Cap-Independent Translational Enhancement by the 3′ Untranslated Region of
            <i>Red Clover Necrotic Mosaic Virus</i>
            RNA1

Mizumoto, Hiroyuki; Tatsuta, Masahiro; Kaido, Masanori; Mise, Kazuyuki; Okuno, Tetsuro

doi:10.1128/jvi.77.22.12113-12121.2003

Cited by 88 publications

(122 citation statements)

References 51 publications

(70 reference statements)

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“…Here we report on a different type of cap-independent translation element discovered in certain uncapped nonpolyadenylated plant viral and satellite RNAs including the Luteoviruses (Wang et al 1997) and members of the Tombusviridae family (Timmer et al 1993;Wu and White 1999;Mizumoto et al 2003;Meulewaeter et al 2004;Shen and Miller 2004;Batten et al 2006;Scheets and Redinbaugh 2006). Unlike IRES-mediated translation, the cap-independent translation element is present in the 39-untranslated region, yet translation initiation occurs at the AUG closest to the 59-end of the mRNA (Kneller et al 2006).…”

Section: Introductionmentioning

confidence: 96%

Oscillating kissing stem–loop interactions mediate 5′ scanning-dependent translation by a viral 3′-cap-independent translation element

Rakotondrafara¹,

Polacek²,

Harris³

et al. 2006

RNA

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The 39-untranslated regions (UTRs) of a group of novel uncapped viral RNAs allow efficient translation initiation at the 59-proximal AUG. A well-characterized model is the Barley yellow dwarf virus class of cap-independent translation elements (BTE). It facilitates translation by forming kissing stem-loops between the BTE in the 39-UTR and a BTE-complementary loop in the 59-UTR. Here we investigate the mechanisms of the long-distance interaction and ribosome entry on the RNA. Upstream AUGs or 59-extensions of the 59-UTR inhibit translation, indicating that, unlike internal ribosome entry sites in many viral RNAs, the BTE relies on 59-end-dependent ribosome scanning. Cap-independent translation occurs when the kissing sites are moved to different regions in either UTR, including outside of the BTE. The BTE can even confer cap-independent translation when fused to the 39-UTR of a reporter RNA harboring dengue virus sequences that cause base-pairing between the 39 and 59 ends. Thus, the BTE serves as a functional sensor to detect sequences capable of long-distance base-pairing. We propose that the kissing interaction is repeatedly disrupted by the scanning ribosome and re-formed in an oscillating process that regulates ribosome entry on the RNA.

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Section: Introductionmentioning

confidence: 96%

Oscillating kissing stem–loop interactions mediate 5′ scanning-dependent translation by a viral 3′-cap-independent translation element

Rakotondrafara¹,

Polacek²,

Harris³

et al. 2006

RNA

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“…These RNA structures have been termed 39-cap-independent translational enhancers (39CITEs) (Miller et al 2007). Functional 39CITEs have been reported for the aureusvirus Cucumber leafspot virus (CLSV) (Xu and White 2009); the carmoviruses Turnip crinkle virus (TCV) (Qu and Morris 2000;Stupina et al 2008), Hibiscus chlorotic ringspot virus (HCRSV) (Koh et al 2002), and Melon necrotic spot virus (MNSV) (Truniger et al 2008); the dianthovirus Red clover necrotic mosaic virus (RCNMV) (Mizumoto et al 2003); the necroviruses Tobacco necrosis virus (TNV) (Shen and Miller 2004;Meulewaeter et al 2004) and Satellite tobacco necrosis virus (STNV) (Danthinne et al 1993;Timmer et al 1993;Meulewaeter et al 1998); the panicovirus Panicum mosaic virus (PMV) (Batten et al 2006); the tombusviruses Tomato bushy stunt virus (TBSV) (Wu and White 1999), Carnation Italian ringspot virus (CIRV) (Nicholson and White 2008), and Maize necrotic streak virus (MNeSV) (Scheets and Redinbaugh 2006); the luteovirus Barley yellow dwarf virus (BYDV) (Wang and Miller 1995;Wang et al 1997); and the umbravirus Pea enation mosaic virus (PEMV) (Wang et al 2009). Of these, detailed RNA structure/function analyses of 39CITEs in BYDV (Guo et al 2000), TBSV White 2004, 2006), TCV (Stupina et al 2008;Zuo et al 2010), and PEMV (Wang et al 2009) have led to sound RNA secondary structure models for these elements.…”

