Skip to main content
Springer Nature - PMC COVID-19 Collection logoLink to Springer Nature - PMC COVID-19 Collection
. 2006 Feb 24;4:309–330. doi: 10.1007/7089_061

The ER in Replication of Positive-Strand RNA Viruses

Christophe Ritzenthaler 1,, Rabab Elamawi 1
Editor: David G Robinson
PMCID: PMC7122339

Abstract

All eukaryotic positive-sense single-strand RNA viruses, (+)ssRNA, replicate their genome in associationwith membranes of host cells. The presence of a replicating virus frequently induces proliferationand rearrangement of the host membranes into various cytopathic structures, including invaginations, vesicles,spherules or membranous webs. Such structures are considered to be virus-induced organelles specializedin replication functions. Virtually all membranes are able to be rearranged to support replication. Thus,membranes from peroxisomes, endosomes, lysosomes, vacuoles, mitochondria, and chloroplasts are used for(+)ssRNA virus replication, but the endoplasmic reticulum (ER) is by far the preferred organelle. The specifictype of membrane system utilized in assembling the viral replication complex is strictly dependent on individualviruses and is likely to be genetically determined. The various molecular interactions that govern ER targetingof plant viruses highlight how viruses can exploit the diversity of interactions that occurs between proteinsand membrane or lipid structures.

Keywords: Mosaic Virus, Tobacco Mosaic Virus, Cucumber Mosaic Virus, Replication Complex, Brome Mosaic Virus

Contributor Information

David G. Robinson, Email: david.robinson@urz.uni-heidelberg.de

Christophe Ritzenthaler, Email: christophe.ritzenthaler@ibmp-ulp.u-strasbg.fr.

References

  • 1.Agirre A, Barco A, Carrasco L, Nieva JL. Viroporin-mediated membrane permeabilization. Pore formation by nonstructural poliovirus 2B protein. J Biol Chem. 2002;277:40434–40441. doi: 10.1074/jbc.M205393200. [DOI] [PubMed] [Google Scholar]
  • 2.Ahlquist P. RNA-dependent RNA polymerases, viruses, and RNA silencing. Science. 2002;296:1270–1273. doi: 10.1126/science.1069132. [DOI] [PubMed] [Google Scholar]
  • 3.Ahlquist P. Bromovirus RNA replication and transcription. Curr Opin Genet Dev. 1992;2:71–76. doi: 10.1016/S0959-437X(05)80325-9. [DOI] [PubMed] [Google Scholar]
  • 4.Ahola T, Ahlquist P. Putative RNA capping activities encoded by brome mosaic virus: methylation and covalent binding of guanylate by replicase protein 1a. J Virol. 1999;73:10061–10069. doi: 10.1128/jvi.73.12.10061-10069.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Ahola T, den Boon, Ahlquist P. Helicase and capping enzyme active site mutations in brome mosaic virus protein 1a cause defects in template recruitment, negative-strand RNA synthesis, and viral RNA capping. J Virol. 2000;74:8803–8811. doi: 10.1128/JVI.74.19.8803-8811.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Ahola T, Lampio A, Auvinen P, Kaariainen L. Semliki Forest virus mRNA capping enzyme requires association with anionic membrane phospholipids for activity. Embo J. 1999;18:3164–3172. doi: 10.1093/emboj/18.11.3164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Andret-Link P, Laporte C, Valat L, Ritzenthaler C, Demangeat G, Vigne E, Laval V, Pfeiffer P, Fuchs M. Grapevine fanleaf virus: still a major threat to the grapevine industry. J Plant Pathol. 2004;86:183–195. [Google Scholar]
  • 8.Banerjee R, Weidman MK, Echeverri A, Kundu P, Dasgupta A. Regulation of poliovirus 3C protease by the 2C polypeptide. J Virol. 2004;78:9243–9256. doi: 10.1128/JVI.78.17.9243-9256.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Bansal PK, Sharma P, Mondal AK. A PBS2 homologue from Debaryomyces hansenii shows a differential effect on calcofluor and polymyxin B sensitivity in Saccharomyces cerevisiae. Yeast. 2001;18:1207–1216. doi: 10.1002/yea.769. [DOI] [PubMed] [Google Scholar]
  • 10.Baulcombe D. RNA silencing in plants. Nature. 2004;431:356–363. doi: 10.1038/nature02874. [DOI] [PubMed] [Google Scholar]
  • 11.Belov GA, Fogg MH, Ehrenfeld E. Poliovirus proteins induce membrane association of GTPase ADP-ribosylation factor. J Virol. 2005;79:7207–7216. doi: 10.1128/JVI.79.11.7207-7216.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Bleve-Zacheo T, Rubino L, Melillo MT, Russo aM. The 33K protein encoded by cymbidium ringspot tombusvirus localizes to modified peroxisomes of infected cells and of uninfected transgenic plant. J Plant Pathol. 1997;79:179–202. [Google Scholar]
