Extracellular ATP reduces HIV-1 transfer from immature dendritic cells to CD4+T lymphocytes

Springer Science and Business Media LLC - Tập 5 - Trang 1-15 - 2008
Corinne Barat1, Caroline Gilbert1, Michael Imbeault1, Michel J Tremblay1
1Laboratoire d'Immuno-Rétrovirologie Humaine, Centre de Recherche en Infectiologie, Laurier, Canada

Tóm tắt

Dendritic cells (DCs) are considered as key mediators of the early events in human immunodeficiency virus type 1 (HIV-1) infection at mucosal sites. Previous studies have shown that surface-bound virions and/or internalized viruses found in endocytic vacuoles of DCs are efficiently transferred to CD4+ T cells. Extracellular adenosine triphosphate (ATP) either secreted or released from necrotic cells induces a distorted maturation of DCs, transiently increases their endocytic capacity and affects their migratory capacity. Knowing that high extracellular ATP concentrations are present in situations of tissue injury and inflammation, we investigated the effect of ATP on HIV-1 transmission from DCs to CD4+ T lymphocytes. In this study, we show that extracellular ATP reduces HIV-1 transfer from immature monocyte-derived DCs (iDCs) to autologous CD4+ T cells. This observed decrease in viral replication was related to a lower proportion of infected CD4+ T cells following transfer, and was seen with both X4- and R5-tropic isolates of HIV-1. Extracellular ATP had no effect on direct CD4+ T cell infection as well as on productive HIV-1 infection of iDCs. These observations indicate that extracellular ATP affects HIV-1 infection of CD4+ T cells in trans with no effect on de novo virus production by iDCs. Additional experiments suggest that extracellular ATP might modulate the trafficking pathway of internalized virions within iDCs leading to an increased lysosomal degradation, which could be partly responsible for the decreased HIV-1 transmission. These results suggest that extracellular ATP can act as a factor controlling HIV-1 propagation.

Tài liệu tham khảo

Smed-Sorensen A, Lore K, Vasudevan J, Louder MK, Andersson J, Mascola JR, Spetz AL, Koup RA: Differential susceptibility to human immunodeficiency virus type 1 infection of myeloid and plasmacytoid dendritic cells. J Virol. 2005, 79 (14): 8861-8869. 10.1128/JVI.79.14.8861-8869.2005. Turville SG, Cameron PU, Handley A, Lin G, Pohlmann S, Doms RW, Cunningham AL: Diversity of receptors binding HIV on dendritic cell subsets. Nat Immunol. 2002, 3 (10): 975-983. 10.1038/ni841. Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, Middel J, Cornelissen IL, Nottet HS, KewalRamani VN, Littman DR, Figdor CG, van Kooyk Y: DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell. 2000, 100 (5): 587-597. 10.1016/S0092-8674(00)80694-7. Geijtenbeek TB, Torensma R, van Vliet SJ, van Duijnhoven GC, Adema GJ, van Kooyk Y, Figdor CG: Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell. 2000, 100 (5): 575-585. 10.1016/S0092-8674(00)80693-5. Magerus-Chatinet A, Yu H, Garcia S, Ducloux E, Terris B, Bomsel M: Galactosyl ceramide expressed on dendritic cells can mediate HIV-1 transfer from monocyte derived dendritic cells to autologous T cells. Virology. 2007, 362 (1): 67-74. 10.1016/j.virol.2006.11.035. Cavrois M, Neidleman J, Kreisberg JF, Greene WC: In vitro derived dendritic cells trans-infect CD4 T cells primarily with surface-bound HIV-1 virions. PLoS Pathog. 2007, 3 (1): e4-10.1371/journal.ppat.0030004. Ganesh L, Leung K, Lore K, Levin R, Panet A, Schwartz O, Koup RA, Nabel GJ: Infection of specific dendritic cells by CCR5-tropic human immunodeficiency virus type 1 promotes cell-mediated transmission of virus resistant to broadly neutralizing antibodies. J Virol. 2004, 78 (21): 11980-11987. 