Inhibition of cellular protein secretion by norwalk virus nonstructural protein p22 requires a mimic of an endoplasmic reticulum export signal

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Sharp, Tyler M ^a,c   Guix, Susana ^a,d   Katayama, Kazuhiko ^a,b   Crawford, Sue E ^a   Estes, Mary K ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^d UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; CELL PROTEIN; COAT PROTEIN COMPLEX II; PROTEIN VP22; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CELL METABOLISM; CONTROLLED STUDY; DRUG DESIGN; DRUG TARGETING; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM EXPORT SIGNAL; GOLGI COMPLEX; HUMAN; HUMAN CELL; NOROVIRUS; PATHOGENESIS; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; VIRUS REPLICATION; ELECTRON MICROSCOPY; METABOLISM; MOLECULAR GENETICS; MOLECULAR MIMICRY; NUCLEAR EXPORT SIGNAL; PHYSIOLOGY; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

NOROVIRUS; NORWALK VIRUS;

AMINO ACID SEQUENCE; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; MICROSCOPY, ELECTRON; MOLECULAR MIMICRY; MOLECULAR SEQUENCE DATA; NORWALK VIRUS; NUCLEAR EXPORT SIGNALS; PROTEIN TRANSPORT; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 78149427285     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013130     Document Type: Article

References (60)

