006. Aberrant homing of mucosal T cells and extra-intestinal manifestations of inflammatory bowel disease. Nat. Rev. Immunol. 6: 244-251.
3. Al-Lahham, S. H., M. P. Peppelenbosch, H. Roelofsen, R. J. Vonk, and K. Venema. 2010. Biological effects of propionic acid in humans; metabolism, potential applications and underlying mechanisms. Biochim. Biophys. Acta 1801: 1175-1183.
4. Seki, S., Y. Habu, T. Kawamura, K. Takeda, H. Dobashi, T. Ohkawa, and H. Hiraide. 2000. The liver as a crucial organ in the first line of host defense: the roles of Kupffer cells, natural killer (NK) cells and NK1.1 Ag+ T cells in T helper 1 immune responses. Immunol. Rev. 174: 35-46.
5. Pellicci, D. G., A. J. Clarke, O. Patel, T. Mallevaey, T. Beddoe, J. Le Nours, A. P. Uldrich, J. McCluskey, G. S. Besra, S. A. Porcelli, et al. 2011. Recognition of β-linked self glycolipids mediated by natural killer T cell antigen receptors. Nat. Immunol. 12: 827-833.
6. Kinjo, Y., D. Wu, G. Kim, G. W. Xing, M. A. Poles, D. D. Ho, M. Tsuji, K. Kawahara, C. H. Wong, and M. Kronenberg. 2005. Recognition of bacterial glycosphingolipids by natural killer T cells. Nature 434: 520-525.
7. Subleski, J. J., V. L. Hall, T. B. Wolfe, A. J. Scarzello, J. M. Weiss, T. Chan, D. L. Hodge, T. C. Back, J. R. Ortaldo, and R. H. Wiltrout. 2011. TCRdependent and -independent activation underlie liver-specific regulation of NKT cells. J. Immunol. 186: 838-847.
8. Wang, X., K. A. Bishop, S. Hegde, L. A. Rodenkirch, J. W. Pike, and J. E. Gumperz. 2012. Human invariant natural killer T cells acquire transient innate responsiveness via histone H4 acetylation induced by weak TCR stimulation. J. Exp. Med. 209: 987-1000.
9. Parekh, V. V., M. T. Wilson, D. Olivares-Villagómez, A. K. Singh, L. Wu, C. R. Wang, S. Joyce, and L. Van Kaer. 2005. Glycolipid antigen induces longterm natural killer T cell anergy in mice. J. Clin. Invest. 115: 2572-2583.
10. György, B., T. G. Szabó, M. Pásztó i, Z. Pál, P. Misják, B. Aradi, V. László, E. Pállinger, E. Pap, A. Kittel, et al. 2011. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell. Mol. Life Sci. 68: 2667-2688.
11. Théry, C., M. Ostrowski, and E. Segura. 2009. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9: 581-593.
12. Van Niel, G., J. Mallegol, C. Bevilacqua, C. Candalh, S. Brugière, E. Tomaskovic-Crook, J. K. Heath, N. Cerf-Bensussan, and M. Heyman. 2003. Intestinal epithelial exosomes carry MHC class II/peptides able to inform the immune system in mice. Gut 52: 1690-1697.
13. Mallegol, J., G. Van Niel, C. Lebreton, Y. Lepelletier, C. Candalh, C. Dugave, J. K. Heath, G. Raposo, N. Cerf-Bensussan, and M. Heyman. 2007. T84-intestinal epithelial exosomes bear MHC class II/peptide complexes potentiating antigen presentation by dendritic cells. Gastroenterology 132: 1866-1876.
14. van Niel, G., G. Raposo, C. Candalh, M. Boussac, R. Hershberg, N. Cerf- Bensussan, and M. Heyman. 2001. Intestinal epithelial cells secrete exosomelike vesicles. Gastroenterology 121: 337-349.
15. Chen, X., C. H. Song, B. S. Feng, T. L. Li, P. Li, P. Y. Zheng, X. M. Chen, Z. Xing, and P. C. Yang. 2011. Intestinal epithelial cell-derived integrin αβ6 plays an important role in the induction of regulatory T cells and inhibits an antigen-specific Th2 response. J. Leukoc. Biol. 90: 751-759.
16. Deng, Z. B., X. Zhuang, S. Ju, X. Xiang, J. Mu, Q. Wang, J. Hong, L. Zhang, M. Kronenberg, J. Yan, et al. Intestinal mucus-derived nanoparticles mediate activation of Wnt/β-catenin signaling plays a role ininduction of liver NKT cell anergy. Hepatology In press.
17. Zhuang, X., X. Xiang, W. Grizzle, D. Sun, S. Zhang, R. C. Axtell, S. Ju, J. Mu, L. Zhang, L. Steinman, et al. 2011. Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain. Mol. Ther. 19: 1769-1779.
18. Spilman, M. S., C. Welbon, E. Nelson, and T. Dokland. 2009. Cryo-electron tomography of porcine reproductive and respiratory syndrome virus: organization of the nucleocapsid. J. Gen. Virol. 90: 527-535.
