HIV-1 Capture and Transmission by Dendritic Cells: The Role of Viral Glycolipids and the Cellular Receptor Siglec-1

PLoS Pathogens

Volumn 10, Issue 7, 2014, Pages

  Izquierdo Useros, Nuria ^a   Lorizate, Maier ^b   McLaren, Paul J ^c   Telenti, Amalio ^c   Kräusslich, Hans Georg ^d   Martinez Picado, Javier ^a,e,f  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^e UNIVERSITY OF VIC CENTRAL UNIVERSITY OF CATALONIA   (Spain)

^f INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOLIPID; SIALOADHESIN; SIGLEC1 PROTEIN, HUMAN;

ANIMAL; DENDRITIC CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; PATHOLOGY; T LYMPHOCYTE; VIROLOGY;

ANIMALS; DENDRITIC CELLS; GLYCOLIPIDS; HIV INFECTIONS; HIV-1; HUMANS; SIALIC ACID BINDING IG-LIKE LECTIN 1; T-LYMPHOCYTES;

EID: 84905386677     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004146     Document Type: Review

References (97)

1. Mellman I, Steinman RM, (2001) Dendritic cells specialized and regulated antigen processing machines. Cell 106: 255-258.
2. Steinman RM, Banchereau J, (2007) Taking dendritic cells into medicine. Nature 449: 419-426.
3. Villadangos JA, Schnorrer P, (2007) Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat Rev Immunol 7: 543-555.
4. Granelli-Piperno A, Moser B, Pope M, Chen D, Wei Y, et al. (1996) Efficient interaction of HIV-1 with purified dendritic cells via multiple chemokine coreceptors. J Exp Med 184: 2433-2438.
5. Turville SG, Cameron PU, Handley A, Lin G, Pöhlmann S, et al. (2002) Diversity of receptors binding HIV on dendritic cell subsets. Nat Immunol 3: 975-983.
6. Granelli-Piperno A, Delgado E, Finkel V, Paxton W, Steinman RM, (1998) 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 72: 2733-2737.
7. Granelli-Piperno A, Finkel V, Delgado E, Steinman RM, (1999) Virus replication begins in dendritic cells during the transmission of HIV-1 from mature dendritic cells to T cells. Curr Biol 9: 21-29.
8. Cameron PU, Forsum U, Teppler H, Granelli-Piperno A, Steinman RM, (1992) During HIV-1 infection most blood dendritic cells are not productively infected and can induce allogeneic CD4+ T cells clonal expansion. Clin Exp Immunol 88: 226-236.
9. Pope M, Gezelter S, Gallo N, Hoffman L, Steinman RM, (1995) Low levels of HIV-1 infection in cutaneous dendritic cells promote extensive viral replication upon binding to memory CD4+ T cells. J Exp Med 182: 2045-2056.
10. Bakri Y, Schiffer C, Zennou V, Charneau P, Kahn E, et al. (2001) The maturation of dendritic cells results in postintegration inhibition of HIV-1 replication. J Immunol 166: 3780-3788.
11. Cameron PU, Freudenthal PS, Barker JM, Gezelter S, Inaba K, et al. (1992) Dendritic cells exposed to human immunodeficiency virus type-1 transmit a vigorous cytopathic infection to CD4+ T cells. Science 257: 383-387.
12. Kawamura T, Gulden FO, Sugaya M, McNamara DT, Borris DL, et al. (2003) R5 HIV productively infects Langerhans cells, and infection levels are regulated by compound CCR5 polymorphisms. Proc Natl Acad Sci U S A 100: 8401-8406.
13. Smed-Sörensen A, Loré K, Vasudevan J, Louder MK, Andersson J, et al. (2005) Differential susceptibility to human immunodeficiency virus type 1 infection of myeloid and plasmacytoid dendritic cells. J Virol 79: 8861-8869.
14. Wu L, KewalRamani VN, (2006) Dendritic-cell interactions with HIV: infection and viral dissemination. Nat Rev Immunol 6: 859-868.
15. Piguet V, Steinman RM, (2007) The interaction of HIV with dendritic cells: outcomes and pathways. Trends Immunol 28: 503-510.
16. Hu Q, Frank I, Williams V, Santos JJ, Watts P, et al. (2004) Blockade of attachment and fusion receptors inhibits HIV-1 infection of human cervical tissue. J Exp Med 199: 1065-1075.
17. Hrecka K, Hao C, Gierszewska M, Swanson SK, Kesik-Brodacka M, et al. (2011) Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474: 658-661.