  • 13.Boguslawski G. PBS2, a yeast gene encoding a putative protein kinase, interacts with the RAS2 pathway and affects osmotic sensitivity of Saccharomyces cerevisiae. J Gen Microbiol. 1992;138:2425–2432. doi: 10.1099/00221287-138-11-2425. [DOI] [PubMed] [Google Scholar]
  • 14.Bolten R, Egger D, Gosert R, Schaub G, Landmann L, Bienz K. Intracellular localization of poliovirus plus- and minus-strand RNA visualized by strand-specific fluorescent In situ hybridization. J Virol. 1998;72:8578–8585. doi: 10.1128/jvi.72.11.8578-8585.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Brill LM, Dechongkit S, DeLaBarre B, Stroebel J, Beachy RN, Yeager M. Dimerization of recombinant tobacco mosaic virus movement protein. J Virol. 2004;78:3372–3377. doi: 10.1128/JVI.78.5.3372-3377.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Brill LM, Nunn RS, Kahn TW, Yeager M, Beachy RN. Recombinant tobacco mosaic virus movement protein is an RNA-binding, alpha-helical membrane protein. Proc Natl Acad Sci USA. 2000;97:7112–7117. doi: 10.1073/pnas.130187897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Buck KW. Replication of tobacco mosaic virus RNA. Philos Trans R Soc Lond B Biol Sci. 1999;354:613–627. doi: 10.1098/rstb.1999.0413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Burgyan J, Rubino L, Russo M. The 5′-terminal region of a tombusvirus genome determines the origin of multivesicular bodies. J Gen Virol. 1996;77:1967–1974. doi: 10.1099/0022-1317-77-8-1967. [DOI] [PubMed] [Google Scholar]
  • 19.Carette JE, Guhl K, Wellink J, Van Kammen A. Coalescence of the sites of cowpea mosaic virus RNA replication into a cytopathic structure. J Virol. 2002;76:6235–6243. doi: 10.1128/JVI.76.12.6235-6243.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Carette JE, Kujawa A, Guhl K, Verver J, Wellink J, Van Kammen A. Mutational analysis of the genome-linked protein of cowpea mosaic virus. Virology. 2001;290:21–29. doi: 10.1006/viro.2001.1137. [DOI] [PubMed] [Google Scholar]
  • 21.Carette JE, Stuiver M, Van Lent J, Wellink J, Van Kammen A. Cowpea mosaic virus infection induces a massive proliferation of endoplasmic reticulum but not Golgi membranes and is dependent on de novo membrane synthesis. J Virol. 2000;74:6556–6563. doi: 10.1128/JVI.74.14.6556-6563.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Carette JE, van Lent J, MacFarlane SA, Wellink J, van Kammen A. Cowpea mosaic virus 32- and 60-kilodalton replication proteins target and change the morphology of endoplasmic reticulum membranes. J Virol. 2002;76:6293–6301. doi: 10.1128/JVI.76.12.6293-6301.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Carette JE, Verver J, Martens J, van Kampen T, Wellink J, van Kammen A. Characterization of plant proteins that interact with cowpea mosaic virus 60 Kprotein in the yeast two-hybrid system. J Gen Virol. 2002;83:885–893. doi: 10.1099/0022-1317-83-4-885. [DOI] [PubMed] [Google Scholar]
  • 24.Carrier K, Xiang Y, Sanfaçon H. Genomic organization of RNA2 of Tomato ringspot virus: processing at a third cleavage site in the N-terminal region of the polyprotein in vitro. J Gen Virol. 2001;82:1785–1790. doi: 10.1099/0022-1317-82-7-1785. [DOI] [PubMed] [Google Scholar]
  • 25.Chen SH, Chen S, Tokarev AA, Liu F, Jedd G, Segev N. Ypt31/32 GTPases and their novel F-box effector protein Rcy1 regulate protein recycling. Mol Biol Cell. 2005;16:178–192. doi: 10.1091/mbc.E04-03-0258. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Cho MW, Teterina N, Egger D, Bienz K, Ehrenfeld E. Membrane rearrangement and vesicle induction by recombinant poliovirus 2C and 2BC in human cells. Virology. 1994;202:129–145. doi: 10.1006/viro.1994.1329. [DOI] [PubMed] [Google Scholar]
  • 27.Choe SS, Dodd DA, Kirkegaard K. Inhibition of cellular protein secretion by picornaviral 3A proteins. Virology. 2005;337:18–29. doi: 10.1016/j.virol.2005.03.036. [DOI] [PubMed] [Google Scholar]
  • 28.Cillo F, Roberts IM, Palukaitis P. In situ localization and tissue distribution of the replication-associated proteins of Cucumber mosaic virus in tobacco and cucumber. J Virol. 2002;76:10654–10664. doi: 10.1128/JVI.76.21.10654-10664.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Cuconati A, Molla A, Wimmer E. Brefeldin A inhibits cell-free, de novo synthesis of poliovirus. J Virol. 1998;72:6456–6464. doi: 10.1128/jvi.72.8.6456-6464.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.de Jong AS, Schrama IW, Willems PH, Galama JM, Melchers WJ, van Kuppeveld FJ. Multimerization reactions of coxsackievirus proteins 2B, 2C and 2BC: a mammalian two-hybrid analysis. J Gen Virol. 2002;83:783–793. doi: 10.1099/0022-1317-83-4-783. [DOI] [PubMed] [Google Scholar]
