The Herpes Virus Fc Receptor gE-gI Mediates Antibody Bipolar Bridging to Clear Viral Antigens from the Cell Surface
Herpes Simplex Virus 1 (HSV-1) infects 40–80% of adults worldwide. HSV-1 initiates infection at mucosal surfaces and spreads along sensory neurons to establish a life-long latent infection that can lead to neurological diseases. Humans usually develop IgG antibodies that specifically recognize pathogens via fragment antigen binding (Fab) variable regions. HSV-1 can avoid the protective effects of antibodies by producing gE-gI, a receptor that binds to the constant portion of IgGs (Fc), thereby tethering the antibody in a position where it cannot trigger downstream immune functions. A gE-gI–bound IgG can participate in antibody bipolar bridging (ABB) such that the Fabs bind a viral antigen and the Fc binds gE-gI. The fate of ABB complexes had been unknown. We used live cell fluorescent imaging to follow ABB complexes during their formation and transport within a cell. We demonstrated that ABB assemblies were internalized into acidic intracellular compartments, where gE-gI dissociated from IgG–viral antigen complexes and the IgG and antigen were targeted for degradation within lysosomes. These results suggest that gE-gI mediates clearance of infected cell surfaces of both anti-viral IgGs and viral antigens, a general mechanism to facilitate latent infection by evading IgG-mediated responses.
Vyšlo v časopise:
The Herpes Virus Fc Receptor gE-gI Mediates Antibody Bipolar Bridging to Clear Viral Antigens from the Cell Surface. PLoS Pathog 10(3): e32767. doi:10.1371/journal.ppat.1003961
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1003961
Souhrn
Herpes Simplex Virus 1 (HSV-1) infects 40–80% of adults worldwide. HSV-1 initiates infection at mucosal surfaces and spreads along sensory neurons to establish a life-long latent infection that can lead to neurological diseases. Humans usually develop IgG antibodies that specifically recognize pathogens via fragment antigen binding (Fab) variable regions. HSV-1 can avoid the protective effects of antibodies by producing gE-gI, a receptor that binds to the constant portion of IgGs (Fc), thereby tethering the antibody in a position where it cannot trigger downstream immune functions. A gE-gI–bound IgG can participate in antibody bipolar bridging (ABB) such that the Fabs bind a viral antigen and the Fc binds gE-gI. The fate of ABB complexes had been unknown. We used live cell fluorescent imaging to follow ABB complexes during their formation and transport within a cell. We demonstrated that ABB assemblies were internalized into acidic intracellular compartments, where gE-gI dissociated from IgG–viral antigen complexes and the IgG and antigen were targeted for degradation within lysosomes. These results suggest that gE-gI mediates clearance of infected cell surfaces of both anti-viral IgGs and viral antigens, a general mechanism to facilitate latent infection by evading IgG-mediated responses.
Zdroje
1. MareschC, GranzowH, NegatschA, KluppBG, FuchsW, et al. (2010) Ultrastructural analysis of virion formation and anterograde intraaxonal transport of the alphaherpesvirus pseudorabies virus in primary neurons. J Virol 84: 5528–5539.
2. GildenDH, MahalingamR, CohrsRJ, TylerKL (2007) Herpesvirus infections of the nervous system. Nat Clin Pract Neurol 3: 82–94.
3. SteinerI (2013) Herpes virus infection of the peripheral nervous system. Handb Clin Neurol 115: 543–558.
4. AntinoneSE, SmithGA (2010) Retrograde axon transport of herpes simplex virus and pseudorabies virus: a live-cell comparative analysis. J Virol 84: 1504–1512.
5. HufnerK, DerfussT, HerbergerS, SunamiK, RussellS, et al. (2006) Latency of alpha-herpes viruses is accompanied by a chronic inflammation in human trigeminal ganglia but not in dorsal root ganglia. J Neuropathol Exp Neurol 65: 1022–1030.
