Home LiteratureArticle Details
PMID: 28614383 Published · epublish English Journal Article

Regulated Erlin-dependent release of the B12 transmembrane J-protein promotes ER membrane penetration of a non-enveloped virus.

PLoS pathogens ·Vol. 13 ·No. 6 ·2017-06-00 ·Pages e1006439

Inoue T, Tsai B

Abstract

The molecular mechanism by which non-enveloped viruses penetrate biological membranes remains enigmatic. The non-enveloped polyomavirus SV40 penetrates the endoplasmic reticulum (ER) membrane to reach the cytosol and cause infection. We previously demonstrated that SV40 creates its own membrane penetration structure by mobilizing select transmembrane proteins to distinct puncta in the ER membrane called foci that likely function as the cytosol entry sites. How these ER membrane proteins reorganize into the foci is unknown. B12 is a transmembrane J-protein that mobilizes into the foci to promote cytosol entry of SV40. Here we identify two closely related ER membrane proteins Erlin1 and Erlin2 (Erlin1/2) as B12-interaction partners. Strikingly, SV40 recruits B12 to the foci by inducing release of this J-protein from Erlin1/2. Our data thus reveal how a non-enveloped virus promotes its own membrane translocation by triggering the release and recruitment of a critical transport factor to the membrane penetration site.