  • 31.De Zoeten GA, Assink AM, van Kammen A. Association of cowpea mosaic virus-induced double-stranded RNA with a cytopathological structure in infected cells. Virology. 1974;59:341–355. doi: 10.1016/0042-6822(74)90449-8. [DOI] [PubMed] [Google Scholar]
  • 32.Dessens JT, Lomonossoff GP. Mutational analysis of the putative catalytic triad of the cowpea mosaic virus 24K protease. Virology. 1991;184:738–746. doi: 10.1016/0042-6822(91)90444-G. [DOI] [PubMed] [Google Scholar]
  • 33.dos Reis, Golem S, Goregaoker SP, Culver JN. A nuclear localization signal and a membrane association domain contribute to the cellular localization of the Tobacco mosaic virus 126-kDa replicase protein. Virology. 2002;301:81–89. doi: 10.1006/viro.2002.1560. [DOI] [PubMed] [Google Scholar]
  • 34.Eggen R, Kaan A, Goldbach R, Van Kammen A. Cowpea mosaic virus RNA replication in crude membrane fractions from infected cowpea and Chenopodium armaranticolor. J Gen Virol. 1988;69:2711–2720. doi: 10.1099/0022-1317-69-11-2711. [DOI] [Google Scholar]
  • 35.Egger D, Gosert R, Bienz K. Role of cellular structures in viral RNA replication. In: Semler BL, Wimmer C, editors. Molecular biology of Picornaviruses. Washington DC: ASM; 2002. pp. 247–253. [Google Scholar]
  • 36.Egger D, Teterina N, Ehrenfeld E, Bienz K. Formation of the poliovirus replication complex requires coupled viral translation, vesicle production, and viral RNA synthesis. J Virol. 2000;74:6570–6580. doi: 10.1128/JVI.74.14.6570-6580.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Egger Da, Bienz K. Intracellular location and translocation of silent and active poliovirus replication complexes. J Gen Virol. 2005;86:707–718. doi: 10.1099/vir.0.80442-0. [DOI] [PubMed] [Google Scholar]
  • 38.Esau K, Cronshaw J. Relation of tobacco mosaic virus to the host cells. J Cell Biol. 1967;33:665–678. doi: 10.1083/jcb.33.3.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39.Faergeman NJ, Feddersen S, Christiansen JK, Larsen MK, Schneiter R, Ungermann C, Mutenda K, Roepstorff P, Knudsen J. Acyl-CoA-binding protein, Acb1p, is required for normal vacuole function and ceramide synthesis in Saccharomyces cerevisiae. Biochem J. 2004;380:907–918. doi: 10.1042/BJ20031949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Francki RIB, Milne RG, Hatta T. Atlas of plant viruses. Boca Raton: CRC; 1985. Nepovirus group. [Google Scholar]
  • 41.Gaire F, Schmitt C, Stussi-Garaud C, Pinck L, Ritzenthaler C. Protein 2A of grapevine fanleaf nepovirus is implicated in RNA2 replication and colocalizes to the replication site. Virology. 1999;264:25–36. doi: 10.1006/viro.1999.9927. [DOI] [PubMed] [Google Scholar]
  • 42.Goelet P, Lomonossoff GP, Butler PJ, Akam ME, Gait MJ, Karn J. Nucleotide sequence of tobacco mosaic virus RNA. Proc Natl Acad Sci USA. 1982;79:5818–5822. doi: 10.1073/pnas.79.19.5818. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Grant B, Greenwald I. Structure, function, and expression of SEL-1, a negative regulator of LIN-12 and GLP-1 in C. elegans. Development. 1997;124:637–644. doi: 10.1242/dev.124.3.637. [DOI] [PubMed] [Google Scholar]
  • 44.Hagiwara Y, Komoda K, Yamanaka T, Tamai A, Meshi T, Funada R, Tsuchiya T, Naito S, Ishikawa M. Subcellular localization of host and viral proteins associated with tobamovirus RNA replication. Embo J. 2003;22:344–353. doi: 10.1093/emboj/cdg033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.Han S, Sanfaçon H. Tomato ringspot virus proteins containing the nucleoside triphosphate binding domain are transmembrane proteins that associate with the endoplasmic reticulum and cofractionate with replication complexes. J Virol. 2003;77:523–534. doi: 10.1128/JVI.77.1.523-534.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Hans F, Sanfaçon H. Tomato ringspot nepovirus protease: characterization and cleavage site specificity. J Gen Virol. 1995;76:917–927. doi: 10.1099/0022-1317-76-4-917. [DOI] [PubMed] [Google Scholar]
  • 47.Hatta T, Bullivant S, Matthews RE. Fine structure of vesicles induced in chloroplasts of Chinese cabbage leaves by infection with turnip yellow mosaic virus. J Gen Virol. 1973;20:37–50. doi: 10.1099/0022-1317-20-1-37. [DOI] [PubMed] [Google Scholar]