18. Laguette N, Sobhian B, Casartelli N, Ringeard M, Chable-Bessia C, et al. (2011) SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474: 654-657.
19. Lahouassa H, Daddacha W, Hofmann H, Ayinde D, Logue EC, et al. (2012) SAMHD1 restricts the replication of human immunodeficiency virus type 1 by depleting the intracellular pool of deoxynucleoside triphosphates. Nat Immunol 13: 223-228.
20. Manel N, Hogstad B, Wang Y, Levy DE, Unutmaz D, et al. (2010) A cryptic sensor for HIV-1 activates antiviral innate immunity in dendritic cells. Nature 467: 214-217.
21. Lahaye X, Satoh T, Gentili M, Cerboni S, Conrad C, et al. (2013) The Capsids of HIV-1 and HIV-2 Determine Immune Detection of the Viral cDNA by the Innate Sensor cGAS in Dendritic Cells. Immunity 39: 1132-1142.
22. Blauvelt A, Asada H, Saville MW, Klaus-Kovtun V, Altman DJ, et al. (1997) Productive infection of dendritic cells by HIV-1 and their ability to capture virus are mediated through separate pathways. J Clin Invest 100: 2043-2053.
23. Sanders RW, de Jong EC, Baldwin CE, Schuitemaker JHN, Kapsenberg ML, et al. (2002) Differential Transmission of Human Immunodeficiency Virus Type 1 by Distinct Subsets of Effector Dendritic Cells. J Virol 76: 7812-7821.
24. McDonald D, Wu L, Bohks SM, KewalRamani VN, Unutmaz D, et al. (2003) Recruitment of HIV and its receptors to dendritic cell-T cell junctions. Science 300: 1295-1297.
25. Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, et al. (2000) DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100: 587-597.
26. Kwon DS, Gregorio G, Bitton N, Hendrickson WA, Littman DR, (2002) DC-SIGN-mediated internalization of HIV is required for trans-enhancement of T cell infection. Immunity 16: 135-144.
27. van Kooyk Y, Geijtenbeek TB, (2003) DC-SIGN: escape mechanism for pathogens. Nat Rev Immunol 3: 697-709.
28. Turville SG, Santos JJ, Frank I, Cameron PU, Wilkinson J, et al. (2004) Immunodeficiency virus uptake, turnover, and 2-phase transfer in human dendritic cells. Blood 103: 2170-2179.
29. Izquierdo-Useros N, Blanco J, Erkizia I, Fernández-Figueras MT, Borràs FE, et al. (2007) Maturation of blood-derived dendritic cells enhances human immunodeficiency virus type 1 capture and transmission. J Virol 81: 7559-7570.
30. Wang JH, Janas AM, Olson WJ, Wu L, (2007) Functionally distinct transmission of human immunodeficiency virus type 1 mediated by immature and mature dendritic cells. J Virol 81: 8933-8943.
31. Garcia E, Pion M, Pelchen-Matthews A, Collinson L, Arrighi JF, et al. (2005) HIV-1 trafficking to the dendritic cell-T-cell infectious synapse uses a pathway of tetraspanin sorting to the immunological synapse. Traffic 6: 488-501.
32. Yu HJ, Reuter MA, McDonald D, (2008) HIV traffics through a specialized, surface-accessible intracellular compartment during trans-infection of T cells by mature dendritic cells. PLoS Pathog 4: e1000134.
33. Welsch S, Keppler OT, Habermann A, Allespach I, Krijnse-Locker J, et al. (2007) HIV-1 buds predominantly at the plasma membrane of primary human macrophages. PLoS Pathog 3: e36.
34. Deneka M, Pelchen-Matthews A, Byland R, Ruiz-Mateos E, Marsh M, (2007) In macrophages, HIV-1 assembles into an intracellular plasma membrane domain containing the tetraspanins CD81, CD9, and CD53. J Cell Biol 177: 329-341.
35. Izquierdo-Useros N, Esteban O, Rodriguez-Plata MT, Erkizia I, Prado JG, et al. (2011) Dynamic Imaging of Cell-Free and Cell-Associated Viral Capture in Mature Dendritic Cells. Traffic 12: 1702-1713.
36. Huppa JB, Davis MM, (2003) T-cell-antigen recognition and the immunological synapse. Nat Rev Immunol 3: 973-983.
37. Arrighi JF, Pion M, Garcia E, Escola JM, van Kooyk Y, et al. (2004) DC-SIGN-mediated infectious synapse formation enhances X4 HIV-1 transmission from dendritic cells to T cells. J Exp Med 200: 1279-1288.