6. CoreyL, SpearPG (1986) Infections with herpes simplex viruses (1). N Engl J Med 314: 686–691.
7. DasguptaG, ChentoufiAA, KalantariM, FalatoonzadehP, ChunS, et al. (2012) Immunodominant “asymptomatic” herpes simplex virus 1 and 2 protein antigens identified by probing whole-ORFome microarrays with serum antibodies from seropositive asymptomatic versus symptomatic individuals. J Virol 86: 4358–4369.
8. JohnsonDC, FeenstraV (1987) Identification of a novel herpes simplex virus type 1-induced glycoprotein which complexes with gE and binds immunoglobulin. J Virol 61: 2208–2216.
9. JohnsonDC, FrameMC, LigasMW, CrossAM, StowND (1988) Herpes simplex virus immunoglobulin G Fc receptor activity depends on a complex of two viral glycoproteins, gE and gI. J Virol 62: 1347–1354.
10. DingwellKS, JohnsonDC (1998) The herpes simplex virus gE-gI complex facilitates cell-to-cell spread and binds to components of cell junctions. J Virol 72: 8933–8942.
11. PolcicovaK, GoldsmithK, RainishBL, WisnerTW, JohnsonDC (2005) The extracellular domain of herpes simplex virus gE is indispensable for efficient cell-to-cell spread: evidence for gE/gI receptors. J Virol 79: 11990–12001.
12. HowardPW, HowardTL, JohnsonDC (2013) Herpes simplex virus membrane proteins gE/gI and US9 act cooperatively to promote transport of capsids and glycoproteins from neuron cell bodies into initial axon segments. J Virol 87: 403–414.
13. ChengSB, FerlandP, WebsterP, BearerEL (2011) Herpes simplex virus dances with amyloid precursor protein while exiting the cell. PLoS One 6: e17966.
14. SnyderA, PolcicovaK, JohnsonDC (2008) Herpes simplex virus gE/gI and US9 proteins promote transport of both capsids and virion glycoproteins in neuronal axons. J Virol 82: 10613–10624.
15. WangF, ZumbrunEE, HuangJ, SiH, MakarounL, et al. (2010) Herpes simplex virus type 2 glycoprotein E is required for efficient virus spread from epithelial cells to neurons and for targeting viral proteins from the neuron cell body into axons. Virology 405: 269–279.
16. FriedmanHM (2003) Immune evasion by herpes simplex virus type 1, strategies for virus survival. Trans Am Clin Climatol Assoc 114: 103–112.
17. GoldwichA, PrechtelAT, Muhl-ZurbesP, PangratzNM, StosselH, et al. (2011) Herpes simplex virus type I (HSV-1) replicates in mature dendritic cells but can only be transferred in a cell-cell contact-dependent manner. J Leukoc Biol 89: 973–979.
18. WisnerT, BrunettiC, DingwellK, JohnsonDC (2000) The extracellular domain of herpes simplex virus gE is sufficient for accumulation at cell junctions but not for cell-to-cell spread. J Virol 74: 2278–2287.
19. MoC, LeeJ, SommerM, GroseC, ArvinAM (2002) The requirement of varicella zoster virus glycoprotein E (gE) for viral replication and effects of glycoprotein I on gE in melanoma cells. Virology 304: 176–186.
20. MaresovaL, PasiekaTJ, HomanE, GerdayE, GroseC (2005) Incorporation of three endocytosed varicella-zoster virus glycoproteins, gE, gH, and gB, into the virion envelope. J Virol 79: 997–1007.
21. OlsonJK, GroseC (1997) Endocytosis and recycling of varicella-zoster virus Fc receptor glycoprotein gE: internalization mediated by a YXXL motif in the cytoplasmic tail. J Virol 71: 4042–4054.
22. OlsonJK, BishopGA, GroseC (1997) Varicella-zoster virus Fc receptor gE glycoprotein: serine/threonine and tyrosine phosphorylation of monomeric and dimeric forms. J Virol 71: 110–119.
