Interaction with Tsg101 Is Necessary for the Efficient Transport and Release of Nucleocapsids in Marburg Virus-Infected Cells

English version České info

Marburg virus (MARV) is endemic in central Africa and causes hemorrhagic fever in humans and non-human primates, with high lethality. Presumably, the disease severity primarily depends on the response of host-cell factors interacting with viral proteins. We generated a recombinant MARV encoding an NP with a mutated PSAP late domain motif, which has previously been shown to mediate interaction with the cellular ESCRT protein Tsg101. We found that the PSAP-mediated interaction with Tsg101 was important at several steps of MARV assembly before viral fission. First, the egress of mature rMARVPSAPmut nucleocapsids from viral inclusions was inhibited. Second, actin-driven transport of rMARVPSAPmut nucleocapsids was impaired, displaying significantly shortened trajectories and reduced movement in the cell periphery. Third, rMARVPSAPmut nucleocapsids accumulated in cell periphery, and the number of filopodia-associated nucleocapsids decreased, indicating that rMARVPSAPmut nucleocapsids were defective to enter filopodia, the major budding sites of MARV. These defects resulted in the attenuated growth of rMARVPSAPmut. Interestingly, IQGAP1, an actin cytoskeleton regulator which interacts with Tsg101, was also recruited to nucleocapsids in dependence of the PSAP late domain. Thus, the interaction of NP with Tsg101 not only impacts viral budding at the plasma membrane but also nucleocapsid transport through the cytoplasm.

Vyšlo v časopise: Interaction with Tsg101 Is Necessary for the Efficient Transport and Release of Nucleocapsids in Marburg Virus-Infected Cells. PLoS Pathog 10(10): e32767. doi:10.1371/journal.ppat.1004463
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004463

Souhrn

Zdroje

1. SlagsvoldT, PattniK, MalerodL, StenmarkH (2006) Endosomal and non-endosomal functions of ESCRT proteins. Trends Cell Biol 16 : 317–326.

2. BieniaszPD (2006) Late budding domains and host proteins in enveloped virus release. Virology 344 : 55–63.

3. CarltonJG, Martin-SerranoJ (2009) The ESCRT machinery: new functions in viral and cellular biology. Biochem Soc Trans 37 : 195–199.

4. ChenBJ, LambRA (2008) Mechanisms for enveloped virus budding: can some viruses do without an ESCRT? Virology 372 : 221–232.

5. VottelerJ, SundquistWI (2013) Virus budding and the ESCRT pathway. Cell Host Microbe 14 : 232–241.

6. WelschS, MullerB, KrausslichHG (2007) More than one door -⁠ Budding of enveloped viruses through cellular membranes. FEBS Lett 581 : 2089–2097.

7. HorganCP, HanscomSR, KellyEE, McCaffreyMW (2012) Tumor susceptibility gene 101 (TSG101) is a novel binding-partner for the class II Rab11-FIPs. PLoS One 7: e32030.

8. MoritaE, SandrinV, ChungHY, MorhamSG, GygiSP, et al. (2007) Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J 26 : 4215–4227.

9. TuC, Ortega-CavaCF, WinogradP, StantonMJ, ReddiAL, et al. (2010) Endosomal-sorting complexes required for transport (ESCRT) pathway-dependent endosomal traffic regulates the localization of active Src at focal adhesions. Proc Natl Acad Sci U S A 107 : 16107–16112.

10. AmitI, YakirL, KatzM, ZwangY, MarmorMD, et al. (2004) Tal, a Tsg101-specific E3 ubiquitin ligase, regulates receptor endocytosis and retrovirus budding. Genes Dev 18 : 1737–1752.

11. FengGH, LihCJ, CohenSN (2000) TSG101 protein steady-state level is regulated posttranslationally by an evolutionarily conserved COOH-terminal sequence. Cancer Res 60 : 1736–1741.

12. JiaoJ, SunK, WalkerWP, BagherP, CotaCD, et al. (2009) Abnormal regulation of TSG101 in mice with spongiform neurodegeneration. Biochim Biophys Acta 1792 : 1027–1035.

13. KimBY, OlzmannJA, BarshGS, ChinLS, LiL (2007) Spongiform neurodegeneration-associated E3 ligase Mahogunin ubiquitylates TSG101 and regulates endosomal trafficking. Mol Biol Cell 18 : 1129–1142.

14. McDonaldB, Martin-SerranoJ (2008) Regulation of Tsg101 expression by the steadiness box: a role of Tsg101-associated ligase. Mol Biol Cell 19 : 754–763.

15. MalerodL, PedersenNM, Sem WegnerCE, LobertVH, LeitheE, et al. (2011) Cargo-dependent degradation of ESCRT-I as a feedback mechanism to modulate endosomal sorting. Traffic 12 : 1211–1226.

16. Sanchez A GT, Feldmann H (2007) Filoviridae: Marburg and Ebola viruses. In: Knipe DM HP, editor. Fields Virology. Philadelphia: Lippincott Williams and Williams. pp. 1409–1448.

