Mouse polyomavirus utilizes recycling endosomes for a traffic pathway independent of COPI vesicle transport

. 2003 Feb ; 77 (3) : 1672-81.

Jazyk angličtina Země Spojené státy americké Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid12525601

Mouse polyomavirus enters host cells internalized, similar to simian virus 40 (SV40), in smooth monopinocytic vesicles, the movement of which is associated with transient actin disorganization. The major capsid protein (VP1) of the incoming polyomavirus accumulates on membranes around the cell nucleus. Here we show that unlike SV40, mouse polyomavirus infection is not substantially inhibited by brefeldin A, and colocalization of VP1 with beta-COP during early stages of polyomavirus infection in mouse fibroblasts was observed only rarely. Thus, these viruses obviously use different traffic routes from the plasma membrane toward the cell nucleus. At approximately 3 h postinfection, a part of VP1 colocalized with the endoplasmic reticulum marker BiP, and a subpopulation of virus was found in perinuclear areas associated with Rab11 GTPase and colocalized with transferrin, a marker of recycling endosomes. Earlier postinfection, a minor subpopulation of virions was found to be associated with Rab5, known to be connected with early endosomes, but the cell entry of virus was slower than that of transferrin or cholera toxin B-fragment. Neither Rab7, a marker of late endosomes, nor LAMP-2 lysosomal glycoprotein was found to colocalize with polyomavirus. In situ hybridization with polyomavirus genome-specific fluorescent probes clearly demonstrated that, regardless of the multiplicity of infection, only a few virions delivered their genomic DNA into the cell nucleus, while the majority of viral genomes (and VP1) moved back from the proximity of the nucleus to the cytosol, apparently for their degradation.

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Anderson, H. A., Y. Chen, and L. C. Norkin. 1996. Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Mol. Biol. Cell 11:1825-1834. PubMed PMC

Anderson, H. A., Y. Chen, and L. C. Norkin. 1998. Major histocompatibility complex class I molecules are enriched in caveolae but do not enter with simian virus 40. J. Gen. Virol. 79:1469-1477. PubMed

Atwood, W. J., and L. C. Norkin. 1989. Class I major histocompatibility proteins as cell surface receptors for simian virus 40. J. Virol. 63:4474-4477. PubMed PMC

Barouch, D. H., and S. C. Harrison. 1994. Interactions among the major and minor coat proteins of polyomavirus. J. Virol. 68:3982-3989. PubMed PMC

Bartlett, J. S., R. Wilcher, and R. J. Samulski. 2000. Infectious entry pathway of adeno-associated virus and adeno-associated virus vectors. J. Virol. 74:2777-2785. PubMed PMC

Brady, J. N., V. D. Winston, and R. A. Consigli. 1978. Characterization of DNA polyomavirus by treatment with ethylene glycol-bis-N,N′-tetraacetic acid and dithiothreitol. J. Virol. 27:193-204. PubMed PMC

Chardonnet, Y., and S. Dales. 1970. Early events in the interaction of adenoviruses with HeLa cells. I. Penetration of type 5 and intracellular release of the DNA genome. Virology 40:462-477. PubMed

Deeks, E. D., J. P. Cook, P. J. Day, D. C. Smith, L. M. Roberts, and J. M. Lord. 2002. The low lysine content of ricin A chain reduces the risk of proteolytic degradation after translocation from the endoplasmic reticulum to the cytosol. Biochemistry 41:3405-3413. PubMed

Dilworth, S. M., and B. E. Griffin. 1982. Monoclonal antibodies against polyomavirus virus tumor antigens. Proc. Natl. Acad. Sci. USA 79:1059-1063. PubMed PMC

Gagescu, R., N. Demaurex, R. G. Parton, W. Hunziker, L. A. Huber, and J. Gruenberg. 2000. The recycling endosome of Madin-Darby canine kidney cells is a mildly acidic compartment rich in raft components. Mol. Biol. Cell 11:2775-2791. PubMed PMC

Gilbert, J. M., and T. L. Benjamin. 2000. Early steps of polyomavirus entry into cells. J. Virol. 74:8582-8588. PubMed PMC

Girod, A., B. Storrie, J. C. Simpson, L. Johannes, B. Goud, L. M. Roberts, J. M. Lord, T. Nilsson, and R. Pepperkok. 1999. Evidence for a COPI-independent transport route from the Golgi complex to the endoplasmic reticulum. Nat. Cell Biol. 1:423-430. PubMed

