Regulatory T cells diminish HIV infection in dendritic cells - conventional CD4+ T cell clusters

Frontiers in Immunology

Volumn 5, Issue MAY, 2014, Pages

  Moreno Fernandez, Maria E ^a,b   Joedicke, Jara J ^c   Chougnet, Claire A ^a  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

Actin cytoskeleton; CTLA 4; Cyclic AMP; Dendritic cells; HIV 1; Regulatory T cells

Indexed keywords

CD40 ANTIGEN; CD83 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; HLA DR ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 6; NTERLEUKIN 12P40; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; ARTICLE; CELL MATURATION; DENDRITIC CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; IMMUNOLOGICAL SYNAPSE; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE;

EID: 84905489638     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00199     Document Type: Article

References (57)

1. Piguet V, Steinman RM. The interaction of HIV with dendritic cells: outcomes and pathways. Trends Immunol (2007) 28(11):503-10. doi: 10.1016/j.it.2007.07.010
2. Granelli-Piperno A, Delgado E, Finkel V, Paxton W, Steinman RM. Immature dendritic cells selectively replicate macrophagetropic (M-tropic) human immunodeficiency virus type 1, while mature cells efficiently transmit both M- and T-tropic virus to T cells. J Virol (1998) 72(4):2733-7.
3. Smed-Sorensen A, Lore K, Vasudevan J, Louder MK, Andersson J, Mascola JR, et al. Differential susceptibility to human immunodeficiency virus type 1 infection of myeloid and plasmacytoid dendritic cells. J Virol (2005) 79(14):8861-9. doi:10.1128/JVI.79.14.8861-8869.2005
4. Burleigh L, Lozach PY, Schiffer C, Staropoli I, Pezo V, Porrot F, et al. Infection of dendritic cells (DCs), not DC-SIGN-mediated internalization of human immunodeficiency virus, is required for long-term transfer of virus to T cells. J Virol (2006) 80(6):2949-57. doi:10.1128/JVI.80.6.2949-2957.2006
5. Harman AN, Wilkinson J, Bye CR, Bosnjak L, Stern JL, Nicholle M, et al. HIV induces maturation of monocyte-derived dendritic cells and Langerhans cells. J Immunol (2006) 177(10):7103-13. doi:10.4049/jimmunol.177.10.7103
6. Gummuluru S, KewalRamani VN, Emerman M. Dendritic cell-mediated viral transfer to T cells is required for human immunodeficiency virus type 1 persistence in the face of rapid cell turnover. J Virol (2002) 76(21):10692-701. doi:10.1128/JVI.76.21.10692-10701.2002
7. Pope M, Betjes MG, Romani N, Hirmand H, Cameron PU, Hoffman L, et al. Conjugates of dendritic cells and memory T lymphocytes from skin facilitate productive infection with HIV-1. Cell (1994) 78(3):389-98. doi:10.1016/0092-8674(94)90418-9
8. Onishi Y, Fehervari Z, Yamaguchi T, Sakaguchi S. Foxp3+ natural regulatory T cells preferentially form aggregates on dendritic cells in vitro and actively inhibit their maturation. Proc Natl Acad Sci U S A (2008) 105(29):10113-8. doi:10.1073/pnas.0711106105
9. Nakamura K, Kitani A, Strober W. Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor beta. J Exp Med (2001) 194(5):629-44. doi:10.1084/jem.194.5.629
10. Bopp T, Becker C, Klein M, Klein-Hessling S, Palmetshofer A, Serfling E, et al. Cyclic adenosine monophosphate is a key component of regulatory T cell-mediated suppression. J Exp Med (2007) 204(6):1303-10. doi:10.1084/jem.20062129
11. Nilsson J, Boasso A, Velilla PA, Zhang R, Vaccari M, Franchini G, et al. HIV-1-driven regulatory T-cell accumulation in lymphoid tissues is associated with disease progression in HIV/AIDS. Blood (2006) 108(12):3808-17. doi:10.1182/blood-2006-05-021576
