The Diversity and Evolution of Wolbachia Ankyrin Repeat Domain Genes

Siozios, Stefanos; Ioannidis, Panagiotis; Klasson, Lisa; Andersson, Siv G. E.; Braig, Henk R.; Bourtzis, Kostas

doi:10.1371/journal.pone.0055390

Cited by 91 publications

(97 citation statements)

References 101 publications

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“…The distal w Pip 0294/0295 pair is immediately surrounded by ankyrin repeat genes, which are thought to have been acquired from a eukaryotic host and potentially interact with host proteins (Siozios et al, 2013). In the genomes of w Mel and w Ri, we note similar associations with genes that encode phage proteins and ankyrin repeats.…”

Section: Resultsmentioning

confidence: 99%

Detection of the Wolbachia protein WPIP0282 in mosquito spermathecae: Implications for cytoplasmic incompatibility

Beckmann¹,

Fallon²

2013

Insect Biochemistry and Molecular Biology

107

144

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Cytoplasmic incompatibility (CI) is a conditional sterility induced by the bacterium Wolbachia pipientis that infects reproductive tissues in many arthropods. Although CI provides a potential tool to control insect vectors of arthropod-borne diseases, the molecular basis for CI induction is unknown. We hypothesized that a Wolbachia-encoded, CI-inducing factor would be enriched in sperm recovered from spermathecae of female mosquitoes. Using SDS-PAGE and mass spectrometry, we detected peptides from the 56 kDa hypothetical protein, encoded by wPip_0282, associated with sperm transferred to females by Wolbachia infected males. We also detected peptides from the same protein in Wolbachia infected ovaries. Homologs of wPip_0282 and the co-transcribed downstream gene, wPip_0283, occur as multiple divergent copies in genomes of CI-inducing strains of Wolbachia. The operon is located in a genomic context that includes mobile genetic elements. The absence of wPip_0282 and wPip_0283 homologs from genomes of Wolbachia in filarial nematodes, as well as other members of the Rickettsiales, suggests a role as a candidate CI effector.

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Section: Resultsmentioning

confidence: 99%

Detection of the Wolbachia protein WPIP0282 in mosquito spermathecae: Implications for cytoplasmic incompatibility

Beckmann¹,

Fallon²

2013

Insect Biochemistry and Molecular Biology

107

144

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“…], 300 m; length, 5 mm; pore size, 100 Å; particle size, 5 m [Dionex Corp.]) and washed with 5% acetonitrile-0.1% FA. The enrichment column was then switched into the nanoflow path (200 nl/min), and the sample was further separated on a C 18 Pep Map column (75-m i.d. by 15-cm length; 3-m particle size and 100-Å pore size [New Objective Inc., Woburn, MA]) by applying an acetonitrile gradient (acetonitrile plus 0.1% FA; 60 min) at a flow rate of 200 nl/min.…”

Section: Figmentioning

confidence: 99%

“…These ANK/PRANC proteins play a critical role in reprogramming various cellular signaling cascades to regulate host cell tropism and permissiveness (16). ANK proteins participate in protein-protein interactions and are involved in many functions, such as cell cycle regulation, signal transduction, and intracellular trafficking (17,18). Experimentally, it has been established that the PRANC domain present in ANK proteins of several poxvirus family members interacts with cellular SCF complexes to redirect ubiquitin ligase activity (9,(19)(20)(21)(22)(23).…”

mentioning

confidence: 99%

Chlorovirus Skp1-Binding Ankyrin Repeat Protein Interplay and Mimicry of Cellular Ubiquitin Ligase Machinery

