Cysteine Residues in the Major Capsid Protein, Vp1, of the JC Virus Are Important for Protein Stability and Oligomer Formation

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Kobayashi, Shintaro ^a   Suzuki, Tadaki ^b   Igarashi, Manabu ^a   Orba, Yasuko ^a   Ohtake, Noriko ^a   Nagakawa, Keita ^a   Niikura, Kenichi ^a   Kimura, Takashi ^a   Kasamatsu, Harumi ^c   Sawa, Hirofumi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL EXTRACT; CYSTEINE; PROTEIN VP1;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; DNA VIRUS INFECTION; GENETIC TRANSFECTION; HELA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; JC VIRUS; JC VIRUS INFECTION; MUTAGENESIS; NUCLEAR LOCALIZATION SIGNAL; OLIGOMERIZATION; PROTEIN FOLDING; PROTEIN PROCESSING; PROTEIN STABILITY; VIRION; VIRUS GENOME; VIRUS HEMAGGLUTINATION; VIRUS INFECTIVITY; VIRUS PARTICLE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CAPSID; CAPSID PROTEINS; CELL NUCLEUS; CYSTEINE; HELA CELLS; HUMANS; JC VIRUS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS; MUTATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY;

EID: 84885098332     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076668     Document Type: Article

References (29)

1. Chen XS, Stehle T, Harrison SC, (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.
2. Chang D, Fung CY, Ou WC, Chao PC, Li SY, et al. (1997) Self-assembly of the JC virus major capsid protein, VP1, expressed in insect cells. J Gen Virol 78 (Pt 6): 1435-1439.
3. Chen PL, Wang M, Ou WC, Lii CK, Chen LS, et al. (2001) Disulfide bonds stabilize JC virus capsid-like structure by protecting calcium ions from chelation. FEBS Lett 500: 109-113.
4. Ou WC, Wang M, Fung CY, Tsai RT, Chao PC, et al. (1999) The major capsid protein, VP1, of human JC virus expressed in Escherichia coli is able to self-assemble into a capsid-like particle and deliver exogenous DNA into human kidney cells. J Gen Virol 80 (Pt 1): 39-46.
5. Neu U, Maginnis MS, Palma AS, Ströh LJ, Nelson CD, et al. (2010) Structure-function analysis of the human JC polyomavirus establishes the LSTc pentasaccharide as a functional receptor motif. Cell Host Microbe 8: 309-319.
6. Shen PS, Enderlein D, Nelson CD, Carter WS, Kawano M, et al. (2011) The structure of avian polyomavirus reveals variably sized capsids, non-conserved inter-capsomere interactions, and a possible location of the minor capsid protein VP4. Virology 411: 142-152.
7. Ou WC, Chen LH, Wang M, Hseu TH, Chang D, (2001) Analysis of minimal sequences on JC virus VP1 required for capsid assembly. J Neurovirol 7: 298-301.
8. Liddington RC, Yan Y, Moulai J, Sahli R, Benjamin TL, et al. (1991) Structure of simian virus 40 at 3.8-A resolution. Nature 354: 278-284.
9. Stehle T, Gamblin SJ, Yan Y, Harrison SC, (1996) The structure of simian virus 40 refined at 3.1 A resolution. Structure 4: 165-182.
10. Li, Nakanishi A, Clark SW, Kasamatsu H, (2002) Formation of transitory intrachain and interchain disulfide bonds accompanies the folding and oligomerization of simian virus 40 Vp1 in the cytoplasm. Proc Natl Acad Sci U S A 99: 1353-1358.
11. Li, Nakanishi A, Fontanes V, Kasamatsu H, (2005) Pairs of Vp1 cysteine residues essential for simian virus 40 infection. J Virol 79: 3859-3864.
12. Li, Nakanishi A, Tran MA, Salazar AM, Liddington RC, et al. (2000) Role of simian virus 40 Vp1 cysteines in virion infectivity. J Virol 74: 11388-11393.
13. Li, Itoh N, Watanabe M, Shi Y, Liu P, et al. (2009) Association of simian virus 40 vp1 with 70-kilodalton heat shock proteins and viral tumor antigens. J Virol 83: 37-46.
14. Ishizu KI, Watanabe H, Han SI, Kanesashi SN, Hoque M, et al. (2001) Roles of disulfide linkage and calcium ion-mediated interactions in assembly and disassembly of virus-like particles composed of simian virus 40 VP1 capsid protein. J Virol 75: 61-72.
15. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, et al. (2004) The role of autophagy during the early neonatal starvation period. Nature 432: 1032-1036.
16. Ashok A, Atwood WJ, (2003) Contrasting roles of endosomal pH and the cytoskeleton in infection of human glial cells by JC virus and simian virus 40. J Virol 77: 1347-1356.
17. Okada Y, Sawa H, Tanaka S, Takada A, Suzuki S, et al. (2000) Transcriptional activation of JC virus by human T-lymphotropic virus type I Tax protein in human neuronal cell lines. J Biol Chem 275: 17016-17023.
18. Suzuki T, Orba Y, Okada Y, Sunden Y, Kimura T, et al. (2010) The human polyoma JC virus agnoprotein acts as a viroporin. PLoS Pathog 6: e1000801.
19. Vacante DA, Traub R, Major EO, (1989) Extension of JC virus host range to monkey cells by insertion of a simian virus 40 enhancer into the JC virus regulatory region. Virology 170: 353-361.
20. Gasparovic ML, Gee GV, Atwood WJ, (2006) JC virus minor capsid proteins Vp2 and Vp3 are essential for virus propagation. J Virol 80: 10858-10861.
21. Gee GV, Tsomaia N, Mierke DF, Atwood WJ, (2004) Modeling a sialic acid binding pocket in the external loops of JC virus VP1. J Biol Chem 279: 49172-49176.
22. Suzuki S, Sawa H, Komagome R, Orba Y, Yamada M, et al. (2001) Broad distribution of the JC virus receptor contrasts with a marked cellular restriction of virus replication. Virology 286: 100-112.
23. Shimizu Y, Inoue A, Tomari Y, Suzuki T, Yokogawa T, et al. (2001) Cell-free translation reconstituted with purified components. Nat Biotechnol 19: 751-755.
24. Shimizu Y, Kanamori T, Ueda T, (2005) Protein synthesis by pure translation systems. Methods 36: 299-304.
25. Okada Y, Sawa H, Endo S, Orba Y, Umemura T, et al. (2002) Expression of JC virus agnoprotein in progressive multifocal leukoencephalopathy brain. Acta Neuropathol 104: 130-136.
26. Orba Y, Sunden Y, Suzuki T, Nagashima K, Kimura T, et al. (2008) Pharmacological cdk inhibitor R-Roscovitine suppresses JC virus proliferation. Virology 370: 173-183.
27. Stehle T, Harrison SC, (1997) High-resolution structure of a polyomavirus VP1-oligosaccharide complex: implications for assembly and receptor binding. EMBO J 16: 5139-5148.
28. Goldberg AL, (2003) Protein degradation and protection against misfolded or damaged proteins. Nature 426: 895-899.
29. Kuruma Y, Suzuki T, Ono S, Yoshida M, Ueda T, (2012) Functional analysis of membranous Fo-a subunit of F1Fo-ATP synthase by in vitro protein synthesis. Biochem J 442: 631-638.