Retromer Regulates HIV-1 Envelope Glycoprotein Trafficking and Incorporation into Virions

English version České info

Virus assembly necessitates the hijacking of the host cell machinery in order for new infectious viral particles to be constructed and disseminate. The envelope glycoprotein (Env) of HIV is a critical determinant of viral infectivity and is also a major target for antiviral immune responses. The long cytoplasmic tail of HIV Env plays an essential role in the assembly of infectious virions and limiting exposure of Env to the immune system, but the cellular machinery that transports HIV Env in virus-infected cells remain poorly understood. Here we have identified the mammalian retromer complex involved in endosomal sorting as a novel cellular factor regulating Env trafficking in virus-infected cells. We show that inactivating retromer alters Env localization, cell surface expression and incorporation into virions and that retromer binds directly to the Env cytoplasmic tail to perform these functions. This study defines an important pathway of Env transport and describes for the first time a role for this highly conserved cellular complex in assembly of a virus.

Vyšlo v časopise: Retromer Regulates HIV-1 Envelope Glycoprotein Trafficking and Incorporation into Virions. PLoS Pathog 10(11): e32767. doi:10.1371/journal.ppat.1004518
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004518

Souhrn

Zdroje

1. CheckleyMA, LuttgeBG, FreedEO (2011) HIV-1 envelope glycoprotein biosynthesis, trafficking, and incorporation. J Mol Biol 410: 582–608.

2. OwensRJ, DubayJW, HunterE, CompansRW (1991) Human immunodeficiency virus envelope protein determines the site of virus release in polarized epithelial cells. Proc Natl Acad Sci U S A 88: 3987–3991.

3. LodgeR, GottlingerH, GabuzdaD, CohenEA, LemayG (1994) The intracytoplasmic domain of gp41 mediates polarized budding of human immunodeficiency virus type 1 in MDCK cells. J Virol 68: 4857–4861.

4. BoschML, EarlPL, FargnoliK, PicciafuocoS, GiombiniF, et al. (1989) Identification of the fusion peptide of primate immunodeficiency viruses. Science 244: 694–697.

5. HallenbergerS, BoschV, AnglikerH, ShawE, KlenkHD, et al. (1992) Inhibition of furin-mediated cleavage activation of HIV-1 glycoprotein gp160. Nature 360: 358–361.

6. PostlerTS, DesrosiersRC (2013) The tale of the long tail: the cytoplasmic domain of HIV-1 gp41. J J Virol 87: 2–15.

7. MurakamiT, FreedEO (2000) The long cytoplasmic tail of gp41 is required in a cell type-dependent manner for HIV-1 envelope glycoprotein incorporation into virions. Proc Natl Acad Sci U S A 97: 343–348.

8. AkariH, FukumoriT, AdachiA (2000) Cell-dependent requirement of human immunodeficiency virus type 1 gp41 cytoplasmic tail for Env incorporation into virions. J Virol 74: 4891–4893.

9. EganMA, CarruthLM, RowellJF, YuX, SilicianoRF (1996) Human immunodeficiency virus type 1 envelope protein endocytosis mediated by a highly conserved intrinsic internalization signal in the cytoplasmic domain of gp41 is suppressed in the presence of the Pr55gag precursor protein. J Virol 70: 6547–6556.

10. Berlioz-TorrentC, ShacklettBL, ErdtmannL, DelamarreL, BouchaertI, et al. (1999) Interactions of the cytoplasmic domains of human and simian retroviral transmembrane proteins with components of the clathrin adaptor complexes modulate intracellular and cell surface expression of envelope glycoproteins. J Virol 73: 1350–1361.

11. BogeM, WyssS, BonifacinoJS, ThaliM (1998) A membrane-proximal tyrosine-based signal mediates internalization of the HIV-1 envelope glycoprotein via interaction with the AP-2 clathrin adaptor. J Biol Chem 273: 15773–15778.

12. WyssS, Berlioz-TorrentC, BogeM, BlotG, HoningS, et al. (2001) The highly conserved C-terminal dileucine motif in the cytosolic domain of the human immunodeficiency virus type 1 envelope glycoprotein is critical for its association with the AP-1 clathrin adaptor [correction of adapter]. J Virol 75: 2982–2992.

13. BylandR, VancePJ, HoxieJA, MarshM (2007) A conserved dileucine motif mediates clathrin and AP-2-dependent endocytosis of the HIV-1 envelope protein. Mol Biol Cell 18: 414–425.

14. SeamanMN, McCafferyJM, EmrSD (1998) A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J Cell Biol 142: 665–681.

15. EdgarAJ, PolakJM (2000) Human homologues of yeast vacuolar protein sorting 29 and 35. Biochem Biophys Res Comm 277: 622–630.

