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Published in: Archives of Virology 7/2010

01-07-2010 | Brief Review

Viral interaction with molecular chaperones: role in regulating viral infection

Authors: Allen Xiao, Jerry Wong, Honglin Luo

Published in: Archives of Virology | Issue 7/2010

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Abstract

As essential effectors in protein quality control, molecular chaperones serve as the primary checkpoint to assist proper protein folding and prevent misfolded proteins from denaturation and aggregation. In addition, chaperones can function to direct terminally misfolded proteins to the proteolytic system for degradation. Viruses rely on host cell machineries for productive infection. Like for many other processes, various viruses have been shown to evolve mechanisms to utilize or subvert the host protein quality control machinery to support the completion of their life cycle. Furthermore, recent studies suggest that some viruses encode for their own chaperone-like proteins to enhance their infectivity. This review summarizes the current understanding of the interplay between molecular chaperones and viral proteins, highlights the chaperone activities of a number of viral proteins, and discusses potential antiviral therapeutic strategies targeting the virus-chaperone interactions.
Literature
1.
go back to reference Agostini I, Popov S, Li J, Dubrovsky L, Hao T, Bukrinsky M (2000) Heat-shock protein 70 can replace viral protein R of HIV-1 during nuclear import of the viral preintegration complex. Exp Cell Res 259:398–403CrossRefPubMed Agostini I, Popov S, Li J, Dubrovsky L, Hao T, Bukrinsky M (2000) Heat-shock protein 70 can replace viral protein R of HIV-1 during nuclear import of the viral preintegration complex. Exp Cell Res 259:398–403CrossRefPubMed
2.
go back to reference Andreeva L, Heads R, Green CJ (1999) Cyclophilins and their possible role in the stress response. Int J Exp Pathol 80:305–315CrossRefPubMed Andreeva L, Heads R, Green CJ (1999) Cyclophilins and their possible role in the stress response. Int J Exp Pathol 80:305–315CrossRefPubMed
3.
go back to reference Arndt V, Rogon C, Hohfeld J (2007) To be, or not to be—molecular chaperones in protein degradation. Cell Mol Life Sci 64:2525–2541CrossRefPubMed Arndt V, Rogon C, Hohfeld J (2007) To be, or not to be—molecular chaperones in protein degradation. Cell Mol Life Sci 64:2525–2541CrossRefPubMed
4.
go back to reference Awe K, Lambert C, Prange R (2008) Mammalian BiP controls posttranslational ER translocation of the hepatitis B virus large envelope protein. FEBS Lett 582:3179–3184CrossRefPubMed Awe K, Lambert C, Prange R (2008) Mammalian BiP controls posttranslational ER translocation of the hepatitis B virus large envelope protein. FEBS Lett 582:3179–3184CrossRefPubMed
5.
go back to reference Babaahmady K, Oehlmann W, Singh M, Lehner T (2007) Inhibition of human immunodeficiency virus type 1 infection of human CD4+ T cells by microbial HSP70 and the peptide epitope 407–426. J Virol 81:3354–3360CrossRefPubMed Babaahmady K, Oehlmann W, Singh M, Lehner T (2007) Inhibition of human immunodeficiency virus type 1 infection of human CD4+ T cells by microbial HSP70 and the peptide epitope 407–426. J Virol 81:3354–3360CrossRefPubMed
6.
go back to reference Babaahmady K, Bergmeier LA, Lehner T (2008) Combining human antisera to human leukocyte antigens, HIVgp120 and 70 kDa heat shock protein results in broadly neutralizing activity to HIV-1. Aids 22:1267–1276CrossRefPubMed Babaahmady K, Bergmeier LA, Lehner T (2008) Combining human antisera to human leukocyte antigens, HIVgp120 and 70 kDa heat shock protein results in broadly neutralizing activity to HIV-1. Aids 22:1267–1276CrossRefPubMed
7.
go back to reference Basha W, Kitagawa R, Uhara M, Imazu H, Uechi K, Tanaka J (2005) Geldanamycin, a potent and specific inhibitor of Hsp90, inhibits gene expression and replication of human cytomegalovirus. Antivir Chem Chemother 16:135–146PubMed Basha W, Kitagawa R, Uhara M, Imazu H, Uechi K, Tanaka J (2005) Geldanamycin, a potent and specific inhibitor of Hsp90, inhibits gene expression and replication of human cytomegalovirus. Antivir Chem Chemother 16:135–146PubMed
8.
go back to reference Beachy SH, Kisailus AJ, Repasky EA, Subjeck JR, Wang XY, Kazim AL (2007) Engineering secretable forms of chaperones for immune modulation and vaccine development. Methods 43:184–193CrossRefPubMed Beachy SH, Kisailus AJ, Repasky EA, Subjeck JR, Wang XY, Kazim AL (2007) Engineering secretable forms of chaperones for immune modulation and vaccine development. Methods 43:184–193CrossRefPubMed
9.
go back to reference Bolt G (2001) The measles virus (MV) glycoproteins interact with cellular chaperones in the endoplasmic reticulum and MV infection upregulates chaperone expression. Arch Virol 146:2055–2068CrossRefPubMed Bolt G (2001) The measles virus (MV) glycoproteins interact with cellular chaperones in the endoplasmic reticulum and MV infection upregulates chaperone expression. Arch Virol 146:2055–2068CrossRefPubMed
10.
go back to reference Brenner BG, Wainberg MA (1999) Heat shock protein-based therapeutic strategies against human immunodeficiency virus type 1 infection. Infect Dis Obstet Gynecol 7:80–90CrossRefPubMed Brenner BG, Wainberg MA (1999) Heat shock protein-based therapeutic strategies against human immunodeficiency virus type 1 infection. Infect Dis Obstet Gynecol 7:80–90CrossRefPubMed
11.
