DC-derived IL-10 modulates pro-inflammatory cytokine production and promotes induction of CD4+IL-10+ regulatory T cells during Plasmodium yoelii infection

Frontiers in Immunology

Volumn 8, Issue FEB, 2017, Pages

  Loevenich, Katharina ^a   Ueffing, Kristina ^a   Abel, Simone ^a   Hose, Matthias ^a   Matuschewski, Kai ^b,c   Westendorf, Astrid M ^a   Buer, Jan ^a   Hansen, Wiebke ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

Interleukin 10; Malaria; Parasitic protozoan; Regulatory T cells; Rodent

Indexed keywords

B7 ANTIGEN; CD11B ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; GLYCOPROTEIN P 15095; IMMUNOSUPPRESSIVE AGENT; INTERLEUKIN 10; INTERLEUKIN 12; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ARTICLE; CD4+ IL-10+ REGULATORY T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL ISOLATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNOMODULATION; MAGNETIC ACTIVATED CELL SORTING; MONONUCLEAR CELL; MOUSE; NONHUMAN; PLASMODIUM YOELII INFECTION; PROCEDURES CONCERNING CELLS; PROTOZOON; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

EID: 85014325084     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.00152     Document Type: Article

References (42)

1. Langhorne J, Ndungu FM, Sponaas AM, Marsh K. Immunity to malaria: more questions than answers. Nat Immunol (2008) 9:725-32. doi:10.1038/ni.f.205
2. Riley EM, Stewart VA. Immune mechanisms in malaria: new insights in vaccine development. Nat Med (2013) 19:168-78. doi:10.1038/nm.3083
3. Abel S, Lückheide N, Westendorf AM, Geffers R, Roers A, Müller W, et al. Strong impact of CD4+ Foxp3+ regulatory T cells and limited effect of T cell-derived IL-10 on pathogen clearance during Plasmodium yoelii infection. J Immunol (2012) 188:5467-77. doi:10.4049/jimmunol.1102223
4. Abel S, Ueffing K, Tatura R, Hutzler M, Hose M, Matuschewski K, et al. Plasmodium yoelii infection of BALB/c mice results in expansion rather than induction of CD4(+) Foxp3(+) regulatory T cells. Immunology (2016) 148:197-205. doi:10.1111/imm.12602
5. Lahl K, Loddenkemper C, Drouin C, Freyer J, Arnason J, Eberl G, et al. Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease. J Exp Med (2007) 204:57-63. doi:10.1084/jem.20061852
6. Couper KN, Blount DG, Riley EM. IL-10: the master regulator of immunity to infection. J Immunol (2008) 180:5771-7. doi:10.4049/jimmunol.180.9.5771
7. Kossodo S, Monso C, Juillard P, Velu T, Goldman M, Grau GE. Interleukin-10 modulates susceptibility in experimental cerebral malaria. Immunology (1997) 91:536-40. doi:10.1046/j.1365-2567.1997.00290.x
8. Li C, Sanni LA, Omer F, Riley E, Langhorne J. Pathology of Plasmodium chabaudi chabaudi infection and mortality in interleukin-10-deficient mice are ameliorated by anti-tumor necrosis factor alpha and exacerbated by anti-transforming growth factor beta antibodies. Infect Immun (2003) 71:4850-6. doi:10.1128/IAI.71.9.4850-4856.2003
9. Couper KN, Blount DG, Wilson MS, Hafalla JC, Belkaid Y, Kamanaka M, et al. IL-10 from CD4CD25Foxp3CD127 adaptive regulatory T cells modulates parasite clearance and pathology during malaria infection. PLoS Pathog (2008) 4:e1000004. doi:10.1371/journal.ppat.1000004
10. Omer FM, de Souza JB, Riley EM. Differential induction of TGF-beta regulates proinflammatory cytokine production and determines the outcome of lethal and nonlethal Plasmodium yoelii infections. J Immunol (2003) 171:5430-6. doi:10.4049/jimmunol.171.10.5430