  • 48.Heinlein M. The spread of tobacco mosaic virus infection: insights into the cellular mechanism of RNA transport. Cell Mol Life Sci. 2002;59:58–82. doi: 10.1007/s00018-002-8406-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49.Heinlein M, Padgett HS, Gens JS, Pickard BG, Casper SJ, Epel BL, Beachy RN. Changing patterns of localization of the tobacco mosaic virus movement protein and replicase to the endoplasmic reticulum and microtubules during infection. Plant Cell. 1998;10:1107–1120. doi: 10.1105/tpc.10.7.1107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Hills GJ, Plaskitt KA, Young ND, Dunigan DD, Watts JW, Wilson TM, Zaitlin M. Immunogold localization of the intracellular sites of structural and nonstructural tobacco mosaic virus proteins. Virology. 1987;161:488–496. doi: 10.1016/0042-6822(87)90143-7. [DOI] [PubMed] [Google Scholar]
  • 51.Hughes TM. The diagnosis of gastrointestinal tract injuries resulting from blunt trauma. Aust N Z J Surg. 1999;69:770–777. doi: 10.1046/j.1440-1622.1999.01693.x. [DOI] [PubMed] [Google Scholar]
  • 52.Ishikawa M, Janda M, Krol MA, Ahlquist P. In vivo DNA expression of functional brome mosaic virus RNA replicons in Saccharomyces cerevisiae. J Virol. 1997;71:7781–7790. doi: 10.1128/jvi.71.10.7781-7790.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.Ivanowski D. Über die Mosaikkrankheit der Tabakspflanze. Z Pflanzenkr Pflanzenschutz. 1903;13:1–41. [Google Scholar]
  • 54.Jackson WT, Giddings TH, Taylor MP, Mulinyawe S, Rabinovitch M, Kopito RR, Kirkegaard K. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 2005;3:e156. doi: 10.1371/journal.pbio.0030156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55.Janda M, Ahlquist P. Brome mosaic virus RNA replication protein 1a dramatically increases in vivo stability but not translation of viral genomic RNA3. Proc Natl Acad Sci USA. 1998;95:2227–2232. doi: 10.1073/pnas.95.5.2227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56.Janda M, Ahlquist P. RNA-dependent replication, transcription, and persistence of brome mosaic virus RNA replicons in S. cerevisiae. Cell. 1993;72:961–970. doi: 10.1016/0092-8674(93)90584-D. [DOI] [PubMed] [Google Scholar]
  • 57.Kao CC, Ahlquist P. Identification of the domains required for direct interaction of the helicase-like and polymerase-like RNA replication proteins of brome mosaic virus. J Virol. 1992;66:7293–7302. doi: 10.1128/jvi.66.12.7293-7302.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.Klapholz S, Esposito RE. Isolation of SPO12-1 and SPO13-1 from a natural variant of yeast that undergoes a single meiotic division. Genetics. 1980;96:567–588. doi: 10.1093/genetics/96.3.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59.Kong F, Sivakumaran K, Kao C. The N-terminal half of the brome mosaic virus 1a protein has RNA capping-associated activities: specificity for GTP and S-adenosylmethionine. Virology. 1999;259:200–210. doi: 10.1006/viro.1999.9763. [DOI] [PubMed] [Google Scholar]
  • 60.Koonin EV, Dolja VV. Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit Rev Biochem Mol Biol. 1993;28:375–430. doi: 10.3109/10409239309078440. [DOI] [PubMed] [Google Scholar]
  • 61.Kushner DB, Lindenbach BD, Grdzelishvili VZ, Noueiry AO, Paul SM, Ahlquist P. Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus. Proc Natl Acad Sci USA. 2003;100:15764–15769. doi: 10.1073/pnas.2536857100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62.Lampio A, Kilpelainen I, Pesonen S, Karhi K, Auvinen P, Somerharju P, Kaariainen L. Membrane binding mechanism of an RNA virus-capping enzyme. J Biol Chem. 2000;275:37853–37859. doi: 10.1074/jbc.M004865200. [DOI] [PubMed] [Google Scholar]
  • 63.Laporte C, Vetter G, Loudes AM, Robinson DG, Hillmer S, Stussi-Garaud C, Ritzenthaler C. Involvement of the secretory pathway and the cytoskeleton in intracellular targeting and tubule assembly of Grapevine fanleaf virus movement protein in tobacco BY-2 cells. Plant Cell. 2003;15:2058–2075. doi: 10.1105/tpc.013896. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Lee WM, Ahlquist P. Membrane synthesis, specific lipid requirements, and localized lipid composition changes associated with a positive-strand RNA virus RNA replication protein. J Virol. 2003;77:12819–12828. doi: 10.1128/JVI.77.23.12819-12828.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 65.Lee WM, Ishikawa M, Ahlquist P. Mutation of host delta9 fatty acid desaturase inhibits brome mosaic virus RNA replication between template recognition and RNA synthesis. J Virol. 2001;75:2097–2106. doi: 10.1128/JVI.75.5.2097-2106.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 66.Li X, Lu HH, Mueller S, Wimmer E. The C-terminal residues of poliovirus proteinase 2A(pro) are critical for viral RNA replication but not for cis- or trans-proteolytic cleavage. J Gen Virol. 2001;82:397–408. doi: 10.1099/0022-1317-82-2-397. [DOI] [PubMed] [Google Scholar]