17. BradfuteSB, DyeJMJr, BavariS (2011) Filovirus vaccines. Hum Vaccin 7 : 701–711.

18. BharatTA, RichesJD, KolesnikovaL, WelschS, KrahlingV, et al. (2011) Cryo-electron tomography of Marburg virus particles and their morphogenesis within infected cells. PLoS Biol 9: e1001196.

19. MühlbergerE, LotferingB, KlenkHD, BeckerS (1998) Three of the four nucleocapsid proteins of Marburg virus, NP, VP35, and L, are sufficient to mediate replication and transcription of Marburg virus-specific monocistronic minigenomes. J Virol 72 : 8756–8764.

20. FeldmannH, VolchkovVE, VolchkovaVA, StroherU, KlenkHD (2001) Biosynthesis and role of filoviral glycoproteins. J Gen Virol 82 : 2839–2848.

21. GeisbertTW, JahrlingPB (1995) Differentiation of filoviruses by electron microscopy. Virus Res 39 : 129–150.

22. KolesnikovaL, MuhlbergerE, RyabchikovaE, BeckerS (2000) Ultrastructural organization of recombinant Marburg virus nucleoprotein: comparison with Marburg virus inclusions. J Virol 74 : 3899–3904.

23. HoenenT, ShabmanRS, GrosethA, HerwigA, WeberM, et al. (2012) Inclusion bodies are a site of ebolavirus replication. J Virol 86 : 11779–11788.

24. DolnikO, KolesnikovaL, BeckerS (2008) Filoviruses: Interactions with the host cell. Cell Mol Life Sci 65 : 756–776.

25. KolesnikovaL, BerghoferB, BambergS, BeckerS (2004) Multivesicular bodies as a platform for formation of the Marburg virus envelope. J Virol 78 : 12277–12287.

26. SchudtG, KolesnikovaL, DolnikO, SodeikB, BeckerS (2013) Live-cell imaging of Marburg virus-infected cells uncovers actin-dependent transport of nucleocapsids over long distances. Proc Natl Acad Sci U S A 110 : 14402–14407.

27. KolesnikovaL, BohilAB, CheneyRE, BeckerS (2007) Budding of Marburgvirus is associated with filopodia. Cell Microbiol 9 : 939–951.

28. WelschS, KolesnikovaL, KrahlingV, RichesJD, BeckerS, et al. (2010) Electron tomography reveals the steps in filovirus budding. PLoS Pathog 6: e1000875.

29. KolesnikovaL, StreckerT, MoritaE, ZieleckiF, MittlerE, et al. (2009) Vacuolar protein sorting pathway contributes to the release of Marburg virus. J Virol 83 : 2327–2337.

30. UrataS, NodaT, KawaokaY, MorikawaS, YokosawaH, et al. (2007) Interaction of Tsg101 with Marburg virus VP40 depends on the PPPY motif, but not the PT/SAP motif as in the case of Ebola virus, and Tsg101 plays a critical role in the budding of Marburg virus-like particles induced by VP40, NP, and GP. J Virol 81 : 4895–4899.

31. DolnikO, KolesnikovaL, StevermannL, BeckerS (2010) Tsg101 is recruited by a late domain of the nucleocapsid protein to support budding of Marburg virus-like particles. J Virol 84 : 7847–7856.

32. MorrisCR, StantonMJ, MantheyKC, OhKB, WagnerKU (2012) A knockout of the Tsg101 gene leads to decreased expression of ErbB receptor tyrosine kinases and induction of autophagy prior to cell death. PLoS One 7: e34308.

33. MittlerE, KolesnikovaL, HerwigA, DolnikO, BeckerS (2013) Assembly of the Marburg virus envelope. Cell Microbiol 15 : 270–284.

34. BeckerS, RinneC, HofsassU, KlenkHD, MühlbergerE (1998) Interactions of Marburg virus nucleocapsid proteins. Virology 249 : 406–417.

35. RemyI, GalarneauA, MichnickSW (2002) Detection and visualization of protein interactions with protein fragment complementation assays. Methods Mol Biol 185 : 447–459.

36. MacDonaldML, LamerdinJ, OwensS, KeonBH, BilterGK, et al. (2006) Identifying off-target effects and hidden phenotypes of drugs in human cells. Nat Chem Biol 2 : 329–337.

37. DussuptV, JavidMP, Abou-JaoudeG, JadwinJA, de La CruzJ, et al. (2009) The nucleocapsid region of HIV-1 Gag cooperates with the PTAP and LYPXnL late domains to recruit the cellular machinery necessary for viral budding. PLoS Pathog 5: e1000339.

38. GottlingerHG, DorfmanT, SodroskiJG, HaseltineWA (1991) Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release. Proc Natl Acad Sci U S A 88 : 3195–3199.

39. JayakarHR, MurtiKG, WhittMA (2000) Mutations in the PPPY motif of vesicular stomatitis virus matrix protein reduce virus budding by inhibiting a late step in virion release. J Virol 74 : 9818–9827.

