Similar inflammatory DC maturation signatures induced by TNF or Trypanosoma brucei antigens instruct default Th2-cell responses

European Journal of Immunology

Volumn 41, Issue 12, 2011, Pages 3479-3494

  Pletinckx, Katrien ^a   Stijlemans, Benoit ^b,c   Pavlovic, Vladimir ^a   Laube, Regina ^a   Brandl, Carolin ^a   Kneitz, Susanne ^a   Beschin, Alain ^b,c   De Baetselier, Patrick ^b,c   Lutz, Manfred B ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b FREE UNIVERSITY OF BRUSSELS   (Belgium)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

DCs; Microarray; Th2 cells; TNF; Trypanosoma

Indexed keywords

GAMMA INTERFERON; GLYCOPROTEIN; INTERLEUKIN 17; MESSENGER RNA; MYD88 DEPENDENT VARIANT SPECIFIC SURFACE GLYCOPROTEIN; MYELOID DIFFERENTIATION FACTOR 88; NOTCH RECEPTOR; PARASITE ANTIGEN; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; ASTHMA; CELL MATURATION; DENDRITIC CELL; GENE EXPRESSION; GENE EXPRESSION PROFILING; IMMUNE RESPONSE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; SYMPTOM; TH1 CELL; TH2 CELL; TRYPANOSOMA BRUCEI;

ANIMALS; ANTIGENS, PROTOZOAN; ASTHMA; CELL DIFFERENTIATION; DENDRITIC CELLS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENE EXPRESSION PROFILING; INFLAMMATION; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; SIGNAL TRANSDUCTION; TH1 CELLS; TH2 CELLS; TRYPANOSOMA BRUCEI BRUCEI; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION; VARIANT SURFACE GLYCOPROTEINS, TRYPANOSOMA;

EID: 82255164211     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201141631     Document Type: Article

References (85)

1. Steinman, R. M., Hawiger, D. and Nussenzweig, M. C., Tolerogenic dendritic cells. Annu. Rev. Immunol. 2003. 21: 685-711.
2. Banchereau, J. and Palucka, A. K., Dendritic cells as therapeutic vaccines against cancer. Nat. Rev. Immunol. 2005. 5: 296-306.
3. Coquerelle, C. and Moser, M., DC subsets in positive and negative regulation of immunity. Immunol. Rev. 2010. 234: 317-334.
4. Akira, S. and Takeda, K., Toll-like receptor signalling. Nat. Rev. Immunol. 2004. 4: 499-511.
5. Zhu, J., Yamane, H. and Paul, W. E., Differentiation of effector CD4T cell populations. Annu. Rev. Immunol. 2010. 28: 445-489.
6. Min, B. and Paul, W. E., Basophils: in the spotlight at last. Nat. Immunol. 2008. 9: 223-225.
7. Kapsenberg, M. L., Dendritic-cell control of pathogen-driven T-cell polarization. Nat. Rev. Immunol. 2003. 3: 984-993.
8. Moser, M. and Murphy, K. M., Dendritic cell regulation of TH1-TH2 development. Nat. Immunol. 2000. 1: 199-205.
9. Kalinski, P., Hilkens, C. M., Wierenga, E. A. and Kapsenberg, M. L., T-cell priming by type-1 and type-2 polarized dendritic cells: the concept of a third signal. Immunol. Today 1999. 20: 561-567.
10. Connerotte, T., Van Pel, A., Godelaine, D., Tartour, E., Schuler-Thurner, B., Lucas, S., Thielemans, K. et al., Functions of Anti-MAGE T-cells induced in melanoma patients under different vaccination modalities. Cancer Res. 2008. 68: 3931-3940.
11. Allard, S. D., Pletinckx, K., Breckpot, K., Heirman, C., Bonehill, A., Michiels, A., van Baalen, C. A. et al., Functional T-cell responses generated by dendritic cells expressing the early HIV-1 proteins Tat, Rev and Nef. Vaccine 2008. 26: 3735-3741.
