Rack-1, GAPDH3, and actin: Proteins of Myzus persicae potentially involved in the transcytosis of beet western yellows virus particles in the aphid

Virology

Volumn 325, Issue 2, 2004, Pages 399-412

  Seddas, Pascale ^a   Boissinot, Sylvaine ^a   Strub, Jean Marc ^b   Van Dorsselaer, Alain ^b   Van Regenmortel, Marc H V ^c   Pattus, Franc ^d  

^a CEMAGREF   (France)

^b Lab Spectrom Masse Bio Organique   (France)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d CNRS   (France)

Author keywords

Actin; Aphid transmission; BWYV; GAPDH3; Luteovirus; Membrane; Myzus persicae; Rack 1; Receptor; Symbionin

Indexed keywords

ACTIN; ACTIVATED C KINASE 1 RECEPTOR; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; POLYPEPTIDE; PROTEIN; RECEPTOR SUBTYPE; SYMBIONIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; APHID; ARTICLE; BEET WESTERN YELLOW VIRUS; CELL FRACTIONATION; CONTROLLED STUDY; DISEASE CARRIER; ELECTROPHORESIS; FEMALE; LUTEOVIRUS; MASS SPECTROMETRY; MEMBRANE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; VIRAL PLANT DISEASE; VIRUS PARTICLE; WILD TYPE;

ACTINS; ANIMALS; APHIDS; BETA VULGARIS; BIOLOGICAL TRANSPORT, ACTIVE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; INSECT PROTEINS; INSECT VECTORS; LUTEOVIRUS; MUTATION; PLANT DISEASES; PROTEIN BINDING; RECEPTORS, CELL SURFACE; VIRULENCE;

APHIDIDAE; BEET WESTERN YELLOWS VIRUS; BETA VULGARIS SUBSP. VULGARIS; LUTEOVIRUS; MYZUS; MYZUS PERSICAE; POLEROVIRUS;

EID: 3142530530     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virol.2004.05.014     Document Type: Article

References (88)