38. Piguet V, Sattentau Q, (2004) Dangerous liaisons at the virological synapse. J Clin Invest 114: 605-610.
39. Curtis BM, Scharnowske S, Watson AJ, (1992) Sequence and expression of membrane-associated C-type lectin that exhibits CD4-independent binding of human immunodeficiency virus envelope glycoprotein gpl20. Proc Natl Acad Sci U S A 89: 8356-8360.
40. Nobile C, Petit C, Moris A, Skrabal K, Abastado JP, et al. (2005) Covert human immunodeficiency virus replication in dendritic cells and in DC-SIGN-expressing cells promotes long-term transmission to lymphocytes. J Virol 79: 5386-5399.
41. Turville SG, Arthos J, Donald KM, Lynch G, Naif H, et al. (2001) HIV gp120 receptors on human dendritic cells. Blood 98: 2482-2488.
42. Wu L, Bashirova AA, Martin TD, Villamide L, Mehlhop E, et al. (2002) Rhesus macaque dendritic cells efficiently transmit primate lentiviruses independently of DC-SIGN. Proc Natl Acad Sci U S A 99: 1568-1573.
43. Gummuluru S, Rogel M, Stamatatos L, Emerman M, (2003) Binding of human immunodeficiency virus type 1 to immature dendritic cells can occur independently of DC-SIGN and mannose binding C-type lectin receptors via a cholesterol-dependent pathway. J Virol 77: 12865-12874.
44. Granelli-Piperno A, Pritsker A, Pack M, Shimeliovich I, Arrighi JF, et al. (2005) Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin/CD209 is abundant on macrophages in the normal human lymph node and is not required for dendritic cell stimulation of the mixed leukocyte reaction. J Immunol 175: 4265-4273.
45. Boggiano C, Manel N, Littman DR, (2007) Dendritic cell-mediated trans-enhancement of human immunodeficiency virus type 1 infectivity is independent of DC-SIGN. J Virol 81: 2519-2523.
46. Lambert AA, Gilbert C, Richard M, Beaulieu AD, Tremblay MJ, (2008) The C-type lectin surface receptor DCIR acts as a new attachment factor for HIV-1 in dendritic cells and contributes to trans- and cis-infection pathways. Blood 112: 1299-1307.
47. Magérus-Chatinet A, Yu H, Garcia S, Ducloux E, Terris B, et al. (2007) Galactosyl ceramide expressed on dendritic cells can mediate HIV-1 transfer from monocyte derived dendritic cells to autologous T cells. Virology 362: 67-74.
48. Beltman JB, Marée AF, Lynch JN, Miller MJ, de Boer RJ, (2007) Lymph node topology dictates T cell migration behavior. J Exp Med 204: 771-780.
49. Relloso M, Puig-Kröger A, Pello OM, Rodríguez-Fernández JL, de la Rosa G, et al. (2002) DC-SIGN (CD209) expression is IL-4 dependent and is negatively regulated by IFN, TGF-beta, and anti-inflammatory agents. J Immunol 168: 2634-2643.
50. Engering A, Geijtenbeek TB, van Vliet SJ, Wijers M, van Liempt E, et al. (2002) The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J Immunol 168: 2118-2126.
51. Granelli-Piperno A, Shimeliovich I, Pack M, Trumpfheller C, Steinman RM, (2006) HIV-1 selectively infects a subset of nonmaturing BDCA1-positive dendritic cells in human blood. J Immunol 176: 991-998.
52. Fahrbach KM, Barry SM, Ayehunie S, Lamore S, Klausner M, et al. (2007) Activated CD34-derived Langerhans cells mediate transinfection with human immunodeficiency virus. J Virol 81: 6858-6868.
53. Hatch SC, Archer J, Gummuluru S, (2009) Glycosphingolipid composition of human immunodeficiency virus type 1 (HIV-1) particles is a crucial determinant for dendritic cell-mediated HIV-1 trans-infection. J Virol 83: 3496-3506.
54. Izquierdo-Useros N, Naranjo-Gómez M, Archer J, Hatch SC, Erkizia I, et al. (2009) Capture and transfer of HIV-1 particles by mature dendritic cells converges with the exosome-dissemination pathway. Blood 113: 2732-2741.
55. Booth AM, Fang Y, Fallon JK, Yang JM, Hildreth JE, et al. (2006) Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane. J Cell Biol 172: 923-935.
