Timing is everything: Dendritic cell subsets in murine Leishmania infection

Trends in Parasitology

Volumn 30, Issue 10, 2014, Pages 499-507

  Ashok, Devika ^a   Acha Orbea, Hans ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Dendritic cell (DC); Leishmania; Resistance; Susceptibility

Indexed keywords

LEISHMANIA VACCINE;

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; CELL MIGRATION; DENDRITIC CELL; EPIDERMIS CELL; HOST; IMMUNE RESPONSE; INFLAMMATION; INNATE IMMUNITY; LANGERHANS CELL; LEISHMANIA; LEISHMANIA MAJOR; LEISHMANIASIS; LYMPH NODE; LYMPHOID TISSUE; MONOCYTE; MONOCYTE DERIVED DENDRITIC CELL; MURINAE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; REVIEW; SKIN CELL; T LYMPHOCYTE; VACCINATION; ANIMAL; DENDRITIC CELL (DC); IMMUNOLOGY; MOUSE; RESISTANCE; SUSCEPTIBILITY; TH1 CELL;

DENDRITIC CELL (DC); LEISHMANIA; RESISTANCE; SUSCEPTIBILITY;

ANIMALS; ANTIGEN PRESENTATION; DENDRITIC CELLS; LEISHMANIA; LEISHMANIASIS; MICE; TH1 CELLS;

EID: 84907993457     PISSN: 14714922     EISSN: 14715007     Source Type: Journal    
DOI: 10.1016/j.pt.2014.08.001     Document Type: Review

References (99)

