Helminth-excreted/secreted products are recognized by multiple receptors on DCs to block the TLR response and bias Th2 polarization in a cRAF dependent pathway

FASEB Journal

Volumn 27, Issue 11, 2013, Pages 4547-4560

  Terrazas, César A ^a,b   Alcántara Hernández, Marcela ^c   Bonifaz, Laura ^c   Terrazas, Luis I ^a   Satoskar, Abhay R ^a,b  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^c INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

Author keywords

CLRs; Dendritic cell; Immunomodulation; Mannose receptor; MGL

Indexed keywords

3 (3,5 DIBROMO 4 HYDROXYBENZYLIDENE) 1,3 DIHYDRO 5 IODO 2 INDOLONE; B7 ANTIGEN; CD14 ANTIGEN; CD86 ANTIGEN; DIMETHYL SULFOXIDE; EGTAZIC ACID; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 4; LECTIN; LECTIN RECEPTOR; LIPOPOLYSACCHARIDE; MACROPHAGE GALACTOSE C TYPE LECTIN; MANNOSE RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; OVALBUMIN; PROTEIN; PROTEIN CRAF; RAS PROTEIN; RECEPTOR; SYNAPTOTAGMIN I; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 6; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CELL LINE; CELL MATURATION; CYTOKINE PRODUCTION; DENDRITIC CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOMODULATION; INTRACELLULAR SIGNALING; MACROPHAGE; MOUSE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; TAENIA CRASSICEPS; TH1 CELL; TH2 CELL; WESTERN BLOTTING; WILD TYPE;

CLRS; DENDRITIC CELL; IMMUNOMODULATION; MANNOSE RECEPTOR; MGL;

ANIMALS; ASIALOGLYCOPROTEINS; DENDRITIC CELLS; DOWN-REGULATION; IMMUNOMODULATION; INTERLEUKIN-12; LECTINS, C-TYPE; MANNOSE-BINDING LECTINS; MAP KINASE SIGNALING SYSTEM; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-RAF; RECEPTORS, CELL SURFACE; TAENIA; TH2 CELLS; TOLL-LIKE RECEPTOR 2; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84887064527     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-228932     Document Type: Article

References (51)

