Trichuris suis soluble products induce Rab7b expression and limit TLR4 responses in human dendritic cells

Genes and Immunity

Volumn 16, Issue 6, 2015, Pages 378-387

  Klaver, E J ^a   Van Der Pouw Kraan, T C T M ^a   Laan, L C ^a   Kringel, H ^b   Cummings, R D ^c   Bouma, G ^a   Kraal, G ^a   Van Die, I ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; GUANINE NUCLEOTIDE BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN P50; PROTEIN P52; RAB7 PROTEIN; RAB7B PROTEIN; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; UNCLASSIFIED DRUG; RAB PROTEIN; TLR4 PROTEIN, HUMAN; TRANSCRIPTOME;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; DOWN REGULATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOSTIMULATION; MYELOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRICHURIS SUIS; UPREGULATION; ANIMAL; DRUG EFFECTS; IMMUNOLOGY; INFLAMMATION; METABOLISM; PARASITOLOGY; TRICHURIS;

ANIMALS; DENDRITIC CELLS; DOWN-REGULATION; HUMANS; INFLAMMATION; LIPOPOLYSACCHARIDES; RAB GTP-BINDING PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TRANSCRIPTOME; TRICHURIS;

EID: 84941025618     PISSN: 14664879     EISSN: 14765470     Source Type: Journal    
DOI: 10.1038/gene.2015.18     Document Type: Article

References (42)