23. KenyonTK, CohenJI, GroseC (2002) Phosphorylation by the varicella-zoster virus ORF47 protein serine kinase determines whether endocytosed viral gE traffics to the trans-Golgi network or recycles to the cell membrane. J Virol 76: 10980–10993.
24. ChapmanTL, YouI, JosephIM, BjorkmanPJ, MorrisonSL, et al. (1999) Characterization of the interaction between the herpes simplex virus type I Fc receptor and immunoglobulin G. J Biol Chem 274: 6911–6919.
25. SpragueER, MartinWL, BjorkmanPJ (2004) pH dependence and stoichiometry of binding to the Fc region of IgG by the herpes simplex virus Fc receptor gE-gI. J Biol Chem 279: 14184–14193.
26. BasuS, DubinG, NagashunmugamT, BasuM, GoldsteinLT, et al. (1997) Mapping regions of herpes simplex virus type 1 glycoprotein I required for formation of the viral Fc receptor for monomeric IgG. J Immunol 158: 209–215.
27. FrankI, FriedmanHM (1989) A novel function of the herpes simplex virus type 1 Fc receptor: participation in bipolar bridging of antiviral immunoglobulin G. J Virol 63: 4479–4488.
28. DubinG, SocolofE, FrankI, FriedmanHM (1991) Herpes simplex virus type 1 Fc receptor protects infected cells from antibody-dependent cellular cytotoxicity. J Virol 65: 7046–7050.
29. Van VlietKE, De Graaf-MiltenburgLA, VerhoefJ, Van StrijpJA (1992) Direct evidence for antibody bipolar bridging on herpes simplex virus-infected cells. Immunology 77: 109–115.
30. LubinskiJM, LazearHM, AwasthiS, WangF, FriedmanHM (2011) The herpes simplex virus 1 IgG fc receptor blocks antibody-mediated complement activation and antibody-dependent cellular cytotoxicity in vivo. J Virol 85: 3239–3249.
31. AlconadaA, BauerU, BaudouxL, PietteJ, HoflackB (1998) Intracellular transport of the glycoproteins gE and gI of the varicella-zoster virus. gE accelerates the maturation of gI and determines its accumulation in the trans-Golgi network. J Biol Chem 273: 13430–13436.
32. OlsonJK, GroseC (1998) Complex formation facilitates endocytosis of the varicella-zoster virus gE:gI Fc receptor. J Virol 72: 1542–1551.
33. ZhangJ, NagelCH, SodeikB, LippéR (2009) Early, active, and specific localization of herpes simplex virus type 1 gM to nuclear membranes. J Virol 83: 12984–12997.
34. CrumpCM, BruunB, BellS, PomeranzLE, MinsonT, et al. (2004) Alphaherpesvirus glycoprotein M causes the relocalization of plasma membrane proteins. J Gen Virol 85: 3517–3527.
35. FriedmanHM, YeeA, DiggelmannH, HastingsJC, Tal-SingerR, et al. (1989) Use of a glucocorticoid-inducible promoter for expression of herpes simplex virus type 1 glycoprotein gC1, a cytotoxic protein in mammalian cells. Mol Cell Biol 9: 2303–2314.
36. TikooSK, FitzpatrickDR, BabiukLA, ZambTJ (1990) Molecular cloning, sequencing, and expression of functional bovine herpesvirus 1 glycoprotein gIV in transfected bovine cells. J Virol 64: 5132–5142.
37. LitwinV, JacksonW, GroseC (1992) Receptor properties of two varicella-zoster virus glycoproteins, gpI and gpIV, homologous to herpes simplex virus gE and gI. J Virol 66: 3643–3651.
38. RyanMD, DrewJ (1994) Foot-and-mouth disease virus 2A oligopeptide mediated cleavage of an artificial polyprotein. EMBO J 13: 928–933.
39. LuoXM, LeiMY, FeidiRA, WestAP, BalazsAB, et al. (2010) Dimeric 2G12 as a potent protection against HIV-1. PLoS Pathog 6: e1001225.