1. Maizels, R. M., Balic, A., Gomez-Escobar, N., Nair, M., and Taylor., M. D., and Allen, J. E. (2004) Helminth parasites-masters of regulation. Immunol. Rev. 201, 89-116
2. Terrazas, C. A., and Terrazas., L. I., and Gomez-Garcia, L. (2010) Modulation of dendritic cell responses by parasites: a common strategy to survive. J. Biomed. Bio/Technol. 2010, 357106 doi: 10.1155/2010/357106
3. MacDonald, A. S., and Maizels, R. M. (2008) Alarming dendritic cells for Th2 induction. J. Exp. Med. 205, 13-17 (Pubitemid 351185710)
4. Kawai, T., and Akira, S. (2007) TLR signaling. Sem. Immunol. 19, 24-32 (Pubitemid 46498752)
5. Pulendran, B., and Artis, D. (2012) New paradigms in type 2 immunity. Science 337, 431-435
6. Tundup, S., Srivastava, L., and Harn, D. A., Jr. (2012) Polarization of host immune responses by helminth-expressed glycans. Ann. N. Y. Acad. Sci. 1253, E1-E13
7. Okano, M., and Satoskar., A. R., Nishizaki, K., Abe, M., Harn, D. A., Jr. (1999) Induction of Th2 responses and IgE is largely due to carbohydrates functioning as adjuvants on Schistosoma mansoni egg antigens. J. Immunol. 163, 6712-6717
8. Gomez-Garcia, L., Rivera-Montoya, I., Rodriguez-Sosa, M., and Terrazas, L. I. (2006) Carbohydrate components of Taenia crassiceps metacestodes display Th2-adjuvant and anti-inflammatory properties when co-injected with bystander antigen. Parasitol. Res. 99, 440-448 (Pubitemid 44426738)
9. Okano, M., and Satoskar., A. R., Nishizaki, K., and Harn, D. A., Jr. (2001) Lacto-N-fucopentaose III found on Schistosoma mansoni egg antigens functions as adjuvant for proteins by inducing Th2-type response. J. Immunol. 167, 442-450 (Pubitemid 32567810)
10. Van Liempt, E., van Vliet, S. J., Engering, A., Garcia Vallejo, J. J., Bank, C. M., Sanchez-Hernandez, M., van Kooyk, Y., and van Die, I. (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 (Pubitemid 46240322)
11. Guasconi, L., and Serradell., M. C., Garro, A. P., Iacobelli, L., and Masih, D. T. (2011) C-type lectins on macrophages participate in the immunomodulatory response to Fasciola hepatica products. Immunology 133, 386-396
12. Terrazas, L. I. (2008) The complex role of pro- and anti-inflammatory cytokines in cysticercosis: immunological lessons from experimental and natural hosts. Curr. Topics Med. Chem. 8, 383-392 (Pubitemid 351791016)
13. Terrazas, L. I., Bojalil, R., Govezensky, T., and Larralde, C. (1998) Shift from an early protective Th1-type immune response to a late permissive Th2-type response in murine cysticercosis (Taenia crassiceps). J. Parasitol. 84, 74-81 (Pubitemid 28125434)
14. Villa, O. F., and Kuhn, R. E. (1996) Mice infected with the larvae of Taenia crassiceps exhibit a Th2-like immune response with concomitant anergy and downregulation of Th1-associated phenomena. Parasitology 112(Pt. 6), 561-570 (Pubitemid 26000515)
15. Terrazas, C. A., Sanchez-Munoz, F., Mejia-Dominguez, A. M., Amezcua-Guerra, L. M., Terrazas, L. I., Bojalil, R., and Gomez-Garcia, L. (2011) Cestode antigens induce a tolerogenic-like phenotype and inhibit LPS inflammatory responses in human dendritic cells. Int. J. Biol. Sci. 7, 1391-1400
16. Terrazas, C. A., Gomez-Garcia, L., and Terrazas, L. I. (2010) Impaired pro-inflammatory cytokine production and increased Th2-biasing ability of dendritic cells exposed to Taenia excreted/secreted antigens: A critical role for carbohydrates but not for STAT6 signaling. Int. J. Parasitol. 40, 1051-1062
17. Gringhuis, S. I., and Geijtenbeek, T. B. (2010) Carbohydrate signaling by C-type lectin DC-SIGN affects NF-kappaB activity. Methods Enzymol. 480, 151-164
18. Lee, J. J., Dissanayake, S., Panico, M., Morris, H. R., Dell, A., and Haslam, S. M. (2005) Mass spectrometric characterisation of Taenia crassiceps metacestode N-glycans. Mol. Biochem. Parasitol. 143, 245-249 (Pubitemid 41206479)
19. Gringhuis, S. I., den Dunnen, J., Litjens, M., van der Vlist, M., Wevers, B., and Bruijns., S. C., and Geijtenbeek, T. B. (2009) Dectin-1 directs T helper cell differentiation by controlling noncanonical NF-kappaB activation through Raf-1 and Syk. Nat. Immunol. 10, 203-213
