CD169-Mediated Trafficking of HIV to Plasma Membrane Invaginations in Dendritic Cells Attenuates Efficacy of Anti-gp120 Broadly Neutralizing Antibodies
Dendritic cells (DCs) are professional antigen presenting cells, and their sentinel roles are important to elicit a potent antiviral immunity. However, HIV-1 has exploited DCs to spread infection by several mechanisms. One such mechanism is the DC-mediated trans-infection pathway, whereby DCs transmit captured virus to CD4+ T cells. We have recently identified the type I interferon (IFN-I) inducible protein, CD169, as a receptor on DCs which mediates HIV-1 capture and trans-infection. We have also demonstrated extensive co-localization of HIV-1 with CD169 within peripheral non-lysosomal compartments in DCs, although the mechanism and biological importance of the compartment formation remain unclear. Here in this study, we report that a myeloid cell specific co-factor interacts with CD169 following virus capture leading to compartment formation. This co-factor is induced in DCs by an IFN-I-inducing TLR ligand LPS, but not by IFN-I itself. Though the CD169+ HIV-1 containing compartments are surface-accessible, these compartments have considerable depth and are connected to the surface, such that captured virus particles localized within these unique structures are protected from detection by anti-gp120 broadly neutralizing antibodies. Our study suggests that CD169–HIV-1 interaction provides an evasion mechanism from degradation by phagocytosis and neutralization by anti-viral humoral responses.
Vyšlo v časopise:
CD169-Mediated Trafficking of HIV to Plasma Membrane Invaginations in Dendritic Cells Attenuates Efficacy of Anti-gp120 Broadly Neutralizing Antibodies. PLoS Pathog 11(3): e32767. doi:10.1371/journal.ppat.1004751
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004751
Souhrn
Dendritic cells (DCs) are professional antigen presenting cells, and their sentinel roles are important to elicit a potent antiviral immunity. However, HIV-1 has exploited DCs to spread infection by several mechanisms. One such mechanism is the DC-mediated trans-infection pathway, whereby DCs transmit captured virus to CD4+ T cells. We have recently identified the type I interferon (IFN-I) inducible protein, CD169, as a receptor on DCs which mediates HIV-1 capture and trans-infection. We have also demonstrated extensive co-localization of HIV-1 with CD169 within peripheral non-lysosomal compartments in DCs, although the mechanism and biological importance of the compartment formation remain unclear. Here in this study, we report that a myeloid cell specific co-factor interacts with CD169 following virus capture leading to compartment formation. This co-factor is induced in DCs by an IFN-I-inducing TLR ligand LPS, but not by IFN-I itself. Though the CD169+ HIV-1 containing compartments are surface-accessible, these compartments have considerable depth and are connected to the surface, such that captured virus particles localized within these unique structures are protected from detection by anti-gp120 broadly neutralizing antibodies. Our study suggests that CD169–HIV-1 interaction provides an evasion mechanism from degradation by phagocytosis and neutralization by anti-viral humoral responses.
Zdroje
1. Banchereau J, Steinman RM (1998) Dendritic cells and the control of immunity. Nature 392: 245–252. 9521319
2. Hladik F, McElrath MJ (2008) Setting the stage: host invasion by HIV. Nat Rev Immunol 8: 447–457. doi: 10.1038/nri2302 18469831
3. Wu L, KewalRamani VN (2006) Dendritic-cell interactions with HIV: infection and viral dissemination. Nat Rev Immunol 6: 859–868. 17063186
4. Aggarwal A, Iemma TL, Shih I, Newsome TP, McAllery S, et al. (2012) Mobilization of HIV spread by diaphanous 2 dependent filopodia in infected dendritic cells. PLoS Pathog 8: e1002762. doi: 10.1371/journal.ppat.1002762 22685410
5. 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. 7500050
6. 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. 14630806
7. 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. 1352913