1. Albinsson B., Kidd A.H. Adenovirus type 41 lacks an RGD αv-integrin binding motif on the penton base and undergoes delayed uptake in A549 cells. Virus Res. 64:1999;125-136
2. Alvarez R.A., Blaylock M.W., Baseman J.B. Surface localized glyceraldehyde-3-phosphate dehydrogenase of Mycoplasma genitalium binds mucin. Mol. Microbiol. 48:2003;1417-1425
3. Bandla M.D., Campbell L.R., Ullman D.E., Sherwood J.L. Interaction of tomato spotted wilt tospovirus (TSWV) glycoproteins with a thrips midgut protein, a potential cellular receptor for TSWV. Phytopathology. 88:1998;98-104
4. Bauman P., Baumann L., Lai C., Rouhbakhsh D., Moran N.A., Clark M.A. Genetics, physiology and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu. Rev. Microbiol. 49:1995;55-94
5. Blum H., Beier H., Gross H.J. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis. 8:1987;93-99
6. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254
7. Brault V., van den Heuvel J.F.J.M., 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. 14:1995;650-659
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. 74:2000;1140-1148
9. Bruyère A., Brault V., Ziegler-Graff V., Simonis M.-T., van den Heuvel J.F.J.M., 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. 230:1997;323-334
10. Buensuceso C.S., Woodside D., Huf J.L., Plopper G.E., O'Tole T.E. The WD protein Rack1 mediates protein kinase C and integrin-dependent cell migration. J. Cell Sci. 64:2001;247-252
11. Cao F., Yanagihara N., Burke J.M. Progressive association of a "soluble" glycolytic enzyme with the detergent-insoluble cytoskeleton during in vitro morphogenesis of MDCK epithelial cells. Cell Motil. Cytoskelet. 44:1999;133-142
12. Chang B.Y., Conroy K.B., Machleder E.M., Cartwright C.A. Rack1, a receptor for activated C kinase and a homolog of the beta subunit of G proteins, inhibits activity of src tyrosine kinases and growth of NIH 3T3 cells. Mol. Cell. Biol. 18:1998;3245-3256
13. Chay C.A., Gunasinghe 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. 219:1996;57-65
14. Choi D.-S., Young H., McMahon T., Wang D., Messing R.O. The mouse RACK1 gene is regulated by nuclear factor-κB and contributes to cell survival. Mol. Pharmacol. 64:2003;1541-1548
15. Chou Y.-C., Chou C.-C., Chen Y.-K., Tsai S., Hsieh F.M.J., Liu H.J., Hseu T.-H. Structure and genomic organization of porcine RACK1 gene. Biochim. Biophys. Acta. 1489:1999;315-322
16. Daubenberger C.A., Tisdale E.J., Curcic M., Diaz D., Silvie O., Mazier D., Eling W., Bohrmann B., Matile H., Pluschke G. The N′-terminal domain of glyceraldehydes-3-phosphate dehydrogenase of the picomplexan Plasmodium falciparum mediates GTPase Rab2-dependent recruitment to membranes. J. Biol. Chem. 384:2003;1227-1237
17. Deckert M., Ticchioni M., Bernard A. Endocytosis of GPI-anchored proteins in human lymphocytes: role of glycolipid-based domains, actin cytoskeleton, and protein kinases. J. Cell Biol. 133:1996;791-799
18. Delgado M.L., O'Connor J.E., Azorin I., Renau-Piqueras J., Gil M.L., Gozalbo D. The glyceraldehydes-3-phosphate dehydrogenase polypeptides encoded by the Saccharomyces cerevisiae TDH1, TDH2 and TDH3 genes are also cell wall proteins. Microbiology. 147:2001;411-417
19. Douglas A.E. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 43:1998;17-37
20. Dozolme P., Marty-Mazars D., Clémencet M.-C., Marty F. Monoclonal antibody TeM 106 reacts with a tonoplast intrinsic protein of 106 kDa from Brassica oleracea L. J. Cell Sci. 108:1995;1509-1517
21. Drücker M., Hinz G., Robinson D.G. ATPases in plant coated vesicles. J. Exp. Bot. 44:1993;283-291
22. Fernandes P.A., Keen J.N., Findlay J.B.C., Moradas-Ferreira P. A protein homologous to glyceraldehyde-3-phosphate dehydrogenase is induced in the cell wall of a flocculent Kluyveromyces marxianus. Biochim. Biophys. Acta. 1159:1992;67-73
