A reinvestigation provides no evidence for sugar residues on structural proteins of poleroviruses and argues against a role for glycosylation of virus structural proteins in aphid transmission

Virology

Volumn 402, Issue 2, 2010, Pages 303-314

  Revollon, S ^a   Strub, J M ^c   Fitchette, A C ^b   Wiss, L ^a   Gomord, V ^b   Van Dorsselaer, A ^c   Brault, V ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITÉ DE ROUEN   (France)

^c CNRS   (France)

Author keywords

Aphid transmission; Glycosylation; Polerovirus

Indexed keywords

CAPSID PROTEIN; STRUCTURAL PROTEIN; SUGAR;

AMINO ACID SEQUENCE; APHID; ARTICLE; BINDING ASSAY; CONTROLLED STUDY; CUCURBIT APHID BORNE YELLOW VIRUS; GLYCOSYLATION; LECTIN BINDING; MASS SPECTROMETRY; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; POLEROVIRUS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; RNA VIRUS; TURNIP YELLOW MOSAIC VIRUS; VIRUS TRANSMISSION;

ANIMALS; ANTIBODIES; APHIDS; BRASSICA NAPUS; CARBOHYDRATES; GLYCOSYLATION; LECTINS; LUTEOVIRIDAE; MASS SPECTROMETRY; VIRAL STRUCTURAL PROTEINS;

APHIDIDAE; CUCURBIT APHID-BORNE YELLOWS VIRUS; POLEROVIRUS; TURNIP YELLOWS VIRUS;

EID: 77953023341     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.03.037     Document Type: Article

References (58)