8. Hladik F, Lentz G, Akridge RE, Peterson G, Kelley H, et al. (1999) Dendritic cell-T-cell interactions support coreceptor-independent human immunodeficiency virus type 1 transmission in the human genital tract. J Virol 73: 5833–5842. 10364335
9. 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. doi: 10.1038/nature09337 20829794
10. Lee B, Sharron M, Montaner LJ, Weissman D, Doms RW (1999) Quantification of CD4, CCR5, and CXCR4 levels on lymphocyte subsets, dendritic cells, and differentially conditioned monocyte-derived macrophages. Proc Natl Acad Sci U S A 96: 5215–5220. 10220446
11. Luban J (2012) Innate immune sensing of HIV-1 by dendritic cells. Cell Host Microbe 12: 408–418. doi: 10.1016/j.chom.2012.10.002 23084911
12. 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. 12730499
13. 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. doi: 10.1371/journal.pbio.1001448 23271952
14. 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. doi: 10.1371/journal.ppat.1003291 23593001
15. 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. 11133773
16. 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. 15882445
17. Izquierdo-Useros N, Blanco J, Erkizia I, Fernandez-Figueras MT, Borras FE, et al. (2007) Maturation of blood-derived dendritic cells enhances human immunodeficiency virus type 1 capture and transmission. J Virol 81: 7559–7570. 17475656
18. Cavrois M, Neidleman J, Greene WC (2008) The achilles heel of the trojan horse model of HIV-1 trans-infection. PLoS Pathog 4: e1000051. doi: 10.1371/journal.ppat.1000051 18584030
19. 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. 17567699
20. Frank I, Piatak M Jr., Stoessel H, Romani N, Bonnyay D, et al. (2002) 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 76: 2936–2951. 11861860
21. 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. 11825572
22. Cavrois M, Neidleman J, Kreisberg JF, Greene WC (2007) In vitro derived dendritic cells trans-infect CD4 T cells primarily with surface-bound HIV-1 virions. PLoS Pathog 3: e4. 17238285
23. 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. doi: 10.1371/journal.ppat.1000134 18725936
24. Izquierdo-Useros N, Naranjo-Gomez M, Archer J, Hatch SC, Erkizia I, et al. (2008) Capture and transfer of HIV-1 particles by mature dendritic cells converges with the exosome-dissemination pathway. Blood.
25. Felts RL, Narayan K, Estes JD, Shi D, Trubey CM, et al. (2010) 3D visualization of HIV transfer at the virological synapse between dendritic cells and T cells. Proc Natl Acad Sci U S A 107: 13336–13341. doi: 10.1073/pnas.1003040107 20624966
26. Delputte PL, Van Gorp H, Favoreel HW, Hoebeke I, Delrue I, et al. (2011) Porcine sialoadhesin (CD169/Siglec-1) is an endocytic receptor that allows targeted delivery of toxins and antigens to macrophages. PLoS One 6: e16827. doi: 10.1371/journal.pone.0016827 21359217
27. Yao Q, Compans RW (1995) Differences in the role of the cytoplasmic domain of human parainfluenza virus fusion proteins. J Virol 69: 7045–7053. 7474124
28. Waning DL, Schmitt AP, Leser GP, Lamb RA (2002) Roles for the cytoplasmic tails of the fusion and hemagglutinin-neuraminidase proteins in budding of the paramyxovirus simian virus 5. J Virol 76: 9284–9297. 12186912
29. Wiley RD, Gummuluru S (2006) Immature dendritic cell-derived exosomes can mediate HIV-1 trans infection. Proc Natl Acad Sci U S A 103: 738–743. 16407131
30. Martinez-Pomares L (2012) The mannose receptor. J Leukoc Biol 92: 1177–1186. doi: 10.1189/jlb.0512231 22966131
31. Schweizer A, Stahl PD, Rohrer J (2000) A di-aromatic motif in the cytosolic tail of the mannose receptor mediates endosomal sorting. J Biol Chem 275: 29694–29700. 10896932
32. Sriram U, Biswas C, Behrens EM, Dinnall JA, Shivers DK, et al. (2007) IL-4 suppresses dendritic cell response to type I interferons. J Immunol 179: 6446–6455. 17982033
33. Cella M, Salio M, Sakakibara Y, Langen H, Julkunen I, et al. (1999) Maturation, activation, and protection of dendritic cells induced by double-stranded RNA. J Exp Med 189: 821–829. 10049946
