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Published in: Virology Journal 1/2011

Open Access 01-12-2011 | Research

Viral and cellular requirements for the budding of Feline Endogenous Retrovirus RD-114

Authors: Aiko Fukuma, Masumi Abe, Shuzo Urata, Rokusuke Yoshikawa, Yuko Morikawa, Takayuki Miyazawa, Jiro Yasuda

Published in: Virology Journal | Issue 1/2011

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Abstract

Background

RD-114 virus is a feline endogenous retrovirus and produced as infectious viruses in some feline cell lines. Recently, we reported the contamination of an infectious RD-114 virus in a proportion of live attenuated vaccines for dogs and cats. It is very difficult to completely knock out the RD-114 proviruses from cells, as endogenous retroviruses are usually integrated multiply into the host genome. However, it may be possible to reduce the risk of contamination of RD-114 virus by regulating the viral release from cells.

Results

In this study, to understand the molecular mechanism of RD-114 virus budding, we attempted to identify the viral and cellular requirements for RD-114 virus budding. Analyses of RD-114 L-domain mutants showed that the PPPY sequence in the pp15 region of Gag plays a critical role in RD-114 virus release as viral L-domain. Furthermore, we investigated the cellular factors required for RD-114 virus budding. We demonstrated that RD-114 virus release was inhibited by overexpression of dominant negative mutants of Vps4A, Vps4B, and WWP2.