1. Altmann F., Lomonossoff G.P. Glycosylation of the capsid proteins of cowpea mosaic virus: a reinvestigation shows the absence of sugar residues. J. Gen. Virol. 2000, 81:1111-1114.
2. Ashoub A., Rohde W., Prufer D. In planta transcription of a second subgenomic RNA increases the complexity of the subgroup 2 luteovirus genome. Nucleic Acids Res. 1998, 26(2):420-426.
3. Bahner I., Lamb J., Mayo M.A., Hay R.T. Expression of the genome of potato leafroll virus: readthrough of the coat protein termination codon in vivo. J. Gen. Virol. 1990, 71:2251-2256.
4. Baratova L.A., Fedorova N.V., Dobrov E.N., Lukashina E.V., Kharlanov A.N., Nasonov V.V., Serebryakova M.V., Kozlovsky S.V., Zayakina O.V., Rodionova N.P. N-Terminal segment of potato virus X coat protein subunits is glycosylated and mediates formation of a bound water shell on the virion surface. Eur. J. Biochem. 2004, 271(15):3136-3145.
5. Bencharki, B., Boissinot, S., Revollon, S., Ziegler-Graff, V., Erdinger, M., Wiss, L., Dinant, S., Renard, D., Beuve, M., Lemaitre-Guillier, C., Brault, V., in press. Phloem protein partners of Cucurbit aphid borne yellows virus: possible involvement of phloem proteins in virus transmission by aphids. Mol Plant Microbe Interact. doi:10.1094/MPMI-23-0-0000.
6. Brault V., Bergdoll M., Mutterer J., Prasad V., Pfeffer S., Erdinger M., Richards K.E., Ziegler-Graff V. Effects of point mutations in the major capsid protein of beet western yellows virus on capsid formation, virus accumulation, and aphid transmission. J. Virol. 2003, 77(5):3247-3256.
7. Brault V., Herrbach E., Reinbold C. Electron microscopy studies on luteovirid transmission by aphids. Micron 2007, 38(3):302-312.
8. Brault V., Mutterer J., Scheidecker D., Simonis M.T., Herrbach E., Richards K., Ziegler-Graff V. Effects of point mutations in the readthrough domain of the beet western yellows virus minor capsid protein on virus accumulation in planta and on transmission by aphids. J. Virol. 2000, 74(3):1140-1148.
9. Brault V., Perigon S., Reinbold C., Erdinger M., Scheidecker D., Herrbach E., Richards K., Ziegler-Graff V. The polerovirus minor capsid protein determines vector specificity and intestinal tropism in the aphid. J. Virol. 2005, 79(15):9685-9693.
10. Brault V., van den Heuvel J.F., Verbeek M., Ziegler-Graff V., Reutenauer A., Herrbach E., Garaud J.C., Guilley H., Richards K., Jonard G. Aphid transmission of beet western yellows luteovirus requires the minor capsid read-through protein P74. EMBO J. 1995, 14(4):650-659.
11. Brown C.M., Dinesh-Kumar S.P., Miller W.A. Local and distant sequences are required for efficient readthrough of the barley yellow dwarf virus PAV coat protein gene stop codon. J. Virol. 1996, 70(9):5884-5892.
12. Bruyère A., Brault V., Ziegler-Graff V., Simonis M.T., Van den Heuvel J.F., Richards K., Guilley H., Jonard G., Herrbach E. Effects of mutations in the beet western yellows virus readthrough protein on its expression and packaging and on virus accumulation, symptoms, and aphid transmission. Virology 1997, 230(2):323-334.
13. Bryant J.E., Calvert A.E., Mesesan K., Crabtree M.B., Volpe K.E., Silengo S., Kinney R.M., Huang C.Y., Miller B.R., Roehrig J.T. Glycosylation of the dengue 2 virus E protein at N67 is critical for virus growth in vitro but not for growth in intrathoracically inoculated Aedes aegypti mosquitoes. Virology 2007, 366(2):415-423.
14. Chay C.A., Gunasinge U.B., Dinesh-Kumar S.P., Miller W.A., Gray S.M. Aphid transmission and systemic plant infection determinants of barley yellow dwarf luteovirus-PAV are contained in the coat protein readthrough domain and 17-kDa protein, respectively. Virology 1996, 219(1):57-65.
15. Chen D., Juarez S., Hartweck L., Alamillo J.M., Simon-Mateo C., Perez J.J., Fernandez-Fernandez M.R., Olszewski N.E., Garcia J.A. Identification of secret agent as the O-GlcNAc transferase that participates in Plum pox virus infection. J. Virol. 2005, 79(15):9381-9387.
16. Clark M.F., Adams A.N. Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. J. Gen. Virol. 1977, 34(3):475-483.
17. Elias J.E., Gygi S.P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 2007, 4(3):207-214.
18. Esau K., Hoefert L.L. Development of infection with beet western yellows virus in the sugarbeet. Virology 1972, 48(3):724-738.