go back to reference Buchkovich NJ, Maguire TG, Yu Y, Paton AW, Paton JC, Alwine JC (2008) Human cytomegalovirus specifically controls the levels of the endoplasmic reticulum chaperone BiP/GRP78, which is required for virion assembly. J Virol 82:31–39CrossRefPubMed Buchkovich NJ, Maguire TG, Yu Y, Paton AW, Paton JC, Alwine JC (2008) Human cytomegalovirus specifically controls the levels of the endoplasmic reticulum chaperone BiP/GRP78, which is required for virion assembly. J Virol 82:31–39CrossRefPubMed
12.
go back to reference Bukrinsky M, Zhao Y (2004) Heat-shock proteins reverse the G2 arrest caused by HIV-1 viral protein R. DNA Cell Biol 23:223–225CrossRefPubMed Bukrinsky M, Zhao Y (2004) Heat-shock proteins reverse the G2 arrest caused by HIV-1 viral protein R. DNA Cell Biol 23:223–225CrossRefPubMed
13.
go back to reference Burch AD, Weller SK (2005) Herpes simplex virus type 1 DNA polymerase requires the mammalian chaperone hsp90 for proper localization to the nucleus. J Virol 79:10740–10749CrossRefPubMed Burch AD, Weller SK (2005) Herpes simplex virus type 1 DNA polymerase requires the mammalian chaperone hsp90 for proper localization to the nucleus. J Virol 79:10740–10749CrossRefPubMed
14.
go back to reference Calderwood SK, Mambula SS, Gray PJ Jr, Theriault JR (2007) Extracellular heat shock proteins in cell signaling. FEBS Lett 581:3689–3694CrossRefPubMed Calderwood SK, Mambula SS, Gray PJ Jr, Theriault JR (2007) Extracellular heat shock proteins in cell signaling. FEBS Lett 581:3689–3694CrossRefPubMed
15.
go back to reference Chabaud S, Lambert H, Sasseville AM, Lavoie H, Guilbault C, Massie B, Landry J, Langelier Y (2003) The R1 subunit of herpes simplex virus ribonucleotide reductase has chaperone-like activity similar to Hsp27. FEBS Lett 545:213–218CrossRefPubMed Chabaud S, Lambert H, Sasseville AM, Lavoie H, Guilbault C, Massie B, Landry J, Langelier Y (2003) The R1 subunit of herpes simplex virus ribonucleotide reductase has chaperone-like activity similar to Hsp27. FEBS Lett 545:213–218CrossRefPubMed
16.
go back to reference Chase G, Deng T, Fodor E, Leung BW, Mayer D, Schwemmle M, Brownlee G (2008) Hsp90 inhibitors reduce influenza virus replication in cell culture. Virology 377:431–439CrossRefPubMed Chase G, Deng T, Fodor E, Leung BW, Mayer D, Schwemmle M, Brownlee G (2008) Hsp90 inhibitors reduce influenza virus replication in cell culture. Virology 377:431–439CrossRefPubMed
17.
go back to reference Chatterji U, Bobardt M, Selvarajah S, Yang F, Tang H, Sakamoto N, Vuagniaux G, Parkinson T, Gallay P (2009) The isomerase active site of cyclophilin A is critical for hepatitis C virus replication. J Biol Chem 284:16998–17005CrossRefPubMed Chatterji U, Bobardt M, Selvarajah S, Yang F, Tang H, Sakamoto N, Vuagniaux G, Parkinson T, Gallay P (2009) The isomerase active site of cyclophilin A is critical for hepatitis C virus replication. J Biol Chem 284:16998–17005CrossRefPubMed
18.
go back to reference Chen S, Zhao X, Tan J, Lu H, Qi Z, Huang Q, Zeng X, Zhang M, Jiang S, Jiang H, Yu L (2007) Structure-based identification of small molecule compounds targeting cell cyclophilin A with anti-HIV-1 activity. Eur J Pharmacol 565:54–59CrossRefPubMed Chen S, Zhao X, Tan J, Lu H, Qi Z, Huang Q, Zeng X, Zhang M, Jiang S, Jiang H, Yu L (2007) Structure-based identification of small molecule compounds targeting cell cyclophilin A with anti-HIV-1 activity. Eur J Pharmacol 565:54–59CrossRefPubMed
19.
go back to reference Cho DY, Yang GH, Ryu CJ, Hong HJ (2003) Molecular chaperone GRP78/BiP interacts with the large surface protein of hepatitis B virus in vitro and in vivo. J Virol 77:2784–2788CrossRefPubMed Cho DY, Yang GH, Ryu CJ, Hong HJ (2003) Molecular chaperone GRP78/BiP interacts with the large surface protein of hepatitis B virus in vitro and in vivo. J Virol 77:2784–2788CrossRefPubMed
20.
go back to reference Choukhi A, Ung S, Wychowski C, Dubuisson J (1998) Involvement of endoplasmic reticulum chaperones in the folding of hepatitis C virus glycoproteins. J Virol 72:3851–3858PubMed Choukhi A, Ung S, Wychowski C, Dubuisson J (1998) Involvement of endoplasmic reticulum chaperones in the folding of hepatitis C virus glycoproteins. J Virol 72:3851–3858PubMed
21.
go back to reference Chromy LR, Pipas JM, Garcea RL (2003) Chaperone-mediated in vitro assembly of Polyomavirus capsids. Proc Natl Acad Sci USA 100:10477–10482CrossRefPubMed Chromy LR, Pipas JM, Garcea RL (2003) Chaperone-mediated in vitro assembly of Polyomavirus capsids. Proc Natl Acad Sci USA 100:10477–10482CrossRefPubMed
22.