12. Holmes D, Jiang Q, Zhang L, Su L. Foxp3 and Treg cells in HIV-1 infection and immuno-pathogenesis. Immunol Res (2008) 41(3):248-66. doi:10.1007/s12026-008-8037-x
13. Ndhlovu LC, Loo CP, Spotts G, Nixon DF, Hecht FM. FOXP3 expressing CD127lo CD4+ T cells inversely correlate with CD38+ CD8+ T cell activation levels in primary HIV-1 infection. J Leukoc Biol (2008) 83(2):254-62. doi:10.1189/jlb.0507281
14. Liu J, Gong N, Huang X, Reynolds AD, Mosley RL, Gendelman HE. Neuromodulatory activities of CD4+CD25+ regulatory T cells in a murine model of HIV-1-associated neurodegeneration. J Immunol (2009) 182(6):3855-65. doi:10.4049/jimmunol.0803330
15. Moreno-Fernandez ME, Rueda CM, Rusie LK, Chougnet CA. Regulatory T cells control HIV replication in activated T cells through a cAMP-dependent mechanism. Blood (2011) 117(20):5372-80. doi:10.1182/blood-2010-12-323162
16. Goujon C, Jarrosson-Wuilleme L, Bernaud J, Rigal D, Darlix JL, Cimarelli A. With a little help from a friend: increasing HIV transduction of monocyte-derived dendritic cells with virion-like particles of SIV(MAC). Gene Ther (2006) 13(12):991-4. doi:10.1038/sj.gt.3302753
17. Chen P, Hubner W, Spinelli MA, Chen BK. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J Virol (2007) 81(22):12582-95. doi:10.1128/JVI.00381-07
18. Lore K, Smed-Sorensen A, Vasudevan J, Mascola JR, Koup RA. Myeloid and plasmacytoid dendritic cells transfer HIV-1 preferentially to antigen-specific CD4+ T cells. J Exp Med (2005) 201(12):2023-33. doi:10.1084/jem.20042413
19. Tadokoro CE, Shakhar G, Shen S, Ding Y, Lino AC, Maraver A, et al. Regulatory T cells inhibit stable contacts between CD4+ T cells and dendritic cells in vivo. J Exp Med (2006) 203(3):505-11. doi:10.1084/jem.20050783
20. Misra N, Bayry J, Lacroix-Desmazes S, Kazatchkine MD, Kaveri SV. Cutting edge: human CD4+CD25+ T cells restrain the maturation and antigen-presenting function of dendritic cells. J Immunol (2004) 172(8):4676-80. doi:10.4049/jimmunol.172.8.4676
21. Matarrese P, Malorni W. Human immunodeficiency virus (HIV)-1 proteins and cytoskeleton: partners in viral life and host cell death. Cell Death Differ (2005) 12(Suppl 1):932-41. doi:10.1038/sj.cdd.4401582
22. Bukrinskaya A, Brichacek B, Mann A, Stevenson M. Establishment of a functional human immunodeficiency virus type 1 (HIV-1) reverse transcription complex involves the cytoskeleton. J Exp Med (1998) 188(11):2113-25. doi:10.1084/jem.188.11.2113
23. Oderup C, Cederbom L, Makowska A, Cilio CM, Ivars F. Cytotoxic T lymphocyte antigen-4-dependent down-modulation of costimulatory molecules on dendritic cells in CD4+ CD25+ regulatory T-cell-mediated suppression. Immunology (2006) 118(2):240-9. doi:10.1111/j.1365-2567.2006.02362.x
24. Ring S, Karakhanova S, Johnson T, Enk AH, Mahnke K. Gap junctions between regulatory T cells and dendritic cells prevent sensitization of CD8(+) T cells. J Allergy Clin Immunol (2010) 125(1):e1-7. doi:10.1016/j.jaci.2009.10.025
25. Hu J, Gardner MB, Miller CJ. Simian immunodeficiency virus rapidly penetrates the cervicovaginal mucosa after intravaginal inoculation and infects intraepithelial dendritic cells. J Virol (2000) 74(13):6087-95. doi:10.1128/JVI.74.13.6087-6095.2000
26. Miller CJ, Shattock RJ. Target cells in vaginal HIV transmission. Microbes Infect (2003) 5(1):59-67. doi:10.1016/S1286-4579(02)00056-4
27. Cameron PU, Freudenthal PS, Barker JM, Gezelter S, Inaba K, Steinman RM. Dendritic cells exposed to human immunodeficiency virus type-1 transmit a vigorous cytopathic infection to CD4+ T cells. Science (1992) 257(5068):383-7. doi:10.1126/science.1352913
28. Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, Middel J, et al. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell (2000) 100(5):587-97. doi:10.1016/S0092-8674(00)80694-7
29. Epple HJ, Loddenkemper C, Kunkel D, Troger H, Maul J, Moos V, et al. Mucosal but not peripheral FOXP3+ regulatory T cells are highly increased in untreated HIV infection and normalize after suppressive HAART. Blood (2006) 108(9):3072-8. doi:10.1182/blood-2006-04-016923
30. Vignali DA, Collison LW, Workman CJ. How regulatory T cells work. Nat Rev Immunol (2008) 8(7):523-32. doi:10.1038/nri2343
31. Zhu T, Mo H, Wang N, Nam DS, Cao Y, Koup RA, et al. Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science (1993) 261(5125):1179-81. doi:10.1126/science.8356453
32. Schuitemaker H, Koot M, Kootstra NA, Dercksen MW, de Goede RE, van Steenwijk RP, et al. Biological phenotype of human immunodeficiency virus type 1 clones at different stages of infection: progression of disease is associated with a shift from monocytotropic to T-cell-tropic virus population. J Virol (1992) 66(3):1354-60.
33. Turville SG, Santos JJ, Frank I, Cameron PU, Wilkinson J, Miranda-Saksena M, et al. Immunodeficiency virus uptake, turnover, and 2-phase transfer in human dendritic cells. Blood (2004) 103(6):2170-9. doi:10.1182/blood-2003-09-3129
34. Moris A, Pajot A, Blanchet F, Guivel-Benhassine F, Salcedo M, Schwartz O. Dendritic cells and HIV-specific CD4+ T cells: HIV antigen presentation, T-cell activation, and viral transfer. Blood (2006) 108(5):1643-51. doi:10.1182/blood-2006-02-006361
35. Esquerre M, Tauzin B, Guiraud M, Muller S, Saoudi A, Valitutti S. Human regulatory T cells inhibit polarization of T helper cells toward antigen-presenting cells via a TGF-beta-dependent mechanism. Proc Natl Acad Sci U S A (2008) 105(7):2550-5. doi:10.1073/pnas.0708350105
36. Rey O, Canon J, Krogstad P. HIV-1 Gag protein associates with F-actin present in microfilaments. Virology (1996) 220(2):530-4. doi:10.1006/viro.1996.0343
37. Sasaki H, Nakamura M, Ohno T, Matsuda Y, Yuda Y, Nonomura Y. Myosin-actin interaction plays an important role in human immunodeficiency virus type 1 release from host cells. Proc Natl Acad Sci U S A (1995) 92(6):2026-30. doi:10.1073/pnas.92.6.2026
38. Spector I, Shochet NR, Blasberger D, Kashman Y. Latrunculins - novel marine macrolides that disrupt microfilament organization and affect cell growth: I. Comparison with cytochalasin D. Cell Motil Cytoskeleton (1989) 13(3):127-44.
39. Nikolic DS, Lehmann M, Felts R, Garcia E, Blanchet FP, Subramaniam S, et al. HIV-1 activates Cdc42 and induces membrane extensions in immature dendritic cells to facilitate cell-to-cell virus propagation. Blood (2011) 118(18):4841-52. doi:10.1182/blood-2010-09-305417
40. del Real G, Jimenez-Baranda S, Mira E, Lacalle RA, Lucas P, Gomez-Mouton C, et al. Statins inhibit HIV-1 infection by down-regulating Rho activity. J Exp Med (2004) 200(4):541-7. doi:10.1084/jem.20040061
41. Permanyer M, Pauls E, Badia R, Este JA, Ballana E. The cortical actin determines different susceptibility of naive and memory CD4+ T cells to HIV-1 cell-to-cell transmission and infection. PLoS One (2013) 8(11):e79221. doi:10.1371/journal.pone.0079221
42. Anand AR, Zhao H, Nagaraja T, Robinson LA, Ganju RK. N-terminal Slit2 inhibits HIV-1 replication by regulating the actin cytoskeleton. Retrovirology (2013) 10:2. doi:10.1186/1742-4690-10-2