  • 67.Loewen CJ, Levine TP. A highly conserved binding site in vesicle-associated membrane protein-associated protein (VAP) for the FFAT motif of lipid-binding proteins. J Biol Chem. 2005;280:14097–14104. doi: 10.1074/jbc.M500147200. [DOI] [PubMed] [Google Scholar]
  • 68.Lyle JM, Bullitt E, Bienz K, Kirkegaard K. Visualization and functional analysis of RNA-dependent RNA polymerase lattices. Science. 2002;296:2218–2222. doi: 10.1126/science.1070585. [DOI] [PubMed] [Google Scholar]
  • 69.Margis R, Ritzenthaler C, Reinbolt J, Pinck M, Pinck L. Genome organization of grapevine fanleaf nepovirus RNA2 deduced from the 122K polyprotein P2 in vitro cleavage products. J Gen Virol. 1993;74:1919–1926. doi: 10.1099/0022-1317-74-9-1919. [DOI] [PubMed] [Google Scholar]
  • 70.Margis R, Viry M, Pinck M, Bardonnet N, Pinck L. Differential proteolytic activities of precursor and mature forms of the 24K proteinase of grapevine fanleaf nepovirus. Virology. 1994;200:79–86. doi: 10.1006/viro.1994.1165. [DOI] [PubMed] [Google Scholar]
  • 71.Martelli GP, Russo M. Plant virus inclusion bodies. Adv Virus Res. 1977;21:175–266. doi: 10.1016/S0065-3527(08)60763-0. [DOI] [PubMed] [Google Scholar]
  • 72.Mas P, Beachy RN. Replication of tobacco mosaic virus on endoplasmic reticulum and role of the cytoskeleton and virus movement protein in intracellular distribution of viral RNA. J Cell Biol. 1999;147:945–958. doi: 10.1083/jcb.147.5.945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 73.Mise K, Ahlquist P. Host-specificity restriction by bromovirus cell-to-cell movement protein occurs after initial cell-to-cell spread of infection in nonhost plants. Virology. 1995;206:276–286. doi: 10.1016/S0042-6822(95)80043-3. [DOI] [PubMed] [Google Scholar]
  • 74.Moche M, Schneider G, Edwards P, Dehesh K, Lindqvist Y. Structure of the complex between the antibiotic cerulenin and its target, beta-ketoacyl-acyl carrier protein synthase. J Biol Chem. 1999;274:6031–6034. doi: 10.1074/jbc.274.10.6031. [DOI] [PubMed] [Google Scholar]
  • 75.Moore PJ, Fenczik CA, Beachy RN. Developmental changes in plasmodesmata in transgenic plants expressing the movement protein of tobacco mosaic virus. Protoplasma. 1992;170:115–127. doi: 10.1007/BF01378787. [DOI] [Google Scholar]
  • 76.Moradpour D, Gosert R, Egger D, Penin F, Blum HE, Bienz K. Membrane association of hepatitis C virus nonstructural proteins and identification of the membrane alteration that harbors the viral replication complex. Antiviral Res. 2003;60:103–109. doi: 10.1016/j.antiviral.2003.08.017. [DOI] [PubMed] [Google Scholar]
  • 77.Moriishi K, Matsuura Y. Mechanisms of hepatitis C virus infection. Antivir Chem Chemother. 2003;14:285–297. doi: 10.1177/095632020301400601. [DOI] [PubMed] [Google Scholar]
  • 78.Nakano A. Yeast Golgi apparatus – dynamics and sorting. Cell Mol Life Sci. 2004;61:186–191. doi: 10.1007/s00018-003-3356-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 79.Natarajan P, Wang J, Hua Z, Graham TR. Drs2p-coupled aminophospholipid translocase activity in yeast Golgi membranes and relationship to in vivo function. Proc Natl Acad Sci USA. 2004;101:10614–10619. doi: 10.1073/pnas.0404146101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 80.Navarro B, Rubino L, Russo M. Expression of the Cymbidium ringspot virus 33-kilodalton protein in Saccharomyces cerevisiae and molecular dissection of the peroxisomal targeting signal. J Virol. 2004;78:4744–4752. doi: 10.1128/JVI.78.9.4744-4752.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 81.Noueiry AO, Ahlquist P. Brome mosaic virus RNA replication: revealing the role of the host in RNA virus replication. Annu Rev Phytopathol. 2003;41:77–98. doi: 10.1146/annurev.phyto.41.052002.095717. [DOI] [PubMed] [Google Scholar]
  • 82.O'Reilly EK, Paul JD, Kao CC. Analysis of the interaction of viral RNA replication proteins by using the yeast two-hybrid assay. J Virol. 1997;71:7526–7532. doi: 10.1128/jvi.71.10.7526-7532.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 83.O'Reilly EK, Tang N, Ahlquist P, Kao CC. Biochemical and genetic analyses of the interaction between the helicase-like and polymerase-like proteins of the brome mosaic virus. Virology. 1995;214:59–71. doi: 10.1006/viro.1995.9954. [DOI] [PubMed] [Google Scholar]