Noel

Kang

Adamec

et al. 2014

J Virol

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The ubiquitin-proteasome system is targeted by many viruses that have evolved strategies to redirect host ubiquitination machinery. Members of the genus Chlorovirus are proposed to share an ancestral lineage with a broader group of related viruses, nucleo-cytoplasmic large DNA viruses (NCLDV). Chloroviruses encode an Skp1 homolog and ankyrin repeat (ANK) proteins. Several chlorovirus-encoded ANK repeats contain C-terminal domains characteristic of cellular F-boxes or related NCLDV chordopox PRANC (pox protein repeats of ankyrin at C-terminal) domains. These observations suggested that this unique combination of Skp1 and ANK repeat proteins might form complexes analogous to the cellular Skp1-Cul1-F-box (SCF) ubiquitin ligase complex. We identified two ANK proteins from the prototypic chlorovirus Paramecium bursaria chlorella virus-1 (PBCV-1) that functioned as binding partners for the virus-encoded Skp1, proteins A682L and A607R. These ANK proteins had a C-terminal Skp1 interactional motif that functioned similarly to cellular F-box domains. A C-terminal motif of ANK protein A682L binds Skp1 proteins from widely divergent species. Yeast two-hybrid analyses using serial domain deletion constructs confirmed the C-terminal localization of the Skp1 interactional motif in PBCV-1 A682L. ANK protein A607R represents an ANK family with one member present in all 41 sequenced chloroviruses. A comprehensive phylogenetic analysis of these related ANK and viral Skp1 proteins suggested partnered function tailored to the host alga or common ancestral heritage. Here, we show proteinprotein interaction between corresponding family clusters of virus-encoded ANK and Skp1 proteins from three chlorovirus types. Collectively, our results indicate that chloroviruses have evolved complementing Skp1 and ANK proteins that mimic cellular SCF-associated proteins. IMPORTANCEViruses have evolved ways to direct ubiquitination events in order to create environments conducive to their replication. As reported in the manuscript, the large chloroviruses encode several components involved in the SCF ubiquitin ligase complex including a viral Skp1 homolog. Studies on how chloroviruses manipulate their host algal ubiquitination system will provide insights toward viral protein mimicry, substrate recognition, and key interactive domains controlling selective protein degradation. These findings may also further understanding of the evolution of other large DNA viruses, like poxviruses, that are reported to share the same monophyly lineage as chloroviruses.T he ubiquitin-proteasome proteolytic pathway is an attractive target for viruses in their battle to create an intracellular environment conducive for their replication. In fact, targeting of ubiquitin-associated enzymes is a reoccurring theme in permissive viral infections (1). This eukaryotic regulatory system mediates a variety of biological processes, including protein turnover, DNA repair, trafficking, and signal transduction (2). Through sequential reactions of three enzyme types, covale...

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“…Ankyrin repeats, tandem motifs of about 33 amino acids, are known to mediate protein-protein interactions in eukaryotes (Caturegli et al 2000). These proteins are found in obligate and facultative endosymbiotic bacteria (Siozios et al 2013 …”

Section: Molecular Mechanisms Underlying the Interaction Between Wolbmentioning

confidence: 99%

Effect of Wolbachia Infection on Aging and Longevity-Associated Genes in Drosophila

et al. 2015

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Microbiota is known to interact with metabolic and regulatory networks of the host affecting its fitness. The composition of microbiota was shown to change throughout the host aging. Such changes can be likely caused by aging process or, vice versa, changes in microbiota composition can impact the aging process. It is suggested that microbiota plays an important role in life span determination. Several species from the genus Drosophila, especially D. melanogaster, are powerful models to study many biological processes including microbiota functioning and its effects on the host aging. The host fitness can be substantially affected by endosymbiotic bacteria such as Wolbachia that infects up to two-thirds of insects taxa, including Drosophila. Wolbachia was shown to significantly affect Drosophila aging and life span. However, the molecular mechanisms underlying interactions between Wolbachia and Drosophila remain mostly unknown. In this chapter, we summarize data suggesting that Wolbachia-Drosophila molecular cross-talk associated with life span determination and aging can occur through the immune deficiency pathway, stress-induced JNK pathway, insulin/IGF signaling pathway, ecdysteroid biosynthesis and signaling pathway, as well as through the heat shock and autophagy-specific genes/proteins.

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The Diversity and Evolution of Wolbachia Ankyrin Repeat Domain Genes

Cited by 91 publications

References 101 publications

Detection of the Wolbachia protein WPIP0282 in mosquito spermathecae: Implications for cytoplasmic incompatibility

Detection of the Wolbachia protein WPIP0282 in mosquito spermathecae: Implications for cytoplasmic incompatibility

Chlorovirus Skp1-Binding Ankyrin Repeat Protein Interplay and Mimicry of Cellular Ubiquitin Ligase Machinery

Effect of Wolbachia Infection on Aging and Longevity-Associated Genes in Drosophila

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