12. Jenkins, S. J., Perona-Wright, G., Worsley, A. G., Ishii, N. and MacDonald, A. S., Dendritic cell expression of OX40 ligand acts as a costimulatory, not polarizing, signal for optimal Th2 priming and memory induction in vivo. J. Immunol. 2007. 179: 3515-3523.
13. Gonzalo, J. A., Tian, J., Delaney, T., Corcoran, J., Rottman, J. B., Lora, J., Al-garawi, A. et al., ICOS is critical for T helper cell-mediated lung mucosal inflammatory responses. Nat. Immunol. 2001. 2: 597-604.
14. Amsen, D., Blander, J. M., Lee, G. R., Tanigaki, K., Honjo, T. and Flavell, R. A., Instruction of distinct CD4 T helper cell fates by different notch ligands on antigen-presenting cells. Cell 2004. 117: 515-526.
15. Rincon, M., Anguita, J., Nakamura, T., Fikrig, E. and Flavell, R. A., Interleukin (IL)-6 directs the differentiation of IL-4-producing CD4+ T cells. J. Exp. Med. 1997. 185: 461-469.
16. Kalinski, P., Vieira, P. L., Schuitemaker, J. H., de Jong, E. C. and Kapsenberg, M. L., Prostaglandin E(2) is a selective inducer of interleukin-12 p40 (IL-12p40) production and an inhibitor of bioactive IL-12p70 heterodimer. Blood 2001. 97: 3466-3469.
17. Theiner, G., Gessner, A. and Lutz, M. B., The mast cell mediator PGD2 suppresses IL-12 release by dendritic cells leading to Th2 polarized immune responses in vivo. Immunobiology 2006. 211: 463-472.
18. Muthuswamy, R., Mueller-Berghaus, J., Haberkorn, U., Reinhart, T. A., Schadendorf, D. and Kalinski, P., PGE(2) transiently enhances DC expression of CCR7 but inhibits the ability of DCs to produce CCL19 and attract naive T cells. Blood 2010. 116: 1454-1459.
19. Maizels, R. M., Balic, A., Gomez-Escobar, N., Nair, M., Taylor, M. D. and Allen, J. E., Helminth parasites - masters of regulation. Immunol. Rev. 2004. 201: 89-116.
20. Anthony, R. M., Rutitzky, L. I., Urban, J. F., Jr., Stadecker, M. J. and Gause, W. C., Protective immune mechanisms in helminth infection. Nat. Rev. Immunol. 2007. 7: 975-987.
21. Perona-Wright, G., Jenkins, S. J. and MacDonald, A. S., Dendritic cell activation and function in response to Schistosoma mansoni. Int. J. Parasitol. 2006. 36: 711-721.
22. Balic, A., Harcus, Y., Holland, M. J. and Maizels, R. M., Selective maturation of dendritic cells by Nippostrongylus brasiliensis-secreted proteins drives Th2 immune responses. Eur. J. Immunol. 2004. 34: 3047-3059.
23. Menges, M., Rossner, S., Voigtlander, C., Schindler, H., Kukutsch, N. A., Bogdan, C., Erb, K. et al., Repetitive injections of dendritic cells matured with tumor necrosis factor alpha induce antigen-specific protection of mice from autoimmunity. J. Exp. Med. 2002. 195: 15-21.
24. Frick, J. S., Zahir, N., Muller, M., Kahl, F., Bechtold, O., Lutz, M. B., Kirschning, C. J. et al., Colitogenic and non-colitogenic commensal bacteria differentially trigger DC maturation and Th cell polarization: an important role for IL-6. Eur. J. Immunol. 2006. 36: 1537-1547.