Conclusions

These results strongly suggest that RD-114 budding utilizes the cellular multivesicular body sorting pathway similar to many other retroviruses.
Appendix
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Literature
1.
go back to reference Fischinger PJ, Peebles PT, Nomura S, Haapala DK: Isolation of RD-114-like oncornavirus from a cat cell line. J Virol 1973, 11: 978-985.PubMedCentralPubMed Fischinger PJ, Peebles PT, Nomura S, Haapala DK: Isolation of RD-114-like oncornavirus from a cat cell line. J Virol 1973, 11: 978-985.PubMedCentralPubMed
2.
go back to reference McAllister RM, Nicolson M, Gardner MB, Rongey RW, Rasheed S, Sarma PS, Huebner RJ, Hatanaka M, Oroszlan S, Gilden RV, et al.: C-type virus released from cultured human rhabdomyosarcoma cells. Nat New Biol 1972, 235: 3-6.CrossRefPubMed McAllister RM, Nicolson M, Gardner MB, Rongey RW, Rasheed S, Sarma PS, Huebner RJ, Hatanaka M, Oroszlan S, Gilden RV, et al.: C-type virus released from cultured human rhabdomyosarcoma cells. Nat New Biol 1972, 235: 3-6.CrossRefPubMed
3.
go back to reference Okabe H, Gilden RV, Hatanaka M: RD 114 virus-specific sequences in feline cellular RNA: detection and characterization. J Virol 1973, 12: 984-994.PubMedCentralPubMed Okabe H, Gilden RV, Hatanaka M: RD 114 virus-specific sequences in feline cellular RNA: detection and characterization. J Virol 1973, 12: 984-994.PubMedCentralPubMed
4.
go back to reference van der Kuyl AC, Dekker JT, Goudsmit J: Discovery of a new endogenous type C retrovirus (FcEV) in cats: evidence for RD-114 being an FcEV(Gag-Pol)/baboon endogenous virus BaEV(Env) recombinant. J Virol 1999, 73: 7994-8002.PubMedCentralPubMed van der Kuyl AC, Dekker JT, Goudsmit J: Discovery of a new endogenous type C retrovirus (FcEV) in cats: evidence for RD-114 being an FcEV(Gag-Pol)/baboon endogenous virus BaEV(Env) recombinant. J Virol 1999, 73: 7994-8002.PubMedCentralPubMed
5.
go back to reference Okada M, Yoshikawa R, Shojima T, Baba K, Miyazawa T: Susceptibility and production of a feline endogenous retrovirus (RD-114 virus) in various feline cell lines. Virus Res 2011, 155: 268-273. 10.1016/j.virusres.2010.10.020CrossRefPubMed Okada M, Yoshikawa R, Shojima T, Baba K, Miyazawa T: Susceptibility and production of a feline endogenous retrovirus (RD-114 virus) in various feline cell lines. Virus Res 2011, 155: 268-273. 10.1016/j.virusres.2010.10.020CrossRefPubMed
6.
go back to reference Baumann JG, Gunzburg WH, Salmons B: CrFK feline kidney cells produce an RD114-like endogenous virus that can package murine leukemia virus-based vectors. J Virol 1998, 72: 7685-7687.PubMedCentralPubMed Baumann JG, Gunzburg WH, Salmons B: CrFK feline kidney cells produce an RD114-like endogenous virus that can package murine leukemia virus-based vectors. J Virol 1998, 72: 7685-7687.PubMedCentralPubMed
7.
go back to reference Miyazawa T: Endogenous retroviruses as potential hazards for vaccines. Biologicals: J Int Assoc Biol Standardization 2010, 38: 371-376.CrossRef Miyazawa T: Endogenous retroviruses as potential hazards for vaccines. Biologicals: J Int Assoc Biol Standardization 2010, 38: 371-376.CrossRef
8.
go back to reference Miyazawa T, Yoshikawa R, Golder M, Okada M, Stewart H, Palmarini M: Isolation of an infectious endogenous retrovirus in a proportion of live attenuated vaccines for pets. J Virol 2010, 84: 3690-3694. 10.1128/JVI.02715-09PubMedCentralCrossRefPubMed Miyazawa T, Yoshikawa R, Golder M, Okada M, Stewart H, Palmarini M: Isolation of an infectious endogenous retrovirus in a proportion of live attenuated vaccines for pets. J Virol 2010, 84: 3690-3694. 10.1128/JVI.02715-09PubMedCentralCrossRefPubMed
9.
go back to reference Yoshikawa R, Sato E, Miyazawa T: Contamination of infectious RD-114 virus in vaccines produced using non-feline cell lines. Biologicals 2011, 39: 33-37. 10.1016/j.biologicals.2010.11.001CrossRefPubMed Yoshikawa R, Sato E, Miyazawa T: Contamination of infectious RD-114 virus in vaccines produced using non-feline cell lines. Biologicals 2011, 39: 33-37. 10.1016/j.biologicals.2010.11.001CrossRefPubMed
