Friend retrovirus infection of myeloid dendritic cells impairs maturation, prolongs contact to naïve T cells, and favors expansion of regulatory T cells

Blood

Volumn 110, Issue 12, 2007, Pages 3949-3958

  Balkow, Sandra ^a   Krux, Frank ^b   Loser, Karin ^a   Becker, Jan U ^b   Grabbe, Stephan ^c   Dittmer, Ulf ^b,d  

^a INST OF REPRO MED OF THE UNIV   (Germany)

^b UNIVERSITY OF DUISBURG ESSEN   (Germany)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

^d UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD69 ANTIGEN; HERMES ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; ARTICLE; BONE MARROW CELL; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL CULTURE; CELL INTERACTION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; DISEASE TRANSMISSION; ELECTRON MICROSCOPY; FRIEND LEUKEMIA VIRUS; IMAGE ANALYSIS; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RETROVIRUS INFECTION; T LYMPHOCYTE ACTIVATION;

EID: 37049024134     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2007-05-092189     Document Type: Article

References (55)

1. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392:245-252.
2. Pollara G, Kwan A, Newton PJ, Handley ME, Chain BM, Katz DR. Dendritic cells in viral pathogenesis: protective or defective? Int J Exp Pathol. 2005;86:187-204.
3. Shishkova Y, Harms H, Krohne G, Avota E, Schneider-Schaulies S. Immune synapses formed with measles virus-infected dendritic cells are unstable and fail to sustain T cell activation. Cell Microbiol. 2007;9:1974-1986.
4. Steinman RM, Granelli-Piperno A, Pope M, et al. The interaction of immunodeficiency viruses with dendritic cells. Curr Top Microbiol Immunol. 2003;276:1-30.
5. Lechmann M, Berchtold S, Hauber J, Steinkasserer A. CD83 on dendritic cells: more than just a marker for maturation. Trends Immunol. 2002;23:273-275.
6. Gunzer M, Schafer A, Borgmann S, et al. Antigen presentation in extracellular matrix: interactions of T cells with dendritic cells are dynamic, short lived, and sequential. Immunity. 2000;13:323-332.
7. Kabat D. Molecular biology of Friend viral erythroleukemia. Curr Top Microbiol Immunol. 1989;148:1-42.
8. Hoatlin ME, Kabat D. Host-range control of a retroviral disease: Friend erythroleukemia. Trends Microbiol. 1995;3:51-57.
9. Hasenkrug KJ, Chesebro B. Immunity to retroviral infection: the Friend virus model. Proc Natl Acad Sci U S A. 1997;94:7811-7816.
10. + T cells and gamma interferon in protection of mice against retrovirus-induced immunosuppression. J Virol. 2002;76:450-454.
11. lo thymocytes in vivo. Science. 1990;250:1720-1723.
12. Inaba K, Inaba M, Romani N, et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med. 1992;176:1693-1702.
13. Dittmer U, Peterson KE, Messer R, Stromnes IM, Race B, Hasenkrug KJ. Role of interleukin-4 (IL-4), IL-12, and gamma interferon in primary and vaccine-primed immune responses to Friend retrovirus infection. J Virol. 2001;75:654-660.
14. Vremec D, Zorbas M, Scollay R, et al. The surface phenotype of dendritic cells purified from mouse thymus and spleen: investigation of the CD8 expression by a subpopulation of dendritic cells. J Exp Med. 1992;176:47-58.
15. + T cells from murine spleen via nylon wool adherence and an optimized antibody cocktail. J Immunol Methods. 2001;258:55-63.
16. Stromnes IM, Dittmer U, Schumacher TN, et al. Temporal effects of gamma interferon deficiency on the course of Friend retrovirus infection in mice. J Virol. 2002;76:2225-2232.
17. Shortman K, Liu YJ. Mouse and human dendritic cell subtypes. Nat Rev Immunol. 2002;2:151-161.
18. Gerlach N, Schimmer S, Weiss S, Kalinke U, Dittmer U. Effects of type I interferons on Friend retrovirus infection. J Virol. 2006;80:3438-3444.
19. Abujamra AL, Spanjaard RA, Akinsheye I, Zhao X, Faller DV, Ghosh SK. Leukemia virus long terminal repeat activates NFkappaB pathway by a TLR3-dependent mechanism. Virology. 2006;345:390-403.
20. Moser M, Murphy KM. Dendritic cell regulation of TH1-TH2 development. Nat Immunol. 2000;1:199-205.
21. Sims TN, Dustin ML. The immunological synapse: integrins take the stage. Immunol Rev. 2002;186:100-117.
22. Bromley SK, Burack WR, Johnson KG, et al. The immunological synapse. Annu Rev Immunol. 2001;19:375-396.
23. Benvenuti F, Lagaudriere-Gesbert C, Grandjean I, et al. Dendritic cell maturation controls adhesion, synapse formation, and the duration of the interactions with naive T lymphocytes. J Immunol. 2004;172:292-301.
24. Hugues S, Fetler L, Bonifaz L, Helft J, Amblard F, Amigorena S. Distinct T cell dynamics in lymph nodes during the induction of tolerance and immunity. Nat Immunol. 2004;5:1235-1242.
25. Dittmer U, He H, Messer RJ, et al. Functional impairment of CD8(+) T cells by regulatory T cells during persistent retroviral infection. Immunity. 2004;20:293-303.
26. + regulatory T cells in immunological tolerance to self and non-self. Nat Immunol. 2005;6:345-352.
27. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25): breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol. 1995;155:1151-1164.
28. Gunzer M, Weishaupt C, Hillmer A, et al. A spectrum of biophysical interaction modes between T cells and different antigen-presenting cells during priming in 3-D collagen and in vivo. Blood. 2004;104:2801-2809.
29. Schneider-Schaulies S, Dittmer U. Silencing T cells or T-cell silencing: concepts in virus-induced immunosuppression. J Gen Virol. 2006;87:1423-1438.
30. Kikutani H, Kumanogoh A. Semaphorins in interactions between T cells and antigen-presenting cells. Nat Rev Immunol. 2003;3:159-167.
31. Rothoeft T, Balkow S, Krummen M, et al. Structure and duration of contact between dendritic cells and T cells are controlled by T cell activation state. Eur J Immunol. 2006;36:3105-3117.
32. Varga G, Balkow S, Wild MK, et al. Active MAC-1 (CD11b/CD18) on DCs inhibits full T-cell activation. Blood. 2007;109:661-669.
33. von Boehmer H. Mechanisms of suppression by suppressor T cells. Nat Immunol. 2005;6:338-344.
34. Jonuleit H, Schmitt E, Schuler G, Knop J, Enk AH. Induction of interleukin 10-producing, nonproliferating CD4(+) T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J Exp Med. 2000;192:1213-1222.
35. Tarbell KV, Yamazaki S, Steinman RM. The interactions of dendritic cells with antigen-specific, regulatory T cells that suppress autoimmunity. Semin Immunol. 2006;18:93-102.
36. + regulatory T cells by dendritic cells during the mixed leukocyte reaction. Proc Natl Acad Sci U S A. 2006;103:2758-2763.
37. Gad M, Kristensen NN, Kury E, Claesson MH. Characterization of T-regulatory cells, induced by immature dendritic cells, which inhibit enteroantigen-reactive colitis-inducing T-cell responses in vitro and in vivo. Immunology. 2004;113:499-508.
38. + Tr cells. Blood. 2005;105:1162-1169.
39. Tang Q, Adams JY, Tooley AJ, et al. Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat Immunol. 2006;7:83-92.
40. Reichardt P, Dornbach B, Rong S, et al. Naive B cells generate regulatory T cells in the presence of a mature immunologic synapse. Blood. 2007;110:1519-1529.
41. Zelinskyy G, Kraft AR, Schimmer S, Arndt T, Dittmer U. Kinetics of CD8(+) effector T cell responses and induced CD4(+) regulatory T cell responses during Friend retrovirus infection. Eur J Immunol. 2006;36:2658-2670.
42. Estes JD, Li Q, Reynolds MR, et al. Premature induction of an immunosuppressive regulatory T cell response during acute simian immunodeficiency virus infection. J Infect Dis. 2006;193:703-712.
43. Kraft AR, Arndt T, Hasenkrug KJ, Dittmer U. Effective treatment of retrovirus-induced suppression of antibody responses with CpG oligodeoxynucleotides. J Gen Virol. 2005;86:3365-3368.
44. Kraft AR, Krux F, Schimmer S, Ohlen C, Greenberg PD, Dittmer U. CpG oligodeoxynucleotides allow for effective adoptive T-cell therapy in chronic retroviral infection. Blood. 2007;109:2982-2984.
45. Knight SC, Elsley W, Wang H. Mechanisms of loss of functional dendritic cells in HIV-1 infection. J Leukoc Biol. 1997;62:78-81.
46. Fantuzzi L, Purificato C, Donato K, Belardelli F, Gessani S. Human immunodeficiency virus type 1 gp120 induces abnormal maturation and functional alterations of dendritic cells: a novel mechanism for AIDS pathogenesis. J Virol. 2004;78:9763-9772.
47. Muthumani K, Hwang DS, Choo AY, et al. HIV-1 Vpr inhibits the maturation and activation of macrophages and dendritic cells in vitro. Int Immunol. 2005;17:103-116.
48. Majumder B, Janket ML, Schafer EA, et al. Human immunodeficiency virus type 1 Vpr impairs dendritic cell maturation and T-cell activation: implications for viral immune escape. J Virol. 2005;79:7990-8003.
49. Granelli-Piperno A, Shimeliovich I, Pack M, Trumpfheller C, Steinman RM. HIV-1 selectively infects a subset of nonmaturing BDCA1-positive dendritic cells in human blood. J Immunol. 2006;176:991-998.
50. Krathwohl MD, Schacker TW, Anderson JL. Abnormal presence of semimature dendritic cells that induce regulatory T cells in HIV-infected subjects. J Infect Dis. 2006;193:494-504.
51. + regulatory T cells, which suppress HIV-specific CD4 T-cell responses in HIV-infected patients. Blood. 2004;104:3249-3256.
52. Kinter AL, Hennessey M, Bell A, et al. CD25(+)CD4(+) regulatory T cells from the peripheral blood of asymptomatic HIV-infected individuals regulate CD4(+) and CD8(+) HIV-specific T cell immune responses in vitro and are associated with favorable clinical markers of disease status. J Exp Med. 2004;200:331-343.
53. Andersson J, Boasso A, Nilsson J, et al. The prevalence of regulatory T cells in lymphoid tissue is correlated with viral load in HIV-infected patients. J Immunol. 2005;174:3143-3147.
54. + regulatory T cells control T-cell responses to human immunodeficiency virus and cytomegalovirus antigens. J Virol. 2004;78:2454-2459.
55. Nilsson J, Boasso A, Velilla PA, et al. HIV-1-driven regulatory T-cell accumulation in lymphoid tissues is associated with disease progression in HIV/AIDS. Blood. 2006;108:3808-3817.