go back to reference Cobbold C, Windsor M, Wileman T (2001) A virally encoded chaperone specialized for folding of the major capsid protein of African swine fever virus. J Virol 75:7221–7229CrossRefPubMed Cobbold C, Windsor M, Wileman T (2001) A virally encoded chaperone specialized for folding of the major capsid protein of African swine fever virus. J Virol 75:7221–7229CrossRefPubMed
23.
go back to reference Cripe TP, Delos SE, Estes PA, Garcea RL (1995) In vivo and in vitro association of hsc70 with polyomavirus capsid proteins. J Virol 69:7807–7813PubMed Cripe TP, Delos SE, Estes PA, Garcea RL (1995) In vivo and in vitro association of hsc70 with polyomavirus capsid proteins. J Virol 69:7807–7813PubMed
24.
go back to reference Daniels R, Kurowski B, Johnson AE, Hebert DN (2003) N-linked glycans direct the cotranslational folding pathway of influenza hemagglutinin. Mol Cell 11:79–90CrossRefPubMed Daniels R, Kurowski B, Johnson AE, Hebert DN (2003) N-linked glycans direct the cotranslational folding pathway of influenza hemagglutinin. Mol Cell 11:79–90CrossRefPubMed
25.
go back to reference Das S, Laxminarayana SV, Chandra N, Ravi V, Desai A (2009) Heat shock protein 70 on Neuro2a cells is a putative receptor for Japanese encephalitis virus. Virology 385:47–57CrossRefPubMed Das S, Laxminarayana SV, Chandra N, Ravi V, Desai A (2009) Heat shock protein 70 on Neuro2a cells is a putative receptor for Japanese encephalitis virus. Virology 385:47–57CrossRefPubMed
26.
go back to reference Dubuisson J, Rice CM (1996) Hepatitis C virus glycoprotein folding: disulfide bond formation and association with calnexin. J Virol 70:778–786PubMed Dubuisson J, Rice CM (1996) Hepatitis C virus glycoprotein folding: disulfide bond formation and association with calnexin. J Virol 70:778–786PubMed
27.
go back to reference Dubuisson J (1998) The role of chaperone proteins in the assembly of envelope proteins of hepatitis C virus. Bull Mem Acad R Med Belg 153:343–349 discussion 350–341PubMed Dubuisson J (1998) The role of chaperone proteins in the assembly of envelope proteins of hepatitis C virus. Bull Mem Acad R Med Belg 153:343–349 discussion 350–341PubMed
28.
go back to reference Ellis J (2005) Chaperone function: The orthodox view. In: Henderson B and Pockley G (ed) Molecular chaperons and cell signaling, Cambridge, pp 3–21. doi:10.2277/0521836549 Ellis J (2005) Chaperone function: The orthodox view. In: Henderson B and Pockley G (ed) Molecular chaperons and cell signaling, Cambridge, pp 3–21. doi:10.​2277/​0521836549
29.
go back to reference Gaudin Y (1997) Folding of rabies virus glycoprotein: epitope acquisition and interaction with endoplasmic reticulum chaperones. J Virol 71:3742–3750PubMed Gaudin Y (1997) Folding of rabies virus glycoprotein: epitope acquisition and interaction with endoplasmic reticulum chaperones. J Virol 71:3742–3750PubMed
30.
go back to reference Geller R, Vignuzzi M, Andino R, Frydman J (2007) Evolutionary constraints on chaperone-mediated folding provide an antiviral approach refractory to development of drug resistance. Genes Dev 21:195–205CrossRefPubMed Geller R, Vignuzzi M, Andino R, Frydman J (2007) Evolutionary constraints on chaperone-mediated folding provide an antiviral approach refractory to development of drug resistance. Genes Dev 21:195–205CrossRefPubMed
31.
go back to reference Gober MD, Wales SQ, Aurelian L (2005) Herpes simplex virus type 2 encodes a heat shock protein homologue with apoptosis regulatory functions. Front Biosci 10:2788–2803CrossRefPubMed Gober MD, Wales SQ, Aurelian L (2005) Herpes simplex virus type 2 encodes a heat shock protein homologue with apoptosis regulatory functions. Front Biosci 10:2788–2803CrossRefPubMed
32.
go back to reference Guerrero CA, Bouyssounade D, Zarate S, Isa P, Lopez T, Espinosa R, Romero P, Mendez E, Lopez S, Arias CF (2002) Heat shock cognate protein 70 is involved in rotavirus cell entry. J Virol 76:4096–4102CrossRefPubMed Guerrero CA, Bouyssounade D, Zarate S, Isa P, Lopez T, Espinosa R, Romero P, Mendez E, Lopez S, Arias CF (2002) Heat shock cognate protein 70 is involved in rotavirus cell entry. J Virol 76:4096–4102CrossRefPubMed
33.
go back to reference Hammond C, Helenius A (1994) Folding of VSV G protein: sequential interaction with BiP and calnexin. Science 266:456–458CrossRefPubMed Hammond C, Helenius A (1994) Folding of VSV G protein: sequential interaction with BiP and calnexin. Science 266:456–458CrossRefPubMed
34.
go back to reference Hu J, Anselmo D (2000) In vitro reconstitution of a functional duck hepatitis B virus reverse transcriptase: posttranslational activation by Hsp90. J Virol 74:11447–11455CrossRefPubMed Hu J, Anselmo D (2000) In vitro reconstitution of a functional duck hepatitis B virus reverse transcriptase: posttranslational activation by Hsp90. J Virol 74:11447–11455CrossRefPubMed
35.