10.
go back to reference Bieniasz PD: Late budding domains and host proteins in enveloped virus release. Virology 2006, 344: 55-63. 10.1016/j.virol.2005.09.044CrossRefPubMed Bieniasz PD: Late budding domains and host proteins in enveloped virus release. Virology 2006, 344: 55-63. 10.1016/j.virol.2005.09.044CrossRefPubMed
11.
go back to reference Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH, Wang HE, Wettstein DA, Stray KM, Cote M, Rich RL, et al.: Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 2001, 107: 55-65. 10.1016/S0092-8674(01)00506-2CrossRefPubMed Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH, Wang HE, Wettstein DA, Stray KM, Cote M, Rich RL, et al.: Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 2001, 107: 55-65. 10.1016/S0092-8674(01)00506-2CrossRefPubMed
12.
go back to reference Kikonyogo A, Bouamr F, Vana ML, Xiang Y, Aiyar A, Carter C, Leis J: Proteins related to the Nedd4 family of ubiquitin protein ligases interact with the L domain of Rous sarcoma virus and are required for gag budding from cells. Proc Natl Acad Sci USA 2001, 98: 11199-11204. 10.1073/pnas.201268998PubMedCentralCrossRefPubMed Kikonyogo A, Bouamr F, Vana ML, Xiang Y, Aiyar A, Carter C, Leis J: Proteins related to the Nedd4 family of ubiquitin protein ligases interact with the L domain of Rous sarcoma virus and are required for gag budding from cells. Proc Natl Acad Sci USA 2001, 98: 11199-11204. 10.1073/pnas.201268998PubMedCentralCrossRefPubMed
13.
go back to reference Martin-Serrano J, Eastman SW, Chung W, Bieniasz PD: HECT ubiquitin ligases link viral and cellular PPXY motifs to the vacuolar protein-sorting pathway. J Cell Biol 2005, 168: 89-101.PubMedCentralCrossRefPubMed Martin-Serrano J, Eastman SW, Chung W, Bieniasz PD: HECT ubiquitin ligases link viral and cellular PPXY motifs to the vacuolar protein-sorting pathway. J Cell Biol 2005, 168: 89-101.PubMedCentralCrossRefPubMed
14.
go back to reference VerPlank L, Bouamr F, LaGrassa TJ, Agresta B, Kikonyogo A, Leis J, Carter CA: Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55(Gag). Proc Natl Acad Sci USA 2001, 98: 7724-7729. 10.1073/pnas.131059198PubMedCentralCrossRefPubMed VerPlank L, Bouamr F, LaGrassa TJ, Agresta B, Kikonyogo A, Leis J, Carter CA: Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55(Gag). Proc Natl Acad Sci USA 2001, 98: 7724-7729. 10.1073/pnas.131059198PubMedCentralCrossRefPubMed
15.
go back to reference Yasuda J, Hunter E, Nakao M, Shida H: Functional involvement of a novel Nedd4-like ubiquitin ligase on retrovirus budding. EMBO Rep 2002, 3: 636-640. 10.1093/embo-reports/kvf132PubMedCentralCrossRefPubMed Yasuda J, Hunter E, Nakao M, Shida H: Functional involvement of a novel Nedd4-like ubiquitin ligase on retrovirus budding. EMBO Rep 2002, 3: 636-640. 10.1093/embo-reports/kvf132PubMedCentralCrossRefPubMed
16.
go back to reference Yasuda J, Nakao M, Kawaoka Y, Shida H: Nedd4 regulates egress of Ebola virus-like particles from host cells. J Virol 2003, 77: 9987-9992. 10.1128/JVI.77.18.9987-9992.2003PubMedCentralCrossRefPubMed Yasuda J, Nakao M, Kawaoka Y, Shida H: Nedd4 regulates egress of Ebola virus-like particles from host cells. J Virol 2003, 77: 9987-9992. 10.1128/JVI.77.18.9987-9992.2003PubMedCentralCrossRefPubMed
17.
go back to reference Strack B, Calistri A, Craig S, Popova E, Gottlinger HG: AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 2003, 114: 689-699. 10.1016/S0092-8674(03)00653-6CrossRefPubMed Strack B, Calistri A, Craig S, Popova E, Gottlinger HG: AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 2003, 114: 689-699. 10.1016/S0092-8674(03)00653-6CrossRefPubMed
18.