10.1128/JVI.78.21.11980-11987.2004. Kwon DS, Gregorio G, Bitton N, Hendrickson WA, Littman DR: DC-SIGN-mediated internalization of HIV is required for trans-enhancement of T cell infection. Immunity. 2002, 16 (1): 135-144. 10.1016/S1074-7613(02)00259-5. McDonald D, Wu L, Bohks SM, KewalRamani VN, Unutmaz D, Hope TJ: Recruitment of HIV and its receptors to dendritic cell-T cell junctions. Science. 2003, 300 (5623): 1295-1297. 10.1126/science.1084238. Wang JH, Janas AM, Olson WJ, Wu L: Functionally distinct transmission of human immunodeficiency virus type 1 mediated by immature and mature dendritic cells. J Virol. 2007, 81 (17): 8933-8943. 10.1128/JVI.00878-07. Turville SG, Santos JJ, Frank I, Cameron PU, Wilkinson J, Miranda-Saksena M, Dable J, Stossel H, Romani N, Piatak M, Lifson JD, Pope M, Cunningham AL: Immunodeficiency virus uptake, turnover, and 2-phase transfer in human dendritic cells. Blood. 2004, 103 (6): 2170-2179. 10.1182/blood-2003-09-3129. Dong C, Janas AM, Wang JH, Olson WJ, Wu L: Characterization of human immunodeficiency virus type 1 replication in immature and mature dendritic cells reveals dissociable cis- and trans-infection. J Virol. 2007, 81 (20): 11352-11362. 10.1128/JVI.01081-07. Arrighi JF, Pion M, Garcia E, Escola JM, van Kooyk Y, Geijtenbeek TB, Piguet V: DC-SIGN-mediated infectious synapse formation enhances X4 HIV-1 transmission from dendritic cells to T cells. J Exp Med. 2004, 200 (10): 1279-1288. 10.1084/jem.20041356. Nobile C, Petit C, Moris A, Skrabal K, Abastado JP, Mammano F, Schwartz O: Covert Human Immunodeficiency Virus Replication in Dendritic Cells and in DC-SIGN-Expressing Cells Promotes Long-Term Transmission to Lymphocytes. J Virol. 2005, 79 (9): 5386-5399. 10.1128/JVI.79.9.5386-5399.2005. Smith AL, Ganesh L, Leung K, Jongstra-Bilen J, Jongstra J, Nabel GJ: Leukocyte-specific protein 1 interacts with DC-SIGN and mediates transport of HIV to the proteasome in dendritic cells. J Exp Med. 2007, 204 (2): 421-430. 10.1084/jem.20061604. Burleigh L, Lozach PY, Schiffer C, Staropoli I, Pezo V, Porrot F, Canque B, Virelizier JL, Arenzana-Seisdedos F, Amara A: 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): 2949-2957. 10.1128/JVI.80.6.2949-2957.2006. Jolly C, Sattentau QJ: Retroviral spread by induction of virological synapses. Traffic. 2004, 5 (9): 643-650. 10.1111/j.1600-0854.2004.00209.x. Gilbert C, Barat C, Cantin R, Tremblay MJ: Involvement of Src and Syk tyrosine kinases in HIV-1 transfer from dendritic cells to CD4+ T lymphocytes. J Immunol. 2007, 178 (5): 2862-2871. Di Virgilio F, Chiozzi P, Ferrari D, Falzoni S, Sanz JM, Morelli A, Torboli M, Bolognesi G, Baricordi OR: Nucleotide receptors: an emerging family of regulatory molecules in blood cells. Blood. 2001, 97 (3): 587-600. 10.1182/blood.V97.3.587. Filippini A, Taffs RE, Sitkovsky MV: Extracellular ATP in T-lymphocyte activation: possible role in effector functions. Proc Natl Acad Sci U S A. 1990, 87 (21): 8267-8271. 10.1073/pnas.87.21.8267. Berchtold S, Ogilvie AL, Bogdan C, Muhl-Zurbes P, Ogilvie A, Schuler G, Steinkasserer A: Human monocyte derived dendritic cells express functional P2X and P2Y receptors as well as ecto-nucleotidases. FEBS Lett. 1999, 458 (3): 424-428. 10.1016/S0014-5793(99)01197-7. la Sala A, Ferrari D, Corinti S, Cavani A, Di Virgilio F, Girolomoni G: Extracellular ATP induces a distorted maturation of dendritic cells and inhibits their capacity to initiate Th1 responses. J Immunol. 2001, 166 (3): 1611-1617. la Sala A, Sebastiani S, Ferrari D, Di Virgilio F, Idzko M, Norgauer J, Girolomoni G: Dendritic cells exposed to extracellular adenosine triphosphate acquire the migratory properties of mature cells and show a reduced capacity to attract type 1 T lymphocytes. Blood. 