go back to reference Iordanskiy S, Zhao Y, Dubrovsky L, Iordanskaya T, Chen M, Liang D, Bukrinsky M (2004) Heat shock protein 70 protects cells from cell cycle arrest and apoptosis induced by human immunodeficiency virus type 1 viral protein R. J Virol 78:9697–9704CrossRefPubMed Iordanskiy S, Zhao Y, Dubrovsky L, Iordanskaya T, Chen M, Liang D, Bukrinsky M (2004) Heat shock protein 70 protects cells from cell cycle arrest and apoptosis induced by human immunodeficiency virus type 1 viral protein R. J Virol 78:9697–9704CrossRefPubMed
36.
go back to reference Jeon YK, Park CH, Kim KY, Li YC, Kim J, Kim YA, Paik JH, Park BK, Kim CW, Kim YN (2007) The heat-shock protein 90 inhibitor, geldanamycin, induces apoptotic cell death in Epstein-Barr virus-positive NK/T-cell lymphoma by Akt down-regulation. J Pathol 213:170–179CrossRefPubMed Jeon YK, Park CH, Kim KY, Li YC, Kim J, Kim YA, Paik JH, Park BK, Kim CW, Kim YN (2007) The heat-shock protein 90 inhibitor, geldanamycin, induces apoptotic cell death in Epstein-Barr virus-positive NK/T-cell lymphoma by Akt down-regulation. J Pathol 213:170–179CrossRefPubMed
37.
go back to reference Kampmueller KM, Miller DJ (2005) The cellular chaperone heat shock protein 90 facilitates Flock House virus RNA replication in Drosophila cells. J Virol 79:6827–6837CrossRefPubMed Kampmueller KM, Miller DJ (2005) The cellular chaperone heat shock protein 90 facilitates Flock House virus RNA replication in Drosophila cells. J Virol 79:6827–6837CrossRefPubMed
38.
go back to reference Kim SS, Shin HJ, Cho YH, Rho HM (2000) Expression of stable hepatitis B viral polymerase associated with GRP94 in E. coli. Arch Virol 145:1305–1320CrossRefPubMed Kim SS, Shin HJ, Cho YH, Rho HM (2000) Expression of stable hepatitis B viral polymerase associated with GRP94 in E. coli. Arch Virol 145:1305–1320CrossRefPubMed
39.
go back to reference Kosmaoglou M, Schwarz N, Bett JS, Cheetham ME (2008) Molecular chaperones and photoreceptor function. Prog Retin Eye Res 27:434–449CrossRefPubMed Kosmaoglou M, Schwarz N, Bett JS, Cheetham ME (2008) Molecular chaperones and photoreceptor function. Prog Retin Eye Res 27:434–449CrossRefPubMed
40.
go back to reference Kotsiopriftis M, Tanner JE, Alfieri C (2005) Heat shock protein 90 expression in Epstein-Barr virus-infected B cells promotes gammadelta T-cell proliferation in vitro. J Virol 79:7255–7261CrossRefPubMed Kotsiopriftis M, Tanner JE, Alfieri C (2005) Heat shock protein 90 expression in Epstein-Barr virus-infected B cells promotes gammadelta T-cell proliferation in vitro. J Virol 79:7255–7261CrossRefPubMed
41.
go back to reference Kuciak M, Gabus C, Ivanyi-Nagy R, Semrad K, Storchak R, Chaloin O, Muller S, Mely Y, Darlix JL (2008) The HIV-1 transcriptional activator Tat has potent nucleic acid chaperoning activities in vitro. Nucleic Acids Res 36:3389–3400CrossRefPubMed Kuciak M, Gabus C, Ivanyi-Nagy R, Semrad K, Storchak R, Chaloin O, Muller S, Mely Y, Darlix JL (2008) The HIV-1 transcriptional activator Tat has potent nucleic acid chaperoning activities in vitro. Nucleic Acids Res 36:3389–3400CrossRefPubMed
42.
go back to reference Kumar M, Mitra D (2005) Heat shock protein 40 is necessary for human immunodeficiency virus-1 Nef-mediated enhancement of viral gene expression and replication. J Biol Chem 280:40041–40050CrossRefPubMed Kumar M, Mitra D (2005) Heat shock protein 40 is necessary for human immunodeficiency virus-1 Nef-mediated enhancement of viral gene expression and replication. J Biol Chem 280:40041–40050CrossRefPubMed
43.
go back to reference Lambert C, Prange R (2003) Chaperone action in the posttranslational topological reorientation of the hepatitis B virus large envelope protein: implications for translocational regulation. Proc Natl Acad Sci USA 100:5199–5204CrossRefPubMed Lambert C, Prange R (2003) Chaperone action in the posttranslational topological reorientation of the hepatitis B virus large envelope protein: implications for translocational regulation. Proc Natl Acad Sci USA 100:5199–5204CrossRefPubMed
44.
go back to reference Lee SH, Song R, Lee MN, Kim CS, Lee H, Kong YY, Kim H, Jang SK (2008) A molecular chaperone glucose-regulated protein 94 blocks apoptosis induced by virus infection. Hepatology 47:854–866CrossRefPubMed Lee SH, Song R, Lee MN, Kim CS, Lee H, Kong YY, Kim H, Jang SK (2008) A molecular chaperone glucose-regulated protein 94 blocks apoptosis induced by virus infection. Hepatology 47:854–866CrossRefPubMed
45.
