Tip-DC development during parasitic infection is regulated by IL-10 and requires CCL2/CCR2, IFN-γ and MyD88 signaling

PLoS Pathogens

Volumn 6, Issue 8, 2010, Pages 35-36

  Bosschaerts, Tom ^a,b   Guilliams, Martin ^a,b   Stijlemans, Benoît ^a,b   Morias, Yannick ^a,b   Engel, Daniel ^c   Tacke, Frank ^d   Hérin, Michel ^e   de Baetselier, Patrick ^a,b   Beschin, Alain ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^c UNIVERSITY HOSPITAL BONN   (Germany)

^d UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^e UNIVERSITY OF NAMUR   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD11B ANTIGEN; CD86 ANTIGEN; CHEMOKINE RECEPTOR CCR2; GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERLEUKIN 10; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYELOID DIFFERENTIATION FACTOR 88; MONOCYTE CHEMOTACTIC PROTEIN 1;

AFRICAN TRYPANOSOMIASIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MATURATION; DENDRITIC CELL; GENE EXPRESSION; GENETIC ANALYSIS; LIVER CELL; MONOCYTE; MOUSE; NONHUMAN; PARASITE VIRULENCE; PHENOTYPE; TRYPANOSOMA BRUCEI; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CELL SEPARATION; CYTOLOGY; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRYPANOSOMIASIS;

MUS; TRYPANOSOMA BRUCEI;

ANIMALS; CELL DIFFERENTIATION; CELL SEPARATION; CHEMOKINE CCL2; DENDRITIC CELLS; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; INTERFERON-GAMMA; INTERLEUKIN-10; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOCYTES; MYELOID DIFFERENTIATION FACTOR 88; RECEPTORS, CCR2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS;

EID: 77958124602     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001045     Document Type: Article

References (43)

1. Sternberg JM (2004) Human African trypanosomiasis: clinical presentation and immune response. Parasite Immunol 26: 469-476.
2. Naessens J (2006) Bovine trypanotolerance: A natural ability to prevent severe anaemia and haemophagocytic syndrome? Int J Parasitol 36: 521-528.
3. Bosschaerts T, Guilliams M, Stijlemans B, De Baetselier P, Beschin A (2009) Understanding the role of monocytic cells in liver inflammation using parasite infection as a model. Immunobiology 214: 737-747.
4. Magez S, Radwanska M, Beschin A, Sekikawa K, De Baetselier P (1999) Tumor necrosis factor alpha is a key mediator in the regulation of experimental Trypanosoma brucei infections. Infect Immun 67: 3128-3132.
5. Drennan MB, Stijlemans B, Van den Abbeele J, Quesniaux VJ, Barkhuizen M, et al. (2005) The induction of a type 1 immune response following a Trypanosoma brucei infection is MyD88 dependent. J Immunol 175: 2501-2509.
6. Magez S, Radwanska M, Drennan M, Fick L, Baral TN, et al. (2006) Interferongamma and nitric oxide in combination with antibodies are key protective host immune factors during trypanosoma congolense Tc13 Infections. J Infect Dis 193: 1575-1583.
7. Shi M, Pan W, Tabel H (2003) Experimental African trypanosomiasis: IFNgamma mediates early mortality. Eur J Immunol 33: 108-118.
8. Guilliams M, Movahedi K, Bosschaerts T, VandenDriessche T, Chuah MK, et al. (2009) IL-10 dampens TNF/inducible nitric oxide synthase-producing dendritic cell-mediated pathogenicity during parasitic infection. J Immunol 182: 1107-1118.
9. Guilliams M, Oldenhove G, Noel W, Herin M, Brys L, et al. (2007) African trypanosomiasis: naturally occurring regulatory T cells favor trypanotolerance by limiting pathology associated with sustained type 1 inflammation. J Immunol 179: 2748-2757.
10. Guilliams M, Bosschaerts T, Herin M, Hunig T, Loi P, et al. (2008) Experimental expansion of the regulatory T cell population increases resistance to African trypanosomiasis. J Infect Dis 198: 781-791.
11. Bosschaerts T, Guilliams M, Noel W, Herin M, Burk RF, et al. (2008) Alternatively activated myeloid cells limit pathogenicity associated with African trypanosomiasis through the IL-10 inducible gene selenoprotein P. J Immunol 180: 6168-6175.
12. Serbina NV, Jia T, Hohl TM, Pamer EG (2008) Monocyte-mediated defense against microbial pathogens. Annu Rev Immunol 26: 421-452.
13. Hertz CJ, Filutowicz H, Mansfield JM (1998) Resistance to the African trypanosomes is IFN-gamma dependent. J Immunol 161: 6775-6783.
14. Blum J, Schmid C, Burri C (2006) Clinical aspects of 2541 patients with second stage human African trypanosomiasis. Acta Trop 97: 55-64.
15. Hertz CJ, Mansfield JM (1999) IFN-gamma-dependent nitric oxide production is not linked to resistance in experimental African trypanosomiasis. Cell Immunol 192: 24-32.
16. Geissmann F, Jung S, Littman DR (2003) Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19: 71-82.
17. Serbina NV, Salazar-Mather TP, Biron CA, Kuziel WA, Pamer EG (2003) TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19: 59-70.
18. Copin R, De Baetselier P, Carlier Y, Letesson JJ, Muraille E (2007) MyD88- dependent activation of B220-CD11b+LY-6C+ dendritic cells during Brucella melitensis infection. J Immunol 178: 5182-5191.
19. De Trez C, Magez S, Akira S, Ryffel B, Carlier Y, et al. (2009) iNOS-producing inflammatory dendritic cells constitute the major infected cell type during the chronic Leishmania major infection phase of C57BL/6 resistant mice. PLoS Pathog 5: e1000494.
20. Aldridge JR, Jr., Moseley CE, Boltz DA, Negovetich NJ, Reynolds C, et al. (2009) TNF/iNOS-producing dendritic cells are the necessary evil of lethal influenza virus infection. Proc Natl Acad Sci U S A 106: 5306-5311.
21. Tokuyama H, Ueha S, Kurachi M, Matsushima K, Moriyasu F, et al. (2005) The simultaneous blockade of chemokine receptors CCR2, CCR5 and CXCR3 by a non-peptide chemokine receptor antagonist protects mice from dextran sodium sulfate-mediated colitis. Int Immunol 17: 1023-1034.
22. Serbina NV, Pamer EG (2006) Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol 7: 311-317.
23. Tacke F, Alvarez D, Kaplan TJ, Jakubzick C, Spanbroek R, et al. (2007) Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest 117: 185-194.
24. Schober A, Bernhagen J, Weber C (2008) Chemokine-like functions of MIF in atherosclerosis. J Mol Med 86: 761-770.
25. Paiva CN, Figueiredo RT, Kroll-Palhares K, Silva AA, Silverio JC, et al. (2009) CCL2/MCP-1 controls parasite burden, cell infiltration, and mononuclear activation during acute Trypanosoma cruzi infection. J Leukoc Biol.
26. Engel D, Dobrindt U, Tittel A, Peters P, Maurer J, et al. (2006) Tumor necrosis factor alpha- and inducible nitric oxide synthase-producing dendritic cells are rapidly recruited to the bladder in urinary tract infection but are dispensable for bacterial clearance. Infect Immun 74: 6100-6107.
27. Fogg DK, Sibon C, Miled C, Jung S, Aucouturier P, et al. (2006) A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 311: 83-87.
28. Varol C, Landsman L, Fogg DK, Greenshtein L, Gildor B, et al. (2007) Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J Exp Med 204: 171-180.
29. Serbina NV, Kuziel W, Flavell R, Akira S, Rollins B, et al. (2003) Sequential MyD88-independent and -dependent activation of innate immune responses to intracellular bacterial infection. Immunity 19: 891-901.
30. Leppert BJ, Mansfield JM, Paulnock DM (2007) The soluble variant surface glycoprotein of African trypanosomes is recognized by a macrophage scavenger receptor and induces I kappa B alpha degradation independently of TRAF6- mediated TLR signaling. J Immunol 179: 548-556.
31. Ngure RM, Eckersall P, Burke J, Karori SM, Mwangi WW, et al. (2009) Endotoxin-like effects in acute phase response to Trypanosoma brucei brucei infection are not due to gastrointestinal leakage. Parasitol Int 58: 325-329.
32. Pentreath VW (1994) Endotoxins and their significance for murine trypanosomiasis. Parasitol Today 10: 226-229.
33. Dagenais TR, Freeman BE, Demick KP, Paulnock DM, Mansfield JM (2009) Processing and presentation of variant surface glycoprotein molecules to T cells in African trypanosomiasis. J Immunol 183: 3344-3355.
34. Geissmann F, Auffray C, Palframan R, Wirrig C, Ciocca A, et al. (2008) Blood monocytes: distinct subsets, how they relate to dendritic cells, and their possible roles in the regulation of T-cell responses. Immunol Cell Biol 86: 398-408.
35. Shi M, Wei G, Pan W, Tabel H (2006) Experimental African trypanosomiasis: a subset of pathogenic, IFN-gamma-producing, MHC class II-restricted CD4+ T cells mediates early mortality in highly susceptible mice. J Immunol 176: 1724-1732.
36. Dempsey WL, Mansfield JM (1983) Lymphocyte function in experimental African trypanosomiasis. V. Role of antibody and the mononuclear phagocyte system in variant-specific immunity. J Immunol 130: 405-411.
37. Namangala B, Noel W, De Baetselier P, Brys L, Beschin A (2001) Relative contribution of interferon-gamma and interleukin-10 to resistance to murine African trypanosomosis. J Infect Dis 183: 1794-1800.
38. Bourdi M, Masubuchi Y, Reilly TP, Amouzadeh HR, Martin JL, et al. (2002) Protection against acetaminophen-induced liver injury and lethality by interleukin 10: role of inducible nitric oxide synthase. Hepatology 35: 289-298.
39. Devey L, Ferenbach D, Mohr E, Sangster K, Bellamy CO, et al. (2009) Tissueresident macrophages protect the liver from ischemia reperfusion injury via a heme oxygenase-1-dependent mechanism. Mol Ther 17: 65-72.
40. Louis H, Le Moine O, Goldman M, Deviere J (2003) Modulation of liver injury by interleukin-10. Acta Gastroenterol Belg 66: 7-14.
41. Holt MP, Cheng L, Ju C (2008) Identification and characterization of infiltrating macrophages in acetaminophen-induced liver injury. J Leukoc Biol 84: 1410-1421.
42. Karlmark KR, Weiskirchen R, Zimmermann HW, Gassler N, Ginhoux F, et al. (2009) Hepatic recruitment of the inflammatory Gr1+ monocyte subset upon liver injury promotes hepatic fibrosis. Hepatology 50: 261-274.
43. Ghassabeh GH, De Baetselier P, Brys L, Noel W, Van Ginderachter JA, et al. (2006) Identification of a common gene signature for type II cytokine-associated myeloid cells elicited in vivo in different pathologic conditions. Blood 108: 575-583.