The Transcription Profile of Aleutian Mink Disease Virus in CRFK Cells Is Generated by Alternative Processing of Pre-mRNAs Produced from a Single Promoter

Qiu, Jianming; Cheng, Fang; Burger, L. Wes; Pintel, David J.

doi:10.1128/jvi.80.2.654-662.2006

Cited by 64 publications

(78 citation statements)

References 38 publications

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“…There is an internal polyadenylation site in the center of the genome, and the capsid-coding mRNAs, which are generated by splicing of the large intron within the NS1 coding region, must read though this (pA)p site to access the capsidcoding ORF in the right-hand end of the genome. These features are similar to the transcription profiles of the erythroviruses and amdoviruses (21,26,28) and underscore the importance of the regulation of alternative polyadenylation in the expression of parvovirus genomes.…”

supporting

confidence: 53%

“…Lane 3 shows an RNA marker ladder. (27), adeno-associated virus (7,30), Aleutian mink disease virus (2,28), and B19 virus (26). Three capsid proteins, VP1 (80 kDa), VP2 (72 kDa), and VP3 (62 kDa), were previously detected, both following BPV infection and from purified virus (14,16).…”

mentioning

confidence: 99%

“…(C) Western blotting analysis of HA-tagged BPV proteins. Protein samples were isolated 48 h following transfection of 293 cells with constructs pSK42BPVNS1HA and pSK42BPVNP1HA, in which an HA tag was inserted into the parent pSKBPV42 construct in the amino terminus of NS1 ORF and the carboxyl terminus of NP1 ORF, respectively, following the method previously reported (28). Protein samples were run on sodium dodecyl sulfate-10% polyacrylamide gels, and Western blotting was performed using a monoclonal antibody against the HA tag (HA-7; Sigma).…”

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confidence: 99%

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The Transcription Profile of the Bocavirus Bovine Parvovirus Is Unlike Those of Previously Characterized Parvoviruses

Qiu

Cheng

Johnson

et al. 2007

J Virol

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The Bocavirus bovine parvovirus generated a single pre-mRNA from a promoter at its left-hand end; however, the pattern of its alternative polyadenylation and splicing was different from that of other parvoviruses. A large left-hand-end open reading frame (ORF) encoded a nonstructural protein of approximately 95 kDa. An abundant, spliced, internally polyadenylated transcript encoded the viral NP1 protein from an ORF in the center of the genome. Transcripts encoding the capsid proteins were polyadenylated in the right-hand terminal palindrome. This is the first published transcription map of a member of the Bocavirus genus of the Parvovirinae.The genus Bocavirus is one of five genera of the subfamily Parvovirinae of the family Parvoviridae (35). The currently recognized members of the Bocavirus genus include bovine parvovirus type 1 (BPV) (1), canine minute virus (32), and the recently identified human bocavirus (HBoV) (4). HBoV, first detected in pooled human samples of lower respiratory tract infections collected by PCR amplification in Sweden (4), has been reported to be associated with acute respiratory illness at incidence rates of between 1.5% and 11.3% worldwide (3, 5, 6, 11-13, 15, 19, 22-24, 34). Isolation of HBoV has not yet been reported.A transcription map of any Bocavirus species based on a nonbiased direct analysis of steady-state RNA has not yet been formally presented. In this report, we describe the transcription map of BPV following infection of permissive bovine turbinate (BT) cells as determined by RNase protection and Northern blotting assays. Like members of the genera Erythrovirus and Amdovirus of the Parvovirinae, the Bocavirus BPV has a single promoter at its left-hand end and uses both an internal and distal polyadenylation site. However, the alternative RNA processing strategy used by BPV generates a transcription profile that is different from that of other characterized parvoviruses.Sequencing of BPV and construction of a nearly full-length BPV clone. Because a previously constructed infectious clone of BPV (33) was no longer available, we recloned the majority of the BPV genome, using a PCR-based strategy, directly from plaque-purified BPV (the prototype Abinanti strain) (1), utilizing the published BPV sequence (GenBank accession no. NC_001540) to design primers. The revised sequence of BPV was deposited in GenBank, and all the nucleotide numbers in the manuscript refer to this revised sequence, unless otherwise specified. This nearly full-length clone, containing the revised BPV sequence (nucleotide [nt] 42 to 5515) in the pBluescript vector (Stratagene), was designated pSK42BPV. This clone was not infectious (data not shown).Our revised BPV sequence showed a number of silent mutations which differed from that of the sequence deposited previously, and these differences may reflect natural variations among isolates. However, in addition, we detected two more significant changes within the NS1 coding region which allowed the opening of the long NS open reading frame 1 (ORF 1) from n...