go back to reference Lehner T, Mitchell E, Bergmeier L, Singh M, Spallek R, Cranage M, Hall G, Dennis M, Villinger F, Wang Y (2000) The role of gammadelta T cells in generating antiviral factors and beta-chemokines in protection against mucosal simian immunodeficiency virus infection. Eur J Immunol 30:2245–2256CrossRefPubMed Lehner T, Mitchell E, Bergmeier L, Singh M, Spallek R, Cranage M, Hall G, Dennis M, Villinger F, Wang Y (2000) The role of gammadelta T cells in generating antiviral factors and beta-chemokines in protection against mucosal simian immunodeficiency virus infection. Eur J Immunol 30:2245–2256CrossRefPubMed
46.
go back to reference Lewthwaite J, Skinner A, Henderson B (1998) Are molecular chaperones microbial virulence factors? Trends Microbiol 6:426–428CrossRefPubMed Lewthwaite J, Skinner A, Henderson B (1998) Are molecular chaperones microbial virulence factors? Trends Microbiol 6:426–428CrossRefPubMed
47.
go back to reference Li YH, Tao PZ, Liu YZ, Jiang JD (2004) Geldanamycin, a ligand of heat shock protein 90, inhibits the replication of herpes simplex virus type 1 in vitro. Antimicrob Agents Chemother 48:867–872CrossRefPubMed Li YH, Tao PZ, Liu YZ, Jiang JD (2004) Geldanamycin, a ligand of heat shock protein 90, inhibits the replication of herpes simplex virus type 1 in vitro. Antimicrob Agents Chemother 48:867–872CrossRefPubMed
48.
go back to reference Liberman E, Fong YL, Selby MJ, Choo QL, Cousens L, Houghton M, Yen TS (1999) Activation of the grp78 and grp94 promoters by hepatitis C virus E2 envelope protein. J Virol 73:3718–3722PubMed Liberman E, Fong YL, Selby MJ, Choo QL, Cousens L, Houghton M, Yen TS (1999) Activation of the grp78 and grp94 promoters by hepatitis C virus E2 envelope protein. J Virol 73:3718–3722PubMed
49.
go back to reference Lim SO, Park SG, Yoo JH, Park YM, Kim HJ, Jang KT, Cho JW, Yoo BC, Jung GH, Park CK (2005) Expression of heat shock proteins (HSP27, HSP60, HSP70, HSP90, GRP78, GRP94) in hepatitis B virus-related hepatocellular carcinomas and dysplastic nodules. World J Gastroenterol 11:2072–2079PubMed Lim SO, Park SG, Yoo JH, Park YM, Kim HJ, Jang KT, Cho JW, Yoo BC, Jung GH, Park CK (2005) Expression of heat shock proteins (HSP27, HSP60, HSP70, HSP90, GRP78, GRP94) in hepatitis B virus-related hepatocellular carcinomas and dysplastic nodules. World J Gastroenterol 11:2072–2079PubMed
50.
go back to reference Liu JS, Kuo SR, Makhov AM, Cyr DM, Griffith JD, Broker TR, Chow LT (1998) Human Hsp70 and Hsp40 chaperone proteins facilitate human papillomavirus-11 E1 protein binding to the origin and stimulate cell-free DNA replication. J Biol Chem 273:30704–30712CrossRefPubMed Liu JS, Kuo SR, Makhov AM, Cyr DM, Griffith JD, Broker TR, Chow LT (1998) Human Hsp70 and Hsp40 chaperone proteins facilitate human papillomavirus-11 E1 protein binding to the origin and stimulate cell-free DNA replication. J Biol Chem 273:30704–30712CrossRefPubMed
51.
go back to reference Liu K, Qian L, Wang J, Li W, Deng X, Chen X, Sun W, Wei H, Qian X, Jiang Y, He F (2009) Two-dimensional blue native/SDS-PAGE analysis reveals heat shock protein chaperone machinery involved in hepatitis B virus production in HepG2.2.15 cells. Mol Cell Proteomics 8:495–505CrossRefPubMed Liu K, Qian L, Wang J, Li W, Deng X, Chen X, Sun W, Wei H, Qian X, Jiang Y, He F (2009) Two-dimensional blue native/SDS-PAGE analysis reveals heat shock protein chaperone machinery involved in hepatitis B virus production in HepG2.2.15 cells. Mol Cell Proteomics 8:495–505CrossRefPubMed
52.
go back to reference Loffler-Mary H, Werr M, Prange R (1997) Sequence-specific repression of cotranslational translocation of the hepatitis B virus envelope proteins coincides with binding of heat shock protein Hsc70. Virology 235:144–152CrossRefPubMed Loffler-Mary H, Werr M, Prange R (1997) Sequence-specific repression of cotranslational translocation of the hepatitis B virus envelope proteins coincides with binding of heat shock protein Hsc70. Virology 235:144–152CrossRefPubMed
53.
go back to reference Ma Y, Hendershot LM (2004) ER chaperone functions during normal and stress conditions. J Chem Neuroanat 28:51–65CrossRefPubMed Ma Y, Hendershot LM (2004) ER chaperone functions during normal and stress conditions. J Chem Neuroanat 28:51–65CrossRefPubMed
54.
go back to reference Maruri-Avidal L, Lopez S, Arias CF (2008) Endoplasmic reticulum chaperones are involved in the morphogenesis of rotavirus infectious particles. J Virol 82:5368–5380CrossRefPubMed Maruri-Avidal L, Lopez S, Arias CF (2008) Endoplasmic reticulum chaperones are involved in the morphogenesis of rotavirus infectious particles. J Virol 82:5368–5380CrossRefPubMed
55.
go back to reference McClellan AJ, Tam S, Kaganovich D, Frydman J (2005) Protein quality control: chaperones culling corrupt conformations. Nat Cell Biol 7:736–741CrossRefPubMed McClellan AJ, Tam S, Kaganovich D, Frydman J (2005) Protein quality control: chaperones culling corrupt conformations. Nat Cell Biol 7:736–741CrossRefPubMed
56.