23. Filichkin S.A., Brumfield S., Filichkin T.P., Young M.J. In vitro interactions of the aphid endosymbiotic symL with Barley yellow dwarf virus. J. Virol. 71:1997;569-577
24. Freund J. The mode of action of immunologic adjuvants. Adv. Tuberc. Res. 7:1956;130-148
25. Garret A., Kerlan C., Thomas D. The intestine is a site of passage for potato leafroll virus from the gut lumen to the haemocoel in the aphid vector, Myzus persicae Sulz. Arch. Virol. 131:1993;377-392
26. Geijsen N., Spaargaren M., Raaijmakers J.A.M., Lammers J.-W.J., Koenderman L., Coffer P.J. Association of RACK1 and PKCβ with the common β-chain of the IL-5/IL-3/GM-CSF receptor. Oncogene. 18:1999;5126-5130
27. Gildow F.E. Virus-membrane interactions involved in circulative transmission of luteoviruses by aphids. Curr. Top. Vector Res. 4:1987;93-120
28. Gildow F.E. Evidence for receptor-mediated endocytosis regulating luteovirus acquisition by aphids. Phytopathology. 83:1993;270-277
29. Gildow F.E. Luteovirus transmission and mechanisms regulating vector specificity. Smith H.G., Barker H. The Luteoviridae. 1999;88-113 CAB International, Oxford
30. Gildow F.E., Gray S.M. The aphid salivary gland basal lamina as a selective barrier associated with vector-specificity transmission of barley yellow dwarf luteovirus. Phytopathology. 83:1993;1293-1302
31. Gildow F.E., Rochow W.F. Role of accessory salivary glands in aphid transmission of barley yellow dwarf virus. Virology. 104:1980;97-108
32. Gildow F.E., Reavy B., Mayo M.A., Duncan G.H., Woodford J.A.T., Lamb J.W., Hay R.T. Aphid acquisition and cellular transport of potato leafroll virus-like particles lacking P5 readthrough protein. Phytopathology. 90:2000;1153-1161
33. Gil-Navarro I., Gil M.L., Casanova M., O'Connor J.E., Martinez J.P., Gozalbo D. The glycolytic enzyme glyceraldehyde-3-phosphate dehydrogenase of Candida albicans is a surface antigen. J. Bacteriol. 179:1997;4992-4999
34. Glaser P.E., Gross R.W. Rapid plasmenylethanolamine-selective fusion of membrane bilayers catalyzed by an isoform of glyceraldehydes-3-phosphate dehydrogenase: discrimination between glycolytic and fusogenic roles of individual isoforms. Biochemistry. 34:1995;12193-12203
35. Glaser P.E., Han X., Gross R.W. Tubulin is the endogenous inhibitor of the glyceraldehydes 3-phosphate dehydrogenase isoform that catalyzes membrane fusion: implications for the coordinated regulation of glycolysis and membrane fusion. Proc. Natl. Acad. Sci. U.S.A. 99:2002;14104-14109
36. Gottlieb T.A., Ivanov I.E., Adesnik M., Sabatini D.D. Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J. Cell Biol. 120:1993;695-710
37. Goudot-Crozel V., Caillol D., Djabali M., Dessein A.J. The major parasite surface antigen associated with human resistance to schistosomiasis is a 37 kDa glyceraldehydes-3P-dehydrogenase. J. Exp. Med. 170:1989;2065-2080
38. Gozalbo D., Gil-Navarro I., Azorin I., Renau-Piqueras J., Martinez J.P., Gil M.L. The cell wall-associated glyceraldehyde-3-phosphate dehydrogenase of Candida albicans is also a fibronectin and laminin binding protein. Infect. Immun. 66:1998;2052-2059
39. Gray S.M., Banerjee N. Mechanisms of arthropod transmission of plant and animal viruses. Microbiol. Mol. Biol. Rev. 3:1999;128-148
40. Gray S.M., Gildow F.E. Luteovirus-aphid interactions. Annu. Rev. Phytopathol. 41:2003;539-566
41. Harrewijn P. The effect of cultural measures on behaviour and population development of potato aphids and transmission of viruses. Meded. Fac. Landbouwwet. - Rijksuniv. Gent. 48:1983;791-799
42. Hermanto U., Zong C.S., Li W., Wang L.H. RACK1, an insulin-like growth factor I (IGF-I) receptor-interacting protein, modulates IGF-I-dependent integrin signaling and promotes cell spreading and contact with extracellular matrix. Mol. Cell. Biol. 22:2002;2345-2365
43. Herrbach E. Vector-virus interactions: Introduction. Smith H.G., Barker H. The Luteoviridae. 1999;85-88 CAB International, Oxford