56. Fang Y, Wu N, Gan X, Yan W, Morrell JC, et al. (2007) Higher-order oligomerization targets plasma membrane proteins and HIV gag to exosomes. PLoS Biol 5: e158.
57. Nguyen DH, Hildreth JE, (2000) Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. J Virol 74: 3264-3272.
58. Izquierdo-Useros N, Lorizate M, Contreras F-X, Rodriguez-Plata MT, Glass B, et al. (2012) Sialyllactose in Viral Membrane Gangliosides Is a Novel Molecular Recognition Pattern for Mature Dendritic Cell Capture of HIV-1. PLoS Biol 10: e1001315.
59. Puryear WB, Yu X, Ramirez NP, Reinhard BM, Gummuluru S, (2012) HIV-1 incorporation of host-cell-derived glycosphingolipid GM3 allows for capture by mature dendritic cells. Proc Natl Acad Sci U S A 109: 7475-7480.
60. Weis W, Brown JH, Cusack S, Paulson JC, Skehel JJ, et al. (1988) Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature 333: 426-431.
61. Merritt EA, Sarfaty S, Akker FVD, L'Hoir C, Martial JA, et al. (1994) Crystal structure of cholera toxin B-pentamer bound to receptor GM1 pentasaccharide. Protein Science 3: 166-175.
62. Markwell MA, Svennerholm L, Paulson JC, (1981) Specific gangliosides function as host cell receptors for Sendai virus. Proc Natl Acad Sci U S A 78: 5406-5410.
63. Tsai B, Gilbert JM, Stehle T, Lencer W, Benjamin TL, et al. (2003) Gangliosides are receptors for murine polyoma virus and SV40. EMBO J 22: 4346-4355.
64. Bergelson LD, Bukrinskaya AG, Prokazova NV, Shaposhnikova GI, Kocharov SL, et al. (1982) Role of gangliosides in reception of influenza virus. Eur J Biochem 128: 467-474.
65. Crocker PR, Paulson JC, Varki A, (2007) Siglecs and their roles in the immune system. Nat Rev Immunol 7: 255-266.
66. Izquierdo-Useros N, Lorizate M, Puertas MC, Rodriguez-Plata MT, Zangger N, et al. (2012) Siglec-1 Is a Novel Dendritic Cell Receptor That Mediates HIV-1 Trans-Infection Through Recognition of Viral Membrane Gangliosides. PLoS Biol 10: e1001448.
67. Puryear WB, Akiyama H, Geer SD, Ramirez NP, Yu X, et al. (2013) Interferon-inducible mechanism of dendritic cell-mediated HIV-1 dissemination is dependent on Siglec-1/CD169. PLoS Pathog 9: e1003291.
68. Zou Z, Chastain A, Moir S, Ford J, Trandem K, et al. (2011) Siglecs facilitate HIV-1 infection of macrophages through adhesion with viral sialic acids. PLoS ONE 6: e24559.
69. Rempel H, Calosing C, Sun B, Pulliam L, (2008) Sialoadhesin expressed on IFN-induced monocytes binds HIV-1 and enhances infectivity. PLoS ONE 3: e1967.
70. Hartnell A, Steel J, Turley H, Jones M, Jackson DG, et al. (2001) Characterization of human sialoadhesin, a sialic acid binding receptor expressed by resident and inflammatory macrophage populations. Blood 97: 288-296.
71. Munday J, Floyd H, Crocker PR, (1999) Sialic acid binding receptors (siglecs) expressed by macrophages. J Leukoc Biol 66: 705-711.
72. Brügger B, Glass B, Haberkant P, Leibrecht I, Wieland FT, et al. (2006) The HIV lipidome: a raft with an unusual composition. Proc Natl Acad Sci U S A 103: 2641-2646.
73. Chan R, Uchil PD, Jin J, Shui G, Ott DE, et al. (2008) Retroviruses human immunodeficiency virus and murine leukemia virus are enriched in phosphoinositides. J Virol 82: 11228-11238.
74. Zhu P, Liu J, Bess J, Chertova E, Lifson JD, et al. (2006) Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 441: 847-852.
75. Kalvodova L, Sampaio JL, Cordo S, Ejsing CS, Shevchenko A, et al. (2009) The lipidomes of vesicular stomatitis virus, semliki forest virus, and the host plasma membrane analyzed by quantitative shotgun mass spectrometry. J Virol 83: 7996-8003.
76. Junt T, Moseman EA, Iannacone M, Massberg S, Lang PA, et al. (2007) Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 450: 110-114.