20. Gringhuis, S. I., den Dunnen, J., Litjens, M., van Het Hof, B., van Kooyk, Y., and Geijtenbeek, T. B. (2007) C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-kappaB. Immunity 26, 605-616 (Pubitemid 46756345)
21. Reyes, J. L., and Terrazas., C. A., Vera-Arias, L., and Terrazas, L. I. (2009) Differential response of antigen presenting cells from susceptible and resistant strains of mice to Taenia crassiceps infection. Infect. Genet. Evol. 9, 1115-1127
22. Reyes, J. L., Espinoza-Jimenez, A. F., Gonzalez, M. I., Verdin, L., and Terrazas, L. I. (2011) Taenia crassiceps infection abrogates experimental autoimmune encephalomyelitis. Cell. Immunol. 267, 77-87
23. Reyes, J. L., and Gonzalez., M. I., Ledesma-Soto, Y., Satoskar, A. R., and Terrazas, L. I. (2011) TLR2 mediates immunity to experimental cysticercosis. Int. J. Biol. Sci. 7, 1323-1333
24. Goodridge, H. S., and Marshall., F. A., Else, K. J., Houston, K. M., Egan, C., Al-Riyami, L., Liew, F. Y., Harnett, W., and Harnett, M. M. (2005) Immunomodulation via novel use of TLR4 by the filarial nematode phosphorylcholine-containing secreted product, ES-62. J. Immunol. 174, 284-293 (Pubitemid 40007415)
25. van der Kleij, D., Latz, E., and Brouwers., J. F., Kruize, Y. C., Schmitz, M., Kurt-Jones, E. A., Espevik, T., de Jong, E. C., Kapsenberg, M. L., Golenbock, D. T., Tielens, A. G., and Yazdanbakhsh, M. (2002) A novel host-parasite lipid cross-talk. Schistosomal lysophosphatidylserine activates toll-like receptor 2 and affects immune polarization. J. Biol. Chem. 277, 48122-48129 (Pubitemid 35470760)
26. Vanhoutte, F., Breuilh, L., Fontaine, J., Zouain, C. S., Mallevaey, T., Vasseur, V., Capron, M., Goriely, S., Faveeuw, C., Ryffel, B., and Trottein, F. (2007) Toll-like receptor (TLR)2 and TLR3 sensing is required for dendritic cell activation, but dispensable to control Schistosoma mansoni infection and pathology. Microbes Infect. 9, 1606-1613 (Pubitemid 350225744)
27. Hovius, J. W., de Jong, M. A., den Dunnen, J., Litjens, M., Fikrig, E., van der Poll, T., Gringhuis, S. I., and Geijtenbeek, T. B. (2008) Salp15 binding to DC-SIGN inhibits cytokine expression by impairing both nucleosome remodeling and mRNA stabilization. PLoS Pathogens 4, e31
28. Roy, S., Wyse, B., and Hancock, J. F. (2002) H-Ras signaling and K-Ras signaling are differentially dependent on endocytosis. Mol. Cell. Biol. 22, 5128-5140 (Pubitemid 34700703)
29. Phythian-Adams, A. T., Cook, P. C., and Lundie., R. J., Jones, L. H., Smith, K. A., and Barr., T. A., Hochweller, K., Anderton, S. M., Hammerling, G. J., Maizels, R. M., and MacDonald, A. S. (2010) CD11c depletion severely disrupts Th2 induction and development in vivo. J. Exp. Med. 207, 2089-2096
30. Whelan, M., and Harnett., M. M., Houston, K. M., Patel, V., Harnett, W., and Rigley, K. P. (2000) A filarial nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 cells. J. Immunol. 164, 6453-6460 (Pubitemid 30408828)
31. Balic, A., Harcus, Y., Holland, M. J., and Maizels, R. M. (2004) Selective maturation of dendritic cells by Nippostrongylus brasiliensis-secreted proteins drives Th2 immune responses. Eur. J. Immunol. 34, 3047-3059 (Pubitemid 39549384)
32. Kane, C. M., Cervi, L., Sun, J., McKee, A. S., and Masek., K. S., Shapira, S., Hunter, C. A., and Pearce, E. J. (2004) Helminth antigens modulate TLR-initiated dendritic cell activation. J. Immunol. 173, 7454-7461 (Pubitemid 39628185)
33. Thomas, P. G., and Carter., M. R., Atochina, O., Da'Dara, A. A., Piskorska, D., McGuire, E., and Harn, D. A. (2003) Maturation of dendritic cell 2 phenotype by a helminth glycan uses a Toll-like receptor 4-dependent mechanism. J. Immunol. 171, 5837-5841 (Pubitemid 37467200)
34. Segura, M., Su, Z., Piccirillo, C., and Stevenson, M. M. (2007) Impairment of dendritic cell function by excretory-secretory products: a potential mechanism for nematode-induced immunosuppression. Eur. J. Immunol. 37, 1887-1904 (Pubitemid 47065127)
35. Everts, B., Hussaarts, L., Driessen, N. N., and Meevissen., M. H., Schramm, G., van der Ham, A. J., van der Hoeven, B., Scholzen, T., Burgdorf, S., Mohrs, M., Pearce, E. J., Hokke, C. H., Haas, H., Smits, H. H., and Yazdanbakhsh, M. (2012) Schistosome-derived omega-1 drives Th2 polarization by suppressing protein synthesis following internalization by the mannose receptor. J. Exp. Med. 209, 1753-1767, S1751
