A Cytosolic Chaperone Complexes with Dynamic Membrane J-Proteins and Mobilizes a Nonenveloped Virus out of the Endoplasmic Reticulum
The nonenveloped simian virus 40 (SV40) is a model member of the Polyomaviridae family of viruses containing several related species that cause diseases in immunocompromised individuals. As with other nonenveloped viruses, the membrane penetration step during SV40 entry is mechanistically obscure. Productive SV40 infection requires trafficking of the viral particle to the endoplasmic reticulum (ER) from where it penetrates the ER membrane to reach the cytosol; further transport of the virus into the nucleus causes infection. How SV40 crosses the ER membrane is an enigmatic step. Here, we identify a cytosolic chaperone protein that physically engages SV40 and facilitates virus ER-to-cytosol transport. This factor called SGTA is hijacked specifically at the site of membrane penetration due to its recruitment by ER membrane proteins B14 and B12 previously implicated in supporting virus infection. Additionally, we observe that B14 and B12 reorganize during SV40 entry into discrete foci on the ER membrane. These virus-induced structures likely represent exit sites for the viral particles and could serve to transiently recruit high concentrations of SGTA to complete membrane penetration. Our data reveal that a cytosolic chaperone can play a direct role in membrane penetration of a nonenveloped virus.
Vyšlo v časopise:
A Cytosolic Chaperone Complexes with Dynamic Membrane J-Proteins and Mobilizes a Nonenveloped Virus out of the Endoplasmic Reticulum. PLoS Pathog 10(3): e32767. doi:10.1371/journal.ppat.1004007
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004007
Souhrn
The nonenveloped simian virus 40 (SV40) is a model member of the Polyomaviridae family of viruses containing several related species that cause diseases in immunocompromised individuals. As with other nonenveloped viruses, the membrane penetration step during SV40 entry is mechanistically obscure. Productive SV40 infection requires trafficking of the viral particle to the endoplasmic reticulum (ER) from where it penetrates the ER membrane to reach the cytosol; further transport of the virus into the nucleus causes infection. How SV40 crosses the ER membrane is an enigmatic step. Here, we identify a cytosolic chaperone protein that physically engages SV40 and facilitates virus ER-to-cytosol transport. This factor called SGTA is hijacked specifically at the site of membrane penetration due to its recruitment by ER membrane proteins B14 and B12 previously implicated in supporting virus infection. Additionally, we observe that B14 and B12 reorganize during SV40 entry into discrete foci on the ER membrane. These virus-induced structures likely represent exit sites for the viral particles and could serve to transiently recruit high concentrations of SGTA to complete membrane penetration. Our data reveal that a cytosolic chaperone can play a direct role in membrane penetration of a nonenveloped virus.
Zdroje
1. MercerJ, SchelhaasM, HeleniusA (2010) Virus entry by endocytosis. Annu Rev Biochem 79: 803–833.
2. TsaiB (2007) Penetration of nonenveloped viruses into the cytoplasm. Annu Rev Cell Dev Biol 23: 23–43.
3. WiethoffCM, WodrichH, GeraceL, NemerowGR (2005) Adenovirus protein VI mediates membrane disruption following capsid disassembly. J Virol 79: 1992–2000.
4. BaerGS, DermodyTS (1997) Mutations in reovirus outer-capsid protein sigma3 selected during persistent infections of L cells confer resistance to protease inhibitor E64. J Virol 71: 4921–4928.
5. FarrGA, ZhangLG, TattersallP (2005) Parvoviral virions deploy a capsid-tethered lipolytic enzyme to breach the endosomal membrane during cell entry. Proc Natl Acad Sci U S A 102: 17148–17153.
6. ChandranK, FarsettaDL, NibertML (2002) Strategy for nonenveloped virus entry: a hydrophobic conformer of the reovirus membrane penetration protein micro 1 mediates membrane disruption. J Virol 76: 9920–9933.