19. Sun, D., X. Zhuang, X. Xiang, Y. Liu, S. Zhang, C. Liu, S. Barnes, W. Grizzle, D. Miller, and H. G. Zhang. 2010. A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol. Ther. 18: 1606-1614.
20. Halder, R. C., C. Aguilera, I. Maricic, and V. Kumar. 2007. Type II NKT cellmediated anergy induction in type I NKT cells prevents inflammatory liver disease. J. Clin. Invest. 117: 2302-2312.
21. Deng, Z. B., Y. Liu, C. Liu, X. Xiang, J. Wang, Z. Cheng, S. V. Shah, S. Zhang, L. Zhang, X. Zhuang, et al. 2009. Immature myeloid cells induced by a high-fat diet contribute to liver inflammation. Hepatology 50: 1412-1420.
22. Deng, Z. B., A. Poliakov, R. W. Hardy, R. Clements, C. Liu, Y. Liu, J. Wang, X. Xiang, S. Zhang, X. Zhuang, et al. 2009. Adipose tissue exosome-like vesicles mediate activation of macrophage-induced insulin resistance. Diabetes 58: 2498-2505.
23. Paget, C., T. Mallevaey, A. O. Speak, D. Torres, J. Fontaine, K. C. Sheehan, M. Capron, B. Ryffel, C. Faveeuw, M. Leite de Moraes, et al. 2007. Activation of invariant NKT cells by toll-like receptor 9-stimulated dendritic cells requires type I interferon and charged glycosphingolipids. Immunity 27: 597-609.
24. Kim, S., S. Lalani, V. V. Parekh, T. L. Vincent, L. Wu, and L. Van Kaer. 2008. Impact of bacteria on the phenotype, functions, and therapeutic activities of invariant NKT cells in mice. J. Clin. Invest. 118: 2301-2315.
25. Xiang, X., X. Zhuang, S. Ju, S. Zhang, H. Jiang, J. Mu, L. Zhang, D. Miller, W. Grizzle, and H. G. Zhang. 2011. miR-155 promotes macroscopic tumor formation yet inhibits tumor dissemination from mammary fat pads to the lung by preventing EMT. Oncogene 30: 3440-3453.
26. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37: 911-917.
27. Yu, S., C. Liu, K. Su, J. Wang, Y. Liu, L. Zhang, C. Li, Y. Cong, R. Kimberly, W. E. Grizzle, et al. 2007. Tumor exosomes inhibit differentiation of bone marrow dendritic cells. J. Immunol. 178: 6867-6875.
28. Laulagnier, K., C. Motta, S. Hamdi, S. Roy, F. Fauvelle, J. F. Pageaux, T. Kobayashi, J. P. Salles, B. Perret, C. Bonnerot, and M. Record. 2004. Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem. J. 380: 161-171.
29. Wang, G. J., Y. Liu, A. Qin, S. V. Shah, Z. B. Deng, X. Xiang, Z. Cheng, C. Liu, J. Wang, L. Zhang, et al. 2008. Thymus exosomes-like particles induce regulatory T cells. J. Immunol. 181: 5242-5248.
30. Xiang, X., Y. Liu, X. Zhuang, S. Zhang, S. Michalek, D. D. Taylor, W. Grizzle, and H. G. Zhang. 2010. TLR2-mediated expansion of MDSCs is dependent on the source of tumor exosomes. Am. J. Pathol. 177: 1606-1610.
31. Johnstone, C. N., N. C. Tebbutt, H. E. Abud, S. J. White, K. L. Stenvers, N. E. Hall, S. H. Cody, R. H. Whitehead, B. Catimel, E. C. Nice, et al. 2000. Characterization of mouse A33 antigen, a definitive marker for basolateral surfaces of intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 279: G500-G510.
32. van Genderen, H. O., H. Kenis, L. Hofstra, J. Narula, and C. P. Reutelingsperger. 2008. Extracellular annexin A5: functions of phosphatidylserine-binding and two-dimensional crystallization. Biochim. Biophys. Acta 1783: 953-963.
33. Morel, O., N. Morel, L. Jesel, J. M. Freyssinet, and F. Toti. 2011. Microparticles: a critical component in the nexus between inflammation, immunity, and thrombosis. Semin. Immunopathol. 33: 469-486.
34. Wang, Y. Y., S. K. Lai, C. So, C. Schneider, R. Cone, and J. Hanes. 2011. Mucoadhesive nanoparticles may disrupt the protective human mucus barrier by altering its microstructure. PLoS ONE 6: e21547.
35. Lai, S. K., Y. Y. Wang, and J. Hanes. 2009. Mucus-penetrating nanoparticles for drug and gene delivery to mucosal tissues. Adv. Drug Deliv. Rev. 61: 158-171.