1. Sacks D., Noben-Trauth N. The immunology of susceptibility and resistance to Leishmania major in mice. Nat. Rev. Immunol. 2002, 2:845-858.
2. Reiner S.L., Locksley R.M. The regulation of immunity to Leishmania major. Annu. Rev. Immunol. 1995, 13:151-177.
3. McDowell M.A., et al. Leishmania priming of human dendritic cells for CD40 ligand-induced interleukin-12p70 secretion is strain and species dependent. Infect. Immun. 2002, 70:3994-4001.
4. Lipoldova M., et al. Susceptibility to Leishmania major infection in mice: multiple loci and heterogeneity of immunopathological phenotypes. Genes Immun. 2000, 1:200-206.
5. Mattner F., et al. The role of IL-12 and IL-4 in Leishmania major infection. Chem. Immunol. 1997, 68:86-109.
6. Nabors G.S., et al. The influence of the site of parasite inoculation on the development of Th1 and Th2 type immune responses in (BALB/c x C57BL/6) F1 mice infected with Leishmania major. Parasite Immunol. 1995, 17:569-579.
7. Beebe A.M., et al. Serial backcross mapping of multiple loci associated with resistance to Leishmania major in mice. Immunity 1997, 6:551-557.
8. Peters N.C., et al. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 2008, 321:970-974.
9. Kopf M., et al. IL-4-deficient Balb/c mice resist infection with Leishmania major. J. Exp. Med. 1996, 184:1127-1136.
10. Himmelrich H., et al. In BALB/c mice, IL-4 production during the initial phase of infection with Leishmania major is necessary and sufficient to instruct Th2 cell development resulting in progressive disease. J. Immunol. 2000, 164:4819-4825.
11. Biedermann T., et al. IL-4 instructs TH1 responses and resistance to Leishmania major in susceptible BALB/c mice. Nat. Immunol. 2001, 2:1054-1060.
12. Hurdayal R., et al. Deletion of IL-4 receptor alpha on dendritic cells renders BALB/c mice hypersusceptible to Leishmania major infection. PLoS Pathog. 2013, 9:e1003699.
13. Moll H., et al. Dendritic cells in Leishmania major-immune mice harbor persistent parasites and mediate an antigen-specific T cell immune response. Eur. J. Immunol. 1995, 25:693-699.
14. von Stebut E., et al. Uptake of Leishmania major amastigotes results in activation and interleukin 12 release from murine skin-derived dendritic cells: implications for the initiation of anti-Leishmania immunity. J. Exp. Med. 1998, 188:1547-1552.
15. Suffia I., et al. A role for CD103 in the retention of CD4+CD25+ Treg and control of Leishmania major infection. J. Immunol. 2005, 174:5444-5455.
16. Gonzalez-Lombana C., et al. IL-17 mediates immunopathology in the absence of IL-10 following Leishmania major infection. PLoS Pathog. 2013, 9:e1003243.
17. Liu K., Nussenzweig M.C. Origin and development of dendritic cells. Immunol. Rev. 2010, 234:45-54.
18. Kamath A.T., et al. The development, maturation, and turnover rate of mouse spleen dendritic cell populations. J. Immunol. 2000, 165:6762-6770.
19. Shortman K., Liu Y.J. Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2002, 2:151-161.
20. Naik S.H. Demystifying the development of dendritic cell subtypes, a little. Immunol. Cell Biol. 2008, 86:439-452.
21. Sathe P., et al. Lymphoid tissue and plasmacytoid dendritic cells and macrophages do not share a common macrophage-dendritic cell-restricted progenitor. Immunity 2014, 41:104-115.
22. Dominguez P.M., Ardavin C. Differentiation and function of mouse monocyte-derived dendritic cells in steady state and inflammation. Immunol. Rev. 2010, 234:90-104.
23. Ardavin C., et al. Origin and differentiation of dendritic cells. Trends Immunol. 2001, 22:691-700.
24. Liu Y.J. Dendritic cell subsets and lineages, and their functions in innate and adaptive immunity. Cell 2001, 106:259-262.
25. Maldonado-Lopez R., Moser M. Dendritic cell subsets and the regulation of Th1/Th2 responses. Semin. Immunol. 2001, 13:275-282.
26. Ardavin C. Origin, precursors and differentiation of mouse dendritic cells. Nat. Rev. Immunol. 2003, 3:582-590.
27. Hochrein H., O'Keeffe M. Dendritic cell subsets and toll-like receptors. Handb. Exp. Pharmacol. 2008, 153-179.
28. Vremec D., et al. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J. Immunol. 2000, 164:2978-2986.
29. Belz G.T., et al. The CD8alpha(+) dendritic cell is responsible for inducing peripheral self-tolerance to tissue-associated antigens. J. Exp. Med. 2002, 196:1099-1104.
30. Lin M.L., et al. Selective suicide of cross-presenting CD8+ dendritic cells by cytochrome c injection shows functional heterogeneity within this subset. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:3029-3034.
31. Edelson B.T., et al. Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. J. Exp. Med. 2010, 207:823-836.
32. Shrimpton R.E., et al. CD205 (DEC-205): a recognition receptor for apoptotic and necrotic self. Mol. Immunol. 2009, 46:1229-1239.
33. Merad M., et al. Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat. Rev. Immunol. 2008, 8:935-947.
34. Idoyaga J., et al. Cutting edge: langerin/CD207 receptor on dendritic cells mediates efficient antigen presentation on MHC I and II products in vivo. J. Immunol. 2008, 180:3647-3650.