19. Estes M.K., Cohen J. Rotavirus gene structure and function. Microbiol. Rev. 1989, 53(4):410-449.
20. Faye L., Chrispeels M.J. Characterization of N-linked oligosaccharides by affinoblotting with concanavalin A-peroxidase and treatment of the blots with glycosidases. Anal. Biochem. 1985, 149(1):218-224.
21. Faye L., Gomord V., Fitchette-Laine A.C., Chrispeels M.J. Affinity purification of antibodies specific for Asn-linked glycans containing alpha 1->3 fucose or beta 1->2 xylose. Anal. Biochem. 1993, 209(1):104-108.
22. Fernandez-Fernandez M.R., Camafeita E., Bonay P., Mendez E., Albar J.P., Garcia J.A. The capsid protein of a plant single-stranded RNA virus is modified by O-linked N-acetylglucosamine. J. Biol. Chem. 2002, 277(1):135-140.
23. Fitchette-Laine A.C., Gomord V., Cabanes M., Michalski J.C., Saint Macary M., Foucher B., Cavelier B., Hawes C., Lerouge P., Faye L. N-glycans harboring the Lewis a epitope are expressed at the surface of plant cells. Plant J. 1997, 12(6):1411-1417.
24. Fournillier A., Wychowski C., Boucreux D., Baumert T.F., Meunier J.C., Jacobs D., Muguet S., Depla E., Inchauspe G. Induction of hepatitis C virus E1 envelope protein-specific immune response can be enhanced by mutation of N-glycosylation sites. J. Virol. 2001, 75(24):12088-12097.
25. Gildow F. Luteovirus transmission mechanisms regulating vector specificity. The Luteoviridae 1999, 88-111. CAB International, Oxon, UK. H.G. Smith, H. Barker (Eds.).
26. Graff J., Zhou Y.H., Torian U., Nguyen H., St Claire M., Yu C., Purcell R.H., Emerson S.U. Mutations within potential glycosylation sites in the capsid protein of hepatitis E virus prevent the formation of infectious virus particles. J. Virol. 2008, 82(3):1185-1194.
27. Guilley H., Wipf-Scheibel C., Richards K., Lecoq H., Jonard G. Nucleotide sequence of cucurbit aphid-borne yellows luteovirus. Virology 1994, 202(2):1012-1017.
28. Holsters M., Silva B., Van Vliet F., Genetello C., De Block M., Dhaese P., Depicker A., Inze D., Engler G., Villarroel R., et al. The functional organization of the nopaline A. tumefaciens plasmid pTiC58. Plasmid 1980, 3(2):212-230.
29. Jolly C.A., Mayo M.A. Changes in the amino acid sequence of the coat protein readthrough domain of potato leafroll luteovirus affect the formation of an epitope and aphid transmission. Virology 1994, 201(1):182-185.
30. Kabcenell A.K., Atkinson P.H. Processing of the rough endoplasmic reticulum membrane glycoproteins of rotavirus SA11. J. Cell Biol. 1985, 101(4):1270-1280.
31. Koch M., Pancera M., Kwong P.D., Kolchinsky P., Grundner C., Wang L., Hendrickson W.A., Sodroski J., Wyatt R. Structure-based, targeted deglycosylation of HIV-1 gp120 and effects on neutralization sensitivity and antibody recognition. Virology 2003, 313(2):387-400.
32. Lecoq H., Bourdin D., Wipf-Scheibel C., Bon M., Lot H., Lemaire O., Herrbach E. A new yellowing disease of cucurbits caused by a luteovirus, cucurbit aphid-borne yellows virus. Plant. Pathol. 1992, 41(6):749-761.
33. Lee L., Palukaitis P., Gray S.M. Host-dependent requirement for the Potato leafroll virus 17-kda protein in virus movement. Mol. Plant Microbe Interact. 2002, 15(10):1086-1094.
34. Lerouge P., Cabanes-Macheteau M., Rayon C., Fischette-Laine A.C., Gomord V., Faye L. N-glycoprotein biosynthesis in plants: recent developments and future trends. Plant Mol. Biol. 1998, 38(1-2):31-48.
35. Li J., Bhuvanakantham R., Howe J., Ng M.L. The glycosylation site in the envelope protein of West Nile virus (Sarafend) plays an important role in replication and maturation processes. J. Gen. Virol. 2006, 87:613-622.
36. Li Y., Luo L., Rasool N., Kang C.Y. Glycosylation is necessary for the correct folding of human immunodeficiency virus gp120 in CD4 binding. J. Virol. 1993, 67(1):584-588.
37. Mutterer J.D., Stussi-Garaud C., Michler P., Richards K.E., Jonard G., Ziegler-Graff V. Role of the beet western yellows virus readthrough protein in virus movement in Nicotiana clevelandii. J. Gen. Virol. 1999, 80:2771-2778.
38. Naidu R.A., Ingle C.J., Deom C.M., Sherwood J.L. The two envelope membrane glycoproteins of Tomato spotted wilt virus show differences in lectin-binding properties and sensitivities to glycosidases. Virology 2004, 319(1):107-117.
39. Nurkiyanova K.M., Ryabov E.V., Commandeur U., Duncan G.H., Canto T., Gray S.M., Mayo M.A., Taliansky M.E. Tagging potato leafroll virus with the jellyfish green fluorescent protein gene. J. Gen. Virol. 2000, 81:617-626.
