CD209a expression on dendritic cells is critical for the development of pathogenic Th17 cell responses in murine schistosomiasis

Journal of Immunology

Volumn 192, Issue 10, 2014, Pages 4655-4665

  Ponichtera, Holly E ^a,b   Shainheit, Mara G ^a   Liu, Beiyun C ^a   Raychowdhury, Raktima ^c   Larkin, Bridget M ^a,b   Russo, Joanne M ^a   Salantes, D Brenda ^a,b   Lai, Chao Qiang ^d   Parnell, Laurence D ^d   Yun, Tae J ^e   Cheong, Cheolho ^e   Bunnell, Stephen C ^a,b   Hacohen, Nir ^c   Stadecker, Miguel J ^a,b  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TUFTS UNIVERSITY   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d TUFTS UNIVERSITY   (United States)

^e CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD209 ANTIGEN; CD209A ANTIGEN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 23; LECTIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; CELL SELECTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SCHISTOSOMIASIS; SEQUENCE HOMOLOGY; TH17 CELL; TRANSGENE;

ANIMALS; CELL ADHESION MOLECULES; CELL LINE; DENDRITIC CELLS; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION REGULATION; GENE SILENCING; GRANULOMA; HUMANS; INTERLEUKIN-1BETA; INTERLEUKIN-23; LECTINS, C-TYPE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED CBA; MITOGEN-ACTIVATED PROTEIN KINASE 3; PROTO-ONCOGENE PROTEINS C-RAF; PROTO-ONCOGENE PROTEINS PP60(C-SRC); RECEPTORS, CELL SURFACE; SCHISTOSOMA; SCHISTOSOMIASIS; SPLEEN; TH17 CELLS;

EID: 84901289099     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400121     Document Type: Article

References (68)

1. Bica, I., D. H. Hamer, and M. J. Stadecker. 2000. Hepatic schistosomiasis. Infect. Dis. Clin. North Am. 14: 583-604, viii.
2. Pearce, E. J., and A. S. MacDonald. 2002. The immunobiology of schistosomiasis. Nat. Rev. Immunol. 2: 499-511.
3. Fallon, P. G. 2000. Immunopathology of schistosomiasis: a cautionary tale of mice and men. Immunol. Today 21: 29-35.
4. Wilson, M. S., M. M. Mentink-Kane, J. T. Pesce, T. R. Ramalingam, R. Thompson, and T. A. Wynn. 2007. Immunopathology of schistosomiasis. Immunol. Cell Biol. 85: 148-154.
5. Larkin, B. M., P. M. Smith, H. E. Ponichtera, M. G. Shainheit, L. I. Rutitzky, and M. J. Stadecker. 2012. Induction and regulation of pathogenic Th17 cell responses in schistosomiasis. Semin. Immunopathol. 34: 873-888.
6. Fanning, M. M., P. A. Peters, R. S. Davis, J. W. Kazura, and A. A. Mahmoud. 1981. Immunopathology of murine infection with Schistosoma mansoni: relationship of genetic background to hepatosplenic disease and modulation. J. Infect. Dis. 144: 148-153.
7. Cheever, A. W., R. H. Duvall, T. A. Hallack, Jr., R. G. Minker, J. D. Malley, and K. G. Malley. 1987. Variation of hepatic fibrosis and granuloma size among mouse strains infected with Schistosoma mansoni. Am. J. Trop. Med. Hyg. 37: 85-97.
8. Hernandez, H. J., W. C. Trzyna, J. S. Cordingley, P. H. Brodeur, and M. J. Stadecker. 1997. Differential antigen recognition by T cell populations from strains of mice developing polar forms of granulomatous inflammation in response to eggs of Schistosoma mansoni. Eur. J. Immunol. 27: 666-670.
9. Rutitzky, L. I., J. R. Lopes da Rosa, and M. J. Stadecker. 2005. Severe CD4 T cell-mediated immunopathology in murine schistosomiasis is dependent on IL-12p40 and correlates with high levels of IL-17. J. Immunol. 175: 3920-3926.
