The trypanosome Pumilio‐domain protein PUF7 associates with a nuclear cyclophilin and is involved in ribosomal RNA maturation

Droll, Dorothea; Archer, Stuart K.; Fenn, Katelyn; Delhi, Praveen; Matthews, Keith R.; Clayton, Christine

doi:10.1016/j.febslet.2010.02.018

Cited by 54 publications

(55 citation statements)

References 34 publications

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“…Transcriptome analysis showed significant upregulation of several RNA binding proteins in the JBPKO cells, including a family of proteins (i.e., PUF8) that are known to affect mRNA stability (14). Therefore, increased abundance of certain trans-acting factors following the reduction in base J would lead to the destabilization of specific mRNA transcripts.…”

Section: Discussionmentioning

confidence: 99%

Epigenetic Regulation of Transcription and Virulence in Trypanosoma cruzi by O-Linked Thymine Glucosylation of DNA

Ekanayake

Minning

Weatherly

et al. 2011

Molecular and Cellular Biology

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Unlike other eukaryotes, the protein-coding genes of Trypanosoma cruzi are arranged in large polycistronic gene clusters transcribed by polymerase II (Pol II). Thus, it is thought that trypanosomes rely solely on posttranscriptional processes to regulate gene expression. Here, we show that the glucosylated thymine DNA base (␤-D-glucosyl-hydroxymethyluracil or base J) is present within sequences flanking the polycistronic units (PTUs) in T. cruzi. The loss of base J at sites of transcription initiation, via deletion of the two enzymes that regulate base J synthesis (JBP1 and JBP2), correlates with an increased rate of Pol II transcription and subsequent genome-wide increase in gene expression. The affected genes include virulence genes, and the resulting parasites are defective in host cell invasion and egress. These studies indicate that base J is an epigenetic factor regulating Pol II transcription initiation in kinetoplastids and provides the first biological role of the only hypermodified DNA base in eukaryotes.Trypanosoma cruzi, the protozoan parasite that causes Chagas' disease, is the major cause of cardiac disease in South and Central America (1). The parasite has a complex life cycle with two hosts and four developmental stages. Epimastigotes develop in the hindgut of the triatomine insect vector and differentiate into metacyclic forms. Infective metacyclic forms enter the vertebrate host, invade the host cell, and differentiate to form amastigotes. Trypomastigotes released from the infected cell are able to reinvade a wide variety of host cells. Success of the parasite throughout the life cycle is ensured by the regulated expression of surface proteins such as mucin and trans-sialidase, which allow differential adherence and evasion of the host immune responses (2). Members of the surface glycoprotein gene family colocalize with a novel hypermodified DNA base, ␤-D-glucosyl-hydroxymethyluracil or base J, suggesting an epigenetic mechanism of regulating T. cruzi pathogenesis (3).In base J, the thymine base exhibits O-linked glucosylation in telomeric DNA of all kinetoplastid flagellates and some closely related unicellular flagellates, but base J is not present in the genomes of other protozoa or metazoa (3, 4). Base J was initially discovered on the basis of its distinct presence within the 19 silent telomeric variant surface glycoprotein (VSG) expression sites (ES) of Trypanosoma brucei but absence from the single transcribed ES, suggesting its role in the regulation of telomeric VSG gene expression (3, 35). Recent genomewide analysis revealed that base J is also present throughout the T. brucei genome, enriched at regions flanking polymerase II (Pol II) polycistronic transcription units (PTUs) (9). PTUs are large gene clusters that are cotranscribed by Pol II to yield polycistronic pre-mRNAs that are then processed into mature mRNAs by trans-splicing and polyadenylation (7). The localization of base J at PTU-flanking regions suggests a role for the modified base in regulating Pol II transcription initi...