go back to reference Miyata Y, Yahara I (2000) p53-independent association between SV40 large T antigen and the major cytosolic heat shock protein, HSP90. Oncogene 19:1477–1484CrossRefPubMed Miyata Y, Yahara I (2000) p53-independent association between SV40 large T antigen and the major cytosolic heat shock protein, HSP90. Oncogene 19:1477–1484CrossRefPubMed
57.
go back to reference Momose F, Naito T, Yano K, Sugimoto S, Morikawa Y, Nagata K (2002) Identification of Hsp90 as a stimulatory host factor involved in influenza virus RNA synthesis. J Biol Chem 277:45306–45314CrossRefPubMed Momose F, Naito T, Yano K, Sugimoto S, Morikawa Y, Nagata K (2002) Identification of Hsp90 as a stimulatory host factor involved in influenza virus RNA synthesis. J Biol Chem 277:45306–45314CrossRefPubMed
58.
go back to reference Muchowski PJ, Wacker JL (2005) Modulation of neurodegeneration by molecular chaperones. Nat Rev Neurosci 6:11–22CrossRefPubMed Muchowski PJ, Wacker JL (2005) Modulation of neurodegeneration by molecular chaperones. Nat Rev Neurosci 6:11–22CrossRefPubMed
59.
go back to reference Naito T, Momose F, Kawaguchi A, Nagata K (2007) Involvement of Hsp90 in assembly and nuclear import of influenza virus RNA polymerase subunits. J Virol 81:1339–1349CrossRefPubMed Naito T, Momose F, Kawaguchi A, Nagata K (2007) Involvement of Hsp90 in assembly and nuclear import of influenza virus RNA polymerase subunits. J Virol 81:1339–1349CrossRefPubMed
60.
go back to reference Neckers L, Tatu U (2008) Molecular chaperones in pathogen virulence: emerging new targets for therapy. Cell Host Microbe 4:519–527CrossRefPubMed Neckers L, Tatu U (2008) Molecular chaperones in pathogen virulence: emerging new targets for therapy. Cell Host Microbe 4:519–527CrossRefPubMed
61.
go back to reference Ni M, Lee AS (2007) ER chaperones in mammalian development and human diseases. FEBS Lett 581:3641–3651CrossRefPubMed Ni M, Lee AS (2007) ER chaperones in mammalian development and human diseases. FEBS Lett 581:3641–3651CrossRefPubMed
62.
go back to reference Okamoto T, Nishimura Y, Ichimura T, Suzuki K, Miyamura T, Suzuki T, Moriishi K, Matsuura Y (2006) Hepatitis C virus RNA replication is regulated by FKBP8 and Hsp90. EMBO J 25:5015–5025CrossRefPubMed Okamoto T, Nishimura Y, Ichimura T, Suzuki K, Miyamura T, Suzuki T, Moriishi K, Matsuura Y (2006) Hepatitis C virus RNA replication is regulated by FKBP8 and Hsp90. EMBO J 25:5015–5025CrossRefPubMed
63.
go back to reference Pack CD, Kumaraguru U, Suvas S, Rouse BT (2005) Heat-shock protein 70 acts as an effective adjuvant in neonatal mice and confers protection against challenge with herpes simplex virus. Vaccine 23:3526–3534CrossRefPubMed Pack CD, Kumaraguru U, Suvas S, Rouse BT (2005) Heat-shock protein 70 acts as an effective adjuvant in neonatal mice and confers protection against challenge with herpes simplex virus. Vaccine 23:3526–3534CrossRefPubMed
64.
go back to reference Pack CD, Gierynska M, Rouse BT (2008) An intranasal heat shock protein based vaccination strategy confers protection against mucosal challenge with herpes simplex virus. Hum Vaccin 4:360–364PubMed Pack CD, Gierynska M, Rouse BT (2008) An intranasal heat shock protein based vaccination strategy confers protection against mucosal challenge with herpes simplex virus. Hum Vaccin 4:360–364PubMed
65.
go back to reference Park SG, Jung G (2001) Human hepatitis B virus polymerase interacts with the molecular chaperonin Hsp60. J Virol 75:6962–6968CrossRefPubMed Park SG, Jung G (2001) Human hepatitis B virus polymerase interacts with the molecular chaperonin Hsp60. J Virol 75:6962–6968CrossRefPubMed
66.
go back to reference Park SG, Lee SM, Jung G (2003) Antisense oligodeoxynucleotides targeted against molecular chaperonin Hsp60 block human hepatitis B virus replication. J Biol Chem 278:39851–39857CrossRefPubMed Park SG, Lee SM, Jung G (2003) Antisense oligodeoxynucleotides targeted against molecular chaperonin Hsp60 block human hepatitis B virus replication. J Biol Chem 278:39851–39857CrossRefPubMed
67.
go back to reference Peng M, Chen M, Ling N, Xu H, Qing Y, Ren H (2006) Novel vaccines for the treatment of chronic HBV infection based on mycobacterial heat shock protein 70. Vaccine 24:887–896CrossRefPubMed Peng M, Chen M, Ling N, Xu H, Qing Y, Ren H (2006) Novel vaccines for the treatment of chronic HBV infection based on mycobacterial heat shock protein 70. Vaccine 24:887–896CrossRefPubMed
68.
go back to reference Perez-Vargas J, Romero P, Lopez S, Arias CF (2006) The peptide-binding and ATPase domains of recombinant hsc70 are required to interact with rotavirus and reduce its infectivity. J Virol 80:3322–3331CrossRefPubMed Perez-Vargas J, Romero P, Lopez S, Arias CF (2006) The peptide-binding and ATPase domains of recombinant hsc70 are required to interact with rotavirus and reduce its infectivity. J Virol 80:3322–3331CrossRefPubMed
69.