40. Partridge J.E., Shannon L.M., Gumpf D.J., Colbaugh P. Glycoprotein in the capsid of plant viruses as a possible determinant of seed transmissibility. Nature 1974, 247:391-392.
41. Peter K.A., Liang D., Palukaitis P., Gray S.M. Small deletions in the potato leafroll virus readthrough protein affect particle morphology, aphid transmission, virus movement and accumulation. J. Gen. Virol. 2008, 89:2037-2045.
42. Pollakis G., Kang S., Kliphuis A., Chalaby M.I., Goudsmit J., Paxton W.A. N-linked glycosylation of the HIV type-1 gp120 envelope glycoprotein as a major determinant of CCR5 and CXCR4 coreceptor utilization. J. Biol. Chem. 2001, 276(16):13433-13441.
43. Prufer D., Wipf-Scheibel C., Richards K., Guilley H., Lecoq H., Jonard G. Synthesis of a full-length infectious cDNA clone of cucurbit aphid-borne yellows virus and its use in gene exchange experiments with structural proteins from other luteoviruses. Virology 1995, 214(1):150-158.
44. Reinbold C., Gildow F.E., Herrbach E., Ziegler-Graff V., Goncalves M.C., van Den Heuvel J.F., Brault V. Studies on the role of the minor capsid protein in transport of Beet western yellows virus through Myzus persicae. J. Gen. Virol. 2001, 82:1995-2007.
45. Reinbold C., Herrbach E., Brault V. Posterior midgut and hindgut are both sites of acquisition of Cucurbit aphid-borne yellows virus in Myzus persicae and Aphis gossypii. J. Gen. Virol. 2003, 84:3473-3484.
46. Roberts D.D., Goldstein I.J. Hydrophobic binding properties of the lectin from lima beans (Phaseolus lunatus). J. Biol. Chem. 1982, 257(19):11274-11277.
47. Scott C.L., Hartweck L.M., de Jesus Perez J., Chen D., Garcia J.A., Olszewski N.E. SECRET AGENT, an Arabidopsis thaliana O-GlcNAc transferase, modifies the Plum pox virus capsid protein. FEBS Lett. 2006, 580(25):5829-5835.
48. Seddas P., Boissinot S. Glycosylation of beet western yellows virus proteins is implicated in the aphid transmission of the virus. Arch. Virol. 2006, 151(5):967-984.
49. Seddas P., Boissinot S., Strub J.M., Van Dorsselaer A., Van Regenmortel M.H., Pattus F. Rack-1, GAPDH3, and actin: proteins of Myzus persicae potentially involved in the transcytosis of beet western yellows virus particles in the aphid. Virology 2004, 325(2):399-412.
50. Shepardson S., Esau K., McCrum R. Ultrastructure of potato leaf phloem infected with potato leafroll virus. Virology 1980, 105(2):379-392.
51. Stoitsova S.R., Boteva R.N., Doyle R.J. Binding of hydrophobic ligands by Pseudomonas aeruginosa PA-I lectin. Biochim. Biophys. Acta 2003, 1619(2):213-219.
52. Van den Heuvel J., Boerma T., Peters D. Transmission of potato leafroll virus from plants and artificial diets by Myzus persicae. Phytopathology 1991, 81(2):150-154.
53. van den Heuvel J.F., Bruyère A., Hogenhout S.A., Ziegler-Graff V., Brault V., Verbeek M., van der Wilk F., Richards K. The N-terminal region of the luteovirus readthrough domain determines virus binding to Buchnera GroEL and is essential for virus persistence in the aphid. J. Virol. 1997, 71(10):7258-7265.
54. Vigerust D.J., Ulett K.B., Boyd K.L., Madsen J., Hawgood S., McCullers J.A. N-linked glycosylation attenuates H3N2 influenza viruses. J. Virol. 2007, 81(16):8593-8600.
55. Wei X., Decker J.M., Wang S., Hui H., Kappes J.C., Wu X., Salazar-Gonzalez J.F., Salazar M.G., Kilby J.M., Saag M.S., Komarova N.L., Nowak M.A., Hahn B.H., Kwong P.D., Shaw G.M. Antibody neutralization and escape by HIV-1. Nature 2003, 422(6929):307-312.
56. Whitfield A.E., Ullman D.E., German T.L. Expression and characterization of a soluble form of tomato spotted wilt virus glycoprotein GN. J. Virol. 2004, 78(23):13197-13206.
57. Yang X., Thannhauser T.W., Burrows M., Cox-Foster D., Gildow F.E., Gray S.M. Coupling genetics and proteomics to identify aphid proteins associated with vector-specific transmission of polerovirus (luteoviridae). J. Virol. 2008, 82(1):291-299.
58. Ziegler-Graff V., Brault V., Mutterer J., Simonis M., Herrbach E., Guilley H., Richards K., Jonard G. The coat protein of beet western yellows luteovirus is essential for systemic infection but the viral gene products P29 and P19 are dispensable for systemic infection and aphid transmission. Mol. Plant Microbe Interact. 1996, 9:501-510.