25. Jiang, A., Bloom, O., Ono, S., Cui, W., Unternaehrer, J., Jiang, S., Whitney, J. A. et al., Disruption of E-cadherin-mediated adhesion induces a functionally distinct pathway of dendritic cell maturation. Immunity 2007. 27: 610-624.
26. Manicassamy, S., Reizis, B., Ravindran, R., Nakaya, H., Salazar-Gonzalez, R. M., Wang, Y. C. and Pulendran, B., Activation of beta-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science 2010. 329: 849-853.
27. Sporri, R. and Reis e Sousa, C., Inflammatory mediators are insufficient for full dendritic cell activation and promote expansion of CD4+ T cell populations lacking helper function. Nat. Immunol. 2005. 6: 163-170.
28. Frick, J. S., Grunebach, F. and Autenrieth, I. B., Immunomodulation by semi-mature dendritic cells: a novel role of Toll-like receptors and interleukin-6. Int. J. Med. Microbiol. 2010. 300: 19-24.
29. Lutz, M. B. and Schuler, G., Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol. 2002. 23: 445-449.
30. O'Garra, A., Vieira, P. L., Vieira, P. and Goldfeld, A. E., IL-10-producing and naturally occurring CD4+ Tregs: limiting collateral damage. J. Clin. Invest. 2004. 114: 1372-1378.
31. Verginis, P., Li, H. S. and Carayanniotis, G., Tolerogenic semimature dendritic cells suppress experimental autoimmune thyroiditis by activation of thyroglobulin-specific CD4+CD25+ T cells. J. Immunol. 2005. 174: 7433-7439.
32. van Duivenvoorde, L. M., Louis-Plence, P., Apparailly, F., van der Voort, E. I., Huizinga, T. W., Jorgensen, C. and Toes, R. E., Antigen-specific immunomodulation of collagen-induced arthritis with tumor necrosis factor-stimulated dendritic cells. Arthritis Rheum. 2004. 50: 3354-3364.
33. Wiethe, C., Schiemann, M., Busch, D., Haeberle, L., Kopf, M., Schuler, G. and Lutz, M. B., Interdependency of MHC class II/self-peptide and CD1d/self-glycolipid presentation by TNF-matured dendritic cells for protection from autoimmunity. J. Immunol. 2007. 178: 4908-4916.
34. Wiethe, C., Debus, A., Mohrs, M., Steinkasserer, A., Lutz, M. and Gessner, A., Dendritic cell differentiation state and their interaction with NKT cells determine Th1/Th2 differentiation in the murine model of Leishmania major infection. J. Immunol. 2008. 180: 4371-4381.
35. Stijlemans, B., Guilliams, M., Raes, G., Beschin, A., Magez, S. and De Baetselier, P., African trypanosomosis: from immune escape and immunopathology to immune intervention. Vet. Parasitol. 2007. 148: 3-13.
36. Vuitton, D. A. and Gottstein, B., Echinococcus multilocularis and its intermediate host: a model of parasite-host interplay. J. Biomed. Biotechnol. 2010. 2010: 923193.
37. Vanhamme, L., Pays, E., McCulloch, R. and Barry, J. D., An update on antigenic variation in African trypanosomes. Trends Parasitol. 2001. 17: 338-343.
38. Magez, S., Stijlemans, B., Radwanska, M., Pays, E., Ferguson, M. A. and De Baetselier, P., The glycosyl-inositol-phosphate and dimyristoylglycerol moieties of the glycosylphosphatidylinositol anchor of the trypanosome variant-specific surface glycoprotein are distinct macrophage-activating factors. J. Immunol. 1998. 160: 1949-1956.
39. Drennan, M. B., Stijlemans, B., Van den Abbeele, J., Quesniaux, V. J., Barkhuizen, M., Brombacher, F., De Baetselier, P. et al., The induction of a type 1 immune response following a Trypanosoma brucei infection is MyD88 dependent. J. Immunol. 2005. 175: 2501-2509.