16. HaftCR, de la Luz SierraM, BaffordR, LesniakMA, BarrVA, et al. (2000) Human orthologs of yeast vacuolar protein sorting proteins Vps26, 29, and 35: assembly into multimeric complexes. Mol Biol Cell 11: 4105–4116.

17. ArighiCN, HartnellLM, AguilarRC, HaftCR, BonifacinoJS (2004) Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J Cell Biol 165: 123–133.

18. SeamanMN (2004) Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J Cell Biol 165: 111–122.

19. SeamanMN (2012) The retromer complex - endosomal protein recycling and beyond. J Cell Sci 125: 4693–4702.

20. BonifacinoJS, HurleyJH (2008) Retromer. Curr Opin Cell Biol 20: 427–436.

21. TemkinP, LaufferB, JagerS, CimermancicP, KroganNJ, et al. (2011) SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signalling receptors. Nat Cell Biol 13: 715–721.

22. ChoyRW, ParkM, TemkinP, HerringBE, MarleyA, et al. (2014) Retromer mediates a discrete route of local membrane delivery to dendrites. Neuron 82: 55–62.

23. CullenPJ, KorswagenHC (2012) Sorting nexins provide diversity for retromer-dependent trafficking events. Nat Cell Biol 14: 29–37.

24. BelenkayaTY, WuY, TangX, ZhouB, ChengL, et al. (2008) The retromer complex influences Wnt secretion by recycling wntless from endosomes to the trans-Golgi network. Dev Cell 14: 120–131.

25. SeamanMN (2007) Identification of a novel conserved sorting motif required for retromer-mediated endosome-to-TGN retrieval. J Cell Sci 120: 2378–2389.

26. TabuchiM, YanatoriI, KawaiY, KishiF (2010) Retromer-mediated direct sorting is required for proper endosomal recycling of the mammalian iron transporter DMT1. J Cell Sci 123: 756–766.

27. ShiH, RojasR, BonifacinoJS, HurleyJH (2006) The retromer subunit Vps26 has an arrestin fold and binds Vps35 through its C-terminal domain. Nat Struct Mol Biol 13: 540–548.

28. FjorbackAW, SeamanM, GustafsenC, MehmedbasicA, GokoolS, et al. (2012) Retromer binds the FANSHY sorting motif in SorLA to regulate amyloid precursor protein sorting and processing. J Neuro 32: 1467–1480.

29. CanuelM, LefrancoisS, ZengJ, MoralesCR (2008) AP-1 and retromer play opposite roles in the trafficking of sortilin between the Golgi apparatus and the lysosomes. Biochem Biophys Res Comm 366: 724–730.

30. PochaSM, WassmerT, NiehageC, HoflackB, KnustE (2011) Retromer controls epithelial cell polarity by trafficking the apical determinant Crumbs. Curr Biol 21: 1111–1117.

31. ZhouB, WuY, LinX (2011) Retromer regulates apical-basal polarity through recycling Crumbs. Dev Biol 360: 87–95.

32. NielsenMS, GustafsenC, MadsenP, NyengaardJR, HermeyG, et al. (2007) Sorting by the cytoplasmic domain of the amyloid precursor protein binding receptor SorLA. Mol Cell Biol 27: 6842–6851.

33. HarbourME, BreusegemSY, AntrobusR, FreemanC, ReidE, et al. (2010) The cargo-selective retromer complex is a recruiting hub for protein complexes that regulate endosomal tubule dynamics. J Cell Sci 123: 3703–3717.

34. NothwehrSF, HaSA, BruinsmaP (2000) Sorting of yeast membrane proteins into an endosome-to-Golgi pathway involves direct interaction of their cytosolic domains with Vps35p. J Cell Biol 151: 297–310.

35. RojasR, van VlijmenT, MardonesGA, PrabhuY, RojasAL, et al. (2008) Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J Cell Biol 183: 513–526.

36. FreedEO, MartinMA (1995) Virion incorporation of envelope glycoproteins with long but not short cytoplasmic tails is blocked by specific, single amino acid substitutions in the human immunodeficiency virus type 1 matrix. J Virol 69: 1984–1989.

37. FreedEO, MartinMA (1996) Domains of the human immunodeficiency virus type 1 matrix and gp41 cytoplasmic tail required for envelope incorporation into virions. J Virol 70: 341–351.

38. BlotG, JanvierK, Le PanseS, BenarousR, Berlioz-TorrentC (2003) Targeting of the human immunodeficiency virus type 1 envelope to the trans-Golgi network through binding to TIP47 is required for env incorporation into virions and infectivity. J Virol 77: 6931–6945.

39. BultmannA, MuranyiW, SeedB, HaasJ (2001) Identification of two sequences in the cytoplasmic tail of the human immunodeficiency virus type 1 envelope glycoprotein that inhibit cell surface expression. J Virol 75: 5263–5276.