go back to reference Pockley AG, Muthana M, Calderwood SK (2008) The dual immunoregulatory roles of stress proteins. Trends Biochem Sci 33:71–79PubMed Pockley AG, Muthana M, Calderwood SK (2008) The dual immunoregulatory roles of stress proteins. Trends Biochem Sci 33:71–79PubMed
70.
go back to reference Prange R, Werr M, Loffler-Mary H (1999) Chaperones involved in hepatitis B virus morphogenesis. Biol Chem 380:305–314CrossRefPubMed Prange R, Werr M, Loffler-Mary H (1999) Chaperones involved in hepatitis B virus morphogenesis. Biol Chem 380:305–314CrossRefPubMed
71.
go back to reference Rainey-Barger EK, Magnuson B, Tsai B (2007) A chaperone-activated nonenveloped virus perforates the physiologically relevant endoplasmic reticulum membrane. J Virol 81:12996–13004CrossRefPubMed Rainey-Barger EK, Magnuson B, Tsai B (2007) A chaperone-activated nonenveloped virus perforates the physiologically relevant endoplasmic reticulum membrane. J Virol 81:12996–13004CrossRefPubMed
72.
go back to reference Ramalanjaona N, de Rocquigny H, Millet A, Ficheux D, Darlix JL, Mely Y (2007) Investigating the mechanism of the nucleocapsid protein chaperoning of the second strand transfer during HIV-1 DNA synthesis. J Mol Biol 374:1041–1053CrossRefPubMed Ramalanjaona N, de Rocquigny H, Millet A, Ficheux D, Darlix JL, Mely Y (2007) Investigating the mechanism of the nucleocapsid protein chaperoning of the second strand transfer during HIV-1 DNA synthesis. J Mol Biol 374:1041–1053CrossRefPubMed
73.
go back to reference Reyes-Del Valle J, Chavez-Salinas S, Medina F, Del Angel RM (2005) Heat shock protein 90 and heat shock protein 70 are components of dengue virus receptor complex in human cells. J Virol 79:4557–4567CrossRefPubMed Reyes-Del Valle J, Chavez-Salinas S, Medina F, Del Angel RM (2005) Heat shock protein 90 and heat shock protein 70 are components of dengue virus receptor complex in human cells. J Virol 79:4557–4567CrossRefPubMed
74.
go back to reference Schelhaas M, Malmstrom J, Pelkmans L, Haugstetter J, Ellgaard L, Grunewald K, Helenius A (2007) Simian Virus 40 depends on ER protein folding and quality control factors for entry into host cells. Cell 131:516–529CrossRefPubMed Schelhaas M, Malmstrom J, Pelkmans L, Haugstetter J, Ellgaard L, Grunewald K, Helenius A (2007) Simian Virus 40 depends on ER protein folding and quality control factors for entry into host cells. Cell 131:516–529CrossRefPubMed
75.
go back to reference Spence SL, Pipas JM (1994) SV40 large T antigen functions at two distinct steps in virion assembly. Virology 204:200–209CrossRefPubMed Spence SL, Pipas JM (1994) SV40 large T antigen functions at two distinct steps in virion assembly. Virology 204:200–209CrossRefPubMed
76.
go back to reference Stahl M, Retzlaff M, Nassal M, Beck J (2007) Chaperone activation of the hepadnaviral reverse transcriptase for template RNA binding is established by the Hsp70 and stimulated by the Hsp90 system. Nucleic Acids Res 35:6124–6136CrossRefPubMed Stahl M, Retzlaff M, Nassal M, Beck J (2007) Chaperone activation of the hepadnaviral reverse transcriptase for template RNA binding is established by the Hsp70 and stimulated by the Hsp90 system. Nucleic Acids Res 35:6124–6136CrossRefPubMed
77.
go back to reference Streblow DN, Kitabwalla M, Malkovsky M, Pauza CD (1998) Cyclophilin a modulates processing of human immunodeficiency virus type 1 p55Gag: mechanism for antiviral effects of cyclosporin A. Virology 245:197–202CrossRefPubMed Streblow DN, Kitabwalla M, Malkovsky M, Pauza CD (1998) Cyclophilin a modulates processing of human immunodeficiency virus type 1 p55Gag: mechanism for antiviral effects of cyclosporin A. Virology 245:197–202CrossRefPubMed
79.
go back to reference Sullivan CS, Pipas JM (2002) T antigens of simian virus 40: molecular chaperones for viral replication and tumorigenesis. Microbiol Mol Biol Rev 66:179–202CrossRefPubMed Sullivan CS, Pipas JM (2002) T antigens of simian virus 40: molecular chaperones for viral replication and tumorigenesis. Microbiol Mol Biol Rev 66:179–202CrossRefPubMed
80.
go back to reference Suzuki H (1996) A hypothesis about the mechanism of assembly of double-shelled rotavirus particles. Arch Virol Suppl 12:79–85PubMed Suzuki H (1996) A hypothesis about the mechanism of assembly of double-shelled rotavirus particles. Arch Virol Suppl 12:79–85PubMed
81.
go back to reference Tanaka Y, Kanai F, Kawakami T, Tateishi K, Ijichi H, Kawabe T, Arakawa Y, Nishimura T, Shirakata Y, Koike K, Omata M (2004) Interaction of the hepatitis B virus X protein (HBx) with heat shock protein 60 enhances HBx-mediated apoptosis. Biochem Biophys Res Commun 318:461–469CrossRefPubMed Tanaka Y, Kanai F, Kawakami T, Tateishi K, Ijichi H, Kawabe T, Arakawa Y, Nishimura T, Shirakata Y, Koike K, Omata M (2004) Interaction of the hepatitis B virus X protein (HBx) with heat shock protein 60 enhances HBx-mediated apoptosis. Biochem Biophys Res Commun 318:461–469CrossRefPubMed
82.