7. EngelS, HegerT, ManciniR, HerzogF, KartenbeckJ, et al. (2011) Role of endosomes in simian virus 40 entry and infection. J Virol 85: 4198–4211.
8. KartenbeckJ, StukenbrokH, HeleniusA (1989) Endocytosis of simian virus 40 into the endoplasmic reticulum. J Cell Biol 109: 2721–2729.
9. NorkinLC, AndersonHA, WolfromSA, OppenheimA (2002) Caveolar endocytosis of simian virus 40 is followed by brefeldin A-sensitive transport to the endoplasmic reticulum, where the virus disassembles. J Virol 76: 5156–5166.
10. NelsonCD, DerdowskiA, MaginnisMS, O'HaraBA, AtwoodWJ (2012) The VP1 subunit of JC polyomavirus recapitulates early events in viral trafficking and is a novel tool to study polyomavirus entry. Virology 428: 30–40.
11. JiangM, AbendJR, TsaiB, ImperialeMJ (2009) Early events during BK virus entry and disassembly. J Virol 83: 1350–1358.
12. QianM, CaiD, VerheyKJ, TsaiB (2009) A lipid receptor sorts polyomavirus from the endolysosome to the endoplasmic reticulum to cause infection. PLoS Pathog 5: e1000465.
13. RichardsAA, StangE, PepperkokR, PartonRG (2002) Inhibitors of COP-mediated transport and cholera toxin action inhibit simian virus 40 infection. Mol Biol Cell 13: 1750–1764.
14. DeCaprioJA, GarceaRL (2013) A cornucopia of human polyomaviruses. Nat Rev Microbiol 11: 264–276.
15. JiangM, AbendJR, JohnsonSF, ImperialeMJ (2009) The role of polyomaviruses in human disease. Virology 384: 266–273.
16. TsaiB, GilbertJM, StehleT, LencerW, BenjaminTL, et al. (2003) Gangliosides are receptors for murine polyoma virus and SV40. EMBO J 22: 4346–4355.
17. Ewers H, Romer W, Smith AE, Bacia K, Dmitrieff S, et al.. (2010) GM1 structure determines SV40-induced membrane invagination and infection. Nat Cell Biol 12: : 11–18; sup pp 11–12.
18. NakanishiA, CleverJ, YamadaM, LiPP, KasamatsuH (1996) Association with capsid proteins promotes nuclear targeting of simian virus 40 DNA. Proc Natl Acad Sci U S A 93: 96–100.
19. NakanishiA, ShumD, MoriokaH, OtsukaE, KasamatsuH (2002) Interaction of the Vp3 nuclear localization signal with the importin alpha 2/beta heterodimer directs nuclear entry of infecting simian virus 40. J Virol 76: 9368–9377.
20. ChenXS, StehleT, HarrisonSC (1998) Interaction of polyomavirus internal protein VP2 with the major capsid protein VP1 and implications for participation of VP2 in viral entry. EMBO J 17: 3233–3240.
21. StehleT, GamblinSJ, YanY, HarrisonSC (1996) The structure of simian virus 40 refined at 3.1 A resolution. Structure 4: 165–182.
22. LiddingtonRC, YanY, MoulaiJ, SahliR, BenjaminTL, et al. (1991) Structure of simian virus 40 at 3.8-A resolution. Nature 354: 278–284.
23. SchelhaasM, MalmstromJ, PelkmansL, HaugstetterJ, EllgaardL, et al. (2007) Simian Virus 40 depends on ER protein folding and quality control factors for entry into host cells. Cell 131: 516–529.
24. MagnusonB, RaineyEK, BenjaminT, BaryshevM, MkrtchianS, et al. (2005) ERp29 triggers a conformational change in polyomavirus to stimulate membrane binding. Mol Cell 20: 289–300.
25. WalczakCP, TsaiB (2011) A PDI family network acts distinctly and coordinately with ERp29 to facilitate polyomavirus infection. J Virol 85: 2386–2396.