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confidence: 53%

mentioning

confidence: 99%

mentioning

confidence: 99%

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The Transcription Profile of the Bocavirus Bovine Parvovirus Is Unlike Those of Previously Characterized Parvoviruses

Qiu

Cheng

Johnson

et al. 2007

J Virol

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“…Splicing of this intron to remove the polyadenylation signal helps govern access to the capsid gene for these viruses (27). The amdoviruses (28,29) and the bocaviruses (3) have polyadenylation sites that lie within their capsid gene; however, these potent motifs are retained in the capsid-encoding mRNA and must be somehow suppressed to allow export and accumulation of mRNAs that encode capsid protein information. We have shown here that the bocavirus MVC has evolved yet another way to allow essential access to its capsid protein gene, namely, by the action of its novel NP1 protein, which is required to read through its internal (pA)p site.…”

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Characterization of the Nonstructural Proteins of the Bocavirus Minute Virus of Canines

Sukhu

Fasina

Burger

et al. 2013

J Virol

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bWe present a detailed characterization of a single-cycle infection of the bocavirus minute virus of canines (MVC) in canine WRD cells. This has allowed identification of an additional smaller NS protein that derives from an mRNA spliced within the NS gene that had not been previously reported. In addition, we have identified a role for the viral NP1 protein during infection. NP1 is required for read-through of the MVC internal polyadenylation site and, thus, access of the capsid gene by MVC mRNAs. Although the mechanism of NP1's action has not yet been fully elucidated, it represents the first parvovirus protein to be implicated directly in viral RNA processing.

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“…Like members in the genus Bocavirus (8,9) and Aleutian mink disease virus (10), also of the Parvoviridae family, the transcription profile of B19V is unusual for a DNA virus in that all of the mRNA transcripts are generated from a single precursor mRNA (pre-mRNA) transcribed from a single promoter at map unit 6 (P6) and feature alternative polyadenylation and splicing (see Fig. 1A) (11,12).…”

Section: Human Parvovirus B19 (B19v)mentioning

confidence: 99%

Internal Polyadenylation of the Parvovirus B19 Precursor mRNA Is Regulated by Alternative Splicing

Guan

Huang

Cheng

et al. 2011

Journal of Biological Chemistry

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Alternative processing of parvovirus B19 (B19V) pre-mRNA is critical to generating appropriate levels of B19V mRNA transcripts encoding capsid proteins and small nonstructural proteins. Polyadenylation of the B19V pre-mRNA at the proximal polyadenylation site ((pA)p), which prevents generation of fulllength capsid proteins encoding mRNA transcripts, has been suggested as a step that blocks B19V permissiveness. We report here that efficient splicing of the B19V pre-mRNA within the first intron (upstream of the (pA)p site) stimulated the polyadenylation; in contrast, splicing of the B19V pre-mRNA within the second intron (in which the (pA)p site resides) interfered with the polyadenylation, leading to the generation of a sufficient number of B19V mRNA transcripts polyadenylated at the distal polyadenylation site ((pA)d). We also found that splicing within the second intron and polyadenylation at the (pA)p site compete during processing of the B19V pre-mRNA. Furthermore, we discovered that the U1 RNA that binds to the 5 splice donor site of the second intron is fully responsible for inhibiting polyadenylation at the (pA)p site, whereas actual splicing, and perhaps assembly of the functional spliceosome, is not required. Finally, we demonstrated that inhibition of B19V pre-mRNA splicing within the second intron by targeting an intronic splicing enhancer using a Morpholino antisense oligonucleotide prevented B19V mRNA transcripts polyadenylated at the (pA)d site during B19V infection of human erythroid progenitors. Thus, our study reveals the mechanism by which alternative splicing coordinates alternative polyadenylation to generate full-length B19V mRNA transcripts at levels sufficient to support productive B19V infection. Human parvovirus B19 (B19V)2 is a member of the genus Erythrovirus of the family Parvoviridae. B19V causes several diseases in humans (1), the most common of which is erythema infectiosum or Fifth disease. Other diseases include acute and chronic arthropathy, transient aplastic crisis (infection of patients with a high rate of red blood cell turnover), pure red cell aplasia (infection of immunocompromised patients), and hydrops fetalis (infection of pregnant women). Like other parvoviruses, B19V contains a linear single-stranded DNA genome of approximately (ϳ)5.6 kb, which is encapsidated by an icosahedrally symmetric capsid without an envelope (2, 3). In addition to infecting only humans, B19V infection shows a remarkable tropism for human erythroid progenitor cells (4 -7).Like members in the genus Bocavirus (8, 9) and Aleutian mink disease virus (10), also of the Parvoviridae family, the transcription profile of B19V is unusual for a DNA virus in that all of the mRNA transcripts are generated from a single precursor mRNA (pre-mRNA) transcribed from a single promoter at map unit 6 (P6) and feature alternative polyadenylation and splicing (see Fig. 1A) (11, 12). The only unspliced mRNA encoding the large nonstructural protein (NS1) is polyadenylated at the proximal poly(A) site ((pA)p) and retains...

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The Transcription Profile of Aleutian Mink Disease Virus in CRFK Cells Is Generated by Alternative Processing of Pre-mRNAs Produced from a Single Promoter

Cited by 64 publications

References 38 publications

The Transcription Profile of the Bocavirus Bovine Parvovirus Is Unlike Those of Previously Characterized Parvoviruses

The Transcription Profile of the Bocavirus Bovine Parvovirus Is Unlike Those of Previously Characterized Parvoviruses

Characterization of the Nonstructural Proteins of the Bocavirus Minute Virus of Canines

Internal Polyadenylation of the Parvovirus B19 Precursor mRNA Is Regulated by Alternative Splicing

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