77. Iannacone M, Moseman EA, Tonti E, Bosurgi L, Junt T, et al. (2010) Subcapsular sinus macrophages prevent CNS invasion on peripheral infection with a neurotropic virus. Nature 465: 1079-1083.
78. Gerl MJ, Sampaio JL, Urban S, Kalvodova L, Verbavatz JM, et al. (2012) Quantitative analysis of the lipidomes of the influenza virus envelope and MDCK cell apical membrane. J Cell Biol 196: 213-221.
79. Rodriguez-Plata MT, Urrutia A, Cardinaud S, Buzón MJ, Izquierdo-Useros N, et al. (2012) HIV-1 Capture and Antigen Presentation by Dendritic Cells: Enhanced Viral Capture Does Not Correlate with Better T Cell Activation. J Immunol 188: 6036-6045.
80. Hajishengallis G, Lambris JD, (2011) Microbial manipulation of receptor crosstalk in innate immunity. Nat Rev Immunol 11: 187-200.
81. Klaas M, Oetke C, Lewis LE, Erwig LP, Heikema AP, et al. (2012) Sialoadhesin promotes rapid proinflammatory and type I IFN responses to a sialylated pathogen, Campylobacter jejuni. J Immunol 189: 2414-2422.
82. Platt CD, Ma JK, Chalouni C, Ebersold M, Bou-Reslan H, et al. (2010) Mature dendritic cells use endocytic receptors to capture and present antigens. Proc Natl Acad Sci U S A 107: 4287-4292.
83. Drutman SB, Trombetta ES, (2010) Dendritic cells continue to capture and present antigens after maturation in vivo. J Immunol 185: 2140-2146.
84. Saunderson SC, Dunn AC, Crocker PR, McLellan AD, (2013) CD169 mediates the capture of exosomes in spleen and lymph node. Blood 123: 208-216.
85. Février B, Raposo G, (2004) Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr Opin Cell Biol 16: 415-421.
86. Théry C, Zitvogel L, Amigorena S, (2002) Exosomes: composition, biogenesis and function. Nat Rev Immunol 2: 569-579.
87. Théry C, Ostrowski M, Segura E, (2009) Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9: 581-593.
88. Théry C, Duban L, Segura E, Véron P, Lantz O, et al. (2002) Indirect activation of naïve CD4+ T cells by dendritic cell-derived exosomes. Nat Immunol 3: 1156-1162.
89. Fontenot D, He H, Hanabuchi S, Nehete PN, Zhang M, et al. (2009) TSLP production by epithelial cells exposed to immunodeficiency virus triggers DC-mediated mucosal infection of CD4+ T cells. Proc Natl Acad Sci U S A 106: 16776-16781.
90. Hladik F, Sakchalathorn P, Ballweber L, Lentz G, Fialkow M, et al. (2007) Initial events in establishing vaginal entry and infection by human immunodeficiency virus type-1. Immunity 26: 257-270.
91. Shattock RJ, Moore JP, (2003) Inhibiting sexual transmission of HIV-1 infection. Nat Rev Microbiol 1: 25-34.
92. Li Q, Estes JD, Schlievert PM, Duan L, Brosnahan AJ, et al. (2009) Glycerol monolaurate prevents mucosal SIV transmission. Nature 458: 1034-1038.
93. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, et al. (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12: 1365-1371.
94. Yonezawa A, Morita R, Takaori-Kondo A, Kadowaki N, Kitawaki T, et al. (2003) Natural alpha interferon-producing cells respond to human immunodeficiency virus type 1 with alpha interferon production and maturation into dendritic cells. J Virol 77: 3777-3784.
95. Jaroenpool J, Rogers KA, Pattanapanyasat K, Villinger F, Onlamoon N, et al. (2007) Differences in the constitutive and SIV infection induced expression of Siglecs by hematopoietic cells from non-human primates. Cellular immunology 250: 91-104.
96. van der Kuyl AC, van den Burg R, Zorgdrager F, Groot F, Berkhout B, Cornelissen M, (2007) Sialoadhesin (CD169) expression in CD14+ cells is upregulated early after HIV-1 infection and increases during disease progression. PLoS ONE 2: e257.
97. Fonteneau JF, Larsson M, Beignon AS, McKenna K, Dasilva I, et al. (2004) Human immunodeficiency virus type 1 activates plasmacytoid dendritic cells and concomitantly induces the bystander maturation of myeloid dendritic cells. J Virol 78: 5223.