40. JiangJ, AikenC (2007) Maturation-dependent human immunodeficiency virus type 1 particle fusion requires a carboxyl-terminal region of the gp41 cytoplasmic tail. J Virol 81: 9999–10008.

41. MurrayJL, MavrakisM, McDonaldNJ, YillaM, ShengJ, et al. (2005) Rab9 GTPase is required for replication of human immunodeficiency virus type 1, filoviruses, and measles virus. J Virol 79: 11742–11751.

42. Lopez-VergesS, CamusG, BlotG, BeauvoirR, BenarousR, et al. (2006) Tail-interacting protein TIP47 is a connector between Gag and Env and is required for Env incorporation into HIV-1 virions. Proc Natl Acad Sci U S A 103: 14947–14952.

43. CheckleyMA, LuttgeBG, MercrediPY, KyereSK, DonlanJ, et al. (2013) Reevaluation of the Requirement for Tip47 in Human Immunodeficiency Virus Type 1 Envelope Glycoprotein Incorporation. J J Virol 87: 3561–3570.

44. BulankinaAV, DeggerichA, WenzelD, MutendaK, WittmannJG, et al. (2009) TIP47 functions in the biogenesis of lipid droplets. J Cell Biol 185: 641–655.

45. DiazE, PfefferSR (1998) TIP47: a cargo selection device for mannose 6-phosphate receptor trafficking. Cell 93: 433–443.

46. BowersK, Pelchen-MatthewsA, HoningS, VancePJ, CrearyL, et al. (2000) The simian immunodeficiency virus envelope glycoprotein contains multiple signals that regulate its cell surface expression and endocytosis. Traffic 1: 661–674.

47. OhnoH, AguilarRC, FournierMC, HenneckeS, CossonP, et al. (1997) Interaction of endocytic signals from the HIV-1 envelope glycoprotein complex with members of the adaptor medium chain family. Virology 238: 305–315.

48. FultzPN, VancePJ, EndresMJ, TaoB, DvorinJD, et al. (2001) In vivo attenuation of simian immunodeficiency virus by disruption of a tyrosine-dependent sorting signal in the envelope glycoprotein cytoplasmic tail. J Virol 75: 278–291.

49. KueckT, NeilSJ (2012) A cytoplasmic tail determinant in HIV-1 Vpu mediates targeting of tetherin for endosomal degradation and counteracts interferon-induced restriction. PloS Pathog 8: e1002609.

50. QiM, WilliamsJA, ChuH, ChenX, WangJJ, et al. (2013) Rab11-FIP1C and Rab14 direct plasma membrane sorting and particle incorporation of the HIV-1 envelope glycoprotein complex. PloS Pathog 9: e1003278.

51. ChertovaE, ChertovO, CorenLV, RoserJD, TrubeyCM, et al. (2006) Proteomic and biochemical analysis of purified human immunodeficiency virus type 1 produced from infected monocyte-derived macrophages. J Virol 80: 9039–9052.

52. BugarcicA, ZheY, KerrMC, GriffinJ, CollinsBM, et al. (2011) Vps26A and Vps26B subunits define distinct retromer complexes. Traffic 12: 1759–1773.

53. KimE, LeeY, LeeHJ, KimJS, SongBS, et al. (2010) Implication of mouse Vps26b-Vps29-Vps35 retromer complex in sortilin trafficking. Biochem Biophys Res Comm 403: 167–171.

54. KerrMC, BennettsJS, SimpsonF, ThomasEC, FleggC, et al. (2005) A novel mammalian retromer component, Vps26B. Traffic 6: 991–1001.

55. KleinJS, BjorkmanPJ (2010) Few and far between: how HIV may be evading antibody avidity. PloS Pathog 6: e1000908.

56. LipovskyA, PopaA, PimientaG, WylerM, BhanA, et al. (2013) Genome-wide siRNA screen identifies the retromer as a cellular entry factor for human papillomavirus. Proc Natl Acad Sci U S A 110: 7452–7457.

57. WilkT, PfeifferT, BoschV (1992) Retained in vitro infectivity and cytopathogenicity of HIV-1 despite truncation of the C-terminal tail of the env gene product. Virology 189: 167–177.

58. JingSQ, SpencerT, MillerK, HopkinsC, TrowbridgeIS (1990) Role of the human transferrin receptor cytoplasmic domain in endocytosis: localization of a specific signal sequence for internalization. J Cell Biol 110: 283–294.

59. SchallerT, OcwiejaKE, RasaiyaahJ, PriceAJ, BradyTL, et al. (2011) HIV-1 capsid-cyclophilin interactions determine nuclear import pathway, integration targeting and replication efficiency. PloS Pathog 7: e1002439.

60. JollyC, SattentauQJ (2007) Human immunodeficiency virus type 1 assembly, budding, and cell-cell spread in T cells take place in tetraspanin-enriched plasma membrane domains. J Virol 81: 7873–7884.