  • 84.O'Reilly EK, Wang Z, French R, Kao CC. Interactions between the structural domains of the RNA replication proteins of plant-infecting RNA viruses. J Virol. 1998;72:7160–7169. doi: 10.1128/jvi.72.9.7160-7169.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 85.Osman TA, Buck KW. Complete replication in vitro of tobacco mosaic virus RNA by a template-dependent, membrane-bound RNA polymerase. J Virol. 1996;70:6227–6234. doi: 10.1128/jvi.70.9.6227-6234.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 86.Pelham HR. The dynamic organisation of the secretory pathway. Cell Struct Funct. 1996;21:413–419. doi: 10.1247/csf.21.413. [DOI] [PubMed] [Google Scholar]
  • 87.Pelham HR. Leaky UAG termination codon in tobacco mosaic virus RNA. Nature. 1978;272:469–471. doi: 10.1038/272469a0. [DOI] [PubMed] [Google Scholar]
  • 88.Peters SA, Verver J, Nollen EA, van Lent JW, Wellink J, van Kammen A. The NTP-binding motif in cowpea mosaic virus B polyprotein is essential for viral replication. J Gen Virol. 1994;75:3167–3176. doi: 10.1099/0022-1317-75-11-3167. [DOI] [PubMed] [Google Scholar]
  • 89.Peters SA, Voorhorst WG, Wery J, Wellink J, van Kammen A. A regulatory role for the 32K protein in proteolytic processing of cowpea mosaic virus polyproteins. Virology. 1992;191:81–89. doi: 10.1016/0042-6822(92)90168-O. [DOI] [PubMed] [Google Scholar]
  • 90.Prod'homme D, Jakubiec A, Tournier V, Drugeon G, Jupin I. Targeting of the turnip yellow mosaic virus 66K replication protein to the chloroplast envelope is mediated by the 140 Kprotein. J Virol. 2003;77:9124–9135. doi: 10.1128/JVI.77.17.9124-9135.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 91.Prod'homme D, Le Panse S, Drugeon G, Jupin I. Detection and subcellular localization of the turnip yellow mosaic virus 66 Kreplication protein in infected cells. Virology. 2001;281:88–101. doi: 10.1006/viro.2000.0769. [DOI] [PubMed] [Google Scholar]
  • 92.Raikhel N, Chrispeels MJ. Membrane structure and membranous organelles. In: Buchanan BB, Gruissem W, Jones LR, editors. Biochemistry & molecular biology of plants. Rockville: American Society of Plant Physiologists; 2000. [Google Scholar]
  • 93.Rasmussen JT, Faergeman NJ, Kristiansen K, Knudsen J. Acyl-CoA-binding protein (ACBP) can mediate intermembrane acyl-CoA transport and donate acyl-CoA for beta-oxidation and glycerolipid synthesis. Biochem J. 1994;299:165–170. doi: 10.1042/bj2990165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 94.Rasmussen JT, Rosendal J, Knudsen J. Interaction of acyl-CoA binding protein (ACBP) on processes for which acyl-CoA is a substrate, product or inhibitor. Biochem J. 1993;292:907–913. doi: 10.1042/bj2920907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 95.Reichel C, Beachy RN. Tobacco mosaic virus infection induces severe morphological changes of the endoplasmic reticulum. Proc Natl Acad Sci USA. 1998;95:11169–11174. doi: 10.1073/pnas.95.19.11169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 96.Restrepo-Hartwig M, Ahlquist P. Brome mosaic virus RNA replication proteins 1a and 2a colocalize and 1a independently localizes on the yeast endoplasmic reticulum. J Virol. 1999;73:10303–10309. doi: 10.1128/jvi.73.12.10303-10309.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 97.Ripmaster TL, Vaughn GP, Woolford JL. DRS1 to DRS7, novel genes required for ribosome assembly and function in Saccharomyces cerevisiae. Mol Cell Biol. 1993;13:7901–7912. doi: 10.1128/mcb.13.12.7901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 98.Ritzenthaler C, Laporte C, Gaire F, Dunoyer P, Schmitt C, Duval S, Piequet A, Loudes AM, Rohfritsch O, Stussi-Garaud C, Pfeiffer P. Grapevine fanleaf virus replication occurs on endoplasmic reticulum-derived membranes. J Virol. 2002;76:8808–8819. doi: 10.1128/JVI.76.17.8808-8819.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 99.Ritzenthaler C, Schmit A-C, Michler P, Stussi-Garaud C, Pinck L. Grapevine fanleaf nepovirus putative movement protein is involved in tubule formation in vivo. Mol Plant-Microbe Interact. 1995;8:379–387. doi: 10.1094/MPMI-8-0379. [DOI] [Google Scholar]
  • 100.Ritzenthaler C, Viry M, Pinck M, Margis R, Fuchs M, Pinck L. Complete nucleotide sequence and genetic organization of grapevine fanleaf nepovirus RNA1. J Gen Virol. 1991;72:2357–2365. doi: 10.1099/0022-1317-72-10-2357. [DOI] [PubMed] [Google Scholar]
  • 101.Rott ME, Gilchrist A, Lee L, Rochon D. Nucleotide sequence of tomato ringspot virus RNA1. J Gen Virol. 1995;76(2):465–473. doi: 10.1099/0022-1317-76-2-465. [DOI] [PubMed] [Google Scholar]
