SV40 Hijacks Cellular Transport, Membrane Penetration, and Disassembly Machineries to Promote Infection

Overview

Journal Viruses

Publisher MDPI

Specialty Microbiology

Date 2019 Oct 9

PMID 31590347

Citations 16

Authors

Yu-Jie Chen

Xiaofang Liu

Billy Tsai

Affiliations

Soon will be listed here.

Abstract

During entry, a virus must be transported through the endomembrane system of the host cell, penetrate a cellular membrane, and undergo capsid disassembly, to reach the cytosol and often the nucleus in order to cause infection. To do so requires the virus to coordinately exploit the action of cellular membrane transport, penetration, and disassembly machineries. How this is accomplished remains enigmatic for many viruses, especially for viruses belonging to the nonenveloped virus family. In this review, we present the current model describing infectious entry of the nonenveloped polyomavirus (PyV) SV40. Insights from SV40 entry are likely to provide strategies to combat PyV-induced diseases, and to illuminate cellular trafficking, membrane transport, and disassembly mechanisms.

Citing Articles

Identification of Host-Protein Interaction Network of Canine Parvovirus Capsid Protein VP2 in F81 Cells.

Zhou H, Zhang H, Su X, Xu F, Xiao B, Zhang J Microorganisms. 2025; 13(1.

PMID: 39858856 PMC: 11767315. DOI: 10.3390/microorganisms13010088.

Reticulophagy and viral infection.

Wilson A, McCormick C Autophagy. 2024; 21(1):3-20.

PMID: 39394962 PMC: 11702952. DOI: 10.1080/15548627.2024.2414424.

Mechanisms of substrate processing during ER-associated protein degradation.

Christianson J, Jarosch E, Sommer T Nat Rev Mol Cell Biol. 2023; 24(11):777-796.

PMID: 37528230 DOI: 10.1038/s41580-023-00633-8.

How host ER membrane chaperones and morphogenic proteins support virus infection.

Woo T, Williams J, Tsai B J Cell Sci. 2023; 136(13).

PMID: 37401530 PMC: 10357032. DOI: 10.1242/jcs.261121.

A plant reovirus hijacks the DNAJB12-Hsc70 chaperone complex to promote viral spread in its planthopper vector.

Liang Q, Wan J, Liu H, Chen M, Xue T, Jia D Mol Plant Pathol. 2021; 23(6):805-818.

PMID: 34668642 PMC: 9104260. DOI: 10.1111/mpp.13152.

References

Inoue T, Tsai B . A large and intact viral particle penetrates the endoplasmic reticulum membrane to reach the cytosol. PLoS Pathog. 2011; 7(5):e1002037. PMC: 3093372. DOI: 10.1371/journal.ppat.1002037. View

Clever J, Yamada M, Kasamatsu H . Import of simian virus 40 virions through nuclear pore complexes. Proc Natl Acad Sci U S A. 1991; 88(16):7333-7. PMC: 52289. DOI: 10.1073/pnas.88.16.7333. View

Anderson H, Chen Y, Norkin L . Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Mol Biol Cell. 1996; 7(11):1825-34. PMC: 276029. DOI: 10.1091/mbc.7.11.1825. View

Damm E, Pelkmans L, Kartenbeck J, Mezzacasa A, Kurzchalia T, Helenius A . Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J Cell Biol. 2005; 168(3):477-88. PMC: 2171728. DOI: 10.1083/jcb.200407113. View

Geiger R, Andritschke D, Friebe S, Herzog F, Luisoni S, Heger T . BAP31 and BiP are essential for dislocation of SV40 from the endoplasmic reticulum to the cytosol. Nat Cell Biol. 2011; 13(11):1305-14. DOI: 10.1038/ncb2339. View

Fahrenkrog B, Aebi U . The nuclear pore complex: nucleocytoplasmic transport and beyond. Nat Rev Mol Cell Biol. 2003; 4(10):757-66. DOI: 10.1038/nrm1230. View