1. Summers RW, Elliott DE, Urban Jr JF, Thompson R, Weinstock JV. Trichuris suis therapy in Crohn's disease. Gut 2005; 54: 87-90
2. Weinstock JV, Elliott DE. Helminths and the IBD hygiene hypothesis. Inflamm Bowel Dis 2009; 15: 128-133
3. Fleming JO, Weinstock JV. Clinical trials of helminth therapy in autoimmune diseases: rationale and findings. Parasite Immunol 2015; 37: 277-292
4. Correale J, Farez M. Association between parasite infection and immune responses in multiple sclerosis. Ann Neurol 2007; 61: 97-108
5. Correale J, Farez MF. The impact of parasite infections on the course of multiple sclerosis. J Neuroimmunol 2011; 233: 6-11
6. Kuijk LM, Van Die I. Worms to the rescue: can worm glycans protect from autoimmune diseases?. IUBMB Life 2010; 62: 303-312
7. McKay DM. The therapeutic helminth?. Trends Parasitol 2009; 25: 109-114
8. Harnett W, McInnes IB, Harnett MM. ES-62, a filarial nematode-derived immunomodulator with anti-inflammatory potential. Immunol Lett 2004; 94: 27-33
9. Sewell D, Qing Z, Reinke E, Elliot D, Weinstock J, Sandor M et al. Immunomodulation of experimental autoimmune encephalomyelitis by helminth ova immunization. Int Immunol 2003; 15: 59-69
10. Zaccone P, Fehervari Z, Jones FM, Sidobre S, Kronenberg M, Dunne DW et al. Schistosoma mansoni antigens modulate the activity of the innate immune response and prevent onset of type 1 diabetes. Eur J Immunol 2003; 33: 1439-1449
11. Kuijk LM, Klaver EJ, Kooij G, Van Der Pol SM, Heijnen P, Bruijns SC, Kringel H et al. Soluble helminth products suppress clinical signs in murine experimental autoimmune encephalomyelitis and differentially modulate human dendritic cell activation. Mol Immunol 2012; 51: 210-218
12. Klaver EJ, Kuijk LM, Laan LC, Kringel H, Van Vliet SJ, Bouma G et al. Trichuris suisinduced modulation of human dendritic cell function is glycan-mediated. Int J Parasitol 2013; 43: 191-200
13. Ottow MK, Klaver EJ, Van Der Pouw Kraan TC, Heijnen PD, Laan LC, Kringel H et al. The helminth Trichuris suis suppresses TLR4-induced inflammatory responses in human macrophages. Genes Immun 2014; 15: 477-486
14. Akira S, Takeda K, Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2001; 2: 675-680
15. Racke MK, Hu W, Lovett-Racke AE. PTX cruiser: driving autoimmunity via TLR4. Trends Immunol 2005; 26: 289-291
16. Hennessy EJ, Parker AE, O'Neill LA. Targeting Toll-like receptors: emerging therapeutics?. Nat Rev Drug Discov 2010; 9: 293-307
17. Palsson-McDermott EM, O'Neill LA. Signal transduction by the lipopolysaccharide receptor, Toll-like receptor-4. Immunology 2004; 113: 153-162
18. Hamilton CM, Dowling DJ, Loscher CE, Morphew RM, Brophy PM, O'Neill SM. The Fasciola hepatica tegumental antigen suppresses dendritic cell maturation and function. Infect Immun 2009; 77: 2488-2498
19. Segura M, Su Z, Piccirillo C, Stevenson MM. Impairment of dendritic cell function by excretory-secretory products: a potential mechanism for nematode-induced immunosuppression. Eur J Immunol 2007; 37: 1887-1904
20. Van Liempt E, Van Vliet SJ, Engering A, Garcia Vallejo JJ, Bank CM, Sanchez-Hernandez M et al. 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 2007; 44: 2605-2615
21. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005; 102: 15545-15550
22. Chen FE, Kempiak S, Huang DB, Phelps C, Ghosh G. Construction, expression, purification and functional analysis of recombinant NFkappaB p50/p65 heterodimer. Protein Eng 1999; 12: 423-428
23. Hoffmann A, Natoli G, Ghosh G. Transcriptional regulation via the NF-kappaB signaling module. Oncogene 2006; 25: 6706-6716
24. Wang Y, Chen T, Han C, He D, Liu H, An H et al. Lysosome-Associated small Rab GTPase Rab7b negatively regulates TLR4 signaling in macrophages by promoting lysosomal degradation of TLR4. Blood 2007; 110: 962-971
25. Vukman KV, Adams PN, O'Neill SM. Fasciola hepatica tegumental coat antigen suppresses MAPK signalling in dendritic cells and up-regulates the expression of SOCS3. Parasite Immunol 2013; 35: 234-238
26. Puneet P, McGrath MA, Tay HK, Al-Riyami L, Rzepecka J, Moochhala SM et al. The helminth product ES-62 protects against septic shock via Toll-like receptor 4-dependent autophagosomal degradation of the adaptor MyD88. Nat Immunol 2011; 12: 344-351
27. Van Stijn CM, Meyer S, Van den Broek M, Bruijns SC, Van Kooyk Y, Geyer R et al. Schistosoma mansoni worm glycolipids induce an inflammatory phenotype in human dendritic cells by cooperation of TLR4 and DC-SIGN. Mol Immunol 2010; 47: 1544-1552
28. Aloisi AL, Bucci C. Rab GTPases-cargo direct interactions: fine modulators of intracellular trafficking. Histol Histopathol 2013; 28: 839-849
29. Yao M, Liu X, Li D, Chen T, Cai Z, Cao X. Late endosome/lysosome-localized Rab7b suppresses TLR9-initiated proinflammatory cytokine and type I IFN production in macrophages. J Immunol 2009; 183: 1751-1758
30. Progida C, Cogli L, Piro F, De Luca A, Bakke O, Bucci C. Rab7b controls trafficking from endosomes to the TGN. J Cell Science 2010; 123: 1480-1491
31. Barton GM, Kagan JC. A cell biological view of Toll-like receptor function: regulation through compartmentalization. Nat Rev Immunol 2009; 9: 535-542
32. Lin YC, Huang DY, Chu CL, Lin YL, Lin WW. The tyrosine kinase Syk differentially regulates Toll-like receptor signaling downstream of the adaptor molecules TRAF6 and TRAF3. Sci Signal 2013; 6: ra71
33. Gringhuis SI, den Dunnen J, Litjens M, Van Het Hof B, Van Kooyk Y, Geijtenbeek TB. C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-kappaB. Immunity 2007; 26: 605-616
34. Van Vliet SJ, Bay S, Vuist IM, Kalay H, Garcia-Vallejo JJ, Leclerc C et al. MGL signaling augments TLR2-mediated responses for enhanced IL-10 and TNF-Alpha secretion. J Leukoc Biol 2013; 94: 315-323
35. Gringhuis SI, Kaptein TM, Wevers BA, Mesman AW, Geijtenbeek TB. Fucose-specific DC-SIGN signalling directs T helper cell type-2 responses via IKKepsilon- and CYLD-dependent Bcl3 activation. Nat Commun 2014; 5: 3898
36. Jex AR, Nejsum P, Schwarz EM, Hu L, Young ND, Hall RS et al. Genome and transcriptome of the porcine whipworm Trichuris suis. Nat Genet 2014; 46: 701-706
37. Van Stijn CM, Van den Broek M, Van De Weerd R, Visser M, Tasdelen I, Tefsen B et al. Regulation of expression and secretion of galectin-3 in human monocyte-derived dendritic cells. Mol Immunol 2009; 46: 3292-3299
38. Schirmer SH, Fledderus JO, Van Der Laan AM, Van Der Pouw-Kraan TC, Moerland PD, Volger OL et al. Suppression of inflammatory signaling in monocytes from patients with coronary artery disease. J Mol Cell Cardiol 2009; 46: 177-185
39. Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003; 19: 185-193
40. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001; 98: 5116-5121
41. Garcia-Vallejo JJ, Van Liempt E, da Costa Martins P, Beckers C, Van het Hof B, Gringhuis SI et al. DC-SIGN mediates adhesion and rolling of dendritic cells on primary human umbilical vein endothelial cells through LewisY antigen expressed on ICAM-2. Mol Immunol 2008; 45: 2359-2369
42. Garcia-Vallejo JJ, Gringhuis SI, Van Dijk W, Van Die I. Gene expression analysis of glycosylation-related genes by real-time polymerase chain reaction. Methods Mol Biol 2006; 347: 187-209