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

Journal of Virology

Volumn 77, Issue 3, 2003, Pages 1672-1681

  Mannová, Petra ^a   Forstová, Jitka ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BREFELDIN A; CAPSID PROTEIN; CHOLERA TOXIN B SUBUNIT; COAT PROTEIN COMPLEX I; GENOMIC DNA; GLYCOPROTEIN; GUANOSINE TRIPHOSPHATASE; PROTEIN VP1; RAB PROTEIN; TRANSFERRIN;

ARTICLE; CELL MEMBRANE; CELL NUCLEUS; CELLULAR DISTRIBUTION; ENDOPLASMIC RETICULUM; ENDOSOME; FIBROBLAST; IN SITU HYBRIDIZATION; INTERNALIZATION; INTRACELLULAR TRANSPORT; NONHUMAN; POLYOMA VIRUS; PRIORITY JOURNAL; SIMIAN VIRUS 40; VIRUS ENVELOPE; VIRUS INFECTION; VIRUS PARTICLE;

ANIMALS; BIOLOGICAL TRANSPORT; BREFELDIN A; CAPSID PROTEINS; CARRIER PROTEINS; CELL NUCLEUS; COATOMER PROTEIN; COP-COATED VESICLES; ENDOSOMES; HEAT-SHOCK PROTEINS; LYSOSOMES; MICE; MOLECULAR CHAPERONES; POLYOMAVIRUS; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; VIRION;

EID: 0037303397     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.3.1672-1681.2003     Document Type: Article

References (50)

1. 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.
2. 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.
3. 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.
4. Barouch, D. H., and S. C. Harrison. 1994. Interactions among the major and minor coat proteins of polyomavirus. J. Virol. 68:3982-3989.
5. 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.
6. 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.
7. 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.
8. 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.
9. Dilworth, S. M., and B. E. Griffin. 1982. Monoclonal antibodies against polyomavirus virus tumor antigens. Proc. Natl. Acad. Sci. USA 79:1059-1063.
10. 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.
11. Gilbert, J. M., and T. L. Benjamin. 2000. Early steps of polyomavirus entry into cells. J. Virol. 74:8582-8588.
12. 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.
13. 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.
14. 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.
15. 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.
16. 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.
17. 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.
18. Joki-Korpela, P., V. Marjomaki, C. Krogerus, J. Heino, and T. Hyypia. 2001. Entry of human parechovirus 1. J. Virol. 75:1958-1967.
19. Kartenbeck, J., H. Stukenbrok, and A. Helenius. 1989. Endocytosis of simian virus 40 into the endoplasmic reticulum. J. Cell Biol. 109:2721-2729.
20. 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.
21. 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.
22. 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.
23. 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.
24. 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.
25. Mackay, R. L., and R. A. Consigli. 1976. Early events in polyomavirus virus infection: attachment, penetration, and nuclear entry. J. Virol. 19:620-636.
26. 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.
27. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
28. Mayor, S., S. Sabharanjak, and F. R. Maxfield. 1998. Cholesterol-dependent retention of GPI-anchored proteins in endosomes. EMBO J. 17:4626-4638.
29. Norkin, L. C. 1999. Simian virus 40 infection via major histocompatibility complex class I molecules and caveolae. Immunol. Rev. 168:13-22.
30. 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.
31. 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.
32. 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.
33. 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.
34. Pelkmans, L., D. Püntener, and A. Helenius. 2002. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 296:535-539.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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 VPI pseudocapsids toward cell nuclei. J. Virol. 75:10880-10891.
41. 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.
42. 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.
43. Somsel Rodman, J., and A. Wandinger-Ness. 2000. Rab GTPases coordinate endocytosis. J. Cell Sci. 113:183-192.
44. 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.
45. Stehle, T., and S. C. Harrison. 1996. Crystal structures of murine polyoma-virus in complex with straight-chain and branched-chain sialyloligosaccharide receptor fragments. Structure 4:183-194.
46. 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.
47. 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.
48. 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.
49. 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.
50. 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.