  • 102.Rubino L, Russo M. Membrane targeting sequences in tombusvirus infections. Virology. 1998;252:431–437. doi: 10.1006/viro.1998.9490. [DOI] [PubMed] [Google Scholar]
  • 103.Rubino L, Weber-Lotfi F, Dietrich A, Stussi-Garaud C, Russo M. The open reading frame 1-encoded (36 K) protein of Carnation Italian ringspot virus localizes to mitochondria. J Gen Virol. 2001;82:29–34. doi: 10.1099/0022-1317-82-1-29. [DOI] [PubMed] [Google Scholar]
  • 104.Rust RC, Landmann L, Gosert R, Tang BL, Hong W, Hauri HP, Egger D, Bienz K. Cellular COPII proteins are involved in production of the vesicles that form the poliovirus replication complex. J Virol. 2001;75:9808–9818. doi: 10.1128/JVI.75.20.9808-9818.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 105.Saito T, Hosokawa D, Meshi T, Okada Y. Immunocytochemical localization of the 130K and 180K proteins (putative replicase components) of tobacco mosaic virus. Virology. 1987;160:477–481. doi: 10.1016/0042-6822(87)90020-1. [DOI] [PubMed] [Google Scholar]
  • 106.Salonen A, Ahola T, Kääriäinen L. Viral RNA replication in association with cellular membranes. In: Marsh M, editor. Current Topics in Microbiology and Immunology, vol 285. Berlin Heidelberg New York: Springer; 2005. pp. 139–173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 107.Santos-Rosa H, Leung J, Grimsey N, Peak-Chew S, Siniossoglou S. The yeast lipin Smp2 couples phospholipid biosynthesis to nuclear membrane growth. Embo J. 2005;24:1931–1941. doi: 10.1038/sj.emboj.7600672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 108.Schaad MC, Jensen PE, Carrington JC. Formation of plant RNA virus replication complexes on membranes: role of an endoplasmic reticulum-targeted viral protein. Embo J. 1997;16:4049–4059. doi: 10.1093/emboj/16.13.4049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 109.Schwartz M, Chen J, Janda M, Sullivan M, den Boon, Ahlquist P. A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol Cell. 2002;9:505–514. doi: 10.1016/S1097-2765(02)00474-4. [DOI] [PubMed] [Google Scholar]
  • 110.Schwartz M, Chen J, Lee WM, Janda M, Ahlquist P. Alternate, virus-induced membrane rearrangements support positive-strand RNA virus genome replication. Proc Natl Acad Sci USA. 2004;101:11263–11268. doi: 10.1073/pnas.0404157101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 111.Shen X, Zhang K, Kaufman RJ. The unfolded protein response – a stress signaling pathway of the endoplasmic reticulum. J Chem Neuroanat. 2004;28:79–92. doi: 10.1016/j.jchemneu.2004.02.006. [DOI] [PubMed] [Google Scholar]
  • 112.Siniossoglou S, Santos-Rosa H, Rappsilber J, Mann M, Hurt E. A novel complex of membrane proteins required for formation of a spherical nucleus. Embo J. 1998;17:6449–6464. doi: 10.1093/emboj/17.22.6449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 113.Sivakumaran K, Bao Y, Roossinck MJ, Kao CC. Recognition of the core RNA promoter for minus-strand RNA synthesis by the replicases of Brome mosaic virus and Cucumber mosaic virus. J Virol. 2000;74:10323–10331. doi: 10.1128/JVI.74.22.10323-10331.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 114.Staehelin LA. The plant ER: a dynamic organelle composed of a large number of discrete functional domains. Plant J. 1997;11:1151–1165. doi: 10.1046/j.1365-313X.1997.11061151.x. [DOI] [PubMed] [Google Scholar]
  • 115.Staehelin LA, Newcomb EH. membrane structure and membranous organelles. In: Buchanan BB, Gruissem W, Jones LR, editors. Biochemistery & molecular biology of plants. Rockville: American Society of Plant Physiologists; 2000. [Google Scholar]
  • 116.Sullivan ML, Ahlquist P. A brome mosaic virus intergenic RNA3 replication signal functions with viral replication protein 1a to dramatically stabilize RNA in vivo. J Virol. 1999;73:2622–2632. doi: 10.1128/jvi.73.4.2622-2632.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 117.Sundaram M, Greenwald I. Suppressors of a lin-12 hypomorph define genes that interact with both lin-12 and glp-1 in Caenorhabditis elegans. Genetics. 1993;135:765–783. doi: 10.1093/genetics/135.3.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 118.Tsujimoto Y, Numaga T, Ohshima K, Yano MA, Ohsawa R, Goto DB, Naito S, Ishikawa M. Arabidopsis Tobamovirus Multiplication (TOM) 2 locus encodes a transmembrane protein that interacts with TOM1. Embo J. 2003;22:335–343. doi: 10.1093/emboj/cdg034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 119.van Bokhoven H, van Lent JW, Custers R, Vlak JM, Wellink J, van Kammen A. Synthesis of the complete 200 Kpolyprotein encoded by cowpea mosaic virus B-RNA in insect cells. J Gen Virol. 1992;73:2775–2784. doi: 10.1099/0022-1317-73-11-2775. [DOI] [PubMed] [Google Scholar]