40. Torri, A., Beretta, O., Ranghetti, A., Granucci, F., Ricciardi-Castagnoli, P. and Foti, M., Gene expression profiles identify inflammatory signatures in dendritic cells. PLoS One 2010. 5: e9404.
41. Yamazaki, S., Bonito, A. J., Spisek, R., Dhodapkar, M., Inaba, K. and Steinman, R. M., Dendritic cells are specialized accessory cells along with TGF- for the differentiation of Foxp3+CD4+ regulatory T cells from peripheral Foxp3 precursors. Blood 2007. 110: 4293-4302.
42. Larche, M., Akdis, C. A. and Valenta, R., Immunological mechanisms of allergen-specific immunotherapy. Nat. Rev. Immunol. 2006. 6: 761-771.
43. Baxter, A. G., The origin and application of experimental autoimmune encephalomyelitis. Nat. Rev. Immunol. 2007. 7: 904-912.
44. Brandl, C., Ortler, S., Herrmann, T., Cardell, S., Lutz, M. B. and Wiendl, H., B7-H1-deficiency enhances the potential of tolerogenic dendritic cells by activating CD1d-restricted type II NKT cells. PLoS One 2010. 5: e10800.
45. Trompette, A., Divanovic, S., Visintin, A., Blanchard, C., Hegde, R. S., Madan, R., Thorne, P. S. et al., Allergenicity resulting from functional mimicry of a Toll-like receptor complex protein. Nature 2009. 457: 585-588.
46. Hammad, H., Chieppa, M., Perros, F., Willart, M. A., Germain, R. N. and Lambrecht, B. N., House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat. Med. 2009. 15: 410-416.
47. Song, J., Duncan, M. J., Li, G., Chan, C., Grady, R., Stapleton, A. and Abraham, S. N., A novel TLR4-mediated signaling pathway leading to IL-6 responses in human bladder epithelial cells. PLoS Pathog. 2007. 3: e60.
48. Tachado, S. D., Mazhari-Tabrizi, R. and Schofield, L., Specificity in signal transduction among glycosylphosphatidylinositols of Plasmodium falciparum, Trypanosoma brucei, Trypanosoma cruzi and Leishmania spp. Parasite Immunol. 1999. 21: 609-617.
49. Krishnegowda, G., Hajjar, A. M., Zhu, J., Douglass, E. J., Uematsu, S., Akira, S., Woods, A. S. and Gowda, D. C., Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J. Biol. Chem. 2005. 280: 8606-8616.
50. Joffre, O., Nolte, M. A., Sporri, R. and Reis e Sousa, C., Inflammatory signals in dendritic cell activation and the induction of adaptive immunity. Immunol. Rev. 2009. 227: 234-247.
51. Perumal, N. B. and Kaplan, M. H., Regulating Il9 transcription in T helper cells. Trends Immunol. 2011. 32: 146-150.
52. Nolte, M. A., Leibundgut-Landmann, S., Joffre, O. and Reis e Sousa, C., Dendritic cell quiescence during systemic inflammation driven by LPS stimulation of radioresistant cells in vivo. J. Exp. Med. 2007. 204: 1487-1501.
53. Eddahri, F., Denanglaire, S., Bureau, F., Spolski, R., Leonard, W. J., Leo, O. and Andris, F., Interleukin-6/STAT3 signaling regulates the ability of naive T cells to acquire B-cell help capacities. Blood 2009. 113: 2426-2433.
54. Naik, S. H., Demystifying the development of dendritic cell subtypes, a little. Immunol. Cell Biol. 2008. 86: 439-452.
55. Maldonado-Lopez, R., De Smedt, T., Michel, P., Godfroid, J., Pajak, B., Heirman, C., Thielemans, K. et al., CD8alpha+ and CD8alpha- subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J. Exp. Med. 1999. 189: 587-592.