10. Rutitzky, L. I., L. Bazzone, M. G. Shainheit, B. Joyce-Shaikh, D. J. Cua, and M. J. Stadecker. 2008. IL-23 is required for the development of severe egginduced immunopathology in schistosomiasis and for lesional expression of IL-17. J. Immunol. 180: 2486-2495.
11. Shainheit, M. G., P. M. Smith, L. E. Bazzone, A. C. Wang, L. I. Rutitzky, and M. J. Stadecker. 2008. Dendritic cell IL-23 and IL-1 production in response to schistosome eggs induces Th17 cells in a mouse strain prone to severe immunopathology. J. Immunol. 181: 8559-8567.
12. Shainheit, M. G., K. W. Lasocki, E. Finger, B. M. Larkin, P. M. Smith, A. H. Sharpe, C. A. Dinarello, L. I. Rutitzky, and M. J. Stadecker. 2011. The pathogenic Th17 cell response to major schistosome egg antigen is sequentially dependent on IL-23 and IL-1b. J. Immunol. 187: 5328-5335.
13. Pearce, E. J., P. Caspar, J. M. Grzych, F. A. Lewis, and A. Sher. 1991. Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J. Exp. Med. 173: 159-166.
14. Dong, C. 2006. Diversification of T-helper-cell lineages: finding the family root of IL-17-producing cells. Nat. Rev. Immunol. 6: 329-333.
15. Bettelli, E., M. Oukka, and V. K. Kuchroo. 2007. T(H)-17 cells in the circle of immunity and autoimmunity. Nat. Immunol. 8: 345-350.
16. Stockinger, B., and M. Veldhoen. 2007. Differentiation and function of Th17 T cells. Curr. Opin. Immunol. 19: 281-286.
17. Iwakura, Y., S. Nakae, S. Saijo, and H. Ishigame. 2008. The roles of IL-17A in inflammatory immune responses and host defense against pathogens. Immunol. Rev. 226: 57-79.
18. Mbow, M., B. M. Larkin, L. Meurs, L. J. Wammes, S. E. de Jong, L. A. Labuda, M. Camara, H. H. Smits, K. Polman, T. N. Dieye, et al. 2013. T-helper 17 cells are associated with pathology in human schistosomiasis. J. Infect. Dis. 207: 186-195.
19. Medzhitov, R. 2007. TLR-mediated innate immune recognition. Semin. Immunol. 19: 1-2.
20. Takeuchi, O., and S. Akira. 2010. Pattern recognition receptors and inflammation. Cell 140: 805-820.
21. Robinson, M. J., D. Sancho, E. C. Slack, S. LeibundGut-Landmann, and C. Reis e Sousa. 2006. Myeloid C-type lectins in innate immunity. Nat. Immunol. 7: 1258-1265.
22. Geijtenbeek, T. B., and S. I. Gringhuis. 2009. Signalling through C-type lectin receptors: shaping immune responses. Nat. Rev. Immunol. 9: 465-479.
23. Cummings, R. D., and A. K. Nyame. 1999. Schistosome glysoconjugates. Biochim. Biophys. Acta 1455: 363-374.
24. Hokke, C. H., and A. M. Deelder. 2001. Schistosome glycoconjugates in hostparasite interplay. Glycoconj. J. 18: 573-587.
25. van Die, I., S. J. van Vliet, A. K. Nyame, R. D. Cummings, C. M. Bank, B. Appelmelk, T. B. Geijtenbeek, and Y. van Kooyk. 2003. The dendritic cellspecific C-type lectin DC-SIGN is a receptor for Schistosoma mansoni egg antigens and recognizes the glycan antigen Lewis x. Glycobiology 13: 471-478.
26. Hokke, C. H., and M. Yazdanbakhsh. 2005. Schistosome glycans and innate immunity. Parasite Immunol. 27: 257-264.
27. Reimand, J., T. Arak, and J. Vilo. 2011. g:Profiler-a web server for functional interpretation of gene lists (2011 update). Nucleic Acids Res. 39(Web Server issue): W307-315.