Section: Introductionmentioning

confidence: 99%

Tombusvirus recruitment of host translational machinery via the 3′ UTR

Nicholson¹,

Wu²,

Chevtchenko³

et al. 2010

RNA

136

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RNA viruses recruit the host translational machinery by different mechanisms that depend partly on the structure of their genomes. In this regard, the plus-strand RNA genomes of several different pathogenic plant viruses do not contain traditional translation-stimulating elements, i.e., a 59-cap structure and a 39-poly(A) tail, and instead rely on a 39-cap-independent translational enhancer (39CITE) located in their 39 untranslated regions (UTRs) for efficient synthesis of viral proteins. We investigated the structure and function of the I-shaped class of 39CITE in tombusviruses-also present in aureusviruses and carmoviruses-using biochemical and molecular approaches and we determined that it adopts a complex higher-order RNA structure that facilitates translation by binding simultaneously to both eukaryotic initiation factor (eIF) 4F and the 59 UTR of the viral genome. The specificity of 39CITE binding to eIF4F is mediated, at least in part, through a direct interaction with its eIF4E subunit, whereas its association with the viral 59 UTR relies on complementary RNA-RNA base-pairing. We show for the first time that this tripartite 59 UTR/39CITE/eIF4F complex forms in vitro in a translationally relevant environment and is required for recruitment of ribosomes to the 59 end of the viral RNA genome by a mechanism that shares some fundamental features with cap-dependent translation. Notably, our results demonstrate that the 39CITE facilitates the initiation step of translation and validate a molecular model that has been proposed to explain how several different classes of 39CITE function. Moreover, the virus-host interplay defined in this study provides insights into natural host resistance mechanisms that have been linked to 39CITE activity.

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“…Other (+)-strand RNA viruses that lack both a 59-cap and a 39-poly(A) tail utilize a different translational strategy involving a 39-proximal RNA element (Kneller et al 2005). Members of the Tombusviridae and Luteoviridae families fall into this category and maintain RNA elements in the 39 region of their genomes that act as translational enhancers, termed 39TEs (Danthinne et al 1993;Timmer et al 1993;Wang and Miller 1995;Wang et al 1997;Oster et al 1998;Wu and White 1999;Qu and Morris 2000;Koh et al 2002;Mizumoto et al 2003;Shen and Miller 2004). The 39TE of Satellite tobacco necrosis virus (STNV) has been shown to interact in vitro with canonical eukaryotic translation nomic (sg) mRNAs that are produced during infections (Choi and White 2002;Lin and White 2004).…”

Section: Introductionmentioning

confidence: 99%

Analysis of a 3′-translation enhancer in a tombusvirus: A dynamic model for RNA–RNA interactions of mRNA termini

Fabian¹,

White²

2006

RNA

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Tomato bushy stunt virus is a (+)-strand RNA virus that is neither 59-capped nor 39-polyadenylated. Translation of viral proteins is instead mediated by an RNA element, the 39-cap-independent translational enhancer (39CITE), which is located in its 39 untranslated region (UTR). The 39CITE is proposed to recruit the translational machinery to the viral message, while a longdistance RNA-RNA interaction between the 39CITE and 59 UTR is thought to deliver the 43S ribosomal subunit to the 59 end of the viral mRNA. Here we provide the first evidence that the 59 UTR and 39CITE interact physically. Mutational analysis showed that formation of this RNA-RNA interaction in vitro correlates well with efficient translation in vivo, thus supporting its functional relevance. Other analyses of the 39CITE confirmed an overall Y-shaped RNA secondary structure and demonstrated the importance of numerous minor structural features for efficient translation of viral mRNAs. Functional studies on the role of the 59 UTR revealed that despite the absence of a cap structure, 43S subunits load at the very 59 end and scan in a 39 direction. These results indicate that the 59-39 RNA-RNA interaction is likely disrupted by scanning ribosomal subunits and suggest a dynamic model for the interaction of mRNA termini during active translation.

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Cap-Independent Translational Enhancement by the 3′ Untranslated Region of Red Clover Necrotic Mosaic Virus RNA1

Cited by 88 publications

References 51 publications

Oscillating kissing stem–loop interactions mediate 5′ scanning-dependent translation by a viral 3′-cap-independent translation element

Oscillating kissing stem–loop interactions mediate 5′ scanning-dependent translation by a viral 3′-cap-independent translation element

Tombusvirus recruitment of host translational machinery via the 3′ UTR

Analysis of a 3′-translation enhancer in a tombusvirus: A dynamic model for RNA–RNA interactions of mRNA termini

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