36. Arshad, M. I., M. Rauch, A. L'helgoualc'h, V. Julia, M. C. Leite-de-Moraes, C. Lucas-Clerc, C. Piquet-Pellorce, and M. Samson. 2011. NKT cells are required to induce high IL-33 expression in hepatocytes during ConA-induced acute hepatitis. Eur. J. Immunol. 41: 2341-2348.
37. Miyagi, T., T. Takehara, T. Tatsumi, T. Suzuki, M. Jinushi, Y. Kanazawa, N. Hiramatsu, T. Kanto, S. Tsuji, M. Hori, and N. Hayashi. 2004. Concanavalin a injection activates intrahepatic innate immune cells to provoke an antitumor effect in murine liver. Hepatology 40: 1190-1196.
38. Xiang, X., A. Poliakov, C. Liu, Y. Liu, Z. B. Deng, J. Wang, Z. Cheng, S. V. Shah, G. J. Wang, L. Zhang, et al. 2009. Induction of myeloid-derived suppressor cells by tumor exosomes. Int. J. Cancer 124: 2621-2633.
39. Subra, C., D. Grand, K. Laulagnier, A. Stella, G. Lambeau, M. Paillasse, P. De Medina, B. Monsarrat, B. Perret, S. Silvente-Poirot, et al. 2010. Exosomes account for vesicle-mediated transcellular transport of activatable phospholipases and prostaglandins. J. Lipid Res. 51: 2105-2120.
40. Kabashima, K., T. Saji, T. Murata, M. Nagamachi, T. Matsuoka, E. Segi, K. Tsuboi, Y. Sugimoto, T. Kobayashi, Y. Miyachi, et al. 2002. The prostaglandin receptor EP4 suppresses colitis, mucosal damage and CD4 cell activation in the gut. J. Clin. Invest. 109: 883-893.
41. Yoshioka, K., Y. Ueno, S. Tanaka, K. Nagai, T. Onitake, R. Hanaoka, H. Watanabe, and K. Chayama. 2012. Role of natural killer T cells in the mouse colitis-associated colon cancer model. Scand. J. Immunol. 75: 16-26.
42. Yao, C., D. Sakata, Y. Esaki, Y. Li, T. Matsuoka, K. Kuroiwa, Y. Sugimoto, and S. Narumiya. 2009. Prostaglandin E2-EP4 signaling promotes immune inflammation through Th1 cell differentiation and Th17 cell expansion. Nat. Med. 15: 633-640.
43. Nataraj, C., D. W. Thomas, S. L. Tilley, M. T. Nguyen, R. Mannon, B. H. Koller, and T. M. Coffman. 2001. Receptors for prostaglandin E(2) that regulate cellular immune responses in the mouse. J. Clin. Invest. 108: 1229-1235.
44. Liu, X., A. J. Lazenby, and G. P. Siegal. 2006. Signal transduction cross-talk during colorectal tumorigenesis. Adv. Anat. Pathol. 13: 270-274.
45. Kornek, M., Y. Popov, T. A. Libermann, N. H. Afdhal, and D. Schuppan. 2011. Human T cell microparticles circulate in blood of hepatitis patients and induce fibrolytic activation of hepatic stellate cells. Hepatology 53: 230-242.
46. Kornek, M., M. Lynch, S. H. Mehta, M. Lai, M. Exley, N. H. Afdhal, and D. Schuppan. 2012. Circulating microparticles as disease-specific biomarkers of severity of inflammation in patients with hepatitis C or nonalcoholic steatohepatitis. Gastroenterology 143: 448-458.
47. Sriram, V., S. Cho, P. Li, P. W. O'Donnell, C. Dunn, K. Hayakawa, J. S. Blum, and R. R. Brutkiewicz. 2002. Inhibition of glycolipid shedding rescues recognition of a CD1+ T cell lymphoma by natural killer T (NKT) cells. Proc. Natl. Acad. Sci. USA 99: 8197-8202.
48. Lombardi, V., P. Stock, A. K. Singh, J. Kerzerho, W. Yang, B. A. Sullivan, X. Li, T. Shiratsuchi, N. E. Hnatiuk, A. R. Howell, et al. 2010. A CD1d-dependent antagonist inhibits the activation of invariant NKT cells and prevents development of allergen-induced airway hyperreactivity. J. Immunol. 184: 2107-2115.
49. Valdez, P. A., P. J. Vithayathil, B. M. Janelsins, A. L. Shaffer, P. R. Williamson, and S. K. Datta. 2012. Prostaglandin E2 suppresses antifungal immunity by inhibiting interferon regulatory factor 4 function and interleukin-17 expression in T cells. Immunity 36: 668-679.
50. Kalinski, P. 2012. Regulation of immune responses by prostaglandin E2. J. Immunol. 188: 21-28.
51. Liu, C., S. Yu, K. Zinn, J. Wang, L. Zhang, Y. Jia, J. C. Kappes, S. Barnes, R. P. Kimberly, W. E. Grizzle, and H. G. Zhang. 2006. Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function. J. Immunol. 176: 1375-1385.