Griffith, G. R., and R. A. Consigli. 1984. Isolation and characterization of monopinocytotic vesicles containing polyomavirus from the cytoplasm of infected mouse kidney cells. J. Virol. 50:77-85. PubMed PMC

Griffith, J. P., D. L. Griffith, I. Rayment, W. T. Murakami, and D. L. D. Caspar. 1992. Inside polyomavirus at 25 Å resolution. Nature 355:625-654. PubMed

Griffiths, G., B. Hoflack, K. Simons, I., Mellman, and S. Kornfeld. 1988. The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell 52:329-341. PubMed

Haun, G., O. T. Keppler, C. T. Bock, M. Herrmann, H. Zentgraf, and M. Pawlita. 1993. The cell surface receptor is a major determinant restricting the host range of the B-lymphotropic papovavirus. J. Virol. 67:7482-7492. PubMed PMC

Hummeler, K., N. Tomassini, and F. Sokol. 1970. Morphological aspect of the uptake of simian virus 40 by permissive cells. J. Virol. 6:87-93. PubMed PMC

Joki-Korpela, P., V. Marjomaki, C. Krogerus, J. Heino, and T. Hyypia. 2001. Entry of human parechovirus 1. J. Virol. 75:1958-1967. PubMed PMC

Kartenbeck, J., H. Stukenbrok, and A. Helenius. 1989. Endocytosis of simian virus 40 into the endoplasmic reticulum. J. Cell Biol. 109:2721-2729. PubMed PMC

Krizanova, O., F. Ciampor, and P. Verber. 1982. Influence of chlorpromazine on the replication of influenza virus in chick embryo fibroblasts. Acta Virol. 26:209-216. PubMed

Lencer, W. I. 2001. Microbes, and microbial toxins. Paradigms for microbial-mucosal toxins. V. Cholera: invasion of the intestinal epithelial barrier by a stably folded protein toxin. Am. J. Physiol. Gastrointest. Liver Physiol. 280:G781-G786. PubMed

Lencer, W. I., C. Constable, S. Moe, M. G. Jobling, H. M. Webb, S. Ruston, J. L. Madara, T. R. Hirst, and R. K. Holmes. 1995. Targeting of cholera toxin and Escherichia coli heat-labile toxin in polarized epithelia: role of COOH-terminal KDEL. J. Cell Biol. 131:951-962. PubMed PMC

Lencer, W. I., T. R. Hirst, and R. K. Holmes. 1999. Membrane traffic and the cellular uptake of cholera toxin. Biochim. Biophys. Acta 1450:177-190. PubMed

Lippincott-Schwartz, J., L. Yuan, C. Tipper, M. Amherdt, L. Orci, and R. D. Klausner. 1991. Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell 67:601-616. PubMed

Mackay, R. L., and R. A. Consigli. 1976. Early events in polyomavirus virus infection: attachment, penetration, and nuclear entry. J. Virol. 19:620-636. PubMed PMC

Mallard, F., C. Antony, D. Tenza, J. Salamero, B. Goud, and L. Johannes. 1998. Direct pathway from early/recycling endosomes to the Golgi apparatus revealed through the study of Shiga toxin B-fragment transport. J. Cell Biol. 143:973-990. PubMed PMC

Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.

Mayor, S., S. Sabharanjak, and F. R. Maxfield. 1998. Cholesterol-dependent retention of GPI-anchored proteins in endosomes. EMBO J. 17:4626-4638. PubMed PMC

Norkin, L. C. 1999. Simian virus 40 infection via major histocompatibility complex class I molecules and caveolae. Immunol. Rev. 168:13-22. PubMed

Norkin, L. C., H. A. Anderson, W. A. Scott, and A. Oppenheim. 2002. Caveolar endocytosis of simian virus 40 is followed by brefeldin A-sensitive transport to the endoplasmic reticulum, where the virus disassembles. J. Virol. 76:5156-5166. PubMed PMC

Orlandi, P. A., and P. H. Fishman. 1998. Filipin-dependent inhibition of cholera toxin: evidence for toxin internalisation and activation through caveolae-like domains. J. Cell Biol. 141:905-915. PubMed PMC

Parker, J. S., and C. R. Parrish. 1999. Cellular uptake and infection by canine parvovirus involves dynamin-regulated clathrin-mediated endocytosis, followed by slower intracellular trafficking. J. Virol. 74:1919-1930. PubMed PMC