2002, 99 (5): 1715-1722. 10.1182/blood.V99.5.1715. Wilkin F, Stordeur P, Goldman M, Boeynaems JM, Robaye B: Extracellular adenine nucleotides modulate cytokine production by human monocyte-derived dendritic cells: dual effect on IL-12 and stimulation of IL-10. Eur J Immunol. 2002, 32 (9): 2409-2417. 10.1002/1521-4141(200209)32:9<2409::AID-IMMU2409>3.0.CO;2-H. Schnurr M, Then F, Galambos P, Scholz C, Siegmund B, Endres S, Eigler A: Extracellular ATP and TNF-alpha synergize in the activation and maturation of human dendritic cells. J Immunol. 2000, 165 (8): 4704-4709. Marteau F, Gonzalez NS, Communi D, Goldman M, Boeynaems JM, Communi D: Thrombospondin-1 and indoleamine 2,3-dioxygenase are major targets of extracellular ATP in human dendritic cells. Blood. 2005, 106 (12): 3860-3866. 10.1182/blood-2005-05-1843. Coutinho-Silva R, Persechini PM, Bisaggio RD, Perfettini JL, Neto AC, Kanellopoulos JM, Motta-Ly I, Dautry-Varsat A, Ojcius DM: P2Z/P2X7 receptor-dependent apoptosis of dendritic cells. Am J Physiol. 1999, 276 (5 Pt 1): C1139-47. Idzko M, Dichmann S, Ferrari D, Di Virgilio F, la Sala A, Girolomoni G, Panther E, Norgauer J: Nucleotides induce chemotaxis and actin polymerization in immature but not mature human dendritic cells via activation of pertussis toxin-sensitive P2y receptors. Blood. 2002, 100 (3): 925-932. 10.1182/blood.V100.3.925. Gilbert C, Cantin R, Barat C, Tremblay MJ: HIV-1 replication in dendritic cell/T-cell co-cultures is increased upon incorporation of host LFA-1 due to a higher virus productive infection in immature dendritic cells. J Virol. 2007 Ohkuma S, Poole B: Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc Natl Acad Sci U S A. 1978, 75 (7): 3327-3331. 10.1073/pnas.75.7.3327. Fredericksen BL, Wei BL, Yao J, Luo T, Garcia JV: Inhibition of endosomal/lysosomal degradation increases the infectivity of human immunodeficiency virus. J Virol. 2002, 76 (22): 11440-11446. 10.1128/JVI.76.22.11440-11446.2002. 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): 2733-2737. Codina J, Gurich R, Dubose TD: Peptides derived from the human transferrin receptor stimulate endosomal acidification via a Gi-type protein. Kidney Int. 1999, 55 (6): 2376-2382. 10.1046/j.1523-1755.1999.00490.x. Baroni M, Pizzirani C, Pinotti M, Ferrari D, Adinolfi E, Calzavarini S, Caruso P, Bernardi F, Di Virgilio F: Stimulation of P2 (P2X7) receptors in human dendritic cells induces the release of tissue factor-bearing microparticles. Faseb J. 2007 Pizzirani C, Ferrari D, Chiozzi P, Adinolfi E, Sandona D, Savaglio E, Di Virgilio F: Stimulation of P2 receptors causes release of IL-1beta-loaded microvesicles from human dendritic cells. Blood. 2007, 109 (9): 3856-3864. 10.1182/blood-2005-06-031377. Bakri Y, Schiffer C, Zennou V, Charneau P, Kahn E, Benjouad A, Gluckman JC, Canque B: The maturation of dendritic cells results in postintegration inhibition of HIV-1 replication. J Immunol. 2001, 166 (6): 3780-3788. Izquierdo-Useros N, Blanco J, Erkizia I, Fernandez-Figueras MT, Borras FE, Naranjo-Gomez M, Bofill M, Ruiz L, Clotet B, Martinez-Picado J: Maturation of blood-derived dendritic cells enhances human immunodeficiency virus type 1 capture and transmission. J Virol. 2007, 81 (14): 7559-7570. 10.1128/JVI.02572-06. Frank I, Piatak M, Stoessel H, Romani N, Bonnyay D, Lifson JD, Pope M: Infectious and whole inactivated simian immunodeficiency viruses interact similarly with primate dendritic cells (DCs): differential intracellular fate of virions in mature and immature DCs. J Virol. 2002, 76 (6): 2936-2951. 