28. Park, C. G., K. Takahara, E. Umemoto, Y. Yashima, K. Matsubara, Y. Matsuda, B. E. Clausen, K. Inaba, and R. M. Steinman. 2001. Five mouse homologues of the human dendritic cell C-type lectin, DC-SIGN. Int. Immunol. 13: 1283-1290.
29. Cheong, C., I. Matos, J. H. Choi, D. B. Dandamudi, E. Shrestha, M. P. Longhi, K. L. Jeffrey, R. M. Anthony, C. Kluger, G. Nchinda, et al. 2010. Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209(+) dendritic cells for immune T cell areas. Cell 143: 416-429.
30. Powlesland, A. S., E. M. Ward, S. K. Sadhu, Y. Guo, M. E. Taylor, and K. Drickamer. 2006. Widely divergent biochemical properties of the complete set of mouse DC-SIGN-related proteins. J. Biol. Chem. 281: 20440-20449.
31. van Vliet, S. J., J. J. García-Vallejo, and Y. van Kooyk. 2008. Dendritic cells and C-type lectin receptors: coupling innate to adaptive immune responses. Immunol. Cell Biol. 86: 580-587.
32. Geijtenbeek, T. B., R. Torensma, S. J. van Vliet, G. C. van Duijnhoven, G. J. Adema, Y. van Kooyk, and C. G. Figdor. 2000. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100: 575-585.
33. Geijtenbeek, T. B., D. S. Kwon, R. Torensma, S. J. van Vliet, G. C. van Duijnhoven, J. Middel, I. L. Cornelissen, H. S. Nottet, V. N. KewalRamani, D. R. Littman, et al. 2000. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100: 587-597.
34. Caparrós, E., P. Munoz, E. Sierra-Filardi, D. Serrano- Gómez, A. Puig-Krölger, J. L. Rodríguez-Fernández, M. Mellado, J. Sancho, M. Zubiaur, and A. L. Corbí. 2006. DC-SIGN ligation on dendritic cells results in ERK and PI3K activation and modulates cytokine production. Blood 107: 3950-3958.
35. Gringhuis, S. I., J. den Dunnen, M. Litjens, B. van Het Hof, Y. van Kooyk, and T. B. Geijtenbeek. 2007. C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NFkappaB. Immunity 26: 605-616.
36. Gringhuis, S. I., J. den Dunnen, M. Litjens, M. van der Vlist, and T. B. Geijtenbeek. 2009. Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori. Nat. Immunol. 10: 1081-1088.
37. Johnson, T. R., J. S. McLellan, and B. S. Graham. 2012. Respiratory syncytial virus glycoprotein G interacts with DC-SIGN and L-SIGN to activate ERK1 and ERK2. J. Virol. 86: 1339-1347.
38. Bettelli, E., Y. Carrier, W. Gao, T. Korn, T. B. Strom, M. Oukka, H. L. Weiner, and V. K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
39. Sansonetti, P. J. 2006. The innate signaling of dangers and the dangers of innate signaling. Nat. Immunol. 7: 1237-1242.
40. Kanneganti, T. D., M. Lamkanfi, and G. Núñez. 2007. Intracellular NOD-like receptors in host defense and disease. Immunity 27: 549-559.
41. Van Liempt, E., A. Imberty, C. M. Bank, S. J. Van Vliet, Y. Van Kooyk, T. B. Geijtenbeek, and I. Van Die. 2004. Molecular basis of the differences in binding properties of the highly related C-type lectins DC-SIGN and L-SIGN to Lewis X trisaccharide and Schistosoma mansoni egg antigens. J. Biol. Chem. 279: 33161-33167.
42. Meyer, S., E. van Liempt, A. Imberty, Y. van Kooyk, H. Geyer, R. Geyer, and I. van Die. 2005. DC-SIGN mediates binding of dendritic cells to authentic pseudo-LewisY glycolipids of Schistosoma mansoni cercariae, the first parasitespecific ligand of DC-SIGN. J. Biol. Chem. 280: 37349-37359.