34. Blanchet FP, Stalder R, Czubala M, Lehmann M, Rio L, et al. (2013) TLR-4 engagement of dendritic cells confers a BST-2/tetherin-mediated restriction of HIV-1 infection to CD4+ T cells across the virological synapse. Retrovirology 10: 6. doi: 10.1186/1742-4690-10-6 23311681
35. Badieirostami M, Lew MD, Thompson MA, Moerner WE (2010) Three-dimensional localization precision of the double-helix point spread function versus astigmatism and biplane. Appl Phys Lett 97: 161103. 21079725
36. Juette MF, Gould TJ, Lessard MD, Mlodzianoski MJ, Nagpure BS, et al. (2008) Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples. Nat Methods 5: 527–529. doi: 10.1038/nmeth.1211 18469823
37. Mlodzianoski MJ, Juette MF, Beane GL, Bewersdorf J (2009) Experimental characterization of 3D localization techniques for particle-tracking and super-resolution microscopy. Opt Express 17: 8264–8277. 19434159
38. Izquierdo-Useros N, Lorizate M, Contreras FX, 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. doi: 10.1371/journal.pbio.1001315 22545022
39. 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. doi: 10.1073/pnas.1201104109 22529395
40. Stacey AR, Norris PJ, Qin L, Haygreen EA, Taylor E, et al. (2009) Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections. J Virol 83: 3719–3733. doi: 10.1128/JVI.01844-08 19176632
41. Krutzik SR, Tan B, Li H, Ochoa MT, Liu PT, et al. (2005) TLR activation triggers the rapid differentiation of monocytes into macrophages and dendritic cells. Nat Med 11: 653–660. 15880118
42. Naik SH, Metcalf D, van Nieuwenhuijze A, Wicks I, Wu L, et al. (2006) Intrasplenic steady-state dendritic cell precursors that are distinct from monocytes. Nat Immunol 7: 663–671. 16680143
43. Randolph GJ, Beaulieu S, Lebecque S, Steinman RM, Muller WA (1998) Differentiation of monocytes into dendritic cells in a model of transendothelial trafficking. Science 282: 480–483. 9774276
44. 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. 17115046
45. Balazs AB, Chen J, Hong CM, Rao DS, Yang L, et al. (2012) Antibody-based protection against HIV infection by vectored immunoprophylaxis. Nature 481: 81–84. doi: 10.1038/nature10660 22139420
46. Johnson PR, Schnepp BC, Zhang J, Connell MJ, Greene SM, et al. (2009) Vector-mediated gene transfer engenders long-lived neutralizing activity and protection against SIV infection in monkeys. Nat Med 15: 901–906. doi: 10.1038/nm.1967 19448633
47. Crocker PR, Paulson JC, Varki A (2007) Siglecs and their roles in the immune system. Nat Rev Immunol 7: 255–266. 17380156
48. 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. 14610207
49. Akiyama H, Miller C, Patel HV, Hatch SC, Archer J, et al. (2014) Virus Particle Release from Glycosphingolipid-Enriched Microdomains Is Essential for Dendritic Cell-Mediated Capture and Transfer of HIV-1 and Henipavirus. J Virol 88: 8813–8825. doi: 10.1128/JVI.00992-14 24872578
50. Moris A, Nobile C, Buseyne F, Porrot F, Abastado JP, et al. (2004) DC-SIGN promotes exogenous MHC-I-restricted HIV-1 antigen presentation. Blood 103: 2648–2654. 14576049
51. Yamashita M, Emerman M (2004) Capsid is a dominant determinant of retrovirus infectivity in nondividing cells. J Virol 78: 5670–5678. 15140964
52. Sagar M, Akiyama H, Etemad B, Ramirez N, Freitas I, et al. (2012) Transmembrane domain membrane proximal external region but not surface unit-directed broadly neutralizing HIV-1 antibodies can restrict dendritic cell-mediated HIV-1 trans-infection. J Infect Dis 205: 1248–1257. doi: 10.1093/infdis/jis183 22396600
53. Vodicka MA, Goh WC, Wu LI, Rogel ME, Bartz SR, et al. (1997) Indicator cell lines for detection of primary strains of human and simian immunodeficiency viruses. Virology 233: 193–198. 9201229
54. 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. doi: 10.1128/JVI.02249-08 19193785
55. Mlodzianoski MJ, Schreiner JM, Callahan SP, Smolkova K, Dlaskova A, et al. (2011) Sample drift correction in 3D fluorescence photoactivation localization microscopy. Opt Express 19: 15009–15019. doi: 10.1364/OE.19.015009 21934862
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Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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