Ashok A, Atwood W . Contrasting roles of endosomal pH and the cytoskeleton in infection of human glial cells by JC virus and simian virus 40. J Virol. 2002; 77(2):1347-56. PMC: 140837. DOI: 10.1128/jvi.77.2.1347-1356.2003. View

Rainey-Barger E, Magnuson B, Tsai B . A chaperone-activated nonenveloped virus perforates the physiologically relevant endoplasmic reticulum membrane. J Virol. 2007; 81(23):12996-3004. PMC: 2169125. DOI: 10.1128/JVI.01037-07. View

Schelhaas M, Malmstrom J, Pelkmans L, Haugstetter J, Ellgaard L, Grunewald K . Simian Virus 40 depends on ER protein folding and quality control factors for entry into host cells. Cell. 2007; 131(3):516-29. DOI: 10.1016/j.cell.2007.09.038. View

10.

DeCaprio J, Garcea R . A cornucopia of human polyomaviruses. Nat Rev Microbiol. 2013; 11(4):264-76. PMC: 3928796. DOI: 10.1038/nrmicro2992. View

11.

Calton C, Bronnimann M, Manson A, Li S, Chapman J, Suarez-Berumen M . Translocation of the papillomavirus L2/vDNA complex across the limiting membrane requires the onset of mitosis. PLoS Pathog. 2017; 13(5):e1006200. PMC: 5412990. DOI: 10.1371/journal.ppat.1006200. View

12.

Chen X, Stehle T, Harrison S . Interaction of polyomavirus internal protein VP2 with the major capsid protein VP1 and implications for participation of VP2 in viral entry. EMBO J. 1998; 17(12):3233-40. PMC: 1170661. DOI: 10.1093/emboj/17.12.3233. View

13.

Butin-Israeli V, Ben-Nun-Shaul O, Kopatz I, Adam S, Shimi T, Goldman R . Simian virus 40 induces lamin A/C fluctuations and nuclear envelope deformation during cell entry. Nucleus. 2011; 2(4):320-30. PMC: 3260569. DOI: 10.4161/nucl.2.4.16371. View

14.

Pelkmans L, Puntener D, Helenius A . Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science. 2002; 296(5567):535-9. DOI: 10.1126/science.1069784. View

15.

Lange A, Mills R, Lange C, Stewart M, Devine S, Corbett A . Classical nuclear localization signals: definition, function, and interaction with importin alpha. J Biol Chem. 2006; 282(8):5101-5. PMC: 4502416. DOI: 10.1074/jbc.R600026200. View

16.

Schlager M, Hoang H, Urnavicius L, Bullock S, Carter A . In vitro reconstitution of a highly processive recombinant human dynein complex. EMBO J. 2014; 33(17):1855-68. PMC: 4158905. DOI: 10.15252/embj.201488792. View

17.

Arora R, Chang Y, Moore P . MCV and Merkel cell carcinoma: a molecular success story. Curr Opin Virol. 2012; 2(4):489-98. PMC: 3422445. DOI: 10.1016/j.coviro.2012.05.007. View

18.

Nakanishi A, Shum D, Morioka H, Otsuka E, Kasamatsu H . Interaction of the Vp3 nuclear localization signal with the importin alpha 2/beta heterodimer directs nuclear entry of infecting simian virus 40. J Virol. 2002; 76(18):9368-77. PMC: 136453. DOI: 10.1128/jvi.76.18.9368-9377.2002. View

19.

Kartenbeck J, Stukenbrok H, Helenius A . Endocytosis of simian virus 40 into the endoplasmic reticulum. J Cell Biol. 1989; 109(6 Pt 1):2721-9. PMC: 2115950. DOI: 10.1083/jcb.109.6.2721. View

20.

Stehle T, Gamblin S, Yan Y, Harrison S . The structure of simian virus 40 refined at 3.1 A resolution. Structure. 1996; 4(2):165-82. DOI: 10.1016/s0969-2126(96)00020-2. View