go back to reference Eastman SW, Martin-Serrano J, Chung W, Zang T, Bieniasz PD: Identification of human VPS37C, a component of endosomal sorting complex required for transport-I important for viral budding. J Biol Chem 2005, 280: 628-636.CrossRefPubMed Eastman SW, Martin-Serrano J, Chung W, Zang T, Bieniasz PD: Identification of human VPS37C, a component of endosomal sorting complex required for transport-I important for viral budding. J Biol Chem 2005, 280: 628-636.CrossRefPubMed
19.
go back to reference Martin-Serrano J, Yarovoy A, Perez-Caballero D, Bieniasz PD: Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Proc Natl Acad Sci USA 2003, 100: 12414-12419. 10.1073/pnas.2133846100PubMedCentralCrossRefPubMed Martin-Serrano J, Yarovoy A, Perez-Caballero D, Bieniasz PD: Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Proc Natl Acad Sci USA 2003, 100: 12414-12419. 10.1073/pnas.2133846100PubMedCentralCrossRefPubMed
20.
go back to reference Stuchell MD, Garrus JE, Muller B, Stray KM, Ghaffarian S, McKinnon R, Krausslich HG, Morham SG, Sundquist WI: The human endosomal sorting complex required for transport (ESCRT-I) and its role in HIV-1 budding. J Biol Chem 2004, 279: 36059-36071. 10.1074/jbc.M405226200CrossRefPubMed Stuchell MD, Garrus JE, Muller B, Stray KM, Ghaffarian S, McKinnon R, Krausslich HG, Morham SG, Sundquist WI: The human endosomal sorting complex required for transport (ESCRT-I) and its role in HIV-1 budding. J Biol Chem 2004, 279: 36059-36071. 10.1074/jbc.M405226200CrossRefPubMed
21.
go back to reference Hurley JH, Emr SD: The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu Rev Biophys Biomol Struct 2006, 35: 277-298. 10.1146/annurev.biophys.35.040405.102126PubMedCentralCrossRefPubMed Hurley JH, Emr SD: The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu Rev Biophys Biomol Struct 2006, 35: 277-298. 10.1146/annurev.biophys.35.040405.102126PubMedCentralCrossRefPubMed
22.
go back to reference Xu HM, Liao B, Zhang QJ, Wang BB, Li H, Zhong XM, Sheng HZ, Zhao YX, Zhao YM, Jin Y: Wwp2, an E3 ubiquitin ligase that targets transcription factor Oct-4 for ubiquitination. J Biol Chem 2004, 279: 23495-23503. 10.1074/jbc.M400516200CrossRefPubMed Xu HM, Liao B, Zhang QJ, Wang BB, Li H, Zhong XM, Sheng HZ, Zhao YX, Zhao YM, Jin Y: Wwp2, an E3 ubiquitin ligase that targets transcription factor Oct-4 for ubiquitination. J Biol Chem 2004, 279: 23495-23503. 10.1074/jbc.M400516200CrossRefPubMed
23.
go back to reference Yeom YI, Fuhrmann G, Ovitt CE, Brehm A, Ohbo K, Gross M, Hubner K, Scholer HR: Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells. Development 1996, 122: 881-894.PubMed Yeom YI, Fuhrmann G, Ovitt CE, Brehm A, Ohbo K, Gross M, Hubner K, Scholer HR: Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells. Development 1996, 122: 881-894.PubMed
24.
go back to reference Chen A, Gao B, Zhang J, McEwen T, Ye SQ, Zhang D, Fang D: The HECT-type E3 ubiquitin ligase AIP2 inhibits activation-induced T-cell death by catalyzing EGR2 ubiquitination. Mol Cell Biol 2009, 29: 5348-5356. 10.1128/MCB.00407-09PubMedCentralCrossRefPubMed Chen A, Gao B, Zhang J, McEwen T, Ye SQ, Zhang D, Fang D: The HECT-type E3 ubiquitin ligase AIP2 inhibits activation-induced T-cell death by catalyzing EGR2 ubiquitination. Mol Cell Biol 2009, 29: 5348-5356. 10.1128/MCB.00407-09PubMedCentralCrossRefPubMed
25.
go back to reference Urata S, Yasuda J: Regulation of Marburg virus (MARV) budding by Nedd4.1: a different WW domain of Nedd4.1 is critical for binding to MARV and Ebola virus VP40. J Gen Virol 2010, 91: 228-234. 10.1099/vir.0.015495-0CrossRefPubMed Urata S, Yasuda J: Regulation of Marburg virus (MARV) budding by Nedd4.1: a different WW domain of Nedd4.1 is critical for binding to MARV and Ebola virus VP40. J Gen Virol 2010, 91: 228-234. 10.1099/vir.0.015495-0CrossRefPubMed
26.
go back to reference Kolesnikova L, Strecker T, Morita E, Zielecki F, Mittler E, Crump C, Becker S: Vacuolar protein sorting pathway contributes to the release of Marburg virus. J Virol 2009, 83: 2327-2337. 10.1128/JVI.02184-08PubMedCentralCrossRefPubMed Kolesnikova L, Strecker T, Morita E, Zielecki F, Mittler E, Crump C, Becker S: Vacuolar protein sorting pathway contributes to the release of Marburg virus. J Virol 2009, 83: 2327-2337. 10.1128/JVI.02184-08PubMedCentralCrossRefPubMed