go back to reference Thomas JA, Bosche WJ, Shatzer TL, Johnson DG, Gorelick RJ (2008) Mutations in human immunodeficiency virus type 1 nucleocapsid protein zinc fingers cause premature reverse transcription. J Virol 82:9318–9328CrossRefPubMed Thomas JA, Bosche WJ, Shatzer TL, Johnson DG, Gorelick RJ (2008) Mutations in human immunodeficiency virus type 1 nucleocapsid protein zinc fingers cause premature reverse transcription. J Virol 82:9318–9328CrossRefPubMed
83.
go back to reference Thomas JA, Gorelick RJ (2008) Nucleocapsid protein function in early infection processes. Virus Res 134:39–63CrossRefPubMed Thomas JA, Gorelick RJ (2008) Nucleocapsid protein function in early infection processes. Virus Res 134:39–63CrossRefPubMed
84.
go back to reference Triantafilou K, Fradelizi D, Wilson K, Triantafilou M (2002) GRP78, a coreceptor for coxsackievirus A9, interacts with major histocompatibility complex class I molecules which mediate virus internalization. J Virol 76:633–643CrossRefPubMed Triantafilou K, Fradelizi D, Wilson K, Triantafilou M (2002) GRP78, a coreceptor for coxsackievirus A9, interacts with major histocompatibility complex class I molecules which mediate virus internalization. J Virol 76:633–643CrossRefPubMed
85.
go back to reference Ujino S, Yamaguchi S, Shimotohno K, Takaku H (2009) Heat-shock protein 90 is essential for stabilization of the hepatitis C virus nonstructural protein NS3. J Biol Chem 284:6841–6846CrossRefPubMed Ujino S, Yamaguchi S, Shimotohno K, Takaku H (2009) Heat-shock protein 90 is essential for stabilization of the hepatitis C virus nonstructural protein NS3. J Biol Chem 284:6841–6846CrossRefPubMed
86.
go back to reference Waxman L, Whitney M, Pollok BA, Kuo LC, Darke PL (2001) Host cell factor requirement for hepatitis C virus enzyme maturation. Proc Natl Acad Sci USA 98:13931–13935CrossRefPubMed Waxman L, Whitney M, Pollok BA, Kuo LC, Darke PL (2001) Host cell factor requirement for hepatitis C virus enzyme maturation. Proc Natl Acad Sci USA 98:13931–13935CrossRefPubMed
87.
go back to reference Wright CM, Seguin SP, Fewell SW, Zhang H, Ishwad C, Vats A, Lingwood CA, Wipf P, Fanning E, Pipas JM, Brodsky JL (2009) Inhibition of Simian Virus 40 replication by targeting the molecular chaperone function and ATPase activity of T antigen. Virus Res 141:71–80CrossRefPubMed Wright CM, Seguin SP, Fewell SW, Zhang H, Ishwad C, Vats A, Lingwood CA, Wipf P, Fanning E, Pipas JM, Brodsky JL (2009) Inhibition of Simian Virus 40 replication by targeting the molecular chaperone function and ATPase activity of T antigen. Virus Res 141:71–80CrossRefPubMed
88.
go back to reference Young P, Anderton E, Paschos K, White R, Allday MJ (2008) Epstein-Barr virus nuclear antigen (EBNA) 3A induces the expression of and interacts with a subset of chaperones and co-chaperones. J Gen Virol 89:866–877CrossRefPubMed Young P, Anderton E, Paschos K, White R, Allday MJ (2008) Epstein-Barr virus nuclear antigen (EBNA) 3A induces the expression of and interacts with a subset of chaperones and co-chaperones. J Gen Virol 89:866–877CrossRefPubMed
89.
go back to reference Zarate S, Cuadras MA, Espinosa R, Romero P, Juarez KO, Camacho-Nuez M, Arias CF, Lopez S (2003) Interaction of rotaviruses with Hsc70 during cell entry is mediated by VP5. J Virol 77:7254–7260CrossRefPubMed Zarate S, Cuadras MA, Espinosa R, Romero P, Juarez KO, Camacho-Nuez M, Arias CF, Lopez S (2003) Interaction of rotaviruses with Hsc70 during cell entry is mediated by VP5. J Virol 77:7254–7260CrossRefPubMed
90.
go back to reference Zhu XD, Li CL, Lang ZW, Gao GF, Tien P (2004) Significant correlation between expression level of HSP gp96 and progression of hepatitis B virus induced diseases. World J Gastroenterol 10:1141–1145PubMed Zhu XD, Li CL, Lang ZW, Gao GF, Tien P (2004) Significant correlation between expression level of HSP gp96 and progression of hepatitis B virus induced diseases. World J Gastroenterol 10:1141–1145PubMed
91.
go back to reference Zuniga S, Sola I, Cruz JL, Enjuanes L (2009) Role of RNA chaperones in virus replication. Virus Res 139:253–266CrossRefPubMed Zuniga S, Sola I, Cruz JL, Enjuanes L (2009) Role of RNA chaperones in virus replication. Virus Res 139:253–266CrossRefPubMed
Metadata
Title
Viral interaction with molecular chaperones: role in regulating viral infection
Authors
Allen Xiao
Jerry Wong
Honglin Luo
Publication date
01-07-2010
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 7/2010
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-010-0691-3

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