40. ObiangL, RauxH, OuldaliM, BlondelD, GaudinY (2011) Phenotypes of vesicular stomatitis virus mutants with mutations in the PSAP motif of the matrix protein. J Gen Virol

41. WirblichC, TanGS, PapaneriA, GodlewskiPJ, OrensteinJM, et al. (2008) PPEY motif within the rabies virus (RV) matrix protein is essential for efficient virion release and RV pathogenicity. J Virol 82 : 9730–9738.

42. KolesnikovaL, MittlerE, SchudtG, Shams-EldinH, BeckerS (2012) Phosphorylation of Marburg virus matrix protein VP40 triggers assembly of nucleocapsids with the viral envelope at the plasma membrane. Cell Microbiol 14 : 182–197.

43. AggarwalA, IemmaTL, ShihI, NewsomeTP, McAlleryS, et al. (2012) Mobilization of HIV spread by diaphanous 2 dependent filopodia in infected dendritic cells. PLoS Pathog 8: e1002762.

44. LehmannMJ, ShererNM, MarksCB, PypaertM, MothesW (2005) Actin -⁠ and myosin-driven movement of viruses along filopodia precedes their entry into cells. J Cell Biol 170 : 317–325.

45. ShererNM, LehmannMJ, Jimenez-SotoLF, HorensavitzC, PypaertM, et al. (2007) Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nat Cell Biol 9 : 310–315.

46. BrandtDT, GrosseR (2007) Get to grips: steering local actin dynamics with IQGAPs. EMBO Rep 8 : 1019–1023.

47. Pelikan-ConchaudronA, Le ClaincheC, DidryD, CarlierMF (2011) The IQGAP1 protein is a calmodulin-regulated barbed end capper of actin filaments: possible implications in its function in cell migration. J Biol Chem 286 : 35119–35128.

48. GladueDP, HolinkaLG, Fernandez-SainzIJ, PraratMV, O'DonnellV, et al. (2011) Interaction between Core protein of classical swine fever virus with cellular IQGAP1 protein appears essential for virulence in swine. Virology 412 : 68–74.

49. LeungJ, YuehA, AppahFSJr, YuanB, de los SantosK, et al. (2006) Interaction of Moloney murine leukemia virus matrix protein with IQGAP. EMBO J 25 : 2155–2166.

50. LuJ, QuY, LiuY, JambusariaR, HanZ, et al. (2013) Host IQGAP1 and Ebola virus VP40 interactions facilitate virus-like particle egress. J Virol 87 : 7777–7780.

51. LiuY, LeeMS, OlsonMA, HartyRN (2011) Bimolecular Complementation to Visualize Filovirus VP40-Host Complexes in Live Mammalian Cells: Toward the Identification of Budding Inhibitors. Adv Virol 2011.

52. RenX, HurleyJH (2011) Proline-rich regions and motifs in trafficking: from ESCRT interaction to viral exploitation. Traffic 12 : 1282–1290.

53. UrataS, YasudaJ Regulation of Marburg virus (MARV) budding by Nedd4.1: a different WW domain of Nedd4.1 is critical for binding to MARV and Ebola virus VP40. J Gen Virol 91 : 228–234.

54. RauchS, Martin-SerranoJ (2011) Multiple interactions between the ESCRT machinery and arrestin-related proteins: implications for PPXY-dependent budding. J Virol 85 : 3546–3556.

55. DemirovDG, OnoA, OrensteinJM, FreedEO (2002) Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function. Proc Natl Acad Sci U S A 99 : 955–960.

56. ImYJ, KuoL, RenX, BurgosPV, ZhaoXZ, et al. (2010) Crystallographic and functional analysis of the ESCRT-I/HIV-1 Gag PTAP interaction. Structure 18 : 1536–1547.

57. DaveyNE, TraveG, GibsonTJ (2011) How viruses hijack cell regulation. Trends Biochem Sci 36 : 159–169.

58. MateerSC, McDanielAE, NicolasV, HabermacherGM, LinMJ, et al. (2002) The mechanism for regulation of the F-actin binding activity of IQGAP1 by calcium/calmodulin. J Biol Chem 277 : 12324–12333.

59. NabhanJF, HuR, OhRS, CohenSN, LuQ (2012) Formation and release of arrestin domain-containing protein 1-mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein. Proc Natl Acad Sci U S A 109 : 4146–4151.

60. KrahlingV, DolnikO, KolesnikovaL, Schmidt-ChanasitJ, JordanI, et al. (2010) Establishment of fruit bat cells (Rousettus aegyptiacus) as a model system for the investigation of filoviral infection. PLoS Negl Trop Dis 4: e802.

61. Hierholzer JC, and R. A. Killington (1996) Virus isolation and quantitation; Kangro BWMaHO, editor. London, United Kingdom: Academic Press Limited 36–38 p.

62. KolesnikovaL, BambergS, BerghoferB, BeckerS (2004) The matrix protein of Marburg virus is transported to the plasma membrane along cellular membranes: exploiting the retrograde late endosomal pathway. J Virol 78 : 2382–2393.

63. MastronardeDN (2005) Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol 152 : 36–51.

64. KremerJR, MastronardeDN, McIntoshJR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116 : 71–76.

65. WeibelER, KistlerGS, ScherleWF (1966) Practical stereological methods for morphometric cytology. J Cell Biol 30 : 23–38.