56. Pulendran, B., Smith, J. L., Caspary, G., Brasel, K., Pettit, D., Maraskovsky, E. and Maliszewski, C. R., Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. Proc. Natl. Acad. Sci. USA 1999. 96: 1036-1041.
57. Kalinski, P. and Moser, M., Consensual immunity: success-driven development of T-helper-1 and T-helper-2 responses. Nat. Rev. Immunol. 2005. 5: 251-260.
58. Granucci, F., Vizzardelli, C., Virzi, E., Rescigno, M. and Ricciardi-Castagnoli, P., Transcriptional reprogramming of dendritic cells by differentiation stimuli. Eur. J. Immunol. 2001. 31: 2539-2546.
59. Constant, S. L. and Bottomly, K., Induction of Th1 and Th2 CD4+T cell responses: the alternative approaches. Annu. Rev. Immunol. 1997. 15: 297-322.
60. Bluestone, J. A., New perspectives of CD28-B7-mediated T cell costimulation. Immunity 1995. 2: 555-559.
61. Boonstra, A., Asselin-Paturel, C., Gilliet, M., Crain, C., Trinchieri, G., Liu, Y. J. and O'Garra, A., Flexibility of mouse classical and plasmacytoid-derived dendritic cells in directing T helper type 1 and 2 cell development: dependency on antigen dose and differential toll-like receptor ligation. J. Exp. Med. 2003. 197: 101-109.
62. Ruedl, C., Bachmann, M. F. and Kopf, M., The antigen dose determines T helper subset development by regulation of CD40 ligand. Eur. J. Immunol. 2000. 30: 2056-2064.
63. Soares, H., Waechter, H., Glaichenhaus, N., Mougneau, E., Yagita, H., Mizenina, O., Dudziak, D. et al., A subset of dendritic cells induces CD4+ T cells to produce IFN-gamma by an IL-12-independent but CD70-dependent mechanism in vivo. J. Exp. Med. 2007. 204: 1095-1106.
64. MacDonald, A. S. and Maizels, R. M., Alarming dendritic cells for Th2 induction. J. Exp. Med. 2008. 205: 13-17.
65. Langenkamp, A., Messi, M., Lanzavecchia, A. and Sallusto, F., Kinetics of dendritic cell activation: impact on priming of TH1, TH2 and nonpolarized T cells. Nat. Immunol. 2000. 1: 311-316.
66. Turner, J. D., Langley, R. S., Johnston, K. L., Gentil, K., Ford, L., Wu, B., Graham, M. et al., Wolbachia lipoprotein stimulates innate and adaptive immunity through Toll-like receptors 2 and 6 to induce disease manifestations of filariasis. J. Biol. Chem. 2009. 284: 22364-22378.
67. Wenink, M. H., Santegoets, K. C., Broen, J. C., van Bon, L., Abdollahi-Roodsaz, S., Popa, C., Huijbens, R. et al., TLR2 promotes Th2/Th17 responses via TLR4 and TLR7/8 by abrogating the type I IFN amplification loop. J. Immunol. 2009. 183: 6960-6970.
68. Kane, C. M., Jung, E. and Pearce, E. J., Schistosoma mansoni egg antigen-mediated modulation of Toll-like receptor (TLR)-induced activation occurs independently of TLR2, TLR4, and MyD88. Infect. Immun. 2008. 76: 5754-5759.
69. Trujillo-Vargas, C. M., Ramirez-Pineda, J. R., Palmetshofer, A., Grunewald, S., Moll, H., Berberich, C. and Erb, K. J., Mice vaccinated with allergen-pulsed myeloid dendritic cells are not protected from developing allergen-induced Th2 responses. Int. Arch. Allergy Immunol. 2005. 137: 219-228.
70. de Heer, H. J., Hammad, H., Soullie, T., Hijdra, D., Vos, N., Willart, M. A., Hoogsteden, H. C. and Lambrecht, B. N., Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J. Exp. Med. 2004. 200: 89-98.