26. GilbertJ, OuW, SilverJ, BenjaminT (2006) Downregulation of protein disulfide isomerase inhibits infection by the mouse polyomavirus. J Virol 80: 10868–10870.
27. Rainey-BargerEK, MagnusonB, TsaiB (2007) A chaperone-activated nonenveloped virus perforates the physiologically relevant endoplasmic reticulum membrane. J Virol 81: 12996–13004.
28. KuksinD, NorkinLC (2012) Disassembly of simian virus 40 during passage through the endoplasmic reticulum and in the cytoplasm. J Virol 86: 1555–1562.
29. GeigerR, AndritschkeD, FriebeS, HerzogF, LuisoniS, et al. (2011) BAP31 and BiP are essential for dislocation of SV40 from the endoplasmic reticulum to the cytosol. Nat Cell Biol 13: 1305–1314.
30. DanielsR, RusanNM, WadsworthP, HebertDN (2006) SV40 VP2 and VP3 insertion into ER membranes is controlled by the capsid protein VP1: implications for DNA translocation out of the ER. Mol Cell 24: 955–966.
31. Olzmann JA, Kopito RR, Christianson JC (2012) The Mammalian Endoplasmic Reticulum-Associated Degradation System. Cold Spring Harb Perspect Biol 5: pii: a013185.
32. HirschC, GaussR, HornSC, NeuberO, SommerT (2009) The ubiquitylation machinery of the endoplasmic reticulum. Nature 458: 453–460.
33. GoodwinEC, LipovskyA, InoueT, MagaldiTG, EdwardsAP, et al. (2011) BiP and Multiple DNAJ Molecular Chaperones in the Endoplasmic Reticulum Are Required for Efficient Simian Virus 40 Infection. MBio 2: e00101–11.
34. BennettSM, JiangM, ImperialeMJ (2013) Role of cell-type-specific endoplasmic reticulum-associated degradation in polyomavirus trafficking. J Virol 87: 8843–8852.
35. LilleyBN, GilbertJM, PloeghHL, BenjaminTL (2006) Murine polyomavirus requires the endoplasmic reticulum protein Derlin-2 to initiate infection. J Virol 80: 8739–8744.
36. GroveDE, FanCY, RenHY, CyrDM (2011) The endoplasmic reticulum-associated Hsp40 DNAJB12 and Hsc70 cooperate to facilitate RMA1 E3-dependent degradation of nascent CFTRDeltaF508. Mol Biol Cell 22: 301–314.
37. SophaP, KadokuraH, YamamotoYH, TakeuchiM, SaitoM, et al. (2012) A novel mammalian ER-located J-protein, DNAJB14, can accelerate ERAD of misfolded membrane proteins. Cell Struct Funct 37: 177–187.
38. YamamotoYH, KimuraT, MomoharaS, TakeuchiM, TaniT, et al. (2010) A novel ER J-protein DNAJB12 accelerates ER-associated degradation of membrane proteins including CFTR. Cell Struct Funct 35: 107–116.
39. KampingaHH, CraigEA (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 11: 579–592.
40. InoueT, TsaiB (2011) A large and intact viral particle penetrates the endoplasmic reticulum membrane to reach the cytosol. PLoS Pathog 7: e1002037.
41. YeY, MeyerHH, RapoportTA (2001) The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414: 652–656.
42. XuY, CaiM, YangY, HuangL, YeY (2012) SGTA recognizes a noncanonical ubiquitin-like domain in the Bag6-Ubl4A-Trc35 complex to promote endoplasmic reticulum-associated degradation. Cell Rep 2: 1633–1644.
43. AngelettiPC, WalkerD, PanganibanAT (2002) Small glutamine-rich protein/viral protein U-binding protein is a novel cochaperone that affects heat shock protein 70 activity. Cell Stress Chaperones 7: 258–268.
44. TobabenS, ThakurP, Fernandez-ChaconR, SudhofTC, RettigJ, et al. (2001) A trimeric protein complex functions as a synaptic chaperone machine. Neuron 31: 987–999.