40. GaoSY, JackMM, O'NeillC (2012) Towards optimising the production of and expression from polycistronic vectors in embryonic stem cells. PLoS One 7: e48668.
41. EdsonCM, HoslerBA, WatersDJ (1987) Varicella-zoster virus gpI and herpes simplex virus gE: phosphorylation and Fc binding. Virology 161: 599–602.
42. NorrildB, VirtanenI, LehtoVP, PedersenB (1983) Accumulation of herpes simplex virus type 1 glycoprotein D in adhesion areas of infected cells. J Gen Virol 64(Pt 11): 2499–2503.
43. SnyderA, BruunB, BrowneHM, JohnsonDC (2007) A herpes simplex virus gD-YFP fusion glycoprotein is transported separately from viral capsids in neuronal axons. J Virol 81: 8337–8340.
44. ReskeA, PollaraG, KrummenacherC, ChainBM, KatzDR (2007) Understanding HSV-1 entry glycoproteins. Rev Med Virol 17: 205–215.
45. BrideauAD, EnquistLW, TirabassiRS (2000) The role of virion membrane protein endocytosis in the herpesvirus life cycle. J Clin Virol 17: 69–82.
46. JohanssonPJ, MyhreEB, BlombergJ (1985) Specificity of Fc receptors induced by herpes simplex virus type 1: comparison of immunoglobulin G from different animal species. J Virol 56: 489–494.
47. BurioniR, WilliamsonRA, SannaPP, BloomFE, BurtonDR (1994) Recombinant human Fab to glycoprotein D neutralizes infectivity and prevents cell-to-cell transmission of herpes simplex viruses 1 and 2 in vitro. Proc Natl Acad Sci U S A 91: 355–359.
48. MayfieldSP, FranklinSE, LernerRA (2003) Expression and assembly of a fully active antibody in algae. Proc Natl Acad Sci U S A 100: 438–442.
49. HaiglerHT, McKannaJA, CohenS (1979) Direct visualization of the binding and internalization of a ferritin conjugate of epidermal growth factor in human carcinoma cells A-431. J Cell Biol 81: 382–395.
50. FutterCE, PearseA, HewlettLJ, HopkinsCR (1996) Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J Cell Biol 132: 1011–1023.
51. ClagueMJ, UrbéS (2001) The interface of receptor trafficking and signalling. J Cell Sci 114: 3075–3081.
52. HaglundK, Di FiorePP, DikicI (2003) Distinct monoubiquitin signals in receptor endocytosis. Trends Biochem Sci 28: 598–603.
53. LiuD, MeckelT, LongEO (2010) Distinct role of rab27a in granule movement at the plasma membrane and in the cytosol of NK cells. PLoS One 5: e12870.
54. LeeJH, YuWH, KumarA, LeeS, MohanPS, et al. (2010) Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 141: 1146–1158.
55. Enns CA (2002) The transferrin receptor. In Molecular and Cellular Iron Transport (Templeton, DM, ed.), pp. 71–94. Marcel and Dekker Inc., New York, NY.; Templeton D, editor. New York, NY.: Marcel and Dekker Inc. 77–94 p.
56. BaliPK, ZakO, AisenP (1991) A new role for the transferrin receptor in the release of iron from transferrin. Biochemistry 30: 324–328.
57. SipeDM, MurphyRF (1991) Binding to cellular receptors results in increased iron release from transferrin at mildly acidic pH. J Biol Chem 266: 8002–8007.
58. ZakO, AisenP (2003) Iron release from transferrin, its C-lobe, and their complexes with transferrin receptor: presence of N-lobe accelerates release from C-lobe at endosomal pH. Biochemistry 42: 12330–12334.
59. YoungSP, BomfordA (1994) Iterative endocytosis of transferrin by K562 cells. Biochem J 298(Pt 1): 165–170.
60. FavoreelHW, NauwynckHJ, Van OostveldtP, MettenleiterTC, PensaertMB (1997) Antibody-induced and cytoskeleton-mediated redistribution and shedding of viral glycoproteins, expressed on pseudorabies virus-infected cells. J Virol 71: 8254–8261.