36. Van Vliet, S. J., Steeghs, L., Bruijns, S. C., and Vaezirad., M. M., Snijders Blok, C., Arenas Busto, J. A., Deken, M., van Putten, J. P., and van Kooyk, Y. (2009) Variation of Neisseria gonorrhoeae lipooligosaccharide directs dendritic cell-induced T helper responses. PLoS Pathogens 5, e1000625
37. Van Vliet, S. J., Bay, S., Vuist, I. M., Kalay, H., Garcia-Vallejo, J. J., Leclerc, C., and van Kooyk, Y. (2013) MGL signaling augments TLR2-mediated responses for enhanced IL-10 and TNF-alpha secretion. [E-pub ahead of print] J. Leukoc. Biol. doi: 10.1189/jlb.1012520
38. Robinson, M. J., Sancho, D., Slack, E. C., Leibund Gut-Landmann, S., and Reis e Sousa, C. (2006) Myeloid C-type lectins in innate immunity. Nat. Immunol. 7, 1258-1265 (Pubitemid 46111243)
39. Saunders, S. P., and Walsh., C. M., Barlow, J. L., Mangan, N. E., and Taylor., P. R., McKenzie, A. N., Smith, P., and Fallon, P. G. (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
40. Zhang, S., and Kaplan, M. H. (2000) The p38 mitogen-activated protein kinase is required for IL-12-induced IFN-gamma expression. J. Immunol. 165, 1374-1380 (Pubitemid 30604568)
41. Terrazas, C. A., Huitron, E., Vazquez, A., Juarez, I., and Camacho., G. M., Calleja, E. A., and Rodriguez-Sosa, M. (2011) MIF synergizes with Trypanosoma cruzi antigens to promote efficient dendritic cell maturation and IL-12 production via p38 MAPK. Int. J. Biol. Sci. 7, 1298-1310
42. Qian, C., Jiang, X., An, H., Yu, Y., Guo, Z., Liu, S., Xu, H., and Cao, X. (2006) TLR agonists promote ERK-mediated preferential IL-10 production of regulatory dendritic cells (diffDCs), leading to NK-cell activation. Blood 108, 2307-2315 (Pubitemid 44497514)
43. Poncini, C. V., Gimenez, G., Pontillo, C. A., Alba-Soto, C. D., de Isola, E. L., Piazzon, I., and Cappa, S. M. (2010) Central role of extracellular signal-regulated kinase and Toll-like receptor 4 in IL-10 production in regulatory dendritic cells induced by Trypanosoma cruzi. Mol. Immunol. 47, 1981-1988
44. Agrawal, S., Agrawal, A., Doughty, B., Gerwitz, A., Blenis, J., Van Dyke, T., and Pulendran, B. (2003) Cutting edge: different Toll-like receptor agonists instruct dendritic cells to induce distinct Th responses via differential modulation of extracellular signal-regulated kinase-mitogen- activated protein kinase and c-Fos. J. Immunol. 171, 4984-4989 (Pubitemid 37432777)
45. Thomas, P. G., and Carter., M. R., Da'dara, A. A., DeSimone, T. M., and Harn, D. A. (2005) A helminth glycan induces APC maturation via alternative NF-kappa B activation independent of I kappa B alpha degradation. J. Immunol. 175, 2082-2090 (Pubitemid 41113813)
46. Gringhuis, S. I., van der Vlist, M., van den Berg, L. M., den Dunnen, J., Litjens, M., and Geijtenbeek, T. B. (2010) HIV-1 exploits innate signaling by TLR8 and DC-SIGN for productive infection of dendritic cells. Nat. Immunol. 11, 419-426
47. Napoletano, C., and Zizzari., I. G., Rughetti, A., Rahimi, H., Irimura, T., Clausen, H., Wandall, H. H., Belleudi, F., Bellati, F., Pierelli, L., Frati, L., and Nuti, M. (2012) Targeting of macrophage galactose-type C-type lectin (MGL) induces DC signaling and activation. Eur. J. Immunol. 42, 936-945
48. Van de Veerdonk, F. L., Marijnissen, R. J., Kullberg, B. J., Koenen, H. J., Cheng, S. C., Joosten, I., van den Berg, W. B., Williams, D. L., van der Meer, J. W., Joosten, L. A., and Netea, M. G. (2009) The macrophage mannose receptor induces IL-17 in response to Candida albicans. Cell. Host. Microbe 5, 329-340
49. Li, S., and Sedivy, J. M. (1993) Raf-1 protein kinase activates the NF-kappa B transcription factor by dissociating the cytoplasmic NF-kappa B-I kappa B complex. Proc. Natl. Acad. Sci. U. S. A. 90, 9247-9251 (Pubitemid 23315760)
50. Abdi, K., and Singh., N. J., and Matzinger, P. (2012) Lipopolysaccharide-activated dendritic cells: "exhausted" or alert and waiting? J. Immunol. 188, 5981-5989
51. Amit, P., and Prasad., K. N., Kumar, G. R., Shweta, T., Sanjeev, J., and Kumar., P. V., and Mukesh, T. (2011) Immune response to different fractions of Taenia solium cyst fluid antigens in patients with neurocysticercosis. Exp. Parasitol. 127, 687-692