27.
go back to reference Fukuma A, Abe M, Morikawa Y, Miyazawa T, Yasuda J: Cloning and characterization of the antiviral activity of feline Tetherin/BST-2. PloS one 2011, 6: e18247. 10.1371/journal.pone.0018247PubMedCentralCrossRefPubMed Fukuma A, Abe M, Morikawa Y, Miyazawa T, Yasuda J: Cloning and characterization of the antiviral activity of feline Tetherin/BST-2. PloS one 2011, 6: e18247. 10.1371/journal.pone.0018247PubMedCentralCrossRefPubMed
28.
go back to reference Yoshikawa R, Sato E, Igarashi T, Miyazawa T: Characterization of RD-114 virus isolated from a commercial canine vaccine manufactured using CRFK cells. J Clin Microbiol 2010, 48: 3366-3369. 10.1128/JCM.00992-10PubMedCentralCrossRefPubMed Yoshikawa R, Sato E, Igarashi T, Miyazawa T: Characterization of RD-114 virus isolated from a commercial canine vaccine manufactured using CRFK cells. J Clin Microbiol 2010, 48: 3366-3369. 10.1128/JCM.00992-10PubMedCentralCrossRefPubMed
29.
go back to reference Urata S, Noda T, Kawaoka Y, Yokosawa H, Yasuda J: Cellular factors required for Lassa virus budding. J Virol 2006, 80: 4191-4195. 10.1128/JVI.80.8.4191-4195.2006PubMedCentralCrossRefPubMed Urata S, Noda T, Kawaoka Y, Yokosawa H, Yasuda J: Cellular factors required for Lassa virus budding. J Virol 2006, 80: 4191-4195. 10.1128/JVI.80.8.4191-4195.2006PubMedCentralCrossRefPubMed
30.
go back to reference Yasuda J, Hunter E: A proline-rich motif (PPPY) in the Gag polyprotein of Mason-Pfizer monkey virus plays a maturation-independent role in virion release. J Virol 1998, 72: 4095-4103.PubMedCentralPubMed Yasuda J, Hunter E: A proline-rich motif (PPPY) in the Gag polyprotein of Mason-Pfizer monkey virus plays a maturation-independent role in virion release. J Virol 1998, 72: 4095-4103.PubMedCentralPubMed
31.
go back to reference Sakuma T, Noda T, Urata S, Kawaoka Y, Yasuda J: Inhibition of Lassa and Marburg virus production by tetherin. J Virol 2009, 83: 2382-2385. 10.1128/JVI.01607-08PubMedCentralCrossRefPubMed Sakuma T, Noda T, Urata S, Kawaoka Y, Yasuda J: Inhibition of Lassa and Marburg virus production by tetherin. J Virol 2009, 83: 2382-2385. 10.1128/JVI.01607-08PubMedCentralCrossRefPubMed
32.
go back to reference Urata S, Noda T, Kawaoka Y, Morikawa S, Yokosawa H, Yasuda J: Interaction of Tsg101 with Marburg virus VP40 depends on the PPPY motif, but not the PT/SAP motif as in the case of Ebola virus, and Tsg101 plays a critical role in the budding of Marburg virus-like particles induced by VP40, NP, and GP. J Virol 2007, 81: 4895-4899. 10.1128/JVI.02829-06PubMedCentralCrossRefPubMed Urata S, Noda T, Kawaoka Y, Morikawa S, Yokosawa H, Yasuda J: Interaction of Tsg101 with Marburg virus VP40 depends on the PPPY motif, but not the PT/SAP motif as in the case of Ebola virus, and Tsg101 plays a critical role in the budding of Marburg virus-like particles induced by VP40, NP, and GP. J Virol 2007, 81: 4895-4899. 10.1128/JVI.02829-06PubMedCentralCrossRefPubMed
33.
go back to reference Sakaguchi S, Baba K, Ishikawa M, Yoshikawa R, Shojima T, Miyazawa T: Focus assay on RD114 virus in QN10S cells. J Vet Med Sci 2008, 70: 1383-1386. 10.1292/jvms.70.1383CrossRefPubMed Sakaguchi S, Baba K, Ishikawa M, Yoshikawa R, Shojima T, Miyazawa T: Focus assay on RD114 virus in QN10S cells. J Vet Med Sci 2008, 70: 1383-1386. 10.1292/jvms.70.1383CrossRefPubMed
Metadata
Title
Viral and cellular requirements for the budding of Feline Endogenous Retrovirus RD-114
Authors
Aiko Fukuma
Masumi Abe
Shuzo Urata
Rokusuke Yoshikawa
Yuko Morikawa
Takayuki Miyazawa
Jiro Yasuda
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2011
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-8-540

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