61. RizviSM, RaghavanM (2003) Responses of herpes simplex virus type 1-infected cells to the presence of extracellular antibodies: gE-dependent glycoprotein capping and enhancement in cell-to-cell spread. J Virol 77: 701–708.
62. FarnsworthA, JohnsonDC (2006) Herpes simplex virus gE/gI must accumulate in the trans-Golgi network at early times and then redistribute to cell junctions to promote cell-cell spread. J Virol 80: 3167–3179.
63. AlconadaA, BauerU, SodeikB, HoflackB (1999) Intracellular traffic of herpes simplex virus glycoprotein gE: characterization of the sorting signals required for its trans-Golgi network localization. J Virol 73: 377–387.
64. ThomasG (2002) Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat Rev Mol Cell Biol 3: 753–766.
65. SzymczakAL, WorkmanCJ, WangY, VignaliKM, DilioglouS, et al. (2004) Correction of multi-gene deficiency in vivo using a single ‘self-cleaving’ 2A peptide-based retroviral vector. Nat Biotechnol 22: 589–594.
66. SzymczakAL, VignaliDA (2005) Development of 2A peptide-based strategies in the design of multicistronic vectors. Expert Opin Biol Ther 5: 627–638.
67. BarsovEV, TrivettMT, MinangJT, SunH, OhlenC, et al. (2011) Transduction of SIV-specific TCR genes into rhesus macaque CD8+ T cells conveys the ability to suppress SIV replication. PLoS One 6: e23703.
68. DonnellyML, HughesLE, LukeG, MendozaH, ten DamE, et al. (2001) The ‘cleavage’ activities of foot-and-mouth disease virus 2A site-directed mutants and naturally occurring ‘2A-like’ sequences. J Gen Virol 82: 1027–1041.
69. HolstJ, Szymczak-WorkmanAL, VignaliKM, BurtonAR, WorkmanCJ, et al. (2006) Generation of T-cell receptor retrogenic mice. Nat Protoc 1: 406–417.
70. TamuraM, TamuraN, IkedaT, KoyamaR, IkegayaY, et al. (2009) Influence of brain-derived neurotrophic factor on pathfinding of dentate granule cell axons, the hippocampal mossy fibers. Mol Brain 2: 2.
71. TrkolaA, PomalesAB, YuanH, KorberB, MaddonPJ, et al. (1995) Cross-clade neutralization of primary isolates of human immunodeficiency virus type 1 by human monoclonal antibodies and tetrameric CD4-IgG. J Virol 69: 6609–6617.
72. TrkolaA, PurtscherM, MusterT, BallaunC, BuchacherA, et al. (1996) Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J Virol 70: 1100–1108.
73. WestAPJr, GalimidiRP, FoglesongCP, GnanapragasamPN, Huey-TubmanKE, et al. (2009) Design and expression of a dimeric form of human immunodeficiency virus type 1 antibody 2G12 with increased neutralization potency. J Virol 83: 98–104.
74. YaoF, SvensjoT, WinklerT, LuM, ErikssonC, et al. (1998) Tetracycline repressor, tetR, rather than the tetR-mammalian cell transcription factor fusion derivatives, regulates inducible gene expression in mammalian cells. Hum Gene Ther 9: 1939–1950.
75. MullickA, XuY, WarrenR, KoutroumanisM, GuilbaultC, et al. (2006) The cumate gene-switch: a system for regulated expression in mammalian cells. BMC Biotechnol 6: 43.
76. CostesSV, DaelemansD, ChoEH, DobbinZ, PavlakisG, et al. (2004) Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J 86: 3993–4003.
77. SpragueER, WangC, BakerD, BjorkmanPJ (2006) Crystal structure of the HSV-1 Fc receptor bound to Fc reveals a mechanism for antibody bipolar bridging. PLoS Biol 4: e148.
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Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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