43. van Vliet, S. J., E. van Liempt, E. Saeland, C. A. Aarnoudse, B. Appelmelk, T. Irimura, T. B. Geijtenbeek, O. Blixt, R. Alvarez, I. van Die, and Y. van Kooyk. 2005. Carbohydrate profiling reveals a distinctive role for the C-type lectin MGL in the recognition of helminth parasites and tumor antigens by dendritic cells. Int. Immunol. 17: 661-669.
44. van Liempt, E., S. J. van Vliet, A. Engering, J. J. García Vallejo, C. M. Bank, M. Sanchez-Hernandez, Y. van Kooyk, and I. van Die. 2007. Schistosoma mansoni soluble egg antigens are internalized by human dendritic cells through multiple C-type lectins and suppress TLR-induced dendritic cell activation. Mol. Immunol. 44: 2605-2615.
45. Cass, C. L., J. R. Johnson, L. L. Califf, T. Xu, H. J. Hernandez, M. J. Stadecker, J. R. Yates, III, and D. L. Williams. 2007. Proteomic analysis of Schistosoma mansoni egg secretions. Mol. Biochem. Parasitol. 155: 84-93.
46. van Stijn, C. M., S. Meyer, M. van den Broek, S. C. Bruijns, Y. van Kooyk, R. Geyer, and I. van Die. 2010. Schistosoma mansoni worm glycolipids induce an inflammatory phenotype in human dendritic cells by cooperation of TLR4 and DC-SIGN. Mol. Immunol. 47: 1544-1552.
47. Meevissen, M. H., M. Yazdanbakhsh, and C. H. Hokke. 2012. Schistosoma mansoni egg glycoproteins and C-type lectins of host immune cells: molecular partners that shape immune responses. Exp. Parasitol. 132: 14-21.
48. Ritter, M., O. Gross, S. Kays, J. Ruland, F. Nimmerjahn, S. Saijo, J. Tschopp, L. E. Layland, and C. Prazeres da Costa. 2010. Schistosoma mansoni triggers Dectin-2, which activates the Nlrp3 inflammasome and alters adaptive immune responses. Proc. Natl. Acad. Sci. USA 107: 20459-20464.
49. Saunders, S. P., C. M. Walsh, J. L. Barlow, N. E. Mangan, P. R. Taylor, A. N. McKenzie, P. Smith, and P. G. Fallon. 2009. The C-type lectin SIGNR1 binds Schistosoma mansoni antigens in vitro, but SIGNR1-deficient mice have normal responses during schistosome infection. Infect. Immun. 77: 399-404.
50. Feinberg, H., D. A. Mitchell, K. Drickamer, and W. I. Weis. 2001. Structural basis for selective recognition of oligosaccharides by DC-SIGN and DC-SIGNR. Science 294: 2163-2166.
51. Figdor, C. G., Y. van Kooyk, and G. J. Adema. 2002. C-type lectin receptors on dendritic cells and Langerhans cells. Nat. Rev. Immunol. 2: 77-84.
52. Lu, X. J., J. Chen, C. H. Yu, Y. H. Shi, Y. Q. He, R. C. Zhang, Z. A. Huang, J. N. Lv, S. Zhang, and L. Xu. 2013. LECT2 protects mice against bacterial sepsis by activating macrophages via the CD209a receptor. J. Exp. Med. 210: 5-13.
53. Wellbrock, C., M. Karasarides, and R. Marais. 2004. The RAF proteins take centre stage. Nat. Rev. Mol. Cell Biol. 5: 875-885.
54. Kolch, W. 2005. Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev. Mol. Cell Biol. 6: 827-837.
55. Numazaki, M., C. Kato, Y. Kawauchi, T. Kajiwara, M. Ishii, and N. Kojima. 2009. Cross-linking of SIGNR1 activates JNK and induces TNF-alpha production in RAW264.7 cells that express SIGNR1. Biochem. Biophys. Res. Commun. 386: 202-206.