35. Coquerelle C., Moser M. DC subsets in positive and negative regulation of immunity. Immunol. Rev. 2010, 234:317-334.
36. Tan J.K., O'Neill H.C. Maturation requirements for dendritic cells in T cell stimulation leading to tolerance versus immunity. J. Leukoc. Biol. 2005, 78:319-324.
37. Brandonisio O., et al. Dendritic cells in Leishmania infection. Microbes Infect. 2004, 6:1402-1409.
38. Mayer C.T., et al. Layers of dendritic cell-mediated T cell tolerance, their regulation and the prevention of autoimmunity. Front. Immunol. 2012, 3:183.
39. Macatonia S.E., et al. Dendritic cells produce IL-12 and direct the development of Th1 cells from naive CD4+ T cells. J. Immunol. 1995, 154:5071-5079.
40. Belkaid Y., et al. CD8+ T cells are required for primary immunity in C57BL/6 mice following low-dose, intradermal challenge with Leishmania major. J. Immunol. 2002, 168:3992-4000.
41. Tacchini-Cottier F., et al. Does T helper differentiation correlate with resistance or susceptibility to infection with L. major? Some insights from the murine model. Front. Immunol. 2012, 3:32.
42. Ritter U., et al. CD8 alpha- and Langerin-negative dendritic cells, but not Langerhans cells, act as principal antigen-presenting cells in leishmaniasis. Eur. J. Immunol. 2004, 34:1542-1550.
43. Moll H., et al. Langerhans cells transport Leishmania major from the infected skin to the draining lymph node for presentation to antigen-specific T cells. Eur. J. Immunol. 1993, 23:1595-1601.
44. Kautz-Neu K., et al. Langerhans cells are negative regulators of the anti-Leishmania response. J. Exp. Med. 2011, 208:885-891.
45. Iezzi G., et al. Lymph node resident rather than skin-derived dendritic cells initiate specific T cell responses after Leishmania major infection. J. Immunol. 2006, 177:1250-1256.
46. Ng L.G., et al. Migratory dermal dendritic cells act as rapid sensors of protozoan parasites. PLoS Pathog. 2008, 4:e1000222.
47. Leon B., et al. Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 2007, 26:519-531.
48. Von Stebut E. Immunology of cutaneous leishmaniasis: the role of mast cells, phagocytes and dendritic cells for protective immunity. Eur. J. Dermatol. 2007, 17:115-122.
49. Romani N., et al. Changing views of the role of Langerhans cells. J. Invest. Dermatol. 2012, 132:872-881.
50. von Stebut E., et al. Leishmania major-infected murine langerhans cell-like dendritic cells from susceptible mice release IL-12 after infection and vaccinate against experimental cutaneous leishmaniasis. Eur. J. Immunol. 2000, 30:3498-3506.
51. Moll H., et al. Increased interleukin 4 (IL-4) receptor expression and IL-4-induced decrease in IL-12 production by Langerhans cells infected with Leishmania major. Infect. Immun. 2002, 70:1627-1630.
52. Brewig N., et al. Priming of CD8+ and CD4+ T cells in experimental leishmaniasis is initiated by different dendritic cell subtypes. J. Immunol. 2009, 182:774-783.
53. Misslitz A.C., et al. Two waves of antigen-containing dendritic cells in vivo in experimental Leishmania major infection. Eur. J. Immunol. 2004, 34:715-725.
54. Carter C.R., et al. Complement receptor 3 deficiency influences lesion progression during Leishmania major infection in BALB/c mice. Infect. Immun. 2009, 77:5668-5675.
55. Wu W., et al. Immunomodulatory effects associated with a live vaccine against Leishmania major containing CpG oligodeoxynucleotides. Eur. J. Immunol. 2006, 36:3238-3247.
56. Laabs E.M., et al. Vaccination with live Leishmania major and CpG DNA promotes interleukin-2 production by dermal dendritic cells and NK cell activation. Clin. Vaccine Immunol. 2009, 16:1601-1606.
57. Ribeiro-Gomes F.L., et al. Efficient capture of infected neutrophils by dendritic cells in the skin inhibits the early anti-leishmania response. PLoS Pathog. 2012, 8:e1002536.
58. Bursch L.S., et al. Identification of a novel population of Langerin+ dendritic cells. J. Exp. Med. 2007, 204:3147-3156.
59. Morimoto N., et al. Requirement of SIRPalpha for protective immunity against Leishmania major. Biochem. Biophys. Res. Commun. 2010, 401:385-389.
60. Shortman K., Heath W.R. The CD8+ dendritic cell subset. Immunol. Rev. 2010, 234:18-31.
61. Hochrein H., et al. Differential production of IL-12, IFN-alpha, and IFN-gamma by mouse dendritic cell subsets. J. Immunol. 2001, 166:5448-5455.
62. Farrand K.J., et al. Langerin+ CD8alpha+ dendritic cells are critical for cross-priming and IL-12 production in response to systemic antigens. J. Immunol. 2009, 183:7732-7742.
63. den Haan J.M., et al. CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J. Exp. Med. 2000, 192:1685-1696.
64. Sancho D., et al. Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature 2009, 458:899-903.
65. Henri S., et al. Hierarchy of susceptibility of dendritic cell subsets to infection by Leishmania major: inverse relationship to interleukin-12 production. Infect. Immun. 2002, 70:3874-3880.
66. Sato N., et al. CC chemokine receptor (CCR)2 is required for Langerhans cell migration and localization of T helper cell type 1 (Th1)-inducing dendritic cells. Absence of CCR2 shifts the Leishmania major-resistant phenotype to a susceptible state dominated by Th2 cytokines, B cell outgrowth, and sustained neutrophilic inflammation. J. Exp. Med. 2000, 192:205-218.