MeSH Terms
Cell Line Endoplasmic Reticulum/virology Gene Knockdown Techniques Humans Intracellular Membranes/metabolism,virology Membrane Proteins/metabolism Nerve Tissue Proteins/metabolism Polyomavirus Infections/metabolism Simian virus 40/physiology Virus Internalization
Chemicals
ERLIN1 protein, human ERLIN2 protein, human Membrane Proteins Nerve Tissue Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Inoue Takamasa ORCID
Department of Cell and Developmental Biology, University of Michigan Medical School, Ann Arbor, MI, United States of America.
Tsai Billy ORCID
Department of Cell and Developmental Biology, University of Michigan Medical School, Ann Arbor, MI, United States of America.
References (42)
42 references, click to expand
  1. Expression of DNAJB12 or DNAJB14 causes coordinate invasion of the nucleus by membranes associated with a novel nuclear pore structure.
    PLoS One. 2014 Apr 14;9(4):e94322 PMID: 24732912
  2. BiP and multiple DNAJ molecular chaperones in the endoplasmic reticulum are required for efficient simian virus 40 infection.
    MBio. 2011 Jun 14;2(3):e00101-11 PMID: 21673190
  3. EMC1-dependent stabilization drives membrane penetration of a partially destabilized non-enveloped virus.
    Elife. 2016 Dec 24;5:null PMID: 28012275
  4. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER.
    Nat Cell Biol. 2001 May;3(5):473-83 PMID: 11331875
  5. GM1 structure determines SV40-induced membrane invagination and infection.
    Nat Cell Biol. 2010 Jan;12(1):11-8; sup pp 1-12 PMID: 20023649
  6. SPFH2 mediates the endoplasmic reticulum-associated degradation of inositol 1,4,5-trisphosphate receptors and other substrates in mammalian cells.
    J Biol Chem. 2007 Jul 13;282(28):20104-15 PMID: 17502376
  7. The endoplasmic reticulum membrane J protein C18 executes a distinct role in promoting simian virus 40 membrane penetration.
    J Virol. 2015 Apr;89(8):4058-68 PMID: 25631089
  8. Attenuated protein expression vectors for use in siRNA rescue experiments.
    Biotechniques. 2012 Aug;0(0):1-5 PMID: 22877307
  9. Virus and Host Mechanics Support Membrane Penetration and Cell Entry.
    J Virol. 2016 Mar 28;90(8):3802-5 PMID: 26842477
  10. How viruses and toxins disassemble to enter host cells.
    Annu Rev Microbiol. 2011;65:287-305 PMID: 21682643
  11. BAP31 and BiP are essential for dislocation of SV40 from the endoplasmic reticulum to the cytosol.
    Nat Cell Biol. 2011 Sep 25;13(11):1305-14 PMID: 21947079
  12. Clonal integration of a polyomavirus in human Merkel cell carcinoma.
    Science. 2008 Feb 22;319(5866):1096-100 PMID: 18202256
  13. Distinct regions within the erlins are required for oligomerization and association with high molecular weight complexes.
    J Biol Chem. 2009 Mar 20;284(12):7766-76 PMID: 19131330
  14. A lipid receptor sorts polyomavirus from the endolysosome to the endoplasmic reticulum to cause infection.
    PLoS Pathog. 2009 Jun;5(6):e1000465 PMID: 19503604
  15. Erlins restrict SREBP activation in the ER and regulate cellular cholesterol homeostasis.
    J Cell Biol. 2013 Nov 11;203(3):427-36 PMID: 24217618
  16. The HSP70 chaperone machinery: J proteins as drivers of functional specificity.
    Nat Rev Mol Cell Biol. 2010 Aug;11(8):579-92 PMID: 20651708
  17. The role of polyomaviruses in human disease.
    Virology. 2009 Feb 20;384(2):266-73 PMID: 18995875
  18. Retrotranslocation of a misfolded luminal ER protein by the ubiquitin-ligase Hrd1p.
    Cell. 2010 Nov 12;143(4):579-91 PMID: 21074049
  19. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor.
    Cell. 2001 Dec 28;107(7):881-91 PMID: 11779464
  20. Membrane-associated ubiquitin ligase complex containing gp78 mediates sterol-accelerated degradation of 3-hydroxy-3-methylglutaryl-coenzyme A reductase.
    J Biol Chem. 2011 Apr 29;286(17 ):15022-31 PMID: 21343306
  21. An endoplasmic reticulum (ER) membrane complex composed of SPFH1 and SPFH2 mediates the ER-associated degradation of inositol 1,4,5-trisphosphate receptors.
    J Biol Chem. 2009 Apr 17;284(16):10433-45 PMID: 19240031
  22. SPFH1 and SPFH2 mediate the ubiquitination and degradation of inositol 1,4,5-trisphosphate receptors in muscarinic receptor-expressing HeLa cells.
    Biochim Biophys Acta. 2009 Nov;1793(11):1710-8 PMID: 19751772
  23. Structure of simian virus 40 at 3.8-A resolution.
    Nature. 1991 Nov 28;354(6351):278-84 PMID: 1659663
  24. The mammalian endoplasmic reticulum-associated degradation system.
    Cold Spring Harb Perspect Biol. 2013 Sep 01;5(9):null PMID: 23232094
  25. A Non-enveloped Virus Hijacks Host Disaggregation Machinery to Translocate across the Endoplasmic Reticulum Membrane.
    PLoS Pathog. 2015 Aug 05;11(8):e1005086 PMID: 26244546
  26. Penetration of nonenveloped viruses into the cytoplasm.
    Annu Rev Cell Dev Biol. 2007;23:23-43 PMID: 17456018
  27. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor.
    Cell. 1997 May 2;89(3):331-40 PMID: 9150132
  28. Interaction of polyomavirus internal protein VP2 with the major capsid protein VP1 and implications for participation of VP2 in viral entry.
    EMBO J. 1998 Jun 15;17(12):3233-40 PMID: 9628860
  29. Endocytosis of simian virus 40 into the endoplasmic reticulum.
    J Cell Biol. 1989 Dec;109(6 Pt 1):2721-9 PMID: 2556405
  30. The structure of simian virus 40 refined at 3.1 A resolution.
    Structure. 1996 Feb 15;4(2):165-82 PMID: 8805523
  31. Erlin-1 and erlin-2 are novel members of the prohibitin family of proteins that define lipid-raft-like domains of the ER.
    J Cell Sci. 2006 Aug 1;119(Pt 15):3149-60 PMID: 16835267
  32. Simian Virus 40 depends on ER protein folding and quality control factors for entry into host cells.
    Cell. 2007 Nov 2;131(3):516-29 PMID: 17981119
  33. A cytosolic chaperone complexes with dynamic membrane J-proteins and mobilizes a nonenveloped virus out of the endoplasmic reticulum.
    PLoS Pathog. 2014 Mar 27;10(3):e1004007 PMID: 24675744
  34. Exploiting the kinesin-1 molecular motor to generate a virus membrane penetration site.
    Nat Commun. 2017 May 24;8:15496 PMID: 28537258
  35. Gangliosides are receptors for murine polyoma virus and SV40.
    EMBO J. 2003 Sep 1;22(17):4346-55 PMID: 12941687
  36. Role of endosomes in simian virus 40 entry and infection.
    J Virol. 2011 May;85(9):4198-211 PMID: 21345959
  37. Key steps in ERAD of luminal ER proteins reconstituted with purified components.
    Cell. 2014 Sep 11;158(6):1375-88 PMID: 25215493
  38. A large and intact viral particle penetrates the endoplasmic reticulum membrane to reach the cytosol.
    PLoS Pathog. 2011 May;7(5):e1002037 PMID: 21589906
  39. Genome engineering using the CRISPR-Cas9 system.
    Nat Protoc. 2013 Nov;8(11):2281-308 PMID: 24157548
  40. ERdj5 Reductase Cooperates with Protein Disulfide Isomerase To Promote Simian Virus 40 Endoplasmic Reticulum Membrane Translocation.
    J Virol. 2015 Sep;89(17):8897-908 PMID: 26085143
  41. Characterization of the FKBP.rapamycin.FRB ternary complex.
    J Am Chem Soc. 2005 Apr 6;127(13):4715-21 PMID: 15796538
  42. Clustered hydrophobic amino acids in amphipathic helices mediate erlin1/2 complex assembly.
    Biochem Biophys Res Commun. 2011 Nov 11;415(1):135-40 PMID: 22020079
Article Info
Journal
PLoS pathogens
Abbr.
PLoS Pathog
ISSN
1553-7374
Published
2017-06-00
Epub
2017-00-14
Pages
e1006439
Language
English
Region
United States
NLM ID
101238921
PMCID
PMC5484543
Subset
IM
Grants
NIAID NIH HHS · R01 AI064296 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]