45. LeznickiP, HighS (2012) SGTA antagonizes BAG6-mediated protein triage. Proc Natl Acad Sci U S A 109: 19214–19219.
46. WangQ, LiuY, SoetandyoN, BaekK, HegdeR, et al. (2011) A ubiquitin ligase-associated chaperone holdase maintains polypeptides in soluble states for proteasome degradation. Mol Cell 42: 758–770.
47. DiacumakosEG, GersheyEL (1977) Uncoating and gene expression of simian virus 40 in CV-1 cell nuclei inoculated by microinjection. J Virol 24: 903–906.
48. BernardiKM, ForsterML, LencerWI, TsaiB (2008) Derlin-1 facilitates the retro-translocation of cholera toxin. Mol Biol Cell 19: 877–884.
49. WilliamsJM, InoueT, BanksL, TsaiB (2013) The ERdj5-Sel1L complex facilitates cholera toxin retrotranslocation. Mol Biol Cell 24: 785–795.
50. ForsterML, SivickK, ParkYN, ArvanP, LencerWI, et al. (2006) Protein disulfide isomerase-like proteins play opposing roles during retrotranslocation. J Cell Biol 173: 853–859.
51. PelkmansL, KartenbeckJ, HeleniusA (2001) Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 3: 473–483.
52. YeY, ShibataY, KikkertM, van VoordenS, WiertzE, et al. (2005) Recruitment of the p97 ATPase and ubiquitin ligases to the site of retrotranslocation at the endoplasmic reticulum membrane. Proc Natl Acad Sci U S A 102: 14132–14138.
53. ChristiansonJC, OlzmannJA, ShalerTA, SowaME, BennettEJ, et al. (2012) Defining human ERAD networks through an integrative mapping strategy. Nat Cell Biol 14: 93–105.
54. LiPP, ItohN, WatanabeM, ShiY, LiuP, et al. (2009) Association of simian virus 40 vp1 with 70-kilodalton heat shock proteins and viral tumor antigens. J Virol 83: 37–46.
55. ChromyLR, OltmanA, EstesPA, GarceaRL (2006) Chaperone-mediated in vitro disassembly of polyoma- and papillomaviruses. J Virol 80: 5086–5091.
56. WangB, Heath-EngelH, ZhangD, NguyenN, ThomasDY, et al. (2008) BAP31 interacts with Sec61 translocons and promotes retrotranslocation of CFTRDeltaF508 via the derlin-1 complex. Cell 133: 1080–1092.
57. CarvalhoP, StanleyAM, RapoportTA (2010) Retrotranslocation of a misfolded luminal ER protein by the ubiquitin-ligase Hrd1p. Cell 143: 579–591.
58. SuhWC, LuCZ, GrossCA (1999) Structural features required for the interaction of the Hsp70 molecular chaperone DnaK with its cochaperone DnaJ. J Biol Chem 274: 30534–30539.
59. AhmadA, BhattacharyaA, McDonaldRA, CordesM, EllingtonB, et al. (2011) Heat shock protein 70 kDa chaperone/DnaJ cochaperone complex employs an unusual dynamic interface. Proc Natl Acad Sci U S A 108: 18966–18971.
60. MillerS, Krijnse-LockerJ (2008) Modification of intracellular membrane structures for virus replication. Nat Rev Microbiol 6: 363–374.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2014 Číslo 3
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Cytomegalovirus m154 Hinders CD48 Cell-Surface Expression and Promotes Viral Escape from Host Natural Killer Cell Control
- Human African Trypanosomiasis and Immunological Memory: Effect on Phenotypic Lymphocyte Profiles and Humoral Immunity
- Conflicting Interests in the Pathogen–Host Tug of War: Fungal Micronutrient Scavenging Versus Mammalian Nutritional Immunity
- DHX36 Enhances RIG-I Signaling by Facilitating PKR-Mediated Antiviral Stress Granule Formation