43. Felts RL, Narayan K, Estes JD, Shi D, Trubey CM, Fu J, et al. 3D visualization of HIV transfer at the virological synapse between dendritic cells and T cells. Proc Natl Acad Sci U S A (2010) 107(30):13336-41. doi:10.1073/pnas.1003040107
44. Oida T, Xu L, Weiner HL, Kitani A, Strober W. TGF-beta-mediated suppression by CD4+CD25+ T cells is facilitated by CTLA-4 signaling. J Immunol (2006) 177(4):2331-9. doi:10.4049/jimmunol.177.4.2331
45. Poli G, Kinter AL, Justement JS, Bressler P, Kehrl JH, Fauci AS. Transforming growth factor beta suppresses human immunodeficiency virus expression and replication in infected cells of the monocyte/macrophage lineage. J Exp Med (1991) 173(3):589-97. doi:10.1084/jem.173.3.589
46. Barat C, Gilbert C, Imbeault M, Tremblay MJ. Extracellular ATP reduces HIV-1 transfer from immature dendritic cells to CD4+ T lymphocytes. Retrovirology (2008) 5:30. doi:10.1186/1742-4690-5-30
47. Sun Y, Li L, Lau F, Beavo JA, Clark EA. Infection of CD4+ memory T cells by HIV-1 requires expression of phosphodiesterase 4. J Immunol (2000) 165(4):1755-61. doi:10.4049/jimmunol.165.4.1755
48. Wilson JM, Ross WG, Agbai ON, Frazier R, Figler RA, Rieger J, et al. The A2B adenosine receptor impairs the maturation and immunogenicity of dendritic cells. J Immunol (2009) 182(8):4616-23. doi:10.4049/jimmunol.0801279
49. Banas B, Eberle J, Schlondorff D, Luckow B. Modulation of HIV-1 enhancer activity and virus production by cAMP. FEBS Lett (2001) 509(2):207-12. doi:10.1016/S0014-5793(01)03182-9
50. Howe AK. Regulation of actin-based cell migration by cAMP/PKA. Biochim Biophys Acta (2004) 1692(2-3):159-74. doi:10.1016/j.bbamcr.2004.03.005
51. Cecchinato V, Tryniszewska E, Ma ZM, Vaccari M, Boasso A, Tsai WP, et al. Immune activation driven by CTLA-4 blockade augments viral replication at mucosal sites in simian immunodeficiency virus infection. J Immunol (2008) 180(8):5439-47. doi:10.4049/jimmunol.180.8.5439
52. Pandrea I, Gaufin T, Brenchley JM, Gautam R, Monjure C, Gautam A, et al. Cutting edge: experimentally induced immune activation in natural hosts of simian immunodeficiency virus induces significant increases in viral replication and CD4+ T cell depletion. J Immunol (2008) 181(10):6687-91. doi:10.4049/jimmunol.181.10.6687
53. Card CM, McLaren PJ, Wachihi C, Kimani J, Plummer FA, Fowke KR. Decreased immune activation in resistance to HIV-1 infection is associated with an elevated frequency of CD4(+)CD25(+)FOXP3(+) regulatory T cells. J Infect Dis (2009) 199(9):1318-22. doi:10.1086/597801
54. Genesca M, Ma ZM, Wang Y, Assaf B, Qureshi H, Fritts L, et al. Live-attenuated lentivirus immunization modulates innate immunity and inflammation while protecting rhesus macaques from vaginal simian immunodeficiency virus challenge. J Virol (2012) 86(17):9188-200. doi:10.1128/JVI.00532-12
55. Kornfeld C, Ploquin MJ, Pandrea I, Faye A, Onanga R, Apetrei C, et al. Antiinflammatory profiles during primary SIV infection in African green monkeys are associated with protection against AIDS. J Clin Invest (2005) 115(4):1082-91. doi:10.1172/JCI200523006
56. Iwashiro M, Messer RJ, Peterson KE, Stromnes IM, Sugie T, Hasenkrug KJ. Immunosuppression by CD4+ regulatory T cells induced by chronic retroviral infection. Proc Natl Acad Sci U S A (2001) 98(16):9226-30. doi:10.1073/pnas.151174198
57. Zelinskyy G, Dietze KK, Husecken YP, Schimmer S, Nair S, Werner T, et al. The regulatory T-cell response during acute retroviral infection is locally defined and controls the magnitude and duration of the virus-specific cytotoxic T-cell response. Blood (2009) 114(15):3199-207. doi:10.1182/blood-2009-03-208736