71. Kool, M., van Nimwegen, M., Willart, M. A., Muskens, F., Boon, L., Smit, J. J., Coyle, A. et al., An anti-inflammatory role for plasmacytoid dendritic cells in allergic airway inflammation. J. Immunol. 2009. 183: 1074-1082.
72. Menges, M., Rossner, S., Voigtlander, C., Schindler, H., Kukutsch, N. A., Bogdan, C., Erb, K. et al., Repetitive injections of dendritic cells matured with tumor necrosis factor alpha induce antigen-specific protection of mice from autoimmunity. J. Exp. Med. 2002. 195: 15-21.
73. Voigtländer, C., Rößner, S., Cierpka, E., Theiner, G., Wiethe, C., Menges, M., Schuler, G. and Lutz, M. B., Dendritic cells matured with TNF can be further activated in vitro and after subcutaneous injection in vivo which converts their tolerogenicity into immunogenicity. J. Immunother. 2006. 29: 407-415.
74. Noel, W., Raes, G., Hassanzadeh Ghassabeh, G., De Baetselier, P. and Beschin, A., Alternatively activated macrophages during parasite infections. Trends Parasitol. 2004. 20: 126-133.
75. Diaz, A. and Allen, J. E., Mapping immune response profiles: the emerging scenario from helminth immunology. Eur. J. Immunol. 2007. 37: 3319-3326.
76. Jenkins, S. J. and Allen, J. E., Similarity and diversity in macrophage activation by nematodes, trematodes, and cestodes. J. Biomed. Biotechnol. 2010. 2010: 262609.
77. Lanham, S. M., Separation of trypanosomes from the blood of infected rats and mice by anion-exchangers. Nature 1968. 218: 1273-1274.
78. Stijlemans, B., Conrath, K., Cortez-Retamozo, V., Van Xong, H., Wyns, L., Senter, P., Revets, H. et al., Efficient targeting of conserved cryptic epitopes of infectious agents by single domain antibodies. African trypanosomes as paradigm. J. Biol. Chem. 2004. 279: 1256-1261.
79. Cross, G. A., Identification, purification and properties of clone-specific glycoprotein antigens constituting the surface coat of Trypanosoma brucei. Parasitology 1975. 71: 393-417.
80. Lanham, S. M. and Godfrey, D. G., Isolation of salivarian trypanosomes from man and other mammals using DEAE-cellulose. Exp. Parasitol. 1970. 28: 521-534.
81. Stijlemans, B., Baral, T. N., Guilliams, M., Brys, L., Korf, J., Drennan, M., Van Den Abbeele, J. et al., A glycosylphosphatidylinositol-based treatment alleviates trypanosomiasis-associated immunopathology. J. Immunol. 2007. 179: 4003-4014.
82. Zamze, S. E., Ferguson, M. A., Collins, R., Dwek, R. A. and Rademacher, T. W., Characterization of the cross-reacting determinant (CRD) of the glycosyl-phosphatidylinositol membrane anchor of Trypanosoma brucei variant surface glycoprotein. Eur. J. Biochem. 1988. 176: 527-534.
83. Lutz, M. B., Kukutsch, N., Ogilvie, A. L., Rossner, S., Koch, F., Romani, N. and Schuler, G., An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 1999. 223: 77-92.
84. Zal, T., Volkmann, A. and Stockinger, B., Mechanisms of tolerance induction in major histocompatibility complex class II-restricted T cells specific for a blood-borne self-antigen. J. Exp. Med. 1994. 180: 2089-2099.
85. Schon, M., Wienrich, B. G., Kneitz, S., Sennefelder, H., Amschler, K., Vohringer, V., Weber, O. et al., KINK-1, a novel small-molecule inhibitor of IKKbeta, and the susceptibility of melanoma cells to antitumoral treatment. J. Natl. Cancer Inst. 2008. 100: 862-875.