  • 120.van Bokhoven H, Verver J, Wellink J, van Kammen A. Protoplasts transiently expressing the 200K coding sequence of cowpea mosaic virus B-RNA support replication of M-RNA. J Gen Virol. 1993;74:2233–2241. doi: 10.1099/0022-1317-74-10-2233. [DOI] [PubMed] [Google Scholar]
  • 121.Van Der Heijden, Carette JE, Reinhoud PJ, Haegi A, Bol JF. Alfalfa mosaic virus replicase proteins P1 and P2 interact and colocalize at the vacuolar membrane. J Virol. 2001;75:1879–1887. doi: 10.1128/JVI.75.4.1879-1887.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 122.Viry M, Serghini MA, Hans F, Ritzenthaler C, Pinck M, Pinck L. Biologically active transcripts from cloned cDNA of genomic grapevine fanleaf nepovirus RNAs. J Gen Virol. 1993;74:169–174. doi: 10.1099/0022-1317-74-2-169. [DOI] [PubMed] [Google Scholar]
  • 123.Wang A, Carrier K, Chisholm J, Wieczorek A, Huguenot C, Sanfaçon H. Proteolytic processing of tomato ringspot nepovirus 3C-like protease precursors: definition of the domains for the VPg, protease and putative RNA-dependent RNA polymerase. J Gen Virol. 1999;80:799–809. doi: 10.1099/0022-1317-80-3-799. [DOI] [PubMed] [Google Scholar]
  • 124.Wang A, Han S, Sanfaçon H. Topogenesis in membranes of the NTB-VPg protein of Tomato ringspot nepovirus: definition of the C-terminal transmembrane domain. J Gen Virol. 2004;85:535–545. doi: 10.1099/vir.0.19612-0. [DOI] [PubMed] [Google Scholar]
  • 125.Wang A, Sanfaçon H. Proteolytic processing at a novel cleavage site in the N-terminal region of the tomato ringspot nepovirus RNA-1-encoded polyprotein in vitro. J Gen Virol. 2000;81:2771–2781. doi: 10.1099/0022-1317-81-11-2771. [DOI] [PubMed] [Google Scholar]
  • 126.Weber-Lotfi F, Dietrich A, Russo M, Rubino L. Mitochondrial targeting and membrane anchoring of a viral replicase in plant and yeast cells. J Virol. 2002;76:10485–10496. doi: 10.1128/JVI.76.20.10485-10496.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 127.Wellink J, Van Lent J, Goldbach R. Detection of viral proteins in cytopathic structures in cowpea protoplasts infected with cowpea mosaic virus. J Gen Virol. 1988;69:751–755. doi: 10.1099/0022-1317-69-3-751. [DOI] [Google Scholar]
  • 128.Wiederkehr A, Avaro S, Prescianotto-Baschong C, Haguenauer-Tsapis R, Riezman H. The F-box protein Rcy1p is involved in endocytic membrane traffic and recycling out of an early endosome in Saccharomyces cerevisiae. J Cell Biol. 2000;149:397–410. doi: 10.1083/jcb.149.2.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 129.Yamanaka T, Imai T, Satoh R, Kawashima A, Takahashi M, Tomita K, Kubota K, Meshi T, Naito S, Ishikawa M. Complete inhibition of tobamovirus multiplication by simultaneous mutations in two homologous host genes. J Virol. 2002;76:2491–2497. doi: 10.1128/jvi.76.5.2491-2497.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 130.Yamanaka T, Ohta T, Takahashi M, Meshi T, Schmidt R, Dean C, Naito S, Ishikawa M. TOM1, an Arabidopsis gene required for efficient multiplication of a tobamovirus, encodes a putative transmembrane protein. Proc Natl Acad Sci USA. 2000;97:10107–10112. doi: 10.1073/pnas.170295097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 131.Zabel P, Weenen-Swaans H, van Kammen A. In vitro replication of cowpea mosaic virus RNA: I. Isolation and properties of the membrane-bound replicase. J Virol. 1974;14:1049–1055. doi: 10.1128/jvi.14.5.1049-1055.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 132.Zhang SC, Zhang G, Yang L, Chisholm J, Sanfaçon H. Evidence that insertion of Tomato ringspot nepovirus NTB-VPg protein in endoplasmic reticulum membranes is directed by two domains: a C-terminal transmembrane helix and an N-terminal amphipathic helix. J Virol. 2005;79:11752–11765. doi: 10.1128/JVI.79.18.11752-11765.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 133.Zhao C, Beeler T, Dunn T. Suppressors of the Ca(2+)-sensitive yeast mutant (csg2) identify genes involved in sphingolipid biosynthesis. Cloning and characterization of SCS1, a gene required for serine palmitoyltransferase activity. J Biol Chem. 1994;269:21480–21488. [PubMed] [Google Scholar]

Articles from The Plant Endoplasmic Reticulum are provided here courtesy of Nature Publishing Group

RESOURCES