56. Tanne, A., B. Ma, F. Boudou, L. Tailleux, H. Botella, E. Badell, F. Levillain, M. E. Taylor, K. Drickamer, J. Nigou, et al. 2009. A murine DC-SIGN homologue contributes to early host defense against Mycobacterium tuberculosis. J. Exp. Med. 206: 2205-2220.
57. Zhu, L., Y. Wu, H. Wei, S. Yang, N. Zhan, X. Xing, and B. Peng. 2012. Upregulation of IL-23 p19 expression in human periodontal ligament fibroblasts by IL-1b via concurrent activation of the NF-kB and MAPKs/AP-1 pathways. Cytokine 60: 171-178.
58. Thomas, P. G., M. R. Carter, O. Atochina, A. A. Da'Dara, D. Piskorska, E. McGuire, and D. A. Harn. 2003. Maturation of dendritic cell 2 phenotype by a helminth glycan uses a Toll-like receptor 4-dependent mechanism. J. Immunol. 171: 5837-5841.
59. Kane, C. M., L. Cervi, J. Sun, A. S. McKee, K. S. Masek, S. Shapira, C. A. Hunter, and E. J. Pearce. 2004. Helminth antigens modulate TLR-initiated dendritic cell activation. J. Immunol. 173: 7454-7461.
60. Goodridge, H. S., M. R. Deehan, W. Harnett, and M. M. Harnett. 2005. Subversion of immunological signalling by a filarial nematode phosphorylcholinecontaining secreted product. Cell. Signal. 17: 11-16.
61. Carvalho, L., J. Sun, C. Kane, F. Marshall, C. Krawczyk, and E. J. Pearce. 2009. Review series on helminths, immune modulation and the hygiene hypothesis: mechanisms underlying helminth modulation of dendritic cell function. Immunology 126: 28-34.
62. Harnett, M. M., A. J. Melendez, and W. Harnett. 2010. The therapeutic potential of the filarial nematode-derived immunodulator, ES-62 in inflammatory disease. Clin. Exp. Immunol. 159: 256-267.
63. van Riet, E., F. C. Hartgers, and M. Yazdanbakhsh. 2007. Chronic helminth infections induce immunomodulation: consequences and mechanisms. Immunobiology 212: 475-490.
64. Everts, B., G. Perona-Wright, H. H. Smits, C. H. Hokke, A. J. van der Ham, C. M. Fitzsimmons, M. J. Doenhoff, J. van der Bosch, K. Mohrs, H. Haas, et al. 2009. Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses. J. Exp. Med. 206: 1673-1680.
65. Steinfelder, S., J. F. Andersen, J. L. Cannons, C. G. Feng, M. Joshi, D. Dwyer, P. Caspar, P. L. Schwartzberg, A. Sher, and D. Jankovic. 2009. The major component in schistosome eggs responsible for conditioning dendritic cells for Th2 polarization is a T2 ribonuclease (omega-1). J. Exp. Med. 206: 1681-1690.
66. Klaver, E. J., L. M. Kuijk, L. C. Laan, H. Kringel, S. J. van Vliet, G. Bouma, R. D. Cummings, G. Kraal, and I. van Die. 2013. Trichuris suis-induced modulation of human dendritic cell function is glycan-mediated. Int. J. Parasitol. 43: 191-200.
67. LeibundGut-Landmann, S., O. Gross, M. J. Robinson, F. Osorio, E. C. Slack, S. V. Tsoni, E. Schweighoffer, V. Tybulewicz, G. D. Brown, J. Ruland, and C. Reis e Sousa. 2007. Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat. Immunol. 8: 630-638.
68. Gringhuis, S. I., T. M. Kaptein, B. A. Wevers, B. Theelen, M. van der Vlist, T. Boekhout, and T. B. Geijtenbeek. 2012. Dectin-1 is an extracellular pathogen sensor for the induction and processing of IL-1b via a noncanonical caspase-8 inflammasome. Nat. Immunol. 13: 246-254.