44. Ishikawa H. Host-symbiont interactions in the protein synthesis in the pea aphid, Acyrthosiphon pisum. Insect Biochem. 12:1982;613-622
45. Kikkert M., Meurs C., van de Wetering F., Dorfmüller S., Peters D., Kormelink R., Goldbach R. Binding of tomato spotted wilt virus to a 94-kDa thrips protein. Virology. 88:1998;63-69
46. γ, λ and RACK1 in baker's yeast, lobster and wheat germ. Biochem. Mol. Biol. Int. 36:1995;957-963
47. Kwon H.-J., Bae S., Son Y.-H., Chung H.-M. Expression of the Xenopus homologue of the receptor for activated C-kinase 1 (RACK1) in the Xenopus embryo. Dev. Genes Evol. 211:2001;195-197
48. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685
49. Lanier L.M., Volkman L.E. Actin binding and nucleation by Autograpa callifornica M nucleopolyhedrovirus. Virology. 243:1998;167-177
50. Li C., Cox-Foster D., Gray S.M., Gildow F.E. Vector specificity of barley yellow dwarf virus (BYDV) transmission: identification of potential cellular receptors binding BYDV-MAV in the aphid, Sitobion avenae. Virology. 286:2001;125-133
51. Liedtke C.M., Yun C.H., Kyle N., Wang D. PKC-epsilon dependent regulation of CFTR involves binding to RACK1, a receptor for activated C kinase and RACK1 binding to NHERF1. J. Biol. Chem. 277:2002;22925-22933
52. Liliental J., Chang D.D. Rack1, a receptor for activated protein kinase C, interacts with integrin beta subunit. J. Biol. Chem. 273:1998;2379-2383
53. Lutomski D., Caron M., Cornillot J.D., Bourin P., Dupuy C., Pontet M., Bladier D., Joubert-Caron R. Identification of different galectins by immunoblotting after two-dimensional polyacrylamide gel electrophoresis with immobilized pH gradients. Electrophoresis. 17:1996;600-606
54. Mayo M.A., D'Arcy C.J. Family Luteoviridae: a reclassification of luteoviruses. Smith H.G., Barker H. The Luteoviridae. 1999;15-22 CAB International, Oxford
55. Mayo M.A., Ziegler-Graff V. Molecular biology of luteoviruses. Adv. Virus Res. 46:1996;413-459
56. McCahill A., Warwicker J., Bolger G.B., Houslay M.D., Yarwood S.J. The RACK1 scaffold protein: a dynamic cog in cell response mechanisms. Mol. Pharmacol. 62:2002;1261-1273
57. Medeiros R.B., Ullman D.E., Sherwood J.L., German T.L. Immuno precipitation of a 50-kDa protein: a candidate receptor component for tomato spotted wilt tospovirus (Bunyaviridae) in its main vector, Frankliniella occidentalis. Virus Res. 67:2000;109-118
58. Neer E.J., Schmidt C.J., Nambudripad R., Smith T.F. The ancient regulatory-protein family of WD-repeat proteins. Nature. 371:1994;297-300
59. Palacios I., Drucker M., Blanc S., Leite S., Moreno A., Fereres A. Cauliflower mosaic virus is preferentially acquired from the phloem by its aphid. J. Gen. Virol. 83:2002;3163-3171
60. Pancholi V., Fischetti V.A. A major surface protein on group A streptococci is a glyceraldehydes-3-phosphate dehydrogenase with multiple activity. J. Exp. Med. 176:1992;415-426
61. Pederson K.J. Structure and composition of basement membranes and other basal lamina matrix systems in selected invertebrates. Acta Zool. 72:1991;181-201
62. Peiffer M.L., Gildow F.E., Gray S.M. Two distinct mechanisms regulate luteovirus transmission efficiency and specificity at the aphid salivary gland. J. Gen. Virol. 78:1997;495-503
63. Reinbold C., Gildow F.E., Herrbach E., Ziegler-Graff V., Gonçalves M.C., van den Heuvel J.F.J.M., Brault V. Studies on the role of the minor capsid protein in transport of beet western yellows virus through Myzus persicae. J. Gen. Virol. 82:2001;1995-2007
64. 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. 84:2003;3473-3484
65. Rochow W.F., Foxe M.J., Muller I. A mechanism of vector specificity for circulative aphid-transmitted plant viruses. Ann. N. Y. Acad. Sci. 266:1975;293-301
66. Roivanen M., Piirainen L., Rysä T., Närvänen A., Hovi T. An immunodominant N-terminal region of VP1 protein of poliovirus that is buried in crystal structure can be exposed in solution. Virology. 195:1993;762-765