1. Scales SJ, Pepperkok R, Kreis TE (1997) Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPII and COPI. Cell 90: 1137-1148.
2. Schekman R, Barlowe C, Yeung T, Hamamoto S, Hosobuchi D, et al. (1994) COPII - A Novel Coat Protein Required for Transport Vesicle Budding from the Endoplasmic-Reticulum. FASEB J 8: A1379.
3. Budnik A, Stephens DJ (2009) ER exit sites-localization and control of COPII vesicle formation. FEBS Lett 583: 3796-3803.
4. Tang BL, Wang Y, Ong YS, Hong WJ, (2005) COPII and exit fromthe endoplasmic reticulum. Biochimica et Biophysica Acta-Mol Cell Res 1744: 293-303.
5. Saraste J, Dale HA, Bazzocco S, Marie M (2009) Emerging new roles of the pre-Golgi intermediate compartment in biosynthetic-secretory trafficking. FEBS Lett 583: 3804-3810.
6. Polishchuk RS, Capestrano M, Polishchuk EV (2009) Shaping tubular carriers for intracellular membrane transport. FEBS Lett 583: 3847-3856.
7. Nakamura N, Yamazaki S, Sato K, Nakano A, Sakaguchi M, et al. (1998) Identification of potential regulatory elements for the transport of Emp24p. MBC 9: 3493-3503.
8. Giraudo CG, Maccioni HJF (2003) Endoplasmic reticulum export of glycosyltransferases depends on interaction of a cytoplasmic dibasic motif with sar1. Mol Biol Cell 14: 3753-3766.
9. Nishimura N, Balch WE (1997) A di-acidic signal required for selective export from the endoplasmic reticulum. Science 277: 556-558.
10. Nishimura N, Bannykh S, Slabough S, Matteson J, Altschuler Y, et al. (1999) A di-acidic (DXE) code directs concentration of cargo during export from the endoplasmic reticulum. J Biol Chem 274: 15937-15946.
11. Chardin P, McCormick F (1999) Brefeldin A: the advantage of being uncompetitive. Cell 97: 153-155.
12. Wessels E, Duijsings D, Niu TK, Neumann S, Oorschot VM, et al. (2006) A viral protein that blocks Arf1-mediated COP-I assembly by inhibiting the guanine nucleotide exchange factor GBF1. Dev Cell 11: 191-201.
13. Wessels E, Duijsings D, Lanke KHW, van Dooren SHJ, Jackson CL, et al. (2006) Effects of picornavirus 3A proteins on protein transport and GBF1-dependent COP-I recruitment. J Virol 80: 11852-11860.
14. Deitz SB, Dodd DA, Cooper S, Parham P, Kirkegaard K (2000) MHC Idependent antigen presentation is inhibited by poliovirus protein 3A. Proc Natl Acad Sci U S A 97: 13790-13795.
15. Dodd DA, Giddings TH, Kirkegaard K (2001) Poliovirus 3A protein limits interleukin-6 (IL-6), IL-8, and beta interferon secretion during viral infection. J Virol 75: 8158-8165.
16. Neznanov N, Kondratova A, Chumakov KM, Angres B, Zhumabayeva B, et al. (2001) Poliovirus protein 3A inhibits tumor necrosis factor (TNF)-induced apoptosis by eliminating the TNF receptor from cell surface. J Virol 75: 10409-10420.
17. Mead PS, Slutsker L, Dietz V, Mccaig LF, Bresee JS, et al. (1999) Food-related illness and death in the United States. EID 5: 607-625.
18. Glass RI, Parashar U, Estes MK (2009) Norovirus gastroenteritis. N Engl J Med 361: 50-59.
19. Estes MK, Prasad BVV, Atmar RL (2006) Noroviruses everywhere: has something changed? Curr Opin Infect Dis 19: 467-474.
20. Blanton LH, Adams SM, Beard RS, Wei G, Bulens SN, et al. (2006) Molecular and epidemiologic trends of caliciviruses associated with outbreaks of acute gastroenteritis in the United States, 2000-2004. J Infect Dis 193: 413-421.
21. Siebenga JJ, Vennema H, Duizer E, Koopmans MPG (2007) Gastroenteritis caused by norovirus GGII.4, the Netherlands, 1994-2005. EID 13: 144-146.
22. Hardy ME (2005) Norovirus protein structure and function. FEMS Microbiol Lett 253: 1-8.
23. Matsui SM, Kim JP, Greenberg HB, Su W, Sun Q, et al. (1991) The isolation and characterization of a Norwalk virus-specific cDNA. J Clin Invest 87: 1456-1461.
24. Green KY, Mory A, Fogg MH, Weisberg A, Belliot G, et al. (2002) Isolation of enzymatically active replication complexes from feline calicivirus-infected cells. J Virol 76: 8582-8595.
25. Wobus CE, Karst SM, Thackray LB, Chang KO, Sosnovtsev SV, et al. (2004) Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol 2: 2076-2084.
26. Bailey D, Kaiser WJ, Hollinshead M, Moffat K, Chaudhry Y, et al. (2010) Feline calicivirus p32, p39 and p30 proteins localize to the endoplasmic reticulum to initiate replication complex formation. J Gen Virol 91: 739-749.
27. Fernandez-Vega V, Sosnovtsev SV, Belliot G, King AD, Mitra T, et al. (2004) Norwalk virus N-terminal nonstructural protein is associated with disassembly of the Golgi complex in transfected cells. J Virol 78: 4827-4837.
28. Cornell CT, Kiosses WB, Harkins S, Whitton JL (2006) Inhibition of protein trafficking by coxsackievirus B3: Multiple viral proteins target a single organelle. J Virol 80: 6637-6647.
29. Doedens JR, Kirkegaard K (1995) Inhibition of Cellular Protein Secretion by Poliovirus Proteins 2B and 3A. EMBO J 14: 894-907.
30. Guix S, Asanaka M, Katayama K, Crawford SE, Neill FH, et al. (2007) Norwalk virus RNA is infectious in mammalian cells. J Virol 81: 12238-12248.
31. Persico A, Cervigni RI, Barretta ML, Colanzi A (2009) Mitotic inheritance of the Golgi complex. FEBS Lett 583: 3857-3862.
32. Zaal KJM, Smith CL, Polishchuk RS, Altan N, Cole NB, et al. (1999) Golgi membranes are absorbed into and reemerge from the ER during mitosis. Cell 99: 589-601.