Pelkmans, L., J. Kartenbeck, and A. Helenius. 2001. Caveolar endocytosis of simian virus 40 reveals a new two step vesicular-transport pathway to the endoplasmic reticulum. Nat. Cell Biol. 3:473-483. PubMed

Pelkmans, L., D. Püntener, and A. Helenius. 2002. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 296:535-539. PubMed

Peter, F., H. Plutner, H. Zhu, T. E. Kreis, and W. E. Balch. 1993. Beta-COP is essential for transport of protein from the endoplasmic reticulum to the Golgi in vitro. J. Cell Biol. 122:1155-1167. PubMed PMC

Pho, M. T., A. Ashok, and W. J. Atwood. 2000. JC virus enters human glial cells by clathrin-dependent receptor-mediated endocytosis. J. Virol. 74:2288-2292. PubMed PMC

Plemper, R. K., and D. H. Wolf. 1999. Retrograde protein translocation: ERADication of secretory proteins in health and disease. Trends Biochem. Sci. 24:266-270. PubMed

Plemper, R. K., S. Bohmler, J. Bordallo, T. Sommer, and D. H. Wolf. 1997. Mutant analysis links the translocon and BiP to retrograde protein transport for endoplasmic reticulum degradation. Nature 388:891-895. PubMed

Richards, A. A., E. Stang, R. Pepperkok, and R. G. Parton. 2002. Inhibitors of COP-mediated transport and cholera toxin action inhibit simian virus 40 infection. Mol. Biol. Cell 13:1750-1764. PubMed PMC

Richterová, Z., D. Liebl, M. Horák, Z. Palková, J. Ŝtokrová, P. Hozák, J. Korb, and J. Forstová. 2001. Caveolae are involved in the trafficking of mouse polyomavirus virions and artificial VP1 pseudocapsids toward cell nuclei. J. Virol. 75:10880-10891. PubMed PMC

Roy, S., R. Luetterforst, A. Harding, A. Apolloni, M. Etheridge, E. Stang, B. Rolls, J. F. Hancock, and R. G. Parton. 1999. Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains. Nat. Cell Biol. 2:98-105. PubMed

Smart, E. J., Y. Yun-Shu, P. A. Conrad, and R. G. W. Anderson. 1994. Caveolin moves from caveolae to the Golgi apparatus in response to cholesterol oxidation. J. Cell Biol. 127:1185-1197. PubMed PMC

Somsel Rodman, J., and A. Wandinger-Ness. 2000. Rab GTPases coordinate endocytosis. J. Cell Sci. 113:183-192. PubMed

Sönnichsen, B., S. De Renzis, E. Nielsen, J. Rietdorf, and M. Zerial. 2000. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol. 149:901-913. PubMed PMC

Stehle, T., and S. C. Harrison. 1996. Crystal structures of murine polyomavirus in complex with straight-chain and branched-chain sialyloligosaccharide receptor fragments. Structure 4:183-194. PubMed

Suikkanen, S., K. Sääjärvi, J. Hirsimäki, O. Välilehto, H. Reunanen, M. Vihinen-Ranta, and M. Vuento. 2002. Role of recycling endosomes and lysosomes in dynein-dependent entry of canine parvovirus. J. Virol. 76:4401-4411. PubMed PMC

Türler, H., and P. Beard. 1985. Simian virus SV40 and polyomavirus: growth, titration, transformation and purification of viral components, p. 169-192. In B. W. J. Mahy (ed.), Virology: a practical approach. IRL Press, Oxford, United Kingdom.

White, J., L. Johannes, F. Mallard, A. Girod, S. Grill, S. Reinsch, P. Keller, B. Tzschaschel, A. Echard, B. Goud, and E. H. K. Stelzer. 1999. Rab6 coordinates a novel Golgi to endoplasmic reticulum retrograde transport pathway in live cells. J. Cell Biol. 147:743-759. PubMed PMC

Wilcke, M., L. Johannes, T. Galli, V. Mayau, B. Goud, and J. Salamero. 2000. Rab11 regulates the compartmentalisation of early endosomes required for efficient transport from early endosomes to the trans-Golgi network. J. Cell Biol. 151:1207-1220. PubMed PMC

Yamashiro, D. J., and F. R. Maxfield. 1987. Acidification of morphologically distinct endosomes in mutant and wild-type Chinese hamster ovary cells. J. Cell Biol. 105:2723-2733. PubMed PMC

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