67. Ron D., Mochly-Rosen D. Agonists and antagonists of protein kinase C function, derived from its binding proteins. J. Biol. Chem. 269:1994;21395-21398
68. Ron D., Mochly-Rosen D. An autoregulatory region in protein kinase C: the pseudoanchoring site. Proc. Natl. Acad. Sci. U.S.A. 92:1995;492-496
69. Ron D., Chen C.H., Caldwell J., Jamieson L., Orr E., Mochly-Rosen D. Cloning of an intracellular receptor for protein kinase C: a homolog of the beta subunit of G proteins. Proc. Natl. Acad. Sci. U.S.A. 91:1995;839-843
70. Ron D., Jiang Z., Yao L., Vagts A., Diamond I., Gordon A. Coordinated movement of RACK1 with activated βIIPKC. J. Biol. Chem. 274:1999;27039-27046
71. Roth M.G. Endocytic receptors. Adv. Cell Mol. Biol. Membr. 1:1993;19-50
72. Rouzé-Jouan J., Terradot L., Pasquer F., Tanguy S., Giblot Ducray-Bourdin D. The passage of potato leafroll virus through Myzus persicae gut membrane regulates transmission efficiency. J. Gen. Virol. 82:2001;17-23
73. Schmitz H.-D., Bereiter-Hahn J. Glyceraldehyde-3-phosphate dehydrogenase associates with actin filaments in serum deprived NIH 3T3 cells only. Cell Biol. Int. 26:2002;155-164
74. Seddas A., Haidar M.M., Greif C., Jacquet C., Cloquemin G., Walter B. Establishment of a serological relationship between grapevine leafroll closteroviruses 1 and 3 by use of monoclonal antibodies. Plant Pathol. 49:2000;80-85
75. Sieczkarski S.B., Whittaker G.R. Dissecting virus entry via endocytosis. J. Gen. Virol. 83:2002;1535-1545
76. Sirover M.A. Role of the glycolytic protein, glyceraldehyde-3-phosphate dehydrogenase, in normal cell function and in cell pathology. J. Cell. Biochem. 66:1997;133-140
77. Sirover M.A. New insights into an old protein: the functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase. Biochim. Biophys. Acta. 1432:1999;159-184
78. Somers M., Engelborghs Y., Baert J. Analysis of the binding of glyceraldehyde-3-phosphate dehydrogenase to microtubules, the mechanism of bundle formation and the linkage effect. Eur. J. Biochem. 193:1990;437-444
79. Tisdale E.J. Glyceraldehyde-3-phosphate dehydrogenase is phosphorylated by protein kinase C ι/λ and plays a role in microtubule dynamics in the early secretory pathway. J. Biol. Chem. 277:2002;3334-3341
80. Van den Heuvel J.F.J.M., Boerma T.M., Peters D. Transmission of potato leafroll virus from plants and artificial diets by Myzus persicae. Phytopathology. 81:1991;150-154
81. Van den Heuvel J.F.J.M., Verbeek M., van der Wilk F. Endosymbiotic bacteria associated with circulative transmission of potato leafroll virus by Myzus persicae. J. Gen. Virol. 75:1994;2559-2565
82. Van den Heuvel J.F.J.M., 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. 71:1997;7258-7265
83. Van de Walle G.R., Favoreel H.W., Nauwynck H.J., Van Oostveldt P., Pensaert M.B. Involvement of cellular cytoskeleton components in antibody-induced internalization of viral glycoproteins in pseudorabies virus-infected monocytes. Virology. 288:2001;129-138
84. Vani K., Yang G., Mohler J. Isolation and cloning of a Drosophila homolog to the mammalian RACK1 gene, implicated in PKC-mediated signalling. Biochim. Biophys. Acta. 1358:1997;67-71
85. Van Regenmortel M.H.V. Monoclonal antibodies in plant virology. Microbiol. Sci. 1:1984;73-78
86. Volker K.W., Reinitz C.A., Knull H.R. Glycolytic enzymes and assembly of microtubule networks. Comp. Biochem. Physiol. 112B:1995;503-514
87. Wang W., Huang Y., Zhou Z., Tang R., Zhao W., Zeng L., Xu M., Cheng C., Gu S., Ying K., Xie Y., Mao Y. Identification and characterization of AGTRAP, a human homolog of murine angiotensin II receptor-associated protein (Agtrap). Int. J. Biochem. Cell Biol. 34:2002;93-102
88. Zhou G., Lu X., Lu H., Lei J., Chen S., Gong Z. Rice ragged stunt oryzavirus: role of the viral spike protein in transmission by the insect vector. Ann. Appl. Biol. 135:1999;573-578