67. Zhan Y., et al. Resident and monocyte-derived dendritic cells become dominant IL-12 producers under different conditions and signaling pathways. J. Immunol. 2010, 185:2125-2133.
68. De Trez C., et al. 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. 2009, 5:e1000494.
69. Ashok D., et al. Cross-presenting dendritic cells are required for control of Leishmania major infection. Eur. J. Immunol. 2014, 44:1422-1432.
70. Hildner K., et al. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 2008, 322:1097-1100.
71. Seillet C., et al. CD8alpha+ DCs can be induced in the absence of transcription factors Id2, Nfil3, and Batf3. Blood 2013, 121:1574-1583.
72. Tussiwand R., et al. Compensatory dendritic cell development mediated by BATF-IRF interactions. Nature 2012, 490:502-507.
73. Qu C., et al. MHC class I/peptide transfer between dendritic cells overcomes poor cross-presentation by monocyte-derived APCs that engulf dying cells. J. Immunol. 2009, 182:3650-3659.
74. Remer K.A., et al. Vaccination with plasmacytoid dendritic cells induces protection against infection with Leishmania major in mice. Eur. J. Immunol. 2007, 37:2463-2473.
75. Baldwin T., et al. Dendritic cell populations in Leishmania major-infected skin and draining lymph nodes. Infect. Immun. 2004, 72:1991-2001.
76. Guillerey C., et al. Pivotal role of plasmacytoid dendritic cells in inflammation and NK-cell responses after TLR9 triggering in mice. Blood 2012, 120:90-99.
77. de Oliveira C.I., et al. Challenges and perspectives in vaccination against leishmaniasis. Parasitol. Int. 2009, 58:319-324.
78. Kaye P.M., Aebischer T. Visceral leishmaniasis: immunology and prospects for a vaccine. Clin. Microbiol. Infect. 2011, 17:1462-1470.
79. Kronenberg K., et al. Vaccination with TAT-antigen fusion protein induces protective, CD8(+) T cell-mediated immunity against Leishmania major. J. Invest. Dermatol. 2010, 130:2602-2610.
80. Mutiso J.M., et al. Development of Leishmania vaccines: predicting the future from past and present experience. J. Biomed. Res. 2013, 27:85-102.
81. Okwor I., et al. Protective immunity and vaccination against cutaneous leishmaniasis. Front. Immunol. 2012, 3:128.
82. Ramirez L., et al. Evaluation of immune responses and analysis of the effect of vaccination of the Leishmania major recombinant ribosomal proteins L3 or L5 in two different murine models of cutaneous leishmaniasis. Vaccine 2013, 31:1312-1319.
83. Matos I., et al. Targeting antigens to dendritic cells in vivo induces protective immunity. PLoS ONE 2013, 8:e67453.
84. Masic A., et al. Dendritic cell-mediated vaccination relies on interleukin-4 receptor signaling to avoid tissue damage after Leishmania major infection of BALB/c mice. PLoS Negl. Trop. Dis. 2012, 6:e1721.
85. Uzonna J.E., et al. Low dose Leishmania major promotes a transient T helper cell type 2 response that is down-regulated by interferon gamma-producing CD8+ T cells. J. Exp. Med. 2004, 199:1559-1566.
86. de Veer M.J., et al. MyD88 is essential for clearance of Leishmania major: possible role for lipophosphoglycan and Toll-like receptor 2 signaling. Eur. J. Immunol. 2003, 33:2822-2831.
87. Kostka S.L., et al. Distinct roles for IL-1 receptor type I signaling in early versus established Leishmania major infections. J. Invest. Dermatol. 2006, 126:1582-1589.
88. Park A.Y., et al. IL-12 is required to maintain a Th1 response during Leishmania major infection. J. Immunol. 2000, 165:896-902.
89. Wang Z.E., et al. CD4+ effector cells default to the Th2 pathway in interferon gamma-deficient mice infected with Leishmania major. J. Exp. Med. 1994, 179:1367-1371.
90. Lopez Kostka S., et al. IL-17 promotes progression of cutaneous leishmaniasis in susceptible mice. J. Immunol. 2009, 182:3039-3046.
91. Mohrs M., et al. Differences between IL-4- and IL-4 receptor alpha-deficient mice in chronic leishmaniasis reveal a protective role for IL-13 receptor signaling. J. Immunol. 1999, 162:7302-7308.
92. Radwanska M., et al. Deletion of IL-4Ralpha on CD4 T cells renders BALB/c mice resistant to Leishmania major infection. PLoS Pathog. 2007, 3:e68.
93. Matthews D.J., et al. IL-13 is a susceptibility factor for Leishmania major infection. J. Immunol. 2000, 164:1458-1462.
94. Belkaid Y., 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, 194:1497-1506.
95. Moskowitz N.H., et al. Efficient immunity against Leishmania major in the absence of interleukin-6. Infect. Immun. 1997, 65:2448-2450.
96. Launois P., et al. IL-4 rapidly produced by V beta 4V alpha 8 CD4+ T cells instructs Th2 development and susceptibility to Leishmania major in BALB/c mice. Immunity 1997, 6:541-549.
97. Wilhelm P., et al. Rapidly fatal leishmaniasis in resistant C57BL/6 mice lacking TNF. J. Immunol. 2001, 166:4012-4019.
98. Kapsenberg M.L. Dendritic-cell control of pathogen-driven T-cell polarization. Nat. Rev. Immunol. 2003, 3:984-993.
99. Lopez-Bravo M., Ardavin C. In vivo induction of immune responses to pathogens by conventional dendritic cells. Immunity 2008, 29:343-351.