10.1128/JVI.76.6.2936-2951.2002. Garcia E, Pion M, Pelchen-Matthews A, Collinson L, Arrighi JF, Blot G, Leuba F, Escola JM, Demaurex N, Marsh M, Piguet V: HIV-1 trafficking to the dendritic cell-T-cell infectious synapse uses a pathway of tetraspanin sorting to the immunological synapse. Traffic. 2005, 6 (6): 488-501. 10.1111/j.1600-0854.2005.00293.x. Engering A, Geijtenbeek TB, van Vliet SJ, Wijers M, van Liempt E, Demaurex N, Lanzavecchia A, Fransen J, Figdor CG, Piguet V, van Kooyk Y: The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J Immunol. 2002, 168 (5): 2118-2126. Carballo E, Colomer D, Vives-Corrons JL, Blackshear PJ, Gil J: Characterization and purification of a protein kinase C substrate in human B cells. Identification as lymphocyte-specific protein 1 (LSP1). J Immunol. 1996, 156 (5): 1709-1713. Huang CK, Zhan L, Ai Y, Jongstra J: LSP1 is the major substrate for mitogen-activated protein kinase-activated protein kinase 2 in human neutrophils. J Biol Chem. 1997, 272 (1): 17-19. 10.1074/jbc.272.1.17. Cao W, Lee SH, Lu J: CD83 is preformed inside monocytes, macrophages and dendritic cells, but it is only stably expressed on activated dendritic cells. Biochem J. 2005, 385 (Pt 1): 85-93. Klein E, Koch S, Borm B, Neumann J, Herzog V, Koch N, Bieber T: CD83 localization in a recycling compartment of immature human monocyte-derived dendritic cells. Int Immunol. 2005, 17 (4): 477-487. 10.1093/intimm/dxh228. Lazarowski ER, Boucher RC, Harden TK: Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol Pharmacol. 2003, 64 (4): 785-795. 10.1124/mol.64.4.785. Robson SC, Kaczmarek E, Siegel JB, Candinas D, Koziak K, Millan M, Hancock WW, Bach FH: Loss of ATP diphosphohydrolase activity with endothelial cell activation. J Exp Med. 1997, 185 (1): 153-163. 10.1084/jem.185.1.153. Wang X, Arcuino G, Takano T, Lin J, Peng WG, Wan P, Li P, Xu Q, Liu QS, Goldman SA, Nedergaard M: P2X7 receptor inhibition improves recovery after spinal cord injury. Nat Med. 2004, 10 (8): 821-827. 10.1038/nm1082. Mizumoto N, Kumamoto T, Robson SC, Sevigny J, Matsue H, Enjyoji K, Takashima A: CD39 is the dominant Langerhans cell-associated ecto-NTPDase: modulatory roles in inflammation and immune responsiveness. Nat Med. 2002, 8 (4): 358-365. 10.1038/nm0402-358. Bounou S, Giguere JF, Cantin R, Gilbert C, Imbeault M, Martin G, Tremblay MJ: The importance of virus-associated host ICAM-1 in human immunodeficiency virus type 1 dissemination depends on the cellular context. Faseb J. 2004, 18 (11): 1294-1296. Zhao C, Cantin R, Breton M, Papadopoulou B, Tremblay MJ: DC-SIGN-mediated transfer of HIV-1 is compromised by the ability of Leishmania infantum to exploit DC-SIGN as a ligand. J Infect Dis. 2005, 191 (10): 1665-1669. 10.1086/429673. Cantin R, Fortin JF, Lamontagne G, Tremblay M: The presence of host-derived HLA-DR1 on human immunodeficiency virus type 1 increases viral infectivity. J Virol. 1997, 71 (3): 1922-1930. Dornadula G, Zhang H, Shetty S, Pomerantz RJ: HIV-1 virions produced from replicating peripheral blood lymphocytes are more infectious than those from nonproliferating macrophages due to higher levels of intravirion reverse transcripts: implications for pathogenesis and transmission. Virology. 1999, 253 (1): 10-16. 10.1006/viro.1998.9465. Levy DN, Aldrovandi GM, Kutsch O, Shaw GM: Dynamics of HIV-1 recombination in its natural target cells. Proc Natl Acad Sci U S A. 2004, 101 (12): 4204-4209. 10.1073/pnas.0306764101. Bounou S, Leclerc JE, Tremblay MJ: Presence of host ICAM-1 in laboratory and clinical strains of human immunodeficiency virus type 1 increases virus infectivity and CD4(+)-T-cell depletion in human lymphoid tissue, a major site of replication in vivo. J Virol. 2002, 76 (3): 1004-1014. Zar JH: Biostatistical Analysis. Edited by: HALL PRENTICE. 1984, New Jersey