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Section: Discussionmentioning

confidence: 99%

Epigenetic Regulation of Transcription and Virulence in Trypanosoma cruzi by O-Linked Thymine Glucosylation of DNA

Ekanayake

Minning

Weatherly

et al. 2011

Molecular and Cellular Biology

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“…29,30 Both are localized in the nucleoli and affect early steps of rRNA processing. ScNop9 is associated with the pre-40S ribosome subunit.…”

Section: Pumilio Puf Domain Rna-binding Proteins In Arabidopsismentioning

confidence: 99%

“…29 Most of the nucleolar Puf proteins are associated with rRNA processing and ribosome biogenesis. Our data on the nucleolar-localized Puf protein, APUM23, provide another example of nucleolar Pufs that are involved in rRNA processing.…”

Section: Other Possible Nucleolar Functions Of Apum23mentioning

confidence: 99%

Pumilio Puf domain RNA-binding proteins in Arabidopsis

Abbasi

Park

Choi

2011

Plant Signaling & Behavior

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“…The inner surface of the PHD binds the RNA. The outer surface of the domain permits protein-protein interactions with diverse proteins, such as deadenylase and general translation factors (9,10). Arabidopsis Pufs also exhibit RNA-binding activity and have conserved binding motifs (11,12).…”

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confidence: 99%

ArabidopsisPumilio protein APUM5 suppressesCucumber mosaic virusinfection via direct binding of viral RNAs

Huh¹,

Kim

Paek

2012

Proc. Natl. Acad. Sci. U.S.A.

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Posttranscriptional/translational regulation of gene expression is mediated by diverse RNA binding proteins and plays an important role in development and defense processes. Among the RNAbinding proteins, the mammalian Pumilio RNA-binding family (Puf) acts as posttranscriptional and translational repressors. An Arabidopsis Puf mutant, apum5-D, was isolated during a T-DNA insertional mutant screen for mutants with reduced susceptibility to Cucumber mosaic virus (CMV) infection. Interestingly, CMV RNA contained putative Pumilio-homology domain binding motifs in its 3′ untranslated region (UTR) and internal places in its genome. APUM5 directly bound to the 3′ UTR motifs and some internal binding motifs in CMV RNAs in vitro and in vivo. We showed that APUM5 acts as a translational repressor that regulates the 3′ UTR of CMV and affects CMV replication. This study uncovered a unique defense system that Arabidopsis APUM5 specifically regulates CMV infection by the direct binding of CMV RNAs. plant defense | Pumilio RNA binding protein | TuMV P lant viruses are the obligate pathogens, and host proteins facilitate the multiplication of viruses by affecting processes such as viral replication, cell-to-cell movement, and systemic movement of the virus (1). These processes occur upon the interaction between the virus and host proteins or after the suppression of the host basal defense mechanism and often lead to abnormal phenotypes of virus-infected host plants, such as small, highly branched bushes with deformed leaves, stunting, and reduced apical dominance (2-4). Thus, the reduced growth and developmental changes in the virus-infected plants are typical symptoms of virus infection and signify that the virus has undergone a successful life cycle. To understand the molecular mechanisms underlying viral multiplication and symptoms in plants, it is necessary to identify and characterize the host factors involved in these processes.To identify novel host factors involved in the multiplication of plant RNA viruses in susceptible plants, T-DNA insertion mutants of Arabidopsis thaliana Col-0 ecotype, in which CMVKor multiplication is abrogated (5), were screened. An Arabidopsis Puf mutant, apum5-D, in which Cucumber mosaic virus (CMV) multiplication was affected during viral spreading, was isolated. APUM5 contains the Pumilio-homology domain (PHD) and encodes a putative Puf, which was originally identified in Drosophila melanogaster and Caenorhabditis elegans (6). Pufs are highly conserved in various organisms and work as posttranscriptional and translational repressors (7,8). PHD has RNA binding activity; there are eight repeats with three alpha helices in each repeat. The inner surface of the PHD binds the RNA. The outer surface of the domain permits protein-protein interactions with diverse proteins, such as deadenylase and general translation factors (9, 10). Arabidopsis Pufs also exhibit RNA-binding activity and have conserved binding motifs (11,12). However, plant Puf functions have not yet been fully identified or charact...

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The trypanosome Pumilio‐domain protein PUF7 associates with a nuclear cyclophilin and is involved in ribosomal RNA maturation

Cited by 54 publications

References 34 publications

Epigenetic Regulation of Transcription and Virulence in Trypanosoma cruzi by O-Linked Thymine Glucosylation of DNA

Epigenetic Regulation of Transcription and Virulence in Trypanosoma cruzi by O-Linked Thymine Glucosylation of DNA

Pumilio Puf domain RNA-binding proteins in Arabidopsis

ArabidopsisPumilio protein APUM5 suppressesCucumber mosaic virusinfection via direct binding of viral RNAs

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