33. Green KY (2007) Caliciviridae: The Noroviruses. In: Knipe DM, Howley PM, eds. Fields Virology. Philadelphia: Lippincott Williams & Wilkins. pp 949-980.
34. Doedens JR, Giddings TH, Kirkegaard K (1997) Inhibition of endoplasmic reticulum-to-Golgi traffic by poliovirus protein 3A: Genetic and ultrastructural analysis. J Virol 71: 9054-9064.
35. Berger J, Hauber J, Hauber R, Geiger R, Cullen BR (1988) Secreted Placental Alkaline-Phosphatase - A Powerful New Quantitative Indicator of Gene-Expression in Eukaryotic Cells. Gene 66: 1-10.
36. Choe SS, Dodd DA, Kirkegaard K (2005) Inhibition of cellular protein secretion by picornaviral 3A proteins. Virology 337: 18-29.
37. Rost B, Fariselli P, Casadio R (1996) Topology prediction for helical transmembrane proteins at 86% accuracy. Protein Sci 5: 1704-1718.
38. Fujita K, Krishnakumar SS, Franco D, Paul AV, London E, et al. (2007) Membrane topography of the hydrophobic anchor sequence of poliovirus 3A and 3AB proteins and the functional effect of 3A/3AB membrane association upon RNA replication. Biochemistry 46: 5185-5199.
39. Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, et al. (2006) Norovirus classification and proposed strain nomenclature. Virology 346: 312-323.
40. Sevier CS, Weisz OA, Davis M, Machamer CE (2000) Efficient export of the vesicular stomatitis virus G protein from the endoplasmic reticulum requires a signal in the cytoplasmic tail that includes both tyrosine-based and di-acidic motifs. Mol Biol Cell 11: 13-22.
41. Paulhe F, Imhof BA, Wehrle-Haller B (2004) A specific endoplasmic reticulum export signal drives transport of stem cell factor (Kitl) to the cell surface. J Biol Chem 279: 55545-55555.
42. Tisdale EJ, Bourne JR, Khosravifar R, Der CJ, Balch WE (1992) Gtp-Binding Mutants of Rab1 and Rab2 Are Potent Inhibitors of Vesicular Transport from the Endoplasmic-Reticulum to the Golgi-Complex. J Cell Biol 119: 749-761.
43. Wessels E, Duijsings D, Lanke KHW, Melchers WJG, Jackson CL, et al. (2007) Molecular determinants of the interaction between coxsackievirus protein 3A and guanine nucleotide exchange factor GBF1. J Virol 81: 5238-5245.
44. Beske O, Reichelt M, Taylor MP, Kirkegaard K, Andino R (2007) Poliovirus infection blocks ERGIC-to-Golgi trafficking and induces microtubule-dependent disruption of the Golgi complex. J Cell Sci 120: 3207-3218.
45. Barr FA, Short B (2003) Golgins in the structure and dynamics of the Golgi apparatus. Curr Opin Cell Biol 15: 405-413.
46. Short B, Haas A, Barr FA (2005) Golgins and GTPases, giving identity and structure to the Golgi apparatus. Biochim Biophys Acta 1744: 383-395.
47. Strating JR, Martens GJ (2009) The p24 family and selective transport processes at the ER-Golgi interface. Biol Cell 101: 495-509.
48. Lev S, Ben Halevy D, Peretti D, Dahan N (2008) The VAP protein family: from cellular functions to motor neuron disease. Trends Cell Biol 18: 282-290.
49. Ettayebi K, Hardy ME (2003) Norwalk virus nonstructural protein p48 forms a complex with the SNARE regulator VAP-A and prevents cell surface expression of vesicular stomatitis virus G protein. J Virol 77: 11790-11797.
50. Kim J, Thanabalasuriar A, Chaworth-Musters T, Fromme JC, Frey EA, et al. (2007) The bacterial virulence factor NleA inhibits cellular protein secretion by disrupting mammalian COPII function. Cell Host Microbe 2: 160-171.
51. Rismanchi N, Puertollano R, Blackstone C (2009) STAM Adaptor Proteins Interact with COPII Complexes and Function in ER-to-Golgi Trafficking. Traffic 10: 201-217.
52. Mukherjee S, Chiu R, Leung SM, Shields D (2007) Fragmentation of the Golgi apparatus: an early apoptotic event independent of the cytoskeleton. Traffic 8: 369-378.
53. Teterina NL, Bienz K, Egger D, Gorbalenya AE, Ehrenfeld E (1997) Induction of intracellular membrane rearrangements by HAV proteins 2C and 2BC. Virology 237: 66-77.
54. Konan KV, Giddings TH, Ikeda M, Li K, Lemon SM, et al. (2003) Nonstructural protein precursor NS4A/B from hepatitis C virus alters function and ultrastructure of host secretory apparatus. J Virol 77: 7843-7855.
55. Hyde JL, Sosnovtsev SV, Green KY, Wobus C, Virgin HW, et al. (2009) Mouse norovirus replication is associated with virus-induced vesicle clusters originating from membranes derived from the secretory pathway. J Virol 83: 9709-9719.
56. Chang KO, Sosnovtsev SV, Belliot G, King AD, Green KY (2006) Stable expression of a Norwalk virus RNA replicon in a human hepatoma cell line. Virology 353: 463-473.
57. Chang KO, George DW (2007) Interferons and ribavirin effectively inhibit Norwalk virus replication in replicon-bearing cells. J Virol 81: 12111-12118.
58. Guix S, Estes MK (2009) Caliciviridae and Astroviridae. In: Brasier AR, Garcia-Sastre A, Lemon SM, eds. Cellular Signaling and Innate Immune Responses to RNA Virus Infections. Washington D.C.: ASM Press. pp 389-402.
59. Aridor M, Weissman J, Bannykh S, Nuoffer C, Balch WE (1998) Cargo selection by the COPII budding machinery during export from the ER. J Cell Biol 141: 61-70.
60. Gilpatrick SG, Schwab KJ, Estes MK, Atmar RL (2000) Development of an immunomagnetic capture reverse transcription-PCR assay for the detection of Norwalk virus. J Virol Methods 90: 69-78.