11. Madan R, Demircik F, Surianarayanan S, Allen JL, Divanovic S, Trompette A, et al. Nonredundant roles for B cell-derived IL-10 in immune counter-regulation. J Immunol (2009) 183:2312-20. doi:10.4049/jimmunol.0900185
12. Moore KW, de Waal MR, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol (2001) 19:683-765. doi:10.1146/annurev.immunol.19.1.683
13. Belkaid Y, Piccirillo CA, Mendez S, Shevach EM, Sacks DL. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature (2002) 420:502-7. doi:10.1038/nature01152
14. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, et al. Immunobiology of dendritic cells. Annu Rev Immunol (2000) 18:767-811. doi:10.1146/annurev.immunol.18.1.767
15. Merad M, Sathe P, Helft J, Miller J, Mortha A. The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu Rev Immunol (2013) 31:563-604. doi:10.1146/annurev-immunol-020711-074950
16. Wykes MN, Good MF. What really happens to dendritic cells during malaria? Nat Rev Microbiol (2008) 6:864-70. doi:10.1038/nrmicro1988
17. Bamboat ZM, Ocuin LM, Balachandran VP, Obaid H, Plitas G, DeMatteo RP. Conventional DCs reduce liver ischemia/reperfusion injury in mice via IL-10 secretion. J Clin Invest (2010) 120:559-69. doi:10.1172/JCI40008
18. Akbari O, DeKruyffRH, Umetsu DT. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat Immunol (2001) 2:725-31. doi:10.1038/90667
19. Igyarto BZ, Jenison MC, Dudda JC, Roers A, Müller W, Koni PA, et al. Langerhans cells suppress contact hypersensitivity responses via cognate CD4 interaction and langerhans cell-derived IL-10. J Immunol (2009) 183:5085-93. doi:10.4049/jimmunol.0901884
20. Jang S, Uematsu S, Akira S, Salgame P. IL-6 and IL-10 induction from dendritic cells in response to Mycobacterium tuberculosis is predominantly dependent on TLR2-mediated recognition. J Immunol (2004) 173:3392-7. doi:10.4049/jimmunol.173.5.3392
21. Freitas do Rosário AP, Lamb T, Spence P, Stephens R, Lang A, Roers A, et al. IL-27 promotes IL-10 production by effector Th1 CD4+ T cells: a critical mechanism for protection from severe immunopathology during malaria infection. J Immunol (2012) 188:1178-90. doi:10.4049/jimmunol.1102755
22. Liu Y, Chen Y, Li Z, Han Y, Sun Y, Wang Q, et al. Role of IL-10-producing regulatory B cells in control of cerebral malaria in Plasmodium berghei infected mice. Eur J Immunol (2013) 43:2907-18. doi:10.1002/eji.201343512
23. Girard-Madoux MJ, Kautz-Neu K, Lorenz B, Ober-Blobaum JL, von SE, Clausen BE. IL-10 signaling in dendritic cells attenuates anti-Leishmania major immunity without affecting protective memory responses. J Invest Dermatol (2015) 135:2890-4. doi:10.1038/jid.2015.236
24. Belkaid Y, Hoffmann KF, Mendez S, Kamhawi S, Udey MC, Wynn TA, et al. The role of interleukin (IL)-10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti-IL-10 receptor antibody for sterile cure. J Exp Med (2001) 194:1497-506. doi:10.1084/jem.194.10.1497
25. Girard-Madoux MJ, Kel JM, Reizis B, Clausen BE. IL-10 controls dendritic cell-induced T-cell reactivation in the skin to limit contact hypersensitivity. J Allergy Clin Immunol (2012) 129:143-50. doi:10.1016/j.jaci.2011.08.032
26. Kapsenberg ML. Dendritic-cell control of pathogen-driven T-cell polarization. Nat Rev Immunol (2003) 3:984-93. doi:10.1038/nri1246
27. Levings MK, Gregori S, Tresoldi E, Cazzaniga S, Bonini C, Roncarolo MG. Differentiation of Tr1 cells by immature dendritic cells requires IL-10 but not CD25+CD4+ Tr cells. Blood (2005) 105:1162-9. doi:10.1182/blood-2004-03-1211
28. McGuirk P, McCann C, Mills KH. Pathogen-specific T regulatory 1 cells induced in the respiratory tract by a bacterial molecule that stimulates interleukin 10 production by dendritic cells: a novel strategy for evasion of protective T helper type 1 responses by Bordetella pertussis. J Exp Med (2002) 195:221-31. doi:10.1084/jem.20011288
29. Kamanaka M, Kim ST, Wan YY, Sutterwala FS, Lara-Tejero M, Galán JE, et al. Expression of interleukin-10 in intestinal lymphocytes detected by an interleukin-10 reporter knockin tiger mouse. Immunity (2006) 25:941-52. doi:10.1016/j.immuni.2006.09.013
30. Roers A, Siewe L, Strittmatter E, Deckert M, Schlüter D, Stenzel W, et al. T cell-specific inactivation of the interleukin 10 gene in mice results in enhanced T cell responses but normal innate responses to lipopolysaccharide or skin irritation. J Exp Med (2004) 200:1289-97. doi:10.1084/jem.20041789
31. Caton ML, Smith-Raska MR, Reizis B. Notch-RBP-J signaling controls the homeostasis of CD8-dendritic cells in the spleen. J Exp Med (2007) 204:1653-64. doi:10.1084/jem.20062648
32. Franken L, Klein M, Spasova M, Elsukova A, Wiedwald U, Welz M, et al. Splenic red pulp macrophages are intrinsically superparamagnetic and contaminate magnetic cell isolates. Sci Rep (2015) 5:12940. doi:10.1038/srep12940
33. Li C, Corraliza I, Langhorne J. A defect in interleukin-10 leads to enhanced malarial disease in Plasmodium chabaudi chabaudi infection in mice. Infect Immun (1999) 67:4435-42.
34. Trinchieri G. Interleukin-10 production by effector T cells: Th1 cells show self control. J Exp Med (2007) 204:239-43. doi:10.1084/jem.20070104
35. Groux H, O'Garra A, Bigler M, Rouleau M, Antonenko S, de Vries JE, et al. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature (1997) 389:737-42. doi:10.1038/39614
36. Urban BC, Willcox N, Roberts DJ. A role for CD36 in the regulation of dendritic cell function. Proc Natl Acad Sci U S A (2001) 98:8750-5. doi:10.1073/pnas.151028698
37. Ocana-Morgner C, Mota MM, Rodriguez A. Malaria blood stage suppression of liver stage immunity by dendritic cells. J Exp Med (2003) 197:143-51. doi:10.1084/jem.20021072
38. Cambos M, Bazinet S, Abed E, Sanchez-Dardon J, Bernard C, Moreau R, et al. The IL-12p70/IL-10 interplay is differentially regulated by free heme and hemozoin in murine bone-marrow-derived macrophages. Int J Parasitol (2010) 40:1003-12. doi:10.1016/j.ijpara.2010.02.007
39. Deshpande P, Shastry P. Modulation of cytokine profiles by malaria pigment-hemozoin: role of IL-10 in suppression of proliferative responses of mitogen stimulated human PBMC. Cytokine (2004) 28:205-13. doi:10.1016/j.cyto.2004.08.002
40. Keller CC, Yamo O, Ouma C, Ong'echa JM, Ounah D, Hittner JB, et al. Acquisition of hemozoin by monocytes down-regulates interleukin-12 p40 (IL-12p40) transcripts and circulating IL-12p70 through an IL-10-dependent mechanism: in vivo and in vitro findings in severe malarial anemia. Infect Immun (2006) 74:5249-60. doi:10.1128/IAI.00843-06
41. Coban C, Ishii KJ, Kawai T, Hemmi H, Sato S, Uematsu S, et al. Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J Exp Med (2005) 201:19-25. doi:10.1084/jem.20041836
42. Coban C, Ishii KJ, Horii T, Akira S. Manipulation of host innate immune responses by the malaria parasite. Trends Microbiol